Download Handbook of Pediatric Strabismus and Amblyopia

Handbook of Pediatric
Strabismus and Amblyopia
Handbook of Pediatric
Strabismus and
Amblyopia
Edited by
Kenneth W. Wright, MD
Director, Wright Foundation for Pediatric Ophthalmology
Director, Pediatric Ophthalmology, Cedars-Sinai Medical
Center, Clinical Professor of Ophthalmology, University of
Southern California—Keck School of Medicine, Los Angeles,
California
Peter H. Spiegel, MD
Focus On You, Inc., Palm Desert, California
Inland Eye Clinic, Murrieta, California
Children’s Eye Institute, Upland, California
Lisa S. Thompson, MD
Attending Physician, Stroger Hospital of Cook County,
Chicago, Illinois
Illustrators
Timothy C. Hengst, CMI
Susan Gilbert, CMI
Faith Cogswell
Kenneth W. Wright, MD
Director, Wright Foundation for
Pediatric Ophthalmology
Director, Pediatric Ophthalmology,
Cedars-Sinai Medical Center,
Clinical Professor of
Ophthalmology, University of
Southern California—Keck School
of Medicine
Los Angeles, CA
USA
Peter H. Spiegel, MD
Focus On You, Inc.
Palm Desert, CA
Inland Eye Clinic,
Murrieta, CA
Children’s Eye
Institute
Upland, CA
USA
Lisa S. Thompson, MD
Attending Physician
Stroger Hospital of Cook County
Chicago, IL
USA
Library of Congress Control Number: 2005932932
ISBN 10: 0-387-27924-5
ISBN 13: 978-0387-27924-4
e-ISBN 0-387-27925-4
Printed on acid-free paper.
© 2006 Springer Science+Business Media, Inc.
Reprinted from Wright and Spiegel: Pediatric Ophthalmology and
Strabismus, second edition, 2003 Springer Science+Business Media.
All rights reserved. This work may not be translated or copied in whole
or in part without the written permission of the publisher (Springer
Science+Business Media, Inc., 233 Spring Street, New York, NY 10013,
USA), except for brief excerpts in connection with reviews or scholarly
analysis. Use in connection with any form of information storage and
retrieval, electronic adaptation, computer software, or by similar or
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The use in this publication of trade names, trademarks, service marks,
and similar terms, even if they are not identified as such, is not to be
taken as an expression of opinion as to whether or not they are subject
to proprietary rights.
While the advice and information in this book are believed to be true and
accurate at the date of going to press, neither the authors nor the editors
nor the publisher can accept any legal responsibility for any errors or
omissions that may be made. The publisher makes no warranty, express
or implied, with respect to the material contained herein.
Printed in the United States of America.
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Preface
The Handbook of Pediatric Strabismus and Amblyopia is a
practical, easy-to-understand resource on the diagnosis and
management of both common and the more esoteric forms of
strabismus. Emphasis is placed on the understanding of the basis
of the strabismus, not rote memorization of strabismus patterns.
Concepts regarding sensory adaptations and sensory testing are
described in a simple way to elucidate rather than confuse the
reader. An in-depth chapter on visual development and the
pathophysiology of amblyopia is included.
The goal of the Handbook of Pediatric Strabismus and
Amblyopia is to make this often confusing subject simple and
easy to understand. This book should make an excellent
resource for board review. Chapters are reader friendly. They are
organized with clear sub-headings that allow the readers to
quickly find their area of interest. Diagrams and drawings
are prevalent throughout the book to help illustrate otherwise
difficult or complex concepts. Composite strabismus photographs are included to demonstrate the strabismus as it actually
appears in the clinical setting and to help with pattern recognition. These composite strabismus photographs are very
useful for board review. Each chapter is fully referenced to
provide evidence-based practice guidelines and further in-depth
reading.
An important use of the handbook is patient and family
education. Families are rightfully concerned about the strabismus and they have often been told conflicting and confusing information about it. Information, including diagrams
and photographs from the handbook, can be shared with the
families to clarify their specific type of strabismus. This
important information is often lacking in general texts on
ophthalmology.
v
vi
preface
I hope you will find the Handbook of Strabismus and
Amblyopia to be an invaluable adjunct to your practice and for
board review.
Kenneth W. Wright, MD
Contents
Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
v
ix
1 Pediatric Eye Examination . . . . . . . . . . . . . . . . . .
Ann U. Stout
1
2 Anatomy and Physiology of Eye Movements . . . .
Kenneth W. Wright
24
3 Binocular Vision and Introduction
to Strabismus . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Kenneth W. Wright
70
4 Visual Development and Amblyopia . . . . . . . . . . .
Kenneth W. Wright
103
5 The Ocular Motor Examination . . . . . . . . . . . . . .
Kenneth W. Wright
138
6 Sensory Aspects of Strabismus . . . . . . . . . . . . . . .
Kenneth W. Wright
174
7 Esodeviations . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Kenneth W. Wright
217
8 Exotropia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Kenneth W. Wright
266
9 Alphabet Patterns and Oblique
Muscle Dysfunctions . . . . . . . . . . . . . . . . . . . . . .
Kenneth W. Wright
284
vii
viii
contents
10 Complex Strabismus: Restriction, Paresis,
Dissociated Strabismus, and Torticollis . . . . . . . .
Kenneth W. Wright
323
11 Strabismus Surgery . . . . . . . . . . . . . . . . . . . . . . . .
Kenneth W. Wright and Pauline Hong
388
12 Ocular Motility Disorders . . . . . . . . . . . . . . . . . .
Mitra Maybodi, Richard W. Hertle, and
Brian N. Bachynski
423
13 Optical Pearls and Pitfalls . . . . . . . . . . . . . . . . . .
David L. Guyton, Joseph M. Miller, and
Constance E. West
520
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
531
Contributors
Brian N. Bachynski, MD
David L. Guyton, MD
Richard W. Hertle, MD, FACS
Pauline Hong, MD
Mitra Maybodi, MD
Joseph M. Miller, MD
Ann U. Stout, MD
Constance E. West, MD
Kenneth W. Wright, MD
ix
1
Pediatric Eye Examination
Ann U. Stout
THE HISTORY AND PHYSICAL
EXAMINATION
In the nonpediatric eye clinic, the physician often views the
presence of a small child in an examining lane with some
anxiety, if not dread. Examination of a child is quite different
from that of the adult. The history is largely from a source other
than the patient, and the examination requires patience and
talent. There are several tricks to make the visit go as smoothly
and efficiently as possible (see the box on the following page).
HISTORY
Although ancillary personnel are often relied on to take the
history, this is best obtained by the physician who knows how
to direct the line of questioning to the most useful information.
The old adage that “the patient is always right” is especially true
in the case of parents’ observations about their children. Most
of the history is obtained from the parents or the referring physician, but any input from the child is equally important. Many
children will not complain of blurry vision or diplopia, but
should they describe these symptoms one must be very alert to
an acute process. This is also an invaluable time to observe the
child in an unobtrusive fashion and preliminarily assess head
position, eye alignment, and overall appearance. Often this may
be the extent of the physical examination that one can obtain;
once children realize that attention is focused on them, they
may become very uncooperative.
The problem precipitating the visit should be stated in the
parents’ or child’s own words and then elaborated. Requisite
1
2
handbook of pediatric strabismus and amblyopia
questioning for all pediatric eye problems should clarify whether
the problem is congenital or acquired and should specify the age
of onset in the latter case. If the chief complaint is a visual
problem, it is helpful for the parents to specify what the child
can or cannot see; that is, does the child respond to lights, faces,
toys near or far, very small items? In cases of strabismus, the frequency and stability of the deviation and any associated head
posture are important. Precipitating factors may include fatigue,
illness, sunlight, and close or distance work. For nystagmus,
medications and the past medical history may be pertinent. With
cataracts, any history of trauma, medications, or associated
medical conditions is important, as well as the family history.
Tearing patients need to be questioned about any redness, photophobia, or crusting of the lashes. In ptosis, the stability or variability is important, as is any associated chin elevation or general
neuromuscular problems. For difficulties in school, it is helpful
to determine if the problem is only visual or is related to a particular subject area (reading, spelling, writing, or math) and if
there are any stress factors in the child’s extracurricular life.
Important aspects of past history include prenatal and perinatal problems, birth weight, gestational age, and mode of delivery. Any medical problems should be elicited, as well as current
medication and allergies. Early development should be assessed
by asking about specific developmental milestones, such as
rolling over, sitting up, and walking. The Denver Developmental Scale is a good reference for developmental norms.10 Later
development can be ascertained by asking about scholastic level
and performance.
The family history is very important because often the young
child does not have enough past history to be useful. The focus
should be on the presence of strabismus, poor vision, and neurological problems. In the case of possible genetic disorders, the
number and sex of siblings, possible consanguinity, and the number
and gestational age of any miscarriages should be documented.
PHYSICAL EXAMINATION
Establishing Rapport
If you approach the examination with dread, the child will sense
your personal tension and become uneasy. Children can be
unpredictable, noncommunicative, and uncooperative, which
chapter 1: pediatric eye examination
3
may make the examination both time consuming and frustrating for a busy practitioner. However, if extra time is taken initially to gain the trust of the child, the rest of the exam will go
much more easily. This “friendship” is often first established
in the waiting room, where toys, appropriate books, and even
small furniture should be made available. In a general practice seeing children on a fairly regular basis, at least one exam
room should be outfitted to make a child feel relaxed and
make the exam go more smoothly. A 20-foot lane is best
because of the frequent use of single Allen cards and the need
for distance measurements in strabismus. Attention-getting
distance targets may include a remote control cartoon movie
or a motorized animal. Near targets should have variety and
appeal, as one frequently finds that “one toy–one look” is the
rule.
Approach young children as though you had come to play
with and entertain them, and you will receive a lot of useful
information in the process. Find out what they like to be called
and use their name frequently, but speak softly and keep a
respectful physical distance from them until they warm up to
you. Also, find out from parents their favorite imaginary or
cartoon characters and refer to these during your exam. Make
a game of the exam; play peek-a-boo with cover testing, swoop
near targets around like an airplane to evaluate the range of
motility, refer to glasses and lenses used as “magic” or “funny
Useful Items for Pediatric Eye Exams
Allen cards (single and linear)
Wright figures (single and linear)
Tumbling E (single and linear)
Eye patches
Interesting distance and near fixation targets
Accommodative near targets (finger puppets, wiggle pictures)
Portable slit lamp
Papoose board
Wire lid speculums (infant and child size)
Loose retinoscopy lenses
Loose prisms
Fusional tests (Worth 4-Dot, Titmus or Randot, Bagolini lenses)
28-diopter lens
Handheld tonometer (Perkins or Tonopen)
Calipers
4
handbook of pediatric strabismus and amblyopia
sunglasses,” make funny sounds to get their attention. Do the
noncontact things first: cover testing, fixation testing, pupillary and red reflex exam. Many small children object to physical contact by a stranger and once they are upset it is usually
the end of the exam for the day. Sometimes they will more
readily tolerate their parents placing glasses or a patch than a
strange doctor. Remember, if you find yourself getting frustrated or impatient with a child in one area, stop and go on to
some other aspect of the exam.
With older children, asking direct questions about their
hobbies, school, and family shows an interest in them and
often distracts them from the anxiety of the exam. They often
appreciate a handshake or pat on the knee. Explain to them
what you are doing before you do it and be honest; avoid
talking down to them. If they ask, do not tell them the mydriatic drops will not hurt, but explain that they will only sting
for a minute, like swimming in a pool with chlorine.
Examination of the Uncooperative Child
Sometimes, despite the best efforts, a child simply will not
cooperate, and urgency of the problem or the need for further
information may require physically restraining or sedating the
child. A papoose board can be used to control a child up to
around 5 years of age, depending on their size and strength. A
lid speculum can then be used with a topical anesthetic to
force the eyes open, although Bell’s phenomenon of the eyes
often makes a thorough examination difficult, and crying can
affect intraocular pressure measurements.
SEDATION
For the child in whom relaxation is important, or when physical restraint seems too psychologically traumatic, as in older
children, sedation should be used. The common modes of outpatient sedation include chloral hydrate (oral or suppository),
Propofol infusion, or a combination injection of Demerol, Phenergan, and Thorazine (DPT). The first has the advantage of good
sedation with a low level of respiratory depression and no effect
on intraocular pressure (IOP). The latter two have analgesic as
well as sedative properties, which may be useful in painful procedures, but there is slightly more respiratory depression and
Propofol will lower IOP.24,37
chapter 1: pediatric eye examination
5
Although chloral hydrate is often not effective if the children are more than 2.5 years old, Propofol and DPT can be used
in older children. Whenever sedatives are given, the child’s vital
signs including pulse oximetry must be monitored until awake,
ventilatory equipment must be available, and appropriately
trained personnel should be in attendance. Any sedative may
have a greater effect in children with underlying neurological
abnormalities.
CHLORAL HYDRATE
The minimal effective dose of chloral hydrate is 50 mg/kg, but
often 80 to 100 mg/kg is needed if manipulation of the eyes is
anticipated or if prolonged sedation is needed for electrophysiological testing.9,45,46 Half the initial dose can be repeated up to a
maximum of 3 g if the child is not sedated in 30 min.22 Any sedative is best given on an empty stomach (4 h since eating) to
increase absorption and decrease the risk of aspiration.
DPT
DPT is given in a dose of 2 : 1 : 1 mg/kg, not to exceed 50 : 25 : 25.
Because of the better analgesic effects, this is probably a better
choice for painful procedures (laceration repairs, chalazion excisions, cryotherapy). Potential complications include respiratory
depression, apnea, dystonic reactions, hypotension, seizures, and
cardiac arrest.37 This mode of sedation should only be used when
the child is under the supervision of a physician with appropriate training to manage complications, as in the emergency room.
EXAMINATION UNDER ANESTHESIA
If it is impractical to sedate the child in the office, or if surgery
is anticipated based on the exam findings, than examination
under anesthesia should be arranged in the operating room.
Modern anesthetic practices make general anesthesia a very safe
procedure, even when done repeatedly. A disadvantage of general
anesthesia is the purported intraocular pressure-lowering effects
of inhalational anesthetics. Pressures taken under inhalational
anesthetics have been lower than those measured in awake
children, but this is probably a result of increased overall relaxation.13 Propofol has a similar effect on IOP.25 The pressure may
actually increase several points after intubation.40 Use of laryngeal mask airways may eliminate this transient pressure rise.43
It is probably best to record the pressure both before and after
intubation.
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handbook of pediatric strabismus and amblyopia
External Examination
The child’s overall appearance and level of alertness can be
judged during the history taking. Head posture may also be
noted then, as well as gross ocular alignment. The history or
appearance may warrant more detailed examination of overall
neuromuscular tone, cranial nerves, head circumference,
extremities, or skin. The head may be assessed for symmetry,
preauricular skin tags, ear position, and shape. The orbits should
be appraised for ptosis, abnormalities in fissure size or shape,
and orbital depth. Many of these findings do not require a systematic search but rather an overall heightened awareness of
what is normal versus abnormal. The general assessment of a
dysmorphic child should push the physician to more precisely
define what abnormalities lead to that impression.
Visual Acuity Assessment: Preverbal
To judge vision in the preverbal child, one must rely on the
smallest age-appropriate target that will hold attention and on
the difference, if any, between the two eyes. An appropriate
target for a 1-year-old child may be a small finger puppet; but a
1-month-old may fixate only on a human face and do that rather
unsteadily. Infants are unable to pursue targets smoothly until
6 to 8 weeks of age but instead will track using hypometric saccades.5 Targets with fine detail that require accommodation
and focused attention are best for children over age 1, for even
though accommodation is appropriate to target distance by age
3 to 4 months, the macula is still immature even at the age of
15 months.6 Children who have developed a pincer grasp can be
asked to pick up small particles from the palm of your hand.
Often cake sprinkles are useful because they are edible and such
a target often ends up in the mouth.
FIXATION
There are two types of fixation testing: monocular and binocular. In monocular fixation testing one assesses whether the
patient fixes with the fovea (centrally) and the quality of fixation.
Each eye should be occluded in turn and the smallest possible
target that elicits a fixation response should be used. Monocular
fixation should be assessed for three separate factors: quality and
accuracy (good, fair, poor), location (central versus eccentric), and
duration (maintained versus sporadic). Clinically, abbreviations
chapter 1: pediatric eye examination
7
are often used to describe fixation including GCM for good,
central, and maintained, CSM for central, steady, and maintained, or FF for fix and follow. Eccentric fixation is an important sign as this shows that the patient is not fixing with the
fovea and vision is in the range of 20/200 or worse. It is important to remember, when testing monocular fixation, that the fixation target should be slowly moved through the visual field to
assess the quality of fixation. The target size and distance should
be estimated and documented in the chart. It is important to be
aware of the normal timetable for visual maturation, although
this may vary widely with individuals. The newborn has only
sporadic saccadic eye movements with very poor fix and follow;
by 6 weeks, most infants will show some smooth pursuit and
central fixation, and by 8 weeks the vast majority of infants will
have central fixation with accurate smooth pursuit and easily
demonstrate optokinetic drum responses.6 Smooth pursuit is
asymmetrical until age 6 months of age, with monocular temporal to nasal pursuit being better than nasal to temporal pursuit.
Tables 1-1 and 1-2 outline normal visual development. One
should remember that there is a subgroup of patients who are
otherwise normal yet show delayed visual maturation. However,
even this group of patients should show improvement of visual
function and should have central fix and follow by at least 6
months, with occasional delays up to 12 months of age.
Binocular fixation preference compares the vision of one eye
to the other. This test presumes that strong fixation preference
in patients with strabismus indicates organic visual loss or
TABLE 1-1. Normal Visual Development.
Pupillary light reaction present: 30 weeks gestation
Blink response to visual threat: 2–5 months
Fixation well developed: 2 months
Smooth pursuit well developed: 6–8 weeks
Saccades well developed (not hypometric): 1–3 months
Optokinetic nystagmus (OKN)
1. Present at birth but with restricted slow-phase velocity.
2. Temporal to nasal monocular response better than nasal to temporal until
2–4 months.
Accommodation appropriate to target: 4 months
Stereopsis well developed: 3–7 months
Contrast sensitivity function well developed: 7 months
Ocular alignment stabilized: 1 month
Foveal maturation complete: 4 months
Optic nerve myelination complete: 7 months to 2 years
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handbook of pediatric strabismus and amblyopia
TABLE 1-2. Age-Related Visual Acuity Estimates by Test Method.
Technique
Birth
2 months
4 months
6 months
1 year
Age for 20/20
(months)
OKN
FPL
VEP
20/400
20/400
20/800
20/400
20/400
20/150
20/200
20/200
20/600
20/100
20/150
20/400
20/60
20/50
20/20
20–30
18–24
6–12
OKN, optokinetic nystagmus; FPL, forced-choice preferential looking; VEP, visual evoked potential.
amblyopia in the nonpreferred eye.12,48 Binocular testing has an
advantage over monocular testing, because vision can be very
poor (20/100 to 20/200) and the patient will still show essentially normal monocular fixation. Binocular fixation preference
testing, however, will identify even mild amblyopia (two lines
of Snellen acuity difference).44,47 It is important to assess monocular fixation before fixation preference testing to rule out the
possibility of bilateral symmetrical visual loss in preverbal children. Fixation preference testing is very accurate for diagnosing
amblyopia in children with large-angle strabismus.48
In patients with straight eyes or microtropias, binocular
fixation preference testing can be done using the vertical prism
test or induced tropia test.47 In patients with straight eyes, one
does not know which eye is fixing; therefore, it is impossible to
determine fixation preference. The vertical prism test induces
a vertical deviation and therefore allows assessment of fixation
preference. In patients with small-angle strabismus (less than
10–15 prism diopters), the induced vertical tropia dissociates
peripheral fusion and eliminates any facultative suppression
scotoma associated with the patient’s baseline ocular alignment.
In turn, this eliminates the problem of overdiagnosis of amblyopia, previously described by Zipf.48 Fixation preference testing
is a quick and accurate way of diagnosing amblyopia in clinical
conditions such as anisometropic amblyopia, unilateral ptosis,
postoperative congenital esotropia, and other conditions that
could cause unilateral amblyopia.
OPTOKINETIC NYSTAGMUS
Children with poor fixation to any targets as a result of either
poor vision or central nervous system problems can be evaluated for the presence of optokinetic nystagmus (OKN) so long
as they are able to generate saccades. Optokinetic nystagmus is
an involuntary pursuit response to moving stripes filling up
chapter 1: pediatric eye examination
9
most of the visual field, so a response may be seen in infants
who are merely uninterested in other targets. Response to a
standard OKN drum implies vision of finger counting at 3 to
5 feet.16,17 One can also assess the damping of the induced
vestibulo-ocular reflex. By spinning the child around, either in
your arms or on a swivel chair, a vestibular nystagmus will be
induced, despite the level of vision. If there is visual input once
the spinning is stopped, the nystagmus should damp in 30 to
60 s due to the fixation reflex.
OTHER TESTS
Many ingenious tests have been devised to try to better correlate the vision to a linear acuity and detect amblyopia. The most
popular are forced-choice preferential looking (FPL) and pattern
visual evoked potentials (PVEP). The preferential looking test
using Teller acuity cards assesses grating acuity by presenting
the child with high-contrast gratings of various spatial frequencies along with a paired blank card. Infants will naturally prefer
to look at patterns if they can be seen, and the examiner assesses
whether the child fixates on the pattern or not.36 This test reliably measures grating acuity, but it may take 20 to 30 min to
perform and may be difficult to perform monocularly in children younger than 2 years old33 (Fig. 1-1). Although useful in the
assessment of anisometropic or deprivation amblyopia, this test
FIGURE 1-1. Teller acuity preferential looking apparatus.
10
handbook of pediatric strabismus and amblyopia
FIGURE 1-2. Two Polaroid photogrpahs from MTI PhotoScreener, taken
by a rotating flash. The white crescent in the pupils denotes a refractive
error. The size and location of the crescent in each photo indicate
the type and example of the problem. Findings: hyperopia, 2.00 D;
astigmatism, 1.00 D. The displaced corneal light reflex demonstrates
esotropia.
may underestimate strabismic amblyopia or decreased acuity
secondary to macular disease, in which grating acuity may be
much less affected than vernier and Snellen acuity. Therefore,
although a detected difference confirms amblyopia, a normal
test result does not rule out amblyopia.26 Fixation preference
testing is more reliable in detecting strabismic amblyopia.
PVEP measures the summed occipital cortical response to a
pattern stimulus (Fig. 1-2). This method reflects the activity
from the central retina and is therefore a good assessment of
macular function.32 The resulting cortical potential can be evaluated by a trained electrophysiologist and Snellen acuity can be
roughly estimated. The important parameters of the PVEP waveform are the amplitude and the latency of the spikes. The first
major large positive deflection is the P1 spike, with a normal
latency of 100 ms. Amblyopia diminishes the amplitude, as do
uncorrected refractive error or organic problems. The difficulty
in the test lies in the need for specially trained personnel to
administer and interpret the test and the frequent need for seda-
chapter 1: pediatric eye examination
11
tion to get good results. Although the test can be administered
while the child is awake, poor fixation may give artificially low
results. In the sedated child (chloral hydrate), cycloplegia and
appropriate refractive correction are necessary because retinal
blur also affects test results.45,46 Despite these drawbacks, the
test is often useful to monitor the progress of amblyopia therapy
and to diagnose amblyopia in preverbal children.
Visual Acuity Assessment: Verbal
OPTOTYPE
Older children who are able to identify character shapes can be
assessed with Allen cards, Wright figures, or Lea symbols.18
Often, a child who is not quite verbal, or is too shy to talk, can
be asked to match a sheet of pictured figures to the displayed
cards. The single cards are most useful in the beginning, because
often the child does not attend well to distance targets such as
projected figures. The child can also take a photocopy of the
cards home to practice as a game with parents. It is best to start
close to the child and work backward. In young children, the
endpoint is more often demonstrated by a loss of attention than
by an incorrect response. The disadvantage of single cards is that
they cannot detect the crowding response that is so often seen
in amblyopia. A child may test equally on single optotypes but
show a marked discrepancy with linear optotypes.34 Once equal
acuity is obtained on single cards, it is important to move to
linear testing to confirm the findings. Both single and linear
figures test only to the level of 20/30, which is adequate for children under the age of 3 years.
The next step in preliterate testing is use of the tumbling E,
Wright figures, or HOTV.18 With the “E game,” the child is asked
to point his fingers in the direction of the “legs on the table.”
Often, vertical orientations are more readily confused by children than horizontal directions, and this should be taken into
account when determining the endpoint.39 The HOTV letters
can be easily identified even if the full alphabet is not known.
Again, single cards or linear projection can be used, the latter
being best for amblyopia. These tests go to the 20/20 level and
are slightly more challenging than picture cards.
Once the child is literate, traditional Snellen letters can be
used. For most children, this occurs around age 5 to 6, but do
not confuse knowing the alphabet with being able to distinguish
12
handbook of pediatric strabismus and amblyopia
random letters. If in doubt about the reliability of letter testing,
return to an easier test.
Visual Fields
As soon as a child is able to fix steadily on a target, a rough estimate of visual fields can be obtained. Even if the child will not
tolerate a patch, binocular fields can be checked for homonymous or bitemporal defects. Infants with good fixation will
usually move to an interesting peripheral target once it comes
into view as a result of the fixation reflex. The examiner captures the attention with a central target and then slowly brings
in a peripheral target, watching for the first jump to the peripheral target. In this manner all four quadrants of the peripheral
field can be tested. Patients with posterior optic pathway lesions
that respect the vertical meridian will often ignore a peripherally advancing target until it crosses the midline and then suddenly move and pursue it. A slightly older child of 3 or 4 years
may be able to respond accurately to finger counting by making
a game of copying the examiner’s actions.
Formal visual field testing such as Goldmann perimetry can
sometimes be performed in preschool children. It is important
to have a good idea of the suspected field loss and concentrate
on these areas first. Usually the largest brightest target (V4e) is
best, but smaller targets should be used if the child is capable of
cooperating. Automated fields require prolonged concentration
and steady fixation and are usually not reliable in children less
than 9 to 10 years old. Some newer user-friendly programs are
being developed that shorten testing time enough to make them
more applicable for children (Welch Allyn; frequency doubling
technology or FDT). The tangent screen is also not useful until
reliable verbal responses can be made because it is difficult to
monitor fixation.
Assessment of Color Vision in Children
Although color vision testing is not often done in children, it
helps in the diagnosis of decreased acuity of uncertain etiology
and monitors progression in cases of macular degenerations or
progressive optic neuropathies. Children on retinal toxic drugs
also need to be evaluated. Congenital red-green color defects are
often detected first by the pediatric ophthalmologist as an incidental finding. Screening questions are often useful in detecting
chapter 1: pediatric eye examination
13
these cases, which occur in 8% to 10% of the male population.
The child may confuse green with brown crayons and purple
with blue crayons; he may confuse yellow and red traffic lights
or green and red lines on a paper. Often he will have no trouble
accurately naming colors of large objects but will mistake
smaller colored objects subtending less than 2°.5
The easiest way to screen for color vision defects is with
color plates. There are two popular types of plates, which are
each useful in specific situations. The Ishihara pseudoisochromatic color plates work on the principle of color confusion,
which is common with dichromats and anomalous trichromats.
These plates are extremely sensitive for red-green defects, which
are usually congenital. Most acquired color defects show some
loss in the blue-yellow range, and the Ishihara plates will miss
these patients unless the loss has extended into the red-green
range. The advantage of these plates is that they come in an
illiterate form with geometric shapes that can be traced with
a finger. This design is useful for children who do not know
numbers but still requires the comprehension and fine motor
skills of a 3- to 4-year-old. The Richmond pseudoisochromatic
plates, formerly called American Optical Hardy-Rand-Rittler
(AO-HRR) plates, work on color saturation and can detect both
red-green and blue-yellow defects, making them more useful in
acquired defects; unfortunately, these do not come in an illiterate format. Both tests use many two-digit numbers, which can
intimidate young children, and often their responses are better
if they are asked to name each digit separately. Another good
test for children is the City University Color Vision Test (TCU
test); this uses the colors in the Farnsworth D-15 in a book
format, so that manipulation of the color discs is not necessary.
Unfortunately, it is not the best test for screening, as 20% of
color defectives will pass the test. In general, optic nerve disease
is more likely to affect red-green perceptions, whereas retinal
disease affects blue-yellow discrimination, although there are
many exceptions to this rule.16,17
Assessment of Contrast Sensitivity
Contrast sensitivity represents the minimal amount of contrast
required to resolve various-sized objects from the background.
As such, it is perhaps a more sensitive test of visual function
than Snellen acuity, which only assesses high-contrast resolution. The contrast sensitivity threshold is the minimal amount
14
handbook of pediatric strabismus and amblyopia
of contrast required to detect sinusoidal gratings of different
spatial frequencies. The contrast sensitivity function (CSF) is the
curve obtained by plotting contrast sensitivity against spatial
frequency. The peak of the curve is usually at three to four cycles
per degree, although the maximal contrast sensitivity for each
spatial frequency increases with age to stabilize in adolescence.
Contrast sensitivity may show decrements in many disease
processes despite a normal Snellen acuity, including cerebral
lesions and multiple sclerosis.4 Amblyopes demonstrate a reduction in the CSF curve that may occur only at the peak (highfrequency loss) or throughout the curve (high- and low-frequency
loss).20 This difference persists after Snellen acuity returns to
normal and may be useful in detecting a continued need for
amblyopia therapy.31A Occlusion therapy for amblyopia has also
been shown to reduce contrast sensitivity in the dominant eye,
even without decreased acuity, a type of mild occlusion amblyopia.24 Although testing previously required fairly complex
equipment and was not suitable for young children, contrast sensitivity function can now be reliably measured on children over
4 years using the Vistech wall chart. The chart presents eight
levels of contrast sensitivity (horizontal axis) for each of five
levels of spatial frequency (vertical axis). The gratings are oriented in one of three directions, 15, 0, or 15, and the child
imitates grating orientation with his hand as in the “E game.”
The minimum contrast detectable at each spatial frequency is
recorded and used to plot a contrast sensitivity function curve.
Red Reflex
Evaluation of the red reflex is often forgone in adults because of
the better sensitivity of other available tests; that is, visual
acuity and high-power biomicroscopy of the anterior segment,
lens and vitreous. In children, these tests may not be applicable
for reasons of youth or lack of cooperation. Evaluation of and
especially binocular comparison of the red reflex are invaluable
in assessing media opacities or refractive aberrancies. The red
reflex is best tested by staying far enough away from the child
to illuminate both pupils with the same direct ophthalmoscope
beam and comparing the quality and intensity of the reflexes
between the two eyes. The exam should be done in dim illumination, to encourage pupil dilatation, and with the child’s attention focused in the distance, to avoid a near response. If the
direct ophthalmoscope beam is too strong, the pupils will con-
chapter 1: pediatric eye examination
15
strict and the child will react to the brightness by blinking or
turning away. It is important to assess the reflex both before and
after dilation, especially if there is a visually significant opacity,
to see how much of the undilated pupillary space is obscured.
Dimming of the red reflex is also an important sign in early
endophthalmitis after cataract or strabismus surgery.
Bruckner described a useful test for strabismus using the red
reflex from the direct ophthalmoscope. In the presence of strabismus, the red reflex will be brighter and the pupil will appear
slightly larger in the deviated eye as the patient fixates on the
light. This test can detect deviations as small as three prism
diopters and is especially useful in evaluating postoperative
alignment.38 The test can be carried a step further to evaluate
amblyopia by narrowing the light beam and illuminating one
eye at a time. Fixation with each eye should be steady on the
light; if amblyopia is present, fixation may waver or the eye may
remain deviated in the presence of strabismus.
Photoscreening is a sophisticated application of the red
reflex test. The MTI photoscreener creates a Polaroid picture of
the red reflex that allows assessment of media opacities and
refractive errors (see Fig. 1-2). Although not as sensitive as a traditional eye examination, it is a useful screening tool for general
practitioners.29,30
Pupillary Examination
Normal pupil size varies with age. The newborn has small,
miotic pupils that increase to an average diameter of 7 mm by
age 12 to 13 and then gradually decrease again throughout life.
Reaction to light in infants is often difficult to assess due to the
natural miosis and uncontrolled near response to the examination light. With careful observation, a small light response can
be seen in addition to the near response, but care must be taken
to not mistake one for the other. Older children should have the
near response controlled as much as possible by a distance fixation target. If the examination light is too bright, the child will
close his eyes; when necessary, they must be held open to get
an adequate exam. It is important to rule out an afferent pupillary defect, especially with unilateral visual loss or strabismus.
The swinging flashlight test is routinely used, as in adults, but
care must be taken to aim the light directly into the pupil, especially in strabismus, or an artificial afferent defect may be produced because of incomplete retinal stimulation. It is important
16
handbook of pediatric strabismus and amblyopia
to remember that only dense amblyopia can produce an afferent
defect and that even then it is barely detectable.31 Any afferent
defect of significance in a patient with presumed amblyopia
must be investigated further.
Slit Lamp Examination
Although most young children who cannot cooperate with a slit
lamp examination can be adequately evaluated with a muscle
light, at times more detailed examination is mandatory. There
are several handheld slit lamps, which have the advantage of
being portable and useful in examining supine patients. The disadvantages are their cost and somewhat limited resolution. They
are not very good for assessing mild intraocular inflammation
or subtle corneal abnormalities, but they are the best alternative. There are several other more readily available magnifiers
such as the direct and indirect ophthalmoscope, both of which
can be focused on the anterior segment. Whichever source is
used, the exam is still limited by the child’s resistance and
movement, even while restrained. At times, sedation is required
to obtain the necessary information. Often a child of 1 or 2 years
will allow a quick look at the standard slit lamp; the key is to
keep the light as dim as possible, have in mind what you most
want to see, and look at that first.
Intraocular Pressure Measurements
Certain children are more prone to develop elevated intraocular
pressure, and these patients must have accurate measurements.
Such patients include aphakes, those with any anterior segment
anomaly, those with orbital vascular lesions, or those on
steroids. Most children under 3 years will not cooperate with
routine applanation tonometry and they must be supine (sedated
or restrained). There are several useful handheld tonometers.
The original Schiotz tonometer is easy to use and read but often
is too large for the infant eye. It has the advantage of being less
sensitive to pressures induced by lids or extraocular muscles but
is more affected by ocular rigidity, which tends to be lower in
infants. The Perkins tonometer is an applanation device using
fluorescein and a split prism to assess the pressure. It is highly
accurate at all ranges of pressure but requires some experience
on the part of the examiner to read and is unreliable with an
abnormal corneal surface. Contact must also be made directly
chapter 1: pediatric eye examination
17
on the cornea, which is often difficult in a struggling child with
a good Bell’s phenomenon. The Tonopen is easier to use and can
obtain approximate readings off the sclera or an irregular cornea,
but it is not accurate at high or low pressures, and it is difficult
to hear the tones that signal endpoint when the child is crying.23
The pneumotonometer is easy to use and does not require
corneal contact, but the equipment is less portable than the
other two. Struggling and crying both cause swings in the
intraocular pressure, which must be taken into account, and
pressures taken with a calm child are more accurate. Small
infants who are drowsy will sometimes allow tonometry, especially if they are held in their mother’s arms and given a bottle
or pacifier. Sedation may be necessary for truly accurate readings. Chloral hydrate has the advantage of not lowering the pressure, whereas inhalation anesthetics and Propofol can.3,25 If an
exam under anesthesia is done, the pressure should be measured
as soon as safely possible after induction because it will become
artificially lower with time.13
Keratometry
Assessment of corneal shape can be done qualitatively or quantitatively. Several conditions predispose to corneal astigmatism,
which may be amblyogenic or require contact lens correction.
Children with limbal dermoids or corneal scars may have poor
retinoscopy reflexes, which make accurate assessment of astigmatism difficult. Placido’s disc is a keratoscope that images a
series of concentric light rings on the cornea. The reflected image
can be used to assess the axis of astigmatism and corneal regularity. It is handheld and nonthreatening to most children but
only gives a rough qualitative assessment. More accurate measurements must be obtained with a keratometer; this may
require a sleeping or sedated infant to get accurate readings, and
the standard keratometer can be mounted on a special bar to use
with supine infants.35 Such measurements are helpful for contact
lens fitting. Alcon Corporation has produced a handheld keratometer that has been very helpful in the pediatric age group.
Dilatation and Cycloplegia
Cycloplegia is essential to eliminate uncontrolled accommodation and adequately assess the refractive error in children.
Several agents are available, but the adequacy of cycloplegia, not
18
handbook of pediatric strabismus and amblyopia
the maximal pupil dilatation, is most important. Tropicamide
is not a strong enough cycloplegic for young children; instead,
cyclopentolate, homatropine, or atropine should be used.
Cyclopentolate has the most rapid onset and shortest duration
and thus lends itself to clinic use. For most children, one drop
each of cyclopentolate 1% in combination with phenylephrine
2.5% is adequate.2 Lighter pigmented eyes may only require one
or two applications, whereas darkly pigmented eyes may require
more than three. For children less than 6 months old, it is safer
to use diluted drops such as Cyclomidril (cyclopentolate 0.2%
and phenylephrine 1%). Homatropine 5% is another choice used
for clinic dilation, especially in darkly pigmented patients, but
this drop lasts up to 3 days. Both cyclopentolate and homatropine produce maximal cycloplegia within 30 min to 1 h, but
the former recovers within 1 day.
Table 1-3 lists the various agents available and their effects.
If cycloplegia seems inadequate, based on either pupil size or
changing retinoscopy streak, it is best to use atropine; this is
usually given to the parents to take home and administer. To
avoid toxicity of frequently administered atropine, the drops are
given twice a day for 3 days prior to the visit.15 For infants and
very young children, the drops should be given only once a day
to each eye, with one eye receiving one drop in the morning and
the other eye receiving one drop at night. As an alternative,
atropine 0.5% could be used. Atropine should not be given to
children with possible heart defects or reactive airways. Punctal
occlusion can be performed for 1 min after the drops to decrease
systemic absorption. Parents should be alerted to discontinue
the drops if signs of toxicity or allergy develop (flushing, tachycardia, fever, delirium, lid edema, redness of the eyes). Most
cases of toxicity respond to discontinuation of the drops, but
more severe cases can require treatment with subcutaneous
physostigmine (Eserine), 0.25 mg every 15 min, until improvement occurs. This treatment is useful for toxicity with any of
the antimuscarinic agents. The phenylephrine drops will occasionally cause blanching of the periocular skin, especially where
the drop contacts the skin either by tears or a tissue; this is seen
most often in infants and does not require treatment or discontinuation of the drops. For examination of premature babies,
dilate with cyclomidril (combination of cyclopentolate and
phenylephrine) and tropicamide 0.5%.
Refraction is always an art, especially in a preverbal child.
Care must be taken to control the working distance and the
0.5, 1, 2
2, 5
0.5, 1
Homatropine
Atropine
0.5, 1
Tropicamide
Cyclopentolate
2.5
Phenylephrine
Agent
Strength
(%)
30–60
40–90
30–60
20–40
20
Maximum
(min)
Mydriasis
7–14 days
1–3 days
6–24 h
2–6 h
2–3 h
Recovery
time
TABLE 1-3. Cycloplegic/Mydriatic Agents in Children.
60–180
30–60
25–75
30
None
3–12 days
1–3 days
6–24 h
2–6 h
Recovery
time
Cycloplegia
Maximum
(min)
Side effects
Flushing tachycardia,
fever, delirium
Ataxia
Psychosis, seizure
Tachycardia, hypertension
chapter 1: pediatric eye examination
19
20
handbook of pediatric strabismus and amblyopia
visual axis, or inaccurate readings will be taken. Expertise with
loose trial lenses or a skiascopy rack is important as the
phoropter is useless in small children. If the endpoint is unclear,
it is best to get a second or even third reading, either by repeat
refraction on another visit or by a second refractionist. There are
several handheld autorefractors on the market now that show
promise in pediatric application (Nikon Retinomax, Welch
Allyn Suresight).1,8,42 Cycloplegia may still be necessary to optimize results.
Fundus Examination
An adequate fundus examination is imperative for all children
who present to the ophthalmologist. The extent of the fundus
exam necessary will vary widely depending on the patient. For
most patients visualization of the posterior pole (optic nerve and
macula) is adequate; this is done quickly and easily in most children by keeping the indirect light low and not touching the
child. A brief look may be all that is obtainable by this technique, but this is often adequate. The optic nerve can be examined in more detail with the direct ophthalmoscope if the
examiner is unhurried and stays several inches away from the
child. By staying focused on the retinal vessels, the observer can
see the nerve as it wanders into view while the child is busy
watching a distant target (moving targets, especially videos,
work best for this). For more detailed fundus examination or
examination of the periphery, sedation or restraints are usually
needed because most children will not tolerate the examining
light for extended periods of time. As fundus examination comes
at the end of the clinic visit, the child may be sleeping, especially if they have taken a bottle after the eyedrops, and this
makes the examination much easier. Children less than 2 years
old can usually be restrained adequately to allow a thorough
fundus examination, even to the periphery, whereas older children require examination under anesthesia if uncooperative.
References
1. Adams RJ, et al. Noncycloplegic autorefraction in infants and young
children (ARVO abstract 2108). Investig Ophthalmol Vis Sci 2001;
42.
2. Altman B. Drugs in pediatric ophthalmology. In: Harley RD (ed)
Pediatric ophthalmology. Philadelphia: Saunders, 1983.
chapter 1: pediatric eye examination
21
3. Ausinsch B, Graves SA, Munson ES, Levy NS. Intraocular pressures
in children during isoflurane and halothane anesthesia. Anesthesiology 1975;42:167.
4. Beazley ID, Illingworth DF, Jahn A, Greer DV. Contrast sensitivity
in children and adults. Br J Ophthalmol 1980;64:863.
5. Birch J, Chisholm IA, Kimear P, et al. Clincal testing methods. In:
Pokorney J, Smith VC, Verriest G, Pinckers AJLG (eds) Congenital
and acquired color vision defects. New York: Grune & Stratton,
1979.
6. Boothe RG, Dobson V, Teller DY. Postnatal development of vision
in human and nonhuman primates. Annu Rev Neurosci 1985;8:495.
7. Breton ME, Nelson LB. What do color blind children really see?
Guidelines for clinical prescreening based on recent findings. Surv
Ophthalmol 1983;27:306.
8. el-Defrawy S, Clarke WN, Belec F, Pham B. Evaluation of a handheld autorefractor in children younger than 6. J Pediatr Ophthalmol
Strabismus 1998;5:107.
9. Fox et al. Use of high dose chloral hydrate for ophthalmic exams in
children: a retrospective review of 302 cases. J Pediatr Ophthalmol
Strabismus 1990;27:242.
10. Frankenburg WK, Dodds JB. The Denver developmental screening
test. J Pediatr 1967;71:181.
11. Fulton AB, Hansen RM, Manning KA. Measuring visual acuity in
infants. Surv Ophthalmol 1981;25:352.
12. Dickey CF, Metz HS, Stewart SA, Scott WE. The diagnosis of amblyopia in cross-fixation. J Pediatr Ophthalmol Strabismus 1991;28:171.
13. Dominguez A, Banos MS, Alvarez G, et al. Intraocular pressure measurement in infants under general anesthesia. Am J Ophthalmol 1974;
78:10.
14. Dobson V, Teller DA. Visual acuity in human infants: a review and
comparison of behavioral and electrophysiologic studies. Vision Res
1978;18:1469.
15. Gilman AG, Goodman LS, Gilman A. The pharmacological basis of
therapeutics, 6th edn, 1980:11.
16. Glaser JS. Neuro-ophthalmologic examination: general considerations and special techniques. In: Glaser JS (ed) NeuroOphthalmology. Philadelphia: Lippincott, 1990.
17. Glaser JS. In: Glaser JS (ed) Neuro-Ophthalmology. Philadelphia:
Lippincott, 1990.
18. Graf MH, Becker R, Kaufmann H. Lea Symbols: visual acuity assessment and detection of amblyopia. Graefe’s Arch Clin Exp Ophthalmol 2000;238:53.
19. Hered RW, Murphy S, Clanay M. Comparison of the HOTV and Lea
Symbols chart for preschool vision screening. J Pediatr Ophthalmol
Strabismus 1997;34:24.
20. Hess RF, Howell ER. The threshold contrast sensitivity function in
strabismic amblyopia: evidence for a two type classification. Vision
Res 1977;17:1049.
22
handbook of pediatric strabismus and amblyopia
21. Hoyt CS, Nickel BL, Billson FA. Ophthalmological examination of
the infant. Dev Aspects Surv Ophthalmol 1982;26:177.
22. Judisch GF, Anderson S, Bell WE. Chloral hydrate sedation as a substitute for examination under anesthesia in pediatric ophthalmology.
Am J Ophthalmol 1980;89:560.
23. Kao SF, Lichter PR, Bergstrom TJ, et al. Clinical comparison of the
oculab tonopen to the Goldmann applanation tonometer. Ophthalmology 1987;94:1541.
24. Koskela PU, Hyvarinen L. Contrast sensitivity in amblyopia. III.
Effect of occlusion. Acta Ophthalmol 1986;64:386.
25. Laurelti GR, Laurelti CR, Laurelti-Filho A. Propofol decreases ocular
pressure in outpatients undergoing trabeculectomy. J Clin Anesth
1997;9:289.
26. Mayer DL, Fulton AB, Rodier D. Grating and recognition acuities of
pediatric patients. Ophthalmology 1984;91:947.
27. McDonald MA. Assessment of visual acuity in toddlers. Surv
Ophthalmol 1986;31:189.
28. McMillan F, Forster RK. Comparison of MacKay-Marg, Goldmann,
and Perkins tonometers in abnormal corneas. Arch Ophthalmol
1975;93:420.
29. Oher WL, Scolt WE, Holgado SI. Photoscreening for amblyogenic
factors. J Pediatr Ophthamol Strabismus 1995;32:289.
30. Simons BD, Siathowski RM, Schiffmen JC, Berry BE, Flynn JJ. Pedatric photoscreening for strabismus and refractive errors and a highrisk population. Ophthalmology 1999;106:1073.
31. Portnoy JZ, Thompson HS, Lennarson L, Corbett JJ. Pupillary defects
in amblyopia. Am J Ophthalmol 1983;96:609.
31a. Rogers GL, Bremer DL, Leguire LE. The contrast sensitivity function
and childhood amblyopia. Am J Ophthalmol 1987;104:64.
32. Sokol S. Visually evoked potentials: theory, techniques and clinical
applications. Surv Ophthalmol 1976;21:18.
33. Sokol S, Hansen VC, Moskowitz A, et al. Evoked potential and
preferential looking estimates of visual acuity in pedatric patients.
Ophthalmology 1983;90:552.
34. Stuart JQ, Burian HM. A study of separation difficulty: its relationship to visual acuity in normal and amblyopic eyes. Am J Ophthalmol 1962;53:471.
35. Szirth B, Matsumoto E, Murphree AL, Wright KW. Attachment for
the Bausch and Lomb keratometer in pediatry. J Pediatr Ophthalmol
Strabismus 1987;24:186.
36. Teller DY, Morse R, Borton R, Regan D. Visual acuity for vertical
and diagonal gratings in human infants. Vision Res 1974;14:1433.
37. Terndrup TE, Cantor RM, Madden MD. Intramuscular meperidine,
promethazine, and chlorpromazine: analysis of use and complications in 487 pediatric emergency department patients. Ann Emerg
Med 1989;18:528.
38. Tongue AC, Cibis GW. Bruckner test. Ophthalmology 1981;88:
1041.
chapter 1: pediatric eye examination
23
39. von Noorden GK. Symptoms in heterophoria and heterotropia and
psychologic effects of strabismus. In: Klein EA (ed) Binocular vision
and ocular motility. St. Louis: Mosby, 1990.
40. Watcha MF, Chu FC, Stevens JL, Forestner JE. Effects of halothane
on intraocular pressure in anesthetized children. Anesth Analg 1990;
71:181.
41. Weiner N. Atropine, scopolamine, and related antimuscarinic drugs.
In: Gilman AG, Goodman LS, Gilman A (eds) The pharmacological
basis of therapeutics, 6th edn. New York: Macmillan, 1980.
42. Wesemann W, Dick B. Accuracy and accommodation capability of a
handheld autorefractor. J Cataract Refract Surg 2000;26:62.
43. Whitford AM, Hone SW, O’Hare B, Magner J, Eustace P. Intraocular
pressure changes following laryngeal mask airway insertion: a comparative study. Anesthesia 1997;52:794.
44. Wright KW, Edelman PM, Walonker F, Yiu S. Reliability of fixation
preference testing in diagnosing amblyopia. Arch Ophthalmol 1986;
104:549–553.
45. Wright KW, Eriksen J, Shors TJ. Detection of amblyopia with P-VEP
during chloral hydrate sedation. J Pediatr Ophthalmol Strabismus
1987;24:170–175.
46. Wright KW, Eriksen J, Shors TJ, Ary JP. Recording pattern visual
evoked potentials under chloral hydrate sedation. Arch Ophthalmol
1986;104:718.
47. Wright KW, Walonker F, Edelman P. 10-diopter fixation test for
amblyopia. Arch Ophthalmol 1981;99:1242.
48. Zipf RF. Binocular fixation pattern. Arch Ophthalmol 1976;94:401–
405.
2
Anatomy and Physiology
of Eye Movements
Kenneth W. Wright
OCULAR POSITION
Within the orbit, the eye is suspended by six extraocular muscles
(four rectus muscles and two oblique muscles), suspensory ligaments, and surrounding orbital fat (Fig. 2-1). A tug-of-war exists
between the rectus and oblique muscles. The four rectus
muscles insert anterior to the equator, and pull the eye posteriorly, while the two oblique muscles insert posterior to the
equator providing anterior counterforces. Posterior orbital fat
also pushes the eye forward. If rectus muscle tension increases,
the eye will be pulled back causing enophthalmos and lid fissure
narrowing. Simultaneous cocontraction of the horizontal rectus
muscles in Duane’s syndrome, for example, can cause significant lid fissure narrowing and enophthalmos. In contrast,
decreased rectus muscle tone causes proptosis and lid fissure
widening. Conditions such as muscle palsies or a detached
rectus muscle allow the eye to move forward and result in lid
fissure widening. Rectus muscle tightening procedures such as
resections tend to cause lid fissure narrowing whereas loosening procedures such as rectus recessions induce lid fissure
widening. When the eye is looking straight ahead with the visual
axis parallel to the sagittal plane of the head, the eye is in
primary position. The vertical rectus muscles follow the orbits
and diverge from the central sagittal plane of the head by 23°.
Thus, the visual axis in primary position is 23° nasal to the
muscle axis of the vertical rectus muscles (Fig. 2-2). This discrepancy between the vertical rectus muscle axis and the visual
axis of the eye explains the secondary and tertiary functions of
the vertical rectus muscles (see muscle functions, following).
24
Whitnall's lig.
Superior oblique m.
Levator palpebrae
Müller's m.
Superior rectus m.
Intraconal fat
Lateral rectus m.
Inferior rectus m.
Lockwood's lig.
Extraconal fat
Inferior oblique m.
FIGURE 2-1. Side view of extraocular muscles. Note that the rectus
muscles pull the eye posteriorly while the oblique muscles pull the eye
anteriorly.
FIGURE 2-2. Diagram shows visual axis versus muscle/orbital axis. Note
that the visual axes parallel the central sagittal plane, while the orbital
axis of each eye diverges 23° from the visual axis.
25
26
handbook of pediatric strabismus and amblyopia
The term position of rest refers to the position of the eyes when
all the extraocular muscles are relaxed or paralyzed. Normally,
the position of rest is divergent (i.e., exotropic), with the visual
axis in line with the orbital axis. The eyes of a patient under
general anesthesia are usually deviated in a divergent position.
OCULAR MOVEMENTS
Ductions
The term ductions is used to describe monocular eye movements without regard for the movement of the fellow eye (Fig.
2-3). Ductions result from an extraocular muscle contraction
A
B
E
C
F
D
G
FIGURE 2-3A–G. Diagram of ductions, which are monocular eye
movements.
27
chapter 2: anatomy and physiology of eye movements
TABLE 2-1. Extraocular Muscles.
Muscle
Medial
rectus
Lateral
rectus
Superior
rectus
Approximate
muscle
length
(mm)
Origin
40
40
40
Annulus
of Zinn
Annulus
of Zinn
Annulus
of Zinn
Anatomic
insertion
(mm)
Tendon Arc of
length contact
(mm)
(mm)
Action
from
primary
position
5.5
4
6
Adduction
7.0
8
10
Abduction
8.0
6
6.5
6.5
7
7
26
12
1
15
Inferior
rectus
40
Annulus
of Zinn
Superior
oblique
32
Inferior
oblique
37
Orbit apex From
above
temporal
annulus
pole of
of Zinn
superior
rectus to
within
6.5 mm
of optic
nerve
Lacrimal
Macular
fossa
area
Elevation
Adduction
Intorsion
Depression
Adduction
Extorsion
Intorsion
Depression
Abduction
Extorsion
Elevation
Abduction
that pulls the scleral insertion site toward the muscle’s origin
while the opposing extraocular muscle simultaneously relaxes.
The contracting muscle is referred to as the agonist and the
relaxing muscle as the antagonist. An upward movement of an
eye is referred to as supraduction or sursumduction, a downward movement is termed infraduction or dorsumduction, a
nasal-ward movement is termed adduction, and a temporal
movement is termed abduction. Torsional rotations (twisting
movements) are known as cycloductions, with incycloduction
(intorsion) referring to a nasal rotation of the 12 o’clock position
of the cornea and excycloduction (extorsion) referring to a temporal rotation of the 12 o’clock position.
Muscle Action Versus Field of Action
The terms “muscle action” and the “field of action” are often
confused. Muscle action refers to the effect of muscle contraction on the rotation of the eye when the eye starts in primary
position. Table 2-1 lists the muscle actions of each extraocular
muscle. Horizontal rectus muscles have but one action: horizontal rotation of the eye. Vertical rectus and oblique muscles,
28
handbook of pediatric strabismus and amblyopia
however, have three actions: vertical, horizontal, and torsional.
The most robust action is termed the primary action, followed
by the less obvious secondary and tertiary actions. It is important to remember the classic descriptions of primary, secondary
and tertiary muscle actions as they relate to the eye when it is
in primary position.
In contrast, the field of action of a muscle is the position of
gaze when an individual muscle is the primary mover of the eye.
Granted, virtually all eye movements are the result of combined
contraction and relaxation of multiple muscles, but there are
eight positions of gaze where one muscle provides the dominant
force (Fig. 2-4). For example, when one looks up, the brain
recruits both the superior rectus and the inferior oblique
muscles. Looking up and nasal, however, is the primary function of the inferior oblique muscle, so this is the field of action
of the inferior oblique muscle. A muscle’s function is best evaluated by having the patient look into the field of action of the
FIGURE 2-4. Diagram of the field of action of the extraocular muscles.
Arrows point to the quadrant where the specified muscle is the major
mover of the eye. SR, superior rectus; IR, inferior oblique; MR, medial
rectus; SO, superior oblique; IO, inferior oblique; IR, inferior rectus; LR,
lateral rectus.
chapter 2: anatomy and physiology of eye movements
29
muscle. Thus, even though the secondary action of the inferior
oblique muscle is abduction, evaluate inferior oblique function
by having the patient look “up and nasal.” A patient with an
inferior oblique palsy will show limitation of eye movement up
and nasal. Note, for straight upgaze, the superior rectus muscle
is the major elevator, and for straight down-gaze the inferior
rectus is the major depressor, with the oblique muscles contributing little.
Smooth Pursuit Versus Saccadic Eye Movements
There are two basic forms of eye movements: smooth pursuit
and saccadic. Smooth pursuit eye movements are generated in
the occipital parietal temporal cortex, with the right cortex controlling movements to the right and the left cortex controlling
movements to the left. In humans, smooth pursuit first occurs
at 4 to 6 weeks of age. These are slow accurate eye movements
requiring visual feedback from central foveal fixation. Smooth
pursuit eye movements can follow visual targets moving at
velocities up to 30° per second (30°/s). Clinically, accurate
smooth pursuit indicates central fixation and in preverbal children is an indication of good vision.
Saccadic movements are rapid eye movements with velocities usually ranging from 200° to 700°/s, but saccades have been
recorded up to 1000°/s. The peak velocity increases as the amplitude of the movement increases, and this relationship is termed
the main sequence. Saccades are movements used to keep up
with targets moving too fast for smooth pursuit and for quick
refixation from one target to another. Saccadic eye movements
develop before smooth pursuits, occurring as early as 1 week of
age. Saccadic eye movements are generated in the frontal lobes
and are under contralateral control; that is, right frontal lobe
stimulation will result in a saccadic eye movement to the left.
Saccadic movements can be voluntarily initiated, but they are
not voluntarily controlled, and there is no significant visual
feedback to adjust the amount of movement. It is thought that
the amplitude of a saccadic movement is preprogrammed based
on the degree of retinal eccentricity of the target; this is why
saccadic movements are termed ballistic, analogous to the ballistic trajectory of a cannon ball. The neuronal signal that initiates a saccade consists of a burst of high-frequency discharge or
pulse to the agonist and inhibition of the antagonist. Because all
neurons available are activated for eye movements greater than
30
handbook of pediatric strabismus and amblyopia
5°, the magnitude of a saccade is determined by the duration of
the pulse. At the end of a saccade, tonic neuronal firing of the
agonist and antagonist muscles occurs to hold the eye position
referred to as the step. Vision during a saccadic eye movement
is suspended or suppressed. Some have used the term saccadic
omission for the process of cortical suppression.1 A tremendous
force is required to produce a saccadic eye movement; therefore,
the presence of saccadic eye movements indicates “good” muscle
function. Only rectus muscles generate saccadic eye movements. When evaluating a patient with limited ductions, look for
the presence of a normal saccadic eye movement into the field
of limited ductions. If there is a brisk saccade in the direction of
the limitation, this indicates good muscle function and suggests
the limited movement is caused by restriction, not a muscle
paresis.
Optokinetic nystagmus (OKN) can be generated by a slowly
rotating drum with stripes and used to evaluate smooth pursuit
and saccadic eye movements. As the drum rotates toward the
patient’s right, there is a smooth pursuit eye movement to the
right to follow the stripe. As the end of the stripe passes, there
is a fast saccadic movement to the left to refixate on the next
stripe. At target velocities less than 30°/s, smooth pursuit keeps
pace with the target. At velocities between 30° and 100°/s,
smooth pursuit movements progressively lag behind the target.
At velocities greater than 100°/s, OKN is not evoked. OKN can
be used to evaluate saccadic and smooth pursuit eye movements. Look at the fast phase of OKN to evaluate saccadic movements and the slow phase to evaluate smooth pursuit.
ANATOMY OF THE EYE MUSCLES
Rectus Muscles
The four rectus muscles originate at the orbital apex at the
annulus of Zinn and course anteriorly to insert on the anterior
aspect of the globe. The “straight” course of the rectus muscles
gives rise to the term rectus. The rectus muscle insertions form
a progressive spiral termed the spiral of Tillaux around the
corneal limbus. The medial rectus muscle is the closest to the
limbus (5.5 mm), then the inferior rectus (at 6.5 mm), the lateral
rectus (at 7.0 mm), and the superior rectus is the furthest from
the limbus (8.0 mm). The muscle–scleral insertion line has
chapter 2: anatomy and physiology of eye movements
31
FIGURE 2-5. Diagram of distance of the rectus muscle insertions from
the limbus (in millimeters, mm). Note that the medial rectus muscle
inserts closest to the limbus and the distances increase, going counterclockwise from the medial rectus toward the superior rectus, which
inserts furthest from the limbus.
a horseshoe configuration with the rounded apex pointing
toward the cornea (Fig. 2-5). One can remember this as the horseshoes are always galloping toward the cornea. The scleral thickness behind the rectus insertions is the thinnest of the eye, being
only 0.3 mm thick. Hooking a rectus muscle requires passing
the hook several millimeters behind the central muscle insertion to clear the posterior aspect of the horseshoe insertion. The
widths of the insertions are all approximately 10 mm, and the
distance between insertions or intermuscle spacing is only 6 to
8 mm. Because of the proximity of the rectus muscle insertions,
it is easier than you might think to hook the wrong muscle
during strabismus surgery. An important number to remember
is the rectus muscle length, which is 40 mm for all rectus
muscles and is also the length of the orbit. Rectus muscles are
innervated from the intraconal side of the muscle belly at the
junction of the anterior two-thirds and posterior one-third of the
muscle.
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handbook of pediatric strabismus and amblyopia
HORIZONTAL RECTUS MUSCLES
The horizontal rectus muscles consist of the medial and lateral
rectus muscles. In primary position, each muscle has one action:
the medial rectus is an adductor and the lateral rectus is an
abductor (Fig. 2-6). When the eye elevates or depresses away
from primary position, however, the horizontal rectus muscles
take on secondary vertical functions. When the eye is “up,” the
horizontal rectus muscles take on a secondary action of supraduction, and when the eye is “down,” the secondary action is
infraduction (Fig. 2-7). In addition, if one surgically transposes a
horizontal rectus muscle insertion up, the muscle becomes an
elevator in addition to the horizontal function. Supraplacing
the horizontal rectus insertions during strabismus surgery will
induce a hyperdeviation whereas infraplacement induces a
hypodeviation. Vertically displacing the medial and lateral
rectus muscle insertion is an excellent way to correct small vertical deviations when performing a recession/resection procedure. In Duane’s syndrome, the common finding of upshoot
and downshoot is probably caused by the secondary elevator
and depressor actions of the cocontracting horizontal rectus
FIGURE 2-6. Diagram of simple function of the medial rectus (MR) and
lateral rectus (LR) muscle with the eye in primary position.
chapter 2: anatomy and physiology of eye movements
33
A
B
C
FIGURE 2-7A–C. Diagram of secondary actions of the medial rectus
when the eye rotates up or down. These secondary actions also relate to
the lateral rectus. (A) Globe rotated superiorly; now the medial rectus acts
as an elevator in addition to its adduction or horizontal function. (B) In
the center part of the figure, the medial rectus is a pure adductor. (C)
Globe rotated down; in this position, the medial rectus acts as a depressor and an adductor.
34
handbook of pediatric strabismus and amblyopia
muscles. Remember, the secondary vertical functions of the
horizontal rectus muscles occur only when the eye is rotated
vertically off primary position.
MEDIAL RECTUS MUSCLE
The medial rectus muscle is innervated by the lower division of
the oculomotor nerve (third cranial nerve) and, in primary position, is a pure adductor. The medial rectus is uniquely diminutive. It has the shortest arc of scleral contact (6 mm) and the
shortest tendon length of the rectus muscles (4 mm). The inferior oblique muscle actually has the shortest tendon (1 mm)
of the extraocular muscles, but it is not a rectus muscle. (Be
careful; this could be the basis of a trick question.) Of the
extraocular muscles, the medial rectus inserts closest to the
limbus and is therefore susceptible to insult during anterior
segment surgical procedures. Inadvertent removal of the medial
rectus muscle is a well-known complication of pterygium
removal. The medial rectus is also unique, as it is the only rectus
muscle without fascial connections to an adjacent oblique
muscle. This lack of oblique muscle connection makes the
medial rectus the most difficult to surgically retrieve if lost.
Once disinserted, the medial rectus is free to retract completely
off the globe into the orbital fat, making retrieval extremely difficult and, in some cases, almost impossible.
LATERAL RECTUS MUSCLE
The lateral rectus muscle is innervated by the sixth cranial nerve
and is a pure abductor. In direct contrast to the medial rectus
muscle, the lateral rectus has the longest tendon (8 mm) and the
longest arc of scleral contact (10 mm) of the rectus muscles. Be
careful, the “longest” cited above refers to only rectus muscles,
as the superior oblique tendon has the longest arc of contact and
tendon length of all the extraocular muscles. (This could be the
source of another trick question.) The long arc of contact occurs
because the lateral rectus muscle initially has a divergent course
following the lateral wall of the orbit. Then, in the anterior orbit,
it turns nasally, wrapping around the globe to its scleral insertion point (see Fig. 2-6). This temporal to nasal wrap around the
globe accounts for the long arc of contact. The inferior border of
the lateral rectus muscle courses above the inferior oblique
insertion, and there are connective tissue bands connecting the
lateral rectus muscle to the inferior oblique muscle.13 This is an
important anatomic relationship, because a lost lateral rectus
chapter 2: anatomy and physiology of eye movements
35
muscle will come to rest at the insertion of the inferior oblique
muscle. The surgeon can often find a lost lateral rectus muscle
by tracing the inferior oblique muscle back to its insertion.
VERTICAL RECTUS MUSCLES
EA
XIS
VISUAL AXIS
The superior and inferior rectus muscles are the vertical rectus
muscles and are the major elevators and depressors of the eye,
respectively. The vertical rectus muscles have secondary and
tertiary actions because, in primary position, the muscle axis
is 23° temporal to the visual axis of the eye (Figs. 2-2, 2-8A).
MU
SC
L
23°
TEMPORAL
VI
MUSUA
SC L &
LE
A
XIS
NASAL
MU
SC
LE
AX
IS
A
B
VISUAL AXIS
C
FIGURE 2-8A–C. Functions of the vertical rectus muscles with the eye
in various positions of gaze. (A) The eye is in primary position with the
visual axis 23° nasal to the muscle axis. (B) The eye is abducted 23° from
the primary position, and the visual axis is in line with the muscle axis.
(C) The eye is abducted more than 23° from the primary position, and the
visual axis is now temporal to the muscle axis.
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handbook of pediatric strabismus and amblyopia
Their secondary action is adduction, and it occurs because the
vertical rectus muscles pull the front of the eye nasal to the
visual axis. Tertiary actions are torsional, consisting of intorsion for the superior rectus muscle and extorsion for the
inferior rectus muscle. These secondary and tertiary muscle
actions are dependent on eye position. If the eye is abducted
23°, for example, the muscle and visual axes will be in line, and
the vertical rectus muscles lose their secondary and tertiary
actions, leaving only their vertical actions (Fig. 2-8B). In this
position of 23° abduction, the superior rectus acts purely as an
elevator, and the inferior rectus purely as a depressor. With
further abduction past 23°, the secondary and tertiary actions
of the vertical rectus muscles return, but they are different.
The secondary action for both vertical rectus muscles becomes
abduction, and the tertiary functions reverse, becoming extorsion for the superior rectus and intorsion for the inferior rectus
muscle (Fig. 2-8C).
SUPERIOR RECTUS MUSCLE
The upper division of the oculomotor nerve innervates the
superior rectus muscle. It is the major elevator of the eye,
and its actions include supraduction (primary), adduction
(secondary), and intorsion (tertiary). The superior rectus
muscle overlies the superior oblique tendon and has connective tissue connections to the superior oblique tendon below
and the levator palpebrae muscle above (Fig. 2-9). This anatomic relationship to the levator palpebrae is important because
a large superior rectus recession can cause upper lid retraction and lid fissure widening. On the other hand, a superior
rectus resection pulls the upper lid down, resulting in lid fissure
narrowing. Lid fissure changes associated with superior rectus
surgery can be minimized by surgically removing the fascial
connections between the levator and the superior rectus
muscles.
INFERIOR RECTUS MUSCLE
The inferior rectus muscle is innervated by the lower division
of the oculomotor nerve and is the principal depressor of the
eye. Actions of the inferior rectus muscle include infraduction
(primary), adduction (secondary), and extorsion (tertiary). The
inferior rectus is sandwiched between the inferior oblique below
chapter 2: anatomy and physiology of eye movements
37
FIGURE 2-9. Diagram of the eye and orbit from a top view looking down
on the superior rectus (SR) muscle. Note that the superior rectus muscle
overlies the superior oblique (SO). T, temporal; N, nasal.
and the sclera above (Fig. 2-10). The fascial connection between
the inferior rectus muscle, the inferior oblique muscle, and the
lower lid retractors (capsulopalpebral fascia) is termed Lockwood’s ligament (Fig. 2-11).17 These fascial connections are
responsible for the eyelid changes that often occur after inferior
rectus surgery. An inferior rectus recession results in lower lid
retraction with lid fissure widening, and a resection causes lid
advancement with lid fissure narrowing. If the inferior rectus is
inadvertently disinserted or lost during surgery, these connections will hold the inferior rectus to the inferior oblique and
keep it from retracting posteriorly. The surgeon who is in search
of a lost inferior rectus muscle can usually find it lying between
the inferior oblique and sclera.
FIGURE 2-10. Diagram of the eye and orbit viewed from below. Note
that the inferior oblique (IO) underlies the inferior rectus (IR) muscle.
Conjunctiva
Tarsus
Fornix
Tenon's capsule
Orbicularis m.
Inf. rectus m.
ITM
CPF
Orbital septum
CPH
Lockwood's lig.
Inf. oblique m.
38
chapter 2: anatomy and physiology of eye movements
39
FIGURE 2-12. Diagram of the superior oblique (SO) muscle and tendon.
The functional muscle axis extends from the trochlea to the superior
oblique insertion. The muscle axis is 54° nasal to the visual axis.
OBLIQUE MUSCLES
Like the vertical rectus muscles, the oblique muscles have
primary, secondary and tertiary actions. In the case of the
oblique muscles, this is because the functional muscle axis is
approximately 50° nasal to the visual axis, and the insertion
extends posterior to the equator of the eye (Figs. 2-12, 2-13). By
FIGURE 2-11. Diagram of the relationship between the inferior rectus,
inferior oblique, lower lid retractors, and Lockwood’s ligament. The inferior tarsal muscle (ITM) courses from the posterior border of the tarsus
toward the inferior oblique muscle. It then passes between the inferior
oblique muscle and the inferior rectus muscle to insert at the capsulopalpebral head (CPH). The CPH extends posteriorly to connect the inferior oblique to the inferior rectus muscle. The capsulopalpebral fascia
(CPF) is the anterior extension of the CPH and courses from the inferior
oblique anteriorly to the tarsus along with the ITM. “Lockwood’s ligament” (Lockwood’s lig.) consists of these fascial attachments that connect the lower lid, inferior rectus, and inferior oblique muscles.
40
handbook of pediatric strabismus and amblyopia
FIGURE 2-13. Diagram of the inferior oblique (IO) from a view from
below. The inferior oblique muscle axis is 51° nasal to the visual axis.
comparing Figures 2-12 and 2-13, one can see that the oblique
muscles have an almost identical functional course with both
muscle axes at approximately 50°. The posterior muscle–scleral
insertion gives the oblique muscles their seemingly paradoxical
vertical functions, with the superior oblique being a depressor
and the inferior oblique an elevator. The oblique muscles have
no anterior ciliary blood supply, and they do not contribute to
the anterior segment circulation. Remember that the “oblique
muscles always course below the corresponding vertical rectus
muscle” (Fig. 2-14).
SUPERIOR OBLIQUE MUSCLE
The primary action of the superior oblique muscle is intorsion,
but it also acts as a depressor (secondary) and an abductor
(tertiary). Depression and abduction occur as the back of the eye
is pulled up and in toward the trochlea. The superior oblique
chapter 2: anatomy and physiology of eye movements
41
muscle originates at the orbital apex just above the annulus of
Zinn and gradually becomes tendon at the trochlea (see Fig.
2-12). After passing through the trochlea, the superior oblique
tendon reverses course and turns in a posterior temporal direction to pass under the superior rectus muscle to insert on sclera
along the temporal border of the superior rectus muscle (Fig.
2-14). Even though the anatomic origin is at the apex of the orbit,
the functional origin of the superior oblique is at the trochlea.
This tendon is the longest tendon of the extraocular muscles,
26 mm in length. The tendon insertion fans out broadly under
the superior rectus muscle, extending from the temporal pole
of the superior rectus muscle to 6.5 mm from the optic nerve.13
Fascial attachments connect the superior oblique tendon to the
superior rectus muscle above and to the sclera below.13 The
tendon insertion can be functionally divided into two basic
parts: the anterior one-third and the posterior two-thirds.
Posterior fibers are responsible for depression and abduction
whereas tendon fibers anterior to the equator are devoted to
intorsion. This distinction between anterior and posterior
superior oblique tendon fibers is important because one can
FIGURE 2-14. Diagram of posterior anatomy of the eye and muscles.
Note the proximity of the inferior oblique to the macula and vortex veins
(vv). The posterior aspect of the superior oblique insertion is in proximity to the superior temporal vortex vein and is approximately 6 to 8 mm
from the optic nerve.
42
handbook of pediatric strabismus and amblyopia
manipulate these functions surgically to correct specific motility disorders. The Harada–Ito procedure, for example, involves
tightening the anterior fibers of the superior oblique tendon.
Because the anterior tendon fibers intort the eye, the Harada–Ito
procedure can be used to treat extorsion associated with superior oblique palsy.
The trochlear nerve innervates the superior oblique muscle
at its midpoint from outside the muscle cone. The superior
oblique muscle is, in fact, the only eye muscle innervated on the
outer surface of the muscle belly. This unique innervation
explains why a retrobulbar anesthetic block results in akinesia
of all the eye muscles except the superior oblique muscle.
TROCHLEA
The trochlea (Latin for pulley) is a cartilaginous U-shaped structure attached to the periosteum that overlies the trochlear fossa
of the frontal bone in the superior nasal quadrant of the orbit. It
has been taught that the superior oblique tendon moves through
the trochlea much like a rope through a pulley. Anatomic
studies have shown, however, that tendon movement is not that
simple. Within the trochlea is a connective tissue capsule with
connective tissue bands that unite the superior oblique tendon
to the surrounding trochlea (Fig. 2-15).46 Some of the tendon
slackening distal to the trochlea may come from a telescoping
elongation of the central tendon (Fig. 2-16).19 This telescoping
elongation of the tendon appears to be caused by movement of
the central tendon fibers that have scant interfiber connections.
Thus, the mechanism for tendon movement is complex, with
at least two mechanisms: (1) tendon movement through
the trochlea (pulley and a rope) and (2) tendon elongation
(telescoping).
INFERIOR OBLIQUE MUSCLE
It is the principal extortor of the eye; however, other actions
include elevation (secondary) and abduction (tertiary). The inferior oblique muscle originates at the lacrimal fossa located at
the anterior aspect of the inferior nasal quadrant of the orbit (see
Fig. 2-13). Starting at the lacrimal fossa, the inferior oblique
muscle courses posteriorly and temporally underneath the inferior rectus muscle to its scleral insertion, which is adjacent to
the inferior border of the lateral rectus muscle (see Fig. 2-14).
The inferior oblique muscle has fascial connections to the lower
chapter 2: anatomy and physiology of eye movements
43
A
B
FIGURE 2-15A–B. Histology of the trochlea. (A) Low-magnification cross
section of midtrochlea. H&E stain. Note horseshoe shape of cartilaginous
tissue and the fibrous connective tissue ring that surrounds the superior
oblique muscle. At this cross section, the superior oblique is two-thirds
muscle and one-third tendon. (B) High-magnification cross section of
superior oblique muscle in midtrochlea shows fibrous connective tissue
ring connecting to muscle via fine fascial septae.
44
handbook of pediatric strabismus and amblyopia
C
D
FIGURE 2-15C–D. (C) Low-magnification cross section of superior
oblique tendon exiting the trochlea. Note small area of cartilage and larger
ring of fibrous connective tissue that surrounds the superior oblique
tendon as the tendon capsule. At this section, the superior oblique is onethird muscle and two-thirds tendon. (D) High magnification of the superior oblique tendon exiting the trochlea. Note the superior oblique tendon
capsule consists of circumferential onionskin layers of fibrous connective
tissue. The tendon capsule is attached to the superior oblique tendon
capsule by circumferential connective tissue fibers. (From Wright et al.,
Ref. 46, with permission.)
chapter 2: anatomy and physiology of eye movements
45
FIGURE 2-16. Diagram of anatomy of the trochlea. Note the central
fibers of the tendon expand and retract more than the peripheral tendon
fibers. (From Ref. 19, with permission.)
border of the lateral rectus muscle and to the overlying inferior
rectus muscle via Lockwood’s ligament (see Fig. 2-11). When the
inferior oblique muscle contracts, it pulls the back of the eye
down and in toward the insertion at the lacrimal fossa. This
action produces elevation, abduction, and extorsion (Fig. 2-14).
Important structures near the inferior oblique insertion include
the macula and inferior temporal vortex vein (Fig. 2-14).
The inferior oblique muscle has only 1 mm of tendon at its
insertion.
The inferior oblique muscle is innervated by the inferior
branch of the third nerve at a point just lateral to the inferior
rectus muscle. Innervation occurs at the posterior aspect of the
inferior oblique muscle belly, and the nerve is accompanied by
blood vessels forming a neurovascular bundle. This neurovascular bundle is surrounded by an inelastic capsule of collagen
tissue that protects the inferior oblique nerve from damage
caused by stretching.39 The neurovascular bundle with its insertion into the posterior aspect of the muscle is an important
structure in regard to inferior oblique surgery. Anterior transposition of the inferior oblique muscle is an effective surgical
46
handbook of pediatric strabismus and amblyopia
procedure used to treat inferior oblique muscle overaction;
however, the complication of postoperative limited elevation
has been reported.5,25,26,47 This complication is caused by anteriorizing the posterior muscle fibers at, or anterior to, the inferior
rectus muscle insertion, because this tightens the inelastic neurovascular bundle.38 The tight neurovascular bundle acts as the
functional origin of the inferior oblique muscle and changes
the action of the inferior oblique muscle from an elevator to
a depressor (Fig. 2-17A).16 This author has coined the term
J-deformity for this acute bend of the anteriorized inferior
oblique.47 When the patient looks up, the inferior oblique muscle
contracts along with the superior rectus muscle, but the anteri-
Inferior oblique
muscle
Neurofibrovascular
bundle
Maxillary bone
Inferior rectus
muscle
FIGURE 2-17A,B. (A) Diagram of inferior oblique muscle anteriorization
with “J-deformity.” The J-deformity is caused by anterior placement of
the posterior inferior oblique muscle fibers to the level of the inferior
rectus muscle insertion. Because the neurovascular bundle of the inferior
oblique muscle inserts in the posterior muscle belly, anteriorization of
the posterior muscle fibers produces a tight neurovascular bundle; this
causes limited elevation of the eye as active contraction of the anteriorized inferior oblique muscle pulls against the tight neurovascular
bundle.16
chapter 2: anatomy and physiology of eye movements
47
Vortex
vein
Inferior oblique
muscle
Inferior rectus
muscle
FIGURE 2-17A,B. (B) Diagram of the “graded anteriorization” technique
described by Guemes and Wright that is effective in reducing inferior
oblique overaction but avoids the postoperative complication of limited
elevation.16 The new inferior oblique muscle insertion is shown being
placed 1 mm behind the inferior rectus muscle insertion, and the posterior muscle fibers are placed an additional 4 to 5 mm further posterior,
and parallel to the inferior rectus muscle axis. Note that the posterior
placement of the posterior muscle fibers avoids the J-deformity. By
keeping the posterior muscle fibers posterior to the anterior fibers and
avoiding the J-deformity, the neurovascular bundle remains loose, preventing postoperative limitation of elevation.
orized inferior oblique muscle now depresses the eye and limits
elevation; this is an active leash caused by inferior oblique contraction, and forced ductions on patients with this complication
of limited elevation often show only slight restriction to supraduction. The complication of limited elevation can be avoided
while maintaining excellent results by anterior transposition of
the anterior muscle fibers at, or a millimeter or two behind, the
inferior rectus insertion. Be sure to keep the posterior fibers
back, behind the anterior fibers. Placing the posterior muscle
fibers several millimeters posterior to the inferior rectus insertion and in line with the inferior rectus muscle prevents the
J-deformity (Fig. 2-17B).16,47
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handbook of pediatric strabismus and amblyopia
EXTRAOCULAR MUSCLE HISTOLOGY
As are other skeletal muscles, extraocular muscles are made up
of striated fibers that, on electron microscopy, show the typical
banding pattern of sarcomeres with overlapping threads of actin
and myosin. Also resembling other muscles, the strength of an
extraocular muscle contraction is dependent on the number of
motor units activated (recruitment) and the frequency of muscle
fiber stimulation. Extraocular muscles, however, do show some
interesting anatomic and physiological differences from other
skeletal muscles. The fibers are variable in size, are considerably
smaller, and contract more than 10 times faster than other
skeletal muscle. Extraocular muscle fibers are innervated at a
high nerve fiber to muscle fiber ratio (almost 1:1), whereas other
skeletal muscle can have up to 100 muscle fibers for every nerve
fiber. This rich innervation, teamed with a fast muscle reaction
time, contributes to the precision, accuracy, and control of eye
movements.
Another distinction of extraocular muscles is the presence
of two distinct muscle fiber types: fast muscle fibers and slow
muscle fibers. The fast, or twitch, fibers are single innervated
fibers (SIF), innervated by a large motor neuron with “en plaque”
neuromuscular junctions and are typical of mammalian skeletal muscle. The SIF can be classified into three types: red,
intermediate, and white. Red SIF have the highest density of
mitochondria and are the most fatigue resistant, while the white
SIF have fewer mitochondria and are less resistant to fatigue.
Intermediate and white fibers provide the high transient force
needed for the extremely fast saccadic eye movements.
Slow, or tonic muscle fibers, are multiple innervated fibers
(MIF) innervated by small-diameter motor nerves with “en
grappe” neuromuscular endings characteristic of avian and
amphibian muscles. MIF are thought to participate in smooth
pursuit movements and static muscle tone to hold and maintain
eye position, and SIF probably also play a supportive role in tonic
control of eye position and pursuit eye movements. The exact
functions of the variety of specific muscle fiber types are
unknown, and it is likely that various fibers have overlapping
functions.28
Within extraocular muscle tissue are neuromuscular
spindles that are concentrated at the muscle–tendon junction.
Neuromuscular spindles are thought to be sensory organs providing information on muscle tone to the brain.9 The exact role
chapter 2: anatomy and physiology of eye movements
49
of the muscle spindles is unknown, but they may provide proprioceptive feedback to motor centers in the brain regarding
muscle tone and eye position. Muscle spindles may explain why
many adult patients experience transient spatial disorientation
after strabismus surgery on the dominant eye.
ARCHITECTURE OF THE EXTRAOCULAR
MUSCLES AND PULLEYS
Extraocular muscles have two distinct muscle layers seen on
transverse sections (cross section). There is a peripheral layer
closest to the orbital wall called the orbital layer (OL) and an
inner layer closest to the eye globe called the global layer
(GL).33,37 OL muscle fibers contain small-diameter fibers with
many mitochondria and abundant vessels, staining dark red by
Masson’s trichrome. The GL, in contrast, contains larger fibers
with variable numbers of mitochondria and fewer vessels; it
stains bright red by Masson’s trichrome. Approximately 90% of
GL muscle fibers are fast-twitch SIF, with one-third of the SIF
being fatigue-resistant red SIF; 80% of OL muscle fibers are
twitch-generating SIF and 20% are MIF.33 In humans, OL muscle
fibers do not appear to run the entire course of the muscle and
do not insert in sclera, as there is a gradual decline in the OL in
the anterior aspect of the muscle.11,28
Elastic fibers connect the OL to a fibromuscular pulley
sleeve that surrounds each extraocular muscle close to the
muscle insertion (see Muscle Pulleys, following) (Fig. 2-18).11
There are also muscle-to-muscle-fiber junctions (myomyous
junctions) within the OL. GL fibers, on the other hand, are continuous from their origin in the orbital apex to their insertion
by tendon into sclera.28 Most GL fibers act in saccadic eye movements and function only in the field of action of the muscle
whereas OL fibers are active throughout the oculomotor range,
providing continuous muscle tone to the pulley system.7 Collins
hypothesized that OL muscle fibers might have a role in
maintaining fixation whereas GL muscle fibers participate in
dynamic eye movements.7 An alternative hypothesis proposed
by Demer is that OL muscle fibers actively control pulley position, thereby influencing the rotational force vectors during eye
movements.11,28
A
FIGURE 2-18A–C. Masson’s trichrome stain of 10-␮m-thick transverse
section of medial rectus at the level of the pulley ring of a 17-month-old
human. (A) Low power shows the overall architecture of the pulley (P)
that surrounds the medial rectus muscle. Fibers in the orbital layer (OL)
(arrowheads) insert in the pulley, shown at high power in (B). The OL
muscle layer takes the form of a C-shape and is on the left, delineated by
the large arrows; the global layer (GL) fibers are to the right. OL on the
left is shown on the bottom.
50
chapter 2: anatomy and physiology of eye movements
51
B
C
FIGURE 2-18A–C. (B) High-power magnification shows the insertion of
the OL into the pulley (taken from the upper left box on A). (C) Highpower magnification of the GL and pulley relationship. The GL does not
insert into the surrounding pulley (taken from the middle right box on
A).11,28
52
handbook of pediatric strabismus and amblyopia
EXTRAOCULAR MUSCLE FASCIA
A smooth white connective tissue, Tenon’s capsule, underlies
the conjunctiva and envelops the globe and extraocular muscles.
This delicate membrane partitions the orbital contents, isolating the globe and extraocular muscles from the surrounding
orbital fat. Another fascial structure interconnected with
Tenon’s capsule is the muscle sleeve or extraocular muscle
pulley, which suspends the extraocular muscles.
Muscle Pulley (Muscle Sleeve)
Each of the rectus muscles passes through a pulley system consisting of a sleeve or ring of collagen, elastic, and smooth muscle
fibers. Previously, this structure was termed muscle sleeve. The
medial rectus muscle pulley has the most fibroelastic tissue and
smooth muscle. Muscle pulleys connect to the orbital layer (OL)
of the rectus muscle, to the orbital wall, to adjacent extraocular
muscles, and to Tenon’s capsule.10 The pulley or sleeve extends
for approximately 10 mm from the equator of the globe anteriorly to approximately 6 mm from the muscle insertion. During
strabismus surgery, one can see these bands as they connect the
surrounding muscle sleeve or pulley to the OL of the rectus
muscle. Similar to the trochlea and superior oblique tendon, the
pulleys guide the rectus muscles to their insertion point. In contrast to the superior oblique muscle, which changes direction
after passing through the trochlea, rectus muscle pulleys keep
the muscle in line with their anatomic origin. Demer has suggested that in secondary gaze positions the extraocular muscle
path is “discretely inflected by the pulley.”6 Demer et al. also
hypothesized that OL muscle fibers insert into the pulley
system and actively influence pulley position and the mechanics of ocular rotation.11,28
Tenon’s Capsule
Tenon’s capsule is a collagen-elastic tissue that is a continuous
membrane surrounding the eye and extraocular muscles.22 This
membrane separates surrounding orbital fat from the globe and
extraocular muscles. The elastic nature of Tenon’s capsule
allows free rotation of the globe and unrestricted muscle relaxation and contraction. For clinical and surgical purposes, it is
useful to subdivide it into the following categories:
chapter 2: anatomy and physiology of eye movements
53
1. Intermuscular septum
2. Anterior Tenon’s capsule
3. Posterior Tenon’s capsule
4. Check ligaments
5. Muscle sleeve (see Pulley System, earlier)
INTERMUSCULAR SEPTUM
This thin tissue lies sandwiched between the conjunctiva
and sclera, spanning between the rectus muscles (Fig. 2-19).30,40
During strabismus surgery, intermuscular septum can be identified as the white membrane on each side of the rectus muscles.
When elevated with muscle hooks, the intermuscular septum
takes on the appearance of the wings of a manta ray (Fig. 2-20).45
The intermuscular septum can be safely incised during strabismus surgery, as it is not a barrier to orbital fat.
ANTERIOR TENON’S CAPSULE
This tissue is the subconjunctival membrane anterior to the
muscle insertions. It proceeds forward with the intermuscular
septum and fuses with the conjunctiva at 2 to 3 mm posterior
to the corneal limbus (Figs. 2-18, 2-20). When suturing a muscle
during strabismus surgery, it is important to dissect anterior
Tenon’s capsule off the tendon insertion to avoid the complica-
Reflected
conjunctiva
SR
IMS
IMS
MR
LR
Anterior
Tenon's Capsule
FIGURE 2-19. Anterior ocular fascia. Intermuscular septum (IMS) is the
connective tissue that spans between the rectus muscles underneath the
conjunctiva. Anterior Tenon’s is that tissue anterior to the rectus muscle
insertions; it fuses with the conjunctiva 3 mm posterior to the limbus.
54
handbook of pediatric strabismus and amblyopia
A
B
FIGURE 2-20A,B. (A) Lateral rectus muscle with intermuscular septum and
check ligaments. Check ligaments overlie the rectus muscle and connect
the muscle to the overlying conjunctiva. Intermuscular septum is seen on
either side of the lateral rectus muscle, spanning between the superior and
inferior rectus muscles. (B) Photograph shows the Jameson hook under the
lateral rectus muscle and Desmarres retractor pulling the conjunctiva
posteriorly. (Figure published with permission of J.B. Lippincott Co. from
Wright KW. Color Atlas of Ophthalmic Surgery: Strabismus. Philadelphia:
Lippincott, 1991.)
chapter 2: anatomy and physiology of eye movements
55
Anterior Tenon's
capsule
Medial rectus
Anterior ciliary
muscle
artery
FIGURE 2-21. Anterior Tenon’s capsule is the white tissue retracted
anteriorly with a small Steven’s hook (bottom left hook). During strabismus surgery, it is important to remove the anterior Tenon’s capsule to
visualize the muscle tendon for suturing. Note the anterior ciliary vessels
on the tendon insertion.
tion of a slipped muscle (Fig. 2-21). If anterior Tenon’s capsule
is left on the tendon, the surgeon may inadvertently suture
and secure anterior Tenon’s capsule, missing all or part of the
tendon. The unsuspecting surgeon then disinserts the unsutured
tendon and allows the muscle to slip posteriorly while anterior
Tenon’s capsule is placed at the intended recession site.31 A
slipped muscle is a frequent cause of unexpected overcorrection
after recession procedures, as it often goes unrecognized at the
time of surgery. Remember that some slipped muscles involve
only part of the muscle and can present as a mild overcorrection
with relatively good muscle function.48
POSTERIOR TENON’S CAPSULE
This tissue lines the posterior globe and functions to separate
orbital fat from the sclera (Fig. 2-22). Just anterior to the equator
of the eye, the four rectus muscles penetrate Tenon’s capsule and
become surrounded by intra- and extraconal orbital fat. At this
juncture, Tenon’s capsule unites with the capsule of the rectus
muscle to form a muscle pulley or muscle sleeve (see Muscle
Pulley, earlier). The muscle sleeve is an important surgical
56
handbook of pediatric strabismus and amblyopia
Posterior
Tenon's capsule
Extraconal fat
Anterior Tenon's
capsule
Muscle sleeve
(pulley)
Conjunctiva
Fused anterior
Tenon's and
conjunctiva
Intraconal
fat
Medial rectus
muscle
FIGURE 2-22. Drawing of a rectus muscle showing fascial relationships.
Note that the muscle penetrates posterior Tenon’s capsule; the capsule at
this point forms a muscle sleeve or muscle pulley. Intraconal and extraconal fat are isolated from the globe by Tenon’s capsule.
landmark when looking for a slipped or lost rectus muscle. A lost
muscle is a rectus muscle that has become completely detached
from the globe because of trauma or a surgical mistake.32,48 Once
lost, the muscle will slip posteriorly within the muscle sleeve
to be surrounded by intra- and extraorbital fat. To find a lost
muscle, first find the muscle sleeve located between the intraand extraconal fat; then, carefully follow the sleeve to retrieve
the muscle. When looking for a lost medial rectus muscle, avoid
the tendency to follow the sclera posteriorly, as this leads to the
optic nerve. An important complication of attempted retrieval
of a lost medial rectus muscle is inadvertent transection of the
optic nerve that is enshrouded in postoperative scar tissue.
Together, posterior Tenon’s capsule, anterior Tenon’s
capsule, and the muscle sleeve are very important structures as
they are the barrier that keeps orbital fat from the globe and
extraocular muscles. If posterior Tenon’s capsule or muscle
sleeve is traumatically or surgically violated, fat adherence can
occur because orbital fat prolapses through the torn Tenon’s
capsule and scars to the sclera or an extraocular muscle (Fig.
2-23). The scarring of orbital fat produces a restrictive scar,
which extends from the periosteum to the eyeball. As the scar
chapter 2: anatomy and physiology of eye movements
57
contracts over weeks to several months, the scar pulls the eye,
producing a restrictive strabismus associated with limitation of
eye movements. Fat adherence can occur as a complication of
almost any extraocular surgery (e.g., strabismus surgery, retina
surgery) or periocular trauma.31,49 Extreme care must be taken
when operating in the area of orbital fat, which starts 10 mm
posterior to the limbus. Once fat adherence occurs, it is almost
impossible to correct. Surgically induced fat adherence can
usually be avoided if the surgeon carefully dissects close to
muscle belly or sclera, thus preserving the integrity of the overlying posterior Tenon’s capsule and muscle sleeve.
CHECK LIGAMENTS
These are fine falciform webs that overlie the rectus muscles
and join the muscle capsule with overlying bulbar conjunctiva
A
B
FIGURE 2-23A,B. Diagram modified after Parks and published in Ophthalmology by Wright (1986)49 shows the pathophysiology of the fat
adherence syndrome. (A) Normal anatomy with orbital bone, periorbita,
extraconal fat, muscle, and intermuscular septum. Note that the fat is
isolated from muscle and sclera by intact Tenon’s capsule and intermuscular septum. (B) Violation of Tenon’s capsule with fat adherence to the
globe and muscle (to right).
58
handbook of pediatric strabismus and amblyopia
at the muscle tendon (see Fig. 2-20). More posteriorly, check ligaments are probably the bands that connect the OL muscle fibers
to the surrounding muscle sleeve (muscle pulley). In the case of
the superior and inferior rectus muscles, check ligaments also
connect to the levator muscle and lower lid retractors, respectively. A recession or resection of vertical rectus muscles requires
removal of these ligaments to avoid lid fissure changes after
surgery.
VASCULAR SUPPLY TO
THE ANTERIOR SEGMENT
The anterior segment and iris are supplied by the anterior ciliary
arteries, conjunctival vessel, and the long posterior ciliary
arteries (Fig. 2-24). Approximately 50% of the anterior segment
circulation comes from the long posterior ciliary arteries and
FIGURE 2-24. Diagram of circulation of the anterior segment with the
rectus muscle supplying the anterior ciliary arteries (aa); the deep long
posterior arteries are also shown. (Figure published with permission of
J.B. Lippincott Co. from Wright KW. Color Atlas of Ophthalmic Surgery:
Strabismus. Philadelphia: Lippincott, 1991.47)
chapter 2: anatomy and physiology of eye movements
44
59
50% from the anterior ciliary arteries. The conjunctival vessels
also contribute to anterior segment circulation.14 Anterior
ciliary arteries and the conjunctival vessels merge at the limbus
to form the episcleral limbal plexus.27 These vessels in turn
connect with the major arterial circle of the iris, which is also
fed by the two long posterior ciliary arteries. The superior rectus,
inferior rectus, and medial rectus muscles have at least two anterior ciliary arteries and are major contributors to the anterior
segment circulation.18 The lateral rectus has a single anterior
ciliary artery and, of the four recti muscles, the lateral rectus
probably provides the least in the way of anterior segment circulation.20,41 The oblique muscles do not have anterior ciliary
arteries, and they do not contribute to the anterior segment
circulation.
Iris angiograms can be used to assess anterior segment
circulation in blue-eyed patients. Removal of a vertical rectus
muscle will cause hypoperfusion in that area that relates to the
vascular input.18 It is interesting that this hypoperfusion lasts
only 1 to 2 months because its collateral circulation and vasodilatation will replenish the hypoperfused area.45 Additionally,
infants and children do not typically show hypoperfusion even
when multiple rectus muscles are removed. Removal of a rectus
muscle during strabismus surgery will permanently interfere
with vascular supply of the anterior ciliary arteries unless the
surgery is performed specifically to maintain anterior segment
circulation. Surgeries have been devised that attempt to maintain anterior segment circulation despite manipulations of the
muscle position.24,45 Iris angiograms can be used to document
anterior segment blood flow from the anterior ciliary arteries in
nonhuman primates. A muscle-to-sclera plication developed by
this author (Wright plication) is designed to tighten a rectus
muscle but spare the anterior ciliary arteries. Instead of resecting the muscle, as is done in the standard muscle tightening procedure, the Wright plication folds the muscle, suturing muscle
to sclera without disrupting the anterior ciliary vessels. Figure
2-25 shows an iris angiogram after inferior rectus muscle plication and surgical removal of the other three rectus muscles in a
nonhuman primate. The iris angiogram demonstrates intact perfusion from the inferior rectus muscle and hypoperfusion superiorly because the arteries of the other three rectus muscles had
been sacrificed on surgical removal.
Anterior segment ischemia can be a consequence of
strabismus surgery, most often after a three- or four-muscle
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handbook of pediatric strabismus and amblyopia
FIGURE 2-25. Monkey fluorescein iris angiogram, early phase after
Wright plication of the inferior rectus muscle and removal of the other
three rectus muscles. Note the hypoperfusion superiorly (black area of
iris) as the medial, lateral, and superior rectus muscles have been
removed. The perfusion from the inferior rectus remains intact after the
Wright plication because fluorescence is seen inferiorly (white vessels on
iris).46
transposition procedure.35,42 This is a rare occurrence, as collateral circulation from the long posterior ciliary arteries can
usually maintain adequate perfusion to the anterior segment
even when three or four rectus muscles have been removed.36
Factors that predispose to anterior segment ischemia include
arteriosclerosis, hyperviscosity of the blood, and scleral encircling elements such as 360° retinal buckles posteriorly, all of
which can compromise the long posterior ciliary arteries. Older
patients have a higher likelihood for developing anterior
segment ischemia, whereas infants and children are generally
protected from this condition.15 Anterior segment ischemia has
even been reported after removing as few as two rectus muscles
in high-risk patients.12,15 It is important to remember, however,
that disruption of anterior ciliary arteries associated with strabismus surgery is permanent, and anterior segment ischemia
can occur years or decades later, as the collateral circulation
diminishes with age.34
chapter 2: anatomy and physiology of eye movements
61
PHYSIOLOGY OF OCULAR ROTATIONS
Donder’s and Listing’s Laws
Ocular movements are a result of contraction and relaxation of
multiple muscle groups that act to rotate the eye around a fixed
center of rotation. There are three axes that pass through the
center of rotation, termed the axes of Fick (Fig. 2-26). The axes
of Fick include the Z axis (vertical orientation) for horizontal
rotation, the X axis (horizontal orientation) for vertical rotation,
and the Y axis (oriented with the visual axis) for torsional rotation. Listing’s plane is a vertical plane that includes the X, Z,
and oblique axes that pass through the center of the eye (Fig.
2-26). Listing’s law states that virtually all positions of gaze can
be achieved by rotations around axes that lie on Listing’s plane.
Donder’s law is related to Listing’s law and states that there is
a specific orientation of the retina and cornea for every position
of gaze. This corneal orientation is specific for each position of
gaze regardless of the path the eye took to achieve that position
of gaze. Figure 2-27 demonstrates Listing’s and Donder’s laws,
showing the specific corneal orientations for ocular rotations
around various axes on Listing’s plane. Note that when rotations
B
A
C
FIGURE 2-26A–C. The three axes of Fick allow horizontal rotation. (A)
Vertical axis (Z axis): horizontal rotations. (B) Horizontal axis (X axis):
vertical rotations. (C) Visual axis (Y axis): torsional rotations.
62
handbook of pediatric strabismus and amblyopia
FIGURE 2-27. Listing’s plane is shown in the center diagram, which
includes the Z and X axes of Fick. Diagram shows that the eye can reach
all positions of gaze by rotations around axes that are on Listing’s plane.
In the center diagram, the O axes represent oblique axes that are on
Listing’s plane and are oriented between the Z and X axes of Fick. Note
that the oblique axes of rotation seen on the four corners of the diagram
allow the eye to rotate obliquely, up and in, up and out, down and in, and
down and out. Also, observe the pseudotorsion of the cornea when the
eye rotates around the oblique axis.
are directly around the X axis (pure vertical movement) or
directly around the Z axis (pure horizontal movement) there is
no associated torsional rotation of the cornea. In contrast,
oblique ocular rotations cause a torsional shift in the corneal orientation relative to the planar coordinates of Listing’s plane.
This torsional shift relative to Listing’s plane is not due to true
rotation around the Y axis and is therefore referred to as pseudotorsion. Active, or true, torsional rotations around the Y axis
(cycloduction) are created by contraction of vertical and oblique
muscles. True torsional movements normally occur to keep the
eyes aligned during head tilting23 or occur pathologically when
a vertical or an oblique muscle over- or underacts.21
chapter 2: anatomy and physiology of eye movements
63
TABLE 2-2. Agonist–Antagonist Muscle Pairs.
Medial rectus—Lateral rectus
Superior rectus—Inferior rectus
Superior oblique—Inferior oblique
Sherrington’s Law: Agonist and
Antagonist Muscles
As described in this chapter previously, ductions are monocular
rotations and are clinically examined with one eye occluded to
force fixation to the eye being tested. Table 2-2 lists agonist–
antagonist pairs for the primary function of the muscles. This
relationship between agonist (contracting muscle) and antagonist (relaxing muscle) muscles is referred to as Sherrington’s
law of reciprocal innervation.
Sherrington’s law can be demonstrated by using electromyography (EMG). The EMG measures electrical potential
changes within a muscle as the muscle fibers contract and indicates the degree of overall neuromuscular activity. The EMG is
performed by placing a needle electrode in the muscle (extracellularly) and then recording the amplified electrical activity
from the muscle. Figure 2-28 shows results of EMG for agonist
and antagonist muscles that demonstrates Sherrington’s law.
The needle electrode is placed in the medial and lateral rectus
muscles. At the beginning of the EMG tracing, there is lowamplitude tonic activity that maintains the eye position in
FIGURE 2-28. Sherrington’s Law: Electromyographic (EMG) tracing from
the lateral rectus muscle (LR) and medial rectus muscle (MR). Note that
when the eye adducts, the medial rectus muscle increases EMG activity
as the muscle contracts. EMG activity from the lateral rectus muscle
diminishes as the antagonist lateral relaxes.
64
handbook of pediatric strabismus and amblyopia
primary position. As the eye is adducted, the medial rectus contracts, resulting in increasing EMG activity, while the lateral
rectus muscle simultaneously relaxes and EMG activity is inhibited. At the end of the tracing, both muscles show tonic activity to maintain eye position. In patients with motor neuron
misdirection syndromes such as Duane’s retraction syndrome,
Sherrington’s law is violated. In Duane’s syndrome, the lateral
rectus muscle is innervated by a branch of the third nerve that
also supplies the medial rectus muscle. When the patient
adducts the eye, instead of the medial rectus contracting and the
lateral rectus relaxing, both the medial and lateral rectus
muscles contract simultaneously. It should be remembered that
Sherrington’s law of reciprocal innervation refers strictly to
monocular eye movements, as does the term ductions. A trick
to remember this, is the S in Sherrington stands for Single eye.
Synergist
The term synergist is used for muscles of the same eye that act
to move the eye in the same direction. In other words, synergist
muscles have common actions. For example, the superior
oblique and the inferior rectus muscles both act as depressors;
therefore, they are synergists for infraduction. These muscles are
not, however, synergists for horizontal or torsional rotations, as
the inferior rectus muscle is an adductor and extortor whereas
the superior oblique muscle is an abductor and intortor. Table
2-3 lists synergist muscles for various duction movements. Note
that synergist muscles relate to monocular rotations, not to be
confused with yoke muscles involved with binocular eye movements (see Hering’s Law of Yoke Muscles, below). Like the S
trick in Sherrington’s law, remember the S in Synergist stands
for Single eye.
TABLE 2-3. Synergist Muscles.
Duction
Primary mover
Secondary mover
Supraduction
Infraduction
Adduction
Abduction
Extorsion
Intorsion
Superior rectus
Inferior rectus
Medial rectus
Lateral rectus
Inferior oblique
Superior oblique
Inferior oblique
Superior oblique
Superior rectus/inferior rectus
Superior oblique/inferior oblique
Inferior rectus
Superior rectus
chapter 2: anatomy and physiology of eye movements
65
Oculomotor Reflexes
Two important oculomotor reflexes are the vestibulo-ocular
reflex (VOR) and optokinetic nystagmus (OKN). The vestibuloocular reflex functions to keep the eyes steady when the head
moves. Vestibular stimulation, induced by turning the head,
results in a compensatory movement of the eyes to maintain the
position of gaze. If the head is rapidly turned to the left, the eyes
move to the right with the same velocity. A similar reflex, the
orthostatic reflex, is responsible for keeping the eyes torsionally
aligned when the head is tilted. This reflex is the basis of the
Bielschowsky head tilt test for vertical muscle palsies. Optokinetic nystagmus is a visually mediated reflex consisting of
smooth pursuit alternating with saccadic refixation as a series
of objects cross the visual field. The eyes follow a moving object
with smooth pursuit, then use a saccadic movement in the opposite direction to refixate on the next approaching target. The
stimulus most commonly used to produce OKN is a pattern of
black and white stripes presented on a rotating drum or moving
tape. The best OKN stimulus fills the visual field so there are
no stationary objects for the subject to fixate.
Hering’s Law of Yoke Muscles
Normally, our two eyes move together in the same direction;
this is termed a version movement. Coordinated binocular eye
movements require symmetrical innervation of each eye. For
example, when one looks to the left, the left lateral rectus and
right medial rectus muscles simultaneously contract as the left
medial and right lateral rectus muscles relax (Fig. 2-29). The
paired agonist muscles from each eye are referred to as yoke
muscles. In Figure 2-29, the left lateral and right medial rectus
muscles are yoke agonist muscles whereas the left medial and
right lateral are yoke antagonists. Hering’s law states that yoke
muscles receive equal innervation. Remember, Hering’s law
relates to yoke muscles and binocular eye movements (versions),
whereas Sherrington’s law explains agonist–antagonist relationships and monocular eye movements (ductions). Figure 2-30
shows the yoke agonist muscles responsible for various fields of
gaze. In most situations, the term yoke muscles refers to yoke
agonist muscles.
FIGURE 2-29. Hering’s Law: Diagram of version movements to the left.
As the left lateral rectus (LR) contracts (), the contralateral medial
rectus (MR) simultaneously contracts (). Also note that the left
medial rectus relaxes () and the right lateral rectus also relaxes
().
FIGURE 2-30. Yoke muscles are shown for specific field of gaze. Top: gaze
up and to the side with yoke muscles being the superior rectus (SR) and
inferior oblique (IO) muscles. Middle: straight sidegaze with the yoke
muscles being lateral rectus (LR) and medial rectus (MR). Bottom: gaze
down and to the side with yoke muscles being the inferior rectus (IR) and
superior oblique (SO).
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chapter 2: anatomy and physiology of eye movements
67
Versions
Versions can be classified as follows: dextroversion for rightgaze,
levoversion for leftgaze, supraversion for upgaze, and infraversion for downgaze. In contrast to ductions, versions are performed with both eyes open and compare how well the eyes
move together in synchrony. Versions will identify a subtle
restriction or paresis and muscle overaction that results in asymmetrical eye movements.
References
1. Atkinson J. Development of optokinetic nystagmus in the human
infant and monkey infant: an analogue to the development in kitten.
In: Freeman RD (ed) Developmental neurobiology of vision. New
York: Plenum Press, 1979.
2. Bartini C, Horcholle-Bossavit G. Extraocular muscle afferents and
visual input interactions in the superior colliculus of the cat. Prog
Brain Res 1979;50:335.
3. Beisner DH. Reduction of ocular torque by medial rectus recession.
Arch Ophthalmol 1971;85:13.
4. Bloom JN, Graviss ER, Mardelli PG. A magnetic resonance imaging
study of the upshoot-downshoot phenomenon of Duane’s retraction
syndrome. Am J Ophthalmol 1991;111:548–554.
5. Bremer DL, Rogers GL, Quick LD. Primary-position hypotropia after
anterior transposition of the inferior oblique. Arch Ophthalmol
1986;104:229–232.
6. Clark RA, Miller JM, Demer JL. Three-dimensional location of
human rectus pulleys by path inflections in secondary gaze positions.
Investig Ophthalmol Vis Sci 2000;41:3787–3797.
7. Collins CC. The human oculomotor control system. In: Lennerstrand
G, Bach–y-Rita P (eds) Basic mechanism of ocular motility and their
clinical implications. New York: Pergamon, 1975:145–180
8. Cynader M, Berman N, Hein A. Recovery of function in cat visual
cortex following prolonged deprivation. Exp Brain Res 1975;25:139–
156.
9. Daniel P. Spiral nerve endings in the extrinsic eye muscles of man.
J Anat 1946;80:189.
10. Demer JL, Poulkens V, Miller JM, Micevych P. Innervation of extraocular pulley smooth muscle in monkeys and humans. Investig
Ophthalmol Vis Sci 1997;38:1774–1785.
11. Demer JL, Oh SY, Poulkens V. Evidence for an active control of rectus
extraocular muscle pulleys. Investig Ophthalmol Vis Sci 2000;41:
1280–1290.
12. Fells P, March RJ. Anterior segment ischemia following surgery on
two rectus muscles. In: Reinecke RD (ed) Strabismus: proceedings of
68
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
handbook of pediatric strabismus and amblyopia
the third meeting of the International Strabismological Association,
May 10–12, 1978, Kyoto, Japan. New York: Grune & Stratton, 1978:
375–380.
Fink WH. Surgery of the oblique muscles of the eye. St. Louis: Mosby,
1951:92–95.
Fishman PH, Repka MX, et al. A primate model of anterior segment
ischemia after strabismus surgery. Ophthalmology 1990;97(4):456–461.
France TD, Simon JW. Anterior segment ischemia syndrome following muscle surgery. The AAPO&S experience. J Pediatr Ophthalmol
Strabismus 1986;23:87–91.
Guemes A, Wright KW. Effect of graded anterior transposition of the
inferior oblique muscle on versions and vertical deviation in primary
position. JAAPOS 1998;201–206.
Hawes MJ, Dortzbach RK. The microscopic anatomy of the lower
eyelid retractors. Arch Ophthalmol 1982;100(8):1313–1318.
Hayreh SS, Scott WE. Fluorescein iris angiography. Arch Ophthalmol
1978;96:1390–1400.
Helveston EM, Merriam WW, Ellis FD, et al. The trochlea: a study
of the anatomy and physiology. Ophthalmology 1982;89:124–133.
Hiatt RL. Production of anterior segment ischemia. Trans Am Ophthalmol Soc 1977;75:87–102.
Jampel RS. The fundamental principle of the action of the oblique
ocular muscles. Am J Ophthalmol 1970;69:623.
Koornneef L. Orbital septa: anatomy and function. Ophthalmology
1979;86:876–880.
Linwong M, Herman SJ. Cycloduction of the eyes with head tilt.
Arch Ophthalmol 1971;85:570.
McKeown CA, Lambert HM, et al. Preservation of the anterior ciliary
vessels during extraocular muscle surgery. Ophthalmology 1989;96:
498–507.
Mims JL, Wood RC. Bilateral anterior transposition of the inferior
obliques. Arch Ophthalmol 1989;107:41–44.
Mims JL, Wood RC. Anti-elevation syndrome after bilateral anterior
transposition of the inferior oblique muscles: incidence and prevention. J Am Assoc Pediatr Ophthalmol Strabismus 1999;3(6):333–336.
Morrison JC, van Buskirk EM. Anterior collateral circulation in the
primate eye. Ophthalmology 1983;90:707–715.
Oh SY, Poulkens V, Demer J. Quantitative analysis of rectus extraocular muscle layers in the monkey and humans. Investig Ophthalmol
Vis Sci 2001;42(1):10–17.
Parks MM, Bloom JN. The “slipped muscle.” In: Symposium on strabismus. Transactions of the New Orleans Academy of Ophthalmology. St. Louis: Mosby, 1978:1389–1396.
Parks MM. Atlas of strabismus surgery. Philadelphia: Harper & Row,
1983.
Parks MM. Causes of the adhesive syndrome. In: Symposium on strabismus. Transactions of the New Orleans Academy of Ophthalmology. St. Louis: Mosby, 1978:269–279.
chapter 2: anatomy and physiology of eye movements
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32. Plager DA, Parks MM. Recognition and repair of the “lost” rectus
muscle. Ophthalmology 1990;97:131.
33. Porter JD, Baker RS, Ragusa RJ, Brueckner JK. Extraocular muscles:
basic and clinical aspects of structure and functions. Surv Ophthalmol 1995;39:451–484.
34. Saunders RA, Sandall GS. Anterior segment ischemia syndrome
following rectus muscle transposition. Am J Ophthalmol 1982;93:
34–38.
35. Saunders RA, Phillips MS. Anterior segment ischemia after three
rectus muscle surgery. Ophthalmology 1988;95:533–537.
36. Simon JW, Price EC, et al. Anterior segment ischemia following strabismus surgery. J Pediatr Ophthalmol Strabismus 1984;21:179–184.
37. Spencer RF, Porter J. Structural organization of the extraocular
muscles. In: Buttner-Ennever J (ed) Neuroanatomy of the oculomotor system. Amsterdam: Elsevier, 1988:33–79.
38. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch
Ophthalmol 1992;110:360–362.
39. Stager DR, Porter J, Weakley DR, Stidham DB. A comparative microscopic analysis of the capsule of the nerve to the inferior oblique
muscle. Trans Am Ophthalmol Soc 1997;95:453–462; discussion
463–465.
40. Swan KC. Fascia in relation to extraocular muscle surgery. Arch
Ophthalmol 1970;83:134–140.
41. Virdi PS, Hayreh SS. Normal fluorescein iris angiographic pattern in
subhuman primates. Investig Ophthalmol Vis Sci 1983;24:790–793.
42. von Noorden GK. Anterior segment ischemia following the Jensen
procedure. Arch Ophthalmol 1976;94:845–847.
43. von Noorden GK. Letter to the Editor. A magnetic resonance imaging
study of the upshoot downshoot phenomenon of Duane’s retraction
syndrome. Am J Ophthalmol 1991;112:358–359.
44. Wilcox LM Jr, Keough EM, et al. The contribution of blood flow by
the anterior ciliary arteries to the anterior segment in the primate
eye. Exp Eye Res 1980;30:167–174.
45. Wright KW, Lanier AB. Effect of a modified rectus tuck on anterior
segment circulation in monkeys. J Pediatr Ophthalmol Strabismus
1991;28:77–81.
46. Wright KW, et al. Acquired inflammatory superior oblique tendon
sheath syndrome: a clinicopathologic study. Arch Ophthalmol 1982;
100:1752–1754.
47. Wright KW. Color atlas of ophthalmic surgery: strabismus. Philadelphia: Lippincott, 1991.
48. Wright KW. Discussion of paper: Recognition and repair of the lost
rectus muscle. Ophthalmology 1990;97:136.
49. Wright KW. The fat adherence syndrome and strabismus after retinal
surgery. Ophthalmology 1986;93:411–415.
3
Binocular Vision and
Introduction to Strabismus
Kenneth W. Wright
I
n normal vision, both eyes are precisely aligned on an object
of regard, so the images from that object fall on the fovea of
each eye. Precise image orientation on corresponding retinal
areas of each eye permits cortical processing, which results in
the merging or fusion of the two images. This process is termed
binocular fusion. There are two important aspects of binocular
fusion: sensory fusion and motor fusion. This chapter discusses
the process of binocular vision and provides an introduction to
strabismus.
SENSORY FUSION
Sensory fusion is the cortical process of blending the images
from each eye into a single binocular stereoscopic image. This
fusing occurs as optic nerve fibers from the nasal retina cross in
the chiasm to join the uncrossed temporal retinal nerve fibers
from the fellow eye. Together, ipsilateral temporal fibers and
contralateral nasal fibers project to the lateral geniculate nucleus
and then on to the striate cortex. This division of hemifields
does not totally respect the midline. There is significant overlap
in the foveal area with some of the nasal foveal fibers projecting
to the ipsilateral cortex and some of the temporal foveal fibers
crossing to the contralateral cortex. Within the striate cortex,
afferent pathways connect to binocular cortical cells that
respond to stimulation of either eye. Retinal areas from each eye
that project to the same cortical binocular cells are called corresponding retinal points. In Figure 3-1, points “A” left eye and
“A” right eye, and points “B” left eye and “B” right eye, are cor70
chapter 3: binocular vision and introduction to strabismus
71
FIGURE 3-1. Vieth–Müller circle and the empirical horopter. By mathematical theorems, points on the Vieth–Müller circle should project to corresponding retinal points. Point A stimulates the nasal retina of the left
eye and the temporal retina of the right eye, and these retinal areas should
mathematically correspond. Psychophysical experiments, however, show
that the retinal architecture does not follow the mathematical circle of
Vieth–Müller and that points on the empirical horopter stimulate corresponding retinal points. The bottom of the figure shows the fusion of the
images from each eye into a binocular perception.
responding retinal points. In humans, approximately 70% of the
cells in the striate cortex are binocular cells whereas the minority are monocular cells. Binocular cortical cells, along with
neurons in visual association areas of the brain, produce single
binocular vision with stereoscopic vision.
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When a subject with normal eye alignment fixes on a target,
that target falls on both foveas. Mathematical theory predicts
that objects peripheral to the fixation target (points A and B in
Fig. 3-1) will project to corresponding retinal points if the peripheral objects lie on a circle that passes through the optical centers
of each eye. This mathematically determined circle of points is
called the Vieth–Müller circle. As is often the case for mathematical explanations of biological phenomena, physiological
experiments have shown that the Vieth–Müller mathematical
model only partially works for visual perception. Psychophysical experiments indicate that the locus of points, which
project to corresponding retinal points of each eye, is not a circle
but actually takes the shape of an ellipse. This elliptical line of
points, which project to corresponding retinal points, is the
empirical horopter and is shown as a dotted line in Figure 3-1.
Remember, the location of the horopter is determined by the
point of fixation. Objects located in front of or behind the empirical horopter will project to noncorresponding retinal points.
In Figure 3-2A, note that point “A” is distal to the empirical
horopter and stimulates binasal retina. Point “B” in Figure 3-2B,
which is proximal to the horopter, stimulates bitemporal
retina. These binasal and bitemporal retinal points are noncorresponding retinal points, and images falling on these points
are termed disparate images. Disparate images have the potential for either producing stereoscopic vision or causing physiological diplopia.
Stereoscopic Vision
The empirical horopter is a theoretical locus of points, and is
infinitely thin. All three-dimensional objects lie in front of and
behind the horopter line; therefore, virtually all solid objects
stimulate noncorresponding retinal points and result in disparate retina images. The brain, however, can merge or “fuse”
images from slightly noncorresponding retinal points. This
finite area in front of and behind the horopter line where objects
stimulate noncorresponding retinal points, yet are still fusible
into a single binocular image, is called Panum’s fusional area
(Fig. 3-3). Stimulation of noncorresponding retinal points within
Panum’s fusional area will produce three-dimensional vision.
This ability for the brain to determine that images are falling on
retinal points that are not exactly corresponding (i.e., disparate
images) produces stereoscopic vision. Only horizontal retinal
chapter 3: binocular vision and introduction to strabismus
73
A
B
FIGURE 3-2A,B. Empirical horopter and Panum’s fusional area. Objects
that lie in front of or behind Panum’s fusional area will stimulate noncorresponding retinal points. (A) Patient fixating on the star in the center
of the empirical horopter. Point A, which is distal to the horopter, stimulates the binasal retinal points that are noncorresponding. (B) Patient fixating on the same spot; however, point B is proximal to the Panum’s
fusional area, and point B stimulates bitemporal retinal points that
are noncorresponding. Point A in (A) would cause uncrossed diplopia,
whereas point B in (B) would cause crossed diplopia. This type of diplopia
is termed physiological diplopia.
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}
Empirical
Horopter
Panum's
fusional
area
Stereoscopic
Image
FIGURE 3-3. Diagrammatic representation of stereoscopic vision. Note
that any three-dimensional objects will straddle the empirical horopter
and parts of that object will be in front of or behind the empirical
horopter; this stimulates noncorresponding retinal points that provide
stereoscopic vision so long as the three-dimensional objects fall within
Panum’s fusional area.
image disparities produce stereoscopic vision; vertical disparities do not. Panum’s fusional area is narrow at the center and
gradually widens in the periphery reflecting the high resolution–small receptive fields in the central visual field and low
resolution–large receptive fields in the periphery. Large displacements are required for the peripheral retina to detect a
change in receptive field.
Figure 3-3 shows a three-dimensional cube as a fixation
target. Note that the cube lies in front of and behind the empiri-
chapter 3: binocular vision and introduction to strabismus
75
cal horopter, projecting to noncorresponding retinal points. The
fovea has high spatial resolution, so even small displacements
off the horopter line (i.e., small image disparities) in the central
visual field are detected, resulting in fine, high-grade stereoscopic vision. In contrast, as one moves to the peripheral fields,
the receptive field size enlarges and the spatial resolution
decreases. The peripheral binocular visual fields are sensitive to
large image disparities and provide coarse stereoacuity. This
retinal architecture of high central resolution versus low peripheral resolution explains the excellent stereoacuity from central
fields and progressively poorer stereoacuity from peripheral
binocular retinal fields.
Physiological Diplopia
If an object is too far off the horopter line and outside of Panum’s
fusional area, then the images can no longer be fused and double
vision may result (diplopia) (Figs. 3-2, 3-4). This type of double
vision is a normal phenomenon and is termed physiological
diplopia. Note that, in Figure 3-4, the pencil is in front of
Panum’s fusional area and the pencil is, therefore, stimulating
the temporal retinas of each eye. Because the temporal retina
projects to the nasal visual field (opposite field), the observer perceives two pencils with the left image coming from the right eye
and the right image coming from the left eye; this is called
“crossed diplopia,” and occurs with bitemporal stimulation.
Physiological diplopia would occur in everyday life; however, it
is normally ignored or suppressed. You can experience physiological diplopia by simply fixating on a distant object several feet
away then placing a pencil a few inches from your nose. While
you are looking at the distant object, the pencil will appear
double. This is crossed diplopia: when you close your right eye
the left pencil disappears, and when you close the left eye the
right pencil disappears. You can demonstrate that Panum’s
fusional area is narrow centrally and wide in the periphery by
moving the pencil held at near to the right or left, while maintaining fixation on a distance target. Observe that the physiological diplopia and image quality diminish when the pencil is
moved into the peripheral binocular fields. (Remember to keep
your fixation on a distant object while the pencil is held at near.)
Objects distal to Panum’s fusional area stimulate binasal retinal
points and can cause uncrossed diplopia (see Fig. 3-2A). You
can experience uncrossed diplopia by fixating on a pencil a few
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FIGURE 3-4. A pencil is seen in front of Panum’s fusional area; this
stimulates noncorresponding bitemporal retinal points. Because the temporal retina projects to the opposite field (arrows), the patient perceives
crossed physiological diplopia.
inches in front of you and observing that the distant objects are
double (this may be difficult to see).
Stereoacuity Testing
Stereoscopic perception can be created from two-dimensional
figures by presenting each eye with similar figures that are
horizontally offset to produce bitemporal or binasal retinal
image disparities. Bitemporal retinal stimulation within Panum’s
fusional area gives the stereoscopic perception of an image
coming toward the observer (Fig. 3-2B), and binasal retinal stimulation within Panum’s fusional area gives the perception of an
image going away from the observer (Fig. 3-2A). Note that the
upper circles in Figure 3-5 are displaced nasally. The displaced
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77
circles result in bitemporal retinal stimulation within Panum’s
fusional area, and the circle will be perceived as a single circle
coming up off the page. In contrast, temporal displacement of
stereoscopic figures results in binasal retinal stimulation, with
the perception of depth away from the observer and into the
page. Most clinical stereoacuity tests present nasally displaced
images to each eye by using mirror systems, red/green glasses
FIGURE 3-5. Diagrammatic representation of a contour stereogram.
Polarized glasses donned by the patient match the orientation of two
polarized plastic plates on the stereo book, so one eye sees one plate and
the fellow eye sees the other plate. The polarization is oriented vertically
over the left eye and horizontally over the right eye, so the left eye views
the left figure with the upper circle shifted to the right, and the right eye
views the right figure with the upper circle shifted to the left. This nasal
displacement of the circles stimulates bitemporal disparate retinal points
and produces the stereoscopic perception that the upper circle is raised
off the page. Titmus testing uses nasally displaced figures to produce
stereoscopic images that come up off the page, towards the observer.
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TABLE 3-1. Visual Acuity (VA) and Titmus Stereoacuity.
Circles
9
8
7
6
5
4
3
2
1
40 s 20/25
50 s 20/30
60 s 20/40
80 s 20/50
100 s 20/60
140 s 20/70
200 s 20/80
400 s 20/100
800 s 20/200
Circles/seconds (s) of arc VA.4
with corresponding red/green figures, or polarized glasses
with corresponding polarized figure plates (see Fig. 3-5). These
systems provide different images to each eye separately
under binocular viewing and are termed haploscopic devices.
Stereoacuity can be quantified by measuring the amount of
image disparity. The angle of disparity can be measured in
seconds of arc. The minimum stereoscopic resolution is a disparity of approximately 30 to 40 s of arc. Stereoscopic resolution
depends upon visual acuity, as poor vision in one or both eyes
will decrease stereoacuity. A general guide on the effect of image
blur on stereoacuity is seen in Table 3-1. Interpupillary distance
also influences stereoacuity. The farther apart the two eyes, the
greater the angle of visual disparity and the greater the stereoscopic potential. Additionally, the closer an object is to the eyes,
the greater the angle of disparity; therefore, the better the stereoscopic view. As objects move away from the observer, the relative interpupillary distance diminishes as does the visual angle,
so stereoscopic vision decreases for distance objects.
CONTOUR STEREOACUITY TEST
Contour stereoacuity tests use stereoscopic figures with a continuous contoured edge (Fig. 3-5). The Titmus test is a popular
contour stereoscopic test and measures disparities from 3000 s
arc (the big fly) to 40 s arc (ninth circle). Some pictures in the
test are stereoscopic and others are flat (two-dimensional). The
patient is required to identify which figure is stereoscopic.
Contour stereoscopic figures are clinically useful because the
stereoscopic effect is obvious and easy to see, but they have
the disadvantage of having monocular clues. Monocular clues
allow patients who are stereoblind to identify the stereoscopic
figures1,3; this occurs because each stereoscopic figure is made
chapter 3: binocular vision and introduction to strabismus
79
up of two drawings, nasally shifted off center (see Fig. 3-5).
Patients with monocular vision can identify which figure is supposed to be stereoscopic, because that figure will be horizontally
off center. Another type of monocular clue used by patients with
alternating strabismus to falsely pass contour stereo tests is
“image jump.”1 These patients alternate fixation between the
two horizontally displaced figures and identify the figure that
jumps back and forth. Monocular clues work for stereoscopic
figures with large disparities and if the stereoscopic figure is
framed so the displaced figure looks off center. The first three
stereoscopic “circles” and first stereoscopic “animal” on the
Titmus stereoacuity test can often be identified by using
monocular clues, but stereo figures with smaller disparities are
difficult to detect using monocular clues.
One way to help verify that the patient has true stereoacuity is to retest with the Titmus test book turned 90° and see if
the patient still sees the stereoscopic target. With the test book
turned 90°, the targets are not stereoscopic, but the monocular
clues still work. If the patient again identifies the stereoscopic
target, they are using monocular clues, not true stereopsis. For
further verification, turn the book 180° (upside down) and see if
the patient notes that the stereo targets have returned but are
now projecting in an opposite direction away from the patient.
The Titmus “fly” can be useful in preverbal children as young
as 1 to 2 years of age. If a child startles to the fly coming out of
the page, then this is suggestive of gross stereopsis. Also, if a
child clearly picks up the wings of the Titmus “fly” well off the
page, this is good evidence for at least some peripheral fusion.
RANDOM DOT STEREOACUITY TEST
Random stereograms consist of two fields of randomly scattered
dots or specks, with one field of dots projected to each eye separately through a haploscopic device. Each field of random dots
is identical except for a group of dots that is displaced nasally.
The group of displaced dots can take the form of any recognizable shape, such as the square shown in Figure 3-6. The nasally
displaced square of dots stimulates bitemporal retinal points and
produces the perception that a single square of dots is coming
up off the page. Random dot stereoacuity tests have an advantage over contour stereo tests, as random dot tests have almost
no monocular clues, and a positive response indicates true
stereopsis with few false-positive responses.8 The problem with
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handbook of pediatric strabismus and amblyopia
FIGURE 3-6. Diagrammatic representation of a Randot stereogram. The
left eye sees one set of dots and the right eye sees a second set of dots.
The dots are identical, except for the dots within the square that have
been horizontally displaced (nasally in the figure). Nasal displacement
stimulates bitemporal disparate retinal points and produces the stereoscopic perception that the square of circles is raised off the page. This
clinical test for Randot stereoacuity consists of nasal displacement, so
that the stereo images appear to come off the page.
random dot stereoacuity testing, however, is that many young,
normal children and some normal adults have trouble seeing the
random dot stereoscopic effect and falsely fail the test.
Monocular Depth Perception
Depth perception can occur without stereoacuity. Monocular
vision can provide information regarding depth and the distance
of an object. Motion parallax, shadows, object overlap, and the
relative size of objects give us monocular clues of depth. Motion
chapter 3: binocular vision and introduction to strabismus
81
parallax is the perception of a change in position of an object
resulting from a change in position from where the object is
viewed. For example, a monocular observer viewing a distant
object will note that near objects move to the left as the observer
moves his head to the right. Monocular clues can be so powerful that one-eyed patients, or patients with large-angle strabismus, can successfully perform a variety of tasks that require
keen depth perception. Professional athletes, microsurgeons,
even ophthalmologists have been successful using monocular
depth perception.2
Bifoveal Fusion
Marshall Parks coined the term “bifoveal fusion” or “bifixation” to indicate the normal state of binocular fusion.7 Bifoveal
fusion includes high-grade stereoacuity of 40 to 50 s of arc, accurate eye alignment, and normal motor fusion. Patients with
bifoveal fusion have normal retinal correspondence.
Rivalry
Rivalry, or as it is sometimes termed, retinal rivalry, is a condition where a patient with normal binocular vision is presented
with different images to corresponding retinal points of each
eye. Instead of seeing two different images superimposed on
each other (termed “confusion”), the subject perceives patchy
dropout of each image where the images binocularly overlap.
Rivalry can be demonstrated most dramatically by presenting
parallel lines to each eye with the lines rotated 90° in one eye
(Fig. 3-7). The observer will perceive that some of the lines disappear in a spotty fashion as they cross over each other. You can
experience rivalry by placing a pencil horizontally 2 inches in
front of one eye and your index finger vertically 2 inches in front
of the other eye. Note that there is patchy dropout of either the
pencil or the index finger where they overlap. The rivalry phenomenon is often described as retinal rivalry; however, it is a
complex interaction involving cortical inhibition. The presence
of rivalry indicates the existence of bifoveal fusion potential.
Motor Fusion
Motor fusion is the mechanism that allows fine-tuning of eye
position to maintain eye alignment. It acts as a locking mecha-
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A
C
B
FIGURE 3-7A–C. Diagonal lines are presented to each eye with the lines
oriented 90° to each other (A,B). The combined binocular perception is a
patchy pattern, with lines from each eye being seen; however, because of
rivalry, crossing lines are not seen (C).
nism to keep the eyes aligned on visual targets as they move
through space. Motor fusion also controls innate tendencies for
the eyes to drift off target. These correctional eye movements
that maintain binocular foveal alignment provided by motor
fusion are termed fusional vergence movements.
Unlike version movements, in which both eyes move in
the same direction, vergence eye movements are in the
opposite direction; they are termed “disjunctive” and disobey
Hering’s law. Convergence, for example, is invoked when one
eye follows an object moving from distance to near and results
in both eyes moving to the midline with the right eye moving
left and the left eye moving right (Fig. 3-8A). You can experience convergence by fixating on a pencil at arm’s length
and slowly bringing the pencil to your nose. As the pencil
approaches your nose, the eyes converge to hold alignment on
the pencil. Convergence movements are the strongest vergence
chapter 3: binocular vision and introduction to strabismus
83
movements, and there are several mechanisms that contribute
to convergence (see Vergence Amplitudes, following).
In addition to convergence, there are two other vergence
movements: divergence and vertical vergence (Fig. 3-8B,C).
Divergence is used to follow an object moving away and consists of the right eye moving right and left eye moving left. Vertical vergence is the weakest vergence movement and keeps our
eyes from drifting vertically. Vertical vergence is depression of
one eye with elevation of the fellow eye.
Measurement of vergence amplitudes and a discussion of
the various mechanisms of convergence are presented next.
A
B
C
FIGURE 3-8A–C. Vergence. (A) Convergence of the eyes as the pencil
approaches from the distance. (B) Divergence as the patient changes fixation from a near target to a distance target. (C) Vertical vergence, as the
patient vertically aligns the eyes to compensate for the vertical phoria or
an induced deviation produced by a vertical prism.
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INTRODUCTION TO STRABISMUS
Normally our eyes are well aligned so the foveas are aimed on
the same visual target; this is termed orthotropia (Fig. 3-9). Strabismus is the term for ocular misalignment, or if there is an
underlying tendency toward misalignment. Another term for
strabismus is “squint.” This term comes from the fact that strabismic patients often squint one eye to block out one of the two
images that they see. A manifest misalignment is called a
heterotropia or tropia for short. A tropia causes double vision
(diplopia) if acquired after 7 to 9 years of age; however, children
under 6 to 7 years of age will cortically suppress vision from the
deviated eye. Cortical suppression is a neurological mechanism
that allows children to eliminate diplopia. Children who alternate fixation between eyes (i.e., alternate suppression) will
retain equal vision, but constant suppression of the deviated eye
can cause decreased vision of the deviated eye, resulting in
strabismic amblyopia.
In contrast, a hidden tendency for an eye to drift is termed
heterophoria or phoria. Patients with a phoria have a latent
tropia and use motor fusion to maintain proper alignment. One
can demonstrate the latent deviation of a phoria by disrupting
binocular fusion. Occluding or fogging the vision of one eye
(either eye) will disrupt fusion, and the eye behind the occluder
will deviate (Fig. 3-10). Identifying a phoria indicates that some
degree of motor fusion is present. Orthophoria is the state of the
eyes where there is no strabismus and not even a tendency for
the eyes to drift (i.e., no phoria). Orthophoria is rare to non-
FIGURE 3-9. Normal eye alignment with image falling on both foveas.
chapter 3: binocular vision and introduction to strabismus
85
A
B
FIGURE 3-10A,B. Alternate cover test in patient with an esophoria. (A)
Eyes are straight; the patient has a tendency to cross (esophoria), but
fusional divergence maintains proper alignment. (B) Left eye is covered,
dissociating fusion and allowing the left eye to manifest the esophoria.
Note that the left eye turns in under the cover.
existent, as virtually all normally sighted people, with normal
bifoveal fusion, have a small phoria but maintain alignment
through motor fusion. Thus, most normal people are orthotropic
but heterophoric.
Phorias may spontaneously become manifest under conditions such as fatigue or illness that can cause central nervous
system depression and diminish motor fusion. Central nervous
system depressants also diminish motor fusion, and a patient
with a large phoria may manifest their deviation after imbibing
alcoholic beverages or taking sedatives. (This explains why the
cowboy sees double after celebrating in town with one too many
whiskies.) A large phoria that is difficult to control may spontaneously become manifest, and this is called an intermittent tropia.
Strabismus most commonly occurs in infancy or childhood
and is usually idiopathic or related to a refractive error. In most
of these cases, the eye muscles are normal and the eye can rotate
freely. Less often, mechanical restriction of eye movements
(restrictive strabismus) or an extraocular muscle paresis (paralytic strabismus) causes the strabismus. A blind eye may also
drift, and this is termed sensory strabismus.
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handbook of pediatric strabismus and amblyopia
Ocular misalignment may be horizontal, vertical, torsional,
or any combination of these. Strabismus is described by prefixes
that tell the direction of the deviation: eso, turning in; exo,
turning out; and hyper, vertical deviation. A suffix is added to
the prefix to denote if the strabismus is a tropia or phoria. An
esodeviation that is a tropia is termed an esotropia (ET) and a
phoria is termed an esophoria (E); likewise, an exodeviation is
either an exotropia (XT) or exophoria (X). The strabismic patient
will have one eye fixing on a target and the fellow eye will
deviate. With esotropia, the deviated eye turns in so the target
image falls nasal to the fovea (Fig. 3-11). In exotropia, the eye
FIGURE 3-11. Alternating esotropia. Top diagram: right eye is fixing and
the image is aligned with the right fovea while the image falls nasal to
the left fovea as the left eye is deviated. Bottom diagram: left eye is fixing
with the image falling on the left fovea and the image falling nasal to the
right fovea as the right eye is deviated.
chapter 3: binocular vision and introduction to strabismus
87
FIGURE 3-12. Alternating exotropia. Top diagram: right eye is fixing
with the left eye and the image falling temporal to the fovea. Bottom
diagram: exotropic left eye is fixing with a right exotropia and the image
falling temporal to the right fovea.
turns out and the target image is temporal to the fovea (Fig. 312). Note that fixation can switch from eye to eye. According to
Hering’s law, as the deviated eye moves into primary position,
the fixing eye turns in the same direction to become the deviated eye (compare upper and lower drawings of Figs. 3-11 and
3-12).
Vertical strabismus can be categorized as hypertropia or
hypotropia. Because of Hering’s law, a left hypertropia is the
same deviation as a right hypotropia, depending on which eye is
fixing (Fig. 3-13). In contrast to a horizontal deviation, when
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handbook of pediatric strabismus and amblyopia
FIGURE 3-13. Alternating left hypertropia. Top left: right eye fixing and
a left hypertropia. Top right: retinal image (x) is falling on the fovea (small
dot) of the right eye; however, the left fovea is rotated down (left hypertropia) so the retinal image (x) is located above the fovea (small dot).
Bottom: left eye fixing with right eye turned down. Now the retinal image
(x) falls below the right fovea, which is rotated up (right hypotropia).
describing a hyperdeviation we must identify which side the
hypertropia is on, either right hypertropia (RHT) or left hypertropia (LHT). By convention, we usually refer to a vertical deviation as a hypertropia, rather than use the term hypotropia,
unless there is an obvious restriction or paresis that keeps one
eye in a hypotropic position. This convention has practical
importance as it minimizes confusion over which terminology
is used, thus reducing the risk of inadvertently operating for
a right hypotropia when the patient actually had a right
hypertropia.
Cyclotropia, or torsion, refers to a twisting misalignment
around the Y axis of Fick. Excyclotropia (extorsion) is a temporal rotation of the 12 o’clock position, whereas incyclotropia
(intorsion) means a nasal rotation of the 12 o’clock position.
Normally the fovea should be aligned between the middle and
the lower pole of the optic disc (Fig. 3-14, top). If the fovea is
below the lower pole of the optic disc by direct view (above the
disc in the indirect ophthalmoscopic view), this indicates objective extorsion (Fig. 3-14, bottom left). A fovea oriented above the
middle of the optic disc by direct view (below the middle in the
indirect ophthalmoscopic view) indicates intorsion (Fig. 3-14,
bottom right). Torsion can also be measured by the Maddox
rod test, and this is termed subjective torsion. Torsional motor
chapter 3: binocular vision and introduction to strabismus
89
fusion is weak to nonexistent; therefore, a tendency for torsional
misalignment is manifest as a tropia and, for practical purposes,
torsional phorias do not exist. There are consequently no torsional vergence eye movements. A small amount of torsional
misalignment, however, is tolerated surprisingly well as the
brain will accept up to 5° of torsional misalignment. Patients
with a tropia less than 10 prism diopters (PD) will often have
peripheral fusion and have a phoria coexisting with a small
tropia. This condition is called the monofixation syndrome and
is associated with peripheral binocular fusion, central fixation
with the preferred eye, and central suppression of the foveal area
in the fellow eye. Tropias greater than 10 PD preclude fusion, as
the disparity of the images is too great to allow for even peripheral fusion. Patients with a tropia greater than 10 PD will not
have motor fusion and will not have a coexisting phoria.
FIGURE 3-14. Ocular torsions through the direct view (left eye). Top:
normal fovea to disc relationship with the fovea located along the lower
half of the disc. Lower left: extorsion with the fovea below the lower half
of the disc. Lower right: intorsion with the fovea above the lower half of
the disc. In actuality, it is the disc that rotates around the fovea.
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Prisms and Strabismus
Prisms are important tools for the diagnosis and treatment of
strabismus, as they are used to measure and neutralize ocular
deviations. A prism bends light toward the base of the prism (Fig.
3-15) because light has both particle and wave characteristics.
As light passes through the prism, the part of the light wave
closest to the prism base has more prism to traverse than the
part of the wave closest to the apex. This is analogous to a row
of soldiers marching through a triangle of sand; the soldiers walk
slowly through sand so those at the base of the triangle exit the
sand after the soldiers at the apex. The direction of the marching soldiers turns toward the base of the triangle as they exit.
The ability of a prism to bend light is measured in prism
diopters (PD). Light travels slower through the plastic prism
than it does through air, so light toward the base of the prism
takes longer to exit than light traversing the apex. The exit time
differential causes the light to bend toward the base of the prism.
One prism diopter will shift light 1 centimeter (cm) at 1 meter
(m) or a displacement of approximately 0.5°. A 20 PD esotropia
A
B
C
FIGURE 3-15A–C. Diagram of the effect of a prism over one eye. (A)
Patient fixates on the X. (B) A prism is introduced, and the image is displaced toward the base of the prism and off the fovea. Note that the
patient will perceive the image to jump in the opposite direction. Thus,
a patient will perceive the image to jump in the direction of the apex of
the prism. (C) Patient refixates to place the image on the fovea by rotating the eye toward the apex of the prism. Note that when a prism is introduced, the patient will always refixate by rotating the eye in the direction
of the apex of the prism.
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91
would mean the eye turns in approximately 10°. When a prism
is placed in front of one eye, it moves the image off the fovea,
causing a perceived image “jump.” The retinal image will shift
toward the base of the prism, but the perceived image jump is
in the opposite direction, toward the apex of the prism; this is
because the retinal images are reversed, right/left and up/down
(Fig. 3-15A,B). To refixate on the shifted image, the eye will
move in the direction of the prism’s apex, thus aligning the fovea
with the new image location (Fig. 3-15C).
Prism Neutralization of a Deviation
Prisms can be used to optically neutralize or correct strabismus.
A prism acts to change the direction of the incoming image so
the retinal image in each eye falls directly on the fovea. Neutralization occurs when enough prism is placed in front of the
eye so the two foveas are aligned on the same object of regard.
For example, when a base-out prism (prism held horizontally
with the apex directed toward the nose) is placed in front of the
deviated eye of a patient with esotropia, the retinal image shifts
temporally toward the fovea (Fig. 3-16). If the correct amount of
prism is used, the retinal image will fall directly on the fovea of
the deviated eye. Thus, as seen in Figure 3-16B, the deviation
has been optically neutralized by the prism even though the eye
is still anatomically deviated.
The rule for neutralizing a deviation is to orient the prism
so the apex is in the direction of the deviation. For esotropia, the
apex is directed nasally and, for exotropia, the apex is directed
temporally. The apex is directed superiorly over a hypertropic
eye and inferiorly over a hypotropic eye.
The prism can also be placed in front of the fixing eye
(straight eye) to neutralize the deviation. If the prism is placed
base-out in front of the fixing eye (Fig. 3-17), the retinal image
will move temporal to the fovea (Fig. 3-17A,B). The fixing eye
will see the image shift and will immediately rotate nasally to
reestablish foveal fixation (Fig. 3-17). As the fixing eye rotates
nasally, the deviated eye rotates temporally causing a version
movement to the right (Fig. 3-17B). Therefore, when a base-out
prism is placed in front of the fixing eye, both eyes move in the
same direction as the apex of the prism, and both foveas shift
into alignment (Fig. 3-17B,C). In Figure 3-17C, both eyes have
shifted to the right, with the left eye now turned in nasally and
the right eye now straight in primary position. The previously
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A
B
FIGURE 3-16A,B. Prism neutralization. (A) Patient with an esotropia. (B)
A prism is introduced to direct the image onto the fovea of the left eye,
thus correcting, or neutralizing, the deviation.
deviated right eye is now straight and in alignment with the
fixation target. Thus, one can place a prism in front of either
eye or even split the prisms between the eyes to neutralize a
strabismic deviation.
Prism-Induced Strabismus
A prism placed over one eye in a patient with straight eyes will
induce a deviation and produce strabismus. A base-in prism
induces esotropia, as the target image is displaced nasal to the
fovea (Fig. 3-18). Likewise, a base-up prism induces a hypertropia
and a base-out prism induces an exotropia.
chapter 3: binocular vision and introduction to strabismus
93
A
B
C
FIGURE 3-17A–C. Neutralization of an esotropia by placing the prism in
front of the fixing eye. (A) Esotropia with left eye fixing. (B) Prism is
placed base out in front of the fixing eye (left eye), which displaces the
image temporally off the fovea. The left eye rotates nasally to refixate to
the displaced image. As stated by Hering’s law, both eyes rotate in the
direction of the apex of the prism. (C) Patient fixing through the prism,
left eye. The left eye has deviated nasally to put the image on the fovea.
The right eye has moved temporally and is also in alignment with the
fixation target.
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handbook of pediatric strabismus and amblyopia
A
B
C
FIGURE 3-18A–C. Prism-induced esotropia. Patient with straight eyes
and binocular vision is given an esotropia by placing a base-in prism over
one eye. (A) Patient orthotropic with images falling on both foveas. (B)
Base-in prism is placed before the left eye causing the image to move
nasally off the fovea. Patient is fixing with right eye. (C) Patient now
fixates with the left eye, viewing through the base-in prism. Left eye
moves temporally to place the image on the fovea and, because of Hering’s
law, the right eye moves nasally to displace the right retinal image nasally
off the fovea.
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95
Prism-Induced Vergence
Normal adult subjects with binocular fusion will see double
when a prism is placed in front of one eye. If the prism is relatively small, the patient’s fusional vergence eye movements will
be able to realign the eyes to keep the images appropriately
placed on the foveas. The prism will initially invoke diplopia
and the patient will realign the eyes within a second or two to
replace the diplopia with single binocular vision. A base-out
prism evokes fusional convergence, a base-in prism causes
fusional divergence, and a base-up or base-down prism will
evoke fusional vertical vergence. Figure 3-19 shows the steps of
prism-induced convergence. A base-out prism placed over one
eye will displace the retinal image off the fovea onto temporal
retina, inducing an exotropia (Fig. 3-19A,B). The eye behind the
prism moves nasally to refixate to the fovea and the fellow eye
moves temporally in a version movement (Hering’s law) (Fig. 319B). Diplopia occurs briefly until fusional convergence is used
to realign the eyes so retinal images can fall directly on each
fovea (Fig. 3-19C,D). The key aspect of the convergence movement is the nasal fusional movement of the eye without the
prism (Fig. 3-19C). Note that, after prism-induced strabismus in
a patient with fusion, a compensatory vergence movement will
occur in the eye without the prism (Fig. 3-19C). Prism-induced
strabismus in a patient without fusion results in a version movement of both eyes without a subsequent vergence movement
(see Fig. 3-18C).
Fusional Vergence Amplitudes
Vergence movements compensate for phorias and keep the eyes
aligned as targets move in depth throughout space. A patient
with an exophoria uses convergence; those with esophorias use
divergence, and hypertropias are controlled with vertical vergence. Convergence is by far the strongest of the vergence movements and can be strengthened by eye exercises if convergence
is ineffective. Divergence is relatively weak and does not significantly improve with eye exercises. The strength of vergence
movements can be measured in prism diopters and is called
fusional vergence amplitudes.
Fusional vergence amplitudes are measured by inducing a
deviation to stimulate a motor fusion to correct the induced
deviation. Induce an exodeviation to test convergence (base-out
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 3-19A–B. Four steps of prism convergence. (A) Eyes are well
aligned in a patient with good fusional convergence. (B) Exophoria is
created by introducing a base-out prism in front of the left eye. Patient initially fixates with the left eye, causing a version movement to the right,
thus placing the left fovea on the image.
prism), an esodeviation for divergence (base-in prism), and a
hyperdeviation for vertical vergence. Start by inducing a small
deviation that can be fused and gradually increase the deviation
until vision is blurred (blur point), then increase until fusion
breaks (break point). A deviation can be induced by placing
prisms (usually in the form of a prism bar) over one eye or by
chapter 3: binocular vision and introduction to strabismus
97
C
D
FIGURE 3-19C–D. (C) Because of Hering’s law, the right eye also rotates
and the image is now off the right fovea. To compensate for this, patient
exercises fusional convergence and the right eye rotates nasally to put
the image on the fovea; this is a vergence movement in distinction to
the version movement seen in (B). (D) Patient is once again fusing, using
fusional convergence to maintain eye alignment on the fixation target.
Note that the eye behind the prism is deviated nasally. The base-out prism
actually induces an exophoria, even though the eye behind the prism is
nasally deviated and looks esotropic.
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TABLE 3-2. Normal Fusion Vergence Amplitudes.
Convergence
Divergence
Vertical vergence
Distance
(6 m)
Near
(1/3 m)
20–25 PD
6–8 PD
2–3 PD
30–35 PD
8–10 PD
2–3 PD
PD, prism diopter.
moving the amblyoscope arms off parallel. Measure nearconvergence amplitudes by placing a base-out prism bar over one
eye, starting with 4 PD, having the patient fixate on an accommodative target at a distance of 33 cm. Then, move the bar up
slowly to increase the base-out prism. The eye behind the prism
bar will progressively turn in to converge as the prism is
increased. The greatest prism that the patient can fuse is the
fusional vergence amplitude. Prisms larger than this will break
fusion and one eye will turn out, usually causing diplopia. Have
the patient note when the fixation target blurs (i.e., blur
point), and when it becomes double (i.e., break point). Table
3-2 shows normal fusion vergence amplitudes based on the
break point.
The maximum base-out prism that can be fused is around
30 PD (convergence), the maximum base-in prism that can be
fused is 6 to 10 PD (divergence), and the maximal vertical prism
that can be fused is usually 2 to 3 PD (vertical vergence). In
certain conditions, divergence and vertical vergence fusional
amplitudes can be quite large. Patients with congenital superior
oblique palsy, for example, can have vertical fusion vergence
amplitudes up to 25 to 30 PD.
Types of Convergence
There are various mechanisms of convergence; these include
fusional convergence, accommodative convergence, tonic convergence, voluntary convergence, and proximal or instrument
convergence.
FUSIONAL CONVERGENCE
Fusional convergence is based on binocular vision. Occluding,
or severely blurring the image of one eye, will disrupt fusional
convergence; however, convergence mechanisms still function
when binocular vision is suspended.
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99
ACCOMMODATIVE CONVERGENCE AND THE NEAR REFLEX
When an object approaches from distance to near, the images
falling on the retina are displaced temporally, then blur and
enlarge. These retinal image changes stimulate the near reflex.
The near reflex includes accommodation, convergence, and
pupillary miosis. The ciliary muscles contract to increase the
lens curvature and focus the image (accommodation). Contraction of both medial rectus muscles occurs to keep the eyes
aligned on target (convergence), and the pupil constricts to
increase the depth of focus. The synkinetic reflex of accommodation and convergence is termed accommodative convergence.
Accommodation is one of the main drivers of convergence. For
any individual, a specific amount of accommodation will result
in a specific amount of convergence. The quantitative relationship between the amount of convergence associated with an
amount of accommodation is referred to as the AC/A ratio
(accommodative convergence/accommodation). A high AC/A
ratio indicates overconvergence whereas a low AC/A ratio indicates convergence insufficiency. Patients with a high AC/A ratio
are predisposed to developing esotropia (crossed eyes) at near,
and a low AC/A ratio causes an exotropia (eye turning out) at
near. The normal AC/A ratio is between 4 and 6 PD of convergence for every diopter of accommodation. Patients with wide
interpupillary distances (PD) will have to have a relatively high
AC/A ratio to converge sufficiently and keep both eyes aligned
on near targets. The methods for measuring the AC/A ratio are
described in Chapter 5.
TONIC FUSIONAL CONVERGENCE
Tonic fusional convergence is a type of fusional convergence
that persists even after monocular occlusion is introduced; this
is a form of proprioceptive eye position control, which keeps the
eyes converging even after one eye is occluded. Tonic fusional
convergence dissipates with prolonged monocular occlusion.
Patching one eye for 30 to 60 min eliminates most tonic fusional
convergence. Tonic fusional convergence is referred to as tenacious proximal fusion by Kushner.5
VOLUNTARY CONVERGENCE
Voluntary convergence is voluntarily invoked. Comedians use
this to cross their eyes, and patients will voluntarily converge
to produce convergence nystagmus.
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PROXIMAL OR INSTRUMENT CONVERGENCE
This type of convergence is induced by a psychological awareness of an object at near, or when one views an object through
an instrument such as a microscope.
Comitant Versus Incomitant Strabismus
Strabismus can be classified into two broad categories: comitant
and incomitant. Comitant strabismus is when the deviation
measures the same in all fields of gaze. Most types of congenital and childhood strabismus are comitant. With comitant strabismus, both eyes move together equally well and there is no
significant restriction or paresis. Comitant strabismus is usually
a “good” sign and indicates that the strabismus is not secondary
to a neurological problem. Occasionally, however, acquired neurological disease processes, such as early-onset myasthenia gravis,
chronic progressive external ophthalmoplegia (CPEO), or even a
mild bilateral sixth nerve palsy, can initially present as a clinically comitant strabismus.
Incomitant strabismus means the deviation is different
in different fields of gaze. In the vast majority of cases,
incomitance is caused by a limitation of ocular rotations
secondary to ocular restriction or extraocular muscle paresis.
Causes of ocular restriction include a tight or stiff muscle
and periocular adhesions to the eye. Muscle paresis can be
caused by a lack of innervation (i.e., third, sixth, or fourth nerve
paresis), traumatic muscle damage, an overrecessed or lost
muscle, or neuromuscular junction disease such as myasthenia
gravis.
Figure 3-20 shows an example of an incomitant esotropia
secondary to limited abduction of the left eye. When the
patient in Figure 3-20 looks to the left, the left eye cannot
fully abduct; thus, the right eye overshoots and creates an
esotropia (ET) that increases in leftgaze (Hering’s law of yoke
muscles). In this example, the limited abduction could be
due to either restriction (e.g., a tight left medial rectus muscle
or a nasal fat adherence scar to the globe) or paresis (e.g., left
sixth nerve palsy or left slipped lateral rectus muscle). Methods
for diagnosing restriction and paresis are presented in
Chapter 5.
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101
FIGURE 3-20. Left lateral rectus paresis. In primary position, there is a
moderate esotropia. In right gaze, the esotropia (ET) diminishes, and in
left gaze the esotropia increases. A tight left medial rectus muscle
would give the same pattern of incomitance.
Primary Versus Secondary Deviation
Patients with incomitant strabismus secondary to ocular restriction or muscle paresis will show a larger deviation when the eye
with limited ductions is fixing (secondary deviation) than when
the eye with full ductions fixates (primary deviation); this is in
accord with Hering’s law. As shown in Figure 3-21, the primary
deviation is small because relatively little innervation (1) is
needed to keep the eye in primary position when the nonparetic
A
B
FIGURE 3-21A,B. Left sixth nerve palsy. (A) Normal right eye fixating
with little effort. Only 1 innervation is needed to put the eye on target;
there is a small esotropia of 25 PD. (B) Change of fixation to the left eye.
Because the left lateral rectus muscle is weak, it requires 4 innervation
to bring the left eye to primary position to view the target. The right
medial rectus muscle is the yoke muscle to the weak left lateral rectus
muscle, so the right medial rectus muscle also gets 4 innervation. The
4 innervation of the normal right medial rectus results in a large
esotropia of 50 PD.
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handbook of pediatric strabismus and amblyopia
right eye is fixing (Fig. 3-21A). The paretic eye receives the same
1 innervation and turns in slightly because the left lateral
rectus muscle is slightly weaker than its antagonist, the left
medial rectus muscle. The secondary deviation is larger because
the weak left lateral rectus muscle must receive a tremendous
amount of innervation (4) to bring the left eye into primary
position when the paretic eye fixates (Fig. 3-21B). Both the
paretic left lateral rectus and its yoke muscle, the right medial
rectus, receive 4 innervation because of Hering’s law. This
excess drive to the healthy right medial rectus muscle causes
a large secondary nasal deviation of the right eye. This same
mechanism of primary and secondary deviations also applies to
restrictions.
Primary overaction of oblique muscles can also cause
incomitance. What we clinically refer to as primary muscle
overaction, however, may actually represent a previous paresis
of the antagonist and secondary overaction of the agonist
muscle.
References
1. Archer SM. Stereotest artifacts and the strabismus patient. Arch Clin
Exp Ophthalmol 1988;226:313–316.
2. Burden AL. The stigma of strabismus. Arch Ophthalmol 1994;112:
302.
3. Clarke WN, Noel LP. Stereoacuity testing in the monofixation syndrome. J Pediatr Ophthalmol Strabismus 1990;27:161–163.
4. Donzis PB, et al. Effect of binocular variations of Snellen’s visual
acuity on Titmus stereoacuity. Arch Ophthalmol 1983;101:930–932.
5. Kushner BJ. Exotropic deviations: a functional classification and
approach to treatment. Am Orthopt J 1988;38:81–93.
6. Levy NS, Glick EB. Stereoscopic perception and Snellen visual
acuity. Am J Ophthalmol 1974;78:722–724.
7. Parks MM. The monofixation syndrome. Trans Am Ophthalmol Soc
1969;12(42):1246.
8. Reincke RD, Simons K. A new stereoscopic test for amblyopia
screening. Am J Ophthalmol 1974;78:714–721.
4
Visual Development
and Amblyopia
Kenneth W. Wright
NORMAL VISUAL DEVELOPMENT
Monocular Visual Development
At birth, visual acuity is poor, in the range of hand motions to
count fingers. For the most part, this is due to immaturity of
visual centers in the brain responsible for vision processing.
Visual acuity rapidly improves during the first few months of
life as clear in-focus retinal images stimulate neurodevelopment
of visual centers, including the lateral geniculate nucleus and
striate cortex.52 Dropout and growth of neuronal connections
give rise to the organizational refinement and establish highresolution receptive fields corresponding to the central foveal
area.18,23 Normal visual development requires appropriate visual
stimulation, including clear retinal images, with equal image
clarity in both eyes (Table 4-1).
Visual development is most active and vulnerable during
the first 3 months of life, which is termed the critical period of
visual development.13 Figure 4-1 shows a curve of visual acuity
improvement versus age. Note the curve is steepest during the
first months of life, relative to the critical period of visual development. Visual acuity development continues up to 7 to 8 years
of age, but development is slower and plasticity is progressively
less in later childhood. Abnormal visual stimulation by a blurred
retinal image or strabismus during early visual development
(e.g., congenital cataract, strabismus) can result in permanent
damage to visual centers in the brain (see section on amblyopia
later in this chapter). Early treatment of pediatric eye disorders
is important to promote normal visual development.
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handbook of pediatric strabismus and amblyopia
TABLE 4-1. Requirements for Normal Visual Development.
Clear retinal images
Equal image clarity
Proper eye alignment
Binocular Visual Development
Binocular visual development occurs in concert with improving
monocular vision.7 Basic neuroanatomy tells us that the two
eyes are linked, as nasal retinal axons cross to meet temporal
retinal axons in the chiasm, then proceed to join neurons in the
lateral geniculate nucleus. Neurons in the lateral geniculate
nucleus project to the striate cortex to connect with binocular
cortical neurons that respond to stimulation of either eye and
monocular cortical neurons that respond to the stimulation of
only one eye. In humans, and in most animals with binocular
vision, approximately 70% of the neurons in the striate cortex
are binocular neurons whereas the minority are monocular.
Binocular cortical neurons along with neurons in visual association areas of the brain produce binocular stereoscopic vision.
Animal studies demonstrate that binocular cortical neurons
are present from birth.37,57 Maintenance and refinement of these
binocular neuroanatomic connections and the development of
normal binocular visual function, however, are dependent on
FIGURE 4-1. Curve represents visual acuity development with age on the
horizontal axis and Snellen acuity on the vertical axis. Note the exponential improvement in visual acuity during the critical period of visual
development (birth to 3 months). m, months; y, years.
chapter 4: visual development and amblyopia
105
appropriate binocular visual stimulation. Requirements for
normal binocular visual development include clear and equal
retinal stimulation and proper eye alignment (see Table 4-1).
Binocular vision and fusion have been found to be present
between 1.5 and 2 months of age,4,26 while stereopsis develops
later, between 3 and 6 months of age.2,3,17 This author cared for
a patient with a transient congenital sixth nerve palsy who presented at 3 weeks of age with a compensatory face turn to obtain
binocular fusion. This single case suggests that early motor
fusion may be present as early as 3 weeks of age.
NEONATAL ALIGNMENT
Eye alignment is variable during the first few weeks of life. In
a study by Sondhi et al.39 of 2271 newborns, 67% showed an
exodeviation, 30% had essentially straight eyes, 2% swung
between eso- and exodeviations, and only 1% had an esodeviation. By 2 months of age, all the esodeviations resolved, and 97%
of exodeviations cleared by 6 months. Thus, almost all newborns have straight eyes or an exotropia, but esotropia is rare.
The presence of an exodeviation at birth allows our innate strong
fusional convergence to align the eyes. An esotropia, on the
other hand, is more difficult to control because fusional divergence is weak.
EYE MOVEMENT DEVELOPMENT AND
SMOOTH PURSUIT ASYMMETRY
Neonates typically have sporadic, jerky eye movements made
up of saccadic eye movements without smooth pursuit. Initially,
saccades are hypometric, but they continue to improve throughout infancy and childhood. Smooth pursuit eye movements
develop after 4 to 6 weeks of age, with most infants having accurate smooth pursuit by 2 months of age. Horizontal smooth
pursuit develops for targets moving in a temporal to nasal direction before pursuit movements in a nasal to temporal direction
develop. This developmental lag in nasally directed smooth
pursuit is called smooth pursuit asymmetry and is only seen
under monocular conditions with one eye covered. During
development, nasal to temporal pursuit movements are hypometric, requiring saccadic intrusion eye movements to keep up
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handbook of pediatric strabismus and amblyopia
with the moving target.1 Smooth pursuit asymmetry can be
detected clinically by testing monocular optokinetic nystagmus
(OKN). Neonates will show a diminished OKN response with
the drum rotating nasal to temporal as compared to temporal
to nasal. Normally, smooth pursuit asymmetry becomes symmetrical between 4 to 6 months of age.31,32 If binocular visual
development is disrupted during the first few months of life
(e.g., congenital esotropia and a unilateral cataract), smooth pursuit asymmetry and OKN asymmetry will persist throughout
life.12,41,42,54,55 Smooth pursuit asymmetry does not interfere with
normal visual function or the ability to read, as it is not present
under binocular viewing. It is, however, an important phenomenon that shows a physiological link between ocular motor
development and the development of binocular vision.
VISUAL DEVELOPMENTAL MILESTONES
Central fixation and accurate smooth pursuit are important clinical milestones of normal visual development (Table 4-2). Most
children will show central fixation and accurate smooth pursuit
eye movements by 2 to 3 months of age, but some infants may
show delayed visual maturation. Poor fixation at 6 months of
age is usually pathological, and should prompt a full evaluation
TABLE 4-2. Important Visual Developmental Milestones.
Age
Visual Milestones
0–2 months
Pupillary response
Sporadic fix and follow
Jerky saccadic eye movements
Alignment: exodeviations common, but esodeviations rare
Central fix and follow (mother’s face)
Accurate binocular smooth pursuit
Monocular smooth pursuit asymmetry: temporally directed,
slow; nasally directed, accurate optokinetic nystagmus
(OKN) present
Alignment: orthotropia with few exodeviations and no
esodeviations
Esotropia considered abnormal
Central fixation, reaches for toys and food
Accurate and smooth pursuit eye movements
Alignment: orthotropia
20/40 and not more than 2 Snellen lines difference
20/30 and not more than 2 Snellen lines difference
2–6 months
6 months–2 years
3–5 years
5 years
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107
for oculomotor or afferent visual pathway disease, including
electrophysiology and neuroimaging studies.
Abnormal Visual Development
A unilateral or bilateral blurred retinal image or strabismus will
disrupt early visual development and can cause permanent
visual loss. Following is a discussion of cortical suppression and
amblyopia.
CORTICAL SUPPRESSION
Strabismus, or a monocular blurred retinal image, causes dissimilar retinal images to fall on corresponding retinal areas of
each eye. If the dissimilarity between the retinal images is great
and the images cannot be fused, the visually immature adapts
by inhibiting cortical activity from the blurred or deviated eye.
This cortical inhibition usually involves the central portion of
the visual field and is termed cortical suppression. Images that
fall within the field of cortical suppression are not perceived,
forming an area called a suppression scotoma. Suppression only
occurs during binocular conditions with the dominant eye
actively viewing or “fixating” and disappears when the dominant eye is occluded. Suppression has been shown to reduce the
first positive peak (P-1) of the pattern visual evoked potential
(P.VEP) (Fig. 4-2).58 The P-1 reflects early visual processing at
the level of striate cortex, so it is likely that suppression occurs
at, or before, the primary visual cortex. In Figure 4-2B, both eyes
are open and the dominant eye is fixing whereas the nondominant eye is stimulated with the pattern. There is no P-1 response
from the nondominant eye because the visual activity from the
fixing eye cortically suppresses visual activity from the nondominant eye. Note that (in Fig. 4-2C) if the dominant eye is
occluded in a patient with esotropia, there is no suppression and
a high-amplitude P-1 is recorded from the nondominant eye.
Cortical suppression interferes with the development of
binocular cortical cells, resulting in abnormal binocular vision
and poor, or no, stereoscopic vision. If suppression alternates
between eyes, visual acuity will develop equally, albeit separately without normal binocular function. Constant suppression
of one eye, on the other hand, not only results in poor binocularity but also causes poor vision (i.e., amblyopia).
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Check stimulus
No stimulus
TV
Monitor
P-VEP
Response
AMP
Amblyopic eye
F ET
F
Occipital
electrode
A
No response
Fixing eye
B
Suppression
amblyopic eye
P-1
No suppression
amblyopic eye
Good response
C
FIGURE 4-2A–C. (A) Diagram of effect of suppression on the pattern
visual evoked potential (P.VEP). The patient being tested has an esotropia
and fixates with the dominant right eye. An alternating check stimulus
is presented to the deviated left eye during binocular viewing (B) and
again to the left eye, but with the dominant right eye occluded (C).
(B) The patient is fixating with the dominant right eye and is cortically
suppressing the deviated left eye. A check stimulus is presented to the
deviated left eye, but there is no P.VEP response recorded when the right
eye is fixing because visual information from the left eye is cortically
suppressed. (C) The dominant right eye is occluded and the left eye is
stimulated, resulting in a high-amplitude P.VEP response. There is no
suppression because the patient is monocularly fixing with the left eye.
The check stimulus now results in a robust cortical response from the
left eye.
AMBLYOPIA
Amblyopia occurs in approximately 2% of the general population and is the most common cause of decreased vision in childhood. The term amblyopia is derived from the Greek language
and means dull vision: amblys dull, ops eye. Generally
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speaking, amblyopia can refer to poor vision from any cause but,
in this volume and in most ophthalmic literature, amblyopia
refers to poor vision caused by abnormal visual development
secondary to abnormal visual stimulation. Other terms for this
type of amblyopia include functional amblyopia and amblyopia
ex anopsia. Children are susceptible to amblyopia between birth
and 7 years of age.25 The earlier the onset of abnormal stimulation, the greater is the visual deficit. The critical period for
visual development is somewhat controversial but probably
ranges from 1 week to 3 months of age. For practical purposes,
amblyopia is defined as at least 2 Snellen lines difference in
visual acuity between the eyes, but amblyopia is truly a spectrum of visual loss, ranging from missing a few letters on the
20/20 line to hand motion vision.
Functional amblyopia, or “amblyopia,” should be distinguished from organic amblyopia, which is poor vision caused by
structural abnormalities of the eye or brain that are independent of sensory input, such as optic atrophy, a macular scar, or
anoxic occipital brain damage. Functional amblyopia is reversible
when treated with appropriate visual stimulation during early
childhood, whereas organic amblyopia does not improve by
visual stimulation.
Pathophysiology and Classification of Amblyopia
Amblyopia is caused by abnormal visual stimulation during
visual development, resulting in abnormalities in the visual
centers of the brain. There are two basic forms of abnormal stimulation: pattern distortion (i.e., blurred retinal image) and cortical suppression (i.e., constant suppression of one eye). Pattern
distortion and cortical suppression can occur independently or
together to cause amblyopia in the visually immature. Amblyopia can be created by blurring one or both retinal images or by
inducing strabismus in visually immature animals (Fig. 4-3).
Strabismus will cause amblyopia in infant animals if the animal
fixates with one eye and constantly suppresses the fellow eye.
Strabismic animals that alternate fixation do not develop amblyopia; however, they do not develop binocular vision. Pathological changes associated with induced amblyopia in the animal
model occur in the lateral geniculate nucleus (LGN) and the
striate cortex.20,21,23,24,44,48,49 Figure 4-4 shows the pathological
changes in the lateral geniculate nucleus of a monkey raised
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with a monocular blurred retinal image. Normally, there are six
nuclear layers of the LGN: three layers corresponding to the
right eye and three layers corresponding to the left eye. Because
of the blurred retinal image, only three layers corresponding
to the eye with the clear retinal image developed. Due to the
increased visual stimulation of the good eye, these three layers
are darker stained and larger than normal.57 Ocular dominance
columns in the striate cortex are also damaged as a result of a
unilateral blurred image during early development (Fig. 4-4B).21
Von Noorden46,47 bridged the gap between human and animal
research when he identified similar neural anatomic changes in
a pathological study of humans with anisometropic amblyopia
and strabismic amblyopia. Thus, this evidence has shown that
the poor vision found with amblyopia is caused by brain damage.
Clinically, amblyopia is associated with strabismus and
strong ocular dominance (monocular suppression), a unilateral
blurred retinal image secondary to refractive error or media
opacity (pattern distortion and suppression), and bilateral
blurred retinal images (bilateral pattern distortion). Table 4-3
lists a classification of amblyopia based on etiology.
Strabismic Amblyopia
Amblyopia can occur in patients with a constant tropia who
show strong fixation preference for one eye and constantly suppress cortical activity from the deviated eye. Amblyopia can also
occur despite the fact that both eyes have clearly focused retinal
images. Patients with strabismus who alternate fixation and
alternate suppression do not have amblyopia, but they do have
abnormal binocular function. The mechanism for strabismic
amblyopia is constant cortical suppression that degrades neuronal connections to the deviated eye. Strabismic amblyopia
occurs in approximately 50% of patients with congenital
esotropia (a constant tropia), but is very uncommon in patients
with intermittent strabismus (e.g., intermittent exotropia) or
those with incomitant strabismus (e.g., Duane’s syndrome and
Brown’s syndrome) as they maintain central fusion by adopting
a compensatory face turn. Strabismic amblyopia can be moderate to severe, and in some cases even results in visual acuity of
20/200 or worse.
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FIGURE 4-3. Diagram of cortical sensory adaptation to various visual
stimuli during early visual development in the cat. Bars indicate percentage of occipital cortical cells that are either monocular cells, connected to the right eye (R) or left eye (L), or binocular cells, connected to
both eyes (B). First column, normal visual development, no amblyopia or
strabismus. Note that the majority of cortical cells are binocular, and the
right and left eye monocular cell populations are equal. Second column,
cortical adaptation to alternating esotropia. Note that the monocular cortical cells of left and right eye are now in the majority and there are relatively few binocular cells. There is no amblyopia, however, as the right
and left eye monocular cell populations are equal. Third column, effect
of a left esotropia with strong preference for the right eye so the left eye
is amblyopic. The majority of cortical cells are right eye monocular cells,
and there is a severe reduction of monocular left eye cells and binocular
cells. Fourth column, effect of monocular pattern distortion by blurring
the vision of the left eye with atropine. Left eye is amblyopic so it has
the lowest representation, and the majority of cortical cells are connected
to the right eye. Note that the binocular cells are diminished from normal
but are relatively well preserved because of peripheral fusion; this is
analogous to the monofixation syndrome associated with anisometropic
amblyopia. Fifth column, effect of equal pattern distortion to both eyes
by blurring vision in both eyes with atropine. Both eyes become amblyopic, but the binocular cortical representation is essentially normal with
the majority of cortical cells being binocular, and the left and right eye
control similar numbers of monocular cells; this is analogous to
ametropic amblyopia. (From Ref. 24, with permission.)
111
A
B1
FIGURE 4-4A,B. (A) Pathology of amblyopia (LGN): Cross-section of
lateral geniculate nucleus (LGN) from a normal monkey (left figure) vs.
amblyopic monkey caused by a unilateral blurred image (right figure).
Note that the normal LGN has 6 nuclear layers (darkly stained cell layerleft figure) and the amblyopic LGN has only 3 layers, and they are thicker
than normal (right figure).56,57
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B2
FIGURE 4-4A,B. (B) Pathology of amblyopia in monkey striate cortex
(visual cortex). Well-defined cortex dominance columns are seen in
normal specimen (B1 figures), but cortex columns are underdeveloped in
specimen for amblyopic monkey (B2 figures).21
Unilateral Pattern Distortion Amblyopia
Unilateral, or asymmetrical, retinal image blur can produce
amblyopia and loss of binocularity depending on the severity of
the condition. The ophthalmic literature often refers to amblyopia associated with monocular image blur as “pattern deprivation amblyopia.” This term is misleading, because unilateral
image blur results in pattern distortion and cortical suppression,
both of which contribute to the amblyopia.
Clinically, mild image blur (e.g., blur associated with mild
anisometropia) causes mild anisometropic amblyopia and allows
for the development of peripheral fusion and stereopsis (i.e.,
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TABLE 4-3. Classification of Amblyopia.
A. Strabismic amblyopia (suppression)
1. Congenital esotropia
2. Congenital exotropia
3. Acquired constant tropia in childhood
4. Accommodative esotropia
5. Small-angle tropia (monofixation syndrome)
6. Intermittent exotropia (rarely associated with amblyopia)
B. Monocular pattern distortion (suppression and pattern distortion)
1. Anisometropia
a. Hyperopia 1.50
b. Myopia 3.00
c. Meridional 1.50
2. Media opacities
a. Unilateral cataract
b. Unilateral corneal opacity (Peter’s anomaly)
c. Unilateral vitreous hemorrhage or vitreous opacity
C. Bilateral pattern distortion (pattern distortion)
1. Ametropia
a. Bilateral high hypermetropia 5.00
b. Bilateral meridional (astigmatic) 2.50
2. Media opacity
a. Bilateral congenital cataracts
b. Bilateral corneal opacities (Peter’s anomaly)
c. Bilateral vitreous hemorrhages
monofixation syndrome). A significant blurred image during
infancy (e.g., unilateral congenital cataract or corneal opacity),
however, can result in severe amblyopia. Vision can be as poor
as count fingers with total loss of binocular function manifested
by the development of sensory strabismus.
Anisometropic amblyopia, one of the most common types
of amblyopia, is caused by a difference in refractive errors that
results in a unilateral or asymmetrical image blur. Most patients
with anisometropic amblyopia have straight eyes and appear
“normal,” so the only way to identify these patients is through
vision screening. Stereoacuity testing has had limited value in
screening for anisometropic amblyopia because most patients
have relatively good stereopsis (between 70 and 3000 s arc).
Patients with anisometropic amblyopia usually have peripheral
fusion, and most have the monofixation syndrome.35 Myopic
anisometropia is generally less amblyogenic than hypermetropic
anisometropia. As little as 1.00 hypermetropic anisometropia
and 2.00 myopic anisometropia can be associated with amblyopia.51 Astigmatic anisometropic amblyopia does not occur
unless there is a unilateral astigmatism greater than 1.50 D.51
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115
For practical purposes, however, we do not see significant anisometropic amblyopia unless differences between the two eyes
are greater than 1.50 in hyperopes and greater than 3.00 in
myopes. Myopic anisometropic amblyopia is often amenable to
treatment even in late childhood whereas hypermetropic amblyopia is often difficult to treat past 4 or 5 years of age, probably
because high myopia is usually acquired after the critical period
of visual development, and the more myopic eye is in focus for
near objects (a baby’s world is up close). In contrast, patients
with hypermetropic anisometropia always use the less hypermetropic eye because it requires less accommodative effort and
constantly suppress the more hypermetropic eye.
Bilateral Blurred Retinal Image
Pattern distortion in its pure form without suppression occurs
when there is bilateral symmetrical image blur and no strabismus. Clinically, the effects of pure image blur are seen in cases
of bilateral high hypermetropia or bilateral symmetrical astigmatism, or with bilateral ocular opacities such as bilateral congenital cataracts and bilateral Peter’s anomaly. Bilateral pattern
distortion causes bilateral poor vision. Depending on the extent
of the distortion, some binocular fusion can develop, usually
associated with gross stereopsis. If severe image blur occurs
during the neonatal period so that essentially no pattern stimulation is provided, extremely poor vision and sensory nystagmus
develop. Bilateral amblyopia and nystagmus will occur in cases
of dense bilateral congenital opacities unless the image is cleared
by 2 months of age. This type of nystagmus is called sensory
nystagmus and is associated with bilateral severe amblyopia, or
other causes of congenital blindness such as macular or optic
nerve pathology. Sensory nystagmus does not occur with cortical blindness because extrastriate visual pathways anterior to
the occipital cortex supply the fixation reflex. Acquired opacities after 6 months of age usually do not cause sensory nystagmus because the motor component of fixation has already been
established. The presence of sensory nystagmus indicates severe
amblyopia, usually 20/200 visual acuity or worse.
Ametropic amblyopia (bilateral hypermetropic amblyopia)
usually occurs with hypermetropia greater than 5.00 D
without significant anisometropia.36 In these cases, visual acuity
is decreased in each eye, the eyes are usually straight, and the
patients usually have gross stereopsis. When patients are first
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given their optical correction, visual acuity does not significantly improve. The lack of improvement with spectacle correction often leads the examiner to seek an organic cause for the
decreased vision. The treatment of bilateral high hypermetropic
amblyopia is to prescribe full hypermetropic correction. In most
cases, visual acuity will slowly improve if the glasses are worn
full-time, with final visual acuity usually in the range of 20/30
to 20/25 achieved over a period of 6 months to a year.
Bilateral meridional amblyopia is caused by bilateral astigmatism and, like bilateral hypermetropic amblyopia, is secondary to pattern distortion. Significant meridional amblyopia
occurs with astigmatism greater than 2.50 D. To avoid meridional amblyopia, astigmatisms of 2.50 D or more should be
treated in preschool children, and astigmatisms over 3.00 D to
4.00 D should be treated in infants.
Amblyopic Vision
The visual deficit associated with amblyopia has certain unique
characteristics, including the crowding phenomenon, the
neutral density filter effect, and eccentric fixation. The crowding phenomenon relates to the fact that patients with amblyopia
have better visual acuity reading single optotype than reading
multiple optotypes in a row (linear optotypes). Often, patients
with amblyopia will perform 1 or 2 Snellen lines better when
presented with single optotypes versus linear optotypes. This
crowding phenomenon may have something to do with the
relatively large receptive field associated with amblyopia.
Crowding bars are often used around a single optotype to provide
a more sensitive test for amblyopia.
A neutral density filter reduces overall luminance without
inducing a color change. Decreased luminance of the visual
target results in diminished central acuity in normal eyes.
Decreased illumination of visual targets has less of an effect on
amblyopic eyes because they are not using central acuity. The
intraocular differences in visual acuity between the amblyopic
eye and the sound eye diminish when the patient looks through
a neutral density filter that lowers the luminance of the visual
target. For example, a patient with a left amblyopia has 20/20
vision in the right eye and 20/60 in the left eye under photopic
conditions (4 lines difference). He may have visual acuities of
20/50 right eye and 20/60 left eye under scotopic conditions
(1 line difference).
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A
B
FIGURE 4-5A,B. Eccentric fixation. (A) Sound eye fixes with the fovea
(left) and the amblyopic eye eccentrically fixates in an area of fixation
(right). (B) Right eye is covered, and eccentric fixation persists with
patient viewing in an eccentric area.
All amblyopes have some degree of extrafoveal fixation.
Mild amblyopes (20/40–20/100) fixate so close to the fovea that
they appear to fixate centrally. Severe amblyopes, usually 20/200
to count fingers, use a large parafoveal area for viewing (Fig. 45). This area of eccentric fixation is not a pinpoint location but
a general area of viewing.
The presence of eccentric fixation is a clinical sign of severe
amblyopia and has a poor visual prognosis. Remember that
anomalous retinal correspondence is quite different from eccentric fixation. Anomalous retinal correspondence (ARC) is a
binocular sensory adaptation to strabismus that allows acceptance of images on noncorresponding retinal points. ARC is only
active during binocular viewing and, when one eye is covered,
fixation reverts back to the true fovea. Eccentric fixation, on the
other hand, is dense amblyopia without foveal fixation and is
present under monocular or binocular conditions.
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DIAGNOSING AMBLYOPIA
Visual Acuity Testing
When evaluating for amblyopia, linear acuity is more desirable
than single optotype presentation because single optotype presentation underestimates the degree of amblyopia. Surround bars
have been used to create crowding in a single optotype and are
useful in children who get confused with the multiple optotypes
used in linear acuity testing. There are many ways to test visual
acuity in preschool children, including Allen picture figures,
LEA figures, HOTV, illiterate E game, and the recently developed Wright figures©. The Wright figures are composed of black
and white bars with a constant gap throughout the figure (Fig.
4-6). A recent study using the Wright figures on the Portal
Stimuli System (Haag-Streit) found that the Wright figures
tested two-point discrimination acuity, similar to Snellen
acuity. Another advantage of the Wright figures is that their
overall shape or footprint is similar for all figures, which prevents the child from determining the figure by the shape rather
than internal two-point discrimination. (Dr. Wright collaborated
with Gregg and Paul Podnar from Accommodata, Inc., Cleveland, OH, developers of the Portal System, to refine the figures
for use in this system and perform the study.) Visual acuity can
often be measured in children as young as 2 to 3 years of age
using preschool optotypes.
FIGURE 4-6. Wright figures consist of black and white bars with constant thickness and white gaps. The overall shape or footprint is similar
for all figures, which prevents the child from determining the figure by
the shape alone. The Wright figures correlate well with Snellen acuity.
© 2000 by Dr. Kenneth W. Wright.
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119
Fixation Testing for Amblyopia
Preverbal children can be tested for amblyopia by examining the
quality of monocular fixation or binocular fixation preference.
MONOCULAR FIXATION TESTING
Normally developed children more than 2 to 3 months of age
should show central fixation with accurate smooth pursuit and
saccadic refixation eye movements. Test for central fixation by
covering one of the patient’s eyes, then move a target slowly
back and forth in front of the child to observe the accuracy
of fixation. A child with central fixation looks directly at the
target, visually locks on the target, and accurately follows the
moving target. Infants often find the human face a much more
compelling target than toys or pictures, so try moving your head
side to side to evaluate the quality of fixation. Central fixation
indicates foveal vision usually in the range of 20/100 or better.
ECCENTRIC FIXATION
Eccentric fixation means the fovea is not fixating and the patient
is viewing from an extrafoveal part of the retina (Fig. 4-5).
Patients with eccentric fixation appear to be looking to the side,
not directly at the fixation target. They have poor smooth pursuits, so they do not accurately follow a moving target.
VISUSCOPE
One way to identify the eccentric fixation point in older cooperative children is to use a Visuscope, which is a type of direct
ophthalmoscope that projects a focused image onto the retina so
the examiner can see the image on the retina. First, the image
is projected onto the parafoveal retina, then the patient is asked
to look at the image. If the patient has central fixation, the
patient refixates to place the image precisely on the fovea.
However, with eccentric fixation, the patient will view with the
parafoveal retinal area and show a wandering, unsteady fixation
(see Fig. 4-5). The more peripheral the eccentric fixation, the
denser the amblyopia.
FIXATION PREFERENCE TESTING
Testing for fixation preference is useful in preverbal strabismic
children to identify amblyopia that might be missed by mono-
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cular fixation testing. It is based on the premise that strong fixation preference indicates amblyopia. If a patient with strabismus spontaneously alternates fixation, using one eye, then the
other, this indicates equal fixation preference and no amblyopia
(Fig. 4-7).
A
B
FIGURE 4-7A,B. Infant with congenital esotropia and alternating fixation. Alternating fixation indicates equal visual preference; no amblyopia.
(A) Patient is fixing with the left eye. (B) Patient has switched fixation to
the right eye.
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121
FIGURE 4-8. Measuring fixation preference. Patient has strong fixation
preference for the left (left figure) and amblyopia in the right eye.
Temporarily covering the left eye (center figure) forces fixation to the right
eye, but when the cover is removed, the patient refixates to the left eye
(right figure). This indicates strong fixation preference, i.e., amblyopia.
Patients with a fixation preference may have amblyopia.
The strength of fixation preference indicates if amblyopia is
present, with the weaker preference for one eye being the amblyopic eye. Fixation preference can be quantified by briefly covering the preferred eye to force fixation to the nonpreferred eye.
Remove the cover from the preferred eye, then observe how well
and how long the patient will maintain fixation with the nonpreferred eye before refixating back to the preferred eye. If fixation immediately goes back to the preferred eye after the cover
is removed, then this indicates strong fixation preference for
the preferred eye and amblyopia of the deviated eye (Fig. 4-8).
However, if the patient maintains fixation with the nonpreferred
eye through smooth pursuit, through a blink, or for at least 5 s,
there is mild fixation preference and no significant amblyopia
(vision within 2 Snellen lines difference) (Fig. 4-9). The ability
to maintain fixation with the nonpreferred eye while following
a moving target is a very reliable indicator of equal vision and
detects no significant amblyopia.
The reliability of fixation preference testing for diagnosing
amblyopia has been shown to be quite good in patients with
large-angle strabismus, more than 10 to 15 PD.62 Patients with
small-angle strabismus, however, will show strong fixation
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FIGURE 4-9. Patient prefers to fix with the left eye (left figure). Occluding left eye forces fixation to right eye (center figure), and when the
occluder is removed (right figure), the patient maintains fixation with the
nonpreferred eye, indicating no amblyopia.
preference in 50% to 70% of cases, even if the vision is equal to
within a 2 Snellen lines difference.63,64 This high overdiagnosis
rate in children with small-angle strabismus occurs because they
have monofixation syndrome. These patients have peripheral
fusion but suppress one fovea, so they show strong fixation preference even if vision is equal. The overdiagnosis of amblyopia
in patients with small-angle strabismus can be rectified by using
the vertical prism test, which disrupts peripheral fusion and
temporarily breaks down the monofixation syndrome.
VERTICAL PRISM TEST (INDUCED TROPIA TEST,
10 DIOPTER FIXATION TEST)
The vertical prism test is used in preverbal children with
straight eyes or small-angle strabismus to accurately diagnose
amblyopia.62,63 It is performed by placing a 10 to 15 PD prism
base-up or base-down in front of one eye, thereby inducing a vertical tropia (Fig. 4-10). With the induced vertical strabismus, fixation preference can be determined as shown in Figure 4-11. In
Figure 4-11A, a base-down prism is placed over the right eye.
The right eye is fixing because both eyes move up as the right
eye fixates through the prism. In Figure 4-11B, the prism is
placed over the left eye, but the patient still fixates with the
right eye, evidenced by the fact that both eyes are in primary
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123
position, ignoring the prism in front of the left eye. If the patient
can hold fixation with either eye through a blink or through
smooth pursuit eye movements, no significant amblyopia is
present. A strong fixation preference indicates amblyopia.
CROSS-FIXATION
Patients with a large-angle esotropia and tight medial rectus
muscles will have difficulty bringing the eyes to primary position, so the eyes stay adducted. These patients “cross-fixate.”
The right adducted eye fixes on objects in left gaze, and the left
adducted eye fixates on objects in right gaze. Cross-fixation has
been said to be a sign of equal vision, but cross-fixation does not
guarantee that a patient sees equally with each eye. The ability
to hold fixation past midline or to hold fixation through smooth
pursuit with either eye is a better criterion for equal vision.
LATENT NYSTAGMUS
Patients with strabismus often have latent nystagmus, which is
a horizontal jerk nystagmus that occurs or gets worse in both
eyes if one eye is occluded. Thus, covering one eye in a patient
with latent nystagmus will increase nystagmus and diminish
visual acuity. To evaluate monocular visual function, blur one
FIGURE 4-10. Vertical prism test of a patient fixing with the left eye
because of a right amblyopia. A vertical prism is placed in front of the
left eye and, because the left eye is fixing, the left eye elevates to pick up
the fixation. As per Hering’s law, both eyes will elevate if the left eye is
fixing.
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A
B
FIGURE 4-11A,B. (A) Vertical prism is placed in front of one eye to identify which eye is fixing, and therefore fixation preference can be determined. (A) One can identify that the right eye is fixing because the right
eye is in primary position and the patient is ignoring the vertical displaced
image in the left eye. (B) Patient is still fixing with the right eye. Both
eyes shift upward because the right eye is viewing through the prism.
This is a base-down prism, so the eyes move up.
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125
eye with a plus lens rather than occluding one eye. Blurring one
eye induces less nystagmus than occlusion. Use the minimum
amount of plus necessary to force fixation to the fellow eye. The
vertical prism test can identify which eye is fixing. Usually, a
5.00 D lens is sufficient to blur distance vision enough to force
fixation to the fellow eye. Linear presentation of optotypes is difficult for patients with nystagmus because the optotypes tend
to run together, so try a single optotype presentation. Also, take
a binocular visual acuity measurement in addition to a monocular acuity in patients with nystagmus because binocular vision
is usually better than monocular vision. To assess the best functional visual acuity potential in a patient with nystagmus, test
binocular vision while allowing the patient to adopt their preferred face turn or head tilt.
VISION SCREENING
Early detection and treatment of pediatric ocular disease is critical. Diseases such as congenital cataracts, retinoblastoma, and
congenital glaucoma require early treatment during infancy.
Delay in diagnosis may result in irreversible vision loss and, in
the case of retinoblastoma, even death. Patients with congenital cataracts treated during the first weeks of life have a relatively good prognosis, whereas surgery performed after 2 to 3
months of age is considered late and is associated with a poor
visual outcome. It is, therefore, imperative to perform effective
vision screening for all children from newborn infants to older
children.
Vision screening examinations should start at birth and continue as part of routine checkups for primary care physicians.
The acronym I-ARM (inspection—acuity, red reflex, and motility) can be a helpful reminder of the essential parts of a pediatric
screening examination. Table 4-4 summarizes the I-ARM
screening eye examination for neonates, babies, and children.
The most important test for the newborn is the red reflex test.
If an abnormal red reflex is present, then an immediate referral
to an ophthalmologist is required. Infant screening examinations
take less than a minute, but this brief exam is quite powerful.
If performed properly, it can detect the vast majority of eye
pathology, including the important diagnoses mentioned previously. Guidelines for visual acuity referral are presented in
Table 4-5.
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TABLE 4-4. Screening Eye Examination: I–ARM.
Neonate
(Birth–2 months)
Babies
(3 months–2 years)
Children
(3 years and older)
Symmetry Face
& eyes
Poor fixation
Pupillary response
Face turn or head tilt
Face turn or head tilt
Good fixation and
smooth pursuit
Red reflex
Red reflex test
Motility
Gross alignment
(70% small
exotropia but
esotropia probably
abnormal
Binocular red reflex
(Brückner)
Good alignment
Light reflex and
Brückner (esotropia
is abnormal after
2 months of age)
Visual acuity: Allen
cards, E-game,
Snellen acuity
Bilateral red reflex test
(Brückner)
Good alignment
Light reflex and
Brückner (any
misalignment is
abnormal)
Steps
Inspection
Acuity
Red Reflex
The red reflex test is the single best vision screening exam for
infants and young children. It is best performed using the Brückner modification, which is simply a simultaneous bilateral red
reflex. Use the direct ophthalmoscope and view the patient’s
eyes at a distance of approximately 2 feet from the patient. Use
a broad beam so that both eyes are illuminated at the same time.
Dim the room lights and have the child look directly into the
ophthalmoscope light. Start with the ophthalmoscope on low
illumination then slowly increase the illumination until a red
reflex is seen. You will observe a red reflex that fills the pupil
and a small (approximately 1 mm) white light reflex that appears
to reflect off the cornea (Fig. 4-12). The white light reflex is actually a reflex coming from just behind the pupil and is called
the “corneal light reflex” or the “Hirschberg reflex.” Thus, the
Brückner test gives both a red reflex and the corneal light reflex
simultaneously.
Blockage of the retinal image or large retinal pathology will
result in an abnormal red reflex. A cataract can either block the
TABLE 4-5. Abnormal Red Reflex: Symmetry Is the Key.
Cataract
Vitreous hemorrhage
Retinoblastoma
Anisometropia
Strabismus
May block the red reflex (dark or dull reflex) or may look
white (leukocoria)
Blocks red reflex (dark or dull reflex)
Appears as a yellow or white reflex (leukocoria)
Results in an unequal red reflex
Causes a brighter red reflex in the deviated eye; the
corneal light reflex will be decentered
chapter 4: visual development and amblyopia
127
FIGURE 4-12. Normal Brückner test with symmetrical red reflex and
centered corneal light reflex.
red reflex or reflect light to give a white reflex. Retinoblastoma
has a yellowish-white color and will produce a yellow reflex. Anisometropia (difference in refractive error) will result in an
unequal red reflex. Strabismus will cause a brighter red reflex in
the deviated eye, and the corneal light reflex will be decentered.
The key sign of a normal exam is symmetry. See Figure 4-13 and
Table 4-5 for examples of abnormal red reflexes.
AMBLYOPIA TREATMENT
Early treatment of amblyopia is critical for best visual acuity
results. The basic strategy for treating amblyopia is to first
provide a clear retinal image, and then correct ocular dominance if dominance is present, as early as possible during the
period of visual plasticity (birth to 8 years). Correction of ocular
dominance is accomplished by forcing fixation to the amblyopic
eye through patching or blurring the vision of the sound eye.
Clear Retinal Image
Patients with bilateral hypermetropia (5.00 D) should receive
the full hypermetropic correction, as amblyopic eyes do not fully
accommodate. Patients who are given partial correction of their
high hypermetropia often show very slow or no improvement
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 4-13A,B. Abnormal reflex. (A) Cataract: left eye.
sometropia: brighter reflex in right eye.
(B) Ani-
in their amblyopia. Patients with large astigmatism (2.50 D)
will also have amblyopia secondary to the astigmatism or
develop meridional amblyopia. Prescribe the full astigmatic correction to provide a clear retinal image. It is important to consider correcting astigmatisms of 2.50 to 3.00 or more in small
children, even if the astigmatism is bilateral. Table 4-6 lists
guidelines for prescribing spectacles in children. In general, if the
patient has anisometropic amblyopia and straight eyes, this
author initially prescribes just glasses and waits to start patch-
129
chapter 4: visual development and amblyopia
C
FIGURE 4-13C. (C) Strabismus: esotropia with brighter reflex from deviated left eye. (Note: This is the author’s youngest son. The author subsequently performed strabismus surgery on him, and the eyes have
remained straight.)
ing of the good eye. Most anisometropic amblyopes will respond
to glasses alone with no or minimal part-time occlusion of the
good eye.19
Children with media opacities, such as a visually significant
cataract, should have immediate surgery with visual rehabilitation using a contact lens or intraocular lens. Early treatment is
critical; infants with a congenital cataract should undergo surgery
within the first month of life, even as early as the first week.
TABLE 4-6. When Should Spectacles Be Prescribed in Children?
Type of refractive error
Hypermetropic anisometropia
Myopic anisometropia
Astigmatic anisometropia
Bilateral hypermetropia
Bilateral astigmatism
Threshold for prescribing spectacles
1.50
3.00
1.50
5.00
2.50
D
D
D
D
D
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handbook of pediatric strabismus and amblyopia
Correct Ocular Dominance
OCCLUSION
Patching or occlusion therapy is based on covering the sound
eye to stimulate the amblyopic eye. Strabismic patients without
binocular fusion can be treated with full-time occlusion;
however, full-time occlusion may result in reverse amblyopia in
children under 4 to 5 years of age. To prevent reverse amblyopia,
do not use full-time occlusion for more than 1 week per the
child’s age in years without reexamining the vision of the good
eye. For example, a 2-year-old child receiving full-time occlusion should be examined every 2 weeks. In children less than 1
year of age, part-time occlusion may be preferable to avoid
reverse amblyopia.
Amblyopic patients with essentially straight eyes (tropias
8 PD) and peripheral fusion (e.g., anisometropic amblyopia and
microtropia monofixators) are best treated with part-time patching (3 to 4 h/day) or no occlusion. For anisometropic amblyopia,
initially prescribe spectacle correction and follow the patient
each month for visual acuity improvement. If vision does not
improve on monthly follow-ups, then part-time patching is
started. Part-time occlusion or penalization therapy is preferred
because these methods help to preserve fusion. If vision does not
improve with part-time occlusion, then full-time occlusion
should be tried.
PENALIZATION
Penalization is a method for blurring the sound eye to force
fixation to the amblyopic eye. Penalization actually switches
ocular suppression, which can be demonstrated by a Polaroid
vectographic chart or by the Worth 4-dot test. Penalization only
works if fixation is switched from the sound eye to the amblyopic eye.59 Blurring of the sound eye can be achieved by various
methods. Optical penalization is based on over-plussing (prescribing more plus sphere than needed) the sound eye to force
fixation to the amblyopic eye for distance targets; the patient
will usually use the sound eye for near targets. Optical penalization works well for mild amblyopia; however, some children
will look over the tops of their glasses to use their sound eye.
Atropine penalization is a stronger form of penalization and is
useful even in dense amblyopia so long as the patient has significant hypermetropia of the good eye.38 Atropine at 0.5% or
chapter 4: visual development and amblyopia
131
1% is placed in the sound eye each day, optical correction is
removed from the sound eye, and the amblyopic eye is given full
optical correction. If the patient switches fixation to the amblyopic eye under these conditions of penalization, then penalization will improve vision.59
Cyclopentolate can be used as an in-office test to predict if
penalization will work.59 The in-office test consists of providing
the amblyopic eye with full optical correction while deadening
the sound eye with cyclopentolate and removing optical correction from the sound eye. If fixation switches to the amblyopic
eye under these conditions, then the patient will improve with
atropine penalization. Atropine penalization usually requires
3.00 or more hypermetropia in the sound eye to obtain significant blur to switch fixation. It is important to note that blurring the sound eye to a visual acuity lower than the amblyopic
eye does not guarantee a switch in fixation to the amblyopic eye.
Penalization in young children may result in reverse amblyopia
(decrease vision in the previously good eye), so patients 4 years
of age or younger should be followed closely when undergoing
atropine penalization therapy.50,59
OCCLUSIVE CONTACT LENS
Occlusive contact lens can be used in treating amblyopia. A
study by Eustis and Chamberlain15 showed 92% of patients
improved at least 1 line of Snellen acuity, but complications
limited the usefulness. Complications included conjunctival
irritation and poor contact lens fit, and one patient even learned
to decenter the lens to peek around the occlusive contact lens.
There was a high recurrence to pretreatment visual acuity, as
55% showed recurrence of amblyopia. The authors concluded
that occlusive contact lenses should only be considered as a last
resort and that these patients require close follow-up.15
BILATERAL LIGHT OCCLUSION
A preventive treatment of amblyopia may be the use of bilateral
light occlusion. Studies on dark-rearing have shown that bilateral total light occlusion prolongs the sensitive period of visual
development. In several animal studies, researchers have shown
that animals placed in total darkness for several months (or the
human equivalent to several years) do not develop dense amblyopia and their visual development is minimally affected.9,10,11,40
A study by Hoyt22 on neonates with hyperbilirubinemia treated
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handbook of pediatric strabismus and amblyopia
under bili-lights who were patched bilaterally from several days
to 2 weeks showed that they did not have an increased incidence
of amblyopia or strabismus. In a separate report by the author,61
a neonate received 17 days of bilateral patching after having 2
weeks of dense vitreous hemorrhage and hyphema. Follow-up at
3 years of age showed visual acuity of 20/30 in each eye and a
small accommodative esophoria with good fusion. Bilateral light
occlusion remains controversial and, in this author’s opinion,
should be used only as a temporary measure in neonates 3
months or younger with ocular opacities such as congenital
cataracts. Urgent surgery is still required but, for visually significant cataracts, bilateral occlusion can be used to prevent
amblyopia until the retinal image is cleared. The author’s
recommendation is to limit bilateral patching to a maximum of
2 weeks.
LEVODOPA/CARBIDOPA IN THE
OF AMBLYOPIA
TREATMENT
Levodopa/carbidopa has been traditionally used to treat Parkinson’s disease. Levodopa is a precursor for the catecholamine
dopamine, a neurotransmitter/neuromodulator known to influence receptive fields. Levodopa/carbidopa has been studied as an
adjunct to patching for the treatment of amblyopia.27,28,29,30 The
treatment remains controversial, as the visual acuity improvement has been relatively small, not clearly better than with
patching alone, and there are questions regarding long-term
stability of vision.
PLEOPTICS
Pleoptics is a method of treating eccentric fixation associated
with dense amblyopia. A bright ring of light is flashed around
the fovea to temporarily “blind” or saturate the photoreceptors
surrounding the fovea, which eliminates vision from the eccentric fixation point and forces fixation to the fovea. Pleoptic treatments are given several times a week to enhance occlusion
therapy. Most practitioners have found pleoptics to be no better
than standard occlusion therapy.16
ACTIVE STIMULATION
Some investigators have suggested active stimulation of the
amblyopic eye as a way to improve vision in the amblyopic eye.
chapter 4: visual development and amblyopia
133
A high-contrast spinning disc with square-wave grading was one
method that has been tried (CAM). The CAM treatment has
been found to be no better than standard occlusion therapy.8
PROGNOSIS OF AMBLYOPIA
The prognosis for amblyopia depends upon the age of the patient,
severity of amblyopia, and type of amblyopia. The earlier the
amblyopia occurs and the longer it remains untreated, the worse
the prognosis. In general, bilateral amblyopia responds better
than unilateral amblyopia, and myopic anisometropic amblyopia responds better than hypermetropic anisometropic amblyopia. Each case must be evaluated individually as to whether the
child is too old to undergo amblyopia therapy. Visual acuity
improvement has been documented when children are treated
in late childhood after 8 years of age.6,33 This author reported
improvement in vision from legally blind to 20/70 and damping
of sensory nystagmus in a 14-year-old who underwent late
cataract surgery for bilateral congenital cataracts.60 Even adults
with dense amblyopia can show visual acuity improvement and
prolonged plasticity. Significant visual acuity improvement of
the amblyopic eye has been reported in adults who have lost
vision in their good eye and relied on the amblyopic eye for their
vision.14,45
References
1. Atkinson J. Development of optokinetic nystagmus in the human
infant and monkey infant: an analogue to development in kittens.
In: Freeman RD (ed) Developmental neurobiology of vision. New
York: Plenum Press, 1979.
2. Birch EE, Gwiazda J, Held R. Stereoacuity development of crossed
and uncrossed disparities in human infants. Vision Res 1982;22:507.
3. Birch E, Petrig B. FPL and VEP measures of fusion, stereopsis and
stereoacuity in normal infants. Vision Res 1996;36(9):1321–1327.
4. Braddick O, et al. Cortical binocularity in infants. Nature (Lond)
1980;288:363–365.
5. Braddick O, Wattam-Bell J. The onset of binocular function in human
infants. Hum Neurobiol 1983;2(2):65–69.
6. Brown MH, Edelman PM. Conventional occlusion in the older
amblyope. Am Orthopt J 1976;26:54–56.
7. Carney T. Evidence for an early motion system which integrates
information from the two eyes. Vision Res 1997;37(17):2361–2368.
134
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8. Crandall MA, Gerhard WC, Ellerhorst B. CAM (stripe) therapy for
amblyopia, Perspect Ophthalmol 1981;5(1):51–55.
9. Cynader M, Berman N, Hein A. Recovery of function in cat visual
cortex following prolonged deprivation. Exp Brain Res 1976:25:139–
156.
10. Cynader M, Mitchell DE. Prolonged sensitivity to monocular
deprivation in dark-reared cats. J Neurophysiol 1980;43:1026–
1040.
11. Cynader M. Prolonged sensitivity to monocular deprivation in darkreared cats: effects of age and visual exposure. Dev Brain Res 1983;
8:155–164.
12. Demer JL, von Noorden GK. Optokinetic asymmetry in esotropia.
J Pediatr Ophthalmol Strabismus 1988;25:286.
13. Daw N. Critical periods and amblyopia. Arch Ophthalmol 1998;
116(4):502–505.
14. Ellis FD, Schlaegel TF. Unexpected visual recovery: organic amblyopia? Am Orthopt J 1991;31:7.
15. Eustis HS, Chamberlain D. Treatment for amblyopia: results using
occlusive contact lens. J Pediatr Ophthalmol Strabismus 1996;33:
319–322.
16. Fletcher MC, Silverman SJ, Boyd J, Callaway M. Biostatistical
studies: comparison of the management of amblyopia by conventional patching, intensive hospital pleoptics, and intermittent office
pleoptics. Am Orthopt J 1969;19:40.
17. Fox R, Aslin RN, Shea SL, Dumais ST. Stereopsis in human infants.
Science 1980;207:323.
18. Garey LJ, De Courten C. Structural development of the lateral geniculate nucleus and visual cortex in monkey and man. Behav Brain Res
1983;10:3–13.
19. Hakim OH, Wright KW. Treatment of anisometropic amblyopia with
minimal or no patching. Abstracts Program #2148. ARVO, May/Ft.
Lauderdale, FL. 2001.
20. Hendrickson AE, Movshon JA, Eggers HM, Gizzi MS, Boothe
RG, Kiorpes L. Effects of early unilateral blur on the macaque’s
visual system. II. Anatomical observations. J Neurosci 1987;7:1327–
1339.
21. Horton JC, Hocking DR. Timing of the critical period for plasticity
of ocular dominance columns in macaque striate cortex. J Neurosci
1997;17(10):3684–3709.
22. Hoyt CS. The long-term visual effects of short-term binocular occlusion of at-risk neonates. Arch Ophthalmol 1980;98:1970.
23. Hubel KH, Weisel TN. Receptive field, binocular interaction and
functional architecture in the cat’s visual cortex. J Physiol 1962;160:
106–154.
24. Ikeda H, Tremain K. Amblyopia and cortical binocularity. Trans
Ophthalmol Soc UK 1980;100:452.
25. Keech RV, Kutschke PJ. Upper age limit for the development of
amblyopia. J Pediatr Ophthalmol Strabismus 1995;32:89–93.
chapter 4: visual development and amblyopia
135
26. Leguire LE, Rogers GL, Bremer DL. Visual-evoked response binocular summation in normal and strabismic infants. Investig Ophthalmol Vis Sci 1991;32:126–133.
27. Leguire LE, Rogers GL, Bremer DL, Walson P, HadjiconstantinouNeff M. Levodopa and childhood amblyopia. J Pediatr Ophthalmol
Strabismus 1992:29:290–298.
28. Leguire LE, Rogers GL, Bremer DL, Walson P, McGregor ML. Levodopa/carbidopa for childhood amblyopia. Investig Ophthalmol Vis
Sci 1993;34:3090–3095.
29. Leguire LE, Rogers GL, Bremer DL, Walson P, McGregor ML. Longitudinal study of levodopa/carbidopa for childhood ambylopia. J
Pediatr Ophthalmol Strabismus 1993;30:354–360.
30. Leguire LE, Rogers GL, Bremer DL, Walson P, McGregor ML. Levodopa/carbidopa treatment for the amblyopia in older children. J
Pediatr Ophthalmol Strabismus 1995;32:143–151.
31. Lewis TL, Maurer D, Brent HP. Optokinetic nystagmus in normal
and visually deprived children: implications for cortical development. Can J Psychol 1989;43:121–140.
32. Naegele JR, Held R. The postnatal development of monocular optokinetic nystagmus in infants. Vision Res 1982;22:341.
33. Oliver M, et al. Compliance and results of treatment for amblyopia
in children more than 8 years old. Am J Ophthalmol 1986;102:340–
345.
34. Ottar WL, Scott WE, Holgado SI. Photoscreening for amblyogenic
factors. J Pediatr Ophthalmol Strabismus 1995;32:289–295.
35. Parks MM. The monofixational syndrome. Trans Am Ophthalmol
Soc 1969;67:609–657.
36. Raab E. Refractive amblyopia. Int Ophthalmol Clin 1971;II:155.
37. Rakic P. Prenatal genesis of connections subserving ocular dominance in rhesus monkey. Nature (Lond) 1976;261:467.
38. Repka MX, Ray JM. The efficacy of optical and pharmacological
penalization. Ophthalmology 1993;100:769–775.
39. Sondhi N, Archer SM, Helveston EM. Development of normal ocular
alignment. J Pediatr Ophthalmol Strabismus 1988;25:210–211.
40. Timney B, Mitchell DE, Giffin F. The development of vision in cats
after extended periods of dark-rearing. Exp Brain Res 1978;31:
547–560.
41. Tychsen L, Lisberger SG. Maldevelopment of visual motion procession in humans who had strabismus with onset in infancy. J Neurosci 1986;6:2495–2508.
42. Tychsen L. Binocular vision. In: Hart WM (ed) Adler’s physiology of
the eye: clinical applications, 9th edn. St. Louis: Mosby, 1992:773–
853.
43. Tychsen L, Boothe RG. Latent fixation nystagmus and nasotemporal
asymmetries of motion visually evoked potentials in naturally strabismic primate. J Pediatr Ophthalmol Strabismus 1996;33:148–152.
44. van Essen DC, Maunsell JHR. Hierarchical organization and functional streams in the visual cortex. Trends Neurosci 1983:6:370–395.
136
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45. Vereecken EP, Brabant P. Prognosis for vision in amblyopia after the
loss of the good eye. Arch Ophthalmol 1984;102:220.
46. von Noorden GK, Crawford ML. The lateral geniculate nucleus in
human strabismic amblyopia. Investig Ophthalmol Vis Sci 1992;
33(9):2729–2732.
47. von Noorden GK, Crawford MLJ, Levacy RA. The lateral geniculate
nucleus in human anisometropic amblyopia. Investig Ophthalmol
Vis Sci 1983;24:788–790.
48. von Noorden GK, Crawford MLJ. The effects of total unilateral occlusion vs. lid suture on the visual system of infant monkeys. Investig
Ophthalmol Vis Sci 1981;21:142–146.
49. von Noorden GK, Crawford MLJ. Form vision deprivation without
light deprivation produces the visual deprivation syndrome in
Macaca mulatta. Brain Res 1977;129:37–44.
50. von Noorden GK. Amblyopia caused by unilateral atropinization.
Ophthalmology 1981;88:131–133.
51. Weakley DR. The association between anisometropia, amblyopia
and binocularity in the absence of strabismus. Trans Am Ophthalmol Soc 1999;48:987–1021.
52. Weinacht S, Kind C, Monting JS, Gottlob I. Visual development in
preterm and full term infants: a prospective masked study. Investig
Ophthalmol Vis Sci 1999;40(2):346–353.
53. Werner DB, Scott WE. Amblyopia case reports: bilateral hypermetropic ametropic amblyopia. J Pediatr Ophthalmol Strabismus 1985;
22:203–205.
54. Westall CA, Woodhouse JM, Brown VA. OKN asymmetries and
binocular function in amblyopia. Ophthalmol Physiol Opt 1989;9:
269–276.
55. Westall CA, Eizenman M, Kraft SP, Panton CM, Chatterjee S.
Cortical binocularity and monocular optokinetic asymmetry in
early onset esotropia. Investig Ophthalmol Vis Sci 1998;39(8):1352–
1360.
56. Wiesel TN, Hubel DH. Single-cell responses in striate cortex of
kittens deprived of vision in one eye. J Neurophysiol 1963;26:1003–
1017.
57. Wiesel TN, Hubel DH. Ordered arrangement of orientation columns
in monkeys lacking visual experience. J Comp Neurol 1974;158:
307.
58. Wright KW, Fox BES, Erikson KJ. PVEP evidence of true suppression
in adult onset strabismus. J Pediatric Ophthalmol Strabismus 1990;
27:196–201.
59. Wright KW, Guyton DL. A test for predicting the effectiveness of
penalization on amblyopia. In: Henkind P (ed) Acta: XXIV international congress of ophthalmology. Philadelphia: Lippincott, 1983:
896–901.
60. Wright KW, Christensen LE, Noguchi BA. Results of late surgery for
presumed congenital cataracts. Am J Ophthalmol 1992;114(4):409–
415.
chapter 4: visual development and amblyopia
137
61. Wright KW, Wehrle MJ, Urrea PT. Bilateral total occlusion during the
critical period of visual development. Letter to the editor. Arch Ophthalmol 1987;105:321.
62. Wright KW, et al. Reliability of fixation preference testing in diagnosing amblyopia. Arch Ophthalmol 1986;104:549–553.
63. Wright KW, Walonker F, Edelman P. 10-diopter fixation test for
amblyopia. Arch Ophthalmol 1981;99:1242–1246.
64. Zipf RF. Binocular fixation pattern. Arch Ophthalmol 1976;94:401–
405.
5
The Ocular Motor
Examination
Kenneth W. Wright
EVALUATION OF THE STRABISMIC
PATIENT
The goals of the strabismus examination are to (1) diagnose
amblyopia; (2) establish a strabismus diagnosis (e.g., pseudoesotropia, congenital esotropia, cranial nerve palsy, or restrictive strabismus); (3) assess the binocular status (e.g., bifoveal
fusion, monofixation–peripheral fusion, anomalous retinal correspondence, no fusion–large suppression, diplopia, and fusion
potential); and (4) measure and characterize the deviation. A
well-focused, goal-oriented evaluation helps prevent a laborious
exhaustive examination that results in patient fatigue, examiner
fatigue, and the collection of spurious data. Even after a full evaluation, a patient’s strabismus may not clearly fall into a specific
category, and the diagnosis may be nebulous. In these cases, the
patient can still be appropriately managed if evaluated for
amblyopia, sensory status, size of the deviation, and the possibility of an underlying neurological problem or systemic disease.
As in all aspects of medicine, the combination of detailed history
and careful physical examination provides the foundation for
making the correct diagnosis and taking the appropriate action.
HISTORY
The character and onset of the strabismus provides information
about binocular fusion potential. The earlier the onset and
longer the duration of the strabismus, the worse the prognosis
for binocular vision. Older children with congenital strabismus
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chapter 5: the ocular motor examination
139
who have never experienced fusion have a poor fusion prognosis, whereas an acquired strabismus of a few months duration
usually indicates the patient has developed at least some binocular vision and has the potential to recover binocular fusion. A
history of compensatory head posturing speaks for binocular
fusion, as does a history of an intermittent strabismus. In the
real world of clinical practice, however, these general rules do
not hold 100% of the time as some patients will obtain binocular fusion after late surgery for a presumed congenital strabismus. The history of an acquired strabismus is important because
it may indicate a neurological or systemic disease, especially
when the strabismus is incomitant and associated with limited
ductions. An unexplained acquired incomitant strabismus requires neurological evaluation. Examining baby photographs,
the family album, or a patient’s driver’s license under magnification can facilitate documenting the onset and type of strabismus. Additionally, patients should be questioned about the
presence of diplopia, as diplopia usually indicates acquired strabismus with onset usually after 4 to 6 years of age.
History regarding birth weight, complications of birth, the
health of the child, and developmental milestones are also an
integral part of a complete evaluation. Finally, the family history
is very important. Although the exact hereditary pattern of strabismus is unclear, most types of strabismus are familial.
PHYSICAL EXAMINATION
Try to obtain as much information as possible by inspection
without touching the child. Use toys to play with the child to
observe eye alignment and eye movements. Save the more intrusive parts of the examination for last. The steps for the strabismic examination are listed in order in Table 5-1. Traditionally,
binocular sensory testing is performed before tests that require
occluding one eye, such as visual acuity testing and the cover/
uncover tests. Covering one eye dissociates the eyes and may
disrupt fusion in a patient with latent strabismus (large phoria
or intermittent tropia). This may be more of a theoretical consideration, as Biedner et al.2 found no significant difference in
stereopsis tested at the beginning versus at the end of the exam.
This author prefers testing vision early, before sensory testing,
as knowledge of the visual acuity sets the tone for the rest of
the examination.
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handbook of pediatric strabismus and amblyopia
TABLE 5-1. Order of Examination.
1.
2.
3.
4.
5.
6.
7.
8.
Inspection: Evaluation and measurement of face turns
Amblyopia assessment/visual acuity
Sensory tests (see Chapter 6)
Ductions and versions
Measurement of deviation
Special tests for identifying restriction and paresis
Cycloplegic refraction
Fundus examination (objective torsion)
ORDER OF EXAMINATION
Inspection
The physical examination actually starts as the patient enters
the room. While taking the history, it is important to observe
the patient’s visual behavior, eye alignment, eye movements,
fixation, and head posturing. By the time the history is recorded,
a good observer will often have established a preliminary differential diagnosis. An initial differential diagnosis helps guide the
direction of the physical examination and minimize extraneous
test. However, be careful not to overanticipate: keep an open
mind.
Much can be learned about the patient’s sensory status from
simple inspection. Do the eyes appear straight? Is there a face
turn or head posturing? The presence of straight eyes with a face
turn in a patient with strabismus can indicate the presence of
binocular fusion even if this cannot be demonstrated by sensory
testing. Often, patients with weak fusion will break down to a
tropia after even a brief cover test or during sensory tests. Therefore, it is important to observe the patient’s alignment and face
posturing before formal testing.
Amblyopia Assessment/Visual Acuity
Techniques for diagnosing amblyopia are covered in Chapter 4.
Always try to document visual function even in neonates or
developmentally delayed children who are unable to cooperate
with standard testing. Preverbal children can be tested for
amblyopia by examining the quality of monocular fixation or
binocular fixation preference. When evaluating amblyopia in
older cooperative children, use linear acuity because single opto-
chapter 5: the ocular motor examination
141
type presentation lacks crowding and slightly underestimates
the degree of amblyopia. In young preliterate children, however,
single optotype testing is quicker, easier, and probably more
accurate than linear optotypes. Crowding bars around an optotype or using the Wright figures have inherent crowding and may
be useful for diagnosing amblyopia with single optotypes. There
are many ways to test visual acuity in preschool children including Wright figures, Allen picture cards, HOTV, and the illiterate
E game.
Sensory Tests
A description of sensory tests is provided in Chapter 6. Evaluation of the sensory status should be part of every strabismus
examination and usually includes a haploscopic fusion/suppression test (e.g., Worth 4-dot test) and a test for stereoacuity (e.g.,
Titmus).
Ductions and Versions
Ductions test monocular movements and are examined with
one eye occluded, forcing fixation to the eye being examined.
Ductions evaluate the ability for the eye to move into extreme
fields of gaze. Figure 5-1 shows both normal and limited abduction; this is a scale of 0 to 4, with 1 limitation meaning slight
limitation and 4 indicating severe limitation with inability of
the eye to move past midline. This scale can be used to measure
horizontal and vertical ductions.
Versions test binocular eye movements and show how well
the eyes move together in synchrony. Versions will detect subtle
imbalance of eye movements and oblique muscle dysfunction
missed on ductions. Evaluation of versions should include eye
movements through the nine cardinal positions of gaze: from
primary position to straight right, straight left, straight up,
straight down, up to the right, up to the left, down to the right,
and down to the left (Fig. 5-2). Abnormal versions can be noted
on a scale of 4 to 4 with 0 indicating normal and 4 indicating maximum overaction (Fig. 5-3A), whereas 4 indicates
severe underaction (Fig. 5-3B). It is important to remember,
when observing for oblique dysfunction, to make sure the
abducting eye is fixing so the adducting eye is free to manifest
the oblique dysfunction; this can be accomplished by partially
occluding the adducting eye (with your thumb or occluder) and
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handbook of pediatric strabismus and amblyopia
A
B
C
D
E
FIGURE 5-1A–E. Ductions are monocular eye movements: (A) normal
abduction; (B) 1 limitation to abduction; (C) 2 limitation to abduction; (D) 3 limitation to abduction; (E) 4 limitation to abduction. This
scheme is used to quantitate limitation of duction movements and can
be used for abduction or vertical ductions as well.
FIGURE 5-2. Versions are binocular eye movements: dextroversion,
rightgaze; levoversion, leftgaze; superversion, upgaze; infraversion,
downgaze.
chapter 5: the ocular motor examination
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A
B
FIGURE 5-3A,B. (A) Versions showing overaction of the oblique muscles:
upper drawing, right inferior oblique overaction 3; lower drawing, right
superior oblique overaction 3. (B) Versions showing underaction of the
oblique muscles: upper drawing, 3 underaction of the right inferior
oblique; lower drawing, 3 underaction of the right superior oblique.
looking around the occluder to see if the eye manifests the
oblique dysfunction (Fig. 5-4).
Measuring Ocular Deviation
The methods for measuring the angle of strabismus have been
divided into the following categories: light reflex tests, cover
tests, and subjective tests. Light reflex tests are the easiest to
perform on young children and infants. These tests, however,
are not as precise as other tests such as the cover tests. The
Lancaster red-green test is useful in adult patients with diplopia
and an incomitant deviation.
Most methods for measuring ocular deviations involve
prisms. There is a basic discussion on the use of prisms in stra-
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FIGURE 5-4. Versions showing an occluder is placed in front of the right
eye to ensure that the patient fixates with the left eye. When patient is
fixing left eye, it allows the inferior oblique overaction to become obvious
and manifest. If the patient were to fix with the right eye, however, one
would not see a downshoot because of Hering’s law.
bismus in Chapter 3. For prism neutralization of a deviation,
remember to orient the prism so the apex points in the same
direction as the deviated eye. Esotropia is corrected with a baseout prism, exotropia with a base-in prism, and hypertropia by a
base-down prism.
When measuring a deviation, it is critical that the patient is
fixating and appropriately accommodating on the fixation target.
Accurate measurements cannot be obtained if the patient is
gazing around the room or daydreaming and not accommodating on the fixation target. An accommodative target is a target
that has fine detail that requires accurate accommodation to be
seen. A penlight, for example, is a poor accommodative target
as there is no fine detail and accommodation is not required to
see the light. One of the best accommodative targets for adults,
in the distance or near, is Snellen letters at a size close to visual
threshold. By having the patient read the letters, the examiner
knows that the patient is accommodating on the fixation target.
For young children, small detailed toys or small pictures with
fine detail can be used at near and a children’s video or animated
toys in the distance.
LIGHT REFLEX TESTS
HIRSCHBERG TEST
The Hirschberg test, or corneal light reflex test, assesses eye
alignment by the noting the location of the corneal light reflex
within the pupil. The term corneal light reflex is a misnomer,
as it is not a reflex off the cornea. What we perceive as the light
reflex is actually the first Purkinje image, which is a virtual
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145
image located behind the pupil. The Hirschberg test should be
performed by holding a light source (muscle light or penlight) in
front of the examiner’s eye and directing the light into the
patient’s eyes. Have the patient look at the light, then assess the
location of the light reflex in each eye. Hirschberg testing is only
valid if the patient fixes on the light source. The examiner must
view the light reflexes from a position directly behind the light
source. Therefore, for practical purposes, the Hirschberg test can
only be performed at near. An accommodative fixation target
can be placed next to the light source to attract the patient’s
attention and provide an accommodative target.
With normal orthotropic alignment, the light reflexes are
slightly decentered nasally, but they are symmetrically located
within each pupil. Slight symmetrical nasal displacement of
approximately 5° is normal and is a “physiological” positive
angle kappa (see Angle Kappa, below). Patients with strabismus
will have an eccentric light reflex in the deviated eye. Temporal displacement of the light reflex indicates esotropia, nasal
displacement indicates exotropia, and inferior displacement
indicates hypertropia (Fig. 5-5). One can estimate the size of an
ocular deviation by the amount of light reflex displacement
within the pupil. Temporal displacement of the light reflex to
the pupillary margin indicates an esotropia of 15° (ET 30 PD),
displacement to the temporal midiris indicates esotropia 30° (ET
60 PD), and temporal displacement to the limbus indicates an
esotropia of 40° (ET 80 PD). Another way to estimate the angle
of deviation is to multiply the millimeters of light displacement
by 15 PD to give the deviation in prism diopters.3,6,7 Thus, 2 mm
of nasal displacement of the reflex from its normal location
when viewing monocularly indicates an exotropia of 30 PD.
These are relatively gross estimates and, as a rule, are not used
to determine the amount of surgery.
ANGLE KAPPA
Angle kappa measures the angle between the line of sight and
the corneal–pupillary axis. The line of sight is a line from the
fixation target to the fovea, and the corneal–pupillary axis is a
line from the center of the pupil that is tangential to the cornea.
Angle kappa is a monocular measurement of monocular alignment to a visual target. Angle kappa does not have any relationship to the fellow eye and does not measure strabismus. If
the fovea is located directly behind the pupil, then the line of
sight would be in line with the corneal–pupillary axis and the
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FIGURE 5-5. Hirschberg test: top drawing, normally centered reflex;
second drawing, esotropia, right eye, with the light reflex deviated temporally; third drawing, exotropia, right eye, with the light reflex deviated
nasally; bottom drawing, right hypertropia, with the light reflex deviated
inferiorly.
angle kappa would be 0°. On the other hand, a fovea located off
center (not directly behind the cornea) creates a discrepancy
between the line of sight and the corneal–pupillary axis, resulting in an angle kappa (Fig. 5-6). A positive angle kappa is associated with a temporally displaced fovea (Fig. 5-6A). With the
fovea displaced temporally, the eye must abduct to put the
image on the fovea, which causes a nasal displacement of the
Hirschberg light reflex and gives an exo-appearance. Figure 5-7A
shows a patient with a positive angle kappa, left eye, caused by
a dragged left macula secondary to retinopathy of prematurity.
This patient appears to have an exotropia but is actually
orthotropic. When the left eye is covered, the right eye remains
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147
abducted, as this is the position necessary to view the target (Fig.
5-7B). Remember, angle kappa relates to the eye position during
monocular viewing and is associated with central fixation by an
ectopic fovea. Note that patients with a positive angle kappa and
esotropia look as if the eyes are straight. A positive angle kappa
can occur congenitally or, if the fovea is dragged temporally, by
retinal fibrosis occurring with diseases such as retinopathy of
prematurity or a temporal retinal scar from Toxocara canis. A
negative angle kappa is caused by nasal displacement of the
fovea toward the optic nerve (see Fig. 5-6B); this results in a
turning in of the eye, a temporal shift of the Hirschberg light
reflex, and an eso-appearance. Nasal macular displacement
can be secondary to a retinal scar located between the fovea
and optic nerve or can occur congenitally without a specific
etiology.
A
B
FIGURE 5-6A,B. (A) Positive angle kappa. The eye turns out to pick up
fixation under monocular viewing conditions as the fovea (F) is displaced
temporally. Note that the line of sight differs from the corneal pupillary
axis. (B) Negative angle kappa. The eye deviates nasally to pick up fixation as the fovea is displaced nasally, close to the optic nerve. Again, the
line of sight is not parallel with the corneal pupillary axis.
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A
B
FIGURE 5-7A,B. Clinical photograph of a patient with retinopathy of
prematurity. Both foveas are dragged temporally. (A) The patient appears
exotropic and both eyes are exotropic, unlike true exotropia where the
fixing eye is straight and the nonfixing fellow eye is deviated. This patient
has a positive angle kappa and is actually fusing with both eyes deviated
temporally to align the foveas. (B) There is no ocular shift when the left
eye is covered: no exotropia.
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Most normal patients have a physiological positive angle
kappa, as the fovea is located 5° temporal to the center of the
posterior pole; this is why we usually see the Hirschberg light
reflex as being slightly decentered nasally in orthotropic
patients. An angle kappa can be distinguished from a tropia by
the cover/uncover test (see following). If the light reflex is displaced from the center of the pupil with monocular viewing, this
indicates an abnormal angle kappa, not strabismus (Fig. 5-7B).
KRIMSKY TEST
The Krimsky test adds use of a prism to the Hirschberg test to
measure a strabismus. This test is indicated to estimate the deviation size in uncooperative patients and patients with sensory
strabismus and poor vision of 20/400 or worse. A prism is placed
in front of one eye, with the base oriented appropriately
(esotropia, base-out; exotropia, base-in; hypertropia, base-down)
to neutralize the deviation. A penlight is then shone into both
eyes as described for the Hirschberg test. The patient is directed
to fixate on an accommodative target juxtaposed to the penlight.
The prism is increased or decreased until the reflex from each
eye becomes equally and symmetrically centered in the pupil.
Placing a prism over the fixing eye in a patient with a tropia will
cause a version movement in which both eyes move in the direction of the apex of the prism, which moves the light reflex in
the deviated eye (Fig. 5-8). Placing the prism over the nonfixing
eye directly moves the light reflex to the center of the pupil
without a version shift. One can place the prism over either eye,
except in cases of a restriction or paresis. In these patients,
measure the primary deviation by placing the prism over the eye
with limited rotations and mesure the secondary deviation by
placing the prism over the eye with full ductions (see primary
versus secondary deviation, following).
BRÜCKNER REFLEX TEST
The Brückner reflex test is performed by using the direct ophthalmoscope to obtain a red reflex from both eyes simultaneously. Make sure that the patient is looking at the light during
the Brückner test; if the patient looks to peripheral targets, the
test is invalid. In patients with strabismus, the Brückner test
will show asymmetrical reflexes with a brighter reflex coming
from the deviated eye. There is less pigment in the peripheral
retina, so the deviated eye will reflect more light. This is a
screening test that identifies strabismus and pathology that
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A
B
FIGURE 5-8A,B. The Krimsky test in a patient with esotropia. (A) The
light reflex is deviated temporally in the esotropic left eye. (B) A base-out
prism is presented in front of the right eye, which is fixing. The patient
continues to fixate with the right eye, but the right eye turns in to pick
up fixation. The left eye, because of Hering’s law, moves temporally. The
left eye is now centered and the right eye is turned in; however, the light
reflex would be centered in both eyes; this is the neutralization point, and
the amount of prism needed to achieve the neutralization point measures
the angle of deviation.
change the normal red reflex including anisometropia, gross
retinal pathology, large retinal detachment, and corneal, lenticular, or vitreous opacities (see Chapter 4; Figs. 4-13, 4-14).
COVER TESTS
COVER/UNCOVER TEST
The cover/uncover test is designed to detect the presence of a
tropia in patients who appear to have straight eyes and may be
fusing. The idea is to test for a tropia without dissociating an
existing phoria. Cover/uncover testing is performed by very
briefly covering the eye that is thought to be the fixing eye while
observing the eye suspected of deviating for a tropia shifts as
the eye picks up fixation. If there is no shift, then perform
cover/uncover testing on the opposite eye. If there is no shift of
either eye after covering and uncovering each eye, then there is
no manifest tropia and the eyes are straight, that is, orthotropia.
If briefly covering one eye produces a refixation shift of the
fellow eye, then a manifest tropia is present. A nasal to tempo-
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151
ral refixation movement indicates an esotropia, a temporal to
nasal shift indicates an exotropia, and a downward shift indicates a hypertropia (Fig. 5-9).
Be sure to have the patient fixate on an accommodative
target during testing, as the test is invalid if fixation is uncontrolled and wandering. Cover the fixing eye for 1 to 2 s, just long
enough to see if there is a shift of the uncovered eye to midline.
The cover/uncover test can be dissociating and can manifest an
underlying phoria if the test is performed improperly by covering one eye for several seconds. Prolonged occlusion of one eye
will break up fusion, and the patient will manifest a phoria that
may erroneously be called a tropia because it is associated with
the cover test. Remember to briefly cover one eye for only 1 or
A
B
C
FIGURE 5-9A–C. Cover/uncover test. (A) Esotropia. Left eye is fixing.
When the left eye is covered, the right eye moves out to pick up fixation.
This outward movement indicates that the right eye is esotropic. (B)
Exotropia. Left eye is fixing. When the left eye is covered, the right eye
turns in to pick up fixation. The inward movement indicates that the
right eye is exotropic. (C) Right hypertropia. Left eye is fixing. Covering
the left eye causes the right eye to come down to pick up fixation. Movement of the right eye indicates a right hypertropia.
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2 s, and to remove the cover for several seconds before covering
the fellow eye to allow for reestablishment of fusion. A properly
performed cover/uncover test will only identify the tropia
without disclosing an underlying phoria. A phoria is detected by
alternate cover testing (see discussion that follows).
ALTERNATE COVER TESTING
The alternate cover test is used to dissociate binocular fusion to
determine the full deviation, including both tropia and phoria.
The test is performed by alternately occluding each eye, then
observing for a refixation shift of the uncovered eye to midline.
It is important to hold the occluder over one eye for several
seconds to dissociate fusion, then rapidly move the occluder to
the fellow eye making sure one eye is always occluded. The
direction of the refixation shifts of the eyes to alternate cover
testing is interpreted the same as for cover/uncover testing,
described previously and shown in Figure 5-9.
INTERPRETING RESPONSES
TO
COVER TESTS
No shift to alternate cover testing indicates orthophoria. A
refixation shift to alternate cover testing indicates a strabismus
is present, either a tropia, a phoria, or a tropia with a phoria
(monofixation syndrome). Patients with a tropia and no fusion
and no phoria will show the same shift on cover test and alternate cover test. Patients with a phoria have straight eyes by
Hirschberg light reflex, and no refixation shift to cover/uncover
testing, but do show a shift to the alternate cover test (Fig.
5-10). Patients with a small-angle strabismus and peripheral
fusion (monofixation syndrome) will have both a phoria and a
tropia. Monofixators, therefore, demonstrate a small shift to
cover/uncover testing and a larger shift to alternate cover
testing. Cover/uncover testing discloses the tropia, and alternate
cover testing breaks down the phoria to show the full deviation,
FIGURE 5-10A–D. Alternate cover test in a patient with an esophoria.
(A) Eyes are straight; however, the patient has a tendency to cross (esophoria), but fusional divergence maintains proper alignment. (B) Left eye is
covered, dissociating fusion and allowing the left eye to manifest the
esophoria. Note that the left eye turns in under the cover. (C) The cover
is quickly shifted from the left eye to the right eye without allowing
binocular fusion. Now the left eye moves out as the right eye turns in
under the cover. (D) The cover is removed and the right eye moves out
by fusional divergence to allow the patient to regain fusion.
A
B
C
D
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TABLE 5-2. Clinical Findings of Phorias, Tropias, and Monofixation.
Orthotropia
Phoria
Tropia 10 PD
Monofixation 10 PD
Corneal light
reflex
Cover/
uncover
Alternate
cover
Fusion
Straight
Straight
Deviation
Small deviation
No shift
No shift
Shift
Small shift
No shift
Shift
Shift
Larger shift
Yes
Yes
No
Yes
tropia plus phoria. Comparing cover/uncover testing to alternate
cover testing is a good way to diagnose the monofixation syndrome, even in children who are too young to cooperate with
sensory testing. Remember, the presence of a phoria is an indication of binocular fusion. Table 5-2 shows the clinical findings
of phorias, tropias, and monofixation.
PRISM ALTERNATE COVER TEST
Prism alternate cover testing determines the amount of prism
necessary to neutralize the full deviation tropia and any latent
phoria. This is the test used to measure a deviation in anticipation of strabismus surgery. The test is performed by first using
the alternate cover test to estimate the size of the deviation. A
prism is then placed over one eye, oriented appropriately, in an
attempt to neutralize the deviation. Alternate cover testing is
then performed with the prism in place. If there is a residual
refixation shift with the prism in place, the prism is changed
(either increased or decreased) to neutralize the deviation (Fig.
5-11). When changing prisms, be sure to always keep one eye
covered to maintain binocular dissociation. Also, be sure not to
stack prisms of the same orientation (horizontal over horizontal
or vertical over vertical) to increase the prism power. It is acceptable to stack horizontal over vertical, but stacking prisms of the
same orientation results in underestimation of the angle size.
COMMON CAUSES
FOR
VARIABLE MEASUREMENTS
1. Poor control of accommodation. Solution: use targets
that require full accommodation to be seen. Targets with small
detail close to visual threshold are the best.
2. Variable working distance (usually at near). Solution:
control working distance to 1/3 meter at near, and standardize
working distance at distance; this is more critical for near measurements. Have a string measured at 1/3 meter to measure the
near working distance.
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3. Tonic fusion not suspended; usually seen in patients with
intermittent exotropia and accommodative esotropia. Solution:
keep binocular vision dissociated by prolonged occlusion with
alternate cover testing. Make sure one eye is always covered
when changing prisms (this is why prism bars are helpful).
4. Physiological redress fixation movements; commonly
associated with large-angle strabismus. Even when the deviation
is neutralized, there is an overshoot of the refixating eye. Solution: move occluder away from the patient’s face to allow
peripheral vision of the occluded eye. Also, judge the point
of neutralization as the point when redress movement is equal
to the refixation movement. Finally, bracket the deviation by
intentionally overcorrecting with too much prism, then reduce
prism until the best neutralization is achieved.
5. Incomitant deviation (A- or V-patterns and lateral gaze
incomitance). Small changes of face turns, head tilts, chin elevation, or chin depressions during the exam will change the deviation measured if the deviation is incomitant. Solution: control the
patient’s head position for primary position and cardinal fields of
gaze. Consistent head positioning is critical if reproducible measurements are to be obtained.
6. Poor vision. Solution: patient should wear full optical
correction during measurements. Use optotypes or fixation
targets that the patient can see. For patients with sensory strabismus and vision of 20/400 or worse, use Krimsky to measure
the deviation.
MEASURING
IN THE
CARDINAL POSITIONS
OF
GAZE
There are nine cardinal positions of gaze; however, in most clinical situations,5 measuring the deviation in primary position,
upgaze, downgaze, rightgaze, and leftgaze is sufficient (see Fig.
5-2). The positions of gaze are usually measured with the patient
fixing on a distance target. Sidegaze measurements are obtained
by moving the head up, down, right, left, and then in the oblique
axes. Measurement of the deviation in primary position should
also be done at near (1/3 m). Measurements in the cardinal positions of gaze are very helpful in identifying and quantifying
incomitance.
SIMULTANEOUS PRISM COVER TEST
The simultaneous prism cover test is used to measure the tropia
component of the monofixation syndrome without dissociating
the phoria and is therefore used only in patients with small-
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A
B
FIGURE 5-11A–B. Prism alternate cover test to measure esotropia. (A)
Left eye is esotropic; right eye fixing. (B) Base-out prism is placed before
the deviated left eye, and the retinal image moves closer to fovea, but the
deviation is still undercorrected.
angle strabismus. The test is performed by first estimating the
size of the tropia with corneal light reflex testing. A prism, as
determined by estimating the size of the tropia, is then presented
in front of the nonfixing eye (i.e., deviated eye) to neutralize the
tropia while the fixing eye is simultaneously covered by an
occluder (Fig. 5-12A). If the prism neutralizes the tropia, the
deviated eye will stay in its deviated position and there will be
no refixation shift. If the deviated eye shows a refixation movement, a residual tropia is present. The prism and occluder are
withdrawn from the eyes and, after several seconds, a different
prism is presented to the deviated eye while the fixing eye is
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F
F
20
20
Undercorrected
with nasal to temporal shift
C
40
No movement
F
F
40
40
40
No shift
D
FIGURE 5-11C–D. (C) Alternate cover testing is performed, covering first
right eye, then left eye. Because the prism undercorrects the deviation,
there is an outward shift of the uncovered eye. (D) Larger prism (40 prism
diopters, PD) is placed in front of the left eye. Alternate cover testing now
reveals there is no shift in eye position, as the deviation is completely
neutralized.
simultaneously covered. It is important to allow several seconds
to elapse before repeating the test so the patient can regain
binocular fusion. This process is repeated until there is no shift
of the deviated eye when the fixing eye is covered (Fig. 5-12B–D).
In patients with the monofixation syndrome, the amount of
tropia can be measured with simultaneous prism cover testing,
and the alternate prism cover test can be used to measure the
total angle, tropia plus phoria. The notation in the clinic chart
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B
C
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for a typical monofixator with a small-angle esotropia would
read ET 6 PD–E 15 PD.
MEASURING INCOMITANT DEVIATIONS
If the deviation is comitant and ductions are full, a prism can
be placed in front of either eye or even split between the eyes
to measure a deviation. However, when measuring patients
with an incomitant deviation secondary to ocular restriction or
muscle paresis, one must consider the primary versus the secondary deviation (see Chapter 3, Fig. 3-21). In accordance with
Hering’s law, the deviation is larger when the eye with limited
ductions is fixing (secondary deviation) than when the eye with
full ductions (primary deviation) fixes. When measuring a deviation with prisms, remember that the eye without the prism is
considered to be the fixing eye, and the eye looking through the
prism is the nonfixing eye, regardless of fixation preference or
the presence of amblyopia; this is because the eye without the
prism must come to primary position to fixate during alternate
cover testing. So, to measure the primary deviation, place a
prism over the eye with limited ductions and measure the
secondary deviation by placing the prism over the good eye
(Fig. 5-13).
The clinically accepted notation for primary and secondary
deviation in Figure 5-13 is
Left eye fixing 20 PD (primary deviation)
Right eye fixing 40 PD (secondary deviation)
FIGURE 5-12A–D. Simultaneous prism cover test for small-angle
esotropia. This test is useful for measuring the tropia in a patient with a
tropia and a phoria (monofixation syndrome). (A) Right esotropia with left
eye fixing. Estimate the deviation, then present a prism over the deviating eye while simultaneously covering the fixing eye. If the prism is sufficient to neutralize the esotropia, the eye behind the prism (in this case
the right eye) does not move. (B) Trying a 5 PD prism; it is too small and
the right eye moves out to pick up fixation. (C) A 10 PD prism is now
used to neutralize the esotropia. In this case, the prism neutralizes the
esotropia. (D) The left eye is covered as the 10 diopter prism is placed in
front of the right eye. No shift occurs because the 10 diopter prism neutralizes the 10 prism diopter esotropia.
A
B
C
FIGURE 5-13A–C. Primary versus secondary deviation. Top figure,
esotropia secondary to a tight medial rectus muscle. Left, diagram of the
primary deviation with the nonrestricted eye (left eye) fixing and a 20 prism
diopter prism placed in front of the restricted right eye. With the prism in
front of the restricted right eye, the image is on the fovea with the eye
resting in esotropic position. Note that the fixing eye is always the eye
without the prism, regardless of which eye is actually viewing. The three
drawings to the right show the secondary deviation (right eye fixing): (A)
A 20 prism diopter prism is placed in front of the left eye. The left eye picks
up fixation by adducting, and causes the right eye to abduct because of
Hering’s law. (B) The amount of force required to move the unrestricted
left eye is minimal, so the right eye gets minimal innervational force. With
a 20 prism diopter base-out prism over the left eye, the right eye does not
abduct sufficiently to place the image on the fovea. (C) A 40 diopter baseout prism causes the left eye to deviate greatly, moving the restricted right
eye enough to place the image on the fovea. Secondary deviation equals 40
prism diopters, whereas the primary deviation is 20. Note that, with the
prism over the left eye, the restricted right eye must come to primary position to fixate.
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Measuring the Accommodative Convergence to
Accommodation (AC/A) Ratio
To understand the AC/A ratio, we must review measurements
of accommodation and convergence. Accommodation is the
increase in lens power to clearly focus at near. The closer the fixation target, the more accommodation is needed to keep the
image focused on the retina. Accommodation is measured in
diopters. The number of diopters of accommodation needed to
focus at a specific near point is the reciprocal of the fixation distance in meters. For example, if the fixation target is at 1/3 m,
then an emmetropic patient has to accommodate 3.00 diopters
to put the image in focus, 2.00 diopters at 1/2 m, and 1.00 diopter
at 1 m. Note, that a 2.00 hypermetrope without correction
would have to accommodate 5.00 diopters at 1/3 m (2.00 diopters
for the hypermetropia and 3.00 diopters for near fixation).
Convergence keeps the eyes aligned on the approaching
targets. Because convergence is linked to accommodation, convergence increases as accommodation increases. Additionally,
the farther apart the eyes, the more convergence is required
to keep the eyes aligned at near. The amount of convergence
needed to keep the eyes aligned on a target at a specific distance
is the reciprocal of the fixation distance in meters times the
interpupillary distance in centimeters. For example, if the
patient has an interpupillary distance of 50 mm and the target
is at 1/3 m, the patient must converge 15 prism diopters to keep
ocular alignment on the near target (3 diopters 5 cm). If the
interpupillary distance is 40 mm for the same working distance
of 1/3 m, the required convergence would be 12 prism diopters.
AC/A RATIO
Accommodative convergence to accommodation ratio (AC/A
ratio) is the amount of change in convergence for a specific
amount of change in accommodation. A high AC/A ratio means
the eyes overconverge for a given amount of accommodation
(eso-shift at near), whereas a low AC/A ratio means there is
underconvergence per diopter of accommodation (exo-shift at
near).
Two methods for measuring the AC/A ratio are the heterophoria method and the lens gradient method. These tests are
based on changing the patient’s accommodation and then measuring the associated change in convergence. Accommodation is
changed by either changing the fixation distance (heterophoria
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method) or by changing the amount of accommodation needed
for a specific fixation distance by introducing various numbers
of plus and minus spherical lenses (lens gradient method). A
third method that does not actually measure the AC/A ratio but
measures the relationsip between the distance and near deviation is the clinical distance–near relationship. The clinical distance–near relationship provides information about the overall
change in convergence when one looks from distance to near,
including the effects of accommodation and proximal convergence. Most clinicians use either the clinical distance–near relationship method or the lens gradient method to determine the
accommodation to convergence relationship.
When measuring the AC/A ratio for any of these methods,
it is important to use accommodative targets, have the patient
wear their full optical correction, use alternate cover testing to
measure the deviation, and control the fixation target distance.
By convention, 6 m (20 ft) is used for distance and 1/3 m (14 in.)
for near. Normal AC/A ratio for the heterophoria method and
lens gradient method is 4:1 and 5:1, and ratios of 6:1 or more are
considered high. For calculations of the AC/A ratio, esodeviations are represented as positive numbers and exodeviations as
negative numbers.
Heterophoria Method The heterophoria method compares
the distance and near deviation to determine the AC/A ratio. It
requires measurement of the distance and near deviation in
prism diopters and the interpupillary distance in centimeters.
The following formula is used to calculate the AC/A ratio by
the heterophoria method, where IPD is interpupillary distance
(cm), D is distance deviation (PD), N is near deviation (PD), and
D A is diopters of accommodation for near fixation (1/3 m 3
diopters):
ND
Formula: AC/A IPD DA
Example 1.
Distance ET 31
Near ET 40
Interpupillary distance 50 mm
Nearest target distance 1/3 m 3 D accommodation
(40 31)
AC/A 5 8 (high AC/A ratio)
3
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LENS GRADIENT METHOD
The lens gradient method determines the AC/A ratio by measuring the change in ocular deviation associated with a specific
change in lens-induced accommodation. This test changes
accommodation by having the patient view an accommodative
target through supplemental plus or minus spherical lens. A plus
lens relaxes accommodation so that with less accommodation
there is less convergence. A minus lens causes increased accommodation, increased convergence, and an eso-shift. The AC/A
ratio is calculated by measuring the deviation at a set distance,
with and without supplemental spherical lenses, and dividing
the difference by the lens power used. Measurements are usually
made in the distance to minimize proximal convergence, and a
3.00 diopter lens is usually used.
The formula for the gradient method is
AC/A Deviation without lens Deviation with lens
Lens in diopters
Example 1.
Deviation without lens ET 40
Deviation with 3.00 lens ET 10
40 10
AC/A 10 (high AC/A ratio)
3
Example 2.
Deviation without lens XT 4
Deviation with 3.00 lens ET 14
4 14
AC/A 6 (normal AC/A ratio)
3
Another useful calculation is to estimate the effect of a spectacle lens on a deviation, given an estimated AC/A ratio, as
shown in Examples 3 and 4:
Example 3.
If a child is assumed to have a normal AC/A ratio (5) and an
exophoria of 10 PD, what is the effect of changing the patient’s
spectacle correction by 2.00 diopters? As the minus 2.00 lens
increases accommodation by 2.00 diopters, and convergence is
increased by a ratio of 5 to 1 (AC/A ratio 5), the 2.00 lens
overcorrection would result in 10 PD of convergence and
orthophoria.
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Example 4.
A child has a 4.00 refractive error and a 30 PD esotropia.
Assuming the AC/A ratio is high normal (6), what will be the
effect of the full hypermetropic correction on the deviation? A
4.00 diopter lens will cause 24 PD of divergence; thus, the deviation with glasses will be esotropia of 6 PD. Thus, prescribing
the hypermetropic glasses would have a good chance of correcting the deviation with only a small residual deviation.
Clinical Distance–Near Relationship
The clinical distance–near relationship does not specifically
measure the accommodative convergence nor is it a ratio. It is
a simple comparison of the deviation in the distance to the deviation at near. One can figure the clinical distance–near relationship by subtracting the distance deviation from the near
deviation. A distance–near difference within 10 PD is considered
normal whereas differences greater than 10 PD are considered
high. This clinical distance–near relationship is a simple, but
very useful, method for identifying patients with a high AC/A
ratio.
N D clinical distance–near relationship
D distance deviation viewing target at 6 m (20 ft)
N near deviation viewing target at 1/3 m
D ET 20
N ET 40
AC/A relationship: 40 20 20 (high AC/A ratio)
Example 1:
D XT 10
N ET 20
AC/A relationship: 20 (10) 30 (high AC/A ratio)
Example 2:
D ortho
N XT 15
AC/A relationship: 15 0 15 (low AC/A ratio)
Example 3:
Lancaster Red-Green Test
The Lancaster red-green test is a fovea-to-fovea test with two
fixation targets, one that the examiner controls and one controlled by the patient. This test is very useful for measuring
incomitant strabismus in patients with diplopia and NRC. The
chapter 5: the ocular motor examination
165
fixation targets are red- and green-colored linear streaks of light
that are projected on a screen. The patient wears red-green
glasses (usually red over right eye) and holds one light (green
light in Fig. 5-14) while the examiner holds the second light (red
light in Fig. 5-14). The examiner projects the red light on the
screen, and the patient is directed to look at the red light.
Because the patient’s right eye with the red filter only sees the
examiner’s red light, the right eye (fovea) aligns with the examiner’s light. Thus, the right eye becomes the fixing eye and its
position is controlled by where the examiner places the red light.
Next, the patient is directed to aim the green light (which they
are holding) over the examiner’s red light. Because the left eye
only sees the green light, the patient moves the green light over
the red light by orienting the green light so it falls on the left
fovea. The patient now sees the two lights superimposed, as both
lights fall on the fovea of each eye. The patient in Figure 5-14
has a left esotropia, so with the green filter over the left eye, the
patient directs the green light to the right of the red light. Patients
with orthotropia will place the lights on top of each other,
whereas a patient with a left exotropia will point the green light
to the left of the red light.
The Lancaster red-green test directly shows the examiner
where the eyes (foveas) are pointing, which is just the opposite
of diplopia tests. The amount of deviation is measured by the
amount of separation between the two projected lights on the
screen. With the Lancaster red-green test, the eye that sees
the examiner’s light is the fixing eye, so the examiner can move
the target to various positions on the screen to measure the
deviation in eccentric fields of gaze. Primary versus secondary
deviations can be measured by the examiner trading lights with
the patient. Torsion can also be assessed in various positions of
gaze by observing the tilt of the lines on the screen. Nasal displacement of the top of the line indicates intorsion, and temporal displacement of the top of the line indicates extorsion.
TORSION
MADDOX ROD
AND
TORSION
The line seen with the Maddox rod can be used to determine
subjective torsion, with a single lens (single Maddox rod test) or
a lens over each eye (double Maddox rod test). With the double
Maddox rod test, the patient is asked to make the two streaks
of the Maddox rod parallel. If the eyes are straight, a prism can
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chapter 5: the ocular motor examination
167
A
B
C
FIGURE 5-15A–C. Double Maddox rod test with the patient perceiving
the streak of light vertically. Remember, this is not a localizing test, and
change in torsion is relative to the fellow eye. (A) Normal patient with
no torsion. The Maddox rods are aligned at the zero position for each eye.
(B) A patient with right incyclotorsion 15°, relative to the left eye, with
the right Maddox rod turned clockwise. (C) Patient with bilateral extorsion, 15° each eye. Total extorsion is 30°.
be used to induce a deviation either horizontally or vertically to
separate the lines of the Maddox rod. Patients without torsion
see parallel lines (Fig. 5-15A), those with intorsion see the 12
o’clock position turned nasally (Fig. 5-15B), and those with
extorsion see the 12 o’clock position turned temporally (Fig. 515C). Note that the Maddox rod tests, and most subjective
torsion tests for that matter, do not localize the eye with the
torsion; they only measure the relative difference in torsion
between the two eyes. One often finds a monocular torsion with
the subjective Maddox rod testing but detects bilateral torsion
by objective testing with indirect ophthalmoscopy because the
eye that the patient perceives to have torsional misalignment
depends on which eye is fixing (ocular dominance). To find the
total torsion with the double Maddox rod, add the torsion of the
two eyes together.
TORSIONAL DIPLOPIA
IN
FREE VIEW
Patients with retinal intorsion view the world as being extorted,
and retinal extorsion cause objects to be perceived as being
intorted. A person with intorsion sees the top of a vertical line
tilted temporally, and extorsion will cause the top of a vertical
line to appear to be shifted nasally.
FIGURE 5-14. Lancaster red-green test in a patient with normal retinal
correspondence (NRC), esotropia, and diplopia; this is a fovea-to-fovea
test. The patient fixates on the streak of light projected by the examiner.
The patient then directs the other light to align with the examiner’s light.
Patient will perceive a single streak of light as each light falls on the corresponding fovea, even though the streaks are separated.
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OBJECTIVE RETINAL TORSION
Objective retinal torsion is used to estimate the relationship of
the fovea to the optic disc. In normal patients, the fovea is
located between the midpoint and the lower border of the optic
nerve. Patients with torsion will have a shift in the position of
the fovea relative to the optic disc. With extorsion, the fovea is
shifted below the inferior border of the optic disc, whereas intorsion shifts the fovea higher than the midpoint of the optic nerve.
In actuality, the fovea is the center of vision and the optic nerve
actually rotates around the fovea. Remember that the indirect
ophthalmoscopic view is inverted, so extorsion is viewed when
the fovea is above the upper pole of the disc, and intorsion is
viewed when the fovea is below the midpoint of the disc. See
Chapter 3 (Fig. 3-14) for an example of objective retinal torsion.
Special Tests for Identifying Restriction
and Paresis
Tests for identifying restriction and paresis include forced
duction testing, generated forced duction testing, and saccadic
velocity measurement. Restriction and paresis can coexist, especially in cases of long-standing muscle paralysis such as a longstanding sixth nerve palsy. In these cases, the antagonist of the
paretic muscle (i.e., the medial rectus muscle in the case of a
sixth nerve palsy) contracts and becomes stiff, thus adding a
component of restriction to the paralytic condition.
FORCED-DUCTION TESTING
Forced ductions are indicated if there is evidence of restricted
ductions. Forced ductions is somewhat invasive, however, but
can be performed on most cooperative adults. In patients who
are scheduled for surgery, forced ductions are performed at the
time of surgery. The technique for rectus muscles is to grasp the
eye at the limbus and slightly proptose the eye, then rotate
the eye into the field of limited ductions. If the eye is inadvertently pushed posteriorly during testing, the rectus muscles will
slacken, which may cause the examiner to possibly miss a rectus
muscle restriction. When examining awake patients, be sure to
ask the patient to look in the direction of the forced ductions to
relax the muscle that is being tested. The tightness of oblique
muscles can be assessed by a retropulse maneuver called the
exaggerated traction test, developed by Guyton.4
chapter 5: the ocular motor examination
169
ACTIVE FORCED-GENERATION TEST
Active forced-generation testing assesses rectus muscle
strength. The eye is anesthetized with a topical anesthetic, and
the eye is grasped with forceps at the limbus in the same fashion
as forced-duction testing. The patient is asked to look into the
field of limitation while the eye is held in primary position (Fig.
5-16). This author prefers to use a cotton tip applicator instead
of forceps, as forceps can tear the conjunctiva. The examiner
feels the force generated by the muscle and compares this with
the fellow, nonaffected eye. This test is useful in assessing the
amount of muscle function associated with any palsy such as
sixth nerve paresis or double elevator palsy.
SACCADIC VELOCITY MEASUREMENT
There are various ways to measure saccadic velocities. Clinical
estimation is available to all clinicians and is simply the observation of fast eye movements. Fast eye movements can be
elicited by having the patient look quickly from side to side or
by using an optokinetic nystagmus (OKN) drum. An OKN drum
is very useful in young children. Patients with rectus palsies will
not be able to generate saccades. Quantitation of eye movements
can be made by special equipment such as the electro-oculogram
(EOG), which measures the velocity of eye movements. Figure
5-17 shows an EOG tracing of a patient with a sixth nerve
paresis. The initial part of the tracing shows a vertical spike indicating adduction movement; however, the end of the tracing
shows a mild slope indicating slow abduction. Clinically, if the
patient is able to generate a saccadic eye movement in the direction of the eye limitation, then the limitation is restrictive and
not secondary to paralysis. Normal saccadic velocity depends on
the size of the saccadic eye movement. Large eye movements
have higher peak velocities. Normal saccadic velocities range
from 200 to 700 degrees per second (°/s).1
RESTRICTION
Forced-duction testing is a useful test for identifying restrictions. If the eye can not be easily rotated into the field of limited
ductions, then a restriction is present. Another sign of restriction is the “dog on a leash” eye movement. A patient with
restrictive strabismus and good muscle function will show
normal saccadic (fast) eye movements until the eye reaches the
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 5-16A,B. Forced-generation test on patient with a right sixth
nerve palsy. (A) Patient viewing in primary position with the right eye
anesthesized and a dry cotton-tipped applicator placed to the temporal
limbus. (B) The patient looks to the right and attempts to abduct the right
eye. Pressure by the cotton-tipped applicator pushing the eye nasally, prevents the right eye from moving. The examiner can feel the amount of
force exerted by the right lateral rectus through the cotton-tipped applicator. Normally, the applicator could not hold the eye in adduction when
the patient is actively abducting.
chapter 5: the ocular motor examination
171
FIGURE 5-17. Electro-oculogram of patient with a sixth nerve palsy.
Upward arrow on the left indicates adduction. Note that the tracing
makes a sharp right upturn, showing normal medial rectus function. On
the right is abduction (downward arrow). Note that the curve is gradual,
indicating decreased lateral rectus function.
restriction; then the eye stops abruptly. If a patient has limited
ductions, yet can generate a saccadic eye movement in the direction of the limitation, restriction instead of paralysis is the cause
of the limitation. A restriction also causes eyeball retraction
and lid fissure narrowing, as the agonist muscle pulls the eye
posteriorly against the restrictive leash. A tight medial rectus
muscle will cause lid fissure narrowing on attempted adduction.
Increased intraocular pressure can also be a clinical sign of
restriction. As the eye rotates against the restriction into abduction for a restricted medial rectus muscle, intraocular pressure
measurements will be higher than in primary position or in
adduction.
PARESIS
The inability for a muscle to generate a saccadic eye movement
is an important indication of paresis. Even patients with severe
restrictive strabismus will be able to generate a small-amplitude
saccade in the direction of the restriction. Patients with a
muscle palsy show a slow eye movement as compared to the
fellow eye or the affected muscle’s antagonist. In contrast to
restriction, which causes lid fissure narrowing, paresis causes
lid fissure widening and relative proptosis as the patient looks
in the field of action of the paretic muscle. A patient with a
sixth nerve palsy, for example, will show lid fissure widening
on attempted abduction because the medial rectus muscles
relaxes on attempted abduction as per Sherrington’s law and,
with the lateral rectus paretic, the posterior pressure of the
orbital fat pushes the eye forward. The active forced-generation
test shows relative weakness of the paretic muscle. One can
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handbook of pediatric strabismus and amblyopia
compare agonist and antagonist muscle strength, as well as
comparing the muscle strength of fellow eyes, to assess muscle
function.
Cycloplegic Refraction
Cycloplegic refraction should be performed on every new strabismus patient. The standard regimen is 1 drop of cyclopentolate 1% and neosynephrine 2.5% in each eye, times two, 5 min
apart; then, perform the refraction 30 min after the last drop. In
patients with dark eyes, the drops should be repeated three
times. Patients with blue eyes, or patients with pigment dilution syndrome such as ocular albinism, should receive one set
of drops. Remember that mydriasis does not mean cycloplegia.
The mydriatic effect comes on sooner and lasts longer than the
cycloplegic effect. If the patient shows varying refractive error
during retinoscopy, then it is likely that the patient has only
partial cycloplegia and requires more drops. In cases of heavily
pigmented eyes or in patients with variable refractions, it may
be advisable to have the patient return for a 1% atropine refraction. In these patients, atropine should be given to both eyes
twice a day for 3 days before the refraction. (See Chapter 3 for
details on cycloplegic agents.)
Fundus Examination (Objective Torsion)
See Chapter 3 and Figure 3-14 for details on fundus
examination.
References
1. Bahill AT, Brockenbrough A, Troost BT. Variability and development of normative data base for saccadic eye movements. Investig
Ophthalmol Vis Sci 1981;21:116–125.
2. Biedner et al. Stereopsis testing: at the beginning or the end of
orthoptic examination. Binoc Vis Q 1992;7:37–39.
3. De Respinis PA, Naidu E, Brodie SE. Calibration of Hirschberg test
photographs under clinical conditions. Ophthalmology 1989;96:
944–949.
4. Guyton DL. Exaggerated traction test for the oblique muscles. Ophthalmology 1981;88:1035.
5. Mitchell PR, Wheeler MB, Parks MM. Kestenbaum surgical procedure of torticollis secondary to congenital nystagmus. J Pediatr
Ophthalmol Strabismus 1987;24:87–92.
chapter 5: the ocular motor examination
173
6. Paliaga GP. Linear strabismometric methods. Binoc Vis 1992;7:134–
154.
7. Ruttum MS, Shimshak KJ, Chesner M. Photographic measurement
of the angle of strabismus. In: Campos EC (ed) Strabismus and
ocular motility disorders. Basingstoke: Macmillan, 1990:155–160.
6
Sensory Aspects of
Strabismus
Kenneth W. Wright
SENSORY ADAPTATIONS
Visual neurodevelopment changes in response to abnormal
stimulation from a blurred retinal image or strabismus. These
changes are referred to as sensory adaptations. The specific type
of sensory adaptation depends on when the abnormal visual
stimulation occurred, the severity of the abnormal stimulation,
and type of binocular disruption. In Chapter 4, we discussed cortical suppression and amblyopia, which are basic sensory adaptations to a blurred image or strabismus. This chapter provides
a list of more specific sensory adaptations that are encountered
clinically. These adaptations are divided into two sections based
on the onset of the sensory insult: (1) visually mature and (2)
visually immature. A discussion of important sensory tests is
provided at the end of this chapter.
MATURE VISUAL SYSTEM
The following sensory adaptations occur after the development
of bifoveal fusion, when the visual system is mature. Visual
development continues until approximately 7 to 8 years of age.
After that, there is minimal visual-neurological plasticity. There
are some exceptions, however, and prolonged visual plasticity
into adulthood has been reported (see discussion at the end of
this section: Prolonged Visual Plasticity).
Diplopia
Acquired strabismus in patients over 7 or 8 years of age usually
results in double vision (i.e., diplopia). Diplopia is also reported
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175
in younger children with acquired strabismus, but it is usually
transient and lasts only 2 to 4 weeks before the diplopia is cortically suppressed. The patient with diplopia will fixate on an
object with one fovea, and see a diplopic image of that object
that comes from the perifoveal retina of the deviated eye (Figs.
6-1, 6-2). The fovea of the deviated eye is suppressed to avoid
simultaneously seeing two different objects, one from each fovea
(see below: Confusion). Thus, the patient with one eye fixing on
Red
Filter
Patient's Perception
Uncrossed Diplopia
FIGURE 6-1. Esotropia with uncrossed diplopia. The image of the skier
falls on the fovea of the left eye and on the nasal retina of the deviated
right eye. A red filter over the right eye causes the diplopic image from
the right eye to be red. Note at the bottom of the figure: the patient perceives the red image from the right eye to be located to the right of the
clear image, resulting in uncrossed diplopia.
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Red
Filter
Patient's Perception
Crossed Diplopia
FIGURE 6-2. Exotropia with image falling on the fovea of the left eye and
on temporal retina of the right eye, causing crossed diplopia. A red filter
over the deviated right eye causes the diplopic image from the right eye
to be red. Note at the bottom of the figure: the patient perceives the red
image from the right eye to be located to the left of the clear image, resulting in crossed diplopia.
a painting and the deviated eye pointed to a lamp will see two
paintings, not a painting superimposed on a lamp. The image
from the fixing eye will be in clear focus located directly in front
of the patient, while the diplopic image from the deviated eye
will appear blurred and off center because it comes from the
peripheral retina.
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chapter 6: sensory aspects of strabismus
OD fixing
RE
LE
FIGURE 6-3. Patient with a left hypertropia. A red filter over the deviated left eye causes the diplopic image from the left eye to be red. The X
projects to the fovea of the fixing right eye and to the superior retina of
the deviated left eye. Because the superior retina views the inferior visual
field, the red diplopic image in the left eye is seen below the clear image
from the right eye.
Esotropia causes the image to fall on the nasal retina of the
esotropic eye, which projects temporally and causes uncrossed
diplopia because diplopic image is on the same side as the
deviated eye (see Fig. 6-1). Exotropia causes the image to fall
temporal to the fovea of the exotropic eye, which projects to
the nasal field, producing crossed diplopia (see Fig. 6-2). We
can remember the s in esotropia means same side diplopia
(uncrossed), and the x in exotropia means a cross for crossed
diplopia. In cases of vertical strabismus, the hypertropic eye perceives the object as being below the image from the fixing eye
(Fig. 6-3).
Aniseikonia is a difference in image size between eyes and
is a cause of diplopia. Aniseikonia is usually caused by anisometropia and is treated with spectacles. An acquired retinal
image size disparity up to 7% is usually tolerated, but aniseikonia over 10% may result in diplopia.
Confusion
Under rare circumstances, instead of diplopia, patients with
acquired strabismus see two different images superimposed on
each other, one image from each fovea. If the right eye is looking
at a painting and the left eye is pointed at a lamp, the patient
with confusion will see the lamp superimposed on the painting.
This simultaneous perception from the fixing fovea and the devi-
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ated fovea is termed confusion. Most patients with acquired
strabismus do not experience confusion because they suppress
the foveal area of the deviated eye and see the diplopic image
from the peripheral retina. Confusion is exceedingly rare;
however, this author has reported a patient with tunnel vision
secondary to glaucoma and acquired strabismus who had confusion rather than diplopia.10 The peripheral visual field loss
associated with the glaucoma probably forced foveal fixation of
the deviated eye. It is likely that suppression of the fovea of the
deviated eye is dependent on peripheral retinal stimulation by
the diplopic image and, therefore, foveal suppression is not possible when the peripheral field is eliminated.
IMMATURE VISUAL SYSTEM
Sensory adaptations occur when the binocularity is disrupted by
strabismus or a blurred retinal image during the first few years
of life, usually before 6 years of age. The specific type of sensory
adaptation depends on many factors, including the size of the
strabismus, whether it is intermittent or constant, the age of
onset of the strabismus, and the age when the strabismus is corrected. Once childhood sensory adaptations are acquired, they
are usually present throughout the patient’s life. Cortical suppression is a basic mechanism present in virtually all sensory
adaptations to strabismus and a unilateral blurred retinal image.
Cortical suppression and amblyopia are discussed in Chapter 4.
Herein is a discussion of specific patterns of suppression and
abnormal binocular vision.
The following discussion of sensory abnormalities presumes
that strabismus is the primary event and that the brain develops sensory adaptations in response to the abnormal visual
stimulation. In this author’s view, this is probably true for the
majority of strabismus cases; however, strabismus can also
occur as a secondary consequence of poor binocular fusion.
Examples of a primary fusion deficit and secondary strabismus
include sensory strabismus (i.e., unilateral congenital cataract)
and central fusion loss associated with closed head trauma. It
should be pointed out that some would argue that most types of
childhood strabismus are a consequence of congenitally abnormal fusion centers within the brain, not motor misalignment
degrading binocular fusion. The answer to this controversy—
which came first, the strabismus or the sensory fusion abnor-
chapter 6: sensory aspects of strabismus
179
mality?—remains unanswered. The fact that one can recover
excellent binocular fusion and stereoscopic vision with early and
aggressive treatment suggests that, at least in some cases, the
sensory abnormality is secondary to the strabismus.
Monofixation Syndrome (Peripheral Fusion)
Small-angle strabismus (10 prism diopters, PD) or mild to moderate unilateral retinal image blur in young children and infants
causes a suppression of the central visual field of the deviated
or blurred eye. The small suppression scotoma allows for peripheral fusion (Fig. 6-4). This sensory adaptation, first described by
Marshall Parks, is termed the “monofixation syndrome.”3 Suppression is localized to within the central 4° to 5° because the
central retina has small receptive fields and high spatial resolution potential; therefore, relatively small differences in image
clarity or retinal image position are recognized. In the peripheral fields, however, slight interocular image differences are not
detected, as the peripheral retina has large receptive fields and
relatively low spatial resolution. Thus, small retinal image discrepancies between the eyes are not disruptive in the peripheral
fields, and peripheral fusion occurs. The size of the suppression
scotoma is directly proportional to the amount of image blur and
size of the strabismus. If the interocular image disparity is too
great, even peripheral fusion will be disrupted. Thus, strabismus
greater than 10 PD or severe unilateral image blur (e.g., unilateral dense cataract) will disrupt even peripheral fusion. These
patients will lack binocular fusion and will not have the
monofixation syndrome.
Because patients with the monofixation syndrome have
motor fusion, they often have a relatively large underlying
phoria in addition to a small tropia, giving rise to the term
phoria-tropia syndrome. Patients with monofixation syndrome
usually have stereoacuity in the range of 3000 to 70 s arc, and
the central suppression scotoma measures between 2° and 5°.
The Bagolini striated lens test is a sensory test that presents a
linear streak of light to each eye oriented 90° apart and centered
on the fixation light (Fig. 6-5). Patients with normal binocular
vision describe a cross through the center of a fixation light (Fig.
6-5A). In contrast, patients with the monofixation syndrome
will describe a cross with a gap in the center of the line presented to the deviated eye (Fig. 6-5B). The gap represents a
central suppression scotoma of the nonfixing eye. It is impor-
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handbook of pediatric strabismus and amblyopia
Small Angle
Esotropia
Patient's Perception
Suppression
Scotoma
A
Anisometropic
Amblyopia
Suppression
B
Scotoma
FIGURE 6-4A,B. (A) Diagram of monofixation syndrome secondary to a
small-angle esotropia. (B) Hypermetropic anisometropia with amblyopia.
In both cases, patient perceives a clear single image, as the suppression
scotoma eliminates the discrepancy from the esotropia and blurred image,
respectively. Because of the suppression scotoma, the patient sees one
clear image.
tant to note that as soon as the dominant fixing eye is occluded,
the suppression scotoma vanishes and the patient fixes with the
fovea (Fig. 6-5C). The suppression scotoma is often referred to
as a facultative scotoma, because its presence is dependent upon
fixation with the dominant eye. Worth 4-dot testing is another
good method to document the monofixation syndrome. Patients
with the monofixation syndrome will fuse the near Worth 4-dot
chapter 6: sensory aspects of strabismus
181
A
B
C
FIGURE 6-5A–C. Monofixation with microtropia and visual perception
with Bagolini lenses. (A) Bagolini lenses over right small-angle esotropia
and suppression scotoma, right eye. (B) Retinal images from (A). Note the
patient’s perception is one continuous line LE, and one line with an interruption in the center RE. (C) Covering the fixing eye (LE) eliminates the
suppression scotoma, and the patient sees a single, continuous line from
RE.
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handbook of pediatric strabismus and amblyopia
(subtends 6° or 12 PD), but suppress the nondominant eye for
the distance Worth 4-dot (subtends 1.25°) because it falls within
the suppression scotoma. Further descriptions of these sensory
tests follow later in the chapter.
Patients with monofixation syndrome often have amblyopia. The amblyopia can be mild (1 or 2 Snellen lines difference)
or quite severe (20/200). Even patients with 20/200 amblyopia
can still maintain the monofixation syndrome with some
peripheral fusion and gross stereopsis. Clinically, the monofixation syndrome is frequently encountered in patients with
anisometropic amblyopia, unilateral partial cataract, and
small-angle strabismus. Parks described a rare condition,
primary monofixation syndrome, which he hypothesized was
caused by a congenital lack of central fusion.3
Anomalous Retinal Correspondence
Normal retinal correspondence (NRC) is the binocular relationship in which the true anatomic foveas of each eye are functionally linked together in the occipital cortex. Anomalous
retinal correspondence, or ARC, is an adaptation to a moderateangle infantile strabismus that allows the brain to accept
parafoveal retinal images from the deviated eye and superimposes them with images fixing from the fixing eye. The angle of
deviation associated with ARC is usually between 15 and 30 PD,
too large to allow peripheral fusion or monofixation. Thus, ARC
is a binocular sensory adaptation used to eliminate diplopia by
accepting the eccentric image location in the deviated eye as
the visual center. This adaptation is a cortical reorganization of
retinal correspondence and establishes a new functional fovea
called the pseudo-fovea that corresponds to the true fovea of the
dominant fellow eye (Fig. 6-6A).8 By cortically establishing a
pseudo-fovea at the site of the diplopic image in the deviated eye
that corresponds with the true fovea of the fixing eye, the retinal
images can be superimposed. ARC and the pseudo-fovea are only
present under binocular conditions. When the fixing eye is
occluded, the patient changes fixation to the true fovea of the
previously deviated eye.
If the strabismus of a patient with ARC is partially or fully
corrected by surgery or a prism, the image will be displaced off
the pseudo-fovea onto the retina that is cortically perceived as
being noncorresponding. Because the image is displaced off the
pseudo-fovea, the patient will see double even if the image falls
chapter 6: sensory aspects of strabismus
183
Patient's Perception
A
B
FIGURE 6-6A,B. Anomalous retinal correspondence with right esotropia.
(A) Left eye fixes with the fovea (F) and right eye fixes with the pseudofovea (PF). The PF corresponds with the esotropia and is located on the
nasal retina. Patient perceives a single image as the pseudo-fovea (PF) of
the right eye corresponds with the true fovea (F) of the left eye. (B) Placing
a base-out prism to partially neutralize the esotropia. The patient fixes
the left eye and sees double, as the image now falls temporal to the
pseudo-fovea (PF). Images temporal to the pseudo-fovea (PF) will project
to the opposite visual field and cause diplopia.
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on the true anatomic fovea. This type of diplopia is called paradoxical diplopia. Remember that under binocular viewing the
pseudo-fovea is the central orientation of the eye and images displaced off the pseudo-fovea will be perceived as falling on noncorresponding retina. Figure 6-6A shows a patient with 20 PD
esotropia and ARC with a nasal pseudo-fovea, right eye. Note
that after partial correction of the esotropia with a 15 PD baseout prism, the image is now temporal to the pseudo-fovea (Fig.
6-6B). This patient will have crossed diplopia because the image
falls on retina that is temporal to the pseudo-fovea, and temporal retina projects to the opposite hemifield. The patient will
experience the crossed diplopia so long as the image is temporal to the pseudo-fovea, even if the eyes are aligned so the image
falls directly on the true fovea.
Adult patients with ARC will often experience some
diplopia after correction of their strabismus. An easy way to
predict if a strabismic patient has ARC and will have postoperative paradoxical diplopia is to neutralize the angle of deviation
with a prism. If the patient has diplopia with prism neutralization of the deviation, then the patient has ARC and the patient
should be informed that postoperative diplopia will occur after
the eyes are straightened. Fortunately, paradoxical diplopia is
usually not so bothersome as true diplopia associated with
normal retinal correspondence and, in most cases, paradoxical
diplopia will vanish within a few weeks after surgery. Only in
rare circumstances is postoperative paradoxical diplopia so
bothersome that it interferes with everyday activities. Even so,
in rare instances, persistent postoperative paradoxical diplopia
has required a reoperation to recreate the initial strabismus to
eliminate paradoxical diplopia. In cases where preoperative
prism neutralization creates paradoxical diplopia that bothers
the patient, one can prescribe press-on prisms (prism adaptation)
to see if the diplopia will subside over several weeks.
Bagolini striated lenses on a patient with a 20 PD esotropia
and ARC are depicted in Figure 6-7A. The patient perceives
a cross (normal response) even though there is an esotropia,
because the line in the deviated eye passes through the pseudofovea. If a strabismic patient reports seeing a complete cross to
Bagolini striated lenses, then they have ARC (Fig. 6-7B). This
cortical reorganization of ARC is only present during binocular
viewing and, when the dominant eye is covered, the patient
reorients to the true anatomic fovea (Fig. 6-7C). ARC should not
be confused with eccentric fixation. Remember, ARC is only
chapter 6: sensory aspects of strabismus
185
A
B
C
FIGURE 6-7A–C. Anomalous retinal correspondence (ARC) as tested
with Bagolini lenses. (A) Bagolini lenses stimulate the right fovea (F) and
left pseudo-fovea (PF). Note that the pseudo-fovea (PF) is nasal to the true
fovea (F). (B) Retinal location of the Bagolini striation when the fovea (F)
of the right eye is being stimulated and the pseudo-fovea (PF) of the left
eye is being stimulated. Patient’s perception is a cross, as the pseudo-fovea
(PF) corresponds to the true fovea (F). (C) When the right eye is occluded,
the patient now fixates with the true fovea (F) of the left eye. Note that
the pseudo-fovea has disappeared. Patient perceives a single line, which
stimulates the visual center.
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present during binocular viewing, whereas eccentric fixation
represents a monocular loss of vision (amblyopia) and is present
during both monocular and binocular viewing.
ARC provides crude binocular vision with superimposition
of retinal images; however, there is not true fusion. Patients
with ARC do not have fusional vergence amplitudes, and they
do not have stereoacuity. ARC can occur in association with
intermittent strabismus. Some patients with intermittent exotropia, for example, have binocular vision with stereopsis when
they are aligned but switch to ARC when they are tropic. In
general, ARC is associated with good vision or only mild
amblyopia.
Harmonious ARC is the term used for the situation as
described previously where the position of the pseudo-fovea
completely compensates for the angle of strabismus (see Fig. 66). Described another way, the strabismic deviation equals the
pseudo-foveal offset from the true fovea. The amount of pseudofoveal offset is termed the angle of anomaly, which is equal to
the strabismic deviation (objective angle). Clinically, however,
there are many cases in which the angle of strabismus does not
exactly match the location of the pseudo-fovea so that the target
image does not fall on the pseudo-fovea. This condition is called
unharmonious ARC.
In Figure 6-8A, the angle of the strabismus measures 20 PD
(objective angle), but the pseudo-fovea is only 15 PD from the
true fovea (angle of anomaly 15 PD). Thus, the image is falling
5 PD nasal to the pseudo-fovea. A 5 PD base-out prism over the
right eye places the image on the pseudo-fovea and eliminates
the diplopia. The discrepancy between the location of the
pseudo-fovea and the location of the target image is called the
subjective angle; in Figure 6-8B, the subjective angle is 5 PD.
Note that neutralizing the subjective angle eliminates diplopia
associated with unharmonious ARC, but neutralizing more
than the subjective angle results in paradoxical diplopia (Fig.
6-8C). In these cases of unharmonious ARC, it is likely that the
angle of strabismus has changed (usually increased) after the
development of the pseudo-fovea. Most patients with unharmonious ARC suppress the target image so as not to experience
diplopia. Others, perhaps those who had a change in the deviation off the pseudo-fovea in late childhood or adulthood, do experience diplopia. Further discussion of unharmonious ARC and
angle of anomaly is located under Amblyoscope, later in this
chapter.
chapter 6: sensory aspects of strabismus
187
A
B
C
FIGURE 6-8A–C. Unharmonious ARC in a patient with esotropia. The
pseudo-fovea (PF) is not in alignment with the retinal image in the deviated eye. (A) Patient perceives uncrossed diplopia or suppresses the image
in the deviated eye. (B) A base-out prism is used to place the image on
the pseudo-fovea (PF). Patient perceives a superimposed single image. A
red filter in front of the right eye causes the image to appear pink, a combination of the clear image (left eye) and the red image (right eye). (C) A
20 PD prism is placed base-out in front of the deviated eye to place the
image on the true fovea (F). Patient now has paradoxical diplopia and sees
the red image on the contralateral side, causing crossed diplopia.
Practically speaking, the differentiation between harmonious versus unharmonious ARC is not of great clinical importance; however, paradoxical diplopia after strabismus surgery is
of clinical concern. Adult patients with long-standing strabis-
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mus should be examined for ARC by neutralizing the deviation
with a prism.
Large Regional Suppression
Children who have large-angle strabismus or severe unilateral
retinal image blur develop a large suppression scotoma to eliminate the image disparity (Fig. 6-9). Patients with large-angle
constant strabismus (e.g., congenital esotropia), will have essentially no binocularity, not even peripheral fusion or ARC. Large
regional suppression, however, is not always constant and can
be intermittent. Patients with large-angle strabismus and large
fusional vergence amplitudes (e.g., intermittent exotropia) have
intermittent strabismus and intermittent regional suppression.
These patients switch from a state of binocular fusion to monocular vision and suppression. Another example of intermittent
large regional suppression is seen in patients with congenital
incomitant strabismus, where the eyes are straight in one field
of gaze (Duane’s syndrome, or congenital superior oblique palsy).
These patients have binocular fusion when their eyes are aligned
with a compensatory face turn, but they suppress when they
look into the field of gaze where they have strabismus. Patients
with intermittent exotropia and Duane’s syndrome that have
developed suppression do not have diplopia when they are
tropic.
Horror Fusionis
Normal sensory and motor fusion, once established, is usually
permanent. Binocular fusion, however, can be lost if severe and
sustained abnormal visual stimulation is acquired. Long-term
occlusion of one eye, especially if it is the dominant eye, can
result in a loss of binocular fusion in some patients. If this loss
of binocular fusion occurs late in visual development or adulthood, the patient will be too old to suppress. The inability to
either fuse or suppress images results in intractable diplopia
and is termed horror fusionis, or acquired disruption of central fusion. Causes of this rare syndrome include a unilateral
acquired cataract occurring in older children and adults.2,4,6 In
these cases, prolonged occlusion caused by a cataract appears to
eliminate binocular fusion and, if the child is too old to suppress, diplopia results. An acquired cataract in the dominant eye
of an adult with previous strabismus or amblyopia can also cause
chapter 6: sensory aspects of strabismus
189
FIGURE 6-9. Worth 4-dot in a patient with large regional suppression of
the right eye. The two dots fall within the suppression scotoma, so the
patient perceives three dots from the left eye.
horror fusionis. In these cases, prolonged occlusion of the dominant eye results in loss of preexisting suppression, leaving the
patient with diplopia. In addition, horror fusionis can be caused
by antisuppression therapy, such as forcing fixation with the
nondominant eye in patients with strabismus. Antisuppression
consists of training the strabismic patient to recognize the
diplopia, which can be done by using dense red filters over the
dominant eye to force fixation to the nondominant eye. Anti-
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suppression is especially dangerous in patients with strabismus
and poor fusion potential.
Prolonged Visual Plasticity
The dogma regarding the relatively short span of visual central
nervous system plasticity has come into question. Veteran strabismologists know that some adult patients with acquired strabismus can eventually learn to ignore or suppress their double
vision. Do these patients actually develop suppression or do they
consciously ignore their diplopia? In a study of acquired strabismus in adults, this author used the pattern visual evoked
potential (VEP) to document suppression of visual cortical
activity in adult patients with acquired strabismus.10 Another
example of prolonged plasticity is seen in adults with amblyopia, who can show significant visual acuity improvement after
losing vision in their good eye.1,7
Sensory Tests
DIPLOPIA TESTS
Diplopia tests use one fixation target seen by both eyes. The
target images fall on both foveas and corresponding retinal
points if the eyes are aligned (Fig. 6-10). If strabismus is present,
the target image falls on the fovea of the fixing eye and an
extrafoveal point in the nonfixing eye (Fig. 6-11). A color filter
is placed over one eye (usually red) or both eyes (usually red for
right eye, green for left eye) to tint the image of each eye. By distinctly tinting the retinal images of each eye, the examiner can
tell which image corresponds to which eye. Lenses that place a
streak of light on the retina (Maddox rod and Bagolini lens) are
also used to stimulate the retina.
Many diplopia tests disrupt fusion by obscuring, or even
eliminating, peripheral fusion clues. Tests that disrupt fusion are
referred to as dissociating tests. Table 6-1 lists different diplopia
tests, with the most dissociating test listed first and the least
dissociating test last. Note that under scotopic conditions tests
that use filters, such as the Worth 4-dot test and red filter test,
become extremely dissociating, because the only images seen
by the patient are the test lights and peripheral fusion clues are
lost.
chapter 6: sensory aspects of strabismus
191
Red Filter Test
Othotropia NRC
Penlight
RE
LE
F
F
L
Center
R
Binocular
Perception
One Pink Light
FIGURE 6-10. Red filter test in a normal patient with straight eye and
normal retinal correspondence. Note that the image from the penlight
falls on both foveas and the patient perceives a single binocular image.
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Red Filter Test
R-Esotropia ARC
Penlight
LE
RE
F
F
P
L
Center
R
Binocular
Perception
One Pink Light
FIGURE 6-11. Red filter test in a patient with a right esotropia and ARC.
Red filter is placed in front of the right eye (RE) and the image falls on
the pseudo-fovea (P) and fovea, representing corresponding retinal points
in a patient with ARC. The patient has a single binocular perception and
sees one pink light. LE, left eye.
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193
TABLE 6-1. Types of Diplopia Tests.
Most dissociating
Maddox rod
Dark red filter
Worth 4-dot with room lights out
Worth 4-dot with room lights on
Least dissociating
Bagolini striated lenses
SPECIFIC DIPLOPIA TESTS
RED FILTER TEST
One of the simplest diplopia tests is the red filter test. Place a
red glass over one eye and direct the patient to fixate on a single
light source, or an accommodative fixation target. Patients
with straight eyes and normal retinal correspondence will see
one pinkish-red light (see Fig. 6-10). If a phoria is present, the
red filter may dissociate the eyes and then the patient will manifest their deviation and see double. The denser the red color,
the more dissociating the test. Another way to make the standard red filter test more dissociating is to turn down the room
lights. In dim illumination, the eye behind the red filter will
only see the light source, not background objects in the room,
which will eliminate peripheral fusion clues. The red filter test
is useful for identifying NRC, ARC, and suppression. Esotropia
with NRC causes uncrossed diplopia, with the red light seen on
the same side as the red filter (see Fig. 6-1). Alternately, exotropia
with NRC is associated with crossed diplopia as the red light is
opposite to the red filter (see Fig. 6-2). When the deviation is
neutralized with a prism, the diplopia disappears and the images
will be superimposed.
Patients with ARC will generally see one light, even though
they have strabismus, because they use a pseudo-fovea. In Figure
6-11, the red light falls on the pseudo-fovea of the right eye. This
image is cortically superimposed with the foveal image of the
left eye to produce the perception of one pink light. If partial or
full prism neutralization of the deviation results in diplopia,
then the patient has ARC.
Strabismus associated with suppression results in the perception of a single light, either a red or a white light, depending
on which eye is fixing. In Figure 6-12, the left eye is fixing, so
the patient sees one white light and suppresses the red light
falling on the right retina. If a dark red filter is placed over the
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Red Filter Test
(Esotropia and Suppression RE)
NRC
Penlight
Red Filter
LE
RE
F
F
Suppression
Scotoma
L
Center
R
Binocular
Perception
LE
One White Light
FIGURE 6-12. Red filter test in a patient with childhood esotropia who
developed suppression and a fixation preference for the left eye. Patient
fixes left eye with a suppression scotoma of the right eye. Note that the
retinal image of the penlight falls within the suppression scotoma, so the
patient only perceives one white light from the left eye.
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195
fixing left eye, then fixation switches to the right eye, and the
left eye is suppressed (Fig. 6-13). Patients who alternate fixation
may report seeing two lights: a red light alternating with a white
light. When a child with a manifest strabismus claims to see two
Red filter over LE
Penlight
Dark red
filter
LE
RE
F
F
Suppression
Scotoma
L
Center
R
Binocular
Perception
RE
One White Light
FIGURE 6-13. A dark red filter is placed over the left eye to shift fixation to the right eye. With the right eye fixing, patient suppresses the
image in the left eye and perceives one white light from the right eye.
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lights, be sure to distinguish between diplopia, where the red
and white lights are seen simultaneously, and alternating suppression, where one light is seen at a time. Partial or full prism
neutralization of the strabismus will not result in diplopia. The
patient with suppression will continue to see just one light.
VERTICAL PRISM RED FILTER TEST/SUPPRESSION
VERSUS ARC
Another way ARC can be distinguished from NRC in patients
with suppression is by placing a red vertical prism (usually 15
PD base-down) over the deviated eye. A vertical prism causes
patients with ARC to see two vertically displaced images, with
the red light directly over the white light (Fig. 6-14). The lights
are vertically aligned because the light in the deviated eye is over
the pseudo-fovea that corresponds to the true fovea of the fixing
eye.
When a vertical prism is introduced to the deviated eye of
a patient with central suppression and NRC, the patient reports
seeing two lights that are horizontally and vertically displaced
because there is no pseudo-fovea and the center of reference is
the true fovea of each eye (Fig. 6-15).
WORTH 4-DOT
The Worth 4-dot test consists of two green lights, one red light,
and one white light (Fig. 6-16). The patient wears red/green
glasses, usually with the red lens over the right eye, and views
a Worth 4-dot flashlight at one-third of a meter, or a Worth 4dot light box at 6 m (20 ft). The near Worth 4-dots are separated
by 6° at near (flashlight at 1/3 m) and by 1.25° for the distance
(light box at 6 m). When the test is performed with the room
lights out, the white dot is the only binocular fusion target, as
it is the only light seen by both eyes. Green lights are seen
through the eye behind the green filter, and the red light is seen
with the eye with the red filter. If the room lights are turned on,
however, the patient can see the room environment with both
eyes, including the Worth flashlight and examiner, thus providing strong fusion clues; this is why Worth 4-dot testing in the
dark is much more dissociating than testing with the room
lights on.
The normal fusion response is seeing four lights, two red
and two green. Another normal response is one red light, two
green lights and one light that flickers between red and green.
The light that flickers is the white light that is seen by both
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Esotropia ARC
Penlight
RE
L-ET
F
P
F
F
Red prism base down
L
Center
R
Binocular
Perception
Vertical Diplopia with
two lights in horizontal alignment
FIGURE 6-14. Patient with esotropia and ARC is presented with a basedown vertical prism and a red filter over the left eye. The prism deflects
the retinal image below the pseudo-fovea (P) and the patient perceives
two images: vertically, one on top of the other. Remember, the pseudofovea (P) is the center of vision during binocular viewing.
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Esotropia NRC Suppression
Penlight
L-ET
RE
ET
F
F
F
Red prism base down
L
Center
R
Binocular
Perception
Vertical and Uncrossed Diplopia
FIGURE 6-15. Patient with esotropia and suppression of left eye. A basedown prism is placed in front of the left eye, which displaces the retinal
image inferiorly and out of the central scotoma. The patient perceives
two images: vertically and horizontally displaced. Note that there is no
pseudo-fovea (F) and the true foveas are at the center of vision.
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199
FIGURE 6-16. Worth 4-dot test in a normal patient with straight eyes.
Three lights are projected to the left eye and two lights to the right eye.
Patient fuses the two images and perceives four lights.
eyes, the flicker being color rivalry. Patients with acquired strabismus and diplopia will see five lights: three green and two red.
Patients with cortical suppression report seeing either three
green lights or two red lights, depending on which eye is fixing.
In Figure 6-9, the left eye is fixing and the right eye is suppressed
so the patient sees three green lights. If the right eye was the
preferred eye and the left eye was suppressed, then the patient
would see two red lights. Patients who alternate fixation usually
describe seeing two red lights, alternating with three green
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lights. A few patients, however, will report the sum total of the
alternating lights, that is, five lights. Thus, alternating suppression can be confused with diplopia, because patients with
diplopia also report seeing five lights. Patients with large scotomas (scotomas greater than 6°) will suppress both the distance
(central field) and near (peripheral field) Worth 4-dot.
Patients with the monofixation syndrome have a small
central suppression scotoma (5°) and peripheral fusion. They
fuse, or see, four lights for the near Worth 4-dot (which subtends
6°) because the dots fall outside the scotoma (Fig. 6-17), but sup-
FIGURE 6-17. Near Worth 4-dot test in a patient with monofixation
syndrome and 8 PD (4°) esotropia. The near Worth 4-dot subtends 6° and
the dots fall outside the scotoma. Patient perceives four dots.
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201
FIGURE 6-18. Distance Worth 4-dot test in a patient with monofixation
syndrome and esotropia of 8 prism diopters. The distance Worth 4-dot
subtends 1.25° and two dots fall within the central suppression scotoma.
Therefore, patient perceives three dots from the left eye and no dots from
the right eye.
press the distance Worth 4-dot (which subtends only 1.25°) as
the dots fall within the scotoma (Fig. 6-18). One of the best uses
of the Worth 4-dot test is to identify the monofixation syndrome
(i.e., central suppression and peripheral fusion) in a patient with
a small-angle strabismus. The results of this test will tell the
examiner if there is peripheral fusion that can be present even
if there is no discernible stereoscopic vision.
Remember, it is important to leave the room lights on when
performing the Worth 4-dot test if the goal is to promote fusion.
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With the room lights on, the patient can see background objects
in the room with both eyes, providing binocular peripheral
fusion clues. If the lights are dimmed or turned off, however,
only the Worth lights can be seen and the only target seen by
both eyes is the single white dot. Because of the lack of peripheral fusion clues, the Worth 4-dot test becomes extremely dissociating in the dark. Once one realizes the dissociating power
of the dark, one can use this phenomenon to estimate how well
a patient fuses. If a patient can maintain fusion of the Worth 4dot test with lights out, then this indicates strong motor fusion.
On the other hand, if dimming the lights changes the response
from fusion to suppression or diplopia, this reveals relatively
weak motor fusion. Patients with intermittent exotropia who
have weak motor fusion manifest their deviation when the
lights are dimmed.
The Worth 4-dot flashlight can be used to plot the size of
suppression scotomas. By moving the flashlight closer to the
patient, the lights subtend a larger angle (i.e., stimulate more
peripheral retina) and by moving the flashlight farther away, the
lights subtend a smaller angle (i.e., stimulate more central
retina). Table 6-2 describes the stimulus angle for the Worth 4dot flashlight at various distances from the patient.
BAGOLINI LENSES
Bagolini striated lenses are clear with a linear scratch through
the center of each lens that provides a streak of light on the
retina when viewing a bright light (see Fig. 6-5). One lens is
placed over each eye, and the lenses are oriented obliquely at
45° and 135°. Because the lenses are otherwise clear, they are
not dissociating. Bagolini lenses, therefore, have the advantage
of providing a free binocular view without dissociation. Patients
with straight eyes and NRC, and those with harmonious ARC,
will report seeing a cross (Fig. 6-19A). Remember, with ARC,
one line is on the true fovea and the other line falls on the
TABLE 6-2. Stimulus Angle for Worth 4-Dot Flashlight.
Flashlight distance from patient
1/6 m
1/3 m (14 in.)
1/2 m
1m
a
Standard near Worth 4-dot.
Worth 4-dot angle
12°
6°a
4°
2°
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203
FIGURE 6-19A–E. Patient perception of Bagolini testing. (A) A cross is
perceived in orthotropia with normal retinal correspondence or strabismus with ARC. (B) Patient with strabismus and large suppression
scotoma sees one line. (C) Patient with monofixation syndrome and small
central scotoma will see one continuous line and one line broken in the
center that corresponds to the eye with the suppression scotoma. (D)
Patient with esotropia and uncrossed diplopia reports a “V” configuration. (E) Patient with exotropia and crossed diplopia reports an “A”
configuration.
pseudo-fovea (see Fig. 6-7). Patients who have large regional
suppression will report seeing only one line (Fig. 6-19B). The
monofixation syndrome, on the other hand, is associated with a
cross, but one line will have a central gap (Figs. 6-19C, 6-5).
Patients with NRC, heterophoria, and diplopia will show the
response of either an “A” or a “V.” Because esotropia is associated with uncrossed diplopia, esotropia will cause the right
line to move to the right and the left line to move to the left,
creating a “V” (Fig. 6-19D). Exotropia produces an “A” because
exotropia is associated with crossed diplopia, with the right
line moving to the left and the left line moving to the right
(Fig. 6-19E).
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MADDOX ROD TEST
The Maddox rod can be used for identifying horizontal, vertical,
and, especially, torsional deviations. The Maddox rod has a
washboard appearance as it is made up of multiple cylindrical
high plus lenses stacked on top of each other. When the patient
views a light through the Maddox rod, a linear streak of light
oriented 90° to the cylindrical ribs of the Maddox rod is seen.
The single Maddox rod test is performed by placing the Maddox
rod over one eye and having the patient view a penlight. The
Maddox rod is aligned so the streak is vertical to detect horizontal deviations and then horizontal for vertical deviations. If
the streak of light passes through the penlight, the patient is
orthophoric, or has harmonious ARC. This is one of the most
dissociating tests, because the images to each eye are totally different and there are essentially no binocular fusion clues. The
Maddox rod test is so dissociating that it will cause patients with
normal bifoveal fusion to manifest their phoria. Because of this,
the Maddox rod test, and dissociating tests in general, do not
distinguish between phorias and tropias. To make the diagnosis
of phoria versus tropia, one must assess the eye alignment
objectively before administering the dissociating diplopia test.
The Maddox rod test can also be used to measure torsion (as
described in Chapter 5).
Haploscopic Tests
In contrast to diplopia tests where there is one stationary fixation target that is viewed by both eyes, haploscopic tests have
two fixation targets, one for each eye, and the targets can be
moved separately to align with each fovea. A haploscopic presentation means each eye receives its own visual stimulus. There
are various ways to separately stimulate each eye. One way to
create haploscopic vision is to place a mirror in front of each
eye, with the mirrors angled so the right eye sees the right temporal side and the left eye sees the left temporal side. Mirror separation of vision is the principle of the amblyoscope. Another
commonly used method is to give the patient color-tinted
glasses with one eye receiving a red filter and the fellow eye a
green filter. Two movable targets are presented on a white
screen: one red and one green. The eye with the red filter sees
only the red target and the eye with the green filter sees only
the green target; thus, separate visual stimuli are presented to
each eye; this is the principle of the Lancaster red/green test. If
chapter 6: sensory aspects of strabismus
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strabismus is present, either the mirrors can be angled or the
red/green targets moved so the fixation target is aligned with
each fovea. Haploscopic tests include the Lancaster Red/Green
Test and the amblyoscope. The Lancaster Red/Green test is used
to measure the angle of strabismus (see Chapter 5; Fig. 5-14).
Note that the Worth 4-dot test is partially haploscopic because
some of the objects in the visual field are seen by both eyes. The
Worth 4-dot test is not a true haploscopic test, as targets are not
independently movable to each eye and cannot be aligned with
each fovea.
AMBLYOSCOPE
The amblyoscope provides a haploscopic view, allowing presentation of images to each eye independently. Two mirrors at the
elbow of the amblyoscope arms reflect images from transparent
picture slides into each eye (Fig. 6-20). The arms can be moved
to measure either subjective or objective angle. The subjective
angle is the amount in degrees the examiner must move the
amblyoscope arms to allow the patient to see the two pictures
FIGURE 6-20. Amblyoscope testing a patient with normal retinal correspondence (NRC) and orthotropia. A dot is a target for the left eye and a
ring is the target for the right eye. Patient sees the dot inside the ring
without moving the arms of the amblyoscope.
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handbook of pediatric strabismus and amblyopia
as being superimposed. The objective angle is measured by alternating the target presentation from right eye to left eye, moving
the arms of the amblyoscope until there is no refixation eye
movement. The objective angle equals the deviation as measured by the alternate prism cover test. The subjective angle is
determined under binocular viewing conditions whereas the
objective angle is measured during monocular viewing.
NORMAL RETINAL CORRESPONDENCE
In a strabismic patient with NRC and diplopia, the subjective
and objective angles are the same (Fig. 6-21) because patients
with NRC always use the fovea as the center of reference.
Patients with NRC and dense large regional suppression will not
have a measurable subjective angle because they suppress one
eye, making subjective superimposition of the images impossible. The subjective angle can be measured in patients with
the monofixation syndrome and a small central suppression
scotoma by using targets that stimulate the peripheral retina.
FIGURE 6-21. Patient with NRC and esotropia. The arms of the
amblyoscope are angled so the image falls on each fovea and the patient
perceives the dot inside the circle. Each arm is moved 20 (10°) for a
total of 40 .
chapter 6: sensory aspects of strabismus
207
FIGURE 6-22. Patient with harmonious ARC and right esotropia. The
arms of the amblyoscope do not have to be angled for the patient to see
the dot inside the ring, as the pseudo-fovea (P) is directly aligned with the
ring target. The patient perceives the dot in the center of the circle with
the arms of the amblyoscope parallel aligned to zero.
ANOMALOUS RETINAL CORRESPONDENCE
(HARMONIOUS)
Patients with strabismus and harmonious ARC have a significant objective angle, but the subjective angle is zero. The subjective angle is zero (or close to zero) because the subjective
angle is measured under binocular conditions and reflects the
alignment based on the relationship between the true fovea of
the fixing eye and the pseudo-fovea of the deviated eye. Because
patients with harmonious ARC have the pseudo-fovea positioned to compensate for the angle of deviation, there is no subjective misalignment. Patients with harmonious ARC will see
the targets from each eye as superimposed with the amblyoscope
arms set to zero (parallel) even though there is a large objective
angle (Fig. 6-22). The objective angle is measured by alternate
cover testing, blocking the vision of each eye (monocular
viewing) so the objective angle reflects the misalignment based
on the true fovea. The displacement of the pseudo-fovea off the
true fovea is called the angle of anomaly. Because the location
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of the pseudo-fovea completely compensates for the objective
deviation in harmonious ARC, the subjective angle is zero, and
the objective angle equals the angle of anomaly. For example, in
Figure 6-22, the objective angle is ET 20 PD and the subjective
angle is zero. The angle of anomaly (i.e., distance of the pseudofovea from the true fovea) is 20 PD (200).
In patients with unharmonious ARC, the pseudo-fovea is
located in a position that does not fully compensate for the
objective deviation. These patients will see double or will suppress the image that does not fall on the pseudo-fovea (Fig. 6-23:
“I” image in right eye). The subjective angle is measured by
moving the arms of the amblyoscope until the two images are
superimposed. When the images are superimposed, the image of
FIGURE 6-23. Patient with unharmonious ARC and 30 PD of esotropia.
The arms of the amblyoscope are set at zero and are not angled. As the
image (I) is falling nasal to the pseudo-fovea (P), the patient perceives
uncrossed diplopia (as diagrammed in the rectangle at the bottom of the
figure). If the arm of the amblyoscope in front of the right eye was moved
10° in to place the image on the pseudo-fovea (P), the patient would perceive the ring around the dot.
chapter 6: sensory aspects of strabismus
209
the fixing eye is on the true fovea, and the image in the nonfixing eye is on the pseudo-fovea. The subjective angle is the
number of degrees from the zero position the amblyoscope arm
needs to move to place the image on the pseudo-fovea. For
example, in Figure 6-23, the subjective angle (I-P, right eye) is 10
PD, and the objective angle (I-F, right eye) is 30 PD. Because the
angle of anomaly (P-F) is equal to the objective angle minus the
subjective angle, the angle of anomaly is 20 PD (3010).
The amblyoscope is a useful tool as it can measure fusional
vergence amplitudes, angle of deviation, area of suppression,
retinal correspondence, and even torsion. Some degree of instrument convergence, however, is usually present when using the
amblyoscope.
AFTERIMAGE TEST
The afterimage test is a fovea-to-fovea sensory test that does not
use a haploscopic apparatus, but each eye is stimulated separately. Each fovea is marked individually during monocular
viewing with a linear strobe light that bleaches the retina; this
causes a linear afterimage shadow through the true fovea that
lasts approximately 10 s. The center of the linear strobe light
is masked to spare the fovea; thus, the afterimage line has a
break in the middle. Testing is performed by having the patient
occlude one eye while the other eye fixates on the central
masked part of the strobe light held vertically in front of the
patient (Fig. 6-24). The fixing eye is stimulated to produce a vertical afterimage. Next, the fellow eye is stimulated with a horizontally oriented strobe light while the first eye is covered (Fig.
6-24B). The occluder is quickly removed, and the patient is asked
where they see the afterimage lines while they are binocularly
viewing (Fig. 6-24C). Because the stimulus is presented under
monocular conditions, the stimulus always marks the true fovea
of each eye unless there is eccentric fixation from dense amblyopia. Patients with NRC will, therefore, always see a cross
whether they are orthophoric, esotropic, exotropic, or hypertropic because their center of reference is the fovea under
monocular or binocular conditions (Fig. 6-25A,B). Patients with
ARC however, use their true fovea during monocular viewing
but, during binocular viewing, the deviated eye switches to the
pseudo-fovea. Consequently, patients with ARC have each fovea
marked by the monocular afterimage, but when binocular vision
is reestablished, the pseudo-fovea takes over as the center of
A
B
C
A
B
C
D
FIGURE 6-25A–D. Perception of afterimage test in patients with (A)
NRC orthotropia, (B) NRC and strabismus, (C) ARC esotropia, and (D)
ARC exotropia. Note that the stimulation for the afterimage test occurs
under monocular conditions and that the light always tags the fovea, even
in patients with ARC. After the stimulation, the patient is again given
binocular vision, so the patient switches back to the pseudo-fovea and
the image tagged on the fovea appears to be in an eccentric location (C
and D).
FIGURE 6-24A–C. Afterimage test of a patient with NRC. If the patient
has NRC, the results of the afterimage test are the same whether the
patient has straight eyes, esotropia (ET), exotropia (XT), or a hyperdeviation. (A) Right eye is stimulated with a vertical strobe while the left eye
is covered. (B) Left eye is stimulated with a horizontal strobe light while
the right eye is covered. (C) The cover is removed and the patient reports
seeing a cross.
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handbook of pediatric strabismus and amblyopia
reference for the deviated eye. As the pseudo-fovea is the center
of reference, the afterimage marked on the true fovea is
perceived as coming from the peripheral visual field. With
esotropia, the fovea is temporal to the pseudo-fovea and temporal retina projects to the opposite hemifield, so the right
afterimage is seen on the left (Fig. 6-25C). Exotropia is just the
opposite, with the fovea nasal to the pseudo-fovea and nasal
retina projecting to the ipsilateral hemifield, so the right
afterimage is seen on the right (Fig. 6-25D).
Other Tests for Suppression and Fusion
VECTOGRAPHIC TEST
The vectographic test is an excellent test for suppression. The
test consists of two superimposed polarized slides of letters that
are projected onto an aluminized screen which reflects the
images while preserving polarization. The patient is asked to
read the letters on the screen while wearing polarized glasses.
The polarization of the glasses and the projected slides are oriented so some of the letters are only seen by the right eye, some
are only seen by the left eye, and some are seen by both eyes
(Fig. 6-26). Patients with normal bifoveal fusion will see all the
letters. If suppression is present, the letters projected only to the
suppressed eye will not be seen (Fig. 6-27). Some patients with
suppression will alternate fixation and will see all the letters,
although viewing them separately.
FOUR BASE-OUT TEST
This test is performed by first placing a 4 PD base-out prism over
one eye. In normal subjects, the 4 base-out test induces fusional
convergence. Remember, there are two movements to prism
convergence: first, a version movement of both eyes in the direction of the apex of the prism, and second, a fusional vergence
movement of the eye without the prism in toward the nose.
With the 4 base-out test, the examiner must look carefully for
the second convergence movement, as it is the sign of fusion.
Patients without motor fusion and large regional suppression
show no movement of either eye when the prism is placed over
the nondominant eye (Fig. 6-28A) and a version (not vergence)
movement of both eyes in the direction of the apex of the prism
when the prism is placed over the fixing eye (Fig. 6-28B).
chapter 6: sensory aspects of strabismus
213
FIGURE 6-26. Diagrammatic representation of vectograph with polarized
glasses in place and lenses oriented 90° to each other. Letters are projected
to a screen through two polarized lenses, which are also oriented 90° to
each other and match the orientation of the glasses. In this patient with
normal binocular vision, the left eye sees AC, right eye sees AB, and the
perception is ABC, which is noted in the rectangle at the bottom of the
figure.
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handbook of pediatric strabismus and amblyopia
FIGURE 6-27. Diagram of vectograph examination of a patient with a
suppression scotoma, left eye. In this case, the patient only sees images
from the right eye and reports seeing an AB.
Patients with the monofixation syndrome and a small
central scotoma usually show no movement when the 4 PD
prism is placed over the nondominant eye. Because these
patients have peripheral fusion, monofixators occasionally show
a normal fusional convergence movement. A prism over the
fixing eye always results in a version movement in monofixa-
chapter 6: sensory aspects of strabismus
215
tors, and some will show fusional convergence movement as
well. Normal patients with bifoveal fusion often show atypical
responses to the 4 base-out test.5 Some normals fail to fuse the
4 PD base-out prism, showing an initial version movement but
no secondary fusional convergence movement. These patients
often alternate fixation and report alternating diplopia. Other
normals seem to ignore the induced phoria and show no move-
A
B
FIGURE 6-28A,B. (A) Esotropia, left eye fixing, right eye deviated with
large suppression scotoma. Placing the 4 base-out prism in front of the
deviated right eye produces no movement of either eye, because the image
falls within the suppression scotoma. (B) Placing the 4 base-out prism in
front of the fixing eye results in a version movement, with both eyes
moving in the direction of the apex of the prism, because there is no suppression scotoma and the movement of the image is perceived.
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ment when the 4 base-out prism is placed over one eye. Thus,
a secondary fusional convergence movement on 4 base-out
prism testing indicates fusion (central fusion or even peripheral
fusion), but because of frequent atypical responses in normals,
absence of a convergence movement does not necessarily mean
an absence of fusion.
References
1. Ellis FD, Schlaegel TF. Unexpected visual recovery: organic amblyopia? Am Orthopt J 1991;31:7.
2. Kushner BJ. Abnormal sensory findings secondary to monocular
cataracts in children and strabismic adults. Am J Ophthalmol 1986;
102(3):349–352.
3. Parks MM. The monofixation syndrome. Trans Am Ophthalmol Soc
1969;1242–1246.
4. Pratt-Johnson JA, Tillson G. Intractable diplopia after vision restoration in unilateral cataract. Am J Ophthalmol 1989;107:23.
5. Romano PE, von Noorden GK. Atypical responses to the four-diopter
prism test. Am J Ophthalmol 1969;67:935.
6. Sharkey JA, Sellar PW. Horror fusionis: a report of five patients. J Am
Optom Assoc 1999;667(12):733–739.
7. Vereecken EP, Brabant P. Prognosis for vision in amblyopia after the
loss of the good eye. Arch Ophthalmol 1984;102:220.
8. Wong AMF, Lueder GT, Burkhalter A, Tychsen L. Anomalous retinal
correspondence: neuroanatomic mechanism in strabismic monkeys
and clinical findings in strabismic children. JAAPOS 2000:168–174.
9. Wright KW, Fox BES, Erikson KJ. P-VEP evidence of true suppression
in adult onset strabismus. J Pediatr Ophthalmol Strabismus 1990;27:
196–201.
10. Wright KW, Hwang JM. Diplopia and strabismus after retinal and
glaucoma surgery. Am Orthopt J 1994;44:26–30.
7
Esodeviations
Kenneth W. Wright
I
n contrast to exodeviations, which are usually acquired and
intermittent, esodeviations often present as a constant
esotropia occurring in infancy or early childhood. Fusional divergence is used to correct for an esodeviation; however, our innate
divergence amplitudes are typically weak, measuring only 6 to
8 prism diopters (PD). It is likely that our weak divergence
amplitudes contribute to the poor control of esodeviation.
Because of the early onset and constant character of esodeviations, they tend to disrupt binocular visual development and are
often associated with amblyopia, poor binocular fusion and
minimal to no stereopsis. Exodeviations, on the other hand, are
characteristically controlled by our strong convergence, highgrade stereoacuity, and amblyopia is rare. It is probable that our
strong innate fusional convergence amplitudes of more than 30
PD allow exodeviations to be better controlled than esodeviations. Not all esotropic patients have a poor prognosis for binocular vision. Patients with late-onset acquired or intermittent
esotropia usually have binocular fusion potential. The duration
of the esotropia is an important factor that determines binocular fusion potential.40 Esodeviations can be classified into the
categories outlined in Table 7-1.
CONGENITAL–INFANTILE ESOTROPIA
Definition and Incidence
Infantile esotropia, or, as it is often termed, congenital esotropia,
is classically defined as a large-angle esotropia that is present
before 6 months of age (Fig. 7-1). Congenital esotropia is less
common than the 1% reported in many texts. Mohoney et al.45
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handbook of pediatric strabismus and amblyopia
TABLE 7-1. Types of Esotropia.
Congenital-infantile esotropia (uncommon)
Accommodative esotropia (common)
Acquired nonaccommodative esotropia (uncommon)
Esotropia nystagmus face turn (uncommon)
Cyclic esotropia (rare)
Esophoria (common)
Divergence insufficiency (uncommon)
Sensory esotropia (common)
reported a birth prevalence of 27 per 10,000 live births, and
Archer et al.2 estimated the incidence of esotropia to be 0.5% in
a study of 582 infants.
Normal Neonatal Alignment
It is well known that newborns usually do not have straight
eyes. A large population study64 documented that 30% of normal
neonates have straight eyes, 70% have a transient exotropia or
a variable angle strabismus, and less than 1% have esotropia. In
that study, only 2 of 2271 neonates had an esotropia at birth and,
in both cases, the esotropia resolved by 2 months of age.2 This
FIGURE 7-1. Four-month-old with the classic large-angle esotropia characteristic of infantile esotropia. The right eye is fixing; the left eye is
deviated.
chapter 7: esodeviations
219
important study indicates that esotropia infrequently occurs at
birth, whereas exodeviations are common.
Etiology
Esotropia occurring in infancy can be caused by a variety of disorders including congenital fibrosis of the extraocular muscles,
Duane’s syndrome, and infantile myasthenia gravis (Table 7-2).
In most of the ophthalmology literature, these rare secondary
causes of esotropia are not included under the category of infantile esotropia. The etiology of primary infantile esotropia is a
source of controversy and remains unknown. Costenbader
suggested that hypermetropia with overconvergence plays an
important role.19 Historically, there have been two basic theories for the cause of congenital esotropia and the poor binocular
sensory outcomes after treatment: the Worth theory and
Chavasse theory.
The Worth theory states that the esotropia is caused by a
congenital absence of cortical fusion potential. This theory
places the blame on a primary cortical fusion deficit present at
birth and states there is no hope for obtaining good binocular
function.
The Chavasse theory contends that congenital esotropia
represents a primary motor misalignment, and the poor binocular sensory status so often seen in these patients is secondary
to a disruption of binocular visual development caused by
the infantile strabismus. Chavasse supporters speculate that
patients with congenital esotropia have binocular cortical potential for high-grade stereopsis and fusion but that the presence of
an esotropia during the early period of binocular visual development permanently damages binocular function.
TABLE 7-2. Differential Diagnosis of Infantile Esotropia.
Pseudo-esotropia
Congenital esotropia
Infantile accommodative esotropia
Duane’s syndrome
Sensory esotropia
Congenital sixth nerve palsy, usually transient
Möbius syndrome
Congenital fibrosis syndrome
Infantile myasthenia gravis
Neurological disease
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handbook of pediatric strabismus and amblyopia
It is likely that infantile esotropia represents a heterogeneous syndrome composed of a variety of different sensory and
motor abnormalities. Factors such as early weakness of the
lateral rectus muscle, hypermetropia causing accommodative
convergence, abnormalities of muscle anatomy, and lack or
immaturity of cortical fusion may independently or collectively
predispose to the development of esotropia.
One possible cause for esotropia may relate to immaturity
of sixth nerve function. The sixth and fourth cranial nerves are
the longest nerves that innervate the extraocular muscles and
are the last to fully myelinate. Perhaps there is a relative delay
in sixth nerve maturation compared to the third nerve, which
myelinates first. A relative sixth nerve palsy occurring at birth
or in the neonatal period might cause the medial rectus muscle
to be unopposed, resulting in infantile esotropia. It is interesting to note that inferior oblique overaction frequently occurs in
patients with infantile esotropia. Inferior oblique overaction
may represent an early superior oblique paresis resulting from
the long fourth nerve and delay in functional maturation.
Whatever the cause or causes of infantile esotropia, there
are compelling basic science and clinical studies indicating that
esotropia occurring during the developmental period can permanently damage binocular vision. In addition, many infants
with esotropia have the cortical potential for binocular
fusion.7,21,33,37,71 These two important principles provide the basis
for our treatment strategy.
Differential Diagnosis of Infantile Esotropia
The differential diagnosis of infantile esotropia includes Duane’s
syndrome, congenital fibrosis syndrome, congenital sixth nerve
palsy (Möbius syndrome associated with sixth nerve paresis),
and infantile myasthenia gravis. These disorders all have limited
abduction and, therefore, can be differentiated from infantile
esotropia where the ductions should be full. This differentiation
may be difficult in patients with large-angle infantile esotropia
and tight medial rectus muscles. Even in these patients,
however, vestibular stimulation by doll’s head maneuver reveals
full ductions and good abduction saccades.
Other diagnoses include pseudo-esotropia secondary to large
epicanthal folds and infantile accommodative esotropia. Infantile accommodative esotropia may be difficult to distinguish
from infantile esotropia. The key to the diagnosis of infantile
chapter 7: esodeviations
221
accommodative esotropia is the presence of straight eyes for
several months, followed by a variable small-angle esodeviation
associated with hypermetropia of 3.00 or more. (See Infantile
Accommodative Esotropia later in this chapter.)
Clinical Features
Infantile esotropia is characterized by a large-angle esotropia presenting from birth to 6 months of age (see Fig. 7-1). There may
be a history of the angle of deviation increasing during the first
few months of life.37 There is often some limitation of abduction to voluntary version testing; however, doll’s head maneuver and abduction saccades reveal normal lateral rectus
function. The majority of children will be in good health otherwise, but there are some systemic associations that are well
known.
Onset
The age of onset of infantile esotropia and whether it is truly
congenital or acquired has been controversial. Nixon et al.
reported no cases of constant esotropia among 1219 newborns,
indirectly suggesting that onset in many cases is postnatal.49 In
contrast, the Congenital Esotropia Observational Study (CEOS)
multicenter study sponsored by the NIH (this author was study
chairman) found that 43% of large-angle infantile esotropia
cases were reported by the parent or guardian to have occurred
at birth, whereas 23% were first noted after the first month of
life.51 In a study of 3324 newborns, Archer et al.2 found three
cases documented to have straight eyes at birth, later acquiring
esotropia at 2 to 4 months of age. In summary, it seems that the
onset of the esotropia is variable, with some cases being truly
congenital while others are acquired, even several months after
birth.
Character of the Esotropia
Infantile esotropia has been classically described as a large-angle
constant esotropia. For the most part, this has been based on
retrospective case series of patients who had undergone strabismus surgery.28,31,48 The CEOS51 also showed that esotropia
occurring in the first few months of life is often small to moderate in size and is frequently variable or intermittent. In this
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multicenter study of 2- to 3-month-old infants with esotropia,
56% of patients were characterized as having a constant
esotropia, 25% a variable deviation, and 19% had an intermittent esotropia. Only half had a deviation measured to be 40 PD
or greater. Larger deviations tended to be constant, whereas the
majority of the smaller-angle deviations were intermittent or
variable.
Spontaneous Resolution of Esotropia
Until the data from the CEOS collaborative group52 became
available, there was limited information on spontaneous resolution of early-onset esotropia. Birch et al.5 prospectively followed 80 infants with esotropia who were first seen at 2 to 4
months of age. Resolution without surgery occurred at 6 months
of age in 3 of 8 patients whose initial deviation was intermittent or variable, 3 of 23 patients with a constant esotropia of 35
PD or less (2 of whom were given spectacle correction for hypermetropia), and 0 of 49 with a constant esotropia of 40 PD or
more. Clarke and Noel16 described 3 cases of constant esotropia
diagnosed by 6 months of age that spontaneously decreased to
less than 10 PD after 1 year of age but retained persistent signs
of abnormal motor development including dissociated vertical
deviation and latent nystagmus. Friedrich and de Decker27
described 1 case of a transient variable large-angle esotropia and
6 cases of small- to moderate-angle, mostly intermittent,
esotropia first noted between 1 and 3 months, of age, that spontaneously resolved.
The findings of CEOS provide the best data on spontaneous
resolution of infantile esotropia.52 This multicenter prospective
study found of 170 patients, 46 (27%) spontaneously resolved to
within 8 PD of orthotropia at the outcome exam either with or
without spectacle correction. Patients with a small angle () 40
PD, and intermittent esotropia had a 50% to 78% rate of spontaneous resolution. In contrast only 2 of (3%) 64 patients with
a constant esotropia of 40 PD or more on both the baseline and
first follow-up exam and with a refractive error of 3.00 diopters
or less, the esotropia resolved at the outcome exam. One patient
had a persistent 40 PD esotropia at the outcome exam; however,
the esotropia improved without treatment to ET 5 PD. The conclusion of CEOS was that early-onset esotropia frequently
resolves if the esotropia is less than 40 PD and is intermittent
or variable. If the esotropia is constant or greater than 40 PD pre-
chapter 7: esodeviations
223
senting on 2 exams with less than 3.00 D refractive error, then
the likelihood of spontaneous resolution is remote.
Ing37 reported that in 41 cases of esotropia seen at an average
age of 6 months, the esotropia increased between the first examination and the time of surgery by 10 PD or more in 61% and
did not decrease by 10 PD or more in any patients. Because this
was a retrospective study of patients who had undergone strabismus surgery, there might have been a selection bias for
patients with an increasing esotropia.
Thus, spontaneous resolution of infantile esotropia does
occur, especially if the deviation is small, variable, or intermittent. However, infants with a constant deviation of 40 PD or
more on two exams and with less than 3.00 D of hyperopia
have a low likelihood of spontaneous resolution and can be considered for early surgery.
Amblyopia Associated with Infantile Esotropia
The ability to alternate fixation, or hold fixation well with either
eye, indicates equal vision (Fig. 7-2).72 Strong fixation preference,
on the other hand, indicates amblyopia of the nonpreferred eye,
and should be treated by patching the preferred eye before strabismus surgery.72 The incidence of amblyopia seems to be proportional to the duration of the esotropia. In the CEOS,51
amblyopia was diagnosed in 19% of patients at the first visit (2
months of age) and doubled to 42% at subsequent visits (after 6
months of age). This frequency is similar to the 22% rate
reported by Hiles et al.31 and to the 13% rate reported by Hoyt
et al.32 for patients examined before 1 year of age. Higher rates
of amblyopia (41%–72%) have been reported in postsurgical case
series extending over many years of follow-up.19,59 Some have
blamed surgery for causing amblyopia because the rates of
amblyopia were higher in the postsurgery patients. It is more
likely, however, that this higher rate of amblyopia reflects the
higher incidence of amblyopia having a longer duration of
esotropia.
Refractive Error
Costenbader found that more than half of 500 children with congenital esotropia had significant hypermetropia ranging from
2.25 to over 5.00.19 The CEOS showed that mild to moderate hypermetropia was present in most patients, with about 20%
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 7-2A,B. Patient with infantile esotropia and alternating fixation,
no amblyopia. (A) Patient is fixing with the right eye. (B) Patient is fixing
with the left eye.
being above 3.00 D, 12% above 4.00 D, and less than 10%
being myopic.51 Similar results have been reported in other
infantile esotropia series, as Birch et al.8 found 17% of cases and
Ing39 found 25% of cases with hyperopia of 3.00 or more. In a
chapter 7: esodeviations
225
31
series by Hiles et al. on older children, hyperopia greater than
3.00 D was present in 15% of the 54 cases.
Mutti et al.47 reported similar incidence of refractive errors
in a study of 288 normal 3-month-old infants with a mean refractive error of 2.10 1.3 D; 21% were greater than 3.00 D, 8%
were greater than 4.00 D, and 3% had myopia of 0.50 D or
greater. It seems, from a review of the literature, that infants
with esotropia have, on average, refractive errors similar to the
normal age-matched population. There are selected patients,
however, with moderate to high hypermetropia who appear to
have esotropia on the basis of accommodative convergence.
Associated Motor Abnormalities
The classic triad of motor abnormalities associated with congenital esotropia is inferior oblique overaction, dissociated
vertical deviation (DVD), and latent nystagmus.36 These three
associated findings may occur individually or in any combination and usually become manifest some time after 1 year of age.68
CEOS found inferior oblique overaction and DVD to be almost
nonexistent at the initial exam at approximately 2 months of
age.51 Eight percent (8%) of patients had inferior oblique overaction and 4% had DVD at 6 months of age.51 Hiles et al.31
reported the rate of 15% for inferior oblique overaction and 2%
for DVD between 3 and 10 months of age, but both increased
to approximately 75% at long-term follow-up examinations.
(See Chapter 9 for a discussion of inferior oblique overaction
and Chapter 10 for DVD.) Latent nystagmus occurs less frequently than inferior oblique overaction or DVD. CEOS51 found
only a 4% frequency at 6 months of age, and Robb and Rodier59
reported a frequency of 16%. Smooth pursuit asymmetry is
another motor finding present in virtually all patients with
infantile esotropia (see Chapter 4, p. 158).1,65 Smooth pursuit
asymmetry is a marker of early disruption of binocular visual
development.
LATENT NYSTAGMUS
Latent nystagmus is a bilateral nystagmus that becomes manifest when one eye is occluded, or the eyes are dissociated by blurring the vision of one eye, or by suppression of one eye associated
with manifest strabismus; this is a jerk-type nystagmus with the
fast phase toward the fixing eye. Velocity recordings show that
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the velocity of the slow phase decreases toward the end of the
slow-phase eye movement (decreasing velocity slow phase).23
Latent nystagmus is also associated with conditions that disrupt
early binocular visual development, such as congenital monocular cataracts.
Systemic Associations
In most cases, congenital esotropia occurs as an isolated problem
in an otherwise healthy child; however, it can be associated with
systemic diseases such as Down’s syndrome, albinism, and cerebral palsy. The differential diagnosis of esotropia occurring in
infancy includes Möbius syndrome, congenital fibrosis syndrome, Duane’s syndrome, infantile myasthenia gravis, and congenital sixth nerve palsy. Congenital sixth nerve palsy is rare
and usually spontaneously resolves over a few weeks. Neurological processes such as hydrocephalus and intracranial tumors
can present as an infantile esotropia. Most clinical studies on
congenital esotropia exclude patients with neurological or systemic disease. Thus, congenital esotropia is usually defined as a
primary esotropia not associated with a sixth nerve palsy, a neurological condition, or a significant restriction, and occurs before
6 months of age.
Clinical Assessment
Evaluation should start with amblyopia assessment, usually by
fixation preference. Assessment of ductions and versions are
important to diagnoses an abduction deficit possibly related to
a sixth nerve palsy or oblique dysfunction. Patients with infantile esotropia often show some limitation of abduction. In these
cases, it is important to verify the abduction deficit by vestibular stimulation with the doll’s head maneuver or by spinning the
infant. Vestibular stimulation is best performed in infants by
gently spinning the child (Fig. 7-3). Many children who show an
abduction deficit to voluntary abduction will have full abductions by vestibular stimulation. If an abduction deficit persists,
assess lateral rectus function by examining the abduction
saccade. If there is a brisk abduction saccade, then the lateral
rectus is functioning and the limited abduction is restrictive,
probably secondary to a tight medial rectus muscle. A slow or
absent abduction saccade indicates a weak lateral rectus, possibly caused by a sixth nerve palsy or a Duane’s syndrome. Opto-
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FIGURE 7-3. Diagram of an infant in examiner’s hands. Infant is moved
to the right, which stimulates eye movement to the left. If the right eye
fully abducts, then lateral rectus function is normal and there is no significant restriction of the medial rectus muscle. Spinning an infant will
cause the eyes to move opposite to the spin, an excellent way to examine
horizontal ductions in an otherwise uncooperative infant.
kinetic stimulation (OKN drum or tape) is a good way to stimulate saccadic eye movements.69 The angle of deviation is measured by cover/uncover testing or with Krimsky light reflex, and
near and distance measurements should be obtained if possible.
A cycloplegic refraction and a dilated fundus exam are also
indicated.
Inheritance
The inheritance of congenital esotropia remains undefined;
however, it is well known that it runs in families.44,45,55 Affected
family members may have congenital esotropia, but other types
of strabismus are often found, including accommodative
esotropia and congenital superior oblique palsy. Maumenee
et al.,44 in an analysis of a large group of families, concluded that
the inheritance is consistent with a Mendelian codominant
model in which there is an admixture of primarily autosomal
recessive cases, some dominant cases, and possibly nongenetic
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cases. Variable patterns of inheritance for infantile esotropia
speak to the heterogeneity of this syndrome. In CEOS,52 a family
history of strabismus was reported for 45% of patients, with 29%
having a family history in a first-degree relative, according to
parental report. Similarly, a study by Mohoney et al.45 found a
family history of strabismus in 34% of cases of early-onset
esotropia compared with this history in 12% of matched controls, and Shauly et al.61 reported 44% of patients who had a
history of strabismus. These studies, however, do not distinguish
between early-onset esotropia and other forms of strabismus.
Types of Infantile Esotropia
PSEUDO-ESOTROPIA
Pseudo-esotropia is a condition in which the eyes are orthotropic
but appear to be crossed; this usually occurs in infants who have
a wide nasal bridge with prominent epicanthal folds (Fig. 7-4).
Pseudo-esotropia usually resolves by 2 or 3 years of age because
the epicanthal folds diminish as the bridge of the nose enlarges.
Patients with a small interpupillary distance may also appear to
be esotropic, especially when the eyes are in sidegaze or are
focusing at near. Often, parents bring photographs that show the
child’s eye “turned in.” Close examination of these photographs
often reveals that the photograph was taken with the child’s
head turned and the eyes in sidegaze. The eye that is turned
nasally is buried under the epicanthal fold. Children with
pseudo-strabismus should have a full ocular examination. It is
important to follow these children, as a small percentage will
end up having a true esodeviation.
INFANTILE ACCOMMODATIVE ESOTROPIA
Accommodative esotropia can occur in babies as young as 2
months of age and are often classified under the diagnosis of
“congenital esotropia.” These infants should be immediately
treated with their full hypermetropic correction (see Infantile
Accommodative Esotropia later in this chapter).
CIANCIA’S SYNDROME
Ciancia’s syndrome is a large-angle congenital esotropia with
cross-fixation, and both eyes appear to be “stuck” in toward the
nose. It consists of the following characteristics: (1) large-angle
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A
B
FIGURE 7-4A,B. Pseudo-strabismus. (A) Note the large epicanthal folds
giving the appearance of esotropia even though the eyes are well aligned.
(B) Pinching the epicanthal skin folds demonstrates the eyes are well
aligned.
deviation (60 PD), (2) bilateral limited abduction with intact
abduction saccades, (3) fixing eye in adduction, (4) nystagmus on
attempted abduction with no nystagmus in adduction, and (5)
face turn to the side of the fixing eye (Fig. 7-5). In Ciancia’s
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A
B
FIGURE 7-5A,B. Patient has Ciancia’s syndrome with bilateral tight
medial rectus muscles causing a large-angle esotropia and limited abduction. The patient is most comfortable with the fixing eye in adduction.
To establish this, the patient adopts a face turn toward the fixing eye,
thus placing the fixing eye in adduction. In (A), the patient is fixing the
right eye, with face turn to the right; in (B), patient is fixing the left eye
and has a face turn to the left. This patient with Ciancia’s syndrome is
showing a pattern of cross-fixation.
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231
syndrome, the abduction deficit is most likely secondary to tight
medial rectus muscles. Clinical examination shows good lateral
rectus function, evidenced by normal brisk abduction saccades.
Forced duction at the time of surgery shows moderately tight
medial rectus muscles. The abduction nystagmus is a subtle jerk
nystagmus with the fast phase in the direction of the fixing eye
and only occurs when the fixing eye abducts. This nystagmus
probably represents an exaggerated endpoint nystagmus, as the
lateral rectus muscle pulls against the tight medial rectus
muscles. Ciancia found that approximately one-third of his
patients with congenital esotropia had this syndrome.15 It is
likely that many of the patients described by Ciancia would have
been classified in the American literature as large-angle congenital esotropia with cross-fixation. The reason for the face turn
in these patients with a large-angle esotropia, and the fixing eye
in adduction is probably not to damp the nystagmus, as the nystagmus is usually minimal if present at all; the face turn is
adopted because the medial rectus is tight and holds the fixing
eye in adduction.
Surgically correcting the esotropia associated with Ciancia’s
syndrome is difficult, as undercorrections are frequent. One of
the problems is measuring the full deviation, as both eyes are
“stuck” in adduction and it is difficult to get the fixing eye into
primary position for a true measurement. The surgery of choice
is large medial rectus recessions, approximately 7 mm posterior
to the insertion site.57
CROSS-FIXATION
Patients with limited abduction and tight medial rectus muscles
adopt a face turn to fixate with an eye in adduction; probably
the same syndrome described by Ciancia (see Ciancia Syndrome
above). These patients may cross-fixate, fixing with the right eye
for objects in the left visual field and fixing with the left eye for
objects in the right visual field. Cross-fixation was once seen as
a sign of equal vision, but Dickey et al.24 reported that crossfixators can have mild amblyopia. Patients have true equal
vision if they can hold fixation with either eye through smooth
pursuit, without refixating to the fellow eye.
CONGENITAL FIBROSIS SYNDROME
This syndrome is a congenital restrictive strabismus, often
inherited as an autosomal dominant trait (see Chapter 10). Con-
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genital fibrosis syndrome may cause virtually any horizontal or
vertical strabismus and is associated with extremely tight
fibrotic rectus muscles on forced duction testing. It frequently
presents as a large-angle congenital esotropia with severe limitation of abduction of one or both eyes; this has also been termed
strabismus fixus. Even though abduction is severely restricted,
OKN stimulus or the doll’s head maneuver will show abduction
saccadic eye movements of brisk, albeit small, amplitudes, indicating intact lateral rectus function.
Treatment of Congenital Esotropia
The treatment of congenital esotropia (ET) is usually surgical.
Occasionally, infants with esotropia may be corrected with
hypermetropic spectacle correction. Spectacles should be tried
in small-angle cases (ET 40) if hypermetropia is 2.00 or
greater and in patients with large-angle esotropia (
40 PD) if the
hypermetropic correction is 3.00 or more. Birch et al.8 reported
that 3 of 84 infants with esotropia of at least 30 PD seen at 2 to
4 months of age achieved alignment with spectacle correction
and required no surgery.
It is important to fully treat amblyopia before performing
surgery, with the endpoint of patching being “holds fixation
well” with either eye by fixation preference testing. If the child
is cosmetically straightened by the surgery, the parents may consider that the problem is cured and they may not return for
amblyopia treatment. The only situation when surgery is indicated in the face of residual amblyopia is a tight medial rectus
muscle that causes one eye to be buried in the medial canthus
even when the good eye is patched as this blocks the vision of
the amblyopic eye and makes effective amblyopia therapy
impossible. This unusual problem most frequently occurs in
association with strabismus fixus of congenital fibrosis syndrome or, rarely, Ciancia’s syndrome.
The standard surgical approach is bilateral medial rectus
recessions using the standard surgical charts (see endpapers).
The amount of recession is usually based on the near deviation
as it is difficult to obtain accurate distance measurements in
infants. In young infants with fusion potential, a small postoperative exodeviation is probably desirable to allow fusional
convergence to align the eyes.60 In older patients with irreversible significant amblyopia, limit surgery to the amblyopic
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eye by performing a recession of the medial rectus muscle and
a resection of the lateral rectus muscle.
PROGNOSIS AND TIMING OF SURGERY
There are few long-term outcome studies on congenital
esotropia and these are retrospective.30,31,61 Historically, alignment and sensory outcomes for patients have been poor using
the standard approach of operating late between 6 months to 2
years of age. Except for rare cases, the best results with standard
surgery have been monofixation with peripheral fusion and only
gross stereopsis. Monofixation and peripheral fusion, however,
do not guarantee long-term stability, as many patients will lose
binocular fusion over time.3,63
There is growing evidence that outcomes from surgery for
infantile esotropia can be improved by early intervention to
align the eyes as soon the diagnosis is firmly established, even
operating before 6 months of age. The best time to operate on
infantile esotropia remains controversial.11,17,30,62,71
At the time of this printing, this author suggests operating
for infantile esotropia as early as 12 to 13 weeks of age, so long
as the esotropia is a constant tropia greater than 40 PD and there
have been two examinations (3–4 weeks apart) documenting
that the deviation is stable or increasing. Infants with small to
moderate deviations, intermittent deviations, or variable-angle
esotropia are observed until 6 months of age or longer. CEOS
data show that these patients have a significant rate of spontaneous resolution. In infants under 5 months of age, this author
performs bilateral medial rectus recessions using the standard
tables, with a maximum recession of 6.0 to 6.5 mm posterior to
the medial rectus muscle insertion.
RATIONALE FOR EARLY SURGERY
The rationale for performing early surgery for infantile esotropia
is derived from basic science research and clinical studies. Hubel
and Wiesel were among the first to show that strabismus occurring during the early period of visual development causes permanent loss of binocular cortical cells and disruption of
binocular visual development.33 Studies by Crawford and von
Noorden21,22 and Crawford et al.20 have shown that as little as 3
weeks of prism-induced esotropia will cause permanent loss of
binocular cells and stereopsis in infant monkeys. Importantly,
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A
B
FIGURE 7-6A,B. Chart from the study by Crawford and von Noorden21,22
shows the results of prism-induced esotropia in infant monkeys. Column
A shows the normal distribution of occipital cortex with the largest spike
in the center representing binocular cells (B) and fewer monocular cells
(R, right eye; L, left eye). Columns B through E represent the cortical cell
distribution after increasing duration of prism-induced esotropia. Note
that after only 20 days of prism-induced esotropia (column C), almost all
the binocular cortical cells are gone and there is a corresponding increase
in monocular cells. Column F plots the binocular cell loss over time from
prism-induced esotropia and shows an inverse relationship, with longer
duration of esotropia corresponding to fewer binocular cells.
loss of binocular cells after brief periods of prism-induced
esotropia persisted after removing the prisms, even after allowing up to 3 years for recovery. These studies also demonstrated
that the loss of binocularity is directly proportional to the duration of the esotropia (Fig. 7-6).
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In humans, the critical period for the development of binocular vision appears to be the first 3 to 4 months of life.6,12,25,41,71
Stereopsis develops rapidly and is nearly completed in
infancy.6,41,53 Birch and Stager10 have demonstrated that, by 5
months of age, about 40% of esotropes corrected with prisms
had stereopsis, similar to that found in infants of this age with
normal visual development. After 5 months of age, only about
20% of the early-onset esotropes demonstrated stereopsis, in
contrast to 100% of normal infants. The timetable for the development of binocular fusion may be even earlier, as this author
has personally seen compensatory head posturing and a gaze
preference associated with incomitant strabismus in infants as
young as 3 weeks, thus indicating the presence of binocular
fusion. It is likely that stereoacuity improved with increasing
visual experience as visual acuity improved.
Clinical studies clearly indicate that early surgery before 1
to 2 years of age is critical to obtaining some binocular fusion,
at least peripheral fusion. Ing,35 in a landmark article, demonstrated the importance of early surgery, reporting that approximately 80% of congenital esotropic patients achieved peripheral
fusion if aligned before 2 years of age. In contrast, patients
aligned after 2 years of age had less than 20% chance of obtaining any fusion. In addition to being a consummate clinician scientist, Dr. Ing is a champion surfer (Fig. 7-7).
More recent studies indicate that surgery performed before
1 year of age results in even better binocular function and estab-
FIGURE 7-7. Photograph of Dr. Malcolm Ing surfing at his home in
Hawaii with Diamond Head in the background. Dr. Ing’s landmark work
on early surgery for congenital esotropia has made a tremendous improvement in the care of our patients.
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handbook of pediatric strabismus and amblyopia
lishes random dot stereoacuity.40,50,99 Very early surgery, that is,
before 6 months of age, remains controversial, but it appears
to be safe and may provide the best sensory outcomes.30,71
Helveston et al.30 reported results on 10 infants operated for
infantile esotropia between 12 and 23 weeks of age. All achieved
a final alignment within 10 PD of orthotropia, although many
required reoperation, as the follow-up was as long as 10 years.
Four patients obtained stereoacuity, 1 with 140 s arc. In 1994,
this author reported results of very early surgery on 7 infants
operated between 13 and 19 weeks of age with a follow-up of 2
to 8 years (mean, 4.1 years). All had excellent alignment at the
final visit with a tropia of 8 PD or less. Five of the 7 required
only one operation to obtain good alignment, and 2 required one
reoperation. Five children could cooperate with stereo testing at
the outcome examination and all 5 showed stereoacuity ranging
from 400 to 40 s arc. Three children achieved high-grade
stereoacuity by random dot testing and 2 had 40 s arc. Figures
7-8 and 7-9 show pre- and postoperative photographs of the two
patients who obtained 40 s arc stereoacuity after very early
surgery.
The basic science data and clinical studies suggest that
many patients with infantile esotropia do have the potential for
A
FIGURE 7-8A. Early surgery for congenital esotropia patient. (A) Photograph of 1-week-old infant with congenital esotropia. Patient’s grandfather is a physician and noted esotropia at birth.
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B
C
FIGURE 7-8B–C. (B) Surgery was performed at 13 weeks of age. Photograph taken 1 day after bilateral medial rectus recessions, 6.0 mm,
showing consecutive exotropia. The exotropia was intermittent and
resolved a few days after surgery. (C) Same patient at 5 years of age. Early
surgery resulted in excellent alignment with best binocular sensory result
ever reported. The patient has now been followed for more than 7 years
with straight eyes, no dissociated vertical deviation, no latent nystagmus,
and no inferior oblique overaction; fusion of Worth 4-dot in the distance
and near, 40 s of stereo by Titmus testing, and Randot stereopsis. The
only binocular functional defect is trace optokinetic nystagmus (OKN)
asymmetry seen only by electro-oculogram (EOG) recording; no OKN
asymmetry is seen clinically.
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 7-9A–B. Early surgery for congenital esotropia patient. (A) Preoperative photograph of patient with infantile esotropia at 19 weeks of
age. (B) Postoperative day 1 with a consecutive exotropia; this was intermittent and lasted only a day or two.
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239
C
D
FIGURE 7-9C–D. (C) Photograph taken at age 8 years. Patient had 40 s
stereoacuity, with slight intermittent exotropia. One year later, patient
underwent bilateral lateral rectus recessions for an exotropia. (D) At a
recent follow-up visit at 14 years of age, patient maintains excellent
alignment and 40 s stereoacuity after early surgery for infantile esotropia.
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stereopsis if surgically aligned early, prior to 1 year of age. In
addition, very early surgery, before 6 months and even as young
as 3 months of age, appears to be safe and may be of critical
importance for establishing a high level of binocular fusion and
stereopsis. It is likely that an important factor is to reduce the
duration of the esotropia.
GOOD STEREOPSIS WITH LATE SURGERY
As already described, basic science research in nonhuman primates has demonstrated that brief periods of strabismus (as little
as 3–4 weeks) during the neonatal period will permanently
disrupt binocular function. Despite these studies, there have
been sporadic cases of infantile esotropia that demonstrated
stereoacuity following “late” surgery, even in adulthood (Fig.
7-10).45 In fact, two patients in Ing’s 1981 study35 achieved 40 s
arc stereoacuity even though the eyes were surgically aligned
after 1 year of age. It is likely that some infants who are classified as having early-onset esotropia actually have straight eyes
or intermittent esotropia during the first few months of life,
probably establishing binocular cortical cells needed for fusion.
Perhaps, once established in early infancy, binocularity may
be reestablished later in life when the eyes are aligned after
strabismus surgery. Because some patients with presumed
congenital-onset esotropia achieve binocular fusion after late
surgery, we should not categorically assume an older patient
with esotropia does not have fusion potential.
POSTOPERATIVE CARE
All patients with congenital esotropia should be followed closely
for amblyopia, even if good motor alignment is achieved. The
goal of surgery is to obtain alignment within 8 to 10 PD of
orthotropia to allow for the establishment of peripheral fusion
and the monofixation syndrome. Deviations larger than 10 PD
preclude the development of even peripheral fusion. Postoperative tropias greater than 10 PD should be treated with either
further surgery or spectacle correction.
Consecutive Exotropia
An initial small-angle exotropia is probably desirable in infants
young enough to have fusion potential; however, a persistent
exotropia 4 to 6 weeks after surgery may require additional
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241
A
B
FIGURE 7-10A,B. (A) Preoperative photograph of teenager with a largeangle esotropia that mother thinks was present since birth. Patient had
no previous surgery. (B) Postoperatively after bilateral medial rectus recessions, the patient achieved excellent alignment, and peripheral fusion
with gross stereoacuity. Old records revealed the patient to be hypermetropic, and the patient probably had an intermittent esotropia acquired during late infancy. If fusion is established in infancy, it is often
retrievable later, in contrast to a constant congenital esotropia, which
has a poor prognosis for fusion if alignment is delayed.
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60,70
surgery.
If the consecutive exotropia increases in sidegaze or
is associated with an adduction deficit, consider the possibility
of a slipped muscle or stretched scar. Explore the medial rectus
muscles if there is a question of muscle stability, as a stretched
scar or slipped medial rectus muscle is fairly common. For
the advancement procedure, this author now prefers a nonabsorbable suture or a long-lasting absorbable suture. The treatment of choice for a consecutive exotropia without a slipped
muscle is bilateral lateral rectus recessions.
Residual Esotropia
A residual esotropia greater than 10 to 15 PD that persists longer
than 6 to 8 weeks after surgery should be treated. The first line
of treatment is to give the full hypermetropic spectacle correction if the cycloplegic refraction is 1.50 or more. If there continues to be a significant esotropia after glasses are prescribed or
there is not enough hypermetropia to warrant glasses, then
surgery should be considered, especially if the child is under
2 years of age and there is fusion potential. If the initial recession was 5.0 mm or less, this author prefers a rerecession of
one or both of the medial rectus muscles. A bilateral 2-mm
re-recession corrects roughly 20 to 25 PD of residual esotropia.
Patients with residual esotropia and initial recessions greater
than 5.0 mm should be managed with lateral rectus resections,
doing slightly less than described on the standard charts.
Because a previously recessed medial rectus muscle is being
resected, remember to do a slightly smaller resection to avoid
an overcorrection. An alternative to surgery in cases of small
residual esotropia is prescribing base-out prism glasses.
The Role of Botulinum Toxin
In addition to surgery, some have advocated the use of botulinum for the treatment of congenital esotropia. The theoretical
advantage would be to create an incomitant deviation so the
patient could adopt a face turn and obtain fusion. Although this
has theoretical merit, there are some problems involved with
the use of botulinum. These complications include secondary
ptosis, initial consecutive exotropia lasting up to 2 to 3 months,
and the temporary effect of the botulin injection itself. Most
studies have shown that multiple injections are needed to
sustain the effect.43 Even with multiple injections, alignment
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243
and sensory outcomes have been significantly worse than
surgery.38 The treatment of choice for most patients with congenital esotropia remains surgical.
ACCOMMODATIVE ESOTROPIA
Accommodative esotropia is usually associated with significant
hypermetropia of 2.00 or more and is termed hypermetropic
accommodative esotropia, or refractive esotropia. Prescribing
the full hypermetropic spectacle correction will improve or, in
many cases, totally correct the esotropia. Some patients with
accommodative esotropia have a high AC/A ratio esotropia,
meaning that they have a greater deviation at near versus distance. They are usually hypermetropic, but may be emmetropic
or even myopic.
Acquired esotropia deserves an urgent consultation. Delay
of treatment will reduce the chances for reestablishing binocular fusion.25 In addition, acquired esotropia may represent a neurological process, so urgent evaluation is important.
HYPERMETROPIC ACCOMMODATIVE
ESOTROPIA
Etiology
Hypermetropic accommodative esotropia is caused by accommodative convergence associated with hypermetropia. These
children have straight eyes as infants but, as they learn to
accommodate to correct for their hypermetropia, they overconverge and develop esotropia. A child with hypermetropia of
3.00 would have to accommodate 3 diopters to create a clear
retinal image for distance viewing. If the AC/A ratio is 6 (high
normal), the accommodative convergence will produce an esodeviation of 18 PD. Depending on the patient’s divergence
fusional amplitudes, this patient may develop an esodeviation.
Clinical Features
Accommodative esotropia usually presents as an acquired intermittent esotropia. The onset ranges from infancy to late childhood, most commonly occurring around 2 years of age. The size
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of a deviation is variable and is typically smaller than congenital esotropia, usually measuring between 20 and 40 PD. Cycloplegic refraction reveals hypermetropia between 1.50 and
6.50 diopters. Parents often give a history that the eyes are
straight some of the time; however, when the child is tired or
focusing at near, the eyes will cross. The esotropia is initially
intermittent but may quickly increase to become a constant
deviation. Patients with constant esotropia may lose fusion
potential and are prone to develop amblyopia.
Cycloplegic Refraction
An accurate cycloplegic refraction is required to determine the
full hypermetropic correction. Young children are often difficult
to refract, and repeat cycloplegic refractions help ensure accuracy. Cyclopentolate is the standard cycloplegic agent.
Cyclopentolate is given topically, one or two doses for a lightly
pigmented iris, and two or three doses for a dark iris. Consider
using atropine in patients with a darkly pigmented iris who
show variable retinoscopy readings. The refraction is performed
30 min after the last dose. Atropine is given twice a day for 3
days, and the refraction is done on the third day. The mydriatic
effect of these drugs lasts much longer than the cycloplegic
effect, so a dilated pupil does not mean complete cycloplegia.
Treatment
The first step in the treatment of hypermetropic accommodative esotropia is to prescribe the full hypermetropic correction
(see example, following). In both juvenile-onset and infantileonset accommodative esotropia, full hypermetropic correction
should be prescribed as soon as the esotropia is identified, even
giving glasses to children as young as 2 months of age (Fig.
7-11). Delay in treatment can result in loss of binocular
potential.25
Example 1. 2-year-old with esotropia for 2 months
Full ductions and versions
Cycloplegic refraction 4.50 OU
Without correction (sc):
With correction (cc) 4.00 OU:
Dsc ET 30
Dcc E 4 (phoria)
Nsc ET 35
Ncc E 2 (phoria)
Treatment: Prescribe spectacles 4.50 sphere OU
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245
A
B
FIGURE 7-11A,B. (A) Three-month-old infant with a 35 PD esotropia and
3.00 D refractive error. (B) Infant now with straight eyes wearing full
hypermetropic correction.
It is important that the child wears the optical correction fulltime. Children who intermittently remove their glasses will not
relax their accommodation and will have blurred vision with
their appropriate hypermetropic correction. For children who
have difficulty relaxing accommodation and therefore do not
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accept their hypermetropic correction, it may be helpful to
prescribe a short course of cycloplegics such as atropine or
cyclopentolate. Parents should be told that the glasses are prescribed to straighten the eyes by relaxing the overfocusing
caused by the farsightedness.
If, after prescribing full hypermetropic correction, the eyes
are straightened to within 10 PD distance and near and the
patient obtains binocular fusion, nothing more need be done but
continue with the full hypermetropic correction. Some advocate
reducing the plus lens until an esophoria is induced; to try to
build fusional divergence and wean the child from glasses. This
author has not seen this practice reduce the need for spectacles
but, all too frequently, has seen it turn a well-controlled deviation into a manifest esotropia. By reducing the plus, you run the
risk of producing a manifest esotropia and losing binocular
fusion. Remember, children with accommodative esotropia have
tenuous fusion. To establish binocular function, the goal must
be to align the eyes to orthotropia.
If, after wearing full hypermetropic spectacles for 4 to 8
weeks, a residual esotropia of more than 10 PD is present for
distance and near (the patient is not fusing), then surgery is
indicated. This residual deviation is termed partially accommodative esotropia (discussed later in this chapter). In some
cases, the full hypermetropic correction will align the eyes for
distance; however, a residual esotropia will persist at near. These
patients have a high AC/A ratio, and bifocals are indicated (see
Prescribing Bifocals below).
High AC/A Ratio Esotropia
A subgroup of patients with accommodative esotropia will have
a high AC/A ratio and have a significantly larger esotropia at
near. High AC/A ratio esotropia usually occurs in patients with
hypermetropia but may occur in patients with myopia or no
refractive error. If the eyes are straight in the distance (10 PD),
a bifocal add is given to correct the near deviation and promote
near fusion.
Example 2.
4-year-old with esotropia for 2 months
Full ductions and versions
Cycloplegic refraction 3.50 OU
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247
With correction (cc) 4.00 OU
Dcc E 4 (phoria—fusing)
Ncc ET 25
Ncc with 3.00 add E 3
(phoria—fusing)
Treatment: Prescribe bifocals (3.50 sphere upper with 3.00
add, OU)
Without correction (sc):
Dsc ET 25
Nsc ET 55
PRESCRIBING BIFOCALS
A bifocal add is indicated for patients who are fusing in the
distance but have an esotropia at near that is large enough to
interfere with near fusion (10 PD).42 The add will relax near
accommodation, thus reducing convergence. If the AC/A ratio
is 7 (high), then a 3.00 add will reduce the near esotropia by
21 PD. In the example above, the 3.00 add reduces the residual near deviation (with correction) to an esophoria of 3 PD,
allowing for binocular fusion. Usually, start with a maximum
near add of 3.00. Over time, the bifocal add can be diminished
slowly to promote divergence. Reduce the reading add to
produce a small esophoria of no more than 4 to 6 PD, which will
stimulate divergence, while maintaining comfortable binocular
fusion. In many cases, the bifocal can be eliminated by 10 to 12
years of age. The best bifocal is a flat-top segment that bisects
the pupil. A common mistake is to prescribe a low bifocal that
a child can easily look over, thus negating the purpose of the
bifocal add.
Remember that bifocals will not treat a manifest esotropia
in the distance. If a patient has an esotropia in the distance
greater than 10 PD with full hypermetropic correction and is not
fusing, then surgery is indicated, not bifocals. Bifocals, however,
may be needed postoperatively if a near esotropia persists.
Partially Accommodative Esotropia
If, after wearing full hypermetropic correction, a residual
esotropia (10 PD) for distance and near exists, it is termed partially accommodative esotropia (Fig. 7-12C). The treatment is
surgery: bilateral medial rectus muscle recessions.
Example 3.
3-year-old with esotropia for 2 months
Full ductions and versions
Cycloplegic refraction 3.50 OU
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A
B
FIGURE 7-12A–B. Infantile accommodative esotropia. The patient is the
author’s youngest son who had partially accommodative esotropia. (A) At
6 weeks of age, the patient’s eyes were well aligned with normal motility. (B) At 3 months of age, a variable esotropia occurred. Deviation measured between essentially straight and an esotropia of 40 prism diopters.
Without correction (sc):
Dsc ET 30
Nsc ET 35
With correction (cc) 3.50, OU:
Dcc ET 20
Ncc ET 25
Treatment: Bilateral medial rectus recessions
C
D
FIGURE 7-12C–D. (C) Cycloplegic refraction revealed a 5.50 refractive
error OU. Patient was given full hypermetropic correction. However, a
small residual esotropia persisted. In this photograph, note that the left
eye is deviated and the Brückner reflex shows a brighter reflex in the left
eye. Augmented surgery was performed at 6 months of age by the author.
(D) Patient 3 years after surgery with straight eyes and excellent binocular function with stereoacuity as measured by Randot testing.
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E
FIGURE 7-12E. (E) At the time of this writing, patient is 13 years old and
is still well aligned with an excellent sensory outcome by Titmus
stereoacuity testing showing a positive fly and 3/3 animals (100 s).
After wearing the 3.50 sphere for 6 weeks, the patient in
Example 3 still had a significant esotropia (Dcc ET 20, Ncc ET
25). This residual esotropia cannot be fused and should be
addressed surgically. Bifocals are not indicated, as they will not
correct the distance deviation. Preoperatively, it is important to
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251
rerefract these patients to make sure that all full latent hypermetropia is corrected.
Surgery for Partially Accommodative Esotropia
Bilateral medial rectus recession is the procedure of choice for
partially accommodative esotropia. There is, however, controversy regarding how to determine the target angle. Most are now
increasing the amount of surgery from the standard approach
using augmented surgery or prism adaptation. Below are various
formulas used to determine the amount of surgery for partially
accommodative esotropia.
STANDARD SURGERY
In Example 3, the standard surgery target angle is ET 20. The
standard surgical approach has been to operate for the residual
deviation measured with correction in the distance (i.e., standard surgery); however, standard surgery has a high undercorrection rate of approximately 25%. Because of this unacceptably
high undercorrection rate, many surgeons are increasing their
surgical numbers to correct partially accommodative esotropia.
The idea of surgery is not to eliminate hypermetropic correction
by overcorrection, but to get the eyes straight and fusing with
full hypermetropic correction. Parents should be advised that
spectacles will be required postoperatively.
AUGMENTED SURGERY
This author has studied results using a target angle determined
by averaging the near deviation with correction and the near
deviation without correction. In Example 3, the augmented
surgery target angle is 30 PD (35 25/2). Results comparing
standard surgery to this augmented surgery formula showed a
26% undercorrection rate for standard surgery, while augmented
surgery resulted in a 93% success rate with 7% overcorrection.70
The patients who were overcorrected all had a high AC/A ratio,
were well aligned at near, and had an intermittent exotropia in
the distance. The augmented surgery formula is based on the
near measurement, so it is not surprising that patients with a
high AC/A ratio have a tendency for overcorrection in the distance. This author augments surgery as described above if the
AC/A ratio is normal; however, if the AC/A ratio is high, average
the near deviation without correction (largest deviation) and the
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distance deviation with correction (smallest deviation), or use
prism adaptation. The high AC/A ratio patients are difficult to
manage.
PRISM ADAPTATION
Another method for determining the amount of surgical correction in patients with partially accommodative esotropia is using
prism adaptation. Prism adaptation consists of prescribing baseout prism for the residual esotropia after prescribing full hypermetropic correction. In Example 3, the initial press-on prism
would be 20 PD base-out. The patient returns in approximately
2 weeks after wearing the prisms. If the esotropia has increased,
then the prisms are increased. This regimen continues at 1- to
2-week intervals until the deviation has stabilized. The surgeon
operates on the full prism-adapted angle as determined by the
press-on prisms. Operating on the larger adapted angle reduces
the undercorrection rate. Results of a multicenter study on
prism adaptation showed that standard surgery resulted in
approximately 75% successful correction rate and operating on
the prism-adapted angle resulted in an 85% success rate;
however, the difficult high AC/A ratio patients were excluded
from the study.58 The disadvantage of prism adaptation is the
cost and time involved with prescribing press-on prisms and
reexamining the patient until the deviation stabilizes.
POSTOPERATIVE CARE
Postoperative care is similar to that described for congenital
esotropia. The goal is to achieve binocular fusion, as most
patients with acquired strabismus have fusion potential.
Patients who are aligned for distance, but have an esotropia
greater than 8 to 10 PD at near, may be candidates for bifocals.
The vast majority of patients will require hypermetropic correction after surgery. A small consecutive exotropia can be
managed by reducing the plus of hypermetropic spectacles, but
do not “cut the plus” more than 2.50 diopters as this results in
instability of the angle. Large overcorrections are rare but when
they occur, they must be managed by surgery.
Miotics
In rare selected patients, miotic drops such as phospholine
iodide (i.e., echothiophate iodide) may be indicated to treat
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253
accommodative esotropia. Miotics, such as phospholine iodide,
are cholinesterase inhibitors and increase the effectiveness of
locally released acetylcholine. Topical phospholine iodine has a
parasympathomimetic effect on the iris sphincter and ciliary
muscles, causing miosis and pharmacological accommodation.
Acetylcholine released in the ciliary body will last longer and
produce more accommodation for a given amount of innervational stimulation. Thus, miotics reduce the accommodative
effort necessary to provide a clear retinal image and will reduce
the amount of associated reflex convergence. When using
miotics, it is preferable to start with a low dose of phospholine
iodide, 0.03%, one drop every morning. If this dose is not sufficient to correct the esotropia, the dose may be increased to twice
a day or use phospholine iodide 0.125%. Miotics truly reduce
the AC/A ratio and esotropia associated with hypermetropia.
Miotics can be tried if the patient has a high AC/A ratio and
has minimal hypermetropia. In most cases, however, bifocal
spectacles are the treatment of choice. Another indication for
the use of miotics is in children who cannot wear spectacles or
contact lenses; this is most useful for short periods of time,
perhaps during the summer months when children are swimming. Miotics are occasionally used as a diagnostic test to determine if an esotropia will respond to hypermetropic optical
correction. If the miotics fail to correct the deviation, this would
identify a nonaccommodative component. Unfortunately, the
only way to know if spectacles will correct the deviation is to
actually prescribe them.
ADVERSE EFFECTS OF MIOTICS
Phospholine iodide, even when given topically, is systemically
absorbed and will lower cholinesterase activity in the blood for
several weeks,14 which is of significant note for those patients
who undergo general anesthesia with succinylcholine. Phospholine iodide prolongs the effect of the succinylcholine and
may prolong respiratory paralysis after surgery. Succinylcholine
should be avoided if phospholine iodide has been used within 6
weeks before surgery. Systemic side effects of miotics may
include brow ache, headaches, nausea, and abdominal cramping.
If the lower dose of phospholine iodide is used, these complications are infrequent.
Ocular side effects of phospholine iodide include iris cysts
along the pupillary margin in 20% to 50% of cases, occurring at
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handbook of pediatric strabismus and amblyopia
any time from several weeks to several months after treatment.
Iris cysts tend to regress after discontinuing phospholine iodide;
however, this author has seen persistent iris cysts several years
after stopping phospholine iodide therapy. Phenylephrine used
in combination with phospholine iodide may prevent iris cysts.
Other rare and unusual complications include lens opacities,
retinal detachment in adults, and angle-closure glaucoma.
INFANTILE ACCOMMODATIVE ESOTROPIA
Infantile accommodative esotropia occurs during the first year
of life. The key to diagnosing infantile accommodative esotropia
is noting the presence of hypermetropia (2.00) and a variableangle esotropia at the onset.4,56 Treatment is to immediately prescribe the full hypermetropic correction, as determined by a good
cycloplegic refraction, and treat amblyopia if present (see Fig.
7-11).18 If spectacles do not align the eyes to within 8 to 10 PD,
then strabismus surgery is indicated (see Partially Accommodative Esotropia, discussed previously). The child should wear
spectacles for at least 4 weeks before going to surgery. Approximately half of diagnosed patients will be corrected with spectacles alone, and half will require spectacles along with surgery
(see Treatment of Partially Accommodative Esotropia, discussed
previously). This author is personally very familiar with this disorder, as his youngest son developed partially accommodative
esotropia that did not respond to full hypermetropic correction
at 4 months of age. The author operated on his son at 6 months
of age using the augmented surgery formula (Fig. 7-12). Now, at
13 years of age, he has done well with just the one surgery, having
straight eyes and high-grade stereoacuity.
The prognosis for binocular fusion in patients with accommodative esotropia is quite good, as these patients have acquired
strabismus. The treatment goal for accommodative esotropia is
establishing binocular fusion and stereopsis.
ACQUIRED NONACCOMMODATIVE
ESOTROPIA
Uncommonly, esotropia is acquired during childhood or even
adulthood without significant hypermetropia. Initially, these
deviations are variable and intermittent. Over time (weeks,
chapter 7: esodeviations
255
months, or even years), however, the esodeviation may become
constant. It is important in these cases of acquired esotropia to
rule out the possibility of an intracranial tumor, Arnold–Chiari
malformation, or other neurological processes such as myasthenia gravis. A divergence paralysis pattern with a larger esotropia
in the distance than at near is a red flag to the possibility of a
mild sixth nerve paresis and a neurological disorder.
The treatment for acquired nonaccommodative esotropia is
usually surgery, and the prognosis for re-establishing binocular
fusion is relatively good. Undercorrections are frequent in this
group, and prism adaptation will help reduce the number of
patients with a residual esotropia.
ESOPHORIA
Small esophorias (8–10 PD) can cause significant asthenopic
symptoms. These patients usually complain of headaches and
fatigue when reading for long periods of time. Small esophorias
are best treated with hypermetropic correction for near esophorias, or base-out prisms if the deviation is present for distance
and near. A reading add relaxes accommodation and convergence, thus correcting the esophoria. Base-out prisms are very
effective; however, patients tend to adapt to the prisms and
require increasing prisms over time. When prescribing prisms,
prescribe just enough for comfortable fusion but slightly less
than the full deviation to stimulate divergence. In cases of a large
esophoria, surgery may be required. In these cases, it is helpful
to use prism adaptation to disclose the full underlying esophoria. In any case of a symptomatic esophoria, a cycloplegic refraction is indicated, as latent hypermetropia is a common cause for
an acquired esodeviation.
ESOTROPIA, NYSTAGMUS, AND
FACE TURN
Nystagmus may occur with esotropia. These patients often
adopt a face turn to damp the nystagmus and improve visual
acuity. Specific types of esotropia, nystagmus, and face turn syndromes include (1) manifest latent nystagmus, (2) congenital
nystagmus with constant esotropia, and (3) nystagmus compen-
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sation syndrome. In these cases, the face turn is used to position the fixing eye at the null point to improve vision. In the
case of manifest latent nystagmus and nystagmus compensation
syndrome, the null point is always in adduction. Consequently,
the fixing eye in these cases is always adducted and the face turn
is toward the side of the fixing eye (Fig. 7-13). Ciancia’s syndrome (see Fig. 7-5 and Congenital Esotropia, discussed previously) is often placed in this category; however, the cause for the
face turn is tight medial rectus muscles, not nystagmus and a
null point.
FIGURE 7-13. Esotropia, nystagmus, and face turn. Drawing shows that
the null point of the nystagmus is in adduction, so the patient adopts a
face turn to the right to place the fixing right eye in adduction. Note that
the face turn is to the same side as the fixing eye.
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257
Manifest Latent Nystagmus
Latent nystagmus (see p. 225) that spontaneously becomes
manifest without monocular occlusion is called manifest latent
nystagmus. The null point for manifest latent nystagmus is
always in adduction. Patients with strabismus and manifest
latent nystagmus will place the fixing eye in adduction to
improve vision; this produces a face turn to the side of the fixing
eye.23 Patients with intermittent strabismus and latent nystagmus will not manifest the nystagmus when they are aligned
and fusing. At these times, the patient has straight eyes or a
microtropia and fusion, so the latent nystagmus is controlled,
and there is no face turn. Other times (e.g., when the patient is
fatigued), the phoria breaks down to a tropia and loss of fusion.
Loss of peripheral fusion changes the latent nystagmus to a manifest latent nystagmus. This causes the patient to adopt a face
turn to place the fixing eye at the null point that is in adduction (Fig. 7-14).
The treatment of manifest latent nystagmus with face turn
is to enhance binocular fusion in order to avoid the tropia phase.
Methods for enhancing binocular fusion in patients with
esotropia include providing hypermetropic correction in
patients with an accommodative component or operating for
the residual esodeviation. In the article by Zubcov et al.,73 five
patients with esotropia and manifest latent nystagmus underwent strabismus surgery resulting in straight eyes; this converted the manifest latent nystagmus to latent nystagmus. Four
of the five patients also showed improvement in binocular visual
acuity because of the improved nystagmus.
Congenital Nystagmus with Constant Esotropia
Patients with congenital nystagmus may have an associated
esotropia. These patients commonly adopt a face turn to place
the fixing eye at the null point. The null point in congenital
nystagmus may be in any gaze position. If the null point is in
adduction, with the right eye fixing, the face turn will be to the
right. Null point in abduction causes the fixing eye to abduct,
and then the face turn is to the left. A vertical null point position causes a compensatory chin depression or chin elevation.
Obviously, there is no face turn if the null point is in primary
position.
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 7-14A,B. Manifest latent nystagmus. Patient with Down’s syndrome and previous surgery for congenital esotropia. Patient now has an
intermittent esotropia with peripheral fusion and monofixation syndrome. (A) Patient is fusing with a microesotropia. There is an underlying latent nystagmus that is controlled because the patient is fusing. Note
that there is no face turn. (B) Now the patient has esotropia, which disrupts fusion and changes the latent nystagmus into a manifest latent nystagmus. The null point of manifest latent nystagmus is in adduction, so
the fixing eye (the right eye) moves into adduction. The patient has developed a face turn to the right. Note the positive Brückner reflex with the
brighter red reflex in the deviated left eye.
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259
Congenital nystagmus is a jerk, or pendular, nystagmus. The
characteristics of congenital nystagmus are different from manifest latent nystagmus. With congenital nystagmus, there is an
increasing velocity of the slow phase and no change in the nystagmus on unilateral occlusion or binocular dissociation. The
nystagmus switches direction on sidegaze with the fast phase to
the right in rightgaze and the fast phase to the left in leftgaze.
Congenital nystagmus and latent, or manifest, nystagmus can
occur concurrently.
The treatment for the face turn with esotropia is strabismus
surgery to move the null point of the fixing eye to primary position. Then, if necessary, move the nonfixing eye to match. For
example, if there is a right esotropia of 40 PD (20°), right eye
fixing in adduction with a face turn to the right 20° (see Fig.
7-13), recess the right medial rectus and resect the right lateral
rectus; this will move the right eye to primary position and
correct the face turn and the esotropia at the same time (also
see Chapter 10).
Nystagmus Compensation Syndrome
(Nystagmus Blockage Syndrome)
Some patients with congenital nystagmus and straight eyes may
use accommodative convergence to damp their nystagmus. In
rare circumstances, this can produce an esotropia. Previously,
this rare syndrome has been termed nystagmus blockage syndrome or nystagmus compensation syndrome.66 These patients
present with straight eyes and congenital nystagmus. On
viewing near targets, they manifest a variable esodeviation while
using accommodative convergence to damp the nystagmus and
improve vision. Key observations include variable-angle intermittent esotropia only at near, and pupillary miosis that occurs
with the esotropia (Fig. 7-15). Many patients who have been previously reported in the literature as having nystagmus blockage
syndrome or nystagmus compensation syndrome actually had
manifest latent nystagmus. Some have doubted the existence
of congenital nystagmus with accommodative convergence
causing esotropia; however, von Noorden66 has documented this
syndrome with EOG recordings. Currently, a good surgical treatment for this esotropia at near does not exist. However, von
Noorden has suggested a small medial rectus recession with
Faden (posterior fixation suture).
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handbook of pediatric strabismus and amblyopia
A
B
FIGURE 7-15A,B. (A) Nystagmus compensation syndrome. Top photograph: patient with congenital nystagmus, straight eyes, and middilated
pupils. Bottom photograph: patient trying to read a near target. When
patient tries to read the near target, the patient invokes accommodative
convergence to damp the nystagmus and an esotropia occurs. Visual
acuity improves to 20/40 at near. (Photograph courtesy of G.K. von
Noorden.) (B) Electro-oculograph of a patient with congenital nystagmus
and nystagmus compensation syndrome. At the beginning of the tracing,
the congenital nystagmus shows large amplitude and visual acuity is
20/100. The patient then uses accommodative convergence to damp the
nystagmus, an esotropia occurs, and visual acuity improves to 20/40 at
near. The amplitude of the nystagmus increases as patient relaxes accommodative convergence and the congenital nystagmus recurs. (From Ref.
67, with permission.)
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261
CYCLIC ESOTROPIA
Cyclic esotropia is a very rare type of esotropia, with most pediatric ophthalmologists only seeing one or two cases in their
entire career. This is an acquired esotropia that occurs at virtually any age, but most frequently between 2 and 6 years of age.
These patients usually cycle between straight eyes and esotropia every 24 to 48 h; however, the interval may vary. To help
establish a pattern, ask the parents to record on a calendar when
the eyes are crossed versus the days when the eyes are straight.
When the eyes are aligned, the patient has good binocular vision
and stereoacuity. Cyclic esotropia is usually progressive and, in
most cases, the esodeviation finally becomes constant over
several months to years. Some cases of cyclic esotropia are associated with hypermetropia and, in these cases, the full cycloplegic correction should be given. Patients in whom there is no
significant hypermetropia, surgery for the full deviation should
be performed to provide appropriate eye alignment and preserve
binocularity and fusion.13,29 Sporadic cases associated with sixth
nerve palsy or central nervous system disease have also been
reported.34,54
DIVERGENCE INSUFFICIENCY
Divergence insufficiency causes an esodeviation that is greater
in the distance than at near and can occur, idiopathically, as a
primary strabismus. An important cause for divergence insufficiency is divergence paralysis secondary to a mild sixth nerve
palsy that causes an esodeviation in the distance. An acquired
esodeviation with a divergence paresis pattern is a red flag for
possible neurological disease. Divergence paresis has been associated with pontine tumor, head trauma, myasthenia gravis, and
Arnold–Chiari malformation. Neuroimaging studies as well as
a neurological consultation are indicated to rule out possible
neurological disease.
SENSORY ESOTROPIA
Sensory esotropia is an esotropia occurring secondary to unilateral blindness. It has been the general teaching that, if the vision
loss occurred before 2 years of age, the patient will develop
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handbook of pediatric strabismus and amblyopia
esotropia and, after 2 years of age, will develop exotropia. This
theory has not been borne out, however, as many infants with
unilateral visual loss develop exotropia. Surgery for sensory
esotropia is a recession of the medial rectus muscle and a resection of the lateral rectus muscle of the blind eye.
References
1. Aiello A, Wright KW, Borchert M. Independence of optokinetic nystagmus asymmetry and binocularity in infantile esotropia. Arch
Ophthalmology 1994;112:1580–1583.
2. Archer SM, Sondhi N, Helveston EM. Strabismus in infancy. Ophthalmology 1989;96:133–137.
3. Arthur BW, Smith JT, Scott WE. Long-term stability of alignment in
the monofixation syndrome. J Pediatr Ophthalmol Strabismus
1989;26:224–231.
4. Baker JD, Parks MM. Early onset accommodative esotropia. Am J
Ophthalmol 1980;90:11.
5. Birch E, Stager D, Wright K, Beck R. The natural history of infantile
esotropia during the first six months of life. J AAPOS 1998;2:325–
329.
6. Birch EE, Gwiazda J, Held RR. Stereo acuity development of crossed
and uncrossed disparities in human infants. Vision Res 1982;22:507.
7. Birch EE, Petrig BL. FPL and VEP measures of fusion, stereopsis, and
stereo acuity. Technical digest series. Noninvasive assessment of
the visual system. Washington, DC: Optical Society of America,
1994.
8. Birch EE, Stager DR, Berry P, Everett ME. Prospective assessment of
acuity and stereopsis in amblyopic infantile esotropes following early
surgery. Investig Ophthalmol Vis Sci 1990;31:758–765.
9. Birch EE, Stager DR, Everett ME. Random dot stereo acuity following surgical correction of infantile esotropia. J Pediatr Ophthalmol
Strabismus 1995;32:231–235.
10. Birch EE, Stager DR. Monocular acuity and stereopsis in infantile
esotropia. Invest Ophthalmol Vis Sci 1985;26:1624–1630.
11. Birch E, Fawcett S, Stager DR. Why does early surgical alignment
improve stereo acuity outcomes in infantile esotropia? J Am Assoc
Pediatr Ophthalmol Strabismus 2000;4(1):10–14.
12. Braddick O, et al. Cortical binocularity in infants. Nature (Lond)
1980;288:363–365.
13. Cahill M, Walsh J, McAleer A. Recurrence of cyclic esotropia after
surgical correction. J Am Assoc Pediatr Ophthalmol Strabismus
1999;3(6):379–380.
14. Chin NV, Gold AA, Breinin GM. Iris cysts and miotics. Arch Ophthalmol 1964;71:611.
15. Ciancia A. La esotropia en el lactante, diagnostico y tratamiento. Arch
Chil Oftalmol 1962;9:117.
chapter 7: esodeviations
263
16. Clarke WN, Noel LP. Vanishing infantile esotropia. Can J Ophthalmol 1982;17:100–102.
17. Clarke WN. Current controversies: very early vs. early or late surgery
for infantile esotropia. Can J Ophthalmol 1995;30:239–240.
18. Coats DK, Avilla CW, Paysse EA, Sprunger DT, Steinkuller PG,
Somaiya M. Early-onset refractive accommodative esotropia. J Am
Assoc Pediatr Ophthalmol Strabismus 1998;2(5):275–278.
19. Costenbader FD. Infantile esotropia. Trans Am Ophthalmol Soc
1961;59:397.
20. Crawford ML, Harwerth RS, Smith EL, von Noorden GK. Loss of
stereopsis in monkeys following prismatic binocular dissociation
during infancy. Behav Brain Res 1996;79(1–2):207–218.
21. Crawford MLJ, von Noorden GK. Optically induced concomitant
strabismus in monkeys. Investig Ophthalmol Vis Sci 1980;19:1105.
22. Crawford MLJ, von Noorden GK. The effects of short-term experimental strabismus on the visual system in Macaca mulatta. Investig Ophthalmol Vis Sci 1979;18:496–505.
23. Dell’Osso LF, Ellenberger C Jr, Abel LA, Flynn JT. The nystagmus
blockage syndrome. Investig Ophthalmol Vis Sci 1983;24:1580.
24. Dickey CF, Metz HS, Stewart SA. The diagnosis of amblyopia in
cross-fixation. J Pediatr Ophthalmol Strabismus 1991;28:171–175.
25. Fawcett S, Leffler J, Birch EE. Factors influencing stereoacuity in
accommodative esotropia. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(1):15–20.
26. Fox R, et al. Stereopsis in human infants. Science 1980;207:323.
27. Friedrich D, de Decker W. Prospective study of the development
of strabismus during the first 6 months of life. Orthopt Hor 1987:
21–28.
28. Helveston EM, Ellis FD, Schott J, et al. Surgical treatment of congenital esotropia. Am J Ophthalmol 1983;96:218–228.
29. Helveston EM. Cyclic strabismus. Am Orthopt J 1971;23:4851.
30. Helveston EM, Neely DF, Stidham DB, Wallace DK, Plager DA,
Sprunger DT. Results of early alignment of congenital esotropia.
Ophthalmology 1999;106:1716–1726.
31. Hiles DA, Watson BA, Biglan AW. Characteristics of infantile
esotropia following early bimedial rectus recession. Arch Ophthalmol 1980;98:697–703.
32. Hoyt C, Jastrzebski G, Marg E. Amblyopia and congenital esotropia.
Visually-evoked potential measurements. Arch Ophthalmol 1984;
102:58–61.
33. Hubel DH, Wiesel TN. Binocular interaction in striate cortex of
kittens reared with artificial squint. J Neurophysiol 1965;28:1041–
1059.
34. Hutcheson KA, Lambert SR. Cyclic esotropia after a traumatic sixth
nerve palsy in a child. J Am Assoc Pediatr Ophthalmol Strabismus
1998;2(6):376–377.
35. Ing MR. Early surgical alignment for congenital esotropia. Trans Am
Ophthalmol Sci 1981;79:625–663.
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36. Ing M, Costenbader FD, Parks MM. Early surgical treatment for congenital esotropia. Am J Ophthalmol 1966;652:1419–1427.
37. Ing MR. Progressive increase in the angle of deviation in congenital
esotropia. Trans Am Ophthalmol Soc 1994;XCII:117–259.
38. Ing MR. Botulinum alignment for congenital esotropia. Ophthalmology 1993;100(3):318–322.
39. Ing MR. Outcome study of surgical alignment before six months of
age for congenital esotropia. Ophthalmology 1995;102:2041–2045.
40. Ing MR. Outcome study of stereoacuity in relation to duration of
misalignment in congenital esotropia. JAAPOS 2001;Feb.6(1):3–8.
41. Leguire LE, Roger GL, Bremer DL. Visual-evoked response binocular
summation in normal and strabismic infants. Investig Ophthalmol
Vis Sci 1991;32:126–133.
42. Ludwig IH, Parks MM, Getson PR. Long-term results of bifocal
therapy for accommodative esotropia. J Pediatr Ophthalmol Strabismus 1989;26:264–270.
43. Magoon E. Chemodenervation of strabismic children. Ophthalmology 1989;96:931–934.
44. Maumenee IH, Alston A, Mets MB, Flynn JT, Mitchell TN, Beaty
TH. Inheritance of congenital esotropia. Trans Am Ophthalmol Soc
1986;84:85–93.
45. Mohoney BG, Erie JC, Hodge DO, Jacobsen SJ. Congenital esotropia
in Olmsted County, Minnesota. Ophthalmology 1998;105:846–850.
46. Morris RJ, Scott WE, Dickey CF. Fusion after alignment of longstanding strabismus in adults. Ophthalmology 1993;100:135–138.
47. Mutti DO, Frane SL, Friedman NE, Lin WK, Sholtz RI, Zadnik K.
Ocular component changes during emmetropization in infancy
(abstract). Investig Ophthalmol Vis Sci 2000;41:S300.
48. Nelson LB, Wagner RS, Simon JW, Harley RD. Congenital esotropia.
Surv Ophthalmol 1987;31:363–383.
49. Nixon RB, Helveston EM, Miller K, Archer SM, Ellis FD. Incidence
of strabismus in neonates. Am J Ophthalmol 1985;100:798–801.
50. Parks MM. Congenital esotropia with a bi-fixation result: report of
a case. Doc Ophthalmol 1984;58:109–114.
51. Pediatric Eye Disease Investigator Group. The clinical spectrum of
early-onset esotropia. Experience of the Congenital Esotropia Observational Study. Am J Ophthalmol 2002;133:102–108.
52. Pediatric Eye Disease Investigator Group. Spontaneous resolution of
early-onset esotropia: experience of the Congenital Esotropia Observational Study. Am J Ophthalmol 2002;133:109–118.
53. Petrig B, Juless B, Kropff W, Baumgartner G, Anliker M. Development of stereopsis and cortical binocularity in human infants: electrophysiological evidence. Science 1981;213:1402–1405.
54. Pillai P, Dhand UK. Cyclic esotropia with central nervous system
disease: report of two cases. J Pediatr Ophthalmol Strabismus
1987;24(5):237–241.
55. Podgor MJ, Remaley NA, Chew E. Associations between siblings for
esotropia and exotropia. Arch Ophthamol 1996;114:739–744.
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56. Pollard ZF. Accommodative esotropia during the first year of life.
Arch Ophthalmol 1976;94:1912.
57. Prieto-Diaz J. Large bilateral medial rectus recession in early
esotropia with bilateral limitation of abduction. J Pediatr Ophthalmol Strabismus 1980;17:101–105.
58. Prism Adaptation Research Group. Efficacy of prism adaptation in
the surgical management of acquired esotropia. Arch Ophthalmol
1990;108:1248–1256.
59. Robb RM, Rodier DW. The variable clinical characteristics and
course of early infantile esotropia. J Pediatr Ophthalmol Strabismus
1987;24:276–281.
60. Scott WE. Temporary surgical overcorrection of infantile esotropia.
Transactions of the New Orleans Academy of Ophthalmology. New
York: Raven Press, 1986.
61. Shauly Y, Prager TC, Mazow ML. Clinical characteristics and longterm postoperative results of infantile esotropia. Am J Ophthalmol
1994;117:183–189.
62. Shirabe H, Mori Y, Dogru M, Yamamoto M. Early surgery for infantile esotropia. Br J Ophthalmol 2000;84:536–538.
63. Smith JT, Scott WE. Long-term stability of alignment in the monofixation syndrome. J Pediatr Ophthalmol Strabismus 1989;Sep.–Oct.
26(5):224–231.
64. Sondhi N, Archer S, Helveston EM. Development of normal ocular
alignment. J Pediatr Ophthalmol Strabismus 1988;25:210.
65. Tychsen L, Lisberger SG. Maldevelopment of visual motion processing in humans who had strabismus with onset in infancy. J Neuroci
1986;6:2495–2508.
66. von Noorden GK. The nystagmus compensation (blockage syndrome). Am J Ophthalmol 1976;82:283.
67. von Noorden GK, Munoz M, Wong SY. Compensatory mechanisms
in congenital nystagmus. Am J Ophthalmol 1987;104:387–397.
68. Wilson ME, Parks MM. Primary inferior oblique overaction in congenital esotropia, accommodative esotropia, and intermittent
exotropia. Ophthalmology 1989;96:950–955.
69. Wright KW. Clinical optokinetic nystagmus asymmetry in treated
esotropes. J Pediatr Ophthalmol Strabismus 1996;33(3):153–155.
70. Wright KW, Bruce-Lyle L. Augmented surgery for esotropia associated with high hypermetropia. J Pediatr Ophthalmol Strabismus
1993;30:167–170.
71. Wright KW, Edelman PM, McVey JH, Terry AP, Lin M. High-grade
stereoacuity after early surgery for congenital esotropia. Arch Ophthalmol 1994;112:913–919.
72. Wright KW, Edelman PM, Walonker F, Yiu S. Reliability of fixation
preference testing in diagnosing amblyopia. Arch Ophthalmol 1986;
104:549.
73. Zubcov AA, Reinecke RD, Gottlob I, Manley DR, Calhoun JH. Treatment of manifest latent nystagmus. Am J Ophthalmol 1990;110:160–
167.
8
Exotropia
Kenneth W. Wright
E
xodeviations are quite common, and they are not necessarily pathological. A small intermittent exotropia is normal
in most newborns, as 70% of normal newborns have a transient
exodeviation that resolves by 2 to 4 months of age.1 Another type
of exodeviation that is considered normal is a small exophoria,
usually less than 10 prism diopters (PD). Most normal adults
have a small exophoria when fully dissociated. Exodeviations are
controlled with our innate strong fusional convergence, typically measuring 30 PD or more. The most common form of
divergent strabismus is intermittent exotropia, which probably
accounts for more than 90% of all exodeviations. Table 8-1 lists
the different categories of pathological exodeviations, with the
one most frequently occurring listed first.
INTERMITTENT EXOTROPIA
Intermittent exotropia is a large phoria that is intermittently
controlled by fusional convergence. Unlike a phoria, intermittent exotropia spontaneously breaks down into a manifest
exotropia (Fig. 8-1).
Clinical Features
Intermittent exotropia is usually first observed by the parents in
early childhood or late infancy as an infrequent drifting or
squinting of one eye. 12 Patients with intermittent exotropia tend
to manifest their deviation when they are tired, have a cold or
the flu, or when they are daydreaming. Adult patients will often
become exotropic after imbibing alcoholic beverages or taking
sedatives.
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267
TABLE 14.1. Classifications of Exodeviations.
Intermittent exotropia (common)
Convergence insufficiency (common)
Sensory exotropia (common)
Congenital exotropia (rare)
Signs of intermittent exotropia include blurred vision,
asthenopia, visual fatigue, and, rarely, diplopia in older children
and adults. Many patients with intermittent exotropia have photophobia (squinting to bright light). Photophobia was originally
thought to be a way for eliminating diplopia or confusion, but
Wiggins and von Noorden have shown that the photophobia may
not be related to diplopia avoidance.39
As a rule, during the phoric phase of intermittent exotropia,
the eyes are perfectly aligned and the patient has bifoveal fusion
with excellent stereoacuity ranging between 40 and 50 s arc. This
excellent bifoveal fusion develops because the eyes are well
aligned in early infancy when the critical binocular cortical connections are being established. A minority of patients with intermittent exotropia are primary monofixators and do not develop
normal bifoveal fusion with good stereopsis. Rarely a patient will
even have significant amblyopia. The poor fusion in these cases
is associated with a predominance of the tropia phase. During the
tropia phase of intermittent exotropia, patients will show large
hemiretinal or regional suppression of the temporal retina.26,30
Anomalous retinal correspondence in the tropia phase and normal
retinal correspondence in the phoria phase have been demonstrated in some patients with intermittent exotropia.4,38
Natural History
The natural history of intermittent exotropia remains obscure,
as there are no longitudinal prospective studies and only a few
retrospective studies of untreated intermittent exotropia. Von
Noorden found that 75% of 51 untreated patients showed progression over an average follow-up period of 3.5 years, whereas
9% worsened and 16% improved.36,38 Hiles et al.,20 in their study
of 48 patients, found no significant change in the deviation after
an average of 11 years follow-up, and 2 patients progressed to a
constant tropia. The most we can say about the natural history
is that, in the majority of cases, intermittent exotropia does not
get better; it either stays the same or progresses. If the tropic
phase increases, patients may develop dense suppression and,
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A
B
FIGURE 8-1A–B. (A) Patient with intermittent exotropia and straight
eyes in the phoric phase. Patient has 40 s arc stereoacuity. (B) Occlusion
of the right eye disrupts fusion and manifests the exotropia. Under the
occluder, the right eye is deviated temporally.
over time, may progress to a constant exotropia with loss of
fusional potential.
Classifications
Intermittent exotropia has been classically categorized into
three subtypes based on the difference between the distance
chapter 8: exotropia
269
C
FIGURE 8-1C. (C) Occluder is removed and the right eye is deviated
temporally, showing the exotropia. Patient is in the tropic phase and
suppresses right eye.
deviation and the near deviation. These three “older” classic categories are (1) basic, (2) pseudodivergence excess, and (3) true
divergence excess. It is important to note that the older terminology uses the term divergence excess, and pseudodivergence
excess is only descriptive as to the difference of the deviation
distance versus near; it is not meant to imply a mechanism
for the distance–near disparities. The mechanism for the distance–near disparities seen in patients with intermittent
exotropia is most likely caused by superimposed overconvergence on the basic exodeviation. These convergence mechanisms include tonic fusional convergence (tenacious proximal
fusion),22 accommodative convergence (AC/A ratio), and proximal convergence (instrument convergence).
BASIC INTERMITTENT EXOTROPIA
With this type of exotropia, there is no significant distance–near
disparity, and the distance deviation is within 10 PD of the near
deviation. Patients with a basic deviation have normal convergence, so their deviation is essentially the same for distance and
near.
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PSEUDODIVERGENCE EXCESS
This is an exodeviation that is measured larger for distance fixation than near fixation by brief alternate cover testing (distance
10 PD greater than near); however, with prolonged monocular
occlusion (patch test for 30–60 min), the near deviation
increases and becomes similar to the distance deviation (within
10 PD). For example, an exodeviation measures 30 PD in the
distance and 10 PD at near to alternate cover testing. One eye
is patched for 30 min, and now the patient measures 30 PD in
the distance and 25 PD at near. This change occurs because
patients with pseudodivergence excess have increased tonic
near fusional convergence that dissipates slowly after monocular occlusion. Prolonged monocular occlusion of 30 to 60 min
is required in these patients to dissipate tonic near fusional convergence and disclose the full latent deviation (see Patch Test,
below). The relatively brief period of monocular occlusion that
occurs with alternate cover testing is not enough to break
up the tonic near fusional convergence and disclose the full
deviation at near. Surgery is performed for the full distance
deviation.
Pseudodivergence excess is quite common. More than 80%
of patients with an apparent divergence excess actually have
pseudodivergence excess, as the near deviation will increase to
within 10 PD of the distance deviation after the patch test.5,22,37
PATCH TEST (OCCLUSION TEST)
The patch test consists of placing an occlusive patch over one
eye for at least 30 to 60 min, then measuring the deviation
without letting the patient restore binocular fusion. The idea is
to totally suspend all tonic fusional convergence by occluding
one eye, forcing the full latent deviation to become manifest.
When performing the patch test, be sure the patient does not
peek around the patch and regain fusion before the deviation is
measured. To measure the deviation, first cover the unpatched
eye with a paddle occluder, then remove the patch and measure
the deviation with alternate cover testing. This method ensures
the patient will not sneak a peek with both eyes and reestablish
fusion before the deviation is measured.
TRUE DIVERGENCE EXCESS
In these cases, the distance deviation is greater than the near
deviation by more than 10 PD, even after performing the patch
chapter 8: exotropia
271
test. For example, the distance deviation would measure 30 PD,
near deviation 10 PD and, after a 30-min patch test, the distance
deviation would be 30 PD and the near deviation 15 PD. This
author and Eugene De Juan (Los Angeles, CA) studied the cause
of true divergence excess at the Wilmer Clinic at Johns Hopkins
Hospital in Baltimore in 1981. They found that most of the
patients with true divergence excess had a high AC/A (accommodative convergence/accommodation) ratio as determined by
a 3.00 add after a 60-min patch test. The patch test relaxes
tonic fusional convergence, and the 3.00 add relaxes accommodation. The high AC/A ratio patients do not show an increase
in the near exotropia to the patch test, but the near deviation
increases dramatically with a 3.00 near add.40 In a similar
study, Kushner22 found approximately 60% of patients with a
true divergence excess had a high AC/A ratio and 40% had a
normal AC/A ratio. The group with a high AC/A ratio was prone
to postoperative overcorrection (75% overcorrection) at near if
the distance measurement is used as the surgical target angle.
The 40% of true divergence excess patients with a normal AC/A
ratio had relatively good results using the distance measurement. Patients with true divergence excess are a difficult group
to surgically correct as they are prone to having a consecutive
esotropia at near, and some will require bifocals or additional
surgery. Following is a summary of the causes of overconvergence that produce true divergence excess.
CAUSES OF TRUE DIVERGENCE EXCESS
HIGH AC/A RATIO
This condition occurs when the distance deviation is larger than
the near deviation even after the patch test, but the near deviation increases close to the distance deviation with a 3.00 add.
High AC/A ratio intermittent exotropia has normal tonic
fusional convergence but has a high AC/A ratio that causes
the distance–near disparity. Surgery is usually performed for a
deviation somewhere between the distance and near deviation
measured without near add. Some of these patients require
bifocals after surgery if there is an esotropia at near.
INCREASED PROXIMAL CONVERGENCE
This situation arises when the distance deviation is larger than
the near deviation after the patch test and a 3.00 add OU.
These patients have a normal tonic fusional convergence and a
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normal AC/A ratio, but have increased proximal convergence
that reduces the near deviation. Proximal convergence is independent of binocular fusion. Surgery should be performed for an
angle between the distance and near deviation.
MIXED CONVERGENCE MECHANISM
There are many cases where more than one mechanism of convergence causes the distance–near disparity. This group with
mixed convergence mechanism explains the patients that do not
specifically fit into the pure categories listed previously. An
example of a mixed convergence mechanism is when the distance deviation is 45 PD and the near deviation is 20 PD. After
the patch test, the near deviation increases to 30 PD and, with
a 3.00 near add and the patch test, the near deviation equals
the distance. In this example, there is a component of increased
tonic fusional convergence brought out by the patch test and a
slightly high AC/A ratio (AC/A ratio 5; i.e., 45 30/3.00)
disclosed by the 3.00 add. Both the increased tonic fusional
convergence and the slightly high AC/A ratio contribute to
the distance–near disparity. Surgery is performed for the angle
measured between the distance deviation and near the deviation
(after the patch test).
Measuring the Exodeviation
Obtaining reproducible measurements in a patient with intermittent exotropia can be difficult, as the angle of deviation is
often variable when measured by routine alternate cover prism
testing. If it is late in the day and the patient is tired, fusional
convergence will be weak and a large deviation will be easily
manifest. On the other hand, if the patient is wide awake and
alert, strong fusional convergence will keep the deviation small
and difficult to elicit. The patch test reduces variability secondary to fusional convergence because prolonged monocular occlusion disrupts fusion and discloses the full latent deviation.
Because most patients with intermittent exotropia often have
strong tonic fusional convergence, they should be measured
using prolonged alternate cover testing, making sure that one
eye is always covered. If there is significant angle variability or
a significant distance–near discrepancy after prolonged alternate
cover testing, then a patch test is indicated. In contrast, patients
who show consistent measurements and no significant distance
near disparity do not need the patch test.
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FAR DISTANCE TEST
Another technique that reduces measurement variability by disclosing the full distance deviation is the far distance test. This
test is performed by simply having the patient fixate on an object
well past 20 feet to relax all proximal convergence. It is preferable to measure the deviation while the patient fixates out a
window to a far distant target. Combining the patch test and the
far distance test has greatly reduced undercorrections and has
improved overall results.
Treatment of Intermittent Exotropia
NONSURGICAL TREATMENT
In general, nonsurgical treatments for intermittent exotropia are
not very effective. One method is to prescribe 2 to 3 diopters
of myopic correction over what is required by cycloplegic
refraction.8 Overminusing induces accommodative convergence,
thus reducing the exodeviation. Another method is part-time
monocular occlusion therapy.15,18 By occluding the dominant
eye, the patient is forced to use the nonpreferred eye, thus providing antisuppression therapy. Although others have found
success with this procedure, in this author’s experience, only a
few patients have responded to this therapy. In virtually every
case, the intermittent exotropia returns when the patching is
stopped. Part-time occlusion therapy may be tried in younger
patients as a method for delaying surgery, but it is only a temporary measure. Convergence exercises are useful for convergence insufficiency but not for most cases of intermittent
exotropia. The use of antisuppression orthoptic therapy and
diplopia awareness are not indicated, as this practice may lead
to intractable diplopia and is detrimental to the patient.
INDICATIONS FOR SURGERY
As with any strabismus, the indications for surgery include
preservation or restoration of binocular function and cosmesis.
In intermittent exotropia, one of the most important indications
for therapeutic intervention is an increasing tropia phase. If the
frequency or duration of the tropia phase increases, this indicates diminished fusional control and a potential for loss of
binocularity. Progression should be monitored by recording size,
frequency, duration of the exotropia, and the ease of dissociation
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handbook of pediatric strabismus and amblyopia
after brief monocular occlusion. Documentation of deteriorating
fusional control is an indication for treatment.
Additionally, if the exotropia is manifest more than 50% of
waking hours, surgery is probably indicated. In most cases,
surgery should be delayed until 4 years of age. A study comparing surgery performed at various ages showed a significant
increase in the incidence of amblyopia and loss of stereopsis
when a consecutive esotropia occurred in children under 4 years
of age.14 Because the desired result is an initial consecutive
esotropia, younger children who have surgery for intermittent
exotropia are at risk for developing amblyopia and losing binocularity. If, however, the exotropia is present more than 50% of
waking hours, and is increasing in size, frequency, or duration,
then early surgery may be indicated even in children under 4
years of age. Richard and Parks32 found no significant difference
in results between early or late surgery, and Pratt-Johnson et al.29
actually had better results when surgery was performed under 4
years of age. The take-home message is that patients can be operated safely under 4 to 6 years of age for intermittent exotropia,
but they must be followed closely, because a persistent consecutive esotropia can cause loss of stereopsis and amblyopia in this
age group.
SURGICAL TREATMENT
CHOICE
OF
PROCEDURE
For all three classic types of intermittent exotropia (i.e., basic,
pseudodivergence excess, and true divergence excess), bilateral
lateral rectus recessions work well. Symmetrical surgery is
usually preferred over a monocular resect/recess procedure, as
recession/resection procedures produce lateral incomitance with
a significant esotropia in the side of the operated eye. This
incomitance can produce diplopia in sidegaze that may persist
for months or even years. In patients with amblyopia of 20/50
or worse, a recession/resection procedure on the amblyopic eye
is preferred, avoiding surgery on the “good” eye.
ROLE
OF THE
PATCH TEST
Historically, the patch test was important to distinguish among
the three subgroups of intermittent exotropia because patients
with basic or pseudodivergence intermittent exotropia would
receive a monocular recess/resect procedure, whereas patients
with true divergence excess would undergo bilateral lateral
chapter 8: exotropia
7,37
275
28
rectus recessions.
Parks has shown that bilateral lateral
rectus recessions work well for all three types of intermittent
exotropias, so the patch test is probably not very important for
determining whether a recess/resect or a bilateral recession
should be performed. The patch test is, however, very useful in
patients with a distance–near disparity to bring out the full deviation. Use the patch test in divergence excess cases to determine
if there is pseudo- or true divergence excess.
AMOUNT
OF
SURGERY
Surgical parameters for patients with basic or pseudodivergence
excess intermittent exotropia should be based on the full distance deviation as determined by alternate cover testing or the
patch test. Patients with true divergence excess, however,
should be treated more conservatively, especially if there is an
associated high AC/A ratio. These patients are difficult to
manage, because totally correcting the distance deviation often
leads to a persistent esotropia at near that may require postoperative bifocal glasses.22 If a true divergence excess associated
with a high AC/A ratio is present, it is best to operate for a deviation somewhere between the distance and near deviations.
These patients with true divergence excess and a high AC/A
ratio should be told they have a significant risk for a persistent
overcorrection and, postoperatively, may require a reoperation,
a bifocal add, or miotic drops.
Moore25 suggested reducing the amount of recession in
patients with lateral incomitance. It is this author’s experience
that even moderate amounts of lateral incomitance are not
important.
A- AND V-PATTERNS: OBLIQUE OVERACTION
Intermittent exotropia may be associated with A- and V-patterns
and inferior and superior oblique overaction (see Chapter 9). In
these cases, it is appropriate to simultaneously operate on the
obliques if dysfunction is present, or vertically offset the horizontal muscles for A- and V-patterns. Inferior oblique weakening procedures are safe in patients with bifoveal fusion and
intermittent exotropia, but beware of performing superior
oblique tenotomies or tenectomies, as this may result in a consecutive superior oblique paresis with intractable cyclovertical
diplopia.41 If significant superior oblique overaction and an “A”
pattern is present, consider an infraplacement of the lateral
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handbook of pediatric strabismus and amblyopia
rectus muscles or the Wright superior oblique tendon expander
procedure, rather than a tenotomy or tenectomy of the superior
oblique muscle. Do not significantly alter the amount of horizontal surgery just because simultaneous oblique surgery is also
being performed.
Small vertical deviations associated with intermittent
exotropia should be ignored, as these small vertical deviations
usually disappear after surgery. Patients with large-angle intermittent exotropia may have an X-pattern, with the exotropia
increasing in upgaze and downgaze relative to the deviation in
primary position. In some cases, there is true overaction of all
four oblique muscles; however, usually this pattern is due to
tight lateral rectus muscles causing a leash effect similar to
Duane’s syndrome upshoot and downshoot. The X-pattern is
usually small, and it is best to address the pattern by simply performing bilateral lateral rectus recessions for the deviation in
primary position.
POSTOPERATIVE CARE
Immediately after surgery, a small consecutive esotropia of 8 to
10 PD is desirable, as even a large consecutive esotropia up to
20 PD may resolve without further surgery.31,33 Be sure to warn
the parents and patients before surgery that postoperative
diplopia may occur so they are not surprised. Postoperative
diplopia associated with the initial overcorrection usually
resolves by 1 to 2 weeks. In children under 4 years of age, alternate part-time patching of each eye helps prevent suppression
and amblyopia and may facilitate straightening of the eyes. If a
residual esotropia persists past 2 to 3 weeks, then the patient
should be treated with prism glasses to neutralize the esotropia
and re-establish fusion.17 Prescribe just enough prism to alleviate the diplopia, but leave a small residual esophoria to encourage divergence. If after 6 to 8 weeks the esotropia persists, then
a reoperation should be considered. Advancement of the lateral
rectus muscle is indicated if there is limited adduction or lateral
incomitance that is consistent with a slipped muscle. Otherwise, bimedial recessions are usually the procedure of choice for
a consecutive esotropia, especially if the esotropia is greater at
near. If the consecutive esotropia is present only at near, one
may consider a bifocal add, miotics, or even a base-out prism to
correct the near esotropia while creating a small exodeviation in
chapter 8: exotropia
277
the distance. Failing this, small bimedial rectus recessions is the
next option, with or without a Faden procedure.
Patients with a residual exotropia greater than 10 PD after
the first postoperative week will probably not improve and most
will require additional surgery. It is best to wait 8 weeks before
reoperating on the residual exotropia. Rerecess both lateral
rectus muscles if the primary surgery was bilateral recessions of
6.0 mm or less. If the primary recessions were greater than 6.0
mm, perform bilateral resections but be conservative, as overcorrections are common after resecting against a large recession.
PROGNOSIS
The success rate, as in most types of strabismus, is dependent
on the length of follow-up and, the longer the follow-up, the
higher the incidence of undercorrection. Richard and Parks,32 in
one of the longest follow-up studies, found a 56% success rate
with one surgery, defining success as a postoperative deviation
less than 10 PD, with a follow-up period of 2 to 8 years (mean,
4 years). Thirty-eight percent (38%) of their patients were undercorrected and 6% were overcorrected. An additional surgery
improved their success rate to just over 80%. Hardesty16 reported
an 80% success rate after no more than two surgeries with a
10-year follow-up. Hardesty attributed the long-term success to
the aggressive use of postoperative prisms for both over- and
undercorrections to maintain constant fusion to prevent
suppression.
CONVERGENCE INSUFFICIENCY
Convergence insufficiency is the inability to maintain convergence on objects as they approach from distance to near. Symptoms usually first occur during the teenage years and include
asthenopia, reading difficulty, blurred near vision, and diplopia.
Alternate cover testing will disclose a near exophoria with
essentially no distance deviation. The exophoria at near intermittently breaks down into a tropia, especially after prolonged
near work such as reading. When tropic, most patients will see
double while some will not, as they have learned to suppress.
Even patients with suppression can experience asthenopia and
are often symptomatic.
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handbook of pediatric strabismus and amblyopia
Patients with convergence insufficiency will show a remote
near point of convergence. The near point of convergence (NPC)
is how close one can bring a fixation target to the nose and still
maintain fusion. The break point is when the target is too close,
fusion breaks, and an exotropia becomes manifest. The normal
NPC is between 5 to 10 cm from the bridge of the nose. Patients
with convergence insufficiency will have a remote break point
ranging from 10 to 30 cm or more. Convergence insufficiency
may also be associated with reduced fusional convergence
amplitudes. Normal fusional convergence amplitudes for near
are between 30 to 35 PD, but patients with convergence
insufficiency usually break with less than 20 PD base-out.
Some patients with convergence insufficiency will initially
show a fairly good near point of convergence and convergence
fusion amplitudes at near; however, on repeat testing, they are
easily fatigued. The diagnosis of convergence insufficiency
should not be based solely on one test trial but, instead, on
repeat testing.
The best treatment for convergence insufficiency is orthoptic convergence exercises.23 The two most useful convergence
exercises are near point exercises (pencil pushups) and prism
convergence exercises. Near point exercises consist of presenting a target at a remote distance where it is easily fused, then
slowly bringing the target in toward the eyes until break point
is achieved (Fig. 8-2). With prism convergence exercises, a prism
bar oriented base-out is presented to one eye to induce fusional
convergence (Fig. 8-3). First, use a small prism that can be easily
fused while the patient fixates on a near target. Increase the baseout prism until the patient notes blurred vision (blur point).
Then, increase prism until fusion breaks (break point). Both convergence exercises should be repeated 15 to 20 times during each
session and repeated 2 to 3 times per day. Convergence exercises
stimulate fusional convergence only if the patient appreciates
diplopia and the break point. Patients who do not appreciate
diplopia can be treated with red glass convergence exercises. A
red filter is placed over the dominant eye and a light is used as
the fixation target. The red filter and light will help the patient
recognize diplopia. Convergence exercises have been found to be
extremely helpful and curative in patients with convergence
insufficiency so long as these exercises are diligently performed.
Improvement of symptoms usually occurs after a few weeks of
exercises, but in some cases several months are needed before
symptoms are relieved. In this author’s experience, almost all
chapter 8: exotropia
279
FIGURE 8-2. Near point convergence exercise showing accommodative
target at near. Patient starts with the target at arm’s length, and then
brings the target toward the nose, converging on the accommodative
target.
patients with convergence insufficiency can be managed by exercises alone; it is the rare case that requires surgery. Always try
orthoptic exercises first and, if they fail to alleviate the symptoms, then surgery may be considered. The standard surgery for
FIGURE 8-3. Photograph of child with congenital exotropia.
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handbook of pediatric strabismus and amblyopia
convergence insufficiency is a small medial rectus resection of
one or both medial rectus muscles. In this author’s experience,
surgery is not effective in most cases of convergence insufficiency.19,35
Accommodative Insufficiency
A common cause of asthenopia and blurred near vision is
convergence insufficiency, but occasionally patients have a
combination of convergence insufficiency and accommodative
insufficiency.24,35 Even more rare is isolated accommodative
insufficiency without convergence insufficiency.11 Obviously,
presbyopia is the most common type of accommodative insufficiency, but primary accommodative insufficiency can occur in
children and young adults as well. Accommodative insufficiency
can be secondary to a systemic disorder such as Parkinson’s
disease, oral lithium, or local ciliary body dysfunction associated with Adie’s pupil.2
According to Duane’s standard curve of accommodation,
normal patients under 20 years of age should be able to accommodate at least 10 diopters, or read the 20/40 line on the near
card at 10 cm.13 Patients with accommodative insufficiency will
have a remote near point of accommodation. There are no
beneficial exercises for treating accommodative insufficiency;
however, accommodative exercises can be tried. Mazow et al.23
found modest improvement with pretreatment accommodation
averaging 7.1 diopters and posttreatment 11.4 diopters. A
reading add can also be prescribed, but prescribe the lowest
power that relieves the symptoms and still stimulate some
accommodation. Prescribing a strong reading add only weakens
the patient’s remaining accommodation.
SENSORY EXOTROPIA
If a patient loses vision in one eye, that eye may drift out
(sensory exotropia). Patients with dense amblyopia may also
develop a sensory exodeviation. It is often said that if the visual
loss occurs before 4 years of age, an esotropia develops. If vision
loss occurs after 4 years of age, an exodeviation results. This
rule, however, is violated as often as it is followed. Studies of
patients with unilateral congenital cataracts show an even distribution between esodeviations and exodeviations.10 Treatment
chapter 8: exotropia
281
for sensory exotropia is performing a recession/resection procedure of the eye with the decreased vision.
CONGENITAL EXOTROPIA
Congenital exotropia is extremely rare, and most ophthalmologists will see only one or two cases during their career (Fig. 83). Congenital exotropia may occur in patients with systemic
disease, craniofacial anomalies, ocular albinism, or cerebral
palsy.21 The treatment for congenital exotropia is bilateral lateral
rectus recessions, which should be performed after 6 months of
age. This syndrome should not be confused with the normal,
variable, small-angle exodeviation seen in 70% of normal newborns. Instead, congenital exotropia is a large-angle constant
exodeviation, with a relatively poor prognosis for fusion. It
has a much higher incidence of amblyopia than intermittent
exotropia, with the incidence of amblyopia being similar to
congenital esotropia (20 to 40%).
References
1. Archer SM, Sondhi N, Helveston EM. Strabismus in infancy.
Ophthalmology 1989;96:133–137.
2. Brown B. The convergence insufficiency masquerade. Am Orthopt J.
1990:40:94–97.
3. Burian HLM. Exodeviations: their classification, diagnosis and treatment. Am J Ophthalmol 1966;62:1161–1166.
4. Burian HM. The sensorial retinal relationship in comitant strabismus. Arch Ophthalmol 1947;337:336.
5. Burian HM, Franceschetti AT. Evaluation of diagnostic methods
for the classification of exodeviations. Trans Am Ophthalmol Soc
1970;68:56.
6. Burian HM, Smith DR. Comparative measurement of exodeviations
at 20 and 100 feet. Trans Am Ophthalmol Soc 1971;69:188.
7. Burian HM, Spivey BE. The surgical management of exodeviations.
Am J Ophthalmol 1965;59:603.
8. Caltrider N, Jampolsky A. Overcorrecting minus lens therapy
for treatment of intermittent exotropia. Ophthalmology 1983;90:
1160.
9. Campos EC. Binocularity in comitant strabismus: binocular visual
field studies. Doc Ophthalmol 1982;53:249.
10. Cheng KP, Hiles DA, Biglan AW, Pettapiece MC. Visual results
after early surgical treatment of unilateral congenital cataract.
Ophthalmology 1991;98:903–910.
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11. Chrousos GA, O’Neill JF, et al. Accommodative deficiency in
healthy young adults. J Pediatr Ophthalmol Strabismus 1988;25:
176–179.
12. Costenbader FD. The physiology and management of divergent
strabismus. In: Allen JH (ed) Strabismic ophthalmic symposium,
vol I. St. Louis: Mosby, 1950:349.
13. Duane A. Studies in monocular and binocular accommodation with
their clinical applications. Am J Ophthalmol 1922;5:865–877.
14. Edelman PM, Murphree AL, Brown MH, Wright KW. Consecutive
esodeviation . . . then what? Am Orthopt J 1988;38:111–116.
15. Freeman RS, Isenberg SJ. The use of part-time occlusion for early
onset unilateral exotropia. J Pediatr Ophthalmol Strabismus 1989;26:
94.
16. Hardesty H. Management of intermittent exotropia. Binoc Vis Q
1990;5:145.
17. Hardesty HH, Boynton JR, Keenan P. Treatment of intermittent
exotropia. Arch Ophthalmol 1978;96:268.
18. Henderson JW, Iacobucci I. Occlusion in the pre-operative treatment
of exodeviations. Am Orthopt J 1965;15:42.
19. Hermann JS. Surgical therapy for convergence insufficiency. J Pediatr
Ophthalmol Strabismus 1981;18:28.
20. Hiles DA, Davies GT, Costenbader FD. Long-term observations
on unoperated intermittent exotropia. Arch Ophthalmol 1968;80:
436.
21. Hunter DG, Ellis FJ. Prevalence of systemic and ocular disease in
infantile exotropia: comparison with infantile esotropia. Ophthalmology 1999;106:1951–1959.
22. Kushner BJ. Exotropic deviations: a functional classification and
approach to treatment. Am Orthopt J 1988;38:81–93.
23. Mazow ML, Musgrove K, Finkelman S. Acute accommodative and
convergence insufficiency. Am Orthopt J 1991;41:102–109.
24. Mazow ML. The convergence insufficiency syndrome. J Pediatr
Ophthalmol Strabismus 1971;8:243–244.
25. Moore S. The prognostic value of lateral gaze measurements in
intermittent exotropia. Am Orthopt J 1969;19:69.
26. Nawratzi I, Jampolsky A. A regional hemiretinal difference in amblyopia. Am J Ophthalmol 1958;46:339.
27. Parks MM. Comitant exodeviations in children. In: Strabismus symposium, New Orleans Academy of Ophthalmology. St. Louis: Mosby,
1962:45.
28. Parks MM. Cocomitant exodeviations. In: Ocular motility and strabismus. Hagerstown: Harper & Row, 1975:113–122.
29. Pratt-Johnson JA, Barlow JM, Tillson G. Early surgery in intermittent exotropia. Am J Ophthalmol 1977;84:689.
30. Pratt-Johnson J, Wee HS. Suppression associated with exotropia.
Can J Ophthalmol 1969;4:136.
31. Raab EL, Parks MM. Recession of the lateral recti: early and late
postoperative alignments. Arch Ophthalmol 1969;82:203.
chapter 8: exotropia
283
32. Richard JM, Parks MM. Intermittent exotropia. Surgical results in
different age groups. Ophthalmology 1983;90:172.
33. Scott WE, Keech R, Mash J. The postoperative results and stability
of exodeviations. Arch Ophthalmol 1981;99:1814.
34. von Noorden GK, Brown DJ, Parks M. Associated convergence and
accommodative insufficiency. Doc Ophthalmol 1973;34:393–403.
35. von Noorden GK. Resection of both medial rectus muscles in organic
convergence insufficiency. Am J Ophthalmol 1976;81:223.
36. von Noorden GK. Some aspects of exotropia. Presented before
meeting of the Wilmer Residents’ Association, Johns Hopkins
Hospital, April 26, 1966.
37. von Noorden GK. Divergence excess and simulated divergence
excess: diagnosis and surgical management. Ophthalmologica
1969;26:719.
38. von Noorden GK. Binocular vision and ocular motility: theory and
management of strabismus. St. Louis: Mosby, 1985.
39. Wiggins RE, von Noorden GK. Monocular eye closure in sunlight.
J Pediatr Ophthalmol Strabismus 1990;27:16.
40. Wright KW, De Juan E. Patch test with and without 3.00 near add.
Wilmer Eye Institute, Johns Hopkins Hospital, 1981 (unpublished
data).
41. Wright KW, Min BM, Park C. Comparison of superior oblique tendon
expander to superior oblique tenotomy for the management of superior oblique overaction and Brown’s syndrome. J Pediatr Ophthalmol
Strabismus 1992;29(2):92–97.
9
Alphabet Patterns and
Oblique Muscle
Dysfunctions
Kenneth W. Wright
I
n this chapter, A- and V-pattern strabismus and oblique
dysfunction are discussed, including management strategies.
Under the category of A- and V-patterns, special subtypes are
described. The section on oblique dysfunction includes the following: head tilt test, inferior oblique paresis and inferior
oblique overaction, superior oblique paresis and superior oblique
overaction, and Brown’s syndrome.
A- AND V-PATTERNS
A significant difference in the horizontal deviation from upgaze
to downgaze is described as an A- or V-pattern. An A-pattern is
described as more divergence in downgaze versus upgaze of at
least 10 prism diopters (PD), whereas a V-pattern is increasing
divergence in upgaze versus downgaze by 15 PD or more. A- and
V-patterns are often a result of oblique muscle overaction
or oblique muscle paresis. Other less common causes include
nerve misdirection such as Duane’s syndrome, ectopic muscle
course with ectopic muscle pulleys, and a rotated orbit associated with craniofacial abnormalities.5,6,29 Examples of strabismus
patterns (1 through 5) follow.
Example 1.
A-pattern
ET A-pattern
XT V-pattern
ET V-pattern
XT 10
XT 20
XT 30
ET 30
ET 20
ET 10
XT 30
XT 20
XT 10
ET 10
ET 20
ET 30
Upgaze
Primary position
Downgaze
XT, exotropia; ET, esotropia.
284
V-pattern
XT A-pattern
chapter 9: alphabet patterns and oblique muscle dysfunctions
285
A- and V-Pattern Subtypes
Look critically at the type of pattern: is it symmetrical or does
the change in horizontal deviation occur more in upgaze or
downgaze? This is important to know, as the configuration or
subtype of the A- or V-pattern can indicate an identifying etiology and can influence the surgical plan. For example, a V-pattern
consisting of convergence in downgaze without significant
change in horizontal deviation from primary position to upgaze
is highly suggestive of a bilateral superior oblique palsy. Listed
below are subtypes of A- and V-patterns in which the change in
horizontal deviation is asymmetrical.
V-PATTERN SUBTYPES
Y-PATTERN
The Y-pattern is a V-pattern subtype with divergence occurring in upgaze and little change in the horizontal deviation
between primary position and downgaze. This pattern is
highly suggestive of bilateral inferior oblique overaction, which
is often associated with infantile esotropia and may also be seen
with intermittent exotropia. Y-pattern can also be seen in
patients with Brown’s syndrome, Duane’s syndrome with
upshoot, and rarely congenital aberrant innervation of the
lateral rectus muscle with the superior rectus nerve (see
Example 2).
Example 2.
Upgaze
Primary position
Downgaze
ET Y-pattern
XT Y-pattern
ET 10
ET 25
ET 30
XT 30
XT 15
XT 10
ARROW PATTERN
Another V-pattern subtype is convergence that largely occurs
between primary position and downgaze. This author has
termed this pattern “arrow” pattern. The presence of an arrow
pattern and extorsion in downgaze is virtually diagnostic for
bilateral superior oblique muscle palsy. The lack of abduction
and intorsion in downgaze because of weak superior oblique
muscles allows unopposed adduction and extorsion by the
inferior recti muscles (see Example 3).
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Example 3.
ET Arrow Pattern
Upgaze
Primary Position
Downgaze
Ortho
ET 5
ET 20
A-PATTERN SUBTYPE
LAMBDA PATTERN
The lambda pattern, an A-pattern subtype, is characterized by a
divergence in downgaze without much change in the horizontal
deviation from primary position to upgaze. A lambda pattern is
most frequently associated with bilateral superior oblique overaction. Overrecessed or slipped inferior rectus muscles will also
cause an A-pattern lambda subtype with apparent superior
oblique muscle overaction. In contrast, inferior oblique muscle
underaction causes an A-pattern with most of the horizontal
change as convergence in upgaze (see Example 4).
Example 4.
XT lambda pattern
Lambda pattern
Upgaze
Primary Position
Downgaze
XT 15
XT 20
XT 35
X-PATTERN
An X-pattern occurs when there is divergence in upgaze and
divergence in downgaze, which can occur without a specific
cause. Patients with long-standing large-angle exotropia will frequently show an X-pattern, presumably caused by a tight contracted lateral rectus muscle. As the eye adducts against the
tight lateral rectus muscle, it acts as a leash and produces lateral
forces. If the eye then rotates up or down the tight lateral rectus
slips above or below the eye and pulls the eye up and out, or
down and out, respectively. This leash effect of the lateral rectus
is also seen in Duane’s syndrome, usually type III, with both
an upshoot and downshoot present on attempted adduction.
Lateral rectus recessions reduce the X-pattern associated with
exotropia, and an ipsilateral lateral rectus recession with a Ysplit works well to reduce the vertical overshoot and X-pattern
associated with Duane’s syndrome type III29 (see Example 5).
chapter 9: alphabet patterns and oblique muscle dysfunctions
287
Example 5.
XT X-Pattern
Upgaze
Primary position
Downgaze
XT40
XT30
XT40
Treatment of A- and V-Patterns
A- and V-patterns with minimal or no oblique overaction can be
managed by offsetting, or transposing, the horizontal rectus
muscles superiorly or inferiorly. Transpose the medial recti
insertions toward the apex of the pattern (up for an A-pattern
and down for a V-pattern) and the lateral recti insertions to the
wide part of the pattern (down for an A-pattern and up for a Vpattern) (Fig. 9-1). An A-pattern exotropia, for example, can be
treated by recessing both lateral rectus muscles and transposing
them inferiorly (Fig. 9-2). Vertical transposition of horizontal
muscles in the treatment of A- or V-patterns changes vector
forces and muscle tension as the eyes rotate up and down. For
example, when the medial recti are infraplaced for a V-pattern,
they gain increased function as the eyes rotate up, thus collapsing the V-pattern. Conversely, when the eyes rotate down, the
infraplaced medial rectus muscles slacken, resulting in divergence of the apex of the V-pattern. One-half-tendon-width
FIGURE 9-1. Direction to transpose the rectus muscles to correct for Aand V-patterns. Left diagram: transposition for a V-pattern, with the
lateral rectus muscles moved up and medial rectus muscles moved down.
Right diagram: transposition for an A-pattern, with the medial rectus
muscles moved up and the lateral rectus muscles moved down. The
medial rectus is moved toward the apex of the A or V and the lateral
rectus is moved away from the apex of the A or V. This transposition
holds true whether the muscles are recessed or resected.
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FIGURE 9-2. Drawing of a one-half-tendon-width inferior transposition
of the lateral rectus muscle with recession for an A-pattern associated
with an intermittent exotropia. A Insertion to limbus distance.
B Recession measured from the insertion.
(5 mm) of vertical displacement results in approximately 15 PD
of pattern correction. A full-tendon-width vertical displacement
results in approximately 25 PD of correction and is reserved for
extremely large A- or V-patterns. Vertical transposition of a
horizontal rectus muscle by one full-tendon-width reduces
the vector forces at the horizontal plane and, in this author’s
opinion, often results in unpredictable horizontal alignment. For
example, a full-tendon-width infra-placement of the lateral
rectus muscles for an A-pattern would predispose to an overcorrection (esotropia) in primary position. This author rarely
performs a horizontal rectus muscle transposition more than
one-half tendon-width (5 mm) except in cases of a large A- or Vpattern associated with craniofacial disorders or absent muscles.
Monocular supraplacement of one rectus muscle and infraplacement of the partner antagonist muscle can be used to correct an
A- or V-pattern in a patient with amblyopia to avoid surgery on
the only good eye. Monocular A- or V-pattern horizontal muscle
offsets can cause significant torsional changes and should be
done only on amblyopic eyes in patients with poor binocular
fusion to avoid inducing torsional diplopia. Thus, monocular
horizontal offsets can be used to correct torsional diplopia.
In cases with significant inferior or superior oblique overaction and an A- or V-pattern, the appropriate oblique muscles
should be weakened rather than performing a horizontal rectus
muscle transposition. An exception exists for patients with
chapter 9: alphabet patterns and oblique muscle dysfunctions
289
superior oblique overaction and binocular fusion. These patients
are at risk for developing cyclovertical diplopia after superior
oblique tenotomy.23 Patients with binocular fusion and mild
superior oblique overaction are best treated with transposition
of the horizontal recti rather than a superior oblique tenotomy.
Another surgical option for the fusing patient is a controlled
tendon elongation procedure, such as the Wright superior
oblique tendon expander or a split-tendon elongation. For large
A- and V-patterns (25 PD) with 3 or more oblique overaction,
consider combining oblique weakening with a half-tendonwidth horizontal rectus muscle transposition.
OBLIQUE DYSFUNCTION
Clinical Evaluation of Oblique Dysfunction
When an oblique muscle overacts or underacts, all three functions of the muscle are involved: torsional, vertical, and horizontal. Clinical quantification of oblique dysfunction, however,
is primarily based on the vertical hyper- or hypofunction seen
on version testing. To assess oblique function, move the eye
under examination into adduction and make an observation.
Then move the eye into the field of action of the muscle: adduction and elevation for the inferior oblique muscle, and adduction and depression for the superior oblique muscle. The amount
of overaction or underaction can be graded on a scale of 1 to
4 for overaction and 1 to 4 for underaction. A measurement
of 1 overaction is recorded if there is no hypertropia with horizontal versions, but there is slight overaction when the eye is
moved into the field of action of the oblique muscle vertically.
With 2 overaction, there is a slight hypertropia in horizontal
gaze, and with 3 overaction, there is obvious hypertropia on
direct horizontal gaze. In 4 overaction, there is a large hypertropia in horizontal gaze with an abduction movement as the
eye moves vertically into its field of action. Figure 5-3 in Chapter
5 shows degrees of inferior oblique overaction on version testing.
The amount of A- or V-pattern and amount of fundus torsion are
additional parameters to help quantitate the amount of oblique
dysfunction.
When evaluating oblique dysfunction, the abducting eye
should be fixing so the adducting eye is free to manifest oblique
dysfunction. For example, when the right inferior oblique is
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handbook of pediatric strabismus and amblyopia
being evaluated, a version movement to the left is directed, the
right eye is partially covered, and the right eye is observed
behind the cover for an upshoot (see Chapter 5, Fig. 5-4).
Discussion of the characteristics of individual oblique muscle
dysfunctions follows.
Primary Oblique Overaction Versus Paresis
Overaction of an oblique muscle can be primary (i.e., unknown
etiology) or can be secondary to a muscle paresis. Primary
oblique muscle overaction is commonly found in association
with A- and V-pattern horizontal strabismus. One possible etiology for what appears to be primary oblique muscle overaction
is ectopic location of rectus muscles and their pulleys.5,6 A
transient congenital oblique muscle paresis could also cause
secondary overaction of its antagonist muscle. A congenital
superior oblique paresis, for example, produces ipsilateral inferior oblique overaction. Oblique overaction can also be caused
by paresis of its yoke vertical rectus muscle of the contralateral
eye (Hering’s law of yoke muscles). For example, a left inferior
rectus paresis causes apparent overaction of the right superior
oblique muscle and is best observed when the patient fixes with
the paretic left eye, down and in abduction.
In general, acquired oblique muscle paresis is associated
with underaction of the agonist and with relatively mild overaction of the antagonist oblique muscle. Congenital and longstanding oblique muscle paresis are usually associated with
minimal superior oblique underaction and significant overaction
of the antagonist oblique muscle. The head tilt test, described
below, is used to distinguish primary oblique dysfunction from
oblique dysfunction secondary to a vertical or oblique muscle
paresis. A positive head tilt test is a strong indication that there
is a vertical rectus or oblique muscle paresis whereas a negative
head tilt usually indicates a primary oblique overaction. If the
vertical deviation changes by more than 5 PD on right tilt versus
left tilt, then the head tilt test is said to be positive. If there is
no significant difference in the deviation (5 PD or less) from right
tilt to left tilt, then the head tilt test is said to be negative.
BIELSCHOWSKY HEAD TILT TEST
Tilting the head stimulates the utricular reflex and invokes torsional eye movements to correct and maintain the appropriate
chapter 9: alphabet patterns and oblique muscle dysfunctions
291
retinal orientation. A tilt right, for example, invokes intorsion
of the right eye and extorsion of the left eye. The intortors are
the superior oblique and the superior rectus muscles, and the
extortors are the inferior oblique and the inferior rectus muscles.
This arrangement keeps vertical forces balanced during the head
tilt. If one of the torsional muscles is paretic, then there will be
an imbalance of vertical forces and a vertical deviation will
occur on head tilt testing. Figure 9-3 demonstrates this concept
for a right superior oblique paresis. As the head tilts to the right,
the right superior oblique and right superior rectus contract to
intort the right eye. Because the superior oblique is paretic, the
superior rectus has unopposed vertical force and elevates the
eye, creating an increasing right hyperdeviation on head tilt to
the right.
The head tilt test is used in patients with a vertical deviation to determine if either a vertical rectus or oblique muscle is
paretic. When a patient presents with a vertical deviation, first
perform the head tilt test to see if a paretic muscle is present. If
the head tilt test is positive (5 PD difference in right tilt vs.
left tilt), then it is likely there is a vertical rectus or oblique
muscle paresis. To determine which muscle is paretic, measure
the deviation in sidegaze and use the three-step test as described
next.
FIGURE 9-3. Diagram of a right superior oblique paresis with a positive
head tilt in tilt right. As the head tilts to the right, the left eye extorts
and the right eye intorts. The extorters of the left eye are the inferior
rectus and the inferior oblique. Their vertical functions cancel each other,
so there is no vertical overshoot. The intortors of the right eye are the
superior rectus (SR) and superior oblique (SO) muscles. Because the right
superior oblique is paretic, the elevation effect of the superior rectus is
unopposed, and a right hypertropia occurs on tilt to the right.
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PARKS THREE-STEP TEST
Marshall Parks in 1958 published the “Three-Step Test” for the
diagnosis of cyclovertical muscle palsies.23 This test identifies
which muscle is paretic in patients with a hypertropia caused
by an isolated vertical rectus muscle or oblique muscle palsy.
The three steps are to determine (1) which paretic muscle might
be causing the hyperdeviation in primary position, (2) where the
hypertropia is greatest, in rightgaze or leftgaze, and (3) on head
tilt, which side the hypertropia is greatest: tilt right or tilt left.
See Table 9-1 for results of the three-step test for both vertical
and oblique muscle palsy.
The first step is to determine which paretic muscle could
be causing a hyperdeviation in primary position. A right hyperdeviation, for example, might be caused by a weak depressor
muscle of the right eye (i.e., right inferior rectus or right superior oblique) or a weak elevator muscle of the left eye (i.e., left
superior rectus or left inferior oblique).
The second step is to determine in which horizontal field of
gaze the hypertropia increases. If the hypertropia increases on
gaze away from the hypertropic eye, the paretic muscle is the
TABLE 9-1. Responses to the Three-Step Test for All Vertical and
Oblique Muscle Palsies.
First step: hyper
in primary
Second
step: hyper
increases
in gaze
Third step: hyper increases with
head tilt (hyper ⬎ ipsilateral
tilt ⫽ oblique
hyper ⬎ contralateral
tilt ⫽ vertical rectus)
RIR
R LIO
LIO
L RIR
RSO
R RSO
LSR
L LSR
RSR
R RSR
LSO
L LSO
RIO
R LIR
LIR
L RIO
RSO
RIR
RHT vs.
R
LSR
LIO
L
RSR
RIO
LHT vs.
R
LSO
LIR
L
chapter 9: alphabet patterns and oblique muscle dysfunctions
293
ipsilateral oblique or contralateral vertical rectus. A hypertropia
that increases to the side of the hypertropia is caused by a paretic
vertical muscle on the side of the hypertropia or the contralateral vertical rectus muscle, that is, the paretic muscle is a
vertical rectus muscle of the abducting eye or an oblique muscle
of the adducting eye. For example, a right hyperdeviation that
increases in leftgaze could only be caused by a paretic left
superior rectus muscle or a paretic right superior oblique muscle.
The third step is based on the Bielschowsky head tilt test
as previously described. This last step can be difficult to calculate, so this author uses a trick that he shamelessly calls Wright’s
rule. The author states, “I am sure others have used the same
trick to simplify the head tilt test, but I like the way it sounds:
Wright’s Rule.” Wright’s rule states that if the hyperdeviation
increases on head tilt to the same side of the hyperdeviation,
then an oblique muscle is paretic. If the hyperdeviation increases
to the opposite side of the hyperdeviation, then a vertical rectus
muscle is paretic. For example, if the right hyper increases on
head tilt to the right (same side as the hyper), then the oblique
muscle is paretic; namely, the right superior oblique (SO) or left
inferior oblique (IO) muscle. If the right hyper increases on left
head tilt (opposite side of the hyper), then it is the vertical rectus
muscle that is weak; namely, the left superior rectus (SR) muscle
or right inferior rectus (IR) muscle. Example 6 describes characteristics of a right superior oblique paresis.
Example 6. Right Superior Oblique Paresis
Rightgaze
RHT10
Leftgaze
RHT 15
RHT 25
Head tilt test: right, RHT 15 PD; left, RHT 4 PD.
PARKS THREE-STEP TEST
FOR
EXAMPLE 6
Step 1: Right hypertropia
Right IR or SO versus left SR or IO (underacting muscles, right
eye vs. left eye).
Step 2: Right hypertropia increases in leftgaze
Left SR or right SO (the muscles with field of action in
leftgaze).
Step 3: Right hypertropia increases in head tilt to the right
Right tilt induces intorsion of the right eye and extorsion of
left eye. Both the muscles in contention (RSO and LSR) are
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handbook of pediatric strabismus and amblyopia
intortors, but only the RSO intorts on right tilt. Therefore, the
diagnosis is right superior oblique paresis.
or, by Wright’s rule:
Right hyperdeviation increases on right head tilt (same side as
the hyper); therefore, it has to be an oblique muscle paresis.
As we are down to two choices from step 2, RSO and LSR, the
paretic muscle is the right superior oblique.
SHORTCUT
TO THE
THREE-STEP TEST
Classically, the paretic muscle is determined by the Parks threestep test as just described. In 1967, Helveston13 described combining steps 1 and 2 to make a two-step test.
This author prefers to start with the head tilt test and use
Wright’s rule. To know which vertical rectus or oblique muscle
is weak, determine in which horizontal gaze the vertical deviation increases, right or left. As an example, a right hypertropia
that increases on head tilt to the right and increases on rightgaze
has to be caused by an oblique muscle paresis because the tilt
is positive to the same side as the hypertropia. Because the right
hypertropia increases on rightgaze, in the field of action of the
left inferior oblique muscle (not in the field of action of the right
superior oblique muscle), the paretic muscle is the left inferior
oblique. Using Wright’s rule alone narrows the choices to two
muscles: either an oblique or a vertical rectus muscle of each
eye. Determining the horizontal gaze where the hypertropia is
greatest tells us which eye, the right eye or the left eye.
PROBLEMS
WITH THE
HEAD TILT TEST
A positive head tilt test is not infallible when diagnosing
cyclovertical muscle paresis. Patients with dissociated vertical
deviations, as well as some patients with intermittent exotropia,
show a positive head tilt. In addition, the head tilt test is
designed to diagnose an isolated paretic muscle, and it may not
be reliable when multiple muscles are paretic or if an ocular
restriction is present.
Superior Oblique Paresis
A superior oblique paresis is the most common cause for an
isolated vertical deviation. The typical findings of a unilateral
superior oblique paresis include an ipsilateral hypertropia that
increases on contralateral side-gaze and a positive head tilt test
with the hyperdeviation increasing on head tilt to the ipsilateral
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295
shoulder (see Example 6). There may be relatively little superior
oblique underaction and mostly inferior oblique overaction (Fig.
9-4A,B). Mild extorsion is recorded if less than 10°. To reduce
the hypertropia and fuse, patients with a unilateral superior
oblique paresis adopt a compensatory head tilt to the side, opposite the paresis, combined with a face turn away from the side
of the palsy. Long-standing unilateral superior oblique paresis
with a large hypertropia may show pseudosuperior oblique overaction of the contralateral eye, as a result of contraction of the
ipsilateral superior rectus muscle because of the long-standing
hypertropia and Hering’s Law of yoke muscles. As the ipsilateral eye has restricted depression in abduction, the yoke
muscle overacts (i.e., contralateral superior rectus muscle).
FIGURE 9-4A,B. Composite nine-gaze photograph of patient with a
congenital right superior oblique palsy. Note the large RHT in primary
position that increases in leftgaze. There is 3 right inferior oblique
overaction and 2 superior oblique underaction. In straight rightgaze, it
appears that the left superior oblique is overacting, but the right superior
oblique is slightly tight because of secondary contracture. (B) Positive
head tilt test with large RHT on tilt right.
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FIGURE 9-5. Composite nine-gaze photograph of patient with bilateral
traumatic superior oblique palsy. Patient has a small esotropia and extorsion in primary position that increases in downgaze. Note the V-pattern
(arrow pattern subtype) with a large esotropia in downgaze. There is also
severe underaction of both superior oblique muscles associated with relatively mild inferior oblique overaction.
Bilateral superior oblique paresis is associated with bilateral superior oblique underaction, a V-pattern (arrow subtype),
little or no hypertropia, and a right hypertropia in leftgaze and
a left hypertropia in rightgaze (Fig. 9-5). Other signs include a
bilateral extorsion (total greater than 10°), a reversing head tilt
test with a right hypertropia in tilt right, and a left hypertropia
in tilt left. The presence of an arrow pattern with extorsion
increasing in downgaze (Example 7) is diagnostic for an acute
bilateral superior oblique palsy and is often seen with traumatic
superior oblique palsies. Clinical signs of unilateral versus
bilateral superior oblique paresis are shown in Table 9-2.
Example 7. Bilateral Superior Oblique Paresis
Rightgaze
LHT10
Leftgaze
RHT 2, ET4
RHT 5, ET 20
Bilateral Maddox Rod—15° Extorsion.
Bilateral extorsion on fundus exam.
Head tilt test: right, RHT 10 PD; left, LHT 10 PD.
ET on downgaze
RHT 10
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TABLE 9-2. Unilateral Versus Bilateral Superior Oblique Paresis.
Clinical sign
Unilateral
Bilateral
Superior oblique underaction
Inferior oblique overaction
V-pattern
Ipsilateral underaction
Ipsilateral overaction
Less than 10 PD
Hypertropia
Greater than 5 PD
Head tilt test
Increasing hyper on
ipsilateral head tilt
(Rt SOP RH tilt
right)
Less than 10°
Bilateral underaction
Bilateral overaction
Greater than 10 PD with
arrow pattern
(convergence in
downgaze)
Less than 5 PD (except
asymmetrical paresis)
Positive head tilt to both
sides (RHT on right tilt
and LHT on left tilt)
Extorsion
Greater than 10°
A bilateral asymmetrical superior oblique paresis can look like
a unilateral superior oblique paresis; this is termed masked
bilateral superior oblique paresis.16,17 Suspect a masked bilateral
paresis if the hypertropia precipitously diminishes in lateral gaze
toward the side of the obvious paretic superior oblique muscle
and if there is even slight inferior oblique overaction of the
fellow eye (see Example 8).
Example 8. Masked Bilateral Superior Oblique Paresis
Rightgaze
RHT5
Leftgaze
RHT 20
RHT 30
Head tilt test: right, RHT 25 PD; left, RHT 3 PD.
The presence of a V-pattern and bilateral extorsion on fundus
examination also suggest bilateral involvement in patients with
a presumed unilateral paresis. In these cases of masked bilateral
superior oblique paresis, if surgery is performed only for a unilateral superior oblique palsy, the contralateral superior oblique
paresis will become evident postoperatively.
FALLEN EYE
Significant underaction of the superior oblique muscle and fixation with the paretic eye will produce the classic finding called
the fallen eye. When a patient with a superior oblique paresis
fixes with the paretic eye and tries to look into the field of action
of the paretic superior oblique muscle, the weak superior oblique
muscle requires a large amount of innervation to make the eye
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FIGURE 9-6. Photograph of a traumatic right superior oblique palsy,
showing the fallen eye, left eye. The right eye is fixing in the field of
action of its paretic superior oblique muscle (i.e., down and in adduction),
requiring a great deal of innervation. Because of Hering’s law of equal
innervation of yoke muscles, the left inferior rectus muscle (yoke muscle
to the paretic right superior oblique muscle) also receives a great deal of
innervation. Because the left inferior rectus is at full strength, it overacts
and pulls the left eye down, thus causing the appearance of a left
fallen eye.
move down and nasally. Because of Hering’s law, the yoke
muscle (contralateral inferior rectus muscle) receives an equally
large amount of innervation. Because the contralateral inferior
rectus muscle has normal function, this increased innervation
produces a large secondary hypotropia, or the fallen eye
(Fig. 9-6).
INHIBITIONAL PALSY
ANTAGONIST
OF THE
CONTRALATERAL
Chavasse, in 1939, described the term inhibitional palsy of the
contralateral antagonist. This term relates to a patient who
chronically fixates with the paretic eye, resulting in an apparent
weakness on version testing of the yoke muscle to the antagonist of the paretic eye. That is, the paretic eye moves easily into
the field of its antagonist with little innervation because the
agonist is weak. The yoke muscle to the antagonist of the paretic
muscle receives the same small innervation (Hering’s law), so it
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299
will appear paretic on versions because its antagonist is innervated. Clinically, this is seen in association with a congenital
fourth nerve palsy and ipsilateral inferior oblique overaction
when the patient fixates with the paretic eye. For example, a left
fourth nerve palsy with left inferior oblique overaction will
produce a left hypertropia increasing in rightgaze. If the patient
fixates with the left eye, the innervation required for the left eye
to look up and right is minimal, as it is in the field of the overacting left inferior oblique muscle. The yoke muscle to the left
inferior oblique muscle is the right superior rectus muscle, and
it too will receive little innervation. The right superior rectus
will appear to underact or be paretic because its antagonist, the
right inferior rectus, is normally innervated and holds the eye
down. Inhibitional palsy of the contralateral antagonist is only
seen on version testing when the paretic eye is fixing.
PRIMARY INFERIOR OBLIQUE OVERACTION VERSUS
SUPERIOR OBLIQUE PALSY
Primary inferior oblique overaction can be differentiated from
superior oblique palsy by the head tilt test and type of V-pattern
(Table 9-3).
Traumatic Superior Oblique Paresis
Traumatic superior oblique paresis is usually associated with
severe closed head trauma, loss of consciousness, and cerebral
concussion; however, even very mild head trauma without loss
of consciousness can cause a superior oblique paresis. Traumatic
superior oblique paresis occurs when the tentorium traumatizes
TABLE 9-3. Primary Inferior Oblique Overaction Versus Superior
Oblique Paresis.
Clinical sign
Primary overaction
Superior oblique paresis
Inferior oblique overaction
V-pattern
Head tilt test
Subjective torsion
Yes
Yes, Y-pattern
Negative
No
Objective extorsion (fundus
examination)
Underaction of ipsilateral
superior oblique muscle
Yes
Yes
Yes, “arrow” pattern
Positive
Yes (except in congenital
superior oblique paresis)
Yes
No (minimal if any)
Yes
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the trochlear nerves as they exit the posterior midbrain posteriorly. Since the two trochlear nerves exit the midbrain together,
only a few millimeters apart, the nerve trauma is almost always
bilateral. Thus, most cases of traumatic superior oblique paresis
are bilateral, although the paresis may be asymmetrical.
The pattern of strabismus is classically, minimal or no
hypertropia in primary position, a left hypertropia in rightgaze,
a right hypertropia in leftgaze, underaction of both superior
oblique muscles, and an esotropia in downgaze (Figs. 9-5, 9-6).
There is a positive head tilt with a right hypertropia on right
tilt and a left hypertropia on left tilt. Extorsion increasing in
downgaze can be demonstrated by Maddox rod and indirect ophthalmoscopy. Patients complain of horizontal or vertical torsional diplopia that is worse in downgaze (Fig. 9-5). In most
cases, there is not much ipsilateral inferior oblique muscle overaction, usually 1 or less. Because the strabismus is acquired,
patients complain of diplopia—torsional, vertical, and horizontal—that increases in downgaze.
The management of traumatic superior oblique paresis
is discussed later in this chapter under Treatment of Superior
Oblique Paresis.
Congenital Superior Oblique Paresis
The cause of congenital superior oblique paresis is usually
unknown. The paresis may be associated with a lax superior
oblique tendon or rarely an absent tendon.12 Most cases present
as a unilateral paresis or an asymmetrical masked bilateral
paresis. Typically, there is a large hypertropia in primary position and significant inferior oblique overaction, usually with
relatively little superior oblique underaction (see Fig. 9-4). The
most common presenting sign is a head tilt opposite to the side
of the palsy. Even though the paresis is present at birth, symptoms often occur in late childhood or even adulthood. It is
common for patients to be diagnosed for the first time in middle
age. Normally vertical fusional amplitudes are weak and even
small acquired hyperdeviations of 3 to 5 PD cannot be fused and
result in constant diplopia. Patients with congenital superior
oblique paresis, however, develop large vertical fusional amplitudes, and fuse large hypertropias up to 35 PD. The presence
of large vertical fusion amplitudes is an important clinical sign
that the hyperdeviation is long-standing, rather than acutely
acquired, and is suggestive of a congenital superior oblique palsy.
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301
Over time, the fusional control weakens, resulting in a deviation that becomes manifest in later life.
In addition to large fusional vergence amplitudes, patients
with congenital superior oblique paresis adopt a compensatory
head tilt opposite to the palsy to minimize the deviation and
establish binocular fusion. Patients with congenital superior
oblique paresis typically have good stereopsis and manifest the
hyperdeviation intermittently, usually when fatigued. Even
though patients with congenital superior oblique paresis have
high-grade stereopsis, most also have the ability to suppress
when tropic so that they usually do not experience diplopia. This
sensory adaptation is similar to the adaptation of patients with
intermittent exotropia. Typically these patients also do not
demonstrate extorsion by Maddox rod testing as they adapt to
the retinal extorsion.
Facial asymmetry is seen in approximately 75% of patients
with congenital superior oblique palsy, with one side of the face
being hypoplastic and smaller.26 The hypoplastic side of the face
is on the side of the head tilt (i.e., the dependent side of the face)
(Fig. 9-7). One theory for the facial asymmetry is that gravita-
FIGURE 9-7. Photograph of patient with a compensatory right head tilt
and right face turn associated with a left congenital superior oblique palsy.
Note the facial asymmetry, as the right side of the face is hypoplastic.
Hypoplasia is ipsilateral to the head tilt and contralateral to the superior
oblique palsy.
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tional pull on the dependent side of the face causes changes in
size of facial structures. Another theory is that facial asymmetry represents a mild form of congenital plagiocephaly associated with the superior oblique palsy.
In summary, signs that a superior oblique palsy is congenital and not acquired include childhood photographs showing a
long-standing head tilt, facial asymmetry, lack of extorsional
diplopia, lack of extorsion by Maddox rod, and large vertical
fusion amplitudes. In most cases, the diagnosis of congenital
superior oblique muscle palsy can be made on the basis of
clinical evaluation.
Other Causes of Superior Oblique Paresis
The majority of superior oblique pareses are either congenital or
traumatic, but other causes include vascular disease with brainstem lacunar infarcts, multiple sclerosis, intracranial neoplasm,
herpes zoster ophthalmicus, diabetes and associated mononeuropathy, and iatrogenic after superior oblique tenotomy. An
acquired idiopathic superior oblique paresis requires a neurological workup including neuroimaging. Patients with craniosynostosis may have bilateral superior oblique palsies caused
by absent superior oblique tendons.
Treatment of Superior Oblique Paresis
The treatment of superior oblique paresis depends on the pattern
of the strabismus. Cardinal position of gaze measurements and
evaluation for inferior oblique overaction and superior oblique
underaction are needed to determine the pattern of strabismus
and where the deviation is greatest. Subjective torsion should be
assessed by double Maddox rod testing in acquired cases;
however, patients with a congenital superior oblique palsy will
not have subjective torsion. Objective torsion evaluated by indirect ophthalmoscopy can be useful for verifying torsional abnormalities but is usually not the major clinical sign that directs
the treatment plan.
Most treatment strategies require identifying where the
hypertropia is greatest, and surgery is then designed to correct
the deviation in primary position while reducing the incomitance.15 For example, a right unilateral superior oblique paresis
with a hypertropia less than 10 PD in primary position, inferior
oblique overaction, and minimal superior oblique underaction
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303
can be treated with a simple ipsilateral inferior oblique weakening procedure (e.g., inferior oblique muscle graded anteriorization). If the hypertropia in primary position is greater than
15 PD, then an isolated inferior oblique recession may not be
enough to correct the hypertropia. In this case, especially if there
is a significant hypertropia in downgaze, one should add a
contralateral inferior rectus recession to an ipsilateral inferior
oblique recession (Table 9-4). Late overcorrections have been
known to occur after inferior rectus recessions. This author has
changed to a nonabsorbable suture or a long lasting absorbable
suture for inferior rectus muscle recessions, and this choice
seems to have solved the late overcorrection problem. In cases
of congenital superior oblique palsies, be conservative in regard
to recessing the contralateral inferior rectus muscle. A small
undercorrection is usually well tolerated, but an overcorrection
and a reverse hypertropia is difficult for these patients to fuse.
Tightening the entire width of the superior oblique tendon
by performing a superior oblique tuck has theoretical utility for
improving superior oblique function. A superior oblique tuck,
however, usually results in minimal to no improvement of superior oblique function, and the tight tendon creates a restrictive
leash of elevation in adduction (i.e., iatrogenic Brown’s syndrome). The tuck has been suggested for patients with congenital superior oblique paresis secondary to a lax superior oblique
tendon.12,27 Plager27 suggests performing exaggerated forced
duction testing of the superior oblique tendon at the beginning
of surgery to see if the tendon is lax or absent. Caution should
TABLE 9-4. Treatment of Unilateral Superior Oblique Paresis.
Clinical manifestation
Procedure
Inferior oblique overaction: small
hypertropia
Hyperdeviation in primary position
15 PD; deviation is greater in upgaze
Inferior oblique overaction: large
hypertropia
Hyperdeviation in primary position
15 PD
Lax superior oblique tendon with
superior oblique underaction
Hyperdeviation in primary position
15 PD; minimal inferior oblique
overaction; deviation is greatest in
downgaze
Inferior oblique weakening (author
prefers graded anteriorization)
(common)
Ipsilateral inferior oblique weakening
(author prefers graded
anteriorization), with contralateral
inferior rectus recession (common)
Small superior oblique tuck (rare)
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be used when tucking the superior oblique, as iatrogenic Brown’s
syndrome is a frequent complication of a superior oblique
tendon tuck. Most surgeons avoid the superior oblique tuck
unless there is significant superior oblique underaction and an
extremely lax tendon or, in cases of bilateral superior oblique
paresis, where there is severe superior oblique underaction.
Traumatic superior oblique palsies should be observed for 6
months following recovery of muscle function. Patients who
have partial recovery of superior oblique muscle function will
often be left with extorsional diplopia worse in downgaze,
without significant oblique dysfunction, V-pattern, or hypertropia. In these cases, extorsion can be improved by the
Harada–Ito procedure, which consists of selectively tightening
the anterior one-fourth to one-third of the superior oblique
tendon fibers.11 Patients with a bilateral superior oblique palsy
and poor recovery of muscle function show a large esotropia
in downgaze (arrow subtype V-pattern), extorsion greater in
downgaze, left hypertropia in rightgaze, and a right hypertropia
in leftgaze, but minimal or no hypertropia in primary position.
In these cases, consider either bilateral Harada–Ito procedures
and bilateral medial rectus muscle recessions with infraplacement one-half-tendon-width or bilateral superior oblique tendon
tucks and bilateral medial rectus muscle recessions with
infraplacement one-half-tendon-width. This is a difficult strabismus to correct; however, surgery can often improve diplopic
symptoms. The superior oblique tucks will create a bilateral
iatrogenic Brown’s syndrome, but this may be an acceptable
trade-off for improved single binocular vision in downgaze.
Table 9-4 lists treatment strategies for unilateral superior
oblique paresis, and Table 9-5 lists treatments for bilateral superior oblique paresis.
Inferior Oblique Paresis
An isolated inferior oblique paresis is extremely rare and, when
it does occur, it is usually idiopathic. Pollard28 reported on 25
patients having an isolated inferior oblique palsy, with 23 being
unilateral and 2 bilateral. All cases were idiopathic and benign
without an identifiable neurological cause. Rarely, inferior
oblique palsy has been reported after head trauma20 or attributed
to a microvascular occlusive event. Patients with isolated inferior oblique paresis show ipsilateral superior oblique overaction,
but they can be distinguished from those with primary superior
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305
TABLE 9-5. Treatment of Bilateral Superior Oblique Paresis.
Clinical manifestation
Procedure
Extorsional diplopia (partially recovered
traumatic SOP)
Extorsional diplopia (5°), minimal
hypertropia, 8 PD, small or no
V-pattern (10 PD), and minimal
inferior oblique overaction and
superior oblique underaction
Bilateral Harada–Ito
Bilateral superior oblique underaction or
(often traumatic SOP, rarely congenital
lax SO tendon)
Bilateral superior oblique tendon
tuck with bilateral medial rectus
recessions with inferior
transposition one-half tendon
width
Hypertropia 8 PD and big arrow pattern
(15 PD increase in esotropia from
primary to downgaze), 10° extorsion in
primary position increasing in downgaze,
and reversing hypertropias in sidegaze
Masked bilateral or asymmetrical bilateral
superior oblique palsy (usually
congenital SOP)
Hyperdeviation in primary position
10 PD, asymmetrical inferior oblique
overaction
Bilateral inferior oblique graded
anteriorization (more
anteriorized on the side of the
obvious SOP) and recession of
inferior rectus contralateral to
the obvious SOP
or
If associated with a large head tilt,
bilateral inferior oblique graded
anteriorization (more
anteriorized on the side of the
obvious SOP) and Harada–Ito on
the side of the obvious SOP
oblique overaction. Unlike primary superior oblique overaction,
inferior oblique paresis is associated with a positive head tilt test
and a hyperdeviation that is greatest when the patient looks up
and in a horizontal gaze away from the affected eye. For example,
a left inferior oblique paresis results in a right hypertropia that
increases in rightgaze and upgaze, and the hyperdeviation
increases on head tilt to the right. Note that, on versions, inferior oblique paresis looks similar to Brown’s syndrome with
limited elevation in adduction; however, there is an A-pattern
and superior oblique overaction with an inferior oblique palsy,
and forced ductions are negative (Table 9-6).
The treatment of a unilateral inferior oblique paresis is an
ipsilateral superior oblique weakening procedure (e.g., Wright
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TABLE 9-6. Differential Diagnoses of Elevation Deficit in Adduction.
Bilateral
involvement
Pattern
Superior oblique
overaction
Inferior oblique
underaction
Standard forced
ductions
Head tilt test
Torsion
Greatest vertical
deviation
Brown’s syndrome
Primary superior
oblique overaction
Inferior oblique
paresis
Unusual
Common
Unusual
“Y” (divergence
in upgaze)
No
Lambda (divergence
in downgaze)
Yes
“A” (convergence
in upgaze)
Yes
Yes
Minimal to
moderate
Negative
Yes
Positive
Negative
None to slight
intorsion in
upgaze
Upgaze
Negative
Intorsion (increasing
in downgaze)
Downgaze
Negative
Positive
Intorsion
(increasing in
upgaze)
Upgaze
superior oblique tendon expander) if the hypotropia is less than
10 PD, or add a recession of the contralateral superior rectus
recession if the hypotropia is greater than 10 PD.30
Superior Oblique Overaction
The cause of superior oblique overaction (SOOA) is unknown.
It may be related to an associated paresis of the contralateral
inferior rectus muscle, thus producing a secondary overaction of
the yoke superior oblique muscle. The author has noted several
patients with superior oblique overaction who also have an
underacting contralateral inferior rectus muscle.
CLINICAL FEATURES OF SUPERIOR OBLIQUE OVERACTION
Superior oblique overaction is an exaggeration of the normal
function of the superior oblique muscle that includes intorsion,
depression, and abduction. Patients with superior oblique overaction show a downshoot of the adducting eye in lateral gaze,
abduction in downgaze causing an A-pattern, and intorsion that
is seen on indirect ophthalmoscopy. The A-pattern is not symmetrical, but shows more divergence from primary position to
downgaze than from upgaze to primary position. This type of Apattern is termed a lambda pattern (Fig. 9-8).
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307
Superior oblique overaction often occurs in association with
horizontal strabismus such as intermittent exotropia. Most
patients with superior oblique overaction do not show subjective incyclotorsion with Maddox rod testing, even though
indirect ophthalmoscopy reveals intorsion, because sensory
adaptation of the superior oblique overaction has been present
since early infancy. Like inferior oblique overaction, superior
oblique overaction is usually bilateral. Another characteristic of
superior oblique overaction is limited elevation in adduction,
which is secondary to a contracted tight superior oblique
muscle.
DIFFERENTIAL DIAGNOSIS OF SUPERIOR
OBLIQUE OVERACTION
The differential diagnosis of limited elevation in adduction
includes superior oblique overaction, Brown’s syndrome, and
inferior oblique paresis (Table 9-6). Brown’s syndrome is caused
by a tight superior oblique muscle–tendon complex. In Brown’s
syndrome, there is no superior oblique overaction, and forced
ductions are positive to elevation in adduction. In addition, the
syndrome is often associated with an exodeviation when the
eyes move from primary position to upgaze (Y-pattern), whereas
superior oblique overaction is associated with a lambda Apattern.
FIGURE 9-8. Composite nine-gaze photograph of a patient with intermittent exotropia and bilateral superior oblique overaction (3 OU)
with typical A-pattern (lambda subtype) with increasing divergence in
downgaze.
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TREATMENT OF SUPERIOR OBLIQUE OVERACTION
The ideal superior oblique weakening procedure produces a
measured slackening of the muscle–tendon complex without
disrupting the functional mechanics of the insertion. Many
surgical approaches to weaken the superior oblique have been
tried.3,31 Presently, the two procedures most commonly used are
the superior oblique tenotomy and the Wright silicone tendon
expander.38,41 The tenotomy technique involves cutting the
tendon in two, while the silicone tendon expander consists
of inserting a segment of a 240 retinal silicone band (4–6 mm)
between the cut ends of a nasal tenotomy to elongate the
tendon.42
Other superior oblique weakening procedures include tenectomy, recession, and posterior tenotomy.3,31 In a comparative
study, this author found the silicone tendon expander procedure
to be superior to a tenotomy, especially in patients with preoperative fusion.40 Performing a superior oblique tenotomy on
patients with high-grade stereopsis and fusion carries a significant risk for creating a secondary superior oblique paresis and
causing postoperative diplopia.25 In these cases, the silicone
tendon expander is preferred. Another situation where superior
oblique weakening procedures can cause problems is in patients
with preexisting dissociated vertical deviation (DVD); weakening the superior obliques will exacerbate DVD. In these cases,
options are to treat the A-pattern with horizontal rectus muscle
transpositions rather than weakening the superior obliques, or
to plan an undercorrection of the superior oblique overaction
with the silicone tendon expander. The advantage of the superior oblique silicone tendon expander is that it lengthens the
superior oblique tendon in a controlled manner and holds the
cut tendon ends apart at a fixed distance. This technique reduces
postoperative superior oblique paresis, allows for controlled
weakening, and makes it possible to find cut tendon ends if a
reoperation is necessary.
Inferior Oblique Overaction
Primary inferior oblique overaction is most commonly associated with a horizontal strabismus such as congenital esotropia
or intermittent exotropia. Isolated primary inferior oblique overaction can also occur without associated horizontal strabismus.
Although primary inferior oblique overaction is bilateral, in
chapter 9: alphabet patterns and oblique muscle dysfunctions
309
most cases it can be quite asymmetrical, with the lesser
overacting inferior oblique muscle difficult to detect.24 When
inferior oblique overaction is identified, it is important to
differentiate primary inferior oblique overaction from a secondary inferior oblique overaction (i.e., superior oblique paresis). It
can be difficult to differentiate primary inferior oblique overaction from secondary overaction, as patients with marked inferior oblique overaction may have significant superior oblique
underaction secondary to the tight inferior oblique muscle. On
the other hand, patients with a superior oblique paresis
often have inferior oblique overaction. In addition, indirect
ophthalmoscopy will show significant objective extorsion in
both primary and secondary inferior oblique overaction.
The key to distinguishing primary from secondary inferior
oblique overaction is the head tilt test. The head tilt test is negative in primary inferior oblique overaction and is positive with
secondary inferior oblique overaction. In both groups, there is
the typical upshoot of the adducting eye, and both types usually
manifest a significant V-pattern, especially if there is bilateral
inferior oblique overaction. The type of V-pattern, however, can
help differentiate primary versus secondary inferior oblique
overaction. Patients with primary inferior oblique overaction
have a Y-pattern with a significant exotropia shift occurring
from primary position to upgaze but relatively little change
between primary position and downgaze (Fig. 9-9). The Y-pattern
FIGURE 9-9. Composite nine-gaze photograph of patient with bilateral
primary inferior oblique overaction. There is a large V-pattern (Y-subtype)
with divergence in upgaze. The inferior oblique overaction is 3 OU with
no significant superior oblique underaction.
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handbook of pediatric strabismus and amblyopia
occurs because the inferior oblique muscles act as abductors in
upgaze. In contradistinction, a V-pattern associated with superior oblique paresis (especially bilateral) shows an arrow pattern
with an esotropic shift that occurs when moving from primary
position to downgaze. Because the inferior oblique muscle is an
extortor, elevator, and abductor, these elements are exaggerated
in direct proportion to the overaction. When quantitating inferior oblique overaction, look at the entire function of the
muscle, including the upshoot, amount of V-pattern, and fundus
extorsion.10,37
See Table 9-3 for a comparison of the clinical signs of
primary inferior oblique overaction with secondary inferior
oblique overaction caused by superior oblique paresis.
MIMICKERS OF INFERIOR OBLIQUE OVERACTION
Inferior oblique overaction is the most common cause of an
ocular upshoot in adduction. Dissociated vertical deviation
(DVD) can look just like inferior oblique overaction, because
DVD will become manifest in sidegaze as the adducted eye is
occluded by the nasal bridge (see Chapter 10); this results in a
hyperdeviation in sidegaze that mimics inferior oblique overaction. DVD can be differentiated from inferior oblique overaction
by occluding the affected eye in abduction as well as adduction
and evaluating for a change in the vertical deviation. If the elevation is the same in adduction and abduction, then this is DVD,
whereas an increasing hyperdeviation in adduction suggests
inferior oblique overaction. Because DVD commonly coexists
with inferior oblique overaction in patients with infantile
esotropia, the distinction can be extremely difficult to see.
Distinguishing clinical features such as the presence of a Vpattern (Y-subtype), a true hyperdeviation in lateral gaze with a
hypotropia of the contralateral eye, and objective extorsion on
indirect ophthalmoscopy will help to identify inferior oblique
overaction rather than DVD.
An upshoot in adduction can be caused by a tight lateral
rectus muscle. As the eye adducts and slightly elevates, the
tight lateral rectus pulls the eye up, causing pseudo-overaction
of the inferior oblique. Aberrant innervation of the inferior
oblique and superior rectus muscles has been documented as
causing an upshoot associated with Duane’s syndrome (see
Chapter 10).
chapter 9: alphabet patterns and oblique muscle dysfunctions
311
TREATMENT OF INFERIOR OBLIQUE OVERACTION
Surgery is indicated when the inferior oblique overaction and
V-pattern interfere with fusion, or if it becomes a cosmetic
problem. In general, 2 or more inferior oblique overaction
should be considered surgically significant whereas 1 or less
overaction usually does not require treatment. There are,
however, two important exceptions to this rule. The first exception is in patients with bilateral asymmetrical inferior oblique
overaction in which one eye shows minimal overaction. In these
cases, both inferior oblique muscles should be weakened, even
if one only shows trace overaction. Unilateral inferior oblique
weakening surgery in an asymmetrical bilateral case unmasks
the inferior oblique overaction of the nonoperated eye. Inferior
oblique surgery should also be considered for bilateral overaction associated with a significant V-pattern (Y-subtype), even if
there is minimal upshoot on sidegaze. Patients who have a significant divergence when the eyes move from primary position
to upgaze should have inferior oblique weakening surgery,
despite the minimal overaction observed with versions.
In most cases, inferior oblique overaction is bilateral and
bilateral surgery should be performed. Patients with amblyopia
of two lines or greater difference in visual acuity, however,
should have monocular surgery, which should be limited to the
amblyopic eye to avoid the risk (although slight) of surgical complications to the nonamblyopic eye. When inferior oblique overaction coexists with horizontal strabismus, both should be
corrected in the same operation. Staged planning of two separate operations does not improve surgical results and requires a
second round of anesthesia. When planning simultaneous horizontal and inferior oblique surgery, the horizontal surgical
numbers are not altered. Even though the inferior oblique
muscles have an abduction function, weakening the inferior
oblique muscles does not significantly alter the horizontal alignment unless there is an extremely large V-pattern and severe
inferior oblique overaction.
SURGICAL TECHNIQUES FOR WEAKENING THE INFERIOR
OBLIQUE MUSCLES (SEE ALSO CHAPTER 11)
Surgical techniques for correcting inferior oblique overaction
include myectomy, recession, and anteriorization.1,7,19 Recently,
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handbook of pediatric strabismus and amblyopia
the anteriorization procedure has become popular, as results
have been good even in cases of severe overaction. Anteriorization works by transposing the inferior oblique insertion from its
normal position posterior to the equator of the eye to a position
anterior to the equator. When the inferior oblique insertion is
anterior to the equator, the inferior oblique muscle no longer
acts as an elevator but, instead, pulls the front of the eye down;
now, it is actually a depressor. This change is why anteriorization procedures that place the inferior oblique muscle anterior
to the inferior rectus insertion can cause the complication of an
ipsilateral hypodeviation and limited elevation.4,33 This complication can be avoided by keeping the anterior inferior oblique
muscle fibers posterior to the inferior rectus insertion. Keeping
the posterior fibers of the inferior oblique muscle at least 3 mm
posterior to the inferior rectus insertion is especially important
because of the inferior oblique neurovascular bundle.34,35 The
neurovascular bundle is a relatively inelastic structure inserting in the posterior aspect of the inferior oblique muscle. If the
posterior fibers are anteriorized to the level of the inferior rectus
insertion, the neurovascular bundle will tighten and act as a
tether holding the eye down. Anteriorizing the posterior fibers
produces a J-deformity of the inferior oblique insertion. This
author prefers avoiding the J-deformity and has developed a
graded anterior transposition procedure that keeps the posterior
fibers posterior to the anterior fibers. The graded anterior transposition procedure yields excellent results, even in severe cases,
without the complication of limited elevation.9 Because the full
anteriorization procedure with a J-deformity causes limited elevation, it is rarely indicated. However, it can be considered if
performed bilaterally for severe bilateral inferior oblique overaction with a large DVD.
Brown’s Syndrome
ETIOLOGY
Brown’s syndrome is a restrictive strabismus characterized by
limitation of elevation that is worse when the eye is in adduction (Fig. 9-10A). It can be congenital or acquired, with a variety
of causes for the restriction of elevation in adduction (see Table
9-7). The term congenital Brown’s syndrome or “true” Brown’s
syndrome, is used to refer to Brown’s syndrome caused by a congenitally inelastic superior oblique muscle–tendon complex.36
chapter 9: alphabet patterns and oblique muscle dysfunctions
313
FIGURE 9-10A,B. (A) Preoperative composite nine-gaze photograph of
patient with congenital Brown’s syndrome, right eye, with limited elevation in adduction and minimal to no superior oblique overaction. Note
Y-pattern with exodeviation in upgaze. Also note there is some limitation of the right eye even in abduction, but the limitation is greatest in
adduction. Despite the severe limitation of elevation, there is only trace
hypotropia in primary position. (B) Postoperative photograph after a
Wright’s superior oblique tendon silicone expander, right eye, for Brown’s
syndrome. Note the versions are almost normal with only a trace limitation to elevation, which is the optimal result, with a slight residual limitation of elevation in adduction right eye. This was the author’s first
silicone expander patient, and the results have remained excellent over
11 years of follow-up.
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handbook of pediatric strabismus and amblyopia
TABLE 15-7. Classification of Brown’s Syndrome.
I. Congenital onset
A. True congenital Brown’s syndrome (superior oblique etiology)
i. Unknown: probable inelastic muscle–tendon complex
B. Congenital pseudo-Brown’s syndrome (nonsuperior oblique cause)
i. Anomalous inferior orbital adhesions
ii. Posterior orbital bands
iii. Anomalous insertion of rectus muscle and pulley (e.g., inferior
displacement of lateral rectus pulley or insertion)
II. Acquired onset
A. Superior pblique or trochlear etiology
i. Peritrochlear scarring and adhesions
1. Chronic sinusitis
2. Trauma: superior temporal orbit
3. Blepharoplasty and fat removal
4. Lichen sclerosus et atrophicus and morphea
ii. Tendon–trochlear inflammation and edema
1. Idiopathic inflammatory (pain and click)
2. Trochleitis with superior oblique myocytis
3. Acute sinusitis
4. Adult rheumatoid arthritis
5. Juvenile rheumatoid arthritis
6. Systemic lupus erythematous
7. Possibly distant trauma (CPR and long bone fractures)
8. Possibly hormonal changes postpartum
iii. Superior nasal orbital mass
1. Glaucoma implant
2. Neoplasm
iv. Tight or inelastic superior oblique muscle
1. Thyroid disease (inelastic muscle)
2. Peribulbar anesthesia (inelastic tendon)
3. Hurler–Scheie’s syndrome (inelastic tendon)
4. Superior oblique tuck (short tendon)
v. Idiopathic
B. Nonsuperior oblique or trochlear causes
i. Floor fracture
ii. Retinal band around inferior oblique muscle
iii. Inferior temporal adhesions
Source: From Ref. 32, with permission.
There are nonsuperior oblique causes for congenital Brown’s
syndrome, including inferior orbital mechanical restriction,
superior nasal orbital mass, and inferior displaced lateral rectus
muscle and pulley.22,36
CLINICAL FEATURES OF BROWN’S SYNDROME
The hallmark of Brown’s syndrome, regardless of the cause, is
limited elevation in adduction. In congenital Brown’s syndrome,
chapter 9: alphabet patterns and oblique muscle dysfunctions
315
this occurs because the tight posterior tendon fibers prevent the
back of the eye from rotating down; therefore, the front of the
eye cannot elevate.36 This restriction is a constant limitation and
does not improve or resolve on its own. Typically, on clinical
examination, there is minimal to no hypotropia in primary position, minimal to no superior oblique overaction, limited elevation in adduction, and divergence (Y-pattern) in upgaze (Fig.
9-10A).36 There is often some limitation of elevation in abduction, but the key is that the limitation is much worse in adduction.36 Limited elevation in abduction can produce
pseudoinferior oblique overaction of the fellow eye because of
Hering’s law.36 Intorsion on attempted upgaze has been
reported.36 Patients with Brown’s syndrome usually have excellent binocular fusion, as they adopt a compensatory chin elevation and a face turn away from the Brown’s eye to maintain
fusion. A patient with a right Brown’s syndrome will have a chin
elevation and a face turn to the left.
Standard forced-duction testing shows a restriction to elevation in adduction. If the Brown’s syndrome is caused by a tight
superior oblique tendon, then Guyton’s exaggerated forcedduction testing of the superior oblique muscle will reveal a
restriction to the eye moving up and in.
ACQUIRED BROWN’S SYNDROME
Causes of acquired Brown’s syndrome include pathology of the
superior oblique tendon and trochlea and nonsuperior oblique
pathology.36 Causes for trochlear or tendon abnormalities
include repeat upper eyelid blepharoplasty, sinusitis with peritrochlear inflammation, rheumatoid arthritis, and a superior
nasal mass deflecting the course of the superior oblique tendon
(e.g., superior nasal glaucoma implant or superior nasal orbital
tumor). Inflammatory Brown’s syndrome may be idiopathic
primary trochleitis or secondary to sinusitis. Acquired nonsuperior oblique or trochlear causes of limited elevation in
adduction include floor fracture, inferior scarring of the globe,
fat adherence after inferior oblique muscle surgery, and strabismus surgery with inferior transposition of horizontal rectus
muscles (e.g., infraplacement of a lateral rectus resection and
medial rectus recession). Furthermore, many patients will
develop an acquired Brown’s syndrome of unknown etiology
(Table 9-6).
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handbook of pediatric strabismus and amblyopia
Idiopathic acquired Brown’s syndrome is often intermittent
and sometimes associated with a “click” that is felt by the
patient in the superior nasal quadrant when the patient looks up
and in. In some cases, the click can be heard with a stethoscope
placed in the superior nasal quadrant. The cause of the click and
limited elevation is not known, but it may represent inflammation or an abnormality of fascial tissue around the superior
oblique tendon. If the cause of an acquired Brown’s syndrome is
in question, then orbital imaging studies are indicated. In many
cases, acquired Brown’s syndrome will spontaneously resolve
over several months to even several years. Surgery should only
be considered after the patient has been observed for at least 6
months to 1 year.
Another form of acquired Brown’s syndrome is inflammatory
Brown’s syndrome, which is associated with superonasal orbital
pain and tenderness. It is hypothesized that trochlear or peritrochlear inflammation is the cause. In some cases, inflammatory Brown’s syndrome is associated with a concurrent sinusitis36
or rheumatoid arthritis (rarely). In the majority of cases, however,
the cause of the inflammation is unknown.
The treatment of inflammatory Brown’s syndrome includes
a trial of systemic nonsteroidal antiinflammatory agents (e.g.,
indomethacin 25–50 mg TID) or a local steroid injection in the
area of the trochlea. A patient diagnosed with acquired Brown’s
syndrome of unknown etiology should undergo workup with
orbital imaging, as a variety of local or systemic diseases involving the trochlea may cause a Brown’s syndrome. Medical
therapy, not surgery, is the treatment of choice for most cases
of inflammatory Brown’s syndrome.
CONGENITAL ELEVATION DEFICIT:
DIFFERENTIAL DIAGNOSIS
Congenital causes for limited elevation include double elevator
palsy (see Chapter 10), Brown’s syndrome, inferior oblique
paresis, and superior oblique overaction. Double elevator palsy
can be distinguished by the presence of similar limitation in
abduction and adduction, while primary superior oblique overaction and inferior oblique paresis may be more difficult to
differentiate because they have a greater elevation deficit in
adduction. See Table 10-6 for a comparison of the clinical
findings of superior oblique overaction, Brown’s syndrome, and
inferior oblique paresis.
chapter 9: alphabet patterns and oblique muscle dysfunctions
317
SURGICAL INDICATIONS FOR CONGENITAL
BROWN’S SYNDROME
In general, surgery should be considered for Brown’s syndrome
if there is a hypodeviation in primary position that causes a significant chin elevation. Patients with a minimal restriction and
no significant face turn can be managed conservatively. Except
for a few exceptions, surgery should be reserved for children
older than 4 years of age; older children are less likely to develop
postoperative suppression and amblyopia. Rarely, one may be
forced to operate on a child under 4 years of age if the hypodeviation is large enough to disrupt fusion.
SURGERY FOR CONGENITAL BROWN’S SYNDROME
Management of congenital Brown’s syndrome is based on lengthening the superior oblique tendon.39 Procedures such as
tenotomy and tenectomy release the restriction but are not
controlled, as the cut ends of the tendon can separate widely and
result in a superior oblique paresis. In Brown’s syndrome, the
superior oblique muscle is not overacting and, therefore, procedures such as tenotomy or tenectomy often result in a secondary superior oblique paresis. In a study by Eustis et al., 85% of
Brown’s patients demonstrated some degree of posttenotomy
superior oblique paresis, with one-third requiring a second operation.8 Sprunger et al. reported that 50% of their study patients
required further surgery caused by an ipsilateral superior oblique
paresis after superior oblique tenotomy.32 To address this
problem, Parks has previously suggested performing an ipsilateral inferior oblique recession at the same time as the superior
oblique tenotomy. This approach, however, results in prolonged
underaction of the inferior oblique and a persistence of Brown’s
syndrome.
To achieve a controlled elongation of the superior oblique
tendon, this author has developed a procedure called the Wright
superior oblique tendon expander (see Chapter 11). A segment
of retinal silicone band (usually 6.0 mm long) is carefully sutured
between the cut ends of the superior oblique tendon, 3 mm nasal
to the superior rectus muscle. The initial conjunctival incision,
however, is made temporal to the superior rectus muscle. The
temporal incision is stretched nasally to expose the nasal aspect
of the superior rectus muscle. This maneuver preserves nasal
intermuscular septum so the silicone segment does not scar to
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sclera. With the capsule floor intact, the silicone is actually
placed within the superior oblique tendon capsule. Parks, this
author, and others have obtained excellent results using the
superior oblique tendon expander. The expander allows for
controlled and reversible elongation of the tendon while maintaining the functional integrity of the superior oblique
muscle–tendon complex. In trained hands, complications of the
procedure are rare, but these include extrusion of silicone and
scarring of the silicone to the sclera, causing postoperative limitation of depression. These complications can be limited by
meticulous technique and limiting the maximum length of the
silicone segment to 7.0 mm. Many now consider the superior
oblique silicone tendon expander the procedure of choice for
Brown’s syndrome.
RESULTS
OF THE
SILICONE TENDON EXPANDER
This author has reported his long-term results using the
Wright superior oblique silicone tendon expander on
patients with severe Brown’s syndrome (see Fig. 9-10A,B).41 Of
15 patients operated on by the author, preoperative limitation
of elevation in adduction measured 3 in 1 patient and 4
in 14 patients. Postoperatively, 14 of the 15 patients showed
improved motility with 10 patients demonstrating essentially
normal versions. The 1 patient who did not improve after the
silicone expander had a nonsuperior oblique tendon cause of
Brown’s syndrome. The average final result graded on a scale
of 1 to 10 (10 being best) was 8.3. Thirteen (13) of 15 patients
(87%) achieved a final result score of 7 or better with a single
surgery, and an additional patient was corrected with a second
surgery providing an overall success rate of 93%. Ten of the
15 patients had at least 11 months follow-up, with 6 of the 10
patients showing a delayed improvement over a 4- to 6-month
period. Five patients had more than 5 years follow-up and 4
(80%) had an excellent long-term outcome (final result, 9–10)
with a single operation. All 5 patients had a good outcome
(final result, 7–10; mean, 9.2) with 1 patient requiring a second
surgery. There were no long-term complications, including
no extrusions, no restriction of ocular rotations, and no
infections.
Stager et al.34 also reported good long-term results; however,
in both papers, Wright and Stager emphasized the importance of
surgical technique.34,41 Keep the nasal intermuscular septum
and the floor of the superior oblique tendon capsule intact. Also,
chapter 9: alphabet patterns and oblique muscle dysfunctions
319
perform the tenotomy at least 3 mm nasal to the superior rectus
muscle to avoid adhesions to the superior rectus muscle. Finally,
use 5 to 6 mm of silicone band segment for Brown’s syndrome.
Both papers also commented on late improvement after surgery.
Some patients showed a significant undercorrection immediately after surgery, but then improved to have excellent result
by weeks, to even months, after surgery. The Wright silicone
tendon expander is an effective option for correcting Brown’s
syndrome, caused by a stiff or inelastic superior oblique tendon,
with excellent long-term outcomes. Proper technique with
maintenance of the tendon capsule is critical to the successful
outcome of the procedure.43
CANINE TOOTH SYNDROME
Scarring in the area of the superior oblique tendon and trochlea
will limit movement of the tendon in both directions, resulting
in a Brown’s syndrome with a superior oblique paresis. This disorder has been called “Canine tooth syndrome” or Knapp type
7 classification.2,14,15,18,21,43 In this author’s thesis43 on Brown’s
syndrome, three patients were diagnosed as having Canine tooth
syndrome with both restrictive elevation in adduction and a
superior oblique palsy. All three cases presented with penetrating trauma to the trochlear area, two by metal hooks and one
from a dog bite. Management of these cases is difficult, as
surgery in the area of the trochlea can lead to further scarring
and worsening of the condition. In the acute phase immediately
after trauma, local corticosteroid injection might help reduce
secondary fibrosis.2 Initial management is conservative observation because spontaneous improvement may occur.18 If the
deviation persists after 4 to 6 months, then surgical correction
can be considered. In these cases, it is best to correct the strabismus by operating on the extraocular muscles rather than
trying to remove fibrosis in the trochlear area.43
References
1. Apt L, Call NB. Inferior oblique muscle recession. Am J Ophthalmol
1978;95:95.
2. Bachynski BN, Flynn JT. Direct trauma to the superior oblique
tendon following penetrating injuries of the upper eyelid. Arch
Ophthalmol 1985;103:1510–1514.
3. Berke RN. Tenotomy of the superior oblique for hypertropia. Trans
Am Ophthalmol Soc 1946;44:304–342.
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4. Bremer DL, Rogers GL, Quick LD. Primary position hypotropia after
anterior transposition of the inferior oblique. Arch Ophthalmol 1986;
104:229–232.
5. Cheng H, Burdon MA, Shun GA, Czypionka S. Dissociated eye
movements in craniosynostosis: a hypothesis revived. Br J Ophthalmol 1993;77:563–568.
6. Demer JL. Orbital connective tissue in binocular alignment and strabismus. In: Lennerstrand G (ed) Advances in strabismus research:
basic and clinical aspects. London: Portland Press, 2000:17–31.
7. Elliot L, Nankin J. Anterior transposition of the inferior oblique.
J Pediatr Ophthalmol Strabismus 1981;18:35.
8. Eustis HS, O’Reily C, Crawford JS. Management of superior oblique
palsy after surgery for true Brown’s syndrome. J Pediatr Ophthalmol
Strabismus 1987;24:10–16.
9. Guemes A, Wright KW. Effect of graded anterior transposition of the
inferior oblique muscle on versions and vertical deviation in primary
position. J Am Assoc Pediatr Ophthalmol Strabismus 1998:2:201–
206.
10. Guyton DL. Clinical assessment of ocular torsion. Am Orthopt J
1983;33:7.
11. Harada M, Ito Y. Visual correction of cyclotropia. Jpn J Ophthalmol
1964;8:88.
12. Helveston EM. Classification of superior oblique muscle palsy. Ophthalmology 1992;99:1609–1615.
13. Helveston EM. A two-step test for diagnosing paresis of a single
vertically acting extraocular muscle. Am J Ophthalmol 1967;64(5):
914–915.
14. Helveston EM, Birchler C. Class VII superior oblique palsy: subclassification and treatment suggestions. Am Orthopt J 1982;32:104–
110.
15. Knapp RP. Classification and treatment of superior oblique palsy. Am
Orthopt J 1974;24:18–22.
16. Kraft SP, Scott WE. Masked bilateral superior oblique palsy: clinical
features and diagnosis. J Pediatr Ophthalmol Strabismus 1986;23(6):
264–272.
17. Kushner BJ. The diagnosis and treatment of bilateral masked
superior oblique palsy. Am J Ophthalmol 1988;105(2):186–194.
18. Legge RH, Hedges TR III, Anderson M, et al. Hypertropia following
trochlear trauma. J Pediatr Ophthalmol Strabismus 1992;29(3):163–
166.
19. Mims JL, Wood RC. Bilateral anterior transposition of the inferior
obliques. Arch Ophthalmol 1989;107:41.
20. Muchnick RS, Stoj M, Hornblass A. Traumatic inferior oblique
muscle paresis. J Pediatr Ophthalmol Strabismus 1985;22(4):143–
146.
21. Neely KA, Ernest JT, Mottier M. Combined superior oblique paresis
and Brown’s syndrome after blepharoplasty. Am J Ophthalmol 1990;
109(3):347–349.
chapter 9: alphabet patterns and oblique muscle dysfunctions
321
22. Oh SY, Clark RA, Velez F, Demer JL. Magnetic resonance imaging
(MRI) demonstration of instability of rectus pulleys as cause of
incomitant strabismus. Investig Ophthalmol Vis Sci 2001;42(4):167.
23. Parks M. Isolated cyclovertical muscle palsy. Arch Ophthalmol
1958;60:1027.
24. Parks MM. The overacting inferior oblique muscle. Am J Ophthalmol 1974;77:787.
25. Parks MM. Bilateral superior oblique tenotomy for A-pattern
strabismus in patients with fusion (commentary). Binoc Vis 1988;
3:39.
26. Paysee EA, Coats DK, Plager DA. Facial asymmetry and tendon
laxity in superior oblique palsy. J Pediatr Ophthalmol Strabismus
1995;32(3):158–161.
27. Plager DA. Traction testing and superior oblique palsy. J Pediatr
Ophthalmol Strabismus 1990;27:136–140.
28. Pollard ZF. Diagnosis and treatment of inferior oblique palsy. J
Pediatr Ophthalmol Strabismus 1993;30(1):15–18.
29. Raina J, Wright KW, Lin MM, McVey JH. Effectiveness of lateral
rectus Y-split surgery for correcting the upshoot and downshoot in
Duane’s retraction syndrome, type III. Binoc Vis Strabismus 1997;
12(4):233–238.
30. Reese PD, Scott WE. Superior oblique tenotomy in the treatment of
isolated inferior oblique paresis. J Pediatr Ophthalmol Strabismus
1987;24(1):4–9.
31. Romano P, Roholt P. Measured graduated recession of the superior
oblique muscle. J Pediatr Ophthalmol Strabismus 1983;20:134–140.
32. Sprunger DT, von Noorden GK, Helveston EM. Surgical results in
Brown’s syndrome. J Pediatr Ophthalmol Strabismus 1991;28(3):164–
167.
33. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch
Ophthalmol 1992;110:360.
34. Stager DR, Stager D, Parks MM. Long-term results of silicone
expander for moderate and severe Brown’s syndrome. J Am Assoc
Pediatr Ophthalmol Strabismus 1999;3:328–332.
35. Stager DR. The neurofibrovascular bundle of the inferior oblique
muscle as its ancillary origin. Trans Am Ophthalmol Soc 1996;94:
1073–1094.
36. Wright KW. Color atlas of strabismus surgery: strategies and techniques. Torrance, CA: Wright 2000:184–203.
37. Wright KW. Current approaches to inferior oblique muscle surgery.
In: Hoyt CS (ed) Focal points 1986: clinical modules for ophthalmologists. Am Acad Ophthalmol 1986;1.
38. Wright KW. Superior oblique silicone expander for Brown’s syndrome
and superior oblique overaction. J Pediatr Ophthalmol Strabismus
1991;28:101–107.
39. Wright KW. Surgical procedure for lengthening the superior oblique
tendon. Investig Ophthalmol Vis Sci 1989;30(suppl):377.
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40. Wright KW, Min BM, Park C. Comparison of superior oblique tendon
expander to superior oblique tenotomy for the management of superior oblique overaction and Brown’s syndrome. J Pediatr Ophthalmol
Strabismus 1992;29:92–99.
41. Wright KW. Results of the superior oblique tendon elongation procedure for severe Brown’s syndrome. Trans Am Ophthalmol Soc
2000;98:41–50.
42. Wright KW. Superior oblique silicone expander for Brown’s syndrome
and superior oblique overaction. J Pediatr Ophthalmol Strabismus
1991;28:101–107.
43. Wright KW. Brown’s syndrome: diagnosis and management. Trans
Am Ophthalmol Soc 1999;97:1023–1109.
10
Complex Strabismus:
Restriction, Paresis,
Dissociated Strabismus,
and Torticollis
Kenneth W. Wright
T
his chapter on complex strabismus reviews the evaluation
and management of incomitant strabismus associated
with rectus muscle paresis and ocular restriction. Other topics
include dissociated strabismus complex, torticollis, and nystagmus. Incomitant strabismus is a deviation that changes in
different fields of gaze. Incomitance can be caused by ocular
restriction, extraocular muscle paresis, or oblique muscle dysfunction or can be associated with a primary A- or V-pattern.
The diagnosis and treatment of oblique muscle dysfunction
(palsy and overaction), Brown’s syndrome, and A- and V-patterns
are covered in Chapter 9.
PARALYTIC RECTUS MUSCLES AND
RESTRICTIVE STRABISMUS:
GENERAL PRINCIPLES
If an eye has limited ductions, there are only two basic causes:
extraocular muscle paresis or ocular restriction. Therefore, a
strabismus associated with limited ductions is secondary to
extraocular muscle paresis, ocular restriction, or both.
Paresis
Extraocular muscle paresis means weak muscle pull, whereas
palsy indicates a complete lack of muscle function. Cranial
323
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handbook of pediatric strabismus and amblyopia
nerve paresis and primary muscle disease are obvious reasons
for a weak muscle that can cause limited ocular rotations. A
muscle paresis can also be caused by ineffective muscle pull on
the eye, or mechanical disadvantage of muscle pull. Clinical
examples of conditions that cause mechanical disadvantage of
muscle pull include:
• A scarred or tethered muscle preventing transmission of
muscle pull to the globe (e.g., floor fracture with entrapped
inferior rectus muscle)
• A posteriorly displaced rectus muscle (e.g., slipped muscle)
• A muscle shifted out of its appropriate plane, thus diminishing the vector force in the field of action of the muscle
(e.g., high myopia with displaced lateral rectus muscle)
Table 10-1 lists the three major causes of a mus-cle paresis:
(1) cranial nerve paresis, (2) primary muscle disease, and (3)
mechanical disadvantage of muscle pull. Specific types of paralytic strabismus, including sixth and third nerve palsies, are
covered later in this chapter.
TABLE 10-1. Causes of Muscle Paresis.
a
Cranial nerve palsy
Primary muscle
disease
Mechanical disadvantage
of muscle pull
Third nerve palsy
Botulism
Fourth nerve palsya
(superior oblique
palsy)
Sixth nerve palsy
Myasthenia gravis
Stretched scar after muscle
surgery
Slipped muscle or lost muscle
CPEO
Trauma to muscle
Miller–Fisher
syndrome
(Guillain-Barré)
Cranial nerve aberrant
innervation
syndromes (e.g.,
Duane’s syndrome)
Agenesis of an
extraocular muscle
often associated
with a craniofacial
disorder
See Chapter 9.
Canine tooth syndrome with
scarring of trochlea causing
Brown’s syndrome with
superior oblique palsy
Floor fracture with an
entrapped inferior rectus
muscle causing limited
depression
High myopia with large
posterior staphyloma, and
slippage of lateral rectus
below globe reducing lateral
rectus abduction force,
causing esotropia
chapter
10:
complex strabismus
325
Ocular Restriction
Classically, the term ocular restriction describes a mechanical
tether or leash that limits ocular rotations. Ocular restriction,
however, can be caused by at least two general mechanisms: a
mechanical tether on eye movements or misdirected muscle
forces that work against the normal agonist muscle function.
The term restriction is often loosely used as a general term for
limited eye movements; however, a clear distinction should be
made between ocular restriction and rectus muscle palsy. If the
cause of diminished eye movements is not known, then use the
term limited rotations or limitation of eye movements until
the etiology is determined. Table 10-2 lists the causes of restrictive strabismus.
Mechanical restriction of eye movement is caused by adhesions to an extraocular muscle or sclera, a tight or inelastic
extraocular muscle, or an orbital mass. Restrictive adhesions can
occur from conjuctival scarring, scarring of Tenon’s capsule,
orbital fat adherence, and, rarely, congenital fibrotic bands that
attach to the eye or extraocular muscles. Inelastic muscle or
muscle fibrosis occurs with thyroid myopathy, local anesthesia
myotoxicity, and congenital muscle fibrosis (e.g., monocular
elevation deficit and congenital fibrosis syndrome). An orbital
mass, such as an orbital hemangioma, or a glaucoma implant
can cause ocular restriction either by direct interference of rotation of the eye or by pressure on an extraocular muscle that
tightens the muscle. Restriction resulting from misdirected
muscle force vectors occurs in conjunction with aberrant innervation of an antagonist muscle and abnormal muscle–pulley
location or a displaced extraocular muscle.20,25,83 An example of
aberrant innervation causing restriction is limited adduction,
often associated with Duane’s syndrome. Restricted adduction
occurs because the lateral rectus muscle is aberrantly innervated
by part of the medial rectus nerve. When the eye attempts to
adduct, the lateral rectus muscles contracts against the contracting medial rectus muscle, thus restricting adduction.
An example of displaced extraocular muscle is the V-pattern
strabismus and superior oblique muscle underaction that are frequently seen in patients with craniosynostosis.20 These patients
have excyclorotation of the orbits that results in superior
displacement of the medial rectus muscle and limited ocular
depression in adduction. The superiorly displaced medial rectus
muscle pulls the eye up in addition to its normal function of
Acquired Brown’s syndrome:
scarring or inflammation
around the trochlea
Thyroid: Graves disease
Congenital fibrosis syndrome
Congenital Brown’s syndrome: inelastic
SO muscle tendon
complex (see Chapter 9)
SO, superior oblique.
Fat adherence to extraocular muscle (e.g.,
after strabismus surgery, retinal surgery,
or periocular trauma)
Monocular elevation deficit syndrome
caused by a fibrotic inferior rectus
Entrapped muscle after orbital fracture
(inferior rectus most common)
Fibrosis after local anesthetic injection
into a muscle (inferior most common)
Structural adhesions
Fat adherence to muscle or sclera
(e.g., after strabismus surgery,
retinal detachment surgery,
or periocular trauma)
Congenital fibrotic band
Tight extraocular muscle
Mechanical restriction
TABLE 10-2. Causes of Ocular Restriction.
Orbital mass
Orbital tumor causing
mass effect on globe
movement
Glaucoma explant with
large bleb causing
mass effect on globe
movement or displace
SO tendon (acquired
Brown’s syndrome)
High myopia with large
posterior staphyloma
(Duane’s syndrome)
Misdirected muscle forces
High myopia with large posterior
staphyloma and slippage of lateral
rectus below globe
Congenital ectopic extraocular muscle
insertion and or pulley
(craniosynostosis, extorted orbit)
Iatrogenic displaced muscle insertion;
antielevation after inferior oblique
anteriorization with J-deformity, and
limited depression after anterior
displacement of SO tendon by
retinal band
Congenital cranial nerve aberrant
innervation
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adduction and limits depression in the field of action of the superior oblique.20 A rare example of restriction caused by a displaced
muscle–pulley was reported by Oh et al.83 They described a
patient with limitation of elevation in adduction, or a pseudoBrown’s syndrome, caused by a congenitally inferiorly displaced
lateral rectus muscle and its pulley. These authors hypothesized
that the infraplaced lateral rectus muscle and pulley act to pull
the eye down, limiting elevation on adduction. Iatrogenic displacement of extraocular muscles during strabismus surgery can
also cause limited eye movements. Inferior oblique muscle
anteriorization anterior to the inferior rectus insertion can also
cause active restriction and limited elevation (see Chapter 2,
Fig. 2–17).15,43,114,135 In some cases, restriction and paresis coexist,
such as with paretic lateral rectus muscle and secondary contracture of its antagonist medial rectus muscle. It is important
to diagnoses the cause of limited ductions to formulate an effective surgical plan. The next section describes methods for diagnosing extraocular muscle paresis and ocular restriction.
Diagnosing Restriction Versus Paresis
The principal diagnostic tests that differentiate paresis from
restriction include saccadic velocity measurements, forced ductions, and forced-generation test. Other signs influencing diagnosis include intraocular pressure changes in various fields of
gaze and lid fissure changes in sidegaze.
SACCADIC VELOCITY MEASUREMENTS
Saccadic velocity measurements can help differentiate restriction from paresis by observation, without touching the eye.
Therefore, this method is useful in young children as well as
adults. Saccadic movements are fast, jerk-like eye movements
that require normal rectus muscle function. The rectus muscles
are the major movers of the eye and are responsible for saccadic
eye movements. The presence of a saccadic eye movement indicates normal rectus muscle function whereas the inability to
stimulate a saccade suggests a rectus muscle palsy. A paretic
rectus muscle does not have the power to generate a saccadic
eye movement, and the eye drifts slowly to the intended field
of gaze. Strabismus associated with limited ductions and
diminished saccadic velocity is caused by a rectus muscle
paresis, not an oblique muscle palsy.
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In contrast to a rectus muscle paresis, ocular restriction is
associated with normal, but shortened, saccadic movements as
the eye stops abruptly when the restriction is met. This eye
movement pattern of a fast eye movement that stops abruptly
as it meets the restriction is termed the dog on a leash; it is analogous to a dog lunging after a cat, then being abruptly stopped
by its leash (Fig. 10-1). In patients with limited eye movements,
it is important to clinically test for saccadic eye movements
before surgery to assess muscle function. At the time of surgery
when the patient is under anesthesia, it is impossible to test
muscle function. Positive forced ductions at the time of surgery
indicate only passive restriction and do not exclude the possibility of coexisting muscle palsy.
Horizontal and vertical eye movements can be measured by
laboratory tests including electro-oculogram (EOG) recordings
and infrared eye trackers. Clinical observation of eye movements can also be used in clinical practice for evaluating the
presence of a saccadic movement; this is facilitated through the
use of an optokinetic nystagmus (OKN) drum for young children
who are not able to follow instructions as well as for cooperative patients to compare eye movements (Fig. 10-2). Rotate the
OKN drum and observe the patient’s eyes for a brisk redress
FIGURE 10-1. “Dog on a Leash.” The pattern of a fast eye movement
that stops abruptly indicates a mechanical restriction. Upper: cartoon
shows a dog on a leash walking toward a cat behind a tree. Lower: The
dog sees the cat and leaps for the cat but is stopped abruptly by the leash.
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FIGURE 10-2. Photograph of a child being examined with an optokinetic
nystagmus (OKN) drum. The saccadic movement will be in the direction
opposite to the drum rotation. This is a good clinical method to estimate
if a saccade is present.
movement opposite to the direction of the drum rotation.
Compare eye to eye and look for asymmetry of the OKN
response. An inability to generate a saccadic movement indicates a paretic rectus muscle.
FORCED DUCTIONS
Forced ductions identify the presence of a mechanical restriction to ocular rotation; these are performed by grasping the eye
with a forceps and then passively moving the eye into the field
of limited ocular rotation. If the eye shows a resistance to rotation with the forceps (positive forced ductions), then there is a
mechanical restriction. When performing forced ductions for
possible rectus muscle restriction, proptose the eye to stretch
the rectus muscles. This maneuver will allow identification of
restriction caused by a tight rectus muscle. If the examiner inadvertently retropulses the eye, the rectus muscles slacken and
produce a negative forced-duction test, even if the rectus muscle
is tight (Fig. 10-3). The opposite holds true for oblique muscle
forced ductions, because retropulsing the eye will stretch the
oblique muscles and accentuate a tight oblique muscle. If a
restriction is worse with retropulsion of the eye, then the restriction is not caused by a tight rectus muscle but, instead, is
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A
B
FIGURE 10-3A,B. (A) The proper technique for rectus muscle forced ductions includes grasping the conjunctiva with a 2 3 Lester forceps at the
limbus, just anterior to the muscle insertion. First, proptose the eye, and
then pull the eye away from the muscle being tested, thus placing the
rectus muscle on stretch. This maneuver allows identification of even
mildly tight or restricted muscles. (B) The improper technique for rectus
muscle forced ductions shows the eye being retropulsed during the
maneuver, causing iatrogenic slackening of the muscle and a false-normal
forced-ductions test. Positive forced ductions that do not improve when
the eye is intentionally retropulsed suggest the presence of a nonrectus
muscle restriction, such as periocular scarring (e.g., fat adherence).
secondary to either a periocular adhesion or a tight oblique
muscle.
Forced-duction testing can be used as an in-office test using
topical anesthesia, or at the time of strabismus surgery. In most
cases, the pattern of the eye movements, including the clinical
evaluation for saccades, establishes the diagnosis of restriction
or paresis. Therefore, in-office forced-duction testing is usually
not necessary. If surgery is indicated, forced- duction testing can
be performed at the time of surgery to verify the diagnosis. It is
important to remember that positive forced ductions does not
exclude the presence of a coexisting palsy. In fact, most cases of
long-standing rectus muscle palsy also have contracture of the
antagonist muscle, so forced ductions will be positive. Preoperative evaluation of muscle function by saccadic eye movement
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testing or the forced-generation test (see next section) is required
to diagnose a rectus muscle palsy.
FORCED-GENERATION TEST
The forced-generation test directly measures active muscle force
and is useful for diagnosing a rectus muscle palsy. To perform
this test, the eye is topically anesthetized and grasped with
forceps; the patient is asked to look into the field of limited rotation. A sterile cotton-tipped applicator can also be used to push
against the eye to feel the abduction force, as noted in Chapter
5 (Fig. 5-16A,B). The examiner feels the pull of the muscle
against the forceps or cotton-tipped applicator and compares this
to the fellow eye or the antagonist muscle. If there is diminished
pull from the muscle into the field of limited rotation, then a
paresis is present. Forced ductions can be used in conjunction
with forced-generation testing. If forced ductions are positive
and the force-generation test shows poor muscle function, then
the diagnosis is a combination of restriction and paresis.
INTRAOCULAR PRESSURE CHANGE ON EYE MOVEMENT
Another sign of restriction is increased intraocular pressure on
attempted duction into the field of limited movements and away
from a restriction or tight muscle. Intraocular pressure increases
as the eye forcibly attempts to move against the restriction.
Patients with thyroid myopathy and strabismus may show
increased intraocular pressure when the pressure reading is
made with the restricted eye in forced primary position.
LID FISSURE CHANGES ON EYE MOVEMENT
Ocular restriction caused by a tight rectus muscle or a restrictive adhesion to the globe will cause globe retraction and lid
fissure narrowing as the agonist rectus muscle attempts to pull
the eye away from the restriction [see Duane’s syndrome (Fig.
10-12), later in this chapter]. These movements occur because
the eye is restricted from rotating; therefore, the contracting
agonist muscle pulls the eye posteriorly and causes globe
retraction and lid fissure narrowing. A rectus muscle paresis
will cause the opposite: lid fissure widening and relative proptosis. As the patient looks into the field of action of the paretic
rectus muscle, the agonist muscle relaxes secondary to
the palsy. The antagonist muscle also relaxes because of
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Sherrington’s law, and pressure from orbital fat pushes the
eye forward. A patient with a sixth nerve palsy, for example,
will show lid fissure widening on attempted abduction (see
Fig. 10-10, later in this chapter). This change occurs because
the medial rectus muscle relaxes on attempted abduction
(Sherrington’s law) and, along with the paretic lateral rectus, it
is loose; therefore, the posterior pressure of the orbital fat
pushes the eye forward.
MANAGEMENT OF INCOMITANT
STRABISMUS: GENERAL PRINCIPLES
Management begins with understanding why the deviation is
incomitant. For example, if an incomitant strabismus is associated with severe limitation of ductions, determine whether the
limitation is caused by restriction or paresis. If a significant
restriction is the cause of limited adduction, then one must
release the restriction. If severe limitation of ocular rotations is
secondary to poor rectus muscle function, then one has to
address the muscle weakness.
In cases in which the incomitance is associated with little
or no limitation of eye movements, the incomitance can be
managed by operating on the good eye to match ocular rotations
of the deviated eye. Determine where the deviation is greatest
and operate to achieve alignment in primary position while
reducing the incomitance. Use this strategy: recession procedures have their greatest effect in the field of action of the
recessed muscle, and resections produce a leash with the greatest effect occurring when the eye rotates away from the resected
muscle (see Chapter 11). Recessing the right medial rectus
muscle will produce an exodeviation greater in leftgaze and
almost no effect in rightgaze, and resecting the right lateral
rectus muscle produces an exodeviation that increases in leftgaze. With this strategy in mind, determine what surgery would
best correct the following strabismus.
Example 1. Trace limitation of abduction of unknown
etiology, left eye; negative forced ductions.
Right
ET2
ET, estropia.
Primary
Left
ET 8
ET 16
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The surgical plan is to recess the right medial rectus muscle 4.0
to 5.0 mm, as this will match the right medial rectus muscle to
its underacting yoke muscle, the left lateral rectus muscle.
Weakening the right medial rectus muscle will slightly reduce
adduction but will not affect abduction; this reduces the large
esotropia in leftgaze without causing an exotropia in rightgaze.
Do not recess the left medial rectus muscle because this surgery
has little effect in leftgaze where the esotropia is largest and will
produce an exo-deviation in rightgaze. Also, avoid a left lateral
rectus resection as this will not strengthen the weak lateral
rectus. Instead, it will cause a tight lateral rectus muscle that
also has little effect in leftgaze where the esotropia is greatest
and will cause an exodeviation in rightgaze. For an incomitant
esodeviation that is greater than 10 to 15 prism diopters (PD) in
primary position and increases in leftgaze, two-muscle surgery
will be required to correct the deviation in primary position.
Consider asymmetrical bilateral medial rectus recessions, with
a larger recession on the right medial rectus muscle.
The Faden operation has also been suggested to reduce
incomitance. Adding a Faden to a recession of the medial rectus
muscle increases the weakening effect of the recession in adduction and improves the incomitance. The use of the Faden is controversial. If it is used, it is most effective on the medial rectus
muscle, as the medial rectus has the shortest arc of contact. Theoretically, the Faden weakens the muscle mostly in the field of
action of the muscle, with little effect in primary position; therefore, it may be helpful in reducing incomitance (see Chapter 11).
A report on the effect of the Faden procedure on the medial
rectus muscles in reducing the AC/A ratio concluded there was
a beneficial effect; however, the table of data in this study
showed no change of the AC/A ratio. It is likely the Faden procedure has little effect, except in extreme fields of gaze.35
If the limitation is severe, recessing the yoke muscle to
match the limitation will not work, as operating on the good
eye will not improve the ability of an eye with limited ductions
to come to midline. In these cases of moderate to severe limitation of ductions, one must release the restriction or, in the case
of a palsy, transpose muscle forces to bring the eye to midline.
Recessing the contralateral yoke muscle only works if the limitation is slight, such as a trace to 1 limitation of ductions.
Vertical incomitance can be treated with the same strategy
as described previously for horizontal strabismus. One special
situation that occurs with Grave’s disease and floor fractures is
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that of a patient with orthotropia in primary position and a
hypotropia in upgaze secondary to a tight inferior rectus muscle.
In this case, recess both inferior rectus muscles, with a larger
recession on the side with the restriction. The diagnosis and
management of specific types of restrictive and paralytic strabismus follow.
SPECIFIC TYPES OF RESTRICTIVE
STRABISMUS
Fat Adherence
Fat adherence is a restrictive form of strabismus occurring after
periocular surgery or accidental trauma. Marshall Parks was the
first to describe the clinical characteristics and etiology of the
fat adherence syndrome or, as it is also called, the adhesive syndrome.84 Normally, Tenon’s capsule and muscle sleeve act as an
elastic barrier separating the globe from the surrounding orbital
fat. Fat adherence is caused by violation of the posterior Tenon’s
capsule, allowing exposure and manipulation of extraconal fat
and fascia, which produces an adhesion of these tissues to the
sclera. Because the septae within the extraconal fat connect to
the periorbita, fibrosis associated with fat adherence can extend
from the orbital bone to the sclera (Fig. 10-4). In severe cases,
the eye is virtually scarred to the orbital bone, immobilizing
ocular rotations. Violation of the muscle sleeve can also result
in fat adherence to a rectus muscle causing a tight muscle. Fat
adherence most frequently occurs after strabismus surgery
involving posterior exposure (especially oblique muscle surgery)
and retinal buckle surgery, but can also occur after any periocular surgery, even after blepharoplasty.57,59,134
Fat adherence is difficult to surgically correct, as recurrence
of fat adherence after removal of adhesions is very common.
Once Tenon’s capsule is violated and a scar established, it is
almost impossible to reestablish the delicate fascial barrier to
prevent recurrence of scarring. Teflon or silicone sheaths have
been used as an artificial barrier, but they become encapsulated
in scar and often make the restriction worse. Amniotic membrane transplantation has been used to create a barrier separating periocular fat from the sclera, but the technique is difficult,
at best, and remains investigational.138 Surgical correction of fat
adherence consists of releasing the scar by dissecting close to
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A
FIGURE 10-4A,B. Fat adherence syndrome. (A) Diagram on the right
shows the normal anatomy of the periocular fascia with Tenon’s capsule
as the barrier separating orbital fat from the sclera and muscle. Diagram
to the left shows fat adherence (after violation of Tenon’s capsule) overlying the rectus muscle in an area away from the rectus muscle over
sclera. Note that a fibrous scar extends throughout the fat septae attaching periosteum to the muscle and sclera. This scar causes a restrictive
leash that limits eye movements. (B) Photograph of fat adherence to the
inferior rectus muscle. (Modified from Parks and Mitchell, 1978, with
permission.)
sclera and removing the adhesions without repenetrating the
orbital fat. (Perform forced ductions after freeing adhesions to
evaluate improvement of the restriction.) Dissect carefully with
direct visualization, as posterior dissections can be dangerous.
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Cases of inadvertent optic nerve transection have occurred,
although they are rarely reported. If fat and scar are adherent to
a rectus muscle, remove a small amount of the anterior scar,
then recess the tight muscle en bloc with the scar rather than
trying to dissect all the scar off the muscle. Avoid extensive dissection of scar off the muscle, as this usually results in further
fat manipulation and worsening of the adherence. Medical treatment with mitomycin-C has not been effective in reducing postoperative fibrosis and may even increase scarring.17 Injection of
peribulbar corticosteroids also fails to prevent postoperative
scarring. The best treatment for fat adherence syndrome is
prevention: avoid penetration of posterior Tenon’s capsule
during the initial surgery. During strabismus surgery, perform
minimal dissection of muscle fascia and, when dissecting,
dissect close to the muscle to stay away from surrounding
orbital fat. If Tenon’s capsule is inadvertently torn so fat is
exposed, cover the exposed fat by repairing the Tenon’s tear with
7-0 vicryl suture.
Grave’s Ophthalmopathy
Grave’s ophthalmopathy is an autoimmune disease associated
with inflammation of the extraocular muscles. Initially, there is
an acute phase during which there is a lymphocytic infiltration
of the extraocular muscles, resulting in extraocular muscle
enlargement and proptosis. This active phase usually lasts
several months to more than a year. Orbital imaging studies
show thickened extraocular muscles, especially posteriorly. The
second phase is a cicatricial phase with quiescence of inflammation and secondary contracture of the muscles. All muscles
are usually involved, but the inferior rectus and medial rectus
are most severely affected.91 Strabismus is caused by tight
fibrotic muscles and can develop in both phases but is most pronounced in the cicatricial phase. A restrictive hypotropia caused
by tight inferior rectus muscles is the most common type of
strabismus, followed by esotropia associated with tight medial
rectus muscles.
The management of Grave’s ophthalmopathy is careful
observation during the acute inflammatory phase. Treatment
with systemic steroids and even external beam radiation may be
indicated for severe disease; however, radiation therapy is not
effective for treatment of the strabismus.126 Orbital decompression is indicated for severe proptosis and visual loss associated
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with optic nerve compression from inflamed extraocular
muscles. In most cases, it is better to perform strabismus surgery
after the active phase has subsided and strabismus measurements have stabilized. A report on eight patients whose eyes
were operated on during the active phase of thyroid ophthalmopathy noted that all eight patients achieved successful longterm alignment (16 months follow-up); however, half the
patients required more than one operation.
Regarding the timing of surgery, strabismus surgery is
usually performed after orbital decompression surgery, because
orbital surgery can alter eye alignment.21,75 The strategy for the
treatment of Grave’s ophthalmopathy strabismus is to release
the restriction from the tight rectus muscle, with a rectus
muscle recession being the procedure of choice. It is not advisable to use rectus muscle resections, as this tightens an already
stiff, inelastic muscle. A right hypotropia less than 15 PD with
a tight right inferior rectus muscle can be surgically addressed
with a right inferior rectus recession, with or without an
adjustable suture technique (Fig. 10-5).8,68 If the deviation in
primary position is greater than 18 to 20 PD with severe restriction, recess the tight inferior rectus muscle more than 5.0 mm
and add a recession of the contralateral superior rectus muscle.
As a rule, expect 3 PD of vertical correction for each millimeter
of vertical rectus muscle recession.135
One common problem with correcting thyroid strabismus
has been late overcorrection after inferior rectus recession,
which occurs in up to 50% of cases.24,56,80 Initially after surgery,
there is a successful result. Then, at 4 to 6 weeks after the inferior rectus recession, a consecutive hypertropia on the side of
the recession occurs, with underaction of the recessed inferior
rectus muscle and ipsilateral lower eyelid retraction.132 R.
Friedman suggested that performing asymmetrical bilateral
inferior rectus recessions avoids late overcorrection. A report by
Cruz and Davitt on eight patients who underwent asymmetrical bilateral inferior rectus recessions showed no overcorrections; however, 25% of these patients were undercorrected.24
Ludwig has suggested that a stretched scar at the new insertion
is the cause of the overcorrection. It is hypothesized that, at 4
to 6 weeks after surgery, the absorbable suture loses its strength.
The muscle–scleral attachment stretches and causes the tight
muscle to retract posteriorly. This author has now switched to
nonabsorbable sutures (6-0 Mersiline), and preliminary results
have been good, even when using an adjustable suture.
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A
B
FIGURE 10-5A,B. Thyroid-associated strabismus. (A) Patient with
Graves’ disease and limited elevation, right eye, secondary to a tight right
inferior rectus muscle. (B) CT scan shows thyroid-associated changes; the
medial inferior and superior rectus muscles are enlarged bilaterally.
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Congenital Fibrosis of the Extraocular Muscles
Congenital fibrosis of the extraocular muscles (CFEOM) is an
autosomal dominant, nonprogressive disorder usually characterized by bilateral congenital ptosis and restrictive external
ophthalmoplegia48,49; however, rare unilateral cases have been
described (CFEOM 8, 21, 26, 29, 30, 31).28,51 Systemic diseases
reported to be associated with CFEOM include Prader–Willi syndrome (CFEOM 25),60 Joubert syndrome (CFEOM 23),3 and cortical and basal ganglia dysplasia (CFEOM 2).123 CFEOM has been
mapped to chromosomes 12, 11, and 16 (CFEOM 3, 5, 6, 7, 9,
18, 16).26,51 There can be significant phenotypic heterogeneity
with a variety of subtypes of CFEOM found in the same family
(CFEOM 6 and 8).96,118
The clinical features of CFEOM have been classified into
five groups: (1) generalized fibrosis syndrome,4 (2) fibrosis of
inferior rectus with blepharophimosis, (3) strabismus fixus,
(4) vertical retraction syndrome,39 and (5) unilateral fibrosis
blepharoptosis and enophthalmos (CFEOM 17).32,34,51 The medial
rectus muscle is one of the most commonly involved, causing a
strabismus fixus esotropia with extreme restriction to abduction
(Fig. 10-6). Strabismus fixus is a term for an eye that is fixed and
cannot move, usually secondary to severe restriction or a combination of restriction and paresis. The strabismus associated
with CFEOM is mostly caused by tight fibrotic muscles, but a
component of paresis can also be a factor. As with thyroidrelated strabismus, the surgical procedure of choice is a recession of the tight rectus muscle. Resections should be avoided.
These CFEOM cases can be technically difficult because exposure of the muscle is limited, especially in cases with a fibrotic
medial rectus muscle.
The etiology of CFEOM is unknown, but the syndrome is
associated with atrophic and fibrotic changes of the extraocular
muscles.33 Light and electron microscopy demonstrated replacement of normal muscle with collagen, dense fibrous tissue, and
areas of degenerated skeletal muscle (CFEOM 29, 30, 31).125
Research suggests that the cause of congenital fibrosis of the
extraocular muscles is an abnormality in the development of
the extraocular muscle lower motor neurons, with agenesis of
the third nerve being most common (CFEOM 1, 14, 11, 10).109
Nakano et al. reported finding three mutations in ARIX gene
(also known as PHOX2A) in four pedigrees of congenital fibrosis of the extraocular muscles type 2 (CFEOM 2).79,123 ARIX
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FIGURE 10-6. Patient with congenital fibrosis syndrome and a large
angle esotropia. There was severe limitation to abduction, bilaterally, and
forced ductions at the time of surgery show severe restriction to abduction in both eyes. Bilateral medial rectus recessions (7.0 mm) resulted in
good alignment with improved abduction.
encodes a homeodomain transcription factor protein shown to
be required for development of cranial nerves III and IV in mouse
and zebrafish. These findings confirm the hypothesis that
CFEOM 2 results from the abnormal development of cranial
nerves III and IV and emphasize a critical role for ARIX in the
development of these midbrain motor nuclei.37,79
Double Elevator Palsy or Monocular Elevation
Deficit Syndrome
Double elevator palsy is classically defined as a congenital
inability to elevate one eye, with the limitation occurring in
adduction and abduction (Fig. 10-7). One might question why
double elevator palsy is included under restrictive strabismus.
The term double elevator palsy is a misnomer because, in most
cases, the cause for the limited elevation is not a palsy of both
elevators but is a tight inferior rectus muscle. Studies using saccadic velocity measurements and forced ductions showed that
approximately 70% of patients diagnosed as having a double elevator palsy actually had limited elevation as a result of inferior
rectus restriction, not a palsy of the superior rectus and inferior
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oblique muscles.73,106 A more descriptive term now used is
monocular elevation deficit syndrome (MED). MED may be
mistaken for Brown’s syndrome, although the limited elevation
is worse in adduction than abduction in the latter. Patients with
MED present with a hypotropia, a chin elevation, and, often, an
ipsilateral ptosis. True congenital ptosis is present in 25% of
cases whereas pseudo-ptosis may occur in almost all patients
with a large hypotropia.2 In those cases with a true double elevator palsy and a lack of an upgaze saccade, forced ductions at
time of surgery usually reveal a tight inferior rectus muscle
coexisting with the superior rectus palsy.
An interesting finding in approximately 25% of patients
with double elevator palsy and congenital ptosis is the Marcus
Gunn jaw-winking phenomenon.133 This association indicates a
congenital misdirection syndrome involving the oculomotor
nerve. It is possible that, as with congenital fibrosis syndrome,
the cause of the tight inferior rectus and, in some cases, superior rectus and inferior oblique palsy, is abnormal development
of cranial nerves (including the oculomotor nerve) with secondary muscle fibrosis.
Surgery for MED is indicated if a significant hypotropia is
present in primary position with an associated chin elevation.
The type of surgery depends on the cause of the elevation deficit
(Table 10-3). If the etiology is a tight inferior rectus muscle and
the upgaze saccade is normal, recess the ipsilateral inferior
rectus muscle, usually around 5 to 6 mm depending on the size
of the hypotropia. It is important to evaluate preoperatively for
the presence of an upgaze saccade and to perform forced ductions at the time of surgery to make the correct procedural
choice. Lack of upgaze saccades, combined with a weak superior rectus muscle on forced generation testing, indicates a true
A
B
C
FIGURE 10-7A–C. Double elevator palsy (monocular deficit syndrome).
Child has had limited elevation of the right eye since birth. Note that
elevation of right eye is worse in abduction (A) than it is in adduction (C).
Patient is fixing with the involved right eye so the left eye is hypertropic
as per Hering’s law of yoke muscles (B). Preoperatively, this patient had
intact upgaze saccades and a tight inferior rectus muscle on forcedduction testing at the time of surgery. The elevation deficit was successfully treated with a right inferior rectus muscle recession of 6.5 mm.
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TABLE 10-3. Treatment of Double Elevator Palsy (Monocular
Elevation Deficit Syndrome).
• Tight inferior rectus muscle: good superior rectus function Recess ipsilateral
inferior rectus muscle (5–6 mm)
• Superior rectus palsy
Recess ipsilateral inferior rectus muscle and ipsilateral transposition of half
the medial and lateral rectus muscles up to the superior rectus insertion
(preferred by author)
or
Knapp procedure: full-tendon transfer up to the superior rectus muscle
double elevator palsy. In these cases, a recession of the ipsilateral inferior rectus will not correct the hypotropia. Treatment of
a true double elevator palsy with weak superior rectus muscle
is to perform a transposition of the ipsilateral medial and lateral
rectus muscles up to the superior rectus muscle. In patients with
the superior rectus palsy type of MED, forced ductions are often
positive, and the ipsilateral inferior rectus muscle should be
recessed. This author prefers the partial tendon transfer
(Hummelsheim) instead of the full-tendon transposition (Knapp)
to avoid the possible complication of anterior segment ischemia
that can occur up to 20 years after strabismus surgery. In severe
cases of hypotropia over 15 PD, consider adding a recession of
the contralateral superior rectus muscle.
Orbital Floor Fracture
Signs of a blowout fracture include diplopia secondary to
restricted vertical eye movement, enophthalmos, and numbness
of face below the traumatized orbit and along the upper teeth.
Restrictive strabismus with limited elevation in orbital floor
fractures is caused by entrapment of fat and the inferior rectus
muscle at the fracture site (Fig. 10-8). Repair of the floor fracture
in most cases will improve ductions. In addition to limited elevation, there can be limited depression on the side of the fracture, often associated with a posterior fracture.108 The cause of
the limited depression could be contributed to scarring of the
inferior rectus to the floor, thus preventing the inferior rectus
muscle from transmitting its contractual pull to the globe.
Adherence of the inferior rectus to the floor would also isolate
the muscle anterior to the fracture and cause the anterior muscle
to slacken on attempted downgaze, producing pseudoinferior
rectus palsy. These patients characteristically have a small
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hypertropia in primary position, underaction of the inferior
rectus muscle, and a large hypertropia in downgaze.
The key to the diagnosis of a pseudoinferior rectus palsy is
normal inferior rectus muscle function and normal saccades
when the eye moves from upgaze to primary position, with inferior rectus muscle weakness and slow ocular movements from
primary position to downgaze. Treatment of pseudoinferior
rectus palsy is to repair the floor fracture. If this does not relieve
symptoms, then strabismus surgery is indicated. This author has
found that a small (3–4 mm) ipsilateral inferior rectus muscle
tightening procedure (Wright plication or resection) helps to
eliminate the anterior muscle slack. A contralateral inferior
rectus recession works well and produces only a slight limitation of elevation. If the muscle is captured in a trap-door fracture, direct damage to the inferior rectus muscle occurs and
can truly weaken the inferior rectus muscles. Small trap-door
floor fractures can pinch and strangle the inferior rectus muscle,
causing necrosis and muscle damage.11 Because of the potential
for permanent damage, some advocate immediate repair within
the first few days if there is imaging evidence that the inferior
rectus is entrapped.29 Strabismus surgery should be performed
after reconstructive orbital surgery. If orbital reconstruction
is not indicated, and the patient has persistent diplopia 4 to
8 weeks after the trauma, then strabismus surgery is indicated.
The strabismus surgical plan depends on the pattern of the
strabismus. Table 10-4 lists patterns of strabismus and their
associated treatment.
Myotoxic Effect of Local Anesthetics
Injection of local anesthetics such as lidocaine and marcaine
into an extraocular muscle can result in myotoxic damage to the
muscle and cause strabismus.19,40,46 Elderly patients are especially susceptible to the myotoxic effects of local anesthetics.
Immediately after the injection of a local anesthetic into an
extraocular muscle, there is an acute paresis of the muscle that
lasts for one to several days. Over the next few weeks, localized
segmental intramuscular fibrosis occurs secondary to local
myotoxicity of the anesthetic. The fibrosis results in a tight and
contracted muscle. What is particularly interesting is that, in
some cases, the injected muscle overacts, producing a deviation
that increases in the field of action of the injected muscle.8,13
This deviation is in contrast to the restriction pattern usually
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A
B
FIGURE 10-8A–B. Orbital floor fracture left eye with entrapment of fat
and the inferior rectus muscle. (A) In primary gaze, there is no significant
deviation. (B) Restricted elevation of left eye in upgaze causes a large right
hypertropia.
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C
FIGURE 10-8C. (C) CT scan shows herniation and entrapment of inferior orbital fat into the maxillary antrum. Note that, after removal of the
fat and repair of the fracture, the restriction resolved.
expected with a tight muscle, where the deviation is greatest in
the gaze opposite to the field of the muscle’s action. The cause
of the muscle overaction is thought to be secondary to intramuscular fibrosis, with stretching of the Z-bands and enhancing
TABLE 10-4. Orbital Floor Fracture: Surgical Plans.
Tight inferior rectus muscle (hypotropia)
• Small hypotropia (8 PD) in primary position, no deviation in downgaze, and
larger hypotropia in upgaze (tight inferior rectus muscle):
Asymmetrical bilateral inferior rectus muscle recessions, with a larger
ipsilateral recession
Add a contralateral superior rectus recession for a large hypotropia in upgaze
• Large hypotropia in primary position, worse in upgaze (tight inferior rectus
muscle):
Hypotropia 8 to 15 PD: recess ipsilateral inferior rectus muscle (3.5–5.0 mm)
Hypotropia 15 PD: recess ipsilateral inferior rectus muscle (5–6 mm) PLUS
a contralateral superior rectus recession (4–6 mm)
Pseudoinferior rectus muscle palsy (hypertropia)
• Hypertropia in primary position increases in downgaze with ipsilateral limited
depression; intact saccades from upgaze to primary position:
Plication of the ipsilateral inferior rectus (3 mm) PLUS contralateral inferior
rectus recession (4–5 mm)
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the action and myosin interaction.19 The fibrosis acts to stretch
the muscle fibers that subsequently increases their force, per the
Starling’s length tension curve.19 For example, inadvertent injection of the inferior rectus muscle associated with a retrobulbar
injection of anesthetic initially results in an ipsilateral hypertropia because of an inferior rectus paresis. Over a few weeks,
this changes into an ipsilateral hypotropia with overaction of
the inferior rectus muscle, resulting in the hypertropia being
greatest in downgaze.
Any of the extraocular muscles can be infiltrated during a
retrobulbar or peribulbar injection of local anesthetics, with the
superior and inferior rectus muscles most commonly affected.
One of the findings is segmental enlargement of the injected
muscle seen on orbital imaging. Hamed and Mancuso46 reported
on eight patients with an ipsilateral hypotropia after a retrobulbar injection of anesthetic, with three patients showing segmental enlargement of the inferior rectus muscle. The treatment
is to recess the tight or overacting muscle. This method has produced excellent results, especially in the cases involving an
overacting injected muscle, with the deviation larger in the field
of action of the muscle. One can help prevent intramuscular
injection injury by injecting into the orbital quadrant away from
the extraocular muscles, using a blunt cannula and limiting
anesthetic volume. The incidence of strabismus after cataract
surgery has diminished dramatically since the widespread use of
topical anesthesia during surgery.
Strabismus After Retinal Surgery
Strabismus can occur virtually after every known retinal surgical procedure.38,57,71,72,103,111,114 The strabismus is usually transient; however, persistent strabismus occurs in approximately
7% of scleral buckling procedures.71,117 Common causes of strabismus after retinal detachment surgery include fat adherence
and restriction, a lost or slipped muscle, a displaced superior
oblique tendon, a large explant under a rectus muscle, and
ectopic fovea.38,47,57,85,110 Other causes of strabismus after retinal
surgery include patients with preexisting strabismus before the
retinal surgery who then experience sensory strabismus secondary to loss of vision.92,130 Of all the causes of persistent
restriction after retinal detachment surgery, fat adherence and
periocular scarring is by far the most common and most difficult to treat.1,57,134 Fat adherence is difficult to treat because there
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is no synthetic substitute to recreate the natural boundary
between the orbital fat and the eye and muscle once Tenon’s
capsule is violated.
Occasionally, a lost muscle is associated with postretinal
surgery, as can occur when the traction sutures around the
muscle are pulled to gain posterior exposure during the retinal
surgery. In elderly patients, the muscle is relatively weak, and
overzealous traction on the rectus muscle can result in a splitting of the muscle; this has been termed pulled-in-two syndrome (PITS). Spontaneous disinsertion and posterior slippage
of a rectus muscle behind an encircling buckle can also occur,
without removal of the muscle at the time of retinal surgery.47,57
In these cases, the silicone band will cheese-wire through the
muscle insertion over several months postoperatively, resulting
in late slippage of the muscle behind the buckle and causing an
underaction of the slipped muscle. The slipped rectus muscle
can almost always be found attached to sclera at the posterior
edge of the encircling buckle or connected to sclera by a pseudotendon. Appropriate treatment is to advance the muscle and
reattach the muscle with nonabsorbable suture.
Another cause for strabismus after retinal surgery is an
oblique muscle that has been displaced anteriorly by an encircling band.57,72 Placement of the band behind the superior
oblique tendon pulls the superior oblique tendon anteriorly to
the nasal aspect of the superior rectus insertion. The superior
oblique tendon now inserts at the nasal side of the superior
rectus insertion, anterior to the equator. The new anterior insertion of the superior oblique tendon changes the action of the
superior oblique muscle from a depressor to an elevator. These
patients typically present with a hypertropia and limitation of
depression of the involved eye. Forced ductions, however, show
relatively mild restriction to depression as compared to the limitation on ductions and versions. Treatment is to release the
entrapped superior oblique tendon from the buckle or, if there
is severe scarring, perform a superior oblique tenotomy. If
the hypertropia is greater than 5 PD in primary position, also
perform a recession of the contralateral inferior rectus muscle
(consider adjustable suture). The inferior oblique muscle can
also be entrapped by an encircling element.57 In this case, the
element is passed behind, or splits, the inferior oblique muscle.
When the band is tied in place, the muscle is pulled anteriorly,
resulting in a hypotropia and excyclotropia. The hypotropia
occurs because the inferior oblique is displaced anteriorly to the
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equator, pulling the front of the eye down. The excyclotropia is
caused by the increased tension on the inferior oblique muscle.
Torsional diplopia after retinal surgery is not always associated
with an entrapped oblique muscle.23 Metz and Norris found two
of four patients with torsional diplopia after retinal surgery to
have no identifiable abnormality of the oblique muscle.72 The
complications of oblique muscle entrapments can be diminished
by passing the encircling elements anteriorly, just behind the
rectus insertions. Extreme posterior passage of the muscle hook
may result in inadvertent hooking of an oblique muscle, especially when working on the superior rectus and lateral rectus
muscles.
The placement of a retinal explant sponge or buckle is often
identified as a primary cause for strabismus after retinal surgery.
Transient strabismus after a retinal encircling procedure is frequent, occurring in approximately 20% of cases. In our experience, however, a retinal encircling element by itself rarely
causes persistent strabismus. Persistent strabismus after retinal
surgery usually results from secondary scarring or a displaced
muscle, as stated previously.78 Infrequently, however, a retinal
explant may be the primary cause of restriction; this occurs
when a large explant is placed directly under a rectus muscle.
The explant causes the muscle to deviate from its normal
course, thus tightening the muscle. For example, a large retinal
sponge placed directly under the medial rectus will cause a tightening of the medial rectus, as the medial rectus courses over the
large sponge and produces an esotropia. Low-profile encircling
elements, such as 240 bands that indent the sclera, do not interfere with the course of the rectus muscle and, therefore, do not
produce strabismus.
Foveal ectopia occurs in association with macular pucker,
peeling of the epiretinal membrane, and retinal translocation
surgery. Acquired foveal ectopia produces an interesting type of
strabismus and diplopia. These patients will observe that objects
in the central visual field appear double, with one image being
distorted by metamorphosia. Objects in the peripheral field,
however, will often be fused, as the peripheral retina may not
be involved with the ectopia. Thus, patients who undergo membrane peeling for a macular pucker may experience postoperative diplopia because of foveal ectopia. The image disparities
tend to be small with this condition, and prism glasses have been
found to be effective in treating this problem.
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Retinal translocation surgery can result in severe torsional
diplopia that prisms cannot correct. Instead, oblique muscle
surgery is required to treat the problem.38 Extorsion is induced
from macular inferior translocation, and intorsion is secondary
to superior macular translocation. Extorsion can be corrected by
a large Harada–Ito procedure, possibly with an inferior oblique
weakening procedure, whereas intorsion can be corrected with
a weakening surgery of the superior oblique muscle, perhaps
with a tuck of the inferior oblique muscle. Vertical offset of the
rectus muscle can also change torsion, but one must consider
the risk of anterior segment ischemia in this group of patients.
Glaucoma Explants and Strabismus
The incidence of strabismus after glaucoma explant surgery
ranges from 10% to 70%, depending on the study.7,90,112 The
cause of the strabismus is, for the most part, the large bleb
created by the glaucoma explant. Strabismus associated with a
large filtering bleb may be caused by the following mechanisms:
(1) orbital mass, which displaces the eye (Fig. 10-9); (2) a mass
directly under a muscle or tendon; or (3) scarring or adhesions
secondary to the surgical dissection during placement of the
glaucoma explant. The old Baerveldt implant had been associated with the highest incidence of strabismus; however, modifications of the Baerveldt implant (fenestrated Baerveldt) have
reduced the bleb size and subsequently reduced the incidence of
strabismus. Valved implants have also reduced the size of the
filtering blebs and have subsequently produced the lowest incidence of strabismus.
A large explant in the superior nasal quadrant may cause a
pseudo-Brown’s syndrome with restricted elevation in adduction, as the bleb displaces and tightens the superior oblique
tendon.7,90 Placement of glaucoma explants should be superotemporal rather than superonasal to avoid the problem of a
secondary Brown’s syndrome. The treatment of a bleb-induced
strabismus is to reduce the size of the bleb by suturing the bleb
wall to the explant so it cannot expand. Additionally, the old
explant can be replaced with a newer valved explant.
An interesting observation of some patients with strabismus
and severe glaucoma is that they do not experience diplopia but,
instead, have visual confusion.57 Visual confusion is the simultaneous perception of two different foveal images in a patient
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A
B
FIGURE 10-9A,B. Patient with a glaucoma explant in the left superior
temporal quadrant. The glaucoma was controlled; however, it produced
a large bleb that limited abduction. (A) Patient is looking left, and the left
eye shows severe restriction (4) to abduction. (B) Large temporal bleb is
causing a mass effect and restricting abduction of the left eye.
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with strabismus. These patients see the superimposed images
from each fovea. Patients with end-stage glaucoma have tunnel
vision and lose their peripheral visual field. If these patients
acquire strabismus, they may experience confusion rather than
a true diplopia, as they only have central vision and are forced
to use the fovea of each eye.
High Myopia and Esotropia
(Myopic Strabismus Fixus)
High myopia, usually greater than 20 diopters, can be associated
with an acquired large-angle esotropia along with limited abduction and a hypotropia9,25,50,63,116; this is a form of acquired strabismus fixus and can be either monocular or binocular. Another
term for the high myopia esotropia syndrome is heavy eye
syndrome, with hypotropia and limited eye movement.116
Restricted abduction is dramatic, and there is limited elevation
of the hypotropic eye. Orbital imaging shows an extremely large
globe with a posterior staphyloma that fills the orbit, a large inferior displacement of the lateral rectus muscle, and a mild nasal
displacement of the superior rectus muscle. The cause of the
esotropia and hypotropia is a combination of restriction, because
of the massive expansion of the posterior globe against a tight
medial rectus muscle, and displaced lateral and superior rectus
muscles that change the normal vector forces. Displacement of
the lateral rectus muscle inferiorly and superior rectus muscles
nasally is most likely caused by the massive expansion of the
posterior aspect of the globe into the superior temporal quadrant.64 The lateral rectus muscle shows the most displacement,
probably due to the laxity of its pulley system. Slippage of the
lateral rectus muscle below the globe weakens the abduction
vector and pulls the eye down, thus contributing to the esotropia
and hypotropia. The nasally displaced superior rectus muscle
also contributes to the esotropia and hypotropia by pulling the
eye nasally and diminishing the elevation vector force.
Treatment is aimed at realigning the lateral rectus muscle
and releasing the medial rectus muscle, which is inevitably
tight. This author prefers a large recession of the medial rectus
muscle, at least 7 to 8 mm on a hang-back suture, and a superior transposition of the lateral rectus muscle with a small resection. The posterior sclera is thin in these cases, and access to
the posterior globe is difficult because of the large eye. The hangback suture of the medial rectus allows for a large recession
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without passing a posterior suture. Union of the superior and
lateral rectus has also been described.
SPECIFIC TYPES OF PARALYTIC
STRABISMUS
Sixth Nerve Palsy
A persistent, isolated, congenital sixth nerve palsy is extremely
rare; however, newborns may have a transient sixth nerve palsy
that resolves spontaneously over a few days to a few weeks. A
common cause of isolated acquired sixth nerve palsy in early
childhood is postviral inflammatory neuropathy, which may
occur 1 to 3 weeks after a viral illness or immunization or spontaneously without obvious cause. These patients should be followed closely to monitor their improvement and watch for the
development of amblyopia. Improvement usually occurs within
6 to 10 weeks. After viral or idiopathic causes, the next most
common causes of acquired sixth nerve palsy in children and
young adults include closed head trauma and intracranial neoplasms. Neuroimaging is indicated for acquired sixth nerve palsy
if the palsy does not improve rapidly or if other neurological
signs are present. Other causes of an acquired sixth nerve palsy
include Gradenigo’s syndrome (mastoiditis and sixth nerve
palsy), meningitis, myasthenia gravis, and cavernous sinus
disease.
Sixth nerve palsy is typically associated with limited abduction and an esotropia that increases upon gaze to the side of the
palsy (Fig. 10-10). On attempted abduction, there is relative lid
fissure widening because both the medial and lateral rectus
muscles are relaxed on attempted adduction and the posterior
orbital pressure proptoses the eye. Remember that, on attempted
abduction, the medial rectus muscle is inhibited (Sherrington’s
law). Mild sixth nerve paresis may allow relatively good lateral
rectus function and show only a trace limitation of abduction.
These patients, however, will have a pattern of divergence
paresis with an esotropia that is greater in the distance than at
near. The divergence paresis pattern should alert the examiner
to the possibility of a sixth nerve paresis.
Initial therapy of a traumatic or vascular sixth nerve palsy
is observation for 6 months while monitoring the patient for
spontaneous recovery. Spontaneous recovery of traumatic sixth
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A
B
FIGURE 10-10A,B. (A) Photographs of a child with a traumatic right sixth
nerve palsy and poor lateral rectus function, evidenced by absent abduction saccades and severe limitation of abduction of the right eye. There
is 4 limitation of abduction as the right eye does not go past midline.
(B) Results after surgery consisting of a right Hummelsheim transposition and a right medial rectus recession of 6.0 mm. Note the eyes are
orthotropic in primary position. There is improved abduction, but abduction remains limited.
nerve palsy is approximately 80% for unilateral cases and 40%
for bilateral cases.53 A complete palsy at the initial presentation
and bilateral involvement indicate a poor prognosis for recovery.52 During the observation period, alternate monocular occlusion or press-on prisms can be used to eliminate diplopia if a
face turn does not allow fusion. To prevent secondary contracture of the medial rectus muscle and increase the chances for
recovery, some advocate the use of botulinum injection into the
ipsilateral medial rectus muscle.10,74 Botulinum paralyzes the
muscle for 3 to 6 months, thus preventing contracture. The hope
is that preventing secondary contracture of the medial rectus
muscle will increase the chances of recovery without strabismus surgery. The use of botulinum remains controversial,
however. Studies comparing botulinum to conservative treatment for the management of nerve palsy have shown no significant difference in recovery rates.53,65 Holmes et al., in a
prospective multicenter study of acute traumatic sixth nerve
palsy or paresis, reported that patients treated either with botulinum or conservatively had similarly high recovery rates.53 It
should be noted that, after a botulinum injection into the medial
rectus muscle for a complete sixth nerve palsy, both the medial
and lateral rectus will be paralyzed, resulting in essentially no
horizontal movement of the paretic eye. Therefore, the patient
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should be warned that the paretic eye may have decreased movement after the injection. In addition, the surgeon should be
aware that the effects of botulinum can last more than 6 months,
and surgery should be delayed until the botulinum has
dissipated.
After the 6-month observation period, lateral rectus muscle
function should be evaluated, as this is critical for determining
the surgical plan. Lateral rectus muscle function can be assessed
by saccadic velocity testing and the active forced-generation
test. If the saccadic velocities are less than 60% of normal or the
active forced-generation test is estimated to be half of the
normal fellow eye, a vertical rectus muscle transposition procedure is indicated.
Transposition procedures act by moving innervated vertical
rectus muscles to the lateral rectus insertion to provide lateral
force. The lateral force of the transposition does not appropriately activate on attempted abduction but, instead, provides a
constant lateral force. Transposition of vertical rectus muscles
can involve the full muscle (full-tendon transfer) or the
muscle can be split longitudinally and only half the muscle is
transferred (partial-tendon transfer). In addition to a transposition, patients with significant residual paresis almost always
require an ipsilateral medial rectus recession to reduce adduction forces.
The vertical rectus muscles provide substantial circulation
to the anterior segment. Older adult patients, especially those
with arteriosclerotic disease or hyperviscosity syndromes, are at
risk for developing anterior segment ischemia after vertical recti
transposition, particularly those receiving full-tendon transfers.
A partial-tendon transfer procedure should be considered in
these patients to maintain anterior circulation and prevent
anterior segment ischemia. Modifications of the Hummelsheim
partial-tendon transposition include suturing the transposed
vertical muscle to the lateral and resecting a few millimeters of
the transposed vertical muscle halves.18,82 An important aspect of
the partial-tendon transfer is to fully mobilize the muscle being
transferred by splitting the vertical rectus muscles for at least
14 mm posterior to their insertions.135 If carefully performed, a
partial-tendon transfer procedure results in long-term good postoperative eye alignment while reducing the risk of anterior
segment ischemia. Other options include full-tendon transposition with injection of botulinum toxin to the medial rectus
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TABLE 10-5. Surgical Treatment for Sixth Nerve Palsy.
Clinical presentation
Surgery
Excellent lateral rectus function
(90%–100%):
Ductions trace limitation
ET in primary position 2 to 8 PD
Diplopia to the side of the palsy
Good lateral rectus function (80%–90%)
Ductions 1
ET in primary position 10 to 20 PD
Recess contralateral medial rectus
5–6 mm (adjustable suture optional)
Fair lateral rectus function (60%–80%)
Ductions 2
ET in primary position 20 to 30 PD
Poor lateral rectus function (⬍60%)
Ductions 3 to 4
ET in primary position 30 PD
Bilateral medial rectus recessions, but
recess the contralateral medial
rectus muscle 6 mm and the
ipsilateral medial rectus muscle
3–5 mm (adjustable suture advised)
Ipsilateral medial rectus recession
6 mm (adjustable suture advised);
lateral rectus resection or Wright
plication 5 mm and contralateral
medial rectus recession
3–5 mm (with optional Faden)
Ipsilateral medial rectus recession
6–7 mm (adjustable suture in adults
or cooperative children), and vertical
rectus partial-tendon transposition
to the lateral rectus muscle (either
Jensen or Hummelsheim); author
prefers modified Hummelsheim
ET, exotropia.
muscle.102 This treatment, however, may not provide a stable
outcome, as an esotropia may recur after 4 to 6 months when
the effect of the botulinum dissipates and medial rectus function returns. This author’s recommendations for the surgical
treatment of sixth nerve palsy are listed in Table 10-5.
Duane’s Retraction Syndrome
The cause of Duane’s retraction syndrome (DRS) has been identified to be an agenesis of the sixth nerve and nucleus, with the
inferior division of the oculomotor nerve (nerve to the medial
rectus muscle) splitting to innervate both the medial and lateral
rectus muscles.19,31 Because both the medial and lateral rectus
muscles are innervated by the nerve to the medial rectus
muscle, both muscles fire and contract simultaneously on
attempted adduction. This cocontraction of the medial and
lateral rectus muscles on adduction gives rise to the term
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Duane’s cocontraction syndrome. Cocontraction of the lateral
rectus muscle against the medial rectus muscle on adduction
causes globe retraction, producing relative enophthalmos and
lid fissure narrowing.94 There are various patterns of innervation that account for the four types of Duane’s syndrome. Figure
10-11 shows a diagram of various patterns of abnormal innervation possible in DRS.
Table 10-6 explains the various types of DRS as they correlate to the innervation patterns noted in Figure 10-11. In
Duane’s type I, there is agenesis of the sixth nerve and the sixth
nerve nucleus, with part of the medial rectus branch of the third
nerve going to the lateral rectus muscle. Because most of the
medial rectus branch of the third nerve appropriately goes to the
medial rectus muscle, the eye will adduct with cocontraction by
the aberrantly innervated lateral rectus muscle. This contraction causes lid fissure narrowing; however, because of the absent
A
B
C
D
FIGURE 10-11A–D. Diagrammatic representation of misdirection of
nerve fibers in Duane’s syndrome. The aberrant nerve pathway is shown
in red, and the dotted lines represent nerve hypoplasia or agenesis. (A)
type I: poor abduction and good adduction. Agenesis of the sixth nerve
and part of the third nerve splits to innervate both the medial and the
lateral rectus muscles, but most of the medial rectus nerve goes to the
medial rectus muscle so adduction is intact. (B) Type II: poor adduction
and good abduction. Sixth nerve is intact and innervates the lateral rectus
muscle, but the medial rectus nerve splits to innervate the medial and
lateral rectus muscles. There is poor adduction because the lateral rectus
contracts against the medial rectus muscle. (C) Type III: poor adduction
and poor abduction. Agenesis of the sixth nerve and part of the third nerve
splits to innervate both the medial and the lateral rectus muscles. The
split is equal so the eye does not move in or out. (D) Synergistic divergence and paradoxical abduction on attempted adduction. Agenesis of the
sixth nerve and part of the third nerve splits to innervate both the medial
and the lateral rectus muscles, but most of the medial rectus innervation
goes to the lateral rectus muscle. When the eye attempts to adduct, it
abducts because the medial rectus nerve innervates the lateral rectus
muscle.
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TABLE 10-6. Classification of Duane’s Syndrome.
Type I Duane’s: most common
Poor abduction and good adduction. The medial rectus muscle receives most of
the medial rectus nerve innervation and the lateral rectus receives minimal
innervation from the medial rectus nerve, with agenesis of the sixth nerve.
Because the medial rectus receives most of the innervation, the Duane’s eye is
usually fixed in an adducted position with an esotropia in primary position, and
there is a compensatory face turn in the direction of the Duane’s eye (i.e., left
face turn for a left Duane’s type I).
Type II Duane’s: least common, extremely rare
Poor adduction and good abduction. EMG recordings show the lateral rectus
muscle to contract appropriately on abduction, but it also contracts
paradoxically on adduction; this probably represents a partial innervation of the
lateral muscle by the sixth nerve nucleus (as purposeful abduction is present),
plus splitting of the medial rectus nerve to innervate the medial and lateral
rectus muscles.
Type III Duane’s: second most common
Poor adduction and poor abduction (the eye has little horizontal movement).
Equal innervation of the medial and lateral rectus muscles by the medial rectus
nerve, with congenital absence of the sixth nerve. Because the medial and lateral
forces are similar, the eye will rest in approximately primary position and there
will be no significant face turn. In some cases, an exotropia is present in primary
position because the lateral rectus receives slightly more innervation than the
medial rectus muscle; this causes a face turn away from the Duane’s eye.
Synergistic divergence: extremely rare
Paradoxical abduction on attempted adduction and poor abduction. Little or no
innervation of the lateral rectus by the sixth nerve. Most of the medial rectus
nerve goes to the lateral rectus muscle. On attempted adduction, the lateral
rectus is stimulated by the medial rectus nerve and the eye paradoxically
abducts.
sixth nerve, there is no abduction (Fig. 10-12). If the medial
rectus nerve equally innervates the medial and lateral rectus
muscles, then the cocontraction of the lateral rectus muscle will
equal the appropriate contraction of the medial rectus muscle,
and the eye will have limited adduction in addition to limited
abduction because of the sixth nerve agenesis. This pattern of
poor adduction and abduction is typical of Duane’s type III (Fig.
10-13). In the rare Duane’s type II syndrome, abduction is intact
but is limited because part of the sixth nerve innervates the
lateral rectus muscle and part of the medial rectus nerve innervates the lateral rectus muscle. Another rare form of Duane’s
syndrome is synergistic divergence. In this syndrome, most of
the third nerve that should innervate the medial rectus muscle
aberrantly innervates the lateral rectus muscle, causing the
Duane’s eye to paradoxically abduct on attempted adduction.124
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FIGURE 10-12. Duane’s syndrome type I, left eye. Inset shows a face turn
to the left, eyes shifted left to maintain binocular fusion. Composite
shows limited abduction in left eye, esotropia in primary position, and
lid fissure narrowing of left eye on adduction. Note that in primary position the Duane’s eye (left eye) is fixing so there is a secondary esodeviation of the right eye. A positive Brückner reflex is seen from the esotropic
right eye.
FIGURE 10-13. Composite photograph of a child with Duane’s syndrome
type III, right eye. There is almost no adduction or abduction in the right
eye, and the right eye is fixed in the abducted position. Lid fissure narrowing of right eye occurs on attempted adduction. In primary position,
there is an exotropia and this patient adopts a compensatory face turn to
the left to keep the eyes aligned in right gaze.
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A patient with right synergistic divergence will diverge and have
a large exotropia on attempted leftgaze.124
Duane’s syndrome is present at birth and is usually unilateral, but it can be bilateral.54 If there is a deviation in primary
position, patients with DRS will adopt a compensatory face turn
to obtain binocular fusion. The face turn is determined by the
resting position of the Duane’s eye. If the medial and lateral
rectus muscles receive comparable innervation from the split
oculomotor nerve and the eye is centered in primary position,
there will be no significant face turn (Duane’s type III). If,
however, the medial rectus muscle receives most of the innervation from the oculomotor nerve, then the affected eye will rest
in adduction and the patient will have an esotropic DRS with a
face turn toward the side of the affected eye (Duane’s type I).
Less commonly, the lateral rectus will receive most of the innervation from the oculomotor nerve. In these cases, the Duane’s
eye will be abducted, causing an exotropia (XT) in primary position and a face turn toward the opposite side of the Duane’s eye
(Duane’s type III with an XT).94
Duane’s syndrome may be associated with an upshoot or a
downshoot on attempted adduction, which may resemble inferior oblique and superior oblique overaction (Fig. 10-14). Studies
utilizing EMGs have identified a variety of aberrant innervation patterns that explain the vertical movements on adduction.55,107,115 In some cases, the upshoot and downshoot are
caused by strong, inappropriate firing of the lateral rectus muscle
on adduction. This leash effect pulls the eye up or down, as the
eye rotates slightly up or down past the horizontal plane. In
other cases, the vertical recti are aberrantly innervated by
part of the medial rectus nerve, so the vertical muscle fires on
adduction.
Other oculomotor misdirection syndromes are associated
with Duane’s syndrome, such as Marcus Gunn jaw-winking.
Duane’s syndrome is associated with numerous systemic
syndromes including Goldenhar’s syndrome, Klippel–Feil syndrome, maternal thalidomide ingestion, fetal alcohol syndrome,
and oculocutaneous albinism.31
SURGICAL EVALUATION
Indications for surgery in DRS include (1) significant misalignment of the eyes in primary position, (2) noticeable abnormal
head position, (3) narrowing of palpebral fissure due to retrac-
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A
B
FIGURE 10-14A,B. Photographs of an upshoot (A) and downshoot (B),
right eye, occurring on attempted adduction associated with Duane’s syndrome of right eye.
tion, and (4) significant upshoot or downshoot. Usually, surgery
is electively performed around age 3 to 8 years, as these patients
have excellent fusion and the condition is stable. Rarely will a
DRS patient have amblyopia and, when present, it is almost
always associated with anisometropia. Amblyopia should be
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the first priority in these unusual cases. In general, muscle resections should be avoided in DRS, because resections can make
the cocontraction and lid fissure narrowing worse.
SURGERY FOR DRS TYPE I
IPSILATERAL FACE TURN
WITH
ESOTROPIA
AND
In cases with esotropia and Duane’s type I, the Duane’s eye is in
an adducted position and there is a face turn toward the Duane’s
eye. The medial rectus muscle is usually contracted and tight.
The simplest, most effective treatment for Duane’s type I with
esotropia is an ipsilateral medial rectus recession (between 5.0
and 7 mm). In adult patients, place the medial rectus muscle on
an adjustable suture and adjust to a 5° to 10° overcorrection so
there is a small exotropia in primary position; this results in
stable long-term correction of the face turn. Remember, the
lateral rectus muscle is not denervated, as in the case of a sixth
nerve palsy, but has innervation provided by part of the medial
rectus nerve. This tonic innervation provides stabilizing abduction force, so a muscle transposition procedure is not required.
Some have advocated a transposition of the vertical rectus
muscles laterally for DRS and esotropia. This procedure is
more invasive and has the risk of producing anterior segment
ischemia. The transposition procedure also has a risk of inducing a vertical deviation in approximately 15% of patients. This
author prefers the simple and effective ipsilateral medial rectus
recession for Duane’s type I with esotropia.
SURGERY FOR DRS TYPE III WITH EXOTROPIA
CONTRALATERAL FACE TURN
AND
In a patient with Duane’s and exotropia, it is almost always a
Duane’s type III. The eye is resting in abduction, and the face
turn is away from the Duane’s eye. There is usually a tight
lateral rectus muscle, and these patients require an ipsilateral
lateral rectus recession. If there is an upshoot or downshoot associated with the Duane’s type III, then consider a Y-split procedure with the lateral rectus recession.
TREATMENT
OF
GLOBE RETRACTION
Globe retraction can be diminished by recessing both the ipsilateral medial rectus and lateral rectus muscles. In patients with
esotropic DRS and severe globe retraction, add a lateral rectus
recession, but recess the medial rectus muscle more than the
lateral rectus to compensate for the esotropia. In exotropic DRS,
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recess the lateral rectus more than the medial rectus muscle or,
for a large exotropia, recess only the lateral rectus muscle (large
recession). For orthotropic DRS without a face turn, recess the
medial and lateral rectus muscles the same amount.
TREATMENT
OF
UPSHOOT
AND
DOWNSHOOT
Two approaches to reduce upshoot and downshoot associated
with DRS include these:
1. Y-splitting with recession of the lateral rectus muscle
2. Posterior fixation suture (Faden) of the lateral rectus and
appropriate recession of horizontal recti
The Y-splitting procedure of the lateral rectus muscle works by
placing some of the lateral rectus muscle above and below the
horizontal midline, thus preventing an upshoot or downshoot
when the eye is in adduction.95,100 By combining a recession of
the lateral rectus muscle with the Y-split, one can treat both an
exotropia Duane’s type III with an upshoot and downshoot. In
patients with orthotropic DRS and a severe upshoot and downshoot, recess the ipsilateral medial rectus muscle along with a
recession and Y-split of the ipsilateral lateral rectus muscle. The
posterior fixation suture acts to stop slippage of the lateral rectus
muscle when the eye rotates up or down, and a concurrent recession reduces cocontraction. The authors have found the Ysplitting procedure is more effective than the posterior fixation
suture.
Fourth Nerve Palsy (Superior Oblique Palsy)
See Chapter 9.
Third Nerve Palsy
Third nerve palsy involves all the extraocular muscles except
the lateral rectus and the superior oblique. The strabismus is
characterized by the eye being “down and out” with a small
hypotropia and a large exotropia (Fig. 10-15). There is limited
depression, elevation, and adduction, along with preservation of
abduction (intact innervation lateral rectus muscle) and intorsion seen on attempted eye movement down and in (intact
innervation superior oblique muscle). Ptosis, pupillary dilatation, and hypoaccommodation are also present in a complete
third nerve palsy. A congenital third nerve paresis is often
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FIGURE 10-15. Photograph of a left third nerve palsy; there is a left ptosis
and the left eye is “down and out” (left exotropia and hypotropia).
partial, without ptosis, with variable amounts of limited elevation, depression, and adduction, with pupillary sparing, and may
show oculomotor synkinesis.
The two most common causes of pediatric third nerve
palsy are idiopathic congenital onset and head trauma. Other
causes include migraine, an association with a viral syndrome,
an intracranial tumor, or, rarely, a posterior communicating
aneurysm.14,62,105 Nontraumatic acquired third nerve palsy cases
must undergo a full workup with neuroimaging.62
TREATMENT
The treatment of complete third nerve palsy is extremely difficult because there are no vertical muscle forces to move nasally,
as all the vertical recti are paretic. Superior oblique tendon transfer to the medial rectus insertion has been suggested as a way
of providing medial forces.104 This procedure, however, does not
increase adduction as it only creates a leash and limits depression of the eye, resulting in a large hypertropia in downgaze. An
ipsilateral superior oblique tenotomy, with ipsilateral recession
of the lateral rectus and a large resection of medial rectus, is
probably the procedure most often used for a third nerve paresis
with an exotropia and hypotropia and some medial rectus function. In cases where this procedure has failed to correct the
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exotropia, this author has split the lateral rectus and transposed
the halves to the nasal border of the superior and inferior rectus
muscles. This procedure has worked in centering the eye;
however, horizontal excursions are minimal.
In addition to the difficulty in treating the strabismus,
patients with a third nerve palsy and ptosis with poor or absent
levator function, are at risk for developing corneal exposure if
the ptosis is repaired. Ptosis should be managed with a silicone
frontalis sling procedure, aiming for intentional undercorrection
of the lid position if there is a poor Bell’s phenomenon. The silicone sling procedure has an advantage of being reversible if
corneal exposure becomes a problem. Patients should be warned
about the risk of corneal exposure and that their diplopia may
be worse after lifting the eyelid, as this removes the occlusion.
Many wise patients and physicians opt for leaving the ptosis
alone if associated with a poor superior rectus muscle function
evidenced by a poor Bell’s phenomenon.
Inferior Oblique Paresis
See Chapter 9.
Möbius Syndrome
Möbius syndrome is characterized by a combination of facial
palsy, sixth nerve palsy, partial third nerve palsy, and distal limb
abnormalities such as syndactyly, club foot, or even amputation
defects.23 There is some degree of intellectual impairment in
75% of patients.23,131 The Möbius infant typically presents with
esotropia, limited abduction, lack of facial expression, and difficulty feeding caused by a poor sucking reflex. Craniofacial
anomalies can occur and include micrognathia, tongue abnormalities, and facial or oral clefts. Ocular motility abnormalities
include limited abduction in more than 90% of cases and limited
adduction in 65% of cases.23,66,86 Some patients have globe retraction on adduction and failure to abduct, typical of Duane’s syndrome. The inheritance pattern of Möbius syndrome is usually
sporadic, and there is great variability of findings,44 suggesting
that the syndrome represents a heterogeneous group of neuromuscular disorders.87 Prenatal exposure to misoprostol, the
abortion-inducing drug, has been implicated as a risk factor.23,41,120
Treatment of the strabismus is tailored to the individual situation. Patients with a large esotropia, tight medial rectus
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muscles, and poor abduction are probably best treated with large
bilateral medial rectus recessions similar to the treatment of a
patient with congenital fibrosis syndrome.
Sinus Surgery and Medial Rectus Muscle Injury
Endoscopic sinus surgery can result in severe damage to the
medial rectus muscle and even visual loss.31,69,98 This damage
occurs when the thin ethmoid bone is violated during endoscopic sinus surgery and the medial rectus muscle is traumatized. In most cases, part of the medial rectus muscle is removed,
often in the area of the neuromuscular junction (two-thirds of
the way back from the insertion or approximately 25 mm posterior to the insertion). On MRI, the medial rectus may be seen
to be myectomized and pulled into the ethmoid sinus (Fig.
10-16). The inferior rectus and inferior oblique muscles can also
be traumatized, but this is less common.98 Treatment of the adduction deficit and exotropia depends on the extent of the damage
to the medial rectus muscle and the state of the innervation.119
Unfortunately, in most cases, there is poor medial rectus muscle
function secondary to neuromuscular junction injury or a
posterior myectomy. If medial rectus muscle function is poor,
a partial-tendon transfer of the vertical rectus muscle to the
medial rectus insertion (Hummelsheim) or a procedure to create
a nasal tether to pull the eye to midline is indicated.6 Standard
exploration and muscle retrieval techniques (used for locating
lost muscles) do not work if the injury involves the neuromuscular junction or if a posterior myectomy was performed.
Aplasia of Extraocular Muscles
Although virtually all extraocular muscles have been described
as being congenitally absent, the inferior rectus is most commonly affected.13,70,101 The condition is often associated with
craniofacial dysostosis, anencephaly, or other congenital head
anomalies.8,22,42,88,113 Aplasia of the inferior rectus, superior
rectus, and superior oblique muscles can occur in otherwise
healthy children without craniofacial abnormalities.27,58,67 Figure
10-17 depicts a case in which this author surgically explored to
find aplasia of the right inferior rectus and hypoplasia of the left
inferior rectus muscle. This child was healthy and presented
with a right hypertropia and bilateral limited depression, right
eye more than left eye. An absent rectus muscle is managed by
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A
B
FIGURE 10-16A–B. Photographs of patient with right medial rectus
injury associated with sinus surgery. (A) Rightgaze, full motility. (B)
Primary position with right exotropia.
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C
D
FIGURE 10-16C–D. (C) Leftgaze, showing no significant adduction of
right eye. This patient had no adduction saccade. (D) MRI shows the posterior aspect of the right medial rectus has been myectomized, and the
posterior cut end of the muscle is entrapped in the ethmoid sinus.
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A
B
FIGURE 10-17A,B. Photographs of bilateral asymmetrical inferior rectus
muscle hypoplasia (surgeon’s view) at the time of surgery. Patient presented with a right hypertropia and severe limitation of depression,
rightgaze. (A) The left eye has an underdeveloped inferior rectus muscle.
(B) The right inferior rectus muscle shows only the anterior ciliary
vessels, but there is no inferior rectus muscle (i.e., aplasia of the inferior
rectus muscle).
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a Hummelsheim-type transposition procedure to substitute for
the absent muscle.
Craniosynostosis
Causes for strabismus associated with craniosynostosis include
divergent orbits, displaced extraocular muscles agenesis of
extraocular muscles, and extorsion of the orbits.22,42,88,113 A
common pattern of strabismus seen in patients with a variety
of craniosynostosis syndromes is exotropia with apparent severe
bilateral inferior oblique overaction, superior oblique underaction, and a large V-pattern (Fig. 10-18). The possible causes for
the inferior oblique overaction and V-pattern can be an absence
of the superior oblique tendon or extorted orbits.9 Extorted orbits
shift the medial rectus up and the lateral rectus down so the
medial rectus pulls the adducting eye up and the lateral rectus
pulls the abducting eye down, which simulates inferior oblique
overaction. Likewise, the inferior rectus muscle are displaced
nasally and the superior rectus muscle temporally so that in
downgaze the eyes converge and in upgaze they diverge.20
FIGURE 10-18. Photograph of patient with Pfeiffer syndrome. Motility
exam showed an exotropia, inferior oblique overaction, superior oblique
underaction, and V-pattern. Note the extreme underaction of the right
superior oblique muscle as the patient looks down and to the left.
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DISSOCIATED VERTICAL DEVIATION AND
DISSOCIATED HORIZONTAL DEVIATION
Dissociated vertical deviation (DVD) is the tendency for an eye
to elevate, abduct, and extort, when binocularity is suspended
by occlusion or the patient spontaneously dissociates (often
when fatigued). DVD is almost always bilateral, but asymmetrical cases may appear to be unilateral. Prolonged occlusion of
the eye that appears not to have DVD, however, will almost
always disclose a latent DVD. Note that, with a true hypertropia, there is a corresponding hypotropia of the fellow eye and,
on alternate cover testing when the hypertropic eye moves
down into primary position, the fellow eye also moves down to
become hypotropic. Thus, a true hypertropia is consistent with
Hering’s law of yoke muscles. In contrast, DVD violates Hering’s
law of yoke muscles because covering the right eye makes the
right eye drift up, and covering the left eye makes the left eye
drift up with no corresponding hypotropia of the fellow eye (Fig.
10-19). One can think of DVD as two individual hypertropias
that are dissociated, thus the term, dissociated vertical deviation. DVD increases on head tilt: head tilt to the right increases
a right DVD and head tilt to the left increases a left DVD.
DVD occurs when normal binocular visual development is
disrupted and is associated with congenital esotropia, congenital exotropia,11 congenital media opacities (e.g., monocular
congenital cataracts), and even unilateral optic nerve hypoplasia.
Rarely, this author has seen patients with primary DVD; that is,
no horizontal strabismus, and no history of previous strabismus
surgery (Fig. 10-19). These patients usually have some degree of
stereoacuity, sometimes high-grade stereoacuity.
On version testing, DVD can mimic inferior oblique overaction because the vision of the adducting eye is blocked by the
bridge of the nose; this dissociates the eyes, causing the DVD of
the adducting eye to be manifest. The two can be distinguished,
however, as DVD has no true hypotropia of the opposite eye,
and the hyperdeviation is the same in abduction as in adduction.
With inferior oblique overaction, there is a hypotropia of the
opposite eye and the deviation increases as the eye moves into
adduction. DVD and inferior oblique overaction often coexist
with congenital esotropia.127
The cause of dissociated vertical deviation is unknown.
Guyton hypothesized that abnormal binocular development
causes unbalanced input to the vestibular system, resulting in
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A
B
FIGURE 10-19A,B. Photographs of bilateral dissociated vertical deviation
(DVD). Patient has primary DVD with excellent stereoacuity and has
never had strabismus surgery. (A) The left eye is covered to manifest the
left DVD. (B) The right eye is covered and discloses a right DVD. Note
that the eye behind the cover is not only elevated but is also slightly
exodeviated.
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latent nystagmus with a cyclovertical movement. Cycloversion/
vertical vergence is invoked to damp the cyclovertical nystagmus
(a cyclovertical “nystagmus blockage” phenomenon), aiding
vision in the fixing eye. Unfortunately, this mechanism also produces unavoidable and undesirable elevation and extorsion of
the fellow eye that results in DVD.45
This author has a theory about the neurophysiological basis
for DVD. It is interesting that DVD is associated with disruption of early binocular visual development. The interstitial
nucleus of Cajal is a brainstem nucleus that regulates cyclovertical movements. The interstitial nucleus of Cajal receives
inhibitory input from binocular cells in the occipital cortex, and
these inhibitory pathways act to control this nucleus. Lesions
around the interstitial nucleus of Cajal that interrupt the binocular inhibitory input result in nucleus disinhibition, which is
clinically manifested as seesaw nystagmus. Seesaw nystagmus
is a dissociated cyclovertical/horizontal nystagmus. When
seesaw nystagmus occurs in infancy, it can look quite similar to
DVD. Infantile strabismus or a dense monocular congenital
cataract disrupts binocular visual development and reduces
binocular cortical cells. Perhaps the lack of binocular cortical
cells associated with congenital strabismus or a unilateral
blurred retinal image in infancy, results in reduced binocular
inhibitory input to the interstitial nucleus of Cajal or similar
cyclovertical brainstem nuclei. Reduced binocular inhibitory
input would cause disinhibition of these cyclovertical nuclei,
giving rise to what we see clinically as DVD.
If early surgery for infantile esotropia improves binocularity, then children who have had early surgery should have less
DVD. Recent reports on the incidence of DVD in children who
have had early surgery for infantile esotropia, however, remain
unchanged from reports 30 years previous.81,136 Even though the
incidence may be the same, the severity of DVD seems to have
diminished over the past few decades. It is this author’s opinion,
along with the observations of senior expert strabismologists,
that the incidence of severe DVD requiring surgery has
decreased. Performing surgery for a large, cosmetically obvious
DVD in the 1970s and early 1980s was commonplace. As a resident in ophthalmology, this author remembers operating every
month on several DVD patients. Over the past several years,
there have only been a few cases requiring surgery, and usually
on older adults with DVD. The author’s visits to countries
where surgeons continue to operate late, after 2 years of age,
have disclosed that a very high prevalence of big, surgically
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significant DVD persists. Perhaps, with the advent of early intervention of infantile esotropia in this country, our children with
infantile esotropia have been able to establish better binocular
fusion, thus reducing the severity, but not the incidence, of the
DVD. In this author’s report on very early surgery for congenital esotropia (surgery between 13 and 19 weeks of age), four of
seven patients had DVD on last examination (2–8 years; mean,
4 years).136 This DVD, however, was very small and could
only be demonstrated by prolonged cover testing. None of the
patients required DVD surgery, although one had surgery for
inferior oblique overaction. M cell afferent pathway development is responsible for motor fusion and control. Because M cell
development starts very early, around 6 weeks to 2 months of
age, perhaps our “very early surgery” is not early enough to
establish strong motor fusion and eliminate DVD.137
The treatment of DVD is surgical, and surgery is indicated
if the DVD exists to the point that it becomes a cosmetic
problem. DVD is most often bilateral, and bilateral surgery is
usually performed. An exception is with amblyopia, where
surgery is performed only on the amblyopic eye. With amblyopia of 2 lines or more, the patient will always fixate with the
sound eye, and the sound eye will not manifest the DVD. Most
consider superior rectus recessions as the treatment choice for
pure DVD without inferior oblique overaction. If DVD and inferior oblique overaction coexist, then an anterior transposition of
the inferior oblique is indicated, as this will address both problems with one procedure.12,43,93,121 Strabismus surgery rarely, if
ever, cures DVD.
Dissociated horizontal deviation (DHD), which may be
unilateral or bilateral, is a subtype of DVD that often occurs
in patients who have had previous strabismus surgery for congenital esotropia.129 This is a dissociated condition like DVD,
but the exocomponent of DVD is exaggerated. Cover/uncover
testing may show no shift or a small esotropia, but prolonged
occlusion produces an exodeviation. Think of DHD when examining patients with a small residual esotropia, who also have a
dissociated exodeviation. The treatment of DHD is recession of
the ipsilateral lateral rectus muscle.128
Torticollis and Face Turns
This section covers the approach to patients who present with
an abnormal head posture. Abnormal head posturing includes
torticollis (head tilt), chin elevation and depression, and face
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turn. These forms of head posturing can occur independently or
in combination, as a patient with a superior oblique palsy will
often have both a head tilt and a face turn. Torticollis can be
secondary to a musculoskeletal abnormality of the neck or to an
ocular problem compensated by head posturing. A simple initial
test to determine the cause is to ask the patients to close their
eyes and observe for several seconds to see if the head posturing
spontaneously improves. If the face turn improves when the
eyes are closed, this suggests an ocular cause. Next, passively
move the patient’s head from side to side with the patient’s eyes
closed. If the range of motion of the head and neck is normal,
this verifies that the head posturing is an ocular torticollis;
however, a stiff neck indicates a musculoskeletal problem.
By far the most common ocular causes of abnormal head
posturing are nystagmus with a null point and incomitant
strabismus with compensatory head posturing to allow fusion.
A face turn is often identified by observing the patient’s head
posture. A better way to evaluate the presence of a face turn is
to observe the position of the eyes. Normal patients with
straight eyes and no face turn will have both eyes centered
within the palpebral fissures. If a face turn is present, there will
be a gaze preference with the eyes constantly shifted opposite to
the face turn. For example, a face turn to the right is associated
with eyes shifted to the left (Fig. 10-20), and a chin elevation
will have the eyes shifted down. When examining a patient for
a face turn, first observe the position of the eyes and the presence of a gaze preference. Next, turn or tilt the head opposite to
the compensatory position to place the eyes into the nonpreferred field of gaze. If there is a face turn to the right, turn the
head to the left; if there is a head tilt to the right, tilt the head
to the left. While the head is held opposite to the compensatory
position, observe for nystagmus or strabismus. If nystagmus
occurs or increases with a forced face turn to the opposite side,
then a compensatory face turn is present to keep the eyes in the
area of the null point. If strabismus is produced by forced head
tilt, or turns the eye in with a previously fusing patient, then
the compensatory head posturing is adopted to maintain fusion,
keeping the eyes in the field of gaze where the eyes are aligned.
In addition to face turns and head tilts, chin elevations or depressions can be compensatory for nystagmus or strabismus, and
chin elevations compensate for ptosis.
The degree of face turn can be measured by using an orthopedic goniometer placed on the head. Any protractor will work
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FIGURE 10-20. Photograph of ocular torticollis in a patient with nystagmus. Patient has a face turn to the right to place the eyes at the null
point in leftgaze. The best way to identify a face turn is to evaluate the
position of the eyes. If there is a strong gaze preference for an eccentric
gaze position, then consider the possibility of a compensatory face turn.
as the line of sight is compared to the direction of the face, with
the nose as the pointer.77 An alternative method for measuring
face turn associated with Duane’s syndrome or unilateral
limited eye movement is to place a prism over the eye with
limited rotation, with the apex pointing toward the direction of
the deviated eye. The prism is progressively increased until the
face turn is corrected. The amount of prism required to neutralize the face turn is recorded in prism diopters. Prism diopters
can be converted to degrees by dividing by 2. Prism correction
of head posturing can also be used to measure face turns associated with nystagmus.
Incomitant Strabismus Causing Compensatory
Head Posturing
Head posturing compensates for incomitant strabismus by
placing the eyes in a field of gaze where the eyes are best aligned
to achieve binocular fusion. For example, a patient with a left
sixth nerve palsy will have a large esotropia in leftgaze and
straight eyes in rightgaze. These patients will adopt a face turn
to the left to keep their eyes aligned in rightgaze. An incomitant
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strabismus where the eyes are aligned in an eccentric field of
gaze can cause an abnormal head posture; this includes cranial
nerve palsies, restrictive strabismus, A- or V-patterns, and
primary oblique dysfunction. For example, patients with fusion
and an A-pattern exotropia or V-pattern esotropia will show a
chin depression (eyes straighter in upgaze), whereas an A-pattern
esotropia or V-pattern exotropia will show a chin elevation (eyes
straighter in downgaze).
The treatment of an abnormal head posture caused by
incomitant strabismus is simply to correct the strabismus in
primary position and provide a large field of single binocular
vision. If the fixing eye has limited ductions, then move the eye
with limited movements to primary position, and the normal
eye will follow.
Nystagmus Causing Compensatory
Head Posturing
A compensatory head posture can stabilize nystagmus by
placing the eyes at the null point. If the null point is to the right,
the patient will shift the eyes to the right and have a face turn
to the left. Head posturing associated with nystagmus can take
the form of a face turn, chin elevation or depression, or a head
tilt.
A compensatory face turn associated with congenital nystagmus can be treated using eye muscle surgery to move the eye
position from the null point to primary position.77 The general
surgical principles for correcting a face turn are as follows5:
1. Kestenbaum–Anderson–Parks (Kestenbaum) procedure:
With a compensatory face turn to the right, the eyes will be
shifted to the left. Therefore, to correct the face turn, move the
eyes to the right into primary position (Fig. 10-21), which is done
by moving the right eye out (right medial rectus recession–right
lateral rectus resection) and moving the left eye in (left lateral
rectus recession and a left medial rectus resection). The amount
of surgery for a specific amount of face turn is listed in Table
10-7. Note, Parks Poker Straight 5-6-7-8 (medial recession 5 mm,
medial resection 6 mm, lateral recession 7 mm, and lateral resection 8 mm) is a way of remembering the amount of surgery for
a small face turn. In most cases, however, larger amounts of
surgery are needed.77 Large recessions and resections are needed
for a face turn associated with nystagmus. Postoperative
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FIGURE 10-21. Drawing showing how to correct a face turn to the right
associated with nystagmus using the Kestenbaum procedure. The view is
looking down on a face turn to the right with eyes in leftgaze at the null
point. Surgically correct the face turn by simply moving the eyes into
primary position. The arrows in the diagram indicate moving the eyes to
the right to place the eyes in primary position. The left eye is shifted
nasally (recess lateral rectus muscle and resect the medial rectus muscle)
and the right eye moved temporally (recess medial rectus muscle and
resect the lateral rectus muscle) to correct the face turn.
TABLE 16-7. Kestenbaum Procedure for Nystagmus with a Face Turn
to the Right (Eyes Shifted Right).
Left eye
Face turn
(degrees)
Right eye
Recess lateral
rectus (mm)
Resect medial
rectus (mm)
Recess medial
rectus (mm)
Resect lateral
rectus (mm)
7
9
10
11
6
8
8.5
9.5
5
6.5
7
8
8
10
11
12.5
20
30
45
50
See Figures 10-20, 10-21.
Source: Modified from Refs. 5, 135, permission.
378
handbook of pediatric strabismus and amblyopia
limitation of ocular movements is to be expected, deemed to be
an acceptable trade-off.
2. Vertical head posturing: Chin depression (eyes up) is
treated with large bilateral superior rectus recessions (8–9 mm)
and inferior rectus resections (6–7 mm). For large chin depressions, this can be combined or performed in stages, the superior
rectus recessions first, then inferior rectus resections later if necessary. Chin elevations (eyes down) can be treated similarly by
recessing the inferior rectus muscles (7–8 mm) and resecting the
superior rectus muscles (6–7 mm).99
Surgical therapy should be based on the greatest amount
of abnormal head posture measured at distance and near. For
example, if the face turn is obvious at distance and not at near,
full correction directed at the face turn in the distance should
be undertaken. When strabismus coexists with nystagmus,
the head posture can be corrected by moving the fixing eye to
primary position. Then adjust the fellow eye to compensate for
the residual strabismus.
Compensatory head tilts are also associated with nystagmus, which can be corrected by rotating the eyes back to
primary position. A head tilt to the right can be treated by surgically extorting the right eye and intorting the left eye.122
SURGICAL TREATMENT OF NYSTAGMUS: NO FACE TURN
Although the Kestenbaum–Anderson–Parks procedure is
directed toward eliminating the abnormal horizontal face turn
associated with nystagmus, another approach has been described
to damp nystagmus in patients without a face turn. Simultaneous retroequatorial recessions of all four horizontal rectus
muscles have been reported to decrease the amplitude of nystagmus and improve visual acuity.30,36,97 The precise mechanism
responsible for damping the nystagmus is not known, and the
long-term effect remains unknown. Vision improves only in
cases of motor nystagmus, not in patients with sensory nystagmus who have an abnormal afferent pathway.
Additional Causes of Ocular Torticollis
Less common mechanisms for head posturing do exist. Rarely,
a patient with diplopia adopts a head posture that induces
maximal image separation rather than fusion, thus making suppression of the diplopic image easier. Other reasons for abnor-
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379
mal head posturing include compensation for visual field
defects, restriction of the good eye in monocular patients, manifest latent nystagmus with a face turn to keep the fixing eye in
adduction, ptosis with chin elevation, tilting for monocular
torsion, and cosmetic reasons. Other causes include asymmetrical dissociated vertical deviation, refractive error in which the
patient adopts a face turn presumably to partially block the
pupil, inducing a pinhole effect that provides better visual acuity.
References
1. Amemiya T, Yoshida H, Harayama K, et al. Long-term results of
retinal detachment surgery. Ophthalmologica 1978;177:64–69.
2. Anderson RL, Baumgartner SA. Strabismus and ptosis. Arch Ophthalmol 1980;98:1062–1067.
3. Appleton RE, Chitayat D, Jan JE, Kennedy R, Hall JG. Joubert’s syndrome associated with congenital ocular fibrosis and histidinemia.
Arch Neurol 1989;46(5):579–582.
4. Apt L, Axelrod RN. Generalized fibrosis of the extraocular muscles.
Am J Ophthalmol 1978;85(6):822–829.
5. Archer SM. Strabismus surgery planning. In: Del Monte MA, Archer
SM (eds) Atlas of pediatric ophthalmology and strabismus surgery.
New York: Churchill Livingstone, 1993:14.
6. Awad AH, Shin GS, Rosenbaum AL, Goldberg RL. Autogenous fascia
augmentation of a partially extirpated muscle with a subperiosteal
medial orbitotomy approach. J AAPOS. 1997;1(3):138–142.
7. Ball SF, Ellis GS, Herrington RG, Liang K. Brown’s superior oblique
tendon syndrome after Baerveldt glaucoma implant. Arch Ophthalmol 1991;110:1368.
8. Barnes RJ. Anencephaly with absence of superior oblique tendon.
Surv Ophthalmol 1972;16:371–374.
9. Bagshaw J. The ‘heavy eye’ phenomenon. A preliminary report. Br J
Ophthalmol 1966;23:73–78.
10. Biglan AW, et al. Management of strabismus with botulinum A
toxin. Ophthalmology 1989;96:935–943.
11. Biglan AW, Davis JS, Cheng KP, Pettapiece MC. Infantile exotropia.
J Pediatr Ophthalmol Strabismus 1996;33(2):79–84.
12. Black BC. Results of anterior transposition of the inferior oblique
muscle in incomitant dissociated vertical deviation. JAAPOS 1997;
1(2):83–87.
13. Brady AP, Stack JP, O’Keeffe M. Congenital absence of extraocular
muscles: MR demonstration. J Comput Assist Tomogr 1992;16(3):
490–491.
14. Branley MG, Wright KW, Borchert MS. Third nerve palsy due to
cerebral artery aneurysm in a child. Aust NZ J Ophthalmol 1992;20:
137–140.
380
handbook of pediatric strabismus and amblyopia
15. Bremer DL, Rogers GL, Quick LD. Primary-position hypotropia after
anterior transposition of the inferior oblique. Arch Ophthalmol
1986;104:229–232.
16. Brodsky MC. Hereditary external ophthalmoplegia synergistic divergence, jaw winking, and oculocutaneous hypopigmentation: a
congenital fibrosis syndrome caused by deficient innervation to
extraocular muscles. Ophthalmology 1998;105(4):717–725.
17. Brooks SE, Ribeiro GB, Archer SM, Elner VM, Del Monte MA. Fat
adherence syndrome treated with intraoperative mitomycin-C: a
rabbit model. J Pediatr Ophthalmol Strabismus 1996;33(1):21–27.
18. Brooks SE, Olitsky SE, de Ribeiro G. Augmented Hummelsheim
procedure for paralytic strabismus. J Pediatr Ophthalmol Strabismus
2000;37(4):189–195; quiz 226–227.
19. Capo H, Guyton DL. Ipsilateral hypermetropia after cataract surgery.
Ophthalmology 1996;103:721–730.
20. Cheng H, Burdon MA, Shun-Shin GA, Czypionka S. Dissociated eye
movements in craniosynostosis: a hypothesis revisited. Br J Ophthalmol 1993;77:563–568.
21. Coats DK, Paysse EA, Plager DA, Wallace DK. Early strabismus
surgery for thyroid ophthalmopathy. Ophthalmology 1999;106(2):
324–329.
22. Coats DK, Ou R. Anomalous medial rectus muscle insertion in a
child with craniosynostosis. Binoc Vis Strabismus Q 2001;16(2):119–
120.
23. Cronenberger MF, de Castro Moreira JB, Brunoni D, et al. Ocular and
clinical manifestations of Möbius’ syndrome. J Pediatr Ophthalmol
Strabismus 2001;38(3):156–162.
24. Cruz OA, Davitt BV. Bilateral inferior rectus muscle recession for
correction of hypotropia in dysthyroid ophthalmopathy. JAAPOS
1999;3(3):157–159.
25. Demer JL, von Noorden GK. High myopia as an unusual cause
of restrictive motility disturbance. Surv Ophthalmol 1989;33:281–
284.
26. Doherty EJ, Macy ME, Wang SM, Dykeman CP, Melanson MT, Engle
EC. CFEOM3: a new extraocular congenital fibrosis syndrome that
maps to 16q24.2–q24.3. Investig Ophthalmol Vis Sci 1999;40(8):
1687–1694.
27. Drummond GT, Keech RV. Absent and anomalous superior oblique
and superior rectus muscles. Can J Ophthalmol 1989;24(6):275–279.
28. Effron L, Price RL, Berlin AJ. Congenital unilateral orbital fibrosis
with suspected prenatal orbital penetration. J Pediatr Ophthalmol
Strabismus 1985;22(4):133–136.
29. Egbert J, May K, Kersten R, Kulwin D. Pediatric orbital floor fracture: direct extraocular muscle involvement. Ophthalmology 2000;
107:1875–1879.
30. Egbert JE, Anderson JH, Summers CG. Increased duration of low
retinal slip velocities following retroequatorial placement of horizontal recti. J Pediatr Ophthalmol Strabismus 1995;32(6):359–363.
chapter
10:
complex strabismus
381
31. Eitzen JP, Elsas FJ. Strabismus following endoscopic intranasal sinus
surgery. J Pediatr Ophthalmol Strabismus 1991;28(3):168–170.
32. Engle EC, Goumnerov BC, McKeown CA, et al. Oculomotor nerve
and muscle abnormalities in congenital fibrosis of the extraocular
muscles. Ann Neurol 1997;41(3):314–325.
33. Engle EC, Marondel I, Houtman WA, et al. Congenital fibrosis of the
extraocular muscles (autosomal dominant congenital external
ophthalmoplegia): genetic homogeneity, linkage refinement, and
physical mapping on chromosome 12. Am J Hum Genet 1995;57(5):
1086–1094.
34. Engle EC, Kunkel LM, Specht LA, Beggs AH. Mapping a gene for congenital fibrosis of the extraocular muscles to the centromeric region
of chromosome 12. Nat Genet 1994;7(1):69–73.
35. Brodsky MC, Fray KJ. Surgical management of intermittent
exotropia with high AC/A ratio. J Am Assoc Pediatr Ophthalmol
Strabismus 1998;2:330–332.
36. Fioretto M, Burtolo C, Fava GP. New surgical method for nystagmus
without null point. Ophthalmologica 1991;203(4):180–183.
37. Flaherty MP, Grattan-Smith P, Steinberg A, Jamieson R, Engle EC.
Congenital fibrosis of the extraocular muscles associated with cortical dysplasia and maldevelopment of the basal ganglia. Ophthalmology 2001;108(7):1313–1322.
38. Fujii GY, Kah-Guan AE, Pieramici DJ, et al. Macular translocation:
unifying concepts, terminology, and classification. Am J Ophthalmol 1992;114:72–80.
39. Gillies WE, Harris AJ, Brooks AM, Rivers MR, Wolfe RJ. Congenital fibrosis of the vertically acting extraocular muscles. A new group
of dominantly inherited ocular fibrosis with radiologic findings.
Ophthalmology 1995;102(4):607–612.
40. Grimmet MR, Lambert S. Superior rectus overcorrection after
cataract extraction. Am J Ophthalmol 1992;114:72–80.
41. Goldberg AB, Greenberg MB, Darney PD. Misoprostol and pregnancy. N Engl J Med 2001;344(1):38–47.
42. Greenberg MF, Pollard ZF. Absence of multiple extraocular muscles
in craniosynostosis. J Am Assoc Pediatr Ophthalmol Strabismus
1998;2(5):307–309.
43. Guemes A, Wright KW. Effect of graded anterior transposition of the
inferior oblique muscle on versions and vertical deviation in primary
position. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2(4):201–
206.
44. Gusek-Schneider GC, Langenbucher A, Seitz B. Association of
keratoconus and Möbius’ syndrome. J Pediatr Ophthalmol Strabismus
2001;38(1):47–48.
45. Guyton DL. Dissociated vertical deviation: etiology, mechanism,
and associated phenomena. Costenbader lecture. J Am Assoc Pediatr
Ophthalmol Strabismus 2000;4(3):131–144.
46. Hamed, Mancuso. Inferior rectus muscle contracture syndrome after
retrobulbar anesthesia. Ophthalmology 1991;98:1506–1512.
382
handbook of pediatric strabismus and amblyopia
47. Hamlet YJ, Goldstein JH, Rosenbaum JD. Dehiscence of lateral
rectus muscle following intrascleral buckling procedure. Ann Ophthalmol 1982;14:694–697.
48. Harley RD, Rodrigues MM, Crawford JS. Congenital fibrosis of the
extraocular muscles. J Pediatr Ophthalmol Strabismus 1978;15(6):
346–358.
49. Harley RD, Rodrigues MM, Crawford JS. Congenital fibrosis of the
extraocular muscles. Trans Am Ophthalmol Soc 1978;76:197–226.
50. Hayashi T, Iwashige H, Maruo T. Clinical features and surgery for
acquired progressive esotropia associated with severe myopia. Acta
Ophthalmol Scand 1999;77(1):66–71.
51. Hertel RW, Katowitz JA, Young PL, et al. Congenital unilateral fibrosis, blepharoptosis, and enophthalmos syndrome. Ophthalmology
1992;99:347–355.
52. Holmes JM, Beck RW, Kip KE, Droste PJ, Leske DA. Predictors of
nonrecovery in acute traumatic sixth nerve palsy and paresis. Ophthalmology 2001;108(8):1457–1460.
53. Holmes JM, Beck RW, Kip KE, Droste PJ, Leske DA. Botulinum toxin
treatment versus conservative management in acute traumatic sixth
nerve palsy or paresis. J Am Assoc Pediatr Ophthalmol Strabismus
2000;4(3):145–149.
54. Hotchkiss MG, Miller NR, Clark AW, et al. Bilateral Duane’s retraction syndrome: a clinical-pathologic case report. Arch Ophthalmol
1980;98:870–874.
55. Huber A. Electrophysiology of the retraction syndromes. Br J Ophthalmol 1974;58:293–300.
56. Hudson HL, Feldon SE. Late overcorrection of hypotropia in Grave’s
ophthalmopathy. Ophthalmology 1992;99:356–360.
57. Hwang JM, Wright KW. Combined study on the causes of strabismus after retinal surgery. Korean J Ophthalmol 1994;8(2):83–91.
58. Ingham PN, McGovern ST, Crompton JL. Congenital absence of the
inferior rectus muscle. Aust NZ J Ophthalmol 1986;14(4):355–358.
59. Jameson NA, Good WV, Hoyt CS. Fat adherence simulating inferior
oblique palsy following blepharoplasty. Arch Ophthalmol 1992;
110(10):1369.
60. Kalpakian B, Bateman JB, Sparkes RS, Wood GK. Congenital ocular
fibrosis syndrome associated with the Prader–Willi syndrome. J
Pediatr Ophthalmol Strabismus 1986;23(4):170–173.
61. Kanski JJ, Elkington AR, Davies MS. Diplopia after retinal detachment surgery. Am J Ophthalmol 1973;76:38–40.
62. Kodsi SR, Younge BR. Acquired oculomotor, trochlear, and abducent
cranial nerve palsies in pediatric patients. Am J Ophthalmol 1992;
114(5):568–574.
63. Krzizok TH, Kaufmann H, Traupe H. New approach in strabismus
surgery in high myopia. Br J Ophthalmol 1997;81:625–630.
64. Krzizok TH, Schroeder BU. Measurement of recti eye muscle paths
by magnetic resonance imaging in highly myopic and normal subjects. Investig Ophthalmol Vis Sci 1999;40(11):2554–2560.
chapter
10:
complex strabismus
383
65. Lee J, et al. Results of a prospective randomized trial of botulinum
toxin therapy in acute unilateral sixth nerve palsy. J Pediatr Ophthalmol Strabismus 1994;31:283–286.
66. Lengyel D, Zaunbauer W, Keller E, Gottlob I. Mobius syndrome: MRI
findings in three cases. J Pediatr Ophthalmol Strabismus 2000;37(5):
305–308.
67. Lin PY, Yen MY. Congenital absence of bilateral inferior rectus
muscles: a case report. J Pediatr Ophthalmol Strabismus 1997;34(6):
382–384.
68. Lueder GT, Scott WE, Kutschke PJ, Keech RV. Long-term results of
adjustable suture surgery for strabismus secondary to thyroid ophthalmopathy. Ophthalmology 1992;99(6):993–997.
69. Mark LE, Kennerdell JS. Medial rectus injury from intranasal
surgery. Arch Ophthalmol 1979;97(3):459–461.
70. Mets MB, Parks MM, Freeley DA, Cornell FM. Congenital absence
of inferior rectus muscle: report of three cases and their management. Binoc Vis 1987;2(2):77–86.
71. Mets MB, Wendell ME, Gieser RG. Ocular deviation after retinal
detachment surgery. Am J Ophthalmol 1985;99:667–672.
72. Metz HS, Norris A. Cyclotorsional diplopia following retinal
detachment surgery. J Pediatr Ophthalmol Strabismus 1987;24(6):
287–290.
73. Metz HS. Double elevator palsy. Arch Ophthalmol 1979;97:901–
909.
74. Metz HS, Dickey CF. Treatment of unilateral acute sixth nerve palsy
with botulinum toxin. Am J Ophthalmol 1991;112:381–384.
75. Michel O, Oberlander N, Neugebauer P, Neugebauer A, Russmann
W. Follow-up of transnasal orbital decompression in severe Graves’
ophthalmopathy. Ophthalmology 2001;108(2):400–404.
76. Miller NR, Kiel SM, Green WR, Clark AW. Unilateral Duane’s
retraction syndrome. Arch Ophthalmol 1982;100:1468–1472.
77. Mitchell PR, Wheeler MB, Parks MM, Kestenbaum surgical procedure for torticollis secondary to congenital nystagmus. J Pediatr
Ophthalmol Strabismus 1987;24(2):87–93.
78. Munoz M, Rosenbaum AL. Long-term strabismus complications following retinal detachment surgery. J Pediatr Ophthalmol Strabismus
1987;24(6):309–314.
79. Nakano M, Yamada K, Fain J, et al. Homozygous mutations in ARIX
(PHOX2A) result in congenital fibrosis of the extraocular muscles
type 2. Nat Genet 2001.
80. Nardi M, Barca L. Hypercorrection of hypotropia in Graves’ ophthalmopathy. Ophthalmology 1993Jan;100(1):1–2.
81. Neely DE, Helveston EM, Thuente DD, Plager DA. Relationship of
dissociated vertical deviation and the timing of initial surgery for
congenital esotropia. Ophthalmology 2001;108(3):487–490.
82. Neugebauer A, Fricke J, Kirsch A, Russmann W. Modified transposition procedure of the vertical recti in sixth nerve palsy. Am J Ophthalmol 2001;131(3):359–363.
384
handbook of pediatric strabismus and amblyopia
83. Oh SY, Clark RA, Velez F, Demer JL. Magnetic resonance imaging
demonstration of instability of rectus pulleys as cause of incomitant
strabismus. Investig Ophthalmol Vis Sci 2001;167:42–44.
84. Parks MM. Causes of the adhesive syndrome In: Symposium on strabismus. Transaction of the New Orleans Academy of Ophthalmology. St Louis: Mosby, 1978:269–279.
85. Pearlman JT, Christensen RE. Motility problems following retinal
detachment surgery. Am Orthopt J 1972;22:64–67.
86. Pedraza S, Gamez J, Rovira A, et al. MRI findings in Möbius
syndrome: correlation with clinical features. Neurology 2000;55(7):
1058–1060.
87. Peleg D, Nelson GM, Williamson RA, Widness JA. Expanded Möbius
syndrome. Pediatr Neurol 2001;24(4):306–309.
88. Pinchoff BS, Sandall G. Congenital absence of the superior oblique
tendon in craniofacial dysostosis. Ophthalmic Surg 1985;16(6):375–
377.
89. Porter JD, Baker RS. Absence of oculomotor and trochlear
motoneurons leads to altered extraocular muscle development in
the Wnt-1 null mutant mouse. Dev Brain Res 1997;100(1):121–
126.
90. Prata JA, Minckler DS, Green RL. Pseudo-Brown’s syndrome as a
complication of glaucoma drainage implant surgery. Ophthalmic
Surg 1993;24:608–611.
91. Prendiville P, Chopra M, Gauderman WJ, Feldon SE. The role of
restricted motility in determining outcomes for vertical strabismus
surgery in Graves’ ophthalmology. Ophthalmology 2000;107(3):545–
549.
92. Price RL, Pederzolli A. Strabismus following retinal detachment
surgery. Am Orthopt J 1982;32:9–17.
93. Quinn AG, Kraft SP, Day C, Taylor RS, Levin AV. A prospective evaluation of anterior transposition of the inferior oblique muscle, with
and without resection, in the treatment of dissociated vertical deviation. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(6):348–
353.
94. Raab EL. Clinical features of Duane’s syndrome. J Pediatr Ophthalmol Strabismus 1986;23:64–68.
95. Raina J, Wright KW, Lin MM, McVey JH. Effectiveness of lateral
rectus Y split surgery for correcting the upshoot and downshoot in
Duane’s retraction syndrome, Type III. Binoc Vis Strabismus 1997;
12(4):233–238.
96. Reck AC, Manners R, Hatchwell E. Phenotypic heterogeneity may
occur in congenital fibrosis of the extraocular muscles. Br J Ophthalmol 1998;82(6):676–679.
97. Reinecke RD. Retroequatorial placement of horizontal recti. J
Pediatr Ophthalmol Strabismus 1996;33(3):201–202.
98. Rene C, Rose GE, Lenthall R, Moseley I. Major orbital complications
of endoscopic sinus surgery. Br J Ophthalmol 2001;85(5):598–603
(review).
chapter
10:
complex strabismus
385
99. Roberts EL, Saunders RA, Wilson ME. Surgery for vertical head position in null point nystagmus. J Pediatr Ophthalmol Strabismus
1996;33(4):219–224.
100. Rogers GL, Bremer DL. Surgical treatment of the upshoot and downshoot in Duane’s retraction syndrome. Ophthalmology 1984;91(11):
1380–1383.
101. Romano PE. Absent or hypoplastic extraocular muscles? J Med
Genet 1989;26(3):216.
102. Rosenbaum A, Kushner BJ, Kirschen D. Vertical rectus muscle transposition and botulinum toxin (oculinum) to medial rectus for
abducens palsy. Arch Ophthalmol 1989;107:820.
103. Roth AM, Sypnicki BA. Motility dysfunction following surgery for
retinal detachment. Am Orthopt J 1975;25:118–121.
104. Saunders RA, Rogers CT. Superior oblique transposition for third
nerve palsy. Ophthalmology 1982;89:310.
105. Schumacher-Feero LA, Yoo KW, Solari FM, Biglan AW. Third
cranial nerve palsy in children. Am J Ophthalmol 1999;128(2):216–
221.
106. Scott WE, Jackson OB. Double elevator palsy: the significance of
inferior rectus restriction. Ophthalmology 1977;27:5–10.
107. Scott AB, Wong GY. Duane’s syndrome: an electromyographic study.
Arch Ophthalmol 1972;87:142–147.
108. Seiff SR, Good WV. Hypertropia and the posterior blowout fracture:
mechanism and management. Ophthalmology 1996;103(1):152–
156.
109. Sener EC, Lee BA, Turgut B, Akarsu AN, Engle EC. A clinically
variant fibrosis syndrome in a Turkish family maps to the CFEOM1
locus on chromosome 12. Arch Ophthalmol 2000;118(8):1090–1097.
110. Sewell JJ, Knobloch WH, Eifrig DE. Extraocular muscle imbalance
after surgical treatment for retinal detachment. Am J Ophthalmol
1974;78:321.
111. Smiddy WE, Loupe D, Michels RG, et al. Extraocular muscle imbalance after scleral buckling surgery. Ophthalmology 1989;96:1485–
1490.
112. Smith SL, Starita RJ, Fellman RL, Lynn JR. Early clinical experience
with the Baerveldt 350-mm2 glaucoma implant and associated
extraocular muscle imbalance. Ophthalmology 1993;100:914–918.
113. Snir M, Gilad E, Ben-Sira I. An unusual extraocular muscle anomaly
in a patient with Crouzon’s disease. Br J Ophthalmol 1982;66(4):253–
257.
114. Stager DR, Weakley DR, Stager D. Anterior transposition of the inferior oblique: anatomic assessment of the neurovascular bundle. Arch
Ophthalmol 1992;110:360–362.
115. Strachan IM, Brown BH. Electromyography of extraocular muscles
in Duane’s syndrome. Br J Ophthalmol 1972;56:594–599.
116. Taylor R, Whale K, Raines M. The heavy eye phenomenon: orthoptic and ophthalmic characteristics. Ger J Ophthalmol 1995;4:252–
255.
386
handbook of pediatric strabismus and amblyopia
117. Theodossiadis G, Nikolakis S, Apostolopoulos M. Immediate postoperative muscular disturbance in retinal detachment surgery. Mod
Probl Ophthalmol 1979;20:367–372.
118. Traboulsi EI, Lee BA, Mousawi A, Khamis AR, Engle EC. Evidence
of genetic heterogeneity in autosomal recessive congenital fibrosis
of the extraocular muscles. Am J Ophthalmol 2000;129(5):658–
662.
119. Trotter WL, Kaw P, Meyer DR, Simon JW. Treatment of subtotal
medial rectus myectomy complicating functional endoscopic sinus
surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(4):250–
253.
120. Vargas FR, Schuler-Faccini L, Brunoni D, et al. Prenatal exposure to
misoprostol and vascular disruption defects: a case-control study.
Am J Med Genet 2000;95(4):302–306.
121. Varn MM, Saunders RA, Wilson ME. Combined bilateral superior
rectus muscle recession and inferior oblique muscle weakening for
dissociated vertical deviation. J Am Assoc Pediatr Ophthalmol Strabismus 1997;1(3):134–137.
122. von Noorden GK, Jenkins RH, Rosenbaum AL. Horizontal transposition of the vertical rectus muscles for treatment of ocular torticollis. J Pediatr Ophthalmol Strabismus 1993;30(1):8–14.
123. Wang SM, Zwaan J, Mullaney PB, et al. Congenital fibrosis of the
extraocular muscles type 2, an inherited exotropic strabismus fixus,
maps to distal 11q13. Am J Hum Genet 1998;63(2):517–525.
124. Wilcox LM, Gittinger JW, Breinen GM. Congenital adduction palsy
and synergistic divergence. Am J Ophthalmol 1981;91:1–7.
125. Wilder WM, Williams JP, Hupp SL. Computerized tomographic findings in two cases of congenital fibrosis syndrome. Comput Med
Imaging Graph 1991;15(5):361–363.
126. Wilson WB, Prochoda M. Radiotherapy for thyroid orbitopathy.
Effects on extraocular muscle balance. Arch Ophthalmol 1995;
113(11):1420–1425.
127. Wilson ME, Parks MM. Primary inferior oblique overaction in
congenital esotropia: accommodative esotropia and intermittent
exotropia. Ophthalmology 1989;96:952–957.
128. Wilson ME, Saunders RA, Berland JE. Dissociated horizontal deviation and accommodative esotropia: treatment options when an esoand an exodeviation co-exist. J Pediatr Ophthalmol Strabismus 1995;
32(4):228–230.
129. Wilson ME, McClatchey SK. Dissociated horizontal deviation. J
Pediatr Ophthalmol Strabismus 1991;28(2):90–95.
130. Wolff SM. Strabismus after retinal detachment surgery. Trans Am
Ophthalmol Soc 1983;81:182–192.
131. Wolff JE, Koutsandreou AC. Analysis of psychomotor development
of ten children with Möbius syndrome. Dev Med Child Neurol 2001;
43(1):71–72.
132. Wright KW. Late overcorrection after inferior rectus recession. Ophthalmology 1996;103(9):1503–1507.
chapter
10:
complex strabismus
387
133. Wright KW, Liu GY, Murphree AL, et al. Double elevator palsy,
ptosis and jaw-winking. Am Orthopt J 1989;39:143–150.
134. Wright KW. The fat adherence syndrome and strabismus after retina
surgery. Ophthalmology 1986;93:411–415.
135. Wright KW. Color atlas of strabismus surgery: strategies and techniques. Torrance, CA: Wright, 2000.
136. Wright KW, Edelman PM, McVey JH, Terry A, Lin M. High-grade
stereoacuity after early surgery for congenital esotropia. Arch Ophthalmol 1994;112:913–919.
137. Wright KW. Clinical optokinetic nystagmus asymmetry in treated
esotropes. J Pediatr Ophthalmol Strabismus 1996;33(3):153–155.
138. Yamada M, Shinoda K, Hatakeyama A, Nishina S, Mashima Y. Fat
adherence syndrome after retinal surgery treated with amniotic
membrane transplantation. Am J Ophthalmol 2001;132(2):280–282.
11
Strabismus Surgery
Kenneth W. Wright and Pauline Hong
T
his chapter discusses various strabismus surgery procedures
and how they work. When a muscle contracts, it produces
a force that rotates the globe. The rotational force that moves
an eye is directly proportional to the length of the moment arm
(m) (Fig. 11-1A) and the force of the muscle contraction (F) (Fig.
11-1B).
Rotational force m F
where m moment arm and F muscle force.
Strabismus surgery corrects ocular misalignment by at least
four different mechanisms: slackening a muscle (i.e., recession),
tightening a muscle (i.e., resection or plication), reducing the
length of the moment arm (i.e., Faden), or changing the vector
of the muscle force by moving the muscle’s insertion site (i.e.,
transposition).
MUSCLE RECESSION
A muscle recession moves the muscle insertion closer to the
muscle’s origin (Fig. 11-2), creating muscle slack. This muscle
slack reduces muscle strength per Starling’s length–tension
curve but does not significantly change the moment arm when
the eye is in primary position (Fig. 11-3). The arc of contact of
the rectus muscles wrapping around the globe to insert anterior
to the equator of the eye allows for large recessions of the rectus
muscles without significantly changing the moment arm. Figure
11-3 shows a 7.0-mm recession of the medial and lateral rectus
muscles. Note there is no change in the moment arm with these
large recessions. Thus, the effect of a recession on eye position
is determined by the amount of muscle slack created.1a The
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FIGURE 11-1A,B. (A) Diagram of the horizontal rectus muscles shows
the relationship of the moment arm (m) to the muscle axis and center of
rotation. The moment arm intersects the center of rotation and is perpendicular to the muscle axis. The longer the moment arm, the greater
the rotational force. (B) Starling’s length–tension curve. The relationship
of a muscle’s force is proportional to the tension on the muscle. More
tension on a muscle increases muscle force and slackening a muscle
reduces its force. Note that the relationship is exponential, not linear:
toward the end of the curve, a small amount of slackening produces a disproportionately large amount of muscle weakening.
A
B
C
FIGURE 11-2A–C. Drawing of rectus muscle recession (shaded muscle).
The effect of the recession is greatest when the eye rotates toward the
recessed muscle. (A) The eye rotates toward the recessed muscle, causing
the recessed muscle to tighten, therefore reducing muscle slack. (B) A
rectus muscle resection resulting in muscle slack. (C) The eye rotates
toward the recessed muscle, and the muscle and the muscle slack
increase.
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5.5
7.0
m
MR
FIGURE 11-3. Medial rectus muscle recession. Diagram shows normal
insertion at 5.5 mm posterior to the limbus and a 7.0-mm medial rectus
recession. In primary position, the moment arm (m) has not changed, so
the effect of the recession is to create muscle slack rather than to change
the moment arm.
amount of muscle slack is most accurately determined by measuring the recession from the muscle insertion.8
Note the exponential character of the length–tension curve,
as there is a precipitous loss of muscle force at the end of the
curve when muscle slack is increased (see Fig. 11-1B); this is why
even small, inadvertent inaccuracies of large recessions (6–
7 mm) can cause dramatic changes in muscle force and result
in an unfavorable outcome. Technical mistakes, such as allowing central muscle sag and not properly securing the muscle,
can lead to large overcorrections. For example, each 0.5 mm of
bilateral medial rectus recessions up to a recession of 5.5 mm
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will correct approximately 5 prism diopters (PD) of esotropia.
However, for recessions greater than 5.5 mm, each additional
0.5 mm of recession results in 10 prism diopters of correction
(see chart on inside cover). Thus, an overrecession of only
1.0 mm on a planned 6.0-mm bilateral medial rectus recession
would result in a 20-prism diopter overcorrection. Figure 11-4
shows the proper rectus muscle recession, with the muscle well
secured and no central muscle sag. The best way to prevent
central muscle sag is to broadly splay the new insertion so it is
approximately the same width as the original insertion.
A rectus muscle recession has its greatest effect in the field
of action of the muscle. Figure 11-2 shows that muscle slack
increases when the eye rotates toward the recessed muscle, thus
reducing the rotational force on gaze toward the recessed
muscle. In contrast, eye rotation away from the recessed muscle
causes muscle slack to be reduced. In addition, on rotation away
from the recessed muscle, the recessed muscle is inhibited
(Sherrington’s law), minimizing the effect of the recession in
this gaze. For example, a right medial rectus recession will
produce an incomitant strabismus, with an exodeviation in
primary position and a larger exodeviation in leftgaze with very
little exodeviation in rightgaze. Induced incomitance can correct
incomitant strabismus. If a patient has a small esotropia in
primary position and a large esotropia in leftgaze, a right medial
rectus recession would reduce the incomitance. Comitant strabismus, on the other hand, is best treated with bilateral symmetrical surgery.
Recessions are routinely performed on rectus muscles but
can also be performed on oblique muscles. Inferior oblique
muscle recession is a popular procedure for weakening the inferior oblique muscle. Recession of the superior oblique tendon
has also been described. It not only slackens the superior oblique
tendon but also changes the function of the muscle. A recession
of the superior oblique tendon collapses the normally broad
insertion and moves the new insertion nasal and anterior to the
globe’s equator. This alteration changes the function of the superior oblique muscle and can result in unpredictable outcomes,
including postoperative limitation of depression. A more controlled way of slackening the superior oblique tendon without
changing the functional mechanics of the tendon insertion is
a tendon-lengthening procedure, such as the Wright silicone
tendon expander.
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FIGURE 11-4A,B. (A) Drawing of rectus muscle recession with the
muscle secured to sclera at the recession point posterior to the original
insertion. Note that the new insertion is almost as wide as the original
scleral insertion, and the new insertion is parallel to the original insertion. There is no central muscle sag. (B) Companion photograph shows a
rectus muscle recession with no central sag because the new insertion is
splayed as wide as the original insertion.
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Hang-Back Technique
A hang-back recession suspends the muscle back, posterior to
the scleral insertion, with a suture (Fig. 11-5). This technique
has the advantage of excellent exposure and relatively easy
needle passes through the thick anterior sclera. On the other
hand, hang-back recessions are potentially less accurate than a
fixed recession. Small to medium-sized hang-back recessions of
3 to 6 mm tend to result in overcorrections because they have
inherent central muscle sag (Fig. 11.5). On the other hand, large
hang-back recessions, over 6 mm, tend to produce undercorrections because an otherwise normal muscle will not consistently
retract more than 6 to 7 mm posterior to the insertion. The
surgeon experienced with adjustable suture surgery knows it is
difficult to recess a rectus muscle more than 6 mm using an
adjustable hang-back suture. Large hang-back recessions are
FIGURE 11-5. Hang-back recession. The suture is passed through sclera
at the original insertion and the muscle is suspended posteriorly to
achieve the recession. Inset: Note the caliper is measuring the planned
recession; however, the muscle is overrecessed because of central sag.
Central sag occurs because the new insertion is lax and not splayed as
widely as the original insertion.
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possible if the muscle is tight and contracted, as in the case of
thyroid-associated strabismus, congenital fibrosis syndrome, or
a slipped muscle. Indications for hang-back recessions include a
recession over a retinal buckle, recession over an area of scleral
ectasia, or large recessions, of a tight contracted muscle, if
posterior exposure is difficult. However, for routine strabismus
surgery, the author (K.W.W.) prefers the fixed recession so the
muscle is secured at the desired recession point.
Adjustable Suture Technique
Adjustable suture techniques allow movement of the muscle
position after surgery when the patient is fully awake and the
anesthesia has dissipated (Fig. 11-6). Unlike fixed sutures,
the adjustable suture technique allows for fine-tuning of ocular
alignment in the immediate postoperative period. The adjustable suture procedure is usually performed on recessions in
two stages: in the first stage, surgery is performed under either
local or general anesthesia, and the muscle is placed on a suture
in such a way that the muscle position can be adjusted later.
The second stage, or adjustment phase, is performed when the
patient is fully awake or after the local anesthetic has worn off
(5 h for lidocaine) and the muscle function has returned to
normal. In this phase, the muscle is adjusted to properly align
the eyes and then permanently tied in place. The adjustment
procedure must be performed within 24 to 48 h after the initial
surgery while the muscle is still freely mobile. Later adjustments have not been recommended because the muscle rapidly
adheres to the globe. However, successful in-office reoperation
within the first week of surgery has been described.5 The muscle
is sutured like a hang-back recession, but the suture is tied in
a bowknot or secured by a sliding noose so the position of the
FIGURE 11-6A–C. (A) Bow tie adjustable suture technique. After the
sutures have been passed through the scleral insertion, they are tied
together in a single-loop bow tie. This bow tie can be untied postoperatively to adjust the muscle. (B) Noose adjustable suture. Sutures suspend
the muscle posteriorly, and a noose around the sutures slides up and down
to secure the muscle at the desired position. The ocular alignment is finetuned with the patient awake. The muscle placement is finalized by tying
off the pole sutures, then trimming all loose sutures. (C) Companion
photograph of (B) shows adjustable suture through fornix, with scleral
traction suture holding the conjunctiva superiorly and exposing the
adjustable suture.
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muscle can be easily changed (Fig. 11-6A–C). Adjustable sutures
have limitations similar to hang-back recessions, with the
maximum recession approximately 6 to 7 mm. Central sag
occurs but, because the muscle position can be changed after
surgery, this is usually not an issue. Plan on a slight overcorrection, as advancing an over-recessed muscle is easier than
trying to increase the recession, especially if the recession is
greater than 6 to 7 mm.
The most important indication for an adjustable suture is
complicated strabismus, including paralytic strabismus, largeangle strabismus, reoperations, and thyroid myopathy. In these
situations, the standard tables for surgical measurements do not
apply, and results with the fixed-suture technique are unpredictable. In addition to the more complicated strabismus cases,
many surgeons routinely use adjustable sutures on most cooperative adult patients, even those undergoing uncomplicated,
horizontal surgery. Adjustable sutures are usually used with
recession procedures, as adjustable tightening procedures are difficult to perform.
Patient selection is crucial for successful implementation of
the adjustable suture technique. The adjustment procedure is
somewhat uncomfortable and can evoke substantial anxiety.
There is no specific age limitation for the use of adjustable
sutures, but patients younger than 15 years of age are often too
anxious about medical procedures. Unless a child is exceptionally calm and cooperative, adjustable sutures should be limited
to cooperative adult patients. Strong sedatives before adjustment
should be avoided because sedation influences eye position. The
patient should wear full optical correction when ocular alignment is being assessed during the adjustment procedure to
ensure proper image clarity and control of accommodation.
MUSCLE SHORTENING PROCEDURES
Muscle shortening procedures include muscle resections, tucks,
and plications. These procedures tighten the muscle, but they
do not actually strengthen the muscle. For the most part, they
correct strabismus by creating a tight muscle that acts like a
leash or tether. These procedures produce incomitance, as the
tightened muscle restricts rotation away from the shortened
muscle (Fig. 11-7). For example, a right medial rectus shortening procedure limits abduction of the right eye and creates an
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A
B
C
FIGURE 11-7A–C. Effect of a rectus muscle resection (shaded muscle).
The resection has its greatest effect on gaze away from the resection. (A)
The muscle tightens on gaze away from the resected muscle. (B) A
resected rectus muscle. (C) The muscle slackens on gaze to the resected
muscle.
esodeviation shift that increases in rightgaze. Right medial
rectus tightening would be indicated to correct an incomitant
exotropia that is greater in rightgaze. Note that tightening the
medial rectus muscle does not strengthen adduction but instead
limits abduction. Bilateral medial rectus resections limit divergence and induce an esodeviation greater for distance fixation;
therefore, it is not the answer for convergence insufficiency.
Resection
A muscle resection consists of tightening a muscle by removing
the anterior part of the muscle and reattaching the shortened
muscle to the original insertion site. The muscle resection is the
most popular tightening procedure and is performed on rectus
muscles.
Tuck
A muscle tuck shortens the muscle by folding the muscle and
suturing the folded muscle to muscle. The muscle tuck has, for
the most part, fallen out of favor partially because the muscleto-muscle suturing does not hold well and tends to become
cheese-wire loose over time. A superior oblique tendon tuck or
plication, however, is used for some cases of superior oblique
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palsy, either as a full-tendon plication or plication of the anterior tendon fibers (i.e., Harada–Ito procedure).
Wright Plication
The author (K.W.W.) developed a rectus muscle plication procedure that tightens the muscle by folding the muscle and suturing it to sclera (Fig. 11-8).14,18 With the plication, the muscle is
sutured to the scleral insertion, in contrast to a tuck, where
muscle is sutured to muscle. The muscle–scleral attachment of
A
B
FIGURE 11-8A,B. Wright rectus muscle plication. (A) The muscle is
secured with the suture placed posterior to the insertion at the desired
plication point (usually 6 mm or less). Once the posterior muscle is
secured, the suture ends are passed through the scleral insertion. The
drawing shows the suture secured to the posterior muscle and the doublearmed needles being passed at the scleral insertion. (B) The plication is
completed with the posterior muscle advanced to the insertion. There is
a small roll of redundant tendon that will flatten and disappear 3 to 4
weeks after surgery.
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the plication is more secure than the muscle-to-muscle union
of a tuck.
The plication can be used in place of a standard resection.
Because there is a fold of tendon associated with the plication,
a small lump is present immediately after surgery but disappears
within 3 to 4 weeks. Important advantages of the plication procedure over resection include reversibility. A plication can be
removed by simply cutting and removing the suture within 2
days of the surgery, before the muscle heals to sclera. Another
advantage is safety against a lost muscle. Because the muscle is
not disinserted, there is little risk of a lost muscle. The plication procedure also preserves the anterior ciliary vessels and
reduces the risk of anterior segment ischemia. These advantages
have made the Wright plication popular for small or mediumsized rectus muscle tightening surgeries.
RECESSION AND RESECTION
Resections (or plications) of rectus muscles can be teamed with
a recession of the antagonist muscle same eye to correct strabismus. This monocular surgery is called a recession–resection,
or “R & R,” procedure. The effect of the recession–resection of
agonist and antagonist induces incomitance and limits ocular
rotation in one direction. For example, a right lateral rectus
muscle recession reduces ocular rotation to the right, and a
resection of the right medial rectus muscle also restricts rotation to the right. Limited rotations after an R & R procedure may
improve over several months to years, but some residual incomitance often persists. Because the R & R procedure induces
incomitance, it can be used to treat incomitant strabismus. It is
also useful in treating sensory strabismus, allowing monocular
surgery to be performed only on the amblyopic eye and sparing
surgery to the good eye.
FADEN
The Faden procedure is performed by suturing the rectus muscle
to sclera, 12 to 14 mm posterior to the rectus muscle insertion.
This technique pins the rectus muscle to the sclera so, when the
eye rotates toward the fadened muscle, the arc of contact cannot
unravel. As a result, the moment arm shortens, thus reducing
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the rotational force. The Faden, however, does not significantly
change the moment arm when the eye is in primary position,
and it has no effect when the eye is turned away from the muscle
with the Faden (Fig. 11-9). Thus, a Faden reduces ocular rotational force when the eye rotates toward the fadened muscle and
is used to correct incomitant strabismus.
The weakening effect of the Faden operation by itself is relatively small, so the fadened muscle is usually also recessed as
part of the Faden procedure. The Faden operation works best on
the medial rectus muscle because the medial rectus muscle has
the shortest arc of contact (approximately 6 mm), and a 12- to
14-mm Faden significantly changes its arc of contact. Alternately, a Faden of the lateral rectus muscle has little effect
because the arc of contact is 10 mm, and pinning the muscle at
12 mm does not significantly change this naturally long arc of
contact. For the most part, the Faden operation is indicated to
correct incomitant esotropia by enhancing the effect of a medial
rectus recession, such as in the case of sixth nerve paresis or
high AC/A esotropia. The following case is an example where a
A
FIGURE 11-9A. Faden of rectus muscle. (A) In primary position, the
Faden does not significantly change the moment arm (m).
FIGURE 11-9B–C. (B) Ocular rotation toward the Faden results in shortening of the moment arm (m) as the muscle is pinned to sclera. (C) On
rotation away from the Faden, the moment arm (m) is normal and the
faden has no significant effect. Thus, the Faden weakens the muscle on
rotation toward the fadened muscle.
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Faden and recession of the right medial rectus muscle is indicated. One may rightfully argue, however, that a large (5-mm)
right medial rectus muscle recession would also work without
the difficulty of performing the Faden. As you will see, there is
often more than one way to approach a strabismus.
Rightgaze
Orthotropia
Primary position
Leftgaze
E4
ET 10
ET, esotropia. Surgery: recess the right medial rectus muscle 3 mm with a Faden.
Sixth Nerve Paresis
An example where the Faden may be effective is a partial sixth
nerve paresis and good lateral rectus function. The standard
surgery has historically been a recession of the medial rectus
muscle and resection of the lateral rectus muscle of the paretic
eye, which helps correct the esodeviation in primary position
but does not address the large esotropia that occurs with gaze to
the side of the paretic lateral rectus muscle. Incomitance can be
improved with a recession and a Faden operation of the contralateral medial rectus muscle. A Faden to the contralateral
medial rectus muscle helps correct the esotropia that increases
in the side of the paretic lateral rectus muscle by decreasing the
rotational force of the yoke medial rectus, thus matching the
paretic lateral rectus muscle. Matching yoke muscles only
works if there is good lateral rectus function with no more than
1 limitation of abduction.
High AC/A Ratio Esotropia
Theoretically, the Faden operation reduces convergence at near,
thus lowering the AC/A ratio. Experience with this procedure
indicates that most patients still require a bifocal add to obtain
fusion at near. Augmented bilateral medial rectus recessions
probably work just as well.7 The use of a Faden operation with
a medial rectus recession in high AC/A ratio esotropia patients
remains controversial.
MUSCLE TRANSPOSITION PROCEDURES
Transposition surgery is based on changing the location of the
muscle insertion so the muscle pulls the eye in a different direction (i.e., changes the vector of force). Transposition surgeries
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can be used to treat A- and V-patterns, small vertical tropias,
rectus muscle paresis, and torsion.
Horizontal Muscle Transposition for Aand V-Patterns
See Chapter 9: A- and V-Patterns and Oblique Dysfunction.
Transposition for Small Vertical Deviations
Transposition surgery can correct small vertical deviations by
vertically offsetting the horizontal rectus muscles. A patient
with an esotropia and a small right hypertropia, for example, can
be corrected by a recession–resection procedure of the right eye
with inferior infraplacement of the horizontal rectus muscles.
By transposing the horizontal rectus muscles inferiorly, they act
to pull the eye down, thus correcting the hypertropia. Each horizontal muscle is recessed or resected as specified by the magnitude of the horizontal deviation.
There is approximately 1 prism diopter of improvement in
the vertical deviation per 1 mm of displacement; this is true
when two muscles in the same eye are transposed in the same
direction. Vertical muscle displacements as large as 6 to 7 mm
may be readily performed with this technique. It is most useful
when the surgeon is performing monocular recession–resection
surgery in which both muscles are moved in the same direction
(Fig. 11-10). This surgery, however, is not effective if restriction
is present (e.g., thyroid orbitopathy).
FIGURE 11-10. Full-tendon-width inferior transposition of both horizontal rectus muscles. The muscle on the left has been resected and
infraplaced; the muscle on the right has been recessed and infraplaced.
This technique would be used with a recession/resection procedure to
correct a hypertropia and horizontal strabismus.
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Transposition Procedures for Rectus Muscle Palsy
Three transposition procedures used to correct severe rectus
muscle palsies are described here: Knapp, Jensen, and
Hummelsheim. In a right lateral rectus palsy, there is limited
abduction and a large esotropia that increases in rightgaze. If
there is less than 50% lateral rectus function, the treatment
should be a lateral transposition of all or part of the superior and
inferior rectus muscles. Because the vertical muscles do not contract on attempted abduction, the amount of abduction would
relate to the elasticity or tonic contraction of the transposed
muscles, rather than the active contraction of the transposed
muscles.
KNAPP PROCEDURE
A full-tendon transfer, or Knapp procedure, was originally
described for the management of double elevator palsy. This procedure, however, can also be used for a sixth nerve palsy. The
key for successful surgery is symmetrical transposition to avoid
induced vertical or horizontal deviations. A large posterior dissection to free the muscle of the intermuscular septum and
check ligaments is necessary to mobilize the muscle for the
tendon transfer (Fig. 11-11).
JENSEN PROCEDURE
The Jensen procedure is a split-tendon transfer with the adjacent
muscle tied together but not disinserted (Fig. 11-12). This procedure has the advantage of leaving the anterior ciliary arteries
intact, diminishing the risk of anterior segment ischemia. Even
with the Jensen procedure, however, some vascular compromise
occurs, and anterior segment ischemia has been associated with
this procedure.
HUMMELSHEIM PROCEDURE
The Hummelsheim procedure is a split-tendon transposition
technique designed to preserve anterior ciliary artery perfusion.
Half of each of the two rectus muscles adjacent to the weak
muscle is mobilized. The halves are then transposed and
inserted at the insertion of the weak or lost muscle (Fig. 11-13).
In contrast to the Jensen procedure, the Hummelsheim procedure can be used for a lost muscle, as it does not require the
FIGURE 11-11. Knapp procedure. The
medial rectus (MR) and lateral rectus (LR)
muscles are transposed superiorly to the
insertion of the superior rectus (SR) muscle.
FIGURE 11-12. Jensen procedure. Nonabsorbable sutures tie muscle
halves from adjacent muscles. The final result shows the tendon unions
of superior rectus to lateral rectus and inferior rectus to lateral rectus
muscles. The posterior location of the union is important, and sutures
should be at least 12 mm posterior to the insertions. Anterior union
sutures will reduce the effect of the transposition.
FIGURE 11-13. Hummelsheim procedure. Half of each of the superior
and inferior rectus muscles is transposed to the lateral rectus insertion.
Note that the transposed muscle halves touch the lateral rectus insertion,
and the muscles are sutured together 3 mm posterior to the insertion
(Foster modification).
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presence of the weak muscle. The Hummelsheim procedure is
the author’s procedure of choice for a muscle palsy.
MODIFICATION
OF THE
HUMMELSHEIM
Two modifications of the Hummelsheim procedure, which
increase the effect of the transposition, are described here.
Augmented Hummelsheim Brooks of Augusta, Georgia,
has augmented the Hummelsheim by resecting 4 to 6 mm of the
transposed rectus muscle halves. Resecting some of the transposed muscle halves tighten the transposition, increasing the
leash effect.
Muscle Union Modification (Foster modification)
Increased effect of the Hummelsheim has been suggested if the
transposed muscle is sutured to the paretic muscle. The transposed and paretic muscles are sutured together and then to
sclera, 4 mm posterior the insertion.
Complications of Transposition Surgery
Transposition procedures for rectus muscle palsies can induce
unwanted deviations if there is asymmetrical muscle placement.
In split-tendon procedures, it is important to split and transpose
the muscle equally to prevent inadvertent deviations.
Anterior segment ischemia is always an important consideration. Split-tendon procedures such as the Jensen and Hummelsheim lessen the risks, but even these procedures have been
associated with anterior segment ischemia. The best strategy is
to preserve as many anterior ciliary arteries as possible. A limbal
conjunctival incision disrupts local vessels and may increase the
risk of anterior segment ischemia, suggesting that a fornix incision may be preferable.
Rectus Muscle Transposition for Torsion
Torsional strabismus can be improved by moving vertical rectus
muscles nasally or temporally. Nasal placement of the superior
rectus causes extorsion (corrects intorsion) whereas temporal
placement causes intorsion (corrects extorsion). The opposite
is true for the inferior rectus muscle, with nasal transposition
induces intorsion (corrects extorsion) and temporal transposition induces extorsion (corrects intorsion). Transposition of a
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tendon width (approximately 7 mm) will induce about 4° to 5°
of torsion. Most of the torsional effect is seen in the field of
action of the transposed muscle. If the superior rectus muscle is
nasally transposed 7 mm and the inferior rectus muscle temporally transposed 7 mm, a total of 8° to 10° of extorsion would be
induced, thus correcting 8° to 10° of intorsion. Horizontal rectus
muscle transposition will also produce some torsional changes,
but less than vertical rectus muscle transpositions. Supraplacement of the medial rectus muscle induces intorsion; infraplacement induces extorsion. The opposite is true for the lateral
rectus muscle. It is unusual for a vertical transposition of a horizontal muscle to induce significant torsion. Most cases of torsional strabismus are caused by oblique dysfunction and are best
treated with oblique muscle surgery to correct the torsion. For
example, extorsion associated with bilateral superior oblique
paresis is usually best handled with a bilateral Harada–Ito procedure, not a rectus muscle transposition.
INFERIOR OBLIQUE MUSCLE
WEAKENING PROCEDURES
Surgical management of inferior oblique muscle overaction is
based on weakening or changing the function of the inferior
oblique muscle. Techniques include myectomy, recession, and
anterior transposition. Inferior oblique myotomy is not effective
because the cut ends of the muscle inevitably reunite or scar to
sclera; this causes residual inferior oblique overaction and an
unacceptably high reoperation rate. Myectomy weakens the
inferior oblique, as removing a portion of muscle reduces the
chance of local reattachment. A very large myectomy with surgical transection of the neurovascular bundle virtually eliminates inferior oblique overaction and is termed inferior oblique
extirpation–denervation. Extirpation–denervation may be indicated for severe residual inferior oblique overaction after previous inferior oblique surgery. An inferior oblique recession places
the insertion closer to the origin and induces muscle slack, thus
reducing muscle tension (Fig. 11-14). Apt1 and Elliot4 were the
first to describe the inferior oblique anterior transposition. It is
similar to a recession, but the inferior oblique muscle insertion
is moved anterior to its origin, thus changing the function of the
inferior oblique muscle from an elevator to more of a depressor
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FIGURE 11-14. Inferior oblique recession. The muscle is reattached along
the path of the inferior oblique, but closer to its origin, thus slackening
the muscle.
(Fig. 11-15). The more anterior the placement of the inferior
oblique muscle insertion, the more the muscle becomes a
depressor. This procedure has been shown to be very effective
for treating both primary inferior oblique overaction and inferior
oblique overaction secondary to superior oblique palsy.6
One possible complication of the anteriorization procedure
is postoperative limited elevation. Limited elevation usually
occurs from three possible mechanisms: (1) the new insertion is
too anterior (i.e., anterior to the inferior rectus insertion); (2)
resection of too much muscle (3 mm) at the time of securing
FIGURE 11-15. Inferior oblique anterior transposition. The diagram
shows placement of the inferior oblique (IO) muscle in relationship to
the inferior rectus (IR) insertion. The inferior oblique muscle is placed
1 mm posterior to the inferior rectus insertion. Note that the posterior
inferior oblique muscle fibers are placed posterior to the anterior fibers
and parallel to the inferior rectus muscle (no J-deformity).
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and disinserting the inferior oblique muscle; and (3) anterior
placement of the posterior fibers of the inferior oblique muscle.
Stager described this last mechanism as a common cause for
limited elevation after the anterior transposition procedure. The
posterior fibers of the inferior oblique muscle are important,
as the neurovascular bundle of the muscle inserts into these
muscle fibers. Because the neurovascular bundle is inelastic,
large anteriorizations of the posterior muscle fibers will create
a J-deformity of the muscle, with the neurovascular bundle
tethering the inferior oblique muscle and limiting elevation of
the eye (Fig. 11-16).12a
To prevent postoperative limitation of elevation, the author
(K.W.W.) recommends:
FIGURE 11-16. Full anteriorization of the inferior oblique muscle including the posterior fibers with J-deformity. Anteriorization of the posterior
fibers creates the J-deformity, as the neurofibrovascular bundle tethers the
posterior muscle fibers; this can limit elevation of the eye. Because of this
complication, the author (K.W.W.) does not perform the “J” deformity
anteriorization, except if performed bilaterally for severe dissociated vertical deviation (DVD) and inferior oblique overaction.
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handbook of pediatric strabismus and amblyopia
1. Keep the new insertion at or behind the inferior rectus
insertion.
2. Secure the muscle close to its insertion to avoid resecting too much muscle (this would shorten the muscle).
3. Avoid the “J” deformity by keeping the posterior muscle
fibers posterior to the anterior muscle fibers and posterior to the
inferior rectus muscle insertion by at least 3 mm.8,14 The full
anteriorization with a “J” deformity has been used for the treatment of bilateral dissociated vertical deviation (DVD) with inferior oblique overaction. If performed, the full anteriorization
with “J” deformity should be performed bilaterally to avoid
asymmetrical elevation of the eyes.
Graded Recession–Anteriorization
The author (K.W.W.) has reported on a graded recession–
anteriorization approach for the management of inferior oblique
overaction.8,14 This procedure tailors the amount of anteriorization according to the amount of inferior oblique overaction. The
basis of the graded anteriorization procedure is that the more
anterior the inferior oblique insertion, the greater the weakening affect. Table 11-1 lists the inferior oblique placement for a
specific amount of inferior oblique overaction and represents
only a guideline for the management of inferior oblique overaction. The final surgical decision must be based on a combination of factors, including the amount of V-pattern and the
presence of a vertical deviation in primary position. Asymmetrical graded anteriorization is indicated if a hypertropia is
present in primary position; otherwise, consider symmetrical
surgery. More anteriorization of the inferior oblique should be
done on the side of the hyperdeviation. A full anteriorization
(without J-deformity) on the side of the hypertropia and 4 mm
anteriorization on the opposite side will correct approximately
6 prism diopters (PD) of hypertropia. In the case of a unilateral
TABLE 11-1. Graded Recession–Anteriorization of Inferior Oblique
Muscle.
Overaction
Inferior oblique placement
1
2
3
4
4 mm posterior and 2 mm lateral to inferior rectus (IR) insertion
3 mm posterior to IR insertion
1–2 mm posterior to IR insertion
At the IR insertion
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inferior oblique overaction (e.g., associated with congenital
superior oblique paresis), a unilateral anteriorization of 1 mm
will correct approximately 8 to 12 PD of hypertropia.
COMPLICATIONS
Limited elevation after inferior oblique anteriorization has been
discussed previously, but another problem of inferior oblique
surgery is persistence or recurrence of the overaction. A
common cause of residual overaction is incomplete isolation
of the inferior oblique muscle, leaving posterior fibers intact.
It is important to explore posteriorly along the globe for bridging muscle fibers that would indicate missed inferior oblique
fibers.
Weakening procedures of the inferior oblique muscle for
primary overaction only rarely produce a postoperative torsional
diplopia. Even so, an adult patient may complain of a transient
excyclodiplopia after weakening of the inferior oblique muscle.
An important anatomic consideration is the proximity of
the inferior oblique muscle insertion to the macula. A misadventure with a stray needle in this area can cause the loss of
central vision. Another consideration is the course of the inferior temporal vortex vein, which lies underneath the inferior
oblique and can be inadvertently traumatized during surgery.
The proximity of extraconal fat to the inferior oblique muscle
is also an important concern, and fat adherence syndrome
should be kept in mind; this may occur when the inferior
oblique muscle is approached blindly and posterior Tenon’s
capsule is violated. Other possible complications of inferior
oblique surgery include orbital hemorrhage, pupillary dilation,
endophthalmitis, and inadvertent surgery or damage to the
lateral rectus muscle.11 Paramount in avoiding these complications is the clear and direct visualization of the inferior oblique
muscle during its isolation. Blind hooking procedures must be
avoided. Meticulous surgical dissection and hemostasis are the
key to proper exposure and visualization of the anatomy.
SUPERIOR OBLIQUE MUSCLE
TIGHTENING PROCEDURES
The superior oblique tendon can be functionally divided into
the anterior third, responsible for intorsion, and posterior twothirds, responsible for depression and abduction (Fig. 11-17).
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handbook of pediatric strabismus and amblyopia
FIGURE 11-17. Diagram of superior oblique tendon insertion. The anterior fibers are responsible for intorsion and the posterior fibers for abduction and depression.
Tightening the anterior fibers will induce intorsion without too
much change in the depression and abduction functions of the
superior oblique muscle; this is the basis of the Harada–Ito procedure, which is used for correcting extorsion. Tightening the
full tendon is termed a superior oblique tuck or plication.
Harada–Ito Procedure
The Harada–Ito procedure is commonly used to treat extorsion
associated with a partially recovered acquired superior oblique
palsy, where the residual strabismus is only extorsion. Tightening the entire tendon will result in depression and abduction and
often produces an iatrogenic Brown’s syndrome. Therefore, the
Harada–Ito has the advantage of correcting extorsion without
causing a significant Brown’s syndrome. Figure 11-18 shows
two techniques for tightening the anterior fibers: Figure 11-18A
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shows the disinsertion technique and Figure 11-18B shows a
classic Harada–Ito procedure. The author prefers the classic
Harada–Ito procedure because it is reversible by simply cutting
the pullover suture.
Full-Tendon Tuck or Plication
The superior oblique tuck or plication is reserved for severe
bilateral superior oblique underaction where the tendon is lax,
usually associated with either a congenital or trauma-induced
palsy. A full-tendon tuck or plication tightens both anterior and
posterior fibers and enhances all three functions of the superior
oblique muscle (Fig. 11-19). Tightening of the entire superior
oblique tendon may improve its function slightly, but this will
consistently cause an iatrogenic Brown’s syndrome or limited
elevation in adduction. Care must be taken to balance the superior oblique tightening against the induced Brown’s syndrome
by performing intraoperative forced ductions of the superior
oblique after tucking or plicating. The amount of tuck or plication should be readjusted appropriately. This author (K.W.W.)
A
B
FIGURE 11-18A,B. Harada–Ito procedure: (A) With the disinsertion technique, the anterior fibers of the superior oblique tendon are sutured, then
disinserted, and moved anteriorly and laterally to be secured to sclera at
a point 8 mm posterior to the superior border of the lateral rectus insertion. Lateralizing the anterior fibers intorts the eye, thus correcting extorsion. (B) In the classic Harada–Ito procedure, the anterior superior oblique
tendon fibers are looped with a suture and displaced laterally without
disinsertion. The anterior superior oblique tendon fibers are sutured to
sclera 8 mm posterior to the superior border of the lateral rectus muscle.
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handbook of pediatric strabismus and amblyopia
FIGURE 11-19. Superior rectus tuck or plication. Inset—Sutures are
placed in the nasal tendon, then passed through sclera at the insertion.
The tendon is pulled to plicate the tendon.
reserves the superior oblique plication for those rare cases of
congenital superior palsy caused by a lax superior oblique
tendon, or severe bilateral traumatic superior oblique palsy with
severe extorsion and esotropia in downgaze. Bilateral medial
rectus recessions with infraplacement usually accompany the
plications.
SUPERIOR OBLIQUE MUSCLE
WEAKENING PROCEDURES
Superior oblique weakening procedures are used in the management of superior oblique overaction and Brown’s syndrome.19
Various weakening procedures have been described including
tenotomy, tenectomy, recession, split-tendon lengthening, and
Z-lengthening of the superior oblique tendon. The split-tendon
lengthening procedure works well but is difficult to perform and
has the disadvantage of causing tendon scarring. The superior
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oblique recession also creates a new insertion site nasal to the
superior rectus muscle, changing the superior oblique muscle
function from a depressor to an elevator. Limited depression has
been described as a complication of the recession procedure. The
superior oblique tenotomy has been popular, but it is an uncontrolled procedure and the tendon ends can separate, resulting in
palsy, or grow back together, causing an undercorrection. A
suture bridge has been used to prevent separation of the tendon
ends, but the suture can act as scaffolding, allowing the tendon
to grow back together. The author (K.W.W.) has developed a procedure to lengthen the superior oblique tendon, the Wright superior oblique tendon expander. This procedure has been very
effective in treating superior oblique overaction and especially
treating Brown’s syndrome.17
Superior Oblique Tenotomy
Superior oblique tenotomy should be performed nasal to the
superior rectus muscle (Fig. 11-20). Guyton’s exaggerated forced
ductions should be performed after tenotomy to verify that the
full tendon was found and tenotomized. Temporal tenotomies
usually have minimal effect, as the superior oblique tendon is
sandwiched between the superior rectus and the sclera. When the
FIGURE 11-20. Berk superior oblique tenotomy performed at the nasal
tendon. (From Ref. 2, with permission.)
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temporal fibers are removed from the sclera, they do not retract
but, instead, scar down to sclera under the superior rectus
muscle. Another disadvantage of the temporal tenotomy is that
the tendon is extremely splayed out at its insertion; thus, it is
difficult to hook and tenotomize all the posterior superior
oblique fibers.
The preferred procedure, developed by Marshall Parks, is
to perform the superior oblique tenotomy nasal to the superior
rectus muscle through a temporal conjunctival incision. By
placing the conjunctival incision temporal to the superior rectus
muscle and reflecting the incision nasally, the surgeon can keep
the nasal intermuscular septum intact and minimize
scleral–tendon scarring. Intact nasal intermuscular septum is
vital to maintain the anatomic relationship of the superior
oblique tendon and helps reduce the incidence of postoperative
superior oblique palsy.
Wright Superior Oblique Tendon Expander
This procedure controls the separation of the ends of the tendon,
allowing quantification of tendon separation.16 A segment of a
silicone 240 retinal band is inserted between the cut ends of the
superior oblique tendon (Fig. 11-21). The length of silicone is
determined by the degree of superior oblique overaction, as well
as the amount of A-pattern and downshoot. The maximum
length of silicone is 7 mm, but most significant Brown’s syndromes can be surgically managed with a segment of 5 to
6 mm.17 Perform the superior oblique expander through a temporal conjunctival incision, even though the silicone is placed
in the nasal tendon. By placing the conjunctival incision temporal to the superior rectus muscle, then reflecting the incision
nasally, the surgeon can keep the nasal superior oblique tendon
capsule floor and intermuscular septum intact and prevent adhesion of the silicone implant to sclera. This maneuver is analogous to cataract surgery and placing an intraocular lens (IOL) in
the capsular bag. An intact nasal tendon capsule floor is important to maintain the anatomic relationships of the superior
FIGURE 11-21A,B. Wright superior oblique tendon expander. (A) A
segment of 240 silicone retinal band is sutured between the cut ends of
the superior oblique tendon. (B) The silicone segment elongates the
tendon.
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handbook of pediatric strabismus and amblyopia
oblique tendon insertion and not create a new insertion site
nasal to the superior rectus muscle. Scarring of the silicone to
nasal sclera or the nasal aspect of the superior rectus muscle can
cause limitation of depression postoperatively.
SLIPPED OR LOST RECTUS MUSCLE
An important complication of strabismus surgery is a slipped or
lost muscle. The medial rectus muscle is the muscle most commonly lost or slipped after strabismus surgery and is the most
difficult to retrieve, as there are no fascial connections to oblique
muscles that keep the muscle from retracting posteriorly. In contrast, the inferior, superior, and the lateral recti have check ligaments that connect to adjacent oblique muscles.
A slipped rectus muscle occurs when a muscle retracts posterior to the intended recession or resection point but there is
some tissue still attached to the intended scleral insertion. A
slipped muscle after strabismus surgery is caused by inadvertently suturing the muscle capsule or anterior Tenon’s capsule
instead of true muscle tendon. Anterior Tenon’s capsule and
muscle capsule are then secured to sclera, so the muscle slips
posteriorly while a “pseudotendon” of connective tissue
remains attached to sclera.
A lost muscle occurs when the muscle retracts posteriorly
and there is no connection of the muscle to sclera. Orbital
trauma or hemorrhage can also result in a lost or damaged
muscle.3 Typical signs of a slipped or lost muscle include
decreased muscle function with limited ductions and lid fissure
widening in the field of action of the lost muscle. On occasion,
the presentation may be subtle, with slight limitation of ductions as the only finding. The key observation is an incomitant
deviation with underaction of the slipped muscle. Initial eye
alignment during the first postoperative week may be fairly good
in primary position, with only a mild limitation of ductions.
Over several weeks to months, however, ductions become progressively more limited. This progression probably represents
muscle slippage in addition to secondary contracture of the
antagonist muscle against a weakened slipped muscle.
Management of a slipped or lost muscle is to find the muscle
and surgically advance it to anterior sclera if possible. Fullthickness locking bites through muscle fibers must be obtained,
because partial-thickness locking bites may result in slippage of
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the posterior tendon fibers. If a lost muscle cannot be retrieved,
then a transposition procedure, such as the Hummelsheim,
should be performed.
STRETCHED INSERTION SCAR
In contrast to a slipped or lost muscle that results in an immediate overcorrection, there are many cases where an overcorrection occurs 4 to 6 weeks, and some-times years, after muscle
surgery (Fig. 11-22). When this overcorrection is associated
with minimal underaction of the operated muscle, consider a
stretched or elongated scar, with the operated muscle migrating
posteriorly. Late overcorrection is particularly common after
inferior rectus recession for a hypotropia associated with thyroid
disease, as it occurs in approximately 50% of cases.12 There has
been much speculation about the cause for this late overcorrection,15 but work by Ludwig probably provides the best explanation.9,10 This theory states that the new insertion scar of the
muscle to sclera stretches after the suture dissolves. The 6-0
vicryl suture used by most ophthalmologists lasts about 3 to 6
weeks, thus explaining the timing of the overcorrection. In this
author’s (K.W.W.) experience, the use of a nonabsorbable suture
reduces the problem of late overcorrection of the inferior rectus
muscle. Any rectus muscle can have a stretched scar and a late
overcorrection including, in order of frequency, inferior rectus,
medial rectus, and superior rectus muscles. The likelihood of
stretched scar formation may be inversely related to the length
of the muscle’s arc of contact.4
BOTULINUM NEUROTOXIN
Botulinum is a cholinergic blocking agent. Blockage in a muscle
occurs by binding sodium at the myoneural junction, causing
the loss of acetylcholine activity that paralyzes the muscle.
Minimal diffusion occurs through the nerve or the muscle
because there is tight binding within the muscle. Injection of
botulinum toxin into a rectus muscle results in paralysis that
occurs after 24 to 48 h and lasts from 3 to 6 months.
The most common strabismus indication for use of botulinum is sixth nerve palsy. The treatment is to inject the ipsi-
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handbook of pediatric strabismus and amblyopia
FIGURE 11-22A,B. Late overcorrection (4 weeks after strabismus
surgery) after a left inferior rectus recession for thyroid-related, tight inferior rectus muscle. The left inferior rectus muscle was found to be posterior, caused by a stretched scar. (A) Note the left hypertropia and lower
lid retraction. (B) Limited depression, left eye.
lateral medial rectus muscle (antagonist of the paretic lateral
rectus muscle). The induced weakness of the medial rectus
muscle from botulinum injection balances forces against the
weak lateral rectus muscle (weakness with weakness), which
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theoretically allows the paretic muscle to regain its strength
without secondary contracture of the antagonist. The use of botulinum is controversial, as studies have not shown an improvement in recovery rates for sixth nerve palsy (see Chapter 10).
Botulinum has also been used for comitant strabismus. The
rationale for using botulinum toxin in nonparalytic strabismus
is twofold: to weaken and lengthen the injected muscle and to
induce a mild secondary contracture in the injected muscle’s
antagonist. Botulinum causes secondary muscle contracture by
paralyzing the injected muscle, producing a large consecutive
deviation in the opposite direction; this causes shortening and
contracture of the antagonist to the injected muscle, theoretically leading to a permanent correction of the strabismus even
after the botulinum wears off. In infantile strabismus, it is theorized that the overacting muscle can be injected before the
development of contracture. Because of the temporary large
overcorrection associated with the initial paralysis and the need
for multiple injections to correct strabismus, strabismus surgery
is usually preferred for the treatment of comitant strabismus.
References
1. Apt L, Call NB. Inferior oblique muscle recession. Am J Ophthalmol
1978;95:95–100.
1a. Beisner DH. Reduction of ocular torque by medial rectus recession.
Arch Ophthalmol 1971;85:13.
2. Berk RN. Tenotomy of the superior oblique for hypertropia. Arch
Ophthalmol 1947;38:605.
3. Cates CA, et al. Slipped medial rectus muscle secondary to orbital
hemorrhage following strabismus surgery. J Pediatr Ophthalmol Strabismus 2000;37:361–362.
4. Chatzistefanou KI, et al. Magnetic resonance imaging of the arc of
contact of extraocular muscles: implications regarding the incidence
of slipped muscles. J Am Assoc Pediatr Ophthalmol Strabismus 2000;
4:84–93.
4a. Elliot L, Nankin J. Anterior transposition of the inferior oblique. J
Pediatr Ophthalmol Strabismus 1981;18:35.
5. Eustis HS, Leoni R. Early reoperation after vertical rectus muscle
surgery. J Am Assoc Pediatr Ophthalmol Strabismus 2001;5:217–220.
6. Guemes A, Wright KW. Effect of graded anterior transposition of the
inferior oblique muscle on versions and vertical deviation in primary
position. J Am Assoc Pediatr Ophthalmol Strabismus 1998;2;201–
206.
7. Kushner BJ. Fifteen-year outcome of surgery for the near angle in
patients with accommodative esotropia and a high accommodative
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convergence to accommodation ratio. Arch Ophthalmol 2001;119:
1150–1153.
8. Kushner BJ, et al. Should recessions of the medial recti be graded
from the limbus or the insertion? Arch Ophthalmol 1989;107:1755–
1758.
9. Ludwig IH. Scar remodeling after strabismus surgery. Trans Am Ophthalmol Soc 1999;97:583–651.
10. Ludwig IH, Chow AY. Scar remodeling after strabismus surgery. J Am
Assoc Pediatr Ophthalmol Strabismus 2000;4:326–333.
10a. Mims JL, Wood RC. Bilateral anterior transposition of the inferior
obliques. Arch Ophthalmol 1989;107:41.
11. Recchia FM, et al. Endophthalmitis after pediatric strabismus
surgery. Arch Ophthalmol 2000;118:939–944.
12. Sprunger DT, Helveston EM. Progressive overcorrection after inferior rectus recession. J Pediatr Ophthalmol Strabismus 1993;30:145–
148.
12a. Stager DR. The neurofibrovascular bundle of the inferior oblique
muscle as its ancillary origin. Trans Am Ophthalmol Soc 1996;94:
1073–1094.
13. Wright KW. Brown’s syndrome: Diagnosis and management. Trans
Am Ophthalmol Soc 1999;XCVII:1023–1109.
14. Wright KW. Color atlas of ophthalmic surgery: strabismus. Philadelphia: Lippincott, 1991:173–193.
15. Wright KW. Late overcorrection after inferior rectus recession. Ophthalmology 1996;103:1503–1507.
16. Wright KW. Superior oblique silicone expander for Brown’s syndrome
and superior oblique overaction. J Pediatr Ophthalmol Strabismus
1991;28(2):101–107.
17. Wright KW. Surgical procedure for lengthening the superior oblique
tendon. Investig Ophthalmol Vis Sci 1989;30(suppl):377.
18. Wright KW, Lanier AB. Effect of a modified rectus tuck on anterior
segment circulation in monkeys. J Pediatr Ophthalmol Strabismus
1991;28:77–81.
19. Wright KW, Min BM, Park C. Comparison of superior oblique tendon
expander to superior oblique tenotomy for the management of superior oblique overaction and Brown’s syndrome. J Pediatr Ophthalmol
Strabismus 1992;29(2):92–97; discussion 98–99.
12
Ocular Motility Disorders
Mitra Maybodi, Richard W. Hertle, and
Brian N. Bachynski
N
ormal individuals and most patients with common concomitant childhood strabismus have full ocular rotations
(versions and ductions). This chapter is devoted to some of the
more frequently encountered childhood disorders of the central
and peripheral nervous systems, neuromuscular junction, and
extraocular muscles that appear clinically to have incomitant
ocular misalignments.
Analysis of ocular alignment, versions, ductions, forced ductions, and generated force allows the examiner to sort the causes
of these limited eye movements into three general categories:
(1) neuromuscular dysfunction, (2) restriction of the globe by
orbital tissues, and (3) combined neuromuscular dysfunction and
restriction (Fig. 12-1). Diagnosis in children is especially challenging because it is rarely possible to clinically test the force
generated by extraocular muscle action. A general anesthetic is
routinely required to perform forced ductions. It may therefore
be necessary to base diagnostic and therapeutic decisions on
incomplete clinical information, and the clinician must rely on
familiarity with the epidemiologic and clinical characteristics of
each disorder.
DISORDERS OF THE CENTRAL AND
PERIPHERAL NERVOUS SYSTEMS
Eye movement disorders arising from disturbance of the normal
neurophysiology may be classified as supranuclear, internuclear,
or infranuclear.
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handbook of pediatric strabismus and amblyopia
FIGURE 12-1. Clinical evaluation of range of eye movements. Versions
and cover test measurements allow the examiner to decide whether the
eye movements are normal (no limitation) or limited. Forced duction
testing is used to differentiate a restriction (positive resistance to movement of the globe) from a “paresis” (no resistance to movement of the
globe).
Supranuclear Eye Movements
Cranial nerves III, IV, and VI serve together with the extraocular muscles as a final mechanism that executes all eye movements. Supranuclear pathways initiate, control, and coordinate
various types of eye movements. Several types of eye movements are briefly mentioned here (Table 12-1), but a detailed and
lucid synthesis of current concepts of the neural control of eye
movements can be found in many other sources.288
PHYSIOLOGY AND CLINICAL ASSESSMENT
The vestibular apparatus drives reflex eye movements, which
allow us to keep images of the world steady on the retinas as we
move our heads during various activities. The eyes move in the
opposite direction to the movement of the head so that they
remain in a steady position in space. The semicircular canals are
the end organs that provide the innervation to the vestibular
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nuclei, which in turn drive cranial nerves III, IV, and VI to compensate for rotations of the head. In contrast, the otoliths
respond to linear accelerations of the head and to gravity when
the head is tilted. You can easily test the effectiveness of input
from the semicircular canals by testing the vestibulo-ocular
reflex (VOR). First, hold your head still and observe an object
such as your index finger as you move it side to side at about 1
to 3 cycles/s. The image is a blur. However, if you hold your
finger steady and rotate your head from side to side at the same
frequency, you are able to maintain a clear image.
Several forms of saccades, fast eye movements, can be
clinically observed. Voluntary saccades may be predictive, in
anticipation of a target appearing in a specific location;
command-generated, in response to a command such as “look
to the right”; memory-guided; or antisaccades, in which a
reflexive saccade to an abruptly appearing peripheral target is
suppressed and, instead, a voluntary saccade is generated in the
equidistant but opposite direction. Involuntary saccades consist
of the fast phase of nystagmus due to vestibular and optokinetic
stimuli; spontaneous saccades, providing repetitive scanning of
the environment, although also occurring in the dark and in
severely visually impaired children; and reflex saccades, occurring involuntarily in response to new visual, auditory, olfactory,
or tactile cues, suppressable by antisaccades.83
TABLE 12-1. Types of Eye Movements.
Type of eye
movement
Function
Stimulus
Clinical tests
Vestibular
Maintain steady
fixation during
head rotation
Head rotation
Fixate on object while
moving head; calorics
Saccades
Rapid refixation
to eccentric
stimuli
Eccentric retinal
image
Voluntary movement
between two objects;
fast phases of OKN or
vestibular nystagmus
Smooth
pursuit
Keep moving
object on fovea
Retinal image slip
Voluntarily follow a
moving target; OKN
slow phases
Vergence
Disconjugate, slow
movement to
maintain
binocular vision
Binasal or
bitemporal
disparity;
retinal blur
Fusional amplitudes; near
point of convergence
OKN, optokinetic nystagmus.
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The pathway of saccades originates in the visual cortex and
projects through the anterior limb of the internal capsule,
through the diencephalon. It then divides into dorsal and ventral
pathways, the dorsal limb going to the superior colliculi, and the
ventral limb (which contains the ocular motor pathways for horizontal and vertical eye movements) to the pons and midbrain.
The superior colliculus acts as an important relay for some of
these projections (Fig. 12-2).
The neurons responsible for generating the burst, or discharge, for saccades are classified as excitatory burst neurons
(EBN); inhibitory burst neurons (IBN) function to silence activ-
FIGURE 12-2. The superior colliculi are a pair of ovoid masses composed
of alternating layers of gray and white matter; they are centers for visual
reflexes and ocular movements, and their connections to other structures
in the brain and spinal cord are varied and complex. Some of these other
structures include the retina, visual and nonvisual cerebral cortex, inferior colliculus, paramedian pontine reticular formation, thalamus, basal
ganglia, and spinal cord ventral gray horn. The fibers of the medial longitudinal fasciculus form a fringe on its ventrolateral side: 1, superior
(cranial) colliculus; 2, brachium of superior (cranial) colliculus; 3, medial
geniculate nucleus; 4, brachium of inferior (caudal) colliculus; 5, central
gray substance; 6, cerebral aqueduct; 7, visceral nucleus of oculomotor
nerve (Edinger–Westphal nucleus); 8, nucleus of oculomotor nerve; 9,
medial lemniscus; 10, central tegmental tract; 11, medial longitudinal fasciculus; 12, red nucleus; 13, fibers of oculomotor nerve; 14, substantia
nigra; 15, basis pedunculi.
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FIGURE 12-3. Brainstem structures controlling eye movements.
Parasagittal section of the cerebrum and brainstem shows areas of the
ocular motor nuclei and brainstem structures involved with internuclear
and supranuclear pathways. PC, posterior commissure; SC, superior colliculus; IC, inferior colliculus; Pi, pineal; riMLF, rostral interstitial
nucleus of the medial longitudinal fasciculus; INC, interstitial nucleus of
Cajal; CN III, IV, VI, cranial nerve III, IV, VI; MLF, medial longitudinal
fasciculus; PPRF, paramedian pontine reticular formation; VN, vestibular nuclei.
ity in the antagonist muscle during the saccade. In the brainstem, the rostral interstitial nucleus of the medial longitudinal
fasciculus (riMLF) and the pontine paramedian reticular formation (PPRF) provide the saccadic velocity commands, by generating the “pulse of innervation” immediately before the eye
movement, to cranial nerves III, IV, and VI. Horizontal saccades
are generated by EBN in the PPRF, which is found just ventral
and lateral to the MLF in the pons (Figs. 12-3, 12-4, 12-5), and
by IBN in the nucleus paragigantocellularis dorsalis just caudal
to the abducens nucleus in the dorsomedial portion of the rostral
medulla. Vertical and torsional components of saccades are generated by EBN and IBN in the riMLF, located in the midbrain.
Following a saccade, a “step of innervation” occurs during
which a higher level of tonic innervation to ocular motoneurons
keeps the eye in its new position, against orbital elastic forces
FIGURE 12-4. Transverse section of caudal pons. AbdNu, abducens
nucleus; AbdNr, abducens nerve; AMV, anterior medullary velum; CSp,
corticospinal tract; FacG, internal genu of facial nerve; FacNr, facial
nerve; FacNu, facial nucleus; LVN, lateral vestibular nucleus; ML, medial
lemniscus; MLF, medial longitudinal fasciculus; MVN, medial vestibular
nucleus; RetF, paramedian pontine reticular formation; SCP, superior
cerebellar peduncle; SpTNu, spinal trigeminal nucleus; SpTT, spinal
trigeminal tract; SVN, superior vestibular nucleus. (Adapted from Haines
DE. Neuroanatomy: an atlas of structures, sections, and systems.
Baltimore: Urban & Schwarzenberg, 1983, with permission.)
FIGURE 12-5. Schematic of brainstem pathways coordinating horizontal
saccades. The PPRF, after receiving input from the ipsilateral cortical
centers and superior colliculus, stimulates two sets of neurons in the
abducens nucleus: (1) those that send axons to innervate the ipsilateral
lateral rectus and (2) those whose axons join the MLF and subsequently
activate the medial rectus subnuclei of the contralateral third nerve.
PPRF, paramedian pontine reticular formation; VI, sixth cranial nerve
nucleus; III, third cranial nerve nucleus.
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that would restore the eye to an anatomically “neutral” position.
For horizontal saccades, the step of innervation comes from the
neural integrator (see following), primarily from the nucleus
prepositus–medial vestibular nucleus complex. The eye is held
steady at the end of vertical and torsional saccades by the step of
innervation provided from the interstitial nucleus of Cajal in the
midbrain.288
In addition to burst neurons, omnipause neurons, located
in the nucleus raphe interpositus in the midline of the pons,
between the rootlets of the abducens nerves, are essential for
normal saccadic activity. Continuous discharge from omnipause
neurons inhibits burst neurons, and this discharge only ceases
immediately before and during saccades.288
Other burst neurons termed long-lead burst neurons (LLBN)
have also been identified that discharge 40 ms before saccades,
whereas the previously mentioned burst cells discharge 12 ms
before saccades. Some LLBN lie in the midbrain, receiving
projections from the superior colliculus and projecting to the
pontine EBN, medullary IBN, and omnipause neurons. Other
LLBN lie in the nucleus reticularis tegmenti pontis (NRTP), projecting mainly to the cerebellum but also to the PPRF. It appears
that LLBN receiving input from the superior colliculus may play
a crucial role in transforming spatially coded to temporally
coded commands, whereas other LLBN may synchronize the
onset and end of saccades.288
If an abnormality of saccadic eye movements is suspected,
the quick phases of vestibular and optokinetic nystagmus (OKN)
can be easily evaluated in infants and young children. To
produce and observe vestibular nystagmus, hold the infant at
arm’s length, maintain eye contact, and spin first in one direction and then in the other. An OKN response can be elicited in
the usual manner by passing a repetitive stimulus, such as
stripes or an OKN drum, in front of the baby first in one direction and then in another. In addition, reflex saccades are induced
in many young patients when toys or other interesting stimuli
are introduced into the visual field. Older children are asked to
fixate alternately upon two targets so that the examiner can
closely observe the saccades for promptness of initiation, speed,
and accuracy.
Smooth pursuit permits us to maintain a steady image of a
moving object on our foveas and thereby to track moving targets
with clear vision. The pathways for smooth pursuit have not
been fully elucidated, but it appears that frontal and extrastriate
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visual cortex transmits information about the motion of both
the target and the eyes to the dorsolateral pontine nuclei
(DLPN). This complex signal travels from the DLPN to the cerebellum (paraflocculus, flocculus, and dorsal vermis), and from
the cerebellum via the vestibular and fastigial nuclei to its final
destination, the ocular motor nerve nuclei III, IV, and VI. Unilateral lesions in the cortex and cerebellum affect smooth
pursuit toward the side of the lesion.
Vergences are eye movements that turn the eyes in opposite
directions so that images of objects will fall on corresponding
retinal points. Two major stimuli are known to elicit vergences:
(1) retinal disparity, which leads to fusional vergences, and (2)
retinal blur, which evokes accommodative vergences. Convergence of the eyes, accommodation of the lens, and constriction
of the pupils occur simultaneously when there is a shift in fixation from distance to near; together, these actions constitute the
near triad.
The neural substrate for vergence lies in the mesencephalic
reticular formation, dorsolateral to the oculomotor nucleus.
Neurons in this region discharge in relation to vergence angle
(vergence tonic cells), to vergence velocity (vergence burst cells),
or to both vergence angle and velocity (vergence burst-tonic
cells). Although most of these neurons also discharge with
accommodation, experiments have shown that some do remain
predominantly related to vergence.32 Like versional movements,
a velocity-to-position integration of vergence signals is necessary. The nucleus reticularis tegmenti pontis (NRTP) has been
shown to be important in the neural integration, that is,
velocity-to-position integration, of vergence signals. The cells in
NRTP that mediate the near response appear to be separate from
the cells which mediate the far response. Lesions of NRTP cause
inability to hold a steady vergence angle. NRTP has reciprocal
connection with the cerebellum (nucleus interpositus) and
receives descending projections from several cortical and subcortical structures.32,288
The cerebellum plays an important role in eye movements.
Together with several brainstem structures, including the nucleus
prepositus and the medial vestibular nucleus, it appears to convert
velocity signals to position signals for all conjugate eye movements through mathematical integration. Because of this, all the
structures involved in this process are often referred to as the
neural integrator. The role of the neural integrator in horizontal
saccades was mentioned earlier.
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To test the neural integrator clinically, observe fixation, fixation in eccentric gaze, saccades, pursuit, and OKN and also test
for rebound nystagmus and VOR cancellation. To examine for
rebound nystagmus, first ask the patient to fixate on a target
from the primary position, then to refixate on an eccentric target
for 30 s, and finally to return to the original primary position
target. A patient with rebound nystagmus will show transient
nystagmus with the slow phases toward the previous gaze position. To evaluate a child’s VOR cancellation, it is easiest to place
your hand on top of the patient’s head to control both the head
and a fixation target that will extend in front of the child’s visual
axis. You may use a Prince rule with a picture attached. Ask the
child to fixate on the target as you passively rotate both the head
and the target side to side. If the child is unable to cancel the
VOR, you will observe nystagmus instead of the steady fixation
expected in normal subjects.
Patients with faulty neural integration may show gazeevoked nystagmus, impaired smooth pursuit, inability to cancel
the vestibulo-ocular reflex during fixation, saccadic dysmetria,
defective OKN response, or rebound nystagmus. Most frequently, gaze-evoked nystagmus is seen in conjunction with use
of anticonvulsants or sedatives. However, because 60% to 70%
of brain tumors in children are subtentorial, acquired eye movement abnormalities suggesting defective neural integration,
whether isolated or associated with other neurological deficits,
alert the examiner to investigate for a serious central nervous
system abnormality.39,110,132 Structural anomalies affecting the
brainstem and cerebellum, for example, the Arnold–Chiari malformation, as well as metabolic, vascular, and neurodegenerative
disorders, may also produce abnormalities of the neural
integrator.
Reflex eye movements such as the vestibulo-ocular reflex
and Bell’s phenomenon are easy to elicit clinically and are very
useful for gross localization of neural lesions. When both saccades and smooth pursuit in a certain direction are limited, the
examiner tries to stimulate eye movements in that same direction with a doll’s head (oculocephalic) maneuver, spin test, or
forced lid closure. If any of the reflex eye movements are intact,
the appropriate cranial nerve(s) and extraocular muscles(s) are
clearly functioning, and the defect is necessarily supranuclear.
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DISORDERS OF SUPRANUCLEAR EYE MOVEMENTS
We focus here on a few disorders in which the normal physiology of supranuclear eye movements, such as saccade, smooth
pursuit, vergence, and gaze holding, is disturbed.
SACCADE INITIATION FAILURE/OCULAR
MOTOR APRAXIA
The term saccade initiation failure or ocular motor apraxia is
used to specify impaired voluntary saccades and variable deficit
of fast-phase saccades during vestibular or optokinetic nystagmus.380,447 Congenital ocular motor apraxia, first described by
Cogan,96 is a congenital disorder that is characterized by defective horizontal saccades, but it does not represent a true apraxia
because reflex saccades may also be impaired. The incidence of
this condition is dependent upon the underlying etiology.
Etiology Patients with congenital saccade initiation failure
show abnormal initiation and decreased amplitude of voluntary
saccades; saccadic velocities in these patients are normal, and
fast phases of nystagmus of large amplitude can occasionally be
generated, suggesting that the brainstem burst neurons that generate saccades are intact.288 Acquired saccade initiation failure
may be caused by any number of conditions, as listed in Table 122. Some of these patients with the acquired type, such as those
with Gaucher’s disease (type 1 and some type 3 patients), do have
abnormal saccadic velocities.83,194 Although the exact cause or
localization of the defect in congenital saccade initiation failure
has not been determined, there is strong evidence suggesting
that most disorders that cause saccade initiation failure can be
localized subtentorially, particularly to the cerebellar
vermis.83,137,196,235,429,450
Clinical Features The clinical presentation varies with the
age and motor development of the child. Infants and children
with poor head control who are affected are commonly thought
to be cortically blind because the expected visually driven eye
movements are not observed.164,417 In such an infant, demonstration of vertical saccades, vertical pursuit, OKN response in
any direction, or normal acuity on visual evoked response
testing suggests the diagnosis of saccade initiation failure.
However, lack of appropriate response to such testing does not
exclude this diagnosis. Another suggestive clinical sign in young
infants is an intermittent tonic deviation of the eyes in the direc-
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TABLE 12-2. Congenital and Acquired Saccade Initiation Failure
(SIF) (Ocular Motor Apraxia).
Classification by cause
Idiopathic195
Perinatal problems
Specific etiologies
Cerebral palsy195; hypoxia195; hydrocephalus195;
seizures195
Congenital
malformations
Agenesis of corpus callosum450; fourth ventricle dilation
and vermis hypoplasia450; Joubert’s syndrome282,332;
macrocerebellum63; dysgenesis of cerebellar vermis
and midbrain523; Dandy–Walker malformation195;
immature development of putamen472; heterotropia of
gray matter472; porencephalic cyst195,515; hamartoma
near foramen of Munro515; macrocephaly195;
microcephaly147,195; posterior fossa cysts375;
chondrodystrophic dwarfism and hydrocephalus98;
encephalocele375; occipital meningocele11; COACH
syndrome162 (cerebellar vermis hypoplasia,
oligophrenia, congenital ataxia, coloboma, hepatic
fibrocirrhosis)
Neurodegenerative
conditions with
infantile onset of SIF
Infantile Gaucher’s disease (type 2, 3)85,100,507; Gaucher’s
disease type 256,497; Pelizaeus–Merbacher disease195;
Krabbe’s leukodystrophy195; proprionic academia195;
GM1 gangliosidosis195; infantile Refsum’s disease195; 4hydroxybutyric aciduria147,397
Neurodegenerative
conditions with
later onset of SIF
Ataxia telangectasia473,499,532; spinocerebellar
degenerations7,21,36,228,270,369,512; juvenile Gaucher’s
disease (type 3)194; Huntington’s disease31,471;
Hallervorden–Spatz disease17; Wilson’s disease265
Acquired disease
Postimmunization encephalopathy195,335; herpes
encephalitis195; posterior fossa tumors195,298,477,536,540
Other associations
Alagille’s syndrome12; Bardet–Biedl syndrome284; carotid
fibromuscular hypoplasia195; Cockayne’s syndrome147;
Cornelia de Lange syndrome195; juvenile
nephronophthisis129; Lowe’s syndrome181;
neurofibromatosis type 1168; orofacial digital
syndrome305; X-linked muscle atrophy with
congenital contractures524
Source: Adapted from Cassidy L, Taylor D, Harris C. Abnormal supranuclear eye movements in the
child: a practical guide to examination and interpretation. Surv Ophthalmol 2000;44:479–506, with
permission.83
tion of slow-phase vestibular or optokinetic nystagmus; in these
infants, fast-phase saccades may be impaired, again confounding
our definition of oculomotor apraxia.288
Natural History With time, often by 4 to 8 months of age,
the child develops a striking stereotypical “head-thrusting”
behavior to refixate. First, the eyelids blink (“synkinetic blink”)
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and the head begins to rotate toward the object of interest. Next,
the head continues to rotate past the intended target, allowing
the tonically deviated eyes, which are now in an extreme contraversive position, to come into alignment with the target.
Finally, as the eyes maintain fixation, the head rotates slowly
back so that the eyes are in primary position. This apparent use
of the VOR to refixate continues for several years, but with
increasing age, patients demonstrate less prominent head thrusting and may even be able to generate some saccades although
these are abnormal.97,542
In some infants, generalized hypotonia may be associated.
This hypotonia seems to be more pronounced in boys and
improves with increasing age. These babies later demonstrate
the motor delay, incoordination, and clumsiness that have been
noted in the literature.153,395
Clinical Assessment The parents of children are asked
about any associated developmental abnormality. A complete
ophthalmic examination is performed to rule out any strabismus or amblyopia, as strabismus has been reported in 22% of
these patients in one series.195 Vision, electroretinogram (ERG),
and visual evoked potential (VEP) are normal in the congenital
saccade initiation failure patients.164,451 Any coexistent abnormal
vision, nystagmus, or abnormal ERG or VEP suggests associated
disease.451 Neurological abnormalities or dysmorphic features
are further investigated by the appropriate subspecialists. A
brain MRI is necessary for any suspected neurological disorder,
to look for any midline malformation, particularly around the
fourth ventricle and cerebellar vermis.83
Systemic Associations Significant structural abnormalities of the central nervous system (CNS) may be associated, such
as lipoma477 or brainstem tumor.540 Joubert’s syndrome is associated with cerebellar hypoplasia and agenesis of the corpus
callosum.282 A neuroradiologic correlation has been made in
children with saccade initiation failure, in which 61% of 62
children had abnormal scans, primarily the brainstem and cerebellar vermis; however, significant abnormalities in the cerebral
cortex and basal ganglia were also found.450
Gaucher’s disease,185,197 ataxia telangiectasia7,473 and its variants, and Niemann–Pick variants100 may also present with the
inability to generate saccades as well as blinking and head
thrusting before refixation. Unlike congenital saccade initiation
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failure, these disorders generally involve vertical as well as horizontal saccades and, of course, eventually manifest systemic
signs.
Early-onset vertical saccade initiation failure has been
observed in children with lesions at the mesencephalic–
diencephalic junction, presumably infarcts resulting from perinatal hypoxia.135,219
Inheritance Occasional familial occurrence,196,345,387,398,501
increased frequency in males, and occurrence in monozygotic
twins67 suggest a genetic process in some cases. Association with
nephronophthisis has been described in two patients, each of
whom exhibited deletions on chromosome 2q13.55
Treatment No treatment is available for congenital
saccade initiation failure, but associated strabismus is treated
accordingly.
Prognosis The visual and clinical prognosis of those
patients with the congenital type is good. Many can adapt over
time to allow gaze shifts with less head thrusting and can even
generate some saccades, albeit still abnormal.97,542
INDUCED CONVERGENCE RETRACTION/PARINAUD
DORSAL MIDBRAIN SYNDROME
OR
Lesions of the posterior commissure in the dorsal rostral midbrain (see Fig. 12-2) may result from many disease processes and
can affect a variety of supranuclear mechanisms, including
those that control vertical gaze, eyelids, vergence, fixation, and
pupils. Other terms such as pretectal syndrome, Koerber–Salus–
Elschnig syndrome, Sylvian aqueduct syndrome, posterior commissural syndrome, and collicular plate syndrome all refer to
this condition.
Incidence A report of 206 patients with pretectal syndrome in one neurologist’s practice at a general hospital in
southern California indicated the incidence to be 2.3% of all
patients examined by this neurologist in an 18-year period.255 Of
these 206 patients, 71 exhibited induced convergence retraction.
Etiology and Systemic Associations The pretectum was
confirmed as the critical structure that is affected in this disorder, investigated clinicopathologically in humans91 and experimentally in monkeys.371,372 Also, isolated interruption of the
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TABLE 12-3. Causes of Childhood Dorsal Midbrain Syndrome.
Classification by cause
Specific etiologies
Tumor
Pineal germinoma, teratoma and glioma;
pineoblastoma; others386
Hydrocephalus
Aqueductal stenosis with secondary dilation of third
ventricle and aqueduct, or with secondary
suprapineal recess compressing posterior
commissure,89,366 commonly caused by
cysticercosis in endemic areas
Metabolic disease
Gaucher100,492; Tay–Sach; Niemann–Pick154;
kernicterus214; Wilson’s disease265; others
Midbrain/thalamic damage
Hemorrhage; infarction
Drugs
Barbiturates138; carbamazepine; neuroleptics
Miscellaneous
Benign transient vertical eye disturbance in infancy;
trauma; neurosurgery445; hypoxia; encephalitis;
tuberculoma; aneurysm102; multiple sclerosis
posterior commissure in humans produces the entire syndrome
of upward gaze palsy, pupillary light–near dissociation, lid
retraction, induced convergence retraction, skew deviation, and
upbeat nystagmus.251 Among the many underlying causes of this
condition are hydrocephalus, stroke, and pinealomas. Table 123 lists other reported etiologies and systemic associations.
Clinical Features and Assessment The constellation of
deficits are (1) vertical gaze palsy, (2) light–near dissociation of
the pupils, (3) eyelid retraction (Collier’s sign), (4) disturbance
of vergence, (5) fixation instability, and (6) skew deviation.
Limitation of upward saccades is the most reliable sign of
the convergence retraction. Upward pursuit, Bell’s phenomenon,
and the fast phases of vestibular and optokinetic nystagmus may
also be affected either at presentation or with progression of the
underlying process. It is rare for upgaze to be unaffected. Pathological lid retraction and lid lag are also common (Collier’s sign).
When the patient attempts upward saccades, a striking phenomenon, convergence and globe retraction, frequently occurs;
this is not true nystagmus, despite the common description of
this clinical finding as convergence-retraction nystagmus,
because there is no true slow phase. This action is best elicited
with down-moving OKN targets because each fast phase is
replaced by a convergence-retraction movement. Cocontraction
of the extraocular muscles has been documented during this
convergence-retraction jerk.161
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Unlike the pathways from upward saccades, the pathways
for downward saccades do not appear to pass through the posterior commissure (Figs. 12-3, 12-6). Perhaps because of this, disturbances of downgaze are not as predictable or uniform. Usually
down-going saccades and pursuit are present, but they may be
slow. Sometimes, especially in infants and children, there is a
tonic downward deviation of the eyes that has been designated
the “setting sun” sign, and down-beating nystagmus may also be
observed. The “setting sun” sign may also be seen in children
with hydrocephalus.
Convergence spasm may occur during horizontal saccades
and produce a “pseudoabducens palsy” because the abducting
eye moves more slowly than the adducting eye.113 This phenomenon can cause reading difficulties early in the course of
dorsal midbrain syndrome because it provides an obstacle to
refixation toward the beginning of a new line of text. Indeed,
older children may present with numerous pairs of corrective
FIGURE 12-6A,B. Schematic of brainstem pathways coordinating downward (A) and upward (B) saccades. (A) Downward saccades. The PPRF
activates neurons in the riMLF that send fibers caudally to synapse upon
the inferior rectus subnucleus of the ipsilateral third nerve and the contralateral superior oblique nucleus. Not shown in this diagram, fibers
from the contralateral PPRF carry corresponding signals simultaneously.
(B) Upward saccades. The PPRF activates neurons in the riMLF that send
fibers through the posterior commisure to the superior rectus subnucleus
of the contralateral third nerve and fibers to the inferior oblique subnucleus of the ipsilateral third nerve. Not shown in this diagram, fibers from
the contralateral PPRF carry corresponding signals simultaneously.
riMLF, rostral interstitial nucleus of the medial longitudinal fasciculus;
INC, interstitial nucleus of Cajal; III, third cranial nerve nucleus; IV,
fourth cranial nerve nucleus; PPRF, paramedian pontine reticular
formation.
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spectacles that have been prescribed due to their “vague” complaints about reading and other near work. In other patients
complaining of difficulties with near vision, convergence may
be paralyzed. “Tectal” pupils are usually large and react more
poorly to light than to near, and anisocoria is not uncommon.
All children with convergence retraction deserve thorough,
prompt neurological and neuroradiologic evaluation because
timely intervention may be decisive. The natural history of this
disorder is dependent on the underlying etiology.
Treatment The underlying medical cause requires investigation and primary treatment. Once the condition is stable for
a period of time, from 3 to 12 months, surgery has been performed with some success. In addition to treating the coexistent
diplopia from skew deviation or horizontal strabismus, which
may be surgically corrected, the anomalous head posture from
defective vertical gaze may also be treated by inferior rectus
recession or vertical transposition of horizontal recti during
simultaneous horizontal strabismus correction.74 Faden operation (posterior fixation suture, or retroequatorial myopexy) on
both medial recti to control convergence spasms and bilateral
superior rectus resection to alleviate the anomalous head
posture have also been reported.465
Prognosis The medical prognosis is dependent upon the
underlying etiology. In the aforementioned review of 206
patients, only 20 patients died: 11 of tumors, 7 after strokes, and
1 with transtentorial hernation with tuberculous abscess. The
good prognosis in this series may have been skewed by the preponderance of patients with cysticercal hydrocephalus.255
The prognosis of strabismus surgery in all eviating anomalous head posture and diplopia was good in all three patients in
one study after a minimum of 6 months follow-up.74 In another
report, head posture and ocular motility improved beyond expectation and remained satisfactory after a minimum of 1 year
follow-up.465
TRANSIENT VERTICAL GAZE DISTURBANCES
IN INFANCY
Vertical gaze abnormalities may be benign and transient in
infants. Four babies with episodic conjugate upgaze that became
less frequent over time have been described.6,113 During these
episodes, normal horizontal and vertical vestibulo-ocular
responses could be observed.
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Tonic downgaze has been observed in 5 of 242 consecutively
examined healthy newborn infants215 as well as in other
infants.113,285 Again, the eyes can easily be driven above the
primary position with the vestibulo-ocular reflex. Also, the eyes
show normal upward movements during sleep. In contrast,
infants with hydrocephalus who manifest the “setting sun” sign
do not elevate the eyes during sleep or with an oculocephalic
maneuver.
Premature infants with intraventricular hemorrhage may
also develop tonic downgaze, usually in association with a largeangle esotropia.480 These infants do not elevate the eyes with
vestibular stimulation. Upgaze often returns during the first 2
years of life, but the esotropia does not resolve when upgaze
returns.
DOUBLE ELEVATOR PALSY/MONOCULAR
ELEVATION DEFICIENCY
Monocular deficiency of elevation, that is, an apparent weakness
of both the superior rectus and inferior oblique muscles, has
been termed double elevator palsy or monocular elevation deficiency. This deficit may be caused by mechanical restriction of
the globe or neural dysfunction at the supranuclear, nuclear, or
infranuclear level. Congenital double elevator palsy of supranuclear origin is confirmed on clinical examination if the
affected eye elevates during Bell’s phenomenon or doll’s head
maneuver.44,52
SPASM
OF THE
NEAR REFLEX
Spasm of the near reflex, also referred to as convergence spasm,
is characterized by intermittent spasm of convergence, of
miosis, and of accommodation.95 Symptoms include headache,
photophobia, eyestrain, blurred vision, and diplopia. Patients
may appear to have bilateral sixth nerve palsies, but careful
observation will reveal miosis and high myopia (8–10 D) on
dry retinoscopy, accompanying the failure of abduction.172 This
key clinical clue prevents misdiagnosis and misdirected
testing.172,182,252,430
Most commonly, spasm of the near reflex is psychogenic,
and treatment may include simple reassurance, psychiatric
counseling, or cycloplegia with bifocals. However, a number of
cases of spasm of the near reflex associated with organic disease
have been reported.487 In a series of seven patients, two had
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posterior fossa abnormalities (cerebellar tumor, Arnold–Chiari
malformation), two had pituitary tumors, one had a vestibulopathy, and two had antecedent trauma.112 None of these patients
appeared to have a personality disorder, and none complained of
significant disability. Nevertheless, no clear causal relationship
or unified neuroanatomic localization has been established. It is
prudent to keep in mind that just as any patient with organic
disease may also have a functional disorder, disturbances that
are clearly functional do not exclude coexisting organic disease.
Internuclear Opththalmoplegia
In the absence of peripheral lesions such as myasthenia gravis,
failure of adduction combined with nystagmus of the contralateral abducting eye is termed internuclear ophthalmoplegia (INO) and localizes the lesion to the medial longitudinal
fasciculus (MLF) unequivocally.
ETIOLOGY
The abducens nucleus consists of two populations of neurons
that coordinate horizontal eye movements (see Fig. 12-5). Fibers
from one group form the sixth nerve itself and innervate the ipsilateral lateral rectus muscle; fibers from the second group join
the contralateral MLF and project to the subnucleus of the third
nerve, which supplies the contralateral medial rectus muscle. In
this way, the neurons of the sixth nerve nucleus yoke the lateral
rectus with the contralateral medial rectus.
CLINICAL FEATURES
Clearly, lesions of the abducens nucleus will cause an ipsilateral
conjugate gaze palsy. Lesions of the MLF between the midpons
and oculomotor nucleus, in turn, disconnect the ipsilateral
medial rectus subnucleus from the contralateral sixth nerve
nucleus and cause diminished adduction of the ipsilateral eye
on attempted versions (see Fig. 12-3). The signs of INO may be
accompanied by an ipsilateral hypertropia or skew deviation.
CLINICAL ASSESSMENT
A subtle adduction deficit is best appreciated when repetitive
saccades are attempted; the adducting eye will demonstrate a
slow, gliding, hypometric movement in conjunction with overshoot of the abducting eye. Usually, the ipsilateral eye can be
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adducted with convergence, but convergence will also be
impaired if the MLF lesion is rostral enough to involve the
medial rectus subnucleus.
SYSTEMIC ASSOCIATIONS
Similar to dorsal midbrain syndrome, INO is an anatomic rather
than etiological diagnosis. A host of structural, metabolic,
immunological, inflammatory, degenerative, and other processes can interfere with the function of the MLF and nearby
structures. In young adults, multiple sclerosis is by far the most
common cause of INO.342 Multiple sclerosis also underlies most
cases of bilateral INO. Although patients with bilateral INO generally remain orthotropic in primary position, they sometimes
exhibit an exotropia in the wall-eyed bilateral internuclear ophthalmoplegia (WEBINO) syndrome.311 Additional causes of INO
include Arnold–Chiari malformation,23,99,118,533 hydrocephalus,352
meningoencephalitis,64,226 brainstem or fourth ventricular
tumors,99,439,482,496 head trauma,49,84,254 metabolic disorders, drug
intoxications, paraneoplastic effect, carcinomatous meningitis,
and others. Peripheral processes, particularly myasthenia gravis
and Miller Fisher syndrome, may closely mimic INO and should
be considered in any patient with INO-like eye movements.
TREATMENT AND PROGNOSIS
The first goal is to treat the underlying etiology. For example,
steroid therapy is necessary in multiple sclerosis, and blood pressure management is required for a hypertensive stroke. After
this initial consideration, if the disorder persists and remains
stable for at least 6 months, the accompanying exotropia may
be corrected by surgery. In a series of three patients treated surgically for diplopia caused by bilateral INO (from brainstem vascular disease) with exotropia of 55 to 70 prism diopters, favorable
results were achieved by bilateral medial rectus resections and
bilateral lateral rectus recessions (with one lateral rectus on an
adjustable suture in each of the three).74 After a minimum of 6
months postoperative follow-up, all three patients achieved
excellent cosmesis. In one of the three patients, binocularity was
restored in the primary position, in the second diplopia was
eliminated in primary and downgaze, and in the third diplopia
was completely eliminated.
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Ocular Motor Cranial Nerve Palsies
The processes that produce ocular motor nerve palsies in infants
and children, as many neurological diseases in this age group,
are commonly diffuse.
GENERAL CLINICAL CONSIDERATIONS
Muscle paralysis is diagnosed by the inability of the eye to move
in the direction of action of the particular muscle voluntarily
and reflexively, tested by the doll’s head maneuver, spin test
(looking for vestibular nystagmus), or forced lid closure (looking
for Bell’s phenomenon). Paresis of a muscle may be detected on
testing of versions, at which time version in a particular direction may be limited but ductions may appear full. If the muscle
is totally paralyzed, the ductions will be limited as well; in this
case, if it is possible to perform a forced duction test, the test
would reveal no restriction in the direction of action of a paretic
muscle. However, after long-standing muscle paresis, the
muscle may become tightened, and forced duction testing in the
direction opposite to that of the muscle action would reveal
restriction.
A subtle paresis is best appreciated when repetitive saccades
are attempted; the eye will demonstrate a slow, gliding, hypometric movement in the direction of action of the particular
muscle(s), in conjunction with overshoot of the other eye in that
direction. The primary deviation, or the measured strabismus
when fixing with the normal eye, is smaller than the secondary
deviation, which is the strabismus measured when fixing with
the restricted or paretic eye.
Significant factors in evaluating a child with ocular motor
cranial palsies include (1) age of the child, (2) history of previous cranial nerve palsies or relevant systemic disease, (3) recent
history of febrile illness, immunization, trauma, or exposure to
toxins, (4) accompanying neurological symptoms or signs, and
(5) the course under careful, regular observation.
Any child exhibiting an ocular motor nerve palsy accompanied by other neurological signs deserves a consultation with a
neurologist and a thorough, timely workup. It is incumbent
upon the ophthalmologist to detect and treat any amblyopia that
may occur. Also, prevention of amblyopia, by alternate patching, for example, can be considered in severely amblyogenic conditions such as third nerve palsies.
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The following discussion sets out an approach to the recognition and initial management of isolated third, fourth, and
sixth nerve palsies and reviews some common childhood causes
of combined ocular motor nerve palsies.
SIXTH NERVE PALSIES
ETIOLOGY
AND
SYSTEMIC ASSOCIATIONS
Acquired sixth nerve palsies, whether isolated or not, are usually
caused by tumors (especially glioma and medulloblastoma) and
trauma (47%–62%).3,24,191,269,287,405 A significant number of cases are
also due to inflammatory causes such as meningitis (including
from Lyme disease), Gradenigo’s syndrome,117 cerebellitis, and
postviral sixth nerve palsy. The clinician is also faced with numerous other possible etiologies (Table 12-4).
CLINICAL FEATURES
AND
ASSESSMENT
As previously mentioned, a lesion affecting the sixth nerve
nucleus produces an ipsilateral horizontal gaze palsy. Injury to
the nerve at any other location along its course results in absent
or poor abduction of the ipsilateral eye (Fig. 12-7).
Of course, poor abduction is not specific to sixth nerve
palsies and may also be caused by disorders of the neuromuscular junction (e.g., myasthenia gravis), restrictions (e.g., medial
orbital wall fractures with tissue entrapment), and inflammation
(e.g., orbital myositis). The examiner considers and excludes
these possibilities before establishing the diagnosis of sixth
nerve palsy. If a congenital anomaly of innervation, such as
Duane’s syndrome, is clearly identified as the cause of abduction deficit, no further investigation of the eye movement abnormality is necessary.
Acute comitant esotropia can also follow head trauma
(usually minor), febrile illness, migraine, or occlusion of an eye
or may not be related to any obvious inciting cause.75,170,385,460
This condition is distinguishable on examination from a bilateral sixth nerve palsy. However, although an acute comitant
esodeviation without accompanying signs is usually benign, it
may in some cases be the harbinger of an intracranial tumor
such as cerebellar astrocytoma or pontine glioma29,526 or other
pathology such as a Chiari 1 malformation.517 Absence of symptoms or signs such as headaches, papilledema, or nystagmus may
not rule out the possibility of an intracranial pathology. There-
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TABLE 12-4. Etiology of Infranuclear Sixth Nerve Palsy.
Location/signs
Etiologies
Fascicle
Ipsilateral VIIth nerve palsy, facial
analgesia, loss of taste from anterior
two thirds of tongue; peripheral
deafness; Horner’s syndrome,
contralateral hemiparesis
Tumor; demyelination; hemorrhage;
infarction
Subarachnoid space
Papilledema; other cranial nerve
palsies
Meningitis; meningeal carcinomatosis;
trauma; increased intracranial
pressure causing downward pressure
on brainstem; after lumbar puncture,
shunt for hydrocephalus, spinal
anesthesia, or halopelvic cervical
traction; clivus tumor;
cerebellopontine angle tumor; berry
aneurysm; abducens neurinoma
Petrous apex
Ipsilateral seventh nerve palsy;
pain in eye or face; otitis media,
leakage of blood or cerebrospinal
fluid from ear; mastoid
ecchymosis; papilledema
Mastoiditis; thrombosis of inferior
petrosal sinus; trauma with
transverse fracture of temporal bone;
persistent trigeminal artery,
aneurysm, or arteriovenous
malformation
Cavernous sinus/superior orbital fissure
Ipsilateral Horner’s syndrome;
ipsilateral IIIrd, IVth, Vth cranial
nerve involvement; proptosis;
disc edema; orbital pain;
conjunctival injection
Cavernous sinus thrombosis;
carotid-cavernous fistula; tumor;
internal carotid aneurysm
Orbit
Ipsilateral IIIrd, IVth, Vth cranial
nerve involvement; proptosis; disc
edema; orbital pain; conjunctival
injection
Tumor; pseudotumor
Uncertain
Transient abducens palsy of newborn;
after febrile illness or immunization;
migraine; toxic; idiopathic
fore, a thorough ophthalmic examination is performed. MRI is
indicated if the esotropia is unresponsive to correction of refractive error, there is no history of flu-like illness, or no improvement is seen over the course of 1 to 4 weeks.
NATURAL HISTORY
AND
CLINICAL WORKUP
Newborns may demonstrate a transient sixth nerve palsy that
is frequently unilateral and occasionally accompanied by a tem-
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FIGURE 12-7. Right sixth cranial nerve palsy. These photos show the
limitation of abduction on attempted right gaze typical of a sixth cranial
nerve palsy. Forced duction testing of this patient’s right eye showed no
restriction to abduction.
porary ipsilateral seventh nerve palsy.53,267,291,400 Simple observation is generally sufficient because resolution typically occurs
within 4 to 10 weeks.
Older infants and children may develop transient isolated
sixth nerve palsies 1 to 3 weeks after nonspecific febrile or respiratory illnesses,267,405 after a specific viral illness such as
varicella,350 after immunization,522 before mononucleosis,273 or
without any obvious precipitating factor.435 Some of these palsies
may recur, and the recurrences have no serious implications.2,60,65,399,474,476 Again, aggressive investigation is not warranted,
but two simple studies are advised: (1) a complete blood count
with differential, which may show lymphocytosis as evidence of
a recent viral infection, and (2) examination of the ears for otitis
media. The parents are warned to observe for any new signs or
symptoms. Careful reexamination at regular intervals is essential;
deterioration or improvement in lateral rectus function provide
important evidence for or against a progressive mass lesion. Most
children in this group recover abducens function within 10 weeks,
although a prolonged (9 months) palsy may rarely occur.267
Persistence, without improvement, or deterioration of an isolated sixth nerve palsy in a child beyond about 3 months requires
an intensive neurological, neuroradiologic, and otolaryngologic
evaluation. In adults, a substantial number of isolated sixth nerve
palsies that last beyond 6 months are caused by potentially treatable, often slow-growing, tumors.111,159,426 In a Mayo Clinic series
of 133 children with acquired sixth nerve paresis, 15 presented
with an isolated sixth nerve palsy due to tumor.405 Of these, 12
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handbook of pediatric strabismus and amblyopia
developed additional neurological signs within a few weeks,
whereas 3 patients took 2 to 3 months to develop additional
signs. An additional problem is that a physician may not always
be able to confirm that the sixth nerve palsy in a child is isolated. Therefore, if close follow-up to resolution of the palsy or
paresis is not possible, neuroimaging is recommended.24
TREATMENT
Amblyopia prevention is always key in children younger than 7
to 9 years of age. Providing full hyperopic correction also relieves
the demand for accommodation and thus decreases the chance
of worsening esotropia.
Treatment options include botulinus toxin injection and
surgery. One approach is to inject botulinus toxin into the antagonist medial rectus muscle to prevent tightening of the unopposed medial rectus,442,444 sometimes allowing binocular vision
in primary position, while the palsy is resolving.218 Reducing
medial rectus contracture with botulinus toxin injection may
also improve a surgical result.302
PROGNOSIS
Spontaneous recovery of abduction in childhood sixth nerve
palsy or paresis is much less common than in adults. The rate
of residual strabismus was found to be 66% in one study of
any sixth nerve palsy or paresis in patients 7 years of age and
younger, likely a result of permanent structural deficits without
complete recovery in the setting of tumor and hydrocephalusshunt malfunction as the most frequent etiologies. The rate of
amblyopia in this study was 20%, thus highlighting the need for
parent education and close follow-up.
The highest rates of spontaneous recovery have been reported
in idiopathic (67%24), infectious (50%24), inflammatory (90%191),
and traumatic (33%–50%24,191) cases.
FOURTH NERVE PALSY
ETIOLOGY
AND
SYSTEMIC ASSOCIATIONS
Of the many causes of trochlear palsy in childhood (Table 12-5),
“congenital” and traumatic are by far the most common.191,209
The cause of most congenital trochlear palsies remains
unknown, but aplasia of the trochlear nucleus has been reported
to accompany the absence of other cranial nerve nuclei.10,317,464
The superior oblique tendon or muscle is often the primary
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TABLE 12-5. Etiology of Fourth Nerve Palsy.
Location/signs
Etiologies
Nucleus and fascicle
Contralateral Horner’s syndrome
Trauma; tumor; demyelination; after
neurosurgery; nuclear aplasia;
arteriovenous malformation;
hemorrhage; infarction
Subarachnoid space
Papilledema; other cranial nerve
palsies
Trauma; tumor; increased intracranial
pressure; after lumbar puncture or
shunt for hydrocephalus; spinal
anesthesia; meningitis; mastoiditis
Cavernous sinus/superior orbital fissure
Ipsilateral Horner’s syndrome,
ipsilateral IIIrd, Vth, VIth nerve
involvement; proptosis; disc
edema; orbital pain
Tumor; internal carotid aneurysm;
Tolosa–Hunt syndrome
Orbit
Ipsilateral IIIrd, VIth nerve
involvement; proptosis;
enophthalmos; disc edema; orbital
pain; conjunctival/episcleral
injection
Tumor; trauma; inflammation
Uncertain location
Congenital; idiopathic
problem. Laxity of this tendon has been described on forced
duction testing381 and correlates well with the presence of attenuated superior oblique muscles on orbital MRI.432 Therefore,
congenital cases may be more correctly termed congenital superior oblique palsy/underaction instead of fourth nerve palsy.
Absence of the superior oblique muscle altogether is also in the
differential of an apparent congenital superior oblique palsy.87
The trochlear nerves are particularly vulnerable to closed
head trauma when there may be contrecoup of the tectum of
the midbrain against the edge of the tentorium.292 In this way,
the nucleus or fascicle may be injured within the substance of the
midbrain, or the nerve itself may be contused as it exits the brainstem dorsally and passes laterally around the midbrain (see Fig. 123). The proximity of the two trochlear nerves to each other at the
site of their crossing in the anterior medullary velum (roof of the
Sylvian aqueduct; see Fig. 12-4) explains the high incidence of bilateral involvement after coup-contrecoup, closed head trauma.286
CLINICAL FEATURES
AND
ASSESSMENT
Vertical deviations may also result from other processes, such
as abnormal neuromuscular transmission, restriction, inflam-
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mation, skew deviation, dissociated vertical divergence, small
nonparalytic vertical deviations associated with horizontal strabismus, and paresis of other cyclovertical muscles. The clinical
assessment of a vertical deviation is carefully executed to
exclude these various possibilities.
It is important to ask about previous extraocular muscle
surgery or orbital trauma and to obtain any history that suggests
myasthenia gravis or skew deviation. The examiner notes any
anomalous head position (Figs. 12-8, 12-9), versions, ductions,
cover test measurements in cardinal fields of gaze, any secondary deviation, forced (Bielschowsky) head tilt test measurements, presence or absence of both subjective and objective
torsion, and presence or absence of dissociated vertical deviation. Forced ductions, Tensilon testing, and other supplemental
tests are performed as appropriate.
A
B
FIGURE 12-8. (A) Unilateral congenital cranial nerve palsy, right eye.
The photograpph demonstrates a right hypertropia that increases in left
gaze. There is slight underaction of the right superior oblique nad
significant overaction of the right inferior oblique muscle. (B) The photograph of head tilt test, with right hypertropia increasing on tilt right
and diminishing on tilt left. Positive head tilt with the right hyper
increasing in left gaze indicates a right superior oblique palsy.
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FIGURE 12-9. Bilateral asymmetric congenital fourth nerve palsy and
esotropia. Note that the right superior oblique palsy is more severe than
the left, and there is a right hypertropia in primary position. There is significant superior oblique underaction, right side more than left side. A
significant V-pattern is present. There is a right hypertropia in right gaze
and a left hypertropia in left gaze.
Several other comments regarding the clinical evaluation are
crucial.
1. The familiar “Parks–Bielschowsky three-step” test helps
to combine information from cover test measurements and the
Bielschowsky head tilt phenomenon.59,370 This test is only useful
when there is a palsy of a single cyclovertical muscle and can
therefore only be applied after the careful assessment just
described.281 A fourth nerve palsy would reveal hypertropia,
worsening on horizontal gaze in the direction contralateral to
the hypertropic eye, and worsening on head tilt ipsilateral to the
hypertropic eye. Infants with congenital superior oblique palsies
present with a head tilt, whereas older children and adults with
decompensated congenital palsies complain of vertical and/or
torsional diplopia.323
To diagnose a congenital superior oblique palsy, old photographs are helpful, often revealing a long-standing head tilt. Also,
vertical fusional amplitudes frequently exceed the normal range
of 3 to 4 prism diopters. The presence of a suppression scotoma
when assessing diplopia or the presence of fusion also aids in
establishing the chronicity of the condition as suppression is
usually a childhood adaptation mechanism. Moreover, the presence of facial asymmetry may be associated with a longstanding head tilt from early childhood.176,202,338,528 The presence
of facial asymmetry may not be a specific sign for congenital
superior oblique palsy, however, because patients with acquired
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superior oblique palsy and heterotopic rectus muscles exhibited
similar features of facial asymmetry.502 The causal relationship
of the head tilt due to an abnormal superior oblique is not established.373 Hemifacial changes are often associated with plagiocephaly as a craniofacial anomaly, and craniofacial anomalies are
commonly associated with anomalous extraocular muscles.124
2. The examiner also checks for bilateral and asymmetrical
superior oblique palsies, because the larger paresis may “mask”
the smaller until unilateral surgery is performed.274,280 Bilateral
involvement should particularly be suspected after closed head
injury. Findings that suggest bilaterality include alternation of
hypertropia with fixation, gaze, or head tilt; excyclotorsion of
10° or more; and V-pattern esotropia.286
3. Excyclodeviations usually occur with trochlear palsies,
may accompany restrictions and myasthenia gravis, and are less
commonly seen with skew deviations.494 The triad of skew deviation, head tilt, and incyclotorsion of the hypertropic eye is
termed the ocular tilt reaction, an entity that can mimic fourth
nerve palsy on the traditional three-step test.128 Therefore, examination for torsion, by double-maddox rod or simple fundoscopy,
is essential in distinguishing a fourth nerve palsy from ocular
tilt reaction.
INHERITANCE
Rarely, congenital superior oblique palsy may be familial.28,198
The mode of inheritance in the described families has not been
determined.
NATURAL HISTORY
Long-standing congenital superior oblique palsy may decompensate in adulthood for a variety of reasons, including trauma,
with the presenting symptom of vertical diplopia. As for traumatic cases, most cases of unilateral injury do resolve (see following). Also, after long-standing fourth nerve palsy, a “spread
of concomitance” may be observed where the deviation in
rightgaze and leftgaze are nearly equal, although the differential
deviation in right versus left head tilt persists. This spread of
concomitance has been attributed to a “contraction” of the ipsilateral superior rectus muscle.26
TREATMENT
Most surgeons wait 6 to 12 months before deciding on strabismus surgery for traumatic cases, to await spontaneous resolu-
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tion of the deviation or stability in measurements. For congenital cases presenting with head tilt in infancy, surgery may
be performed as soon as possible to correct the head posture and
thus to aid in normal development of the neck muscles and the
alignment of cervical vertebrae. It is unknown, however,
whether early strabismus surgery can prevent or reverse facial
asymmetry. For the large head tilts in infancy, a superior oblique
tuck may treat the head tilt quickly; the benefit of normalizing
head posture with this procedure may outweigh the resultant
iatrogenic Brown’s syndrome.
For long-standing fourth nerve or superior oblique palsy, a
variety of options exist. One approach is to operate on one
muscle for vertical deviations of up to 15 prism diopters and to
consider two-muscle surgery in deviations above 15 prism
diopters. The first choice of procedure is often ipsilateral inferior oblique muscle weakening. The second procedure often performed when the deviation is greater than 15 prism diopters is
either ipsilateral superior rectus recession,26 when the vertical
deviation is worse in upgaze, or contralateral inferior rectus
recession, when the deviation is worse in downgaze.202
A fast and easy approach to deciding which muscle to
weaken first is to perform a “modified Parks three-step test”205
to determine which muscle is overacting and then to weaken
that muscle first. This modified three-step test is performed in
the same manner as the traditional one, except for the first step,
in which the overacting vertical muscles are circled in each eye
(instead of the traditional method of circling the presumed weak
vertical muscles).
In the case of bilateral palsy, bilateral inferior rectus recession and Harada–Ito procedures are recommended, both able to
treat excyclotorsional diplopia.
PROGNOSIS
When a child presents with a postinfectious, isolated trochlear
palsy that cannot be explained as congenital, traumatic, restrictive, myasthenic, or neoplastic, the prognosis is good and observation alone is sufficient.
Overall prognosis for recovery of isolated fourth nerve palsies
in adults and children was reported to be 53.5% combined (1000
total patients from 2 months to 91 years of age, 90% of whom
were over 19 years and 75% of whom were over 35 years of
age).424 Unilateral traumatic fourth nerve palsies in a series of 24
pediatric and adult patients (ages 7–78 years; mean, 35.4 years),
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handbook of pediatric strabismus and amblyopia
46% of whom sustained minor head trauma, resulted in 75% resolution.483 Another series reported 65% resolution in unilateral
but 25% in bilateral cases of traumatic fourth nerve palsy.479
THIRD NERVE PALSY
ETIOLOGY
AND
SYSTEMIC ASSOCIATIONS
In childhood, a third nerve palsy typically keeps company with
other neurological findings, which aid in localization and diagnosis (Table 12-6), but isolated palsies do occur and are generally
congenital, traumatic, infectious, or migrainous.191,225,257,326,339,440
An acquired, isolated oculomotor nerve palsy in a child may also
result from tumor, preceding viral illness, bacterial meningitis
(most commonly pneumococcal, Haemophilus influenzae type
b, or Neisseria meningitidis), or immunization.76,77,86,191,225,257,309,
326,339,347,430,440,446
Rarely, children may demonstrate gradually
progressive paresis because of a slowly growing tumor1 or a
truly cryptogenic oculomotor palsy. Posterior communicating
aneurysms, although extremely rare in children, should be considered as well.313 Microvascular infarction due to atherosclero-
TABLE 12-6. Etiology of Infranuclear Third Nerve Palsy.
Location/signs
Etiologies
Fascicle
Ipsilateral cerebellar ataxia;
contralateral rubral tremor;
contralateral hemiparesis; vertical
gaze palsy
Demyelination; hemorrhage; infarction
(rare in childhood)
Subarachnoid space
Papilledema; other cranial nerve
palsies
Meningitis; trauma or surgery; tumor;
increased intracranial pressure;
uncal herniation
Cavernous sinus/superior orbital fissure
Ipsilateral Horner’s syndrome;
ipsilateral IVth, Vth, VIth nerve
involvement; proptosis; disc edema;
orbital pain; conjunctival/episcleral
injection
Cavernous sinus thrombosis; tumor;
internal carotid artery aneurysm;
carotid–cavernous fistula; Tolosa–
Hunt syndrome; pituitary apoplexy;
sphenoid sinusitis, mucocele;
mucormycosis
Orbit
Ipsilateral IVth, Vth, VIth nerve
involvement; proptosis;
enophthalmos; disc edema; orbital
pain; conjunctival/episcleral
injection
Trauma; tumor; inflammation
Uncertain location
After febrile illness or immunization;
migraine; idiopathic
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sis, hypertension, or diabetes mellitus, a common cause of isolated third nerve palsy in adults, is extremely rare in children.
CLINICAL–ANATOMIC CORRELATION
The anatomic organization of the third nerve nucleus, like that
of the sixth nerve nucleus, provides constraints that help differentiate the rare nuclear third nerve palsy from an infranuclear
third nerve palsy. Because the superior rectus subnucleus supplies the contralateral superior rectus muscle, and the central
caudal nucleus innervates both levator muscles, damage to a
single oculomotor nerve nucleus gives rise to contralateral superior rectus weakness and bilateral ptosis. Also, because of the
arrangement of the three medial rectus subnuclei and the visceral nuclei within the oculomotor nucleus, a nuclear third
nerve palsy is not likely to produce isolated medial rectus
involvement or unilateral pupillary involvement. In addition,
other midbrain signs such as vertical gaze abnormalities are
often associated with lesions of the oculomotor nucleus (see
Fig. 12-6).
Because the oculomotor nerve innervates the levator palpebrae superioris, the sphincter of the pupil and ciliary body, as
well as four extraocular muscles (the medial rectus, superior
rectus, inferior rectus, and inferior oblique), it is easy to identify
a complete infranuclear third nerve palsy by the presence of
ptosis; a fixed, dilated pupil; and a “down-and-out” eye position
resulting from the unopposed lateral rectus and superior oblique
muscles (Fig. 12-10). However, third nerve palsies can be
“partial”; any individual sign or combination of signs may be
present and, if present, may be complete or incomplete. Numerous patterns can therefore arise.
CLINICAL FEATURES
HISTORY
AND
ASSESSMENT/NATURAL
Oculomotor nerve palsies, like abducens and trochlear nerve
palsies, should be distinguished from myasthenia and mechanical restrictions. Clinically observable involvement of the pupil
or signs of oculomotor synkinesis (aberrant regeneration) establish involvement of the third nerve, assuming pharmacological
and traumatic mydriasis can be excluded.
The manner through which neural impulses become misdirected is not always clear.455 Misrouting of regenerating motor
axons is firmly documented152,392,456 and corroborates the frequent
clinical observation of the appearance of synkinesis at about 8 to
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handbook of pediatric strabismus and amblyopia
B
C
FIGURE 12-10. Patient with traumatic left third nerve palsy. The top
photograph shows the classic appearance of a left third nerve palsy with
ptosis and the eye in a down and out position. The left photograph shows
full abduction, left eye. The bottom right photograph shows left eye with
limited adduction. Note, there is lid retraction and miosis, left eye, on
attempted adduction indicating aberrant innervation of the levator
muscle and pupillary sphincter with part of the medial rectus nerve.
12 weeks after an acute palsy.277 However, aberrant regeneration
cannot comfortably account for transient oculomotor synkinesis239,289,454 or spontaneous “primary” oculomotor synkinesis.66,105,289,436,493 Ephaptic transmission, conduction of a nerve
impulse across a point of lateral contact, and synaptic reorganization of the oculomotor nucleus are two proposed theories of synkinesis.289,455 The presence of oculomotor synkinesis has not been
reported with demyelination, but it does not otherwise narrow the
differential diagnosis of third nerve palsy in the pediatric age group.
Congenital third nerve palsy is usually incomplete and unilateral and is frequently associated with oculomotor synkinesis
and “miosis” of the pupil in the affected eye.191,326,504 Although
many children with congenital oculomotor nerve palsies have
no associated neurological findings, some do,41 and a thorough
neurological evaluation of these infants is suggested. If there are
additional neurological signs or bilateral third nerve palsies, MRI
may also provide useful information.175
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Rarely, paresis and spasm of the extraocular and intraocular
muscles innervated by the third nerve may alternate, typically
every few minutes, to produce oculomotor palsy with cyclic
spasms.295 With few exceptions, these cycles accompany congenital, rather than acquired, oculomotor palsies and continue
throughout life. In some instances, several months to several
years may elapse between the discovery of the paresis and the
onset of the cyclic spasms. Investigation is not necessary unless
the third nerve palsy is acquired or there is progressive neurological dysfunction. The pathogenesis of this phenomenon remains
obscure.272
Ophthalmoplegic migraine generally begins in childhood40
but may even be seen in infancy.13,534 It is an uncommon disorder despite the fact that 2.5% of children experience a migraine
attack by age 7 and 5% by age 15.43 Symptoms of migraine in
children include nausea, vomiting, abdominal pain, and relief
after sleep in 90%.419 The headaches, which may be accompanied by an aura, are often unilateral and throbbing in quality.
Family history is positive in 70% to 90%. With ophthalmoplegic
migraine, the patient characteristically experiences pain in and
about the involved eye, nausea, and vomiting; often the third
nerve palsy ensues as the pain resolves. Full recovery of third
nerve function within 1 to 2 months is typical, but resolution
may be incomplete and oculomotor sykinesis has been
reported.355 Multiple attacks may occur, and years may pass
between episodes.133 Most patients with ophthalmoplegic
migraine have normal angiograms, but one 31-year-old with
recurrent episodes of ophthalmoplegic migraine, which had
begun at age 5, and partial third nerve palsy since age 7, demonstrated a small perimensencephalic vascular anomaly.224
Aneurysms have been reported to cause isolated third
nerve palsies during the first and the second decades of
life71,135,157,158,313,383 and carry a high risk of mortality or significant morbidity if left undetected and untreated. On the other
hand, aneurysms appear to be rare in children.158,495 Angiography
with general anesthesia can be risky in the childhood age group,
and the gap between the sensitivity of angiography and MRI for
detecting aneurysms continues to narrow. The clinician assesses
all these variables along with the history and physical examination to decide on the appropriate workup for each patient. For
example, in the child under age 10 with a family history of
migraine who presents with nausea, vomiting, and headache,
followed by third nerve palsy as these symptoms resolve, that
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is, with typical ophthalmoplegic migraine, angiography may
not be necessary.166 However, when a third nerve palsy acquired
in childhood cannot be explained on the basis of the clinical
examination or noninvasive neuroimaging, the cerebrospinal
fluid should be evaluated and angiography considered.
TREATMENT
After diagnosis and treatment of the underlying disorder, observation of any recovery of oculomotor nerve function is necessary before surgical intervention. When partial or full recovery
occurs, it often does so within 3 to 6 months but it may take 1
year or more. Surgical treatment includes strabismus surgery
and ptosis correction. The latter is approached with caution in
an eye that lacks a functional Bell’s phenomenon because of the
risk of exposure keratopathy.
PROGNOSIS
Two recent series have found fair to poor visual and sensorimotor outcome in oculomotor nerve palsy/paralysis of children
with comparable mix of congenital, traumatic, and neoplastic
cases.339,440 The best ophthalmologic outcome with measurable
stereopsis was in the resolved cases (3 of 20; 15%) in the first
study, and in 4 of 31 patients with partial third nerve palsy in the
second study, 2 of whom had spontaneous resolution. In the first
series, amblyopia therapy was most effective with congenital
causes, but treatment results were poor with other causes; young
children with posttraumatic and postneoplastic oculomotor nerve
injuries demonstrated the worst ophthalmologic outcomes.
COMBINED OCULAR MOTOR NERVE PALSIES
As the oculomotor, trochlear, and abducens nerves are in relatively close physical proximity from brainstem to orbit, it is not
surprising that many diseases occurring at numerous locations
can affect these nerves simultaneously.
CLINICAL ASSESSMENT
The evaluation begins by establishing that the eye movement
abnormality is due to cranial nerve disease rather than supranuclear lesions, disorders of the neuromuscular junction, restrictive or inflammatory myopathies, or chronic progressive
“neuromyopathies,” for example, Kearns–Sayre syndrome. In
the presence of a third nerve palsy, the fourth nerve function is
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tested by observing for intorsion of the affected eye in downgaze.
If multiple ocular motor nerve palsies are indeed present, a
thorough history and examination; neuroimaging of the rostral
brainstem, cavernous sinuses, and orbits; and examination of
the cerebrospinal fluid (CSF) are typically necessary to distinguish between the myriad possible localizations and etiologies.
Prompt diagnosis is particularly important for children with
infections or pituitary apoplexy; the latter is often accompanied
by severe headache, ophthalmoplegia caused by rapid expansion
into the cavernous sinus, and rapid mental status deterioration.
ETIOLOGIES
Processes in the brainstem (tumor, encephalitis), subarachnoid
space (meningitis, trauma, tumor), and of uncertain localization
(postinfectious polyneuropathy) tend to produce bilateral combined ocular motor nerve palsies whereas processes in the cavernous sinus/superior orbital fissure (tumor, pituitary apoplexy,
cavernous sinus thrombosis, carotid-cavernous fistula) and orbit
(trauma, tumor, mucormycosis) usually cause unilateral combined ocular motor nerve palsies.
The ophthalmologist needs to be familiar with certain generalized neuropathies that may initially present with acute ophthalmoplegia. In a series of 60 patients with acute bilateral
ophthalmoplegia, Guillain–Barre and Miller Fisher syndromes
accounted for the diagnosis in 15 of 28 patients under age 45.253
The bulbar variant of Guillain–Barre syndrome (acute postinfectious polyneuritis) frequently presents as a rapidly progressive, painless ophthalmoplegia. Early in the course, involvement
of eye movements may be incomplete and mimic either unilateral or bilateral oculomotor nerve palsies, but complete ophthalmoplegia with or without involvement of the pupils and
accommodation typically evolves within several days. Partial
ptosis usually accompanies severe limitation of eye movements,413 but levator function may be entirely normal or completely absent. Some degree of cranial nerve involvement occurs
in about 50% of children with Guillain–Barre syndrome,413 and
in the setting of rapidly progressing bilateral ophthalmoplegia,
dysfunction of other cranial nerves, particularly bilateral facial
nerve involvement, strongly supports the diagnosis of acute
postinfectious polyneuritis.
A variety of infections have been reported to precede Guillain–Barre syndrome in 50% to 70% of children; these include
gastroenteritis, tonsillitis, measles, mumps, varicella, pertussis,
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hepatitis, Epstein–Barr virus, Campylobacter jejuni, coxsackie
virus, and nonspecific upper respiratory infections. Two of these,
varicella103,521 and acute Epstein–Barr virus infection,184 precede or
accompany the onset of Guillain–Barre syndrome with noteworthy frequency in children and young adults. Paresthesias, often
painful, commonly appear early in the course, and signs of
meningeal irritation may also appear early in children. Although
a rise in CSF protein levels without pleocytosis is the rule, it generally does not occur for several days to weeks after the onset of
symptoms and, in a small percentage of patients, is not observed
at all. The patient should be referred to a neurologist for management in a hospital setting with materials for tracheostomy and
mechanical ventilation readily available.
Ophthalmoplegia (external and sometimes internal), ataxia,
and areflexia constitute Miller Fisher syndrome,155 and diplopia
is usually the first symptom. At least 20 children (under age 18
years) with Miller Fisher syndrome have been reported.50 A preceding febrile or “viral” illness may be reported with many of
the same infectious agents previously listed.
Although the eye movements often suggest unilateral or
asymmetrical bilateral abducens pareses, many patterns have
been reported including horizontal gaze palsy, upgaze palsy,249
pupil-sparing oculomotor nerve palsy, and pseudointernuclear
ophthalmoplegia.30,125,478,520 All these eye movement patterns generally progress to severe bilateral ophthalmoplegia within 2 or 3
days. Ptosis and pupillary involvement may occur but are often
absent.78 Limb and gait ataxia typically appear 3 or 4 days after
the ophthalmoparesis but are, at times, concurrent with it. Areflexia is almost invariably present by the end of a week.141 An
association with demyelinating optic neuropathy has also been
reported.368,488
Miller Fisher syndrome is considered to be a variant of
Guillain–Barre syndrome. However, there is some controversy
as to the site of the lesion in Miller Fisher syndrome,8,315,414,415,488
whereas Guillain–Barre is clearly a peripheral neuropathy. Clinical observations suggesting the possibility of CNS involvement
in Miller Fisher syndrome have included apparently supranuclear eye movement abnormalities314,459 and clouding of consciousness.8,50 In some cases, evoked potentials232 and MRI416
have been normal; in others, CT images121,541 and MRI136,163 have
displayed clear abnormalities in the brainstem as well as in the
cerebral white matter and cerebellum. In yet another group,
absent F waves and H reflexes on peripheral nerve testing and
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markedly abnormal electroencephalograms suggested both
peripheral and central involvement.50 Two neuropathological
studies demonstrated normal CNS in both,119,378 and another
showed inflammatory infiltration of peripheral and cranial nerve
roots25; however, central chromatolysis in the nuclei of the third,
fourth, fifth, and twelfth nerves and of the anterior horn cells
has also been reported.186 Additionally, anticerebellar antibody
has been found to be reactive to a significantly greater number
of bands on Western blotting of serum from Miller Fisher
patients (6 of 7) compared to that of Guillain–Barre (3 of 6) or
healthy controls (4 of 10).227
As with acute postinfectious polyneuritis, if the CSF is
examined late enough in the course, the protein concentration
is elevated in most cases.141 A useful diagnostic tool is the presence of antiganglioside antibodies in serum of patients with
Guillain–Barre and Miller Fisher syndromes. Patients with
Guillain–Barre syndrome subsequent to Campylobacter jejuni
enteritis frequently have IgG antibody to GM1 ganglioside.
Miller Fisher syndrome is associated with IgG antibody to GQ1b
and GT1a ganglioside in 90% of cases.527,539 Moreover, acute ophthalmoparesis without ataxia has also been found to be associated with anti-GQ1b antibody, suggesting that this is a milder
variant of Miller Fisher syndrome.539 These antibody findings are
evidence for the molecular mimicry theory of postinfectious
autoimmune pathology.
Despite its dramatic and alarming presentation, Miller
Fisher syndrome generally has a benign prognosis. Careful observation is, however, recommended because ophthalmoplegia
occurred early in one case of childhood Guillain–Barre syndrome
that progressed to respiratory failure.179 Occasionally, “relapsing
Miller Fisher syndrome” appears to occur,434,506 which should not
be confused with recurrent ocular motor palsies that may
accompany a rare familial syndrome of recurrent Bell’s palsy.9
Treatment of Guillain–Barre and Miller Fisher syndromes may,
in severe cases, require plasmapheresis or intravenously administered immunoglobulin.241,538
Acute hemorrhagic conjunctivitis caused by enterovirus 70
can be accompanied by dysfunction of any of the cranial or
spinal motor nerves,220,246,513 resulting in a polio-like paralysis
(radiculomyelitis) in approximately 1 in 10,000 patients infected
with this virus.535 Cranial nerve involvement occurred in 50% of
the patients in one series.246 Solitary seventh or fifth nerve palsies
were most common, followed in frequency by combined fifth and
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seventh nerve palsies. Prognosis correlates with severity and
pattern of cranial nerve involvement; patients with mild weakness and involvement of cranial nerves VII, IX, and X tend to
resolve fully, whereas those with severe weakness and involvement of cranial nerves III, IV, V, and VI often do not significantly
improve. Optic atrophy may also occur. Treatment is only
symptomatic.
Anomalies of Innervation
Some ocular motility disturbances, both congenital and
acquired, arise when an inappropriate nerve or nerve branch
innervates an extraocular muscle. Such “miswiring” immediately suspends the laws of extraocular motor physiology (e.g.,
Hering’s and Sherrington’s laws) and produces bizarre, intriguing eye movements. In certain cases, electromyographic (EMG)
and pathological studies have confirmed the defective anatomy
and physiology underlying the clinical presentation. Although
miswiring can generate many types of abnormal eye movements, only the more common anomalous motility patterns are
detailed here.
SIXTH NERVE
DUANE’S SYNDROME
Duane’s syndrome is characterized by retraction of the globe and
narrowing of the lid fissure on attempted adduction as well as
limited eye movements. Three forms of abnormal motility have
been classified217:
Type I: limited abduction with intact adduction (Fig. 12-11)
Type II: limited adduction with intact abduction
Type III: limited abduction and limited adduction
Incidence Duane’s syndrome has been reported to account
for 1% to 4% of all strabismus cases.122
Etiology Electromyographic data indicate that the medial
and lateral recti contract simultaneously, that is, they “cocontract,” and may thereby produce both the retraction of the
globe into the orbit and the limitation of eye movement.216,217,308
One can speculate as to how different distributions of inappropriate neural input from the oculomotor and abducens nerves to
the lateral and medial recti could produce each of the three patterns of limited ocular motility seen in Duane’s syndrome. This
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FIGURE 12-11. Duane’s syndrome, left eye. This montage demonstrates
the limitation of abduction (middle, right photo), palpebral lid fissure narrowing on adduction (middle, left photo), upshoot in adduction (top, left
photo), and “Y” pattern (middle, top photo) seen with Duane’s syndrome.
aberrant innervation is thought to be a result of congenitally
deficient innervation of the VIth nucleus, leading to a fibrotic
lateral rectus muscle (Fig. 12-12).
Neuropathological investigations of three patients with
Duane’s syndrome have all revealed aplasia or hypoplasia of the
abducens nucleus and nerve, and in two of these cases, branches
of the third nerve “substituted” for the defective sixth nerve by
supplying some of its fibers to the lateral rectus. The first case
was unilateral and demonstrated a hypoplastic lateral rectus
muscle in addition to hypoplasia of the abducens nucleus and
nerve.310 In a second patient with bilateral type III Duane’s syndrome, both abducens nuclei and nerves were absent; also, both
lateral recti were found to be partially innervated by the inferior
division of the oculomotor nerves and were histologically
normal in innervated areas but fibrotic in areas not innervated.213 The third patient had unilateral, left type I Duane’s syndrome and showed, as did the previous case, absence of the sixth
nerve, partial innervation of the lateral rectus by the inferior
division of the oculomotor nerve, and fibrosis of the lateral
rectus muscle in areas not innervated. However, although the
left abducens nucleus was hypoplastic, containing less than half
the number of neurons seen in the right nucleus, both medial
longitudinal fasciculi were normal and the remaining cell bodies
in the nucleus were interpreted to be internuclear neurons. This
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finding corroborates the clinical observation that, in unilateral
type I Duane’s syndrome, adducting saccades in the unaffected
eye are usually normal.177,322,333 This finding also indicates an
exquisitely specific neural deficit. Electrophysiological techniques such as auditory evoked potentials237 and eye movement
recordings351,537 have suggested that there may be other associated brainstem dysfunction, but these studies have not produced
conclusive evidence or have not been reproducible.403,481
“Upshoots” and/or “downshoots” on attempted adduction
are common motility findings. Theoretically, the cause of the
upshoots and downshoots may be mechanical, innervational, or
a combination of the two. In most cases, the mechanics of the
lateral rectus seem to be largely responsible because weakening
or eradicating the action of a tight lateral rectus results in significant reduction or elimination of upshoots and downshoots.
The “bridle-effect theory” postulates that vertical sideslip of a
tight lateral rectus across the adducting globe produces these
movements234,510; however, neuroimaging has not confirmed
vertical displacement of the lateral rectus during upshoots
and downshoots.62,511 In certain individuals, an innervational
anomaly may account for upshoots and downshoots. For
example, one of the authors (B.N.B.) has observed that continued severe upshoot on adduction in a patient whose lateral
rectus was detached from the globe and allowed to retract far
FIGURE 12-12. Proposed embryonal etiopathogenesis of Duane’s syndrome as a congenitally deficient innervation syndrome. The developing
cranial nerves have a “trophic” function on the developing mesenchyme
of the future extraocular muscles. If there is late or no innervation to the
developing mesenchyme, the muscle becomes dysplastic, fibrotic, and
inelastic. If there is early aberrant innervation of the developing mesenchyme by cranial nerve III, the lateral rectus has a “normal” architecture but abnormal innervation, leading to limited abduction only (type I).
The later during embryogenesis the innervation, the more dysplastic the
lateral rectus, leading to limited adduction as well (type III). The balance
between the quantitative amount of aberrant innervation and the degree
of lateral rectus fibrosis creates relatively different patterns of abduction
and adduction, leading to the different “types” of Duane’s syndrome. Type
II Duane’s syndrome (not depicted) may be caused by more innervation
from the third cranial nerve to the lateral rectus compared to the medial
rectus. Dotted lines represent absent or hypoplastic innervation; dashed
lines represent later onset of innervation; thickness of lines represents
quantitative amounts of innervation. LR, lateral rectus; MR, medial
rectus; III, oculomotor nucleus; VI, abducens nucleus.
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into the orbit before suture adjustment. In addition, there is
EMG evidence for cocontraction of appropriate cyclovertical
muscles and the lateral rectus during upshoots and downshoots217,322,443; such cocontraction could play a substantial role
in some cases.
Clinical Features and Natural History Most large series
indicate that females represent about two-thirds of cases and
that the left eye is affected in about two-thirds of unilateral
cases. Approximately 75% are type I; type III accounts for most
of the rest, and type II is quite rare. Types I and II may occasionally coexist in the 10% to 20% of cases that are bilateral.
Many Duane’s syndrome patients are orthotropic in primary
position or with a small head turn and have excellent binocular
function.229,391,402 Although amblyopia can occur in the involved
eye, the reported incidence of amblyopia as well as anisometropia varies widely.448,491 Most Duane’s syndrome patients
ignore or are unaware of sensory disturbances,300 but occasionally an older child presents with “acute” awareness of diplopia
in the appropriate fields of gaze.
As mentioned, upshoots and downshoots on attempted
adduction may occur and may be accompanied by A, V, or X patterns, giving the appearance of oblique muscle dysfunction.
Clinical Assessment Other diseases should be considered
in the differential diagnosis. Rarely, acquired orbital disease
may produce limitations of abduction and retraction, thereby
mimicking Duane’s syndrome. This effect has been observed
with medial orbital wall fractures, fixation of muscle by
orbital metastases, orbital myositis, and a variety of other
conditions.165,266,367,469
Systemic Associations Although Duane’s syndrome is
usually an isolated finding, it may accompany any of a multitude of other congenital anomalies in 5% to 57% of cases (Table
12-7).307,363,377
Inheritance Familial cases are not uncommon, and an
autosomal dominant mode of inheritance best fits most, but not
all, of the reported pedigrees.126 Duane’s syndrome, sensorineural
deafness, upper limb defects, facio-auriculo-vertebral anomalies,
and genitourinary and cardiac malformations appear as isolated
findings or in combination throughout certain families and
may all, perhaps, be ascribed to a highly pleiotropic autosomal
dominant gene that is frequently nonpenetrant.198a,361 Studies of
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TABLE 12-7. Congenital Anomalies Associated with Duane’s
Syndrome.
Structure
Associated anomalies
Ocular/external
Microphthalmos; coloboma; heterochromia iridis; flocculi
iridis; congenital cataract33,34,363
Ptosis; nevus of Ota; hypertelorism; prominent
epicanthus33,34,210,377,448
Epibulbar dermoid307,363,377,379
Neural
Optic nerve anomalies34,120,248,261,307,377; DeMorsier syndrome5
Sensorineural deafness261–264,307,448
Seventh nerve palsy106,307,377,428
Marcus Gunn jaw winking230,307
Gusto-lacrimal reflex58,307,393
Fourth nerve palsy307
Möbius syndrome307
Musculoskeletal
Craniofacial anomalies; skeletal anomalies; Klippel–Feil
syndrome; Goldenhar’s syndrome; Marfanoid
hypermotility syndrome; cleft lip/palate; muscular
dystrophy34,35,106,212,261–264,307,361,363,377,379,393,421,448
Miscellaneous
Cardiac anomalies35,307,377
Genitourinary anomalies106,377
Noonan syndrome
Fetal alcohol syndrome211
Congenital panhypopituitarism107
Oculocutaneous albinism208
monozygotic twins have revealed both concordance and discordance in more than one family.207,247
Two recent reports of large families with autosomal dominant Duane’s syndrome, one in the U.K. and the other in
Mexico, have both found linkage to chromosome 2q31.20,148
Other reports have found deletions in chromosome 8q in
patients with Duane’s syndrome associated with other abnormalities such as mental retardation and hydrocephalus.79,505
Treatment A patient with unacceptable primary position
deviation, head position, globe retraction, upshoot, or downshoot may require surgery. All these factors as well as the
relative contributions of mechanical and innervational factors
are considered during surgical planning. As a general recommendation, resections of the horizontal recti of an affected eye
is usually avoided because this may increase globe retraction.
Otherwise, the surgical approach is individualized.275 Depending on the situation, a wide variety of techniques may prove
helpful, including transposition of the vertical recti with or
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without medial rectus recession,169,331 Y-splitting of the lateral
rectus,410 adjustable sutures,388 and posterior fixation
sutures.293,510
Prognosis Recession of horizontal rectus muscle eliminates the face turn in 79% of cases and significantly reduces the
face turn in most of the remaining patients.276,388 Undercorrection of primary position esotropia may occur postoperatively as
the amount of recession needs to be larger than indicated in the
traditional tables for concomitant strabismus; rerecession is recommended for these cases if the initial recession was less than
8 mm or if forced duction testing still indicates restriction. The
occasional overcorrections may be reversed by advancing the
recessed muscle or recessing the antagonist horizontal rectus
muscle if tight.171,348,353
SYNERGISTIC DIVERGENCE
Synergistic divergence is a striking motility pattern consisting
of an adduction deficit with simultaneous bilateral abduction
on attempted gaze into the field of action of the involved medial
rectus.109,514,525 As with Duane’s syndrome, cocontraction of the
lateral and medial recti has been demonstrated on EMG,525 and
it has therefore been suggested that synergistic divergence may
be placed along the Duane’s “spectrum” of congenital anomalous innervation. In this conceptual scheme, synergistic divergence is similar to type II Duane’s syndrome, except that the
larger part of the branch of the third nerve “intended” for the
medial rectus is misdirected to the lateral rectus. The globe
retraction characteristic of Duane’s syndrome does not accompany synergistic divergence, presumably because there is so
little innervation to the medial rectus. However, this hypothesis has not been verified by clinicopathological study, and saccadic velocity studies in two patients indicate that the abducens
nerve may not necessarily be absent or severely hypoplastic.188
Synergistic divergence has been observed as early as 5
months of age,108 may be bilateral,187,188,486 and has been associated with other abnormalities including Marcus Gunn jawwinking,72,73,187 ipsilateral congenital Horner’s syndrome,238
arthrogryposis multiplex congenita,109 congenital fibrosis syndrome, and oculocutaneous albinism.72,73
Surgical crippling of the ipsilateral lateral rectus has been
combined with a variety of other procedures such as medial
rectus resection and superior oblique tenotomy and inferior
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330
oblique myectomy to eliminate the simultaneous abduction
as well as to correct the exotropia in primary position.188
Other types of anomalous innervation that may involve
the sixth nerve include congenital or acquired synkinesis of
the levator and lateral rectus during abduction,242,343 acquired
trigemino-abducens synkinesis with abduction accompanying
jaw movements,312,349,453 congenital twitch abduction on
attempted upgaze,271 or lateral gaze synkinesis on downward
saccades.503
THIRD NERVE
OCULOMOTOR SYNKINESIS
Oculomotor synkinesis (aberrant regeneration of the third nerve)
commonly accompanies third nerve palsies, usually those of
congenital or traumatic origin, but also those caused by
aneurysm, migraine, or tumor. This condition is discussed in
detail in the section on third nerve palsies. Although oculomotor synkinesis is, perhaps, the most familiar form of anomalous
innervation involving the oculomotor nerve, other patterns do
occur.
VERTICAL RETRACTION SYNDROME
Vertical retraction syndrome is exceedingly rare with only several
case reports in the literature.258,376,389,433,518 Typically, elevation or
depression of the globe is limited, and when attempted, it is
associated with narrowing of the lid fissure and retraction. There
may be an associated horizontal deviation that is greater with
gaze in the direction of the limited vertical eye movements.
Forced ductions are positive, although this does not preclude a
central mechanism.
EMG study of one patient revealed lateral rectus muscle
contraction on upgaze and downgaze. Eye movement recordings
of this and two other patients in the same study showed a twitch
abduction of the occluded eye on upward saccades, followed
by a postsaccadic drift back and a slower abduction in downgaze; this phenomenon was seen in each nonfixing of all
three patients, suggesting a synergistic innervation between the
abducens nerve and the upper and lower divisions of the oculomotor nerve.
EMG in one atypical case of vertical retraction syndrome
showed cocontraction of the vertical recti in upgaze, downgaze,
and adduction, and electro-oculography was also consistent with
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an anomalous innervational pattern.389 The clinical findings
included exotropia; poor elevation and adduction; retraction of
the globe on upgaze, downgaze, and adduction; and downshoot
on adduction.
MARCUS GUNN JAW-WINKING
Marcus Gunn jaw-winking is not usually accompanied by abnormal eye movements but is included here as another instance of
anomalous innervation. This congenital trigemino-oculomotor
synkinesis links innervation of jaw and eyelid levator muscles
and is characterized by congenital ptosis, usually unilateral,
with elevation of the ptotic lid when the jaw is moved. This ipsilateral associated ptosis accounts for 5% to 10% of all congenital ptosis.57,193
Etiology Because normal subjects demonstrate EMG
cocontraction of the muscles supplied by the oculomotor nerve
and certain muscles of mastication supplied by the trigeminal
nerve,427 Marcus Gunn jaw-winking may represent an exaggeration of a physiological synkinesis that is normally present but
clinically undetectable. The precise mechanism for failure of
higher inhibition remains unclear. EMG evidence and histological study of the levator muscles suggest an underlying brainstem process because the levator muscles are involved
bilaterally.204,299,427
Clinical Features There are two major categories of
trigemino-oculomotor synkinesis. The first, and most common,
consists of external pterygoid-levator synkinesis and is characterized by lid elevation when the jaw is projected forward, thrust
to the opposite side, or opened widely. In the second form, internal pterygoid-levator synkinesis, lid elevation is triggered by
clenching of the teeth. Rarely, a number of stimuli other than
pterygoid contraction can cause eyelid elevation, and these
include smiling, inspiration, sternocleidomastoid contraction,
tongue protrusion, and voluntary nystagmus. Conversely, in an
unusual case of trigemino-oculomotor sykinesis, pterygoid contraction was associated with contraction of the inferior rectus
rather than the levator, thereby producing monocular bobbing
eye movements rather than eyelid elevation.356
Marcus Gunn jaw-winking typically presents shortly after
birth with rhythmic elevation of the affected upper lid during
feeding. The ipsilateral associated ptosis may be of any degree
of severity. A significant number of patients have amblyopia,
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anisometropia, strabismus, superior rectus palsy, or double
elevator palsy.57,193
Natural History It is interesting to note that, in many
cases, parents remark that the synkinesis seems less apparent as
the child becomes older. As this observation is not supported by
objective examination, it may occur because the child learns to
control both lid position and excursion.
Systemic Associations Marcus Gunn jaw-winking can be
bilateral; has been reported in association with other forms of
anomalous innervation such as synergistic divergence, Duane’s
syndrome, and trigemino-abducens synkinesis; and is rarely
familial or associated with heritable diseases such as Waardenburg syndrome, Rubinstein–Taybi syndrome (author’s observation; M.M.), Hirschsprung megacolon, neuroblastoma, and
neurofibromatosis type 1.94,268,316
Treatment Strabismus, amblyopia, and anisometropia are
treated when necessary. Surgical management of the ptosis may
be achieved by conventional levator resection in mild cases of
jaw-winking. In moderate to severe cases, bilateral levator excision and bilateral frontalis suspension have been shown to
provide satisfactory correction of both jaw-winking and ptosis.
The frontalis suspensions may be achieved by using fascia lata,
either autologous or homologous, or strips of the levator muscle
after transsecting the muscle, but still attached distally via the
aponeurosis to the tarsus.45,259
SEVENTH NERVE
The seventh nerve may also be involved in several anomalous
innervational patterns that do not affect eye movements but
may present to the ophthalmologist.
INTRAFACIAL SYNKINESIS
Intrafacial synkinesis commonly appears after peripheral facial
nerve palsies; branches of the regenerating seventh nerve are
misrouted to inappropriate muscles. Frequently, for example,
the orbicularis oculi contracts simultaneously with lower facial
muscles, and there may be significant narrowing of the palpebral fissure with smiling. Other patterns can occur and, on occasion, are bothersome enough for a patient to require botulinus
toxin injection or surgery.22,390,411
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MARIN–AMAT SYNDROME
This syndrome, also known as inverse Marcus Gunn phenomenon, is a rare disorder in which the upper eyelid falls when the
mouth opens. This syndrome is observed after peripheral facial
nerve palsies and has been suggested to be a result of aberrant
reinnervation. However, EMG shows inhibition, rather than
excitation, of the affected levator muscle during external pterygoid contraction,296 and absence of orbicularis oculi activity may
differentiate this condition from the typical forms of intrafacial
synkinesis. Wide jaw opening causes synkinetic contraction of
the orbicularis oculi and lid closure, possibly triggered by
stretching of the facial muscles.394
DISORDERS AT THE NEUROMUSCULAR
JUNCTION
Myasthenia Gravis in Infancy
Myasthenia gravis in the infant takes one of three clinical forms.
TRANSIENT NEONATAL MYASTHENIA
Transient neonatal myasthenia is seen in approximately one of
seven infants born to mothers with myasthenia gravis. All these
babies develop a weak cry and difficulty sucking in the first
several days of life, and about half become generally hypotonic.
This condition, caused by antiacetylcholine receptor antibody
(anti-AChR antibody) received by the baby from the mother’s circulation,292 responds promptly to anticholinesterase agents but
will resolve in 1 to 12 weeks if untreated.344,530 There is no relapse
or long-term sequela.
FAMILIAL INFANTILE MYASTHENIA GRAVIS
Familial infantile myasthenia is rare, appears in children of
mothers without myasthenia gravis, and presents in early
infancy with ptosis, poor suck and cry, and secondary respiratory infections. Episodic crises of severe respiratory depression
and apnea are precipitated by fever, excitement, or vomiting.151,180,406 Other features include hypotonia, proximal muscle
weakness, and easy fatigability, but the extraocular muscles
are usually not involved. Inheritance of familial infantile
myasthenia gravis has been reported to be autosomal recessive
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with localization to the telomeric region of chromosome 17,
on 17p13.90 A candidate gene under study for this disease in the
17p region is synaptobrevin-2, a synaptic vesicle protein; this
protein probably participates in neurotransmitter release at a
step between docking and fusion.221 This disorder responds to
anticholinesterase medications and tends to ameliorate with
age.
CONGENITAL MYASTHENIC SYNDROMES
A third type of myasthenia seen in infants is the group of congenital myasthenic syndromes, a heterogeneous group of disorders that may affect presynaptic or postsynaptic mechanisms.
Various acetylcholine receptor subunit defects as well as genetic
defects in endplate acetylcholinesterase have been related to different congenital myasthenic syndromes.144
The frequency of congenital myasthenic syndromes varies
from 8% to 21% in reported series of childhood myasthenia
gravis, reportedly higher where consanguineous marriages are
frequent.18,340 In the fetal period, decreased fetal movements have
been reported, resulting in arthrogryposis multiplex congenital,
congenital flexures, and contractures of multiple joints.498
Affected patients are born to mothers without myasthenia and
may demonstrate ptosis and ophthalmoparesis during infancy.
Severe generalized weakness may also present in the postnatal
period with frequent apneic episodes, recurrent aspiration,
failure to thrive, and poor sucking. Other patients may present
during the first or second year of life with ocular signs and only
mild systemic signs. Although ptosis was reported to be present
in all of seven patients in one series,340 it was generally mild and
not incapacitating.
These disorders persist throughout life and can be distinguished from acquired myasthenia gravis and from each other
by combining clinical, electrophysiological, ultrastructural, and
cytochemical investigations.144–146 Tensilon testing can be positive, and a patient may respond to a trial of pyridostigmine. Presence of anti-AChR antibody excludes this disease.340 Inheritance
in one type termed slow-channel congenital myasthenia gravis
has been attributed to mutations in the AChR subunit genes,
and depending on which subunit is mutated, the disease is transmitted in an autosomal dominant or autosomal recessive
fashion. Treatment in congenital myasthenic syndrome patients
is generally supportive, and the use of acetylcholinesterase
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handbook of pediatric strabismus and amblyopia
inhibitors is disease specific. Surgery for stable strabimsus in a
child can yield a stable long-term result.340
Autoimmune Myasthenia Gravis
INCIDENCE
Acquired myasthenia gravis affects overall about 1 in 20,000 per
year to 0.4 in 1,000,000 per year.519 Girls are affected two to six
times as frequently as boys, and the incidence of the condition
increases progressively through childhood until the end of the
second decade of life. Afer the age of 50 years, males predominate;
the mean age of onset in women is 28 years and in men 42 years.519
Among the various childhood forms of myasthenia gravis, a
recent series identified 25 (71%) of 35 children as having the
autoimmune disease.340
ETIOLOGY
Acquired myasthenia gravis is an autoimmune disorder. The
myasthenic patient has fewer available skeletal muscle acetylcholine receptors because of antibodies produced against these
receptors130 and also because of complement activation.16 Neuromuscular transmission is thereby poised to fail. Normally,
with repetitive stimulation of a motor nerve, the amount of
acetylcholine released from that nerve diminishes. In the delicately balanced myasthenic, this decrease in neurotransmitter
may well lead to a failure of muscular response. In this context,
it is easy to understand why muscle fatigue is the clinical hallmark of myasthenia gravis and why the constant activity of the
extraocular muscles, among other activities,243,354 particularly predisposes them to demonstrate fatigue. The exact reasons for
predilection for the extraocular muscles are under study, one
explanation potentially lying in the differential expression of
acetylcholine receptor subunits in extraocular versus skeletal
muscle.47,244,301
A number of medications are known to produce myasthenia gravis in normal individuals or to exacerbate already existing disease. The list includes D-penicillamine, antibiotics,
anticonvulsants, intravenous contrast dye, anticholinesterase
agents, neuromuscular blocking agents, antiarrhythmic drugs,
phenothiazines, beta-blockers, and quinine. For example, myasthenia produced by D-penicillamine is indistinguishable from
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primary acquired myasthenia clinically, immunologically, and
electrophysiologically.519
CLINICAL FEATURES
Several general clinical observations may be made concerning
myasthenia gravis. Muscle weakness is not accompanied by
other neurological signs; muscle function, which may fluctuate
even within the course of an office visit, is improved by cholinergic medications; and extraocular, facial, and oropharyngeal
muscles are most commonly involved. Beyond this, there are
numerous variations of presentation, and no single sign is solely
reliable.
NATURAL HISTORY
Of patients who present initially with purely ocular symptoms
and signs, 50% to 80% subsequently develop generalized myasthenia within about 2 years.519 In a large study of 1487 patients
with myasthenia, 53% presented with ocular symptoms.183,519 Of
the entire group of myasthenic patients in this study, 15% continued to demonstrate purely ocular manifestations (with
follow-up to 45 years; mean, 17 years). Of the 40% of patients
in this study with strictly ocular involvement during the first
month after onset of symptoms, 66% developed generalized
disease. Of these who subsequently developed generalized
disease, 78% did so within 1 year, and 94% within 3 years after
onset of symptoms and signs.
In a series of 24 children in Toronto with acquired autoimmune myasthenia (age, 11 months to 16 years; median age, 4.7
years), 14 (58%) patients initially had ocular involvement only
(median follow-up time, 2.6 years). Of these 14, 5 (36%) progressed to generalized myasthenia gravis in a mean time of 7.8
months (range, 1–23 months). Patients with ocular myasthenia
presented at an average of 6.8 years; those with systemic disease
presented on average at 7.1 years.340
CLINICAL ASSESSMENT
Variable diplopia or ptosis most often prompt an ophthalmologic
evaluation. Patients with these symptoms are evaluated for
signs and symptoms of generalized myasthenia such as facial
weakness, dysphonia, arm or leg weakness, chewing weakness,
and respiratory difficulties. In “ocular myasthenia,” however,
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the findings are restricted to the levator and extraocular
muscles. Because there is no stereotypical myasthenic eye
movement, this diagnosis should be considered in any child with
an unexplained, acquired ocular motility disturbance and clinically normal pupils, particularly when the deviation is variable,
whether or not ptosis is present. Any pattern of abnormal motility is suspect, including an apparent gaze palsy, internuclear
ophthalmoplegia,167 isolated cranial nerve palsy,423 one and onehalf syndrome,116,468 incomitant strabismus, accommodative and
vergence insufficiency,101 and gaze-evoked nystagmus.250,288 Prolonged OKN may demonstrate slowing of the quick phases; large
saccades may be hypometric; small saccades may be hypermetric; and characteristic “quiver movements,” which consist of an
initial small saccadic movement followed by a rapid drift backward, may be seen.46,288
In addition to the eye movements, lid function is assessed.
Ptosis can be elicited or accentuated by fatiguing the levator
palpebrae superioris with prolonged upgaze or repeated lid
closure. Because Hering’s law of equal innervation applies to the
levator muscles as it does to the extraocular muscles, the contralateral lid may be retracted but falls to a normal position
when the ptotic lid is lifted with a finger. Through the same
mechanism, in bilateral ptosis, manual elevation of one lid
increases the amount of ptosis on the other side by diminishing
the amount of innervation necessary to fixate. Cogan’s lid
twitch sign can be elicited in some myasthenic patients by
having the patient look down for 20 s and then making an
upward saccade to the primary position; the lid twitches upward
one or more times and then slowly drops to its ptotic position.
Finally, the orbicularis oculi muscles are often weak, and the
patient may not be able to sustain lid closure.
Examination of the patient before and after the administration of anticholinesterase agents is, arguably, of more limited
use in children than in adults. This method may be most helpful
in children whose history and physical examination do not
permit a clear diagnosis yet who have such significant deficits
in lid elevation or ocular motility that a response is easily
observed. A positive test consists of the direct observation of a
weak muscle becoming stronger after the administration of
intravenous edrophonium hydrochloride (Tensilon) or intramuscular neostigmine methylsulfate (Prostigmin). The initial
dose is 2 mg, given up to 10 mg total. The onset of action for
Tensilon is 30 s, lasting up to 5 min. This drug is contraindicated
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in patients who are elderly or have heart disease, and other
workup should be performed before considering the Tensilon
test. Intramuscular Prostigmin is longer acting than Tensilon
and allows more time for measurement of changes, but its
absorption rate and hence onset of action are quite variable; its
onset of action is generally between 15 to 20 min and the peak
response occurs about 30 to 40 min after administration. In children the dose is 0.02 mg/kg, always with a total of less than
1.5 mg; and in adults the dose is 1.5 mg, with atropine 0.6 mg,
coadministered.279 Choice of drug can be individualized according to the endpoints that are being assessed and to the ability of
the child to cooperate.
To make a decisive observation, it is important, both before
and after giving these drugs, to quantitate as accurately as possible the function of the affected muscle(s) through measurement of pertinent indicators such as lid height in primary
position, levator function, saccadic velocities, ocular movement,
ocular alignment, and orbicularis strength. After administering
Tensilon, the examiner observes for tearing and lid fasciculations as evidence of cholinergic effect, and draws no conclusion
if a paradoxic decrease in muscle function occurs, because this
may happen in the presence or absence of myasthenia. Positive
responses after either drug are fairly reliable evidence for myasthenia but can, on rare occasions, occur in nonmyasthenic
patients. False-negative responses, however, are common and
therefore do not exclude myasthenia gravis.
Alternatively, a rest test may be used by allowing the patient
to rest with eyes closed for a period of 10 to 15 min.337 An “ice
test” has also been reported to improve ptosis173,278,425 and motility142 after applying an ice pack to the eyes for 2 to 5 min.
However, subsequent report of four patients337 revealed no difference among an ice test, a heat test, or a rest test, so long as
the rest period was at least 10 to 15 min.
Further diagnostic testing may include anti-AChR antibody
titer and electromyography. EMG is particularly useful in generalized myasthenia but is difficult to perform in a frightened,
uncooperative child. The electromyographer looks for a characteristic decrement in the muscle action potentials with
repetitive supramaximal nerve stimulation and for the “jitter
phenomenon” on single muscle fiber studies, difficult responses
to elicit and observe even in a cooperative patient. Anti-AChR
antibody is most helpful in generalized myasthenia as it is
reportedly present in 80% to 90% of those patients but only 50%
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or fewer of ocular myasthenics.149,463,519 According to other
reports, specifically on juvenile myasthenia gravis patients, the
frequency of postive AChR antibody was between 56% and
63%.4,15,19
SYSTEMIC ASSOCIATIONS
Associated immune disorders to be considered in children
include rheumatoid arthritis, juvenile-onset diabetes mellitus,
asthma, and thyroid disease; neoplasia (breast cancer, uterine
cancer, carcinoma of the colon, pinealoma) is also seen.408
Thymoma rarely occurs in children although it is recognized to
accompany 10% of myasthenia gravis.
INHERITANCE
Inheritance is usually sporadic. Approximately 1% to 4% of
cases are familial without a clear Mendelian pattern. This familial predisposition may be due to predilection for autoimmunity
in general.
TREATMENT
Once the ophthalmologist diagnoses or strongly suspects myasthenia, a neurologist generally directs further testing and treatment. The ophthalmologist’s role remains important, however. In
addition to monitoring the motility and lid dysfunction and providing symptomatic relief for these disorders, the ophthalmologist should be alert to the possibility of amblyopia. If not promptly
detected and attended to, amblyopia can be extremely difficult to
treat, particularly when there is sufficient ptosis to necessitate
taping or a ptosis crutch for the lid during occlusion of the sound
eye.
Current therapy aims to increase the amount of acetylcholine available through the use of anticholinesterase agents
or to diminish the autoimmune reaction with corticosteroids,
other immunosuppressive agents, such as azathioprine,
cyclosporin A, and mycophenolate mofetil,93,150 plasmapheresis,
or thymectomy. Supervision of these treatments is clearly in the
bailiwick of the neurologist. It is worth noting that anticholinesterase agents are not as effective in ameliorating ocular
motility as they are for other manifestations of myasthenia149
nor are they as effective as steroids462 or other treatments
directed against the autoimmune response.431 However, because
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of the risks and complications, the use of steroids, immunosuppressives, plasmapheresis, and thymectomy in pure ocular
myasthenia gravis remains controversial.68,365,441 In a recent pilot
study, cyclosporin A was found to be effective in a series of
eight patients, resulting in complete remission in seven of the
eight, with a mean follow-up of 14 months; the eighth patient
was noncompliant.80
Strabismus surgery has been performed on patients with
stable deviations of at least 5 months, using conventional
strabismus surgical techniques.115,360 The presence of systemic
disease is an important consideration in deciding on the method
of anesthesia, although general anesthesia is not an absolute
contraindication when the disease is clinically controlled.
PROGNOSIS
The prognosis for survival, improvement, and remission in a
child with myasthenia gravis is better than that in an adult,
according to most studies.327,408,462 Rodriquez and coworkers408
studied 149 children who were less than 17 years old at the onset
of autoimmune myasthenia gravis and had a median follow-up
of 17 years with minimum follow-up of 4 years. An estimated
80% of these patients were alive at age 40, about 90% of the
survival expected in the general population. Improvement or
remission was seen in 79% of the 85 patients who underwent
thymectomy and 62% of the remaining 64 patients. In the
smaller Toronto series, children required an average of 2 years
on medication before entering remission.340 Complete remission
in adults has been reported as 40% to 70%, generally achieved
after 1 to 3 years of treatment.519
In 9% of children in the Rodriquez series, the disease
remained strictly ocular; this is comparable to the 14% found
in a large adult series observed over a similar interval.183 In
the Toronto series, 38% of the 24 children remained strictly
ocular, although the mean follow-up period was 3.5 years.340
Children with ocular myasthenia gravis may also show
prolonged remissions and respond well to steroid therapy on
relapse.412,437
The result of strabismus surgery for myasthenia gravis has
reportedly been favorable in two studies, after a follow-up of
4 months to 14 years (median, 12 months).115,360 In these two
studies combined, 2 of 10 patients required reoperations, and 1
of the 10 required prisms postoperatively.
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handbook of pediatric strabismus and amblyopia
Botulism
Numerous pharmacological agents and toxins may interfere
with transmission at the neuromuscular junction. The neurotoxin produced by the bacterium Clostridium botulinum irreversibly impedes the intracellular mechanisms responsible
for the release of acetylcholine from the presynaptic nerve
terminals.458
ETIOLOGY
The different neurotoxins produced in botulism exhibit different clinical characteristics. Type E botulism is usually associated with eating seafood; pupillary abnormalities and ptosis may
be seen as early signs. Gastrointestinal symptoms are more
prevalent in type E and type B. The most severe form is type A,
which carries the highest risk for ventilatory support and the
highest mortality.
CLINICAL FEATURES
Children may develop botulism from ingestion of contaminated
food, wound infection, or intestinal infection in infants. Infants usually come to attention because of lethargy, weakness,
feeding difficulty, a feeble cry, and constipation.240 Older children report nausea, vomiting, blurred vision, dysphagia, and
pooling of secretions in the mouth, followed by generalized
weakness and diplopia. In both groups, ophthalmologic findings
are common and may include any type or degree of external
ophthalmoplegia, dilated pupils that react poorly to light, and
ptosis.485
In one outbreak of 27 patients in the U.K., the complaints
were of blurred vision in 78%, drooping lids in 56%, and double
vision in 30%. In this report, 11 of 14 (79%) of reviewed records
revealed sixth nerve palsy and 13 of 14 (93%) revealed accommodative paresis, both of which were early ophthalmic signs.
The severity of ophthalmoparesis was a good indicator of the
overall severity and progression of disease. When there was ventilatory failure, it occurred 12 h after third cranial nerve palsy.457
In another report, it was noted that sixth cranial nerve palsy
may be the initial neurological manifestation of type B botulism.485 In 8 of 11 (73%) of their patients diagnosed with third
nerve palsy, respiratory insufficiency eventually ensued.
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Quivering eye movements on attempted saccades have also
been observed and analyzed on eye movement recordings, consisting of hypometric saccades with subnormal and stuttering
velocities.200
CLINICAL ASSESSMENT
Because botulism may be difficult to distinguish clinically from
Guillain–Barre syndrome,241 pupillary findings, which are rare
in Guillain–Barre, become particularly important. Botulism
may also be mistaken for myasthenia gravis (again, the pupils
are helpful; a Tensilon test may be falsely positive in mild forms
of botulism457), sudden infant death syndrome, and hypothyroidism in infants. In infants, EMG is the primary means of
diagnosis.241
TREATMENT
Treatment is essentially supportive. Antitoxin has been shown
only to shorten the duration of illness in type E botulism, but
is considered in patients with botulism as soon as the diagnosis
is suspected as it can only act before the toxin is irreversibly
bound to its receptor. Adverse reactions to the antitoxin have
been reported in up to 20% of patients. Guanidine, a drug that
enhances release of acetylcholine from the presynaptic nerve terminal, has only a slight effect on limb and ocular muscles and
no effect on respiratory muscles.457
PROGNOSIS
Recovery does not occur until new neuromuscular junctions
are established, a process that may take weeks to months.
The mortality from this condition in the United States has
been reported as 7.5%; this figure is higher in developing
countries.457
DISORDERS OF THE EXTRAOCULAR
MUSCLES
Abnormal extraocular muscles may limit eye movements
through decreased function or through restriction. The pattern
of limitation may simulate neural and neuromuscular disorders
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handbook of pediatric strabismus and amblyopia
FIGURE 12-13. Fibrosis of the extraocular muscles. Severe ptosis (right
photo) and eyes fixed in depression with minimal to no movement typical
of severe fibrosis of the extraocular muscles.
so closely that force ductions, special imaging (echography, CT,
MRI), or even surgical exploration may be necessary for
differentiation.
These disorders may be either congenital or acquired. Congenital anomalies of the extraocular muscles include agenesis,
duplication, abnormal origins and insertions, fascial anomalies,
and fibrous bands.297,500,508,509,529 Congenital absence of one or
more extraocular muscles limits movement of the globe in the
direction of action of the missing muscle(s) and may mimic a
nerve palsy. Indeed, in one series of presumed congenital superior oblique palsies for which a superior oblique tuck was
deemed necessary and attempted, 18% of the patients were
found to have congenital absence of the superior oblique.201 Agenesis and other forms of maldevelopment of the extraocular
muscles have long been recognized and associated with craniofacial anomalies.124,384
At times, certain extraocular muscles mechanically restrict
eye movements from birth, for example, in the congenital fibrosis syndrome (Fig. 12-13) or congenital Brown’s syndrome.
Acquired disorders such as trauma, dysthyroid myopathy,
acquired Brown’s syndrome, and orbital myositis may all cause
weakness or restriction of extraocular muscles. Although investigation of these disorders requires careful attention to the
history and systemic health of the child as well as local ocular
and orbital signs, such advertence is frequently rewarded.
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DISORDERS OF NERVE AND MUSCLE
Kearns–Sayre Syndrome
(Chronic Progressive Ophthalmoplagia)
CLINICAL FEATURES AND NATURAL HISTORY
Ptosis and chronic progressive limitation of eye movements,
usually without diplopia, are features of a variety of disorders.
Among these, Kearns–Sayre syndrome (KSS) is singularly apt to
come to attention in childhood, most often because of ocular
signs. The triad of external ophthalmoplegia, heart block, and
retinal pigmentary degeneration identified in the original
description of KSS256 remains the cornerstone of diagnosis,
although a multitude of associated signs have since been recognized (Table 12-8).
The eye movements in KSS show gradually progressive limitation, which is usually symmetrical and affects all directions
of gaze. Bell’s phenomenon and eye movement responses to
caloric stimulation or head rotation are also slowly lost. Anticholinesterase agents do not improve the range of eye movements. Pupils remain normal. The lids are typically ptotic and
often close weakly because of involvement of the orbicularis
TABLE 12-8. Manifestations of Kearns–Sayre Syndrome.
System
Findings
Cardinal features
Chronic progressive external ophthalmoplegia; degenerative
pigmentary retinopathy; cardiac conduction defects/sudden
death; no family history
Musculoskeletal
Short stature; “ragged-red” fibers by light microscopy of
muscle tissue; skeletal and dental anomalies
Neurological
Elevated CSF protein; deafness; vestibular dysfunction;
cerebellar ataxia; “descending” myopathy of face and
limbs; mild corticospinal tract signs; subnormal
intelligence; demyelinating polyradiculopathy; slowed
electroencephalogram; decreased ventilatory drive/sudden
death; spongiform degeneration of cerebrum and brainstem
Endocrine
Diabetes mellitus; hypogonadism; hypoparathyroidism;
growth hormone deficiency; adrenal dysfunction;
hyperglycemic acidotic coma/death; elevated serum lactate
and pyruvate
Other
Corneal edema; nephropathy
Source: Modified from Glaser JS, Bachynski BN. Infranuclear disorders of eye movement. In: Glaser JS
(ed) Neuro-ophthalmology, 2nd edn. Philadelphia: Lippincott, 1990:402, with permission.166
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handbook of pediatric strabismus and amblyopia
oculi. Indeed, generalized facial weakness is frequent and contributes to a typical facial appearance.
Affected fundi demonstrate a diffuse pigmentary retinopathy that characteristically involves the posterior pole as well
as the periphery and generally consists of a “salt-and-pepper”
pattern of pigment clumping. Commonly both rod and cone
function are reduced on electroretinography,341 and although it
has been noted that only 40% of patients have decreased visual
acuity or night blindness,54 photoreceptor function can diminish insidiously with time.
SYSTEMIC ASSOCIATIONS
Cardiac conduction defects, a cardinal feature of KSS, can be heralded by an interval of enhanced conduction at the A-V node and
may lead to death at any time.88,404 Other systemic associations
include small stature, ataxia, deafness, raised cerebrospinal fluid
protein, diabetes, and hypoparathyroidism (see Table 12-8).
CLINICAL ASSESSMENT
On any patient suspected of KSS, an electrocardiogram is performed. Abnormal blood lactate and pyruvate levels may be
found. On skeletal muscle biopsy, “ragged-red fibers” and abnormal mitochondria are expected. In diagnosing patients suspected
of KSS but with an incomplete constellation of findings, analysis of muscle mtDNA to look for mitochondrial deletions may
be more critical than mitochondrial morphological examination
(see following).178 The brain MRI of patients with KSS may show
normal or atrophied brain, but the characteristic finding is a
combination of high-signal foci in subcortical cerebral white
matter, brainstem, globus pallidus, or thalamus.92
ETIOLOGY
A protracted and shifting debate over the etiology and nosology
of KSS has continued for decades. Early on, chronic progressive
external ophthalmoplegia (CPEO) was considered to be an isolated myopathy of the extraocular muscles, with occasional
weakness of the extremities.260 However, many subsequent
reports described CPEO in conjunction with multisystem
disease, with KSS itself serving as a good example. When spongiform degeneration of the brainstem and cerebrum, which is
observed on neuropathological examination of patients with
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114
KSS, was highlighted,
the neural structures governing eye
movements became suspect. Next, myopathological findings
pointed investigators in yet a different direction. In CPEO, light
microscopy of muscle preparations processed with the modified
Gomori trichrome stain frequently demonstrates “ragged-red”
muscle fibers among normal extraocular muscle fibers, orbicularis oculi fibers, and, at times, other skeletal muscle fibers.
With electron microscopy, these ragged-red fibers as well as
other muscle fibers demonstrate markedly abnormal mitochondria. In KSS, such abnormal mitochondria were detected in a
variety of other tissues as well, including sweat glands,245 liver
cells,174 and cerebellar neurons.438 Experimental infusion of a
chemical that uncouples oxidative phosphorylation produced
reversible ragged-red fibers.318 This morphological evidence combined with biochemical abnormalities indicating mitochondrial
dysfunction led to speculation about the role of mitochondrial
DNA (mtDNA) in the pathogenesis of these disorders.
INHERITANCE
The majority of KSS and CPEO cases are sporadic. In one
review, only a single family demonstrated more than one
person manifesting the entire KSS.420 When small pedigrees
with multiple individuals exhibiting CPEO have been
reported, transmission has generally been maternal and compatible with mitochondrial inheritance,140,223,236 but paternal
transmission of CPEO has also been observed, suggesting a
defective autosomal nuclear gene in some cases.139,140,467
New techniques in molecular biology have triggered an
explosion of studies of mtDNA in patients with KSS and
CPEO.178,334 A significant proportion of these patients show
large-scale heteroplasmic deletions in mtDNA, and these deletions play a pivotal role in the pathogenesis of these disorders.
Heteroplasmy denotes the presence of several different mtDNA
in a cell, some of which may be pathogenic. KSS and CPEO
patients have heteroplasmy in different proportions depending
on the tissue studied222: large-scale deletions of mtDNA have
been observed in muscle of 80% of KSS patients and 70% of
those with CPEO.178 Based on these observations, it has been
suggested that CPEO and KSS are different severities along the
same clinical spectrum.131,178
Another finding that may explain the overlap between the
clinical presentations of KSS and CPEO is that patients with
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handbook of pediatric strabismus and amblyopia
these two diseases have identical mtDNA deletions, but in KSS
they are localized to the muscle and neural tissues, whereas in
CPEO they are localized to muscle. Another disease called
Pearson syndrome also has the identical deletions as in KSS and
CPEO but is localized to the blood. In fact, patients with Pearson
syndrome may develop KSS later in life.
On the other hand, mtDNA duplications have been
observed in KSS but not in CPEO patients,178 a difference that
lends support to the idea that these are two distinct clinical entities, as suggested earlier.54
The severity of disease in patients with mitochondrial deletions apparently depends on a variety of factors: (1) the degree
of heteroplasmy, or the distribution of normal and mutant
mitochondria; (2) the nature of the mitochondrial mutation; (3)
reduction in absolute amounts of normal mtDNA; and (4) a
homoplasmic mutation that leads to a large deletion.178
TREATMENT AND PROGNOSIS
The prognosis for patients with KSS is fair, and treatment is
largely symptomatic. Patients can frequently be managed with
a cardiac pacemaker382 to obviate conducting fibers that, on
pathological study, are fibrotic and infiltrated by fat.156,160
Despite cardiac pacing, patients may die suddenly of inadequate
brainstem ventilatory response to hypoxia.82,104
Abrupt and fatal endocrine dysfunction may also be triggered by steroids,38 and there can be hypersensitivity to agents
used during induction of general anesthesia.233 For many pediatric patients, however, it is the relentless progression of neurological deficits, especially weakness and ataxia, rather than the
possibility of sudden demise, that proves to be particularly
trying.
Preliminary reports suggest that administration of coenzyme Q10, a quinone found in the mitochondrial oxidative
system (with reported doses of 60–120 mg daily for 3 months in
one patient,357 50 mg 3 times a day for 3 months in two others359),
may improve A-V block as well as normalize serum pyruvate
and lactate levels358; improve neurological function without an
effect on the ophthalmoplegia or the electrocardiogram70; and
increase respiratory vital capacity when used with succinate.452
Surgery is generally not recommended for either ptosis or
strabismus in these patients as it is a progressive disease. Surgical correction of ptosis would involve a high risk of exposure
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keratopathy, especially because the eye will lose its Bell’s phenomenon during the course of the disease and corneal wetting
would not occur. Diplopia from strabismus may be treated with
prisms and, as a last resort, monocular occlusion.
Myotonic Dystrophy
Myotonic dystrophy, also known as dystrophia myotonica or
Steinert’s disease, is an autosomal dominant multisystem disorder with variable phenotype. Early investigators focused on
muscle as the primary site of involvement; subsequent studies
revealed that the nervous system231 as well as a variety of other
tissues are affected in addition to the muscles. At least two main
types of myotonic dystrophy exist, termed DM1 and DM2. Two
other described forms, called proximal myotonic myopathy
(PROMM) and proximal myotonic dystrophy (PDM), are closely
linked to the DM2 locus and may be caused by the same genetic
defect with different phenotypic expression.
INCIDENCE
Myotonic dystrophy is considered as one of the most frequent
“dystrophies” in adulthood, with a prevalence of approximately
5 in 100,000 in white European populations.401
ETIOLOGY
The fascinating pathogenesis of DM1 has been described as a
result of various mechanisms.319 The most important factor is
the expanded trinucleotide cytosine-thymidine-guanine (CTG)
repeats in the 3-untranslated region of the disease gene, dystrophia myotonica protein kinase (DMPK) gene, which leads to
decreased DMPK messenger RNA (mRNA) expression and
protein levels. However, DMPK knockout mice showed only
mild muscle weakness and abnormal cardiac conduction. On
further investigation, it was found that the expanded trinucleotide repeat in the mRNA is toxic to the muscle, because
when transgenic mice were developed that express human skeletal actin—unrelated to the DMPK gene—with expanded CTG
repeats in the 3-untranslated region, the mice developed
myotonia and myopathy.304
A significant correlation exists between age of onset and
number of CTG repeats and a general correlation between the
degree of CTG expansion and the severity of disease manifesta-
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handbook of pediatric strabismus and amblyopia
tions. Mildly affected patients have 50 to 150 repeats, classic
DM1 patients have 100 to 1000, and congenital cases may have
more than 2000.319
The exact pathological mechanism remains unclear, but a
theory unifying the protean manifestations of the disease has
been proposed, namely that the fundamental defect is a generalized abnormality of cell membranes.418 Recent evidence supports the hypothesis that DMPK deficiency is associated with
sodium channel abnormality in DM.336
CLINICAL FEATURES AND NATURAL HISTORY
Unlike KSS, ocular motility abnormalities in myotonic dystrophy are commonly subclinical and have been observed for the
most part in adults. A number of authors have described progressive limitation of voluntary eye movements as well as
markedly decreased maximum saccadic velocity and reduced
smooth pursuit gain, but it is not clear whether these eye movement disorders result from a neurological or myopathic defect
or both.14,123,143,290,364,449,484,503 Clinical myotonia, that is, delayed
muscular relaxation, most strikingly affects the limb muscles
(e.g., persistent grip), but may on occasion involve the extraocular muscles134; immediately after sustaining gaze in a certain
direction, the patient cannot promptly move the eyes in the
opposite direction. Bell’s phenomenon is particularly useful to
elicit sustained upgaze in an infant or uncooperative child.
Although the manifestations of myotonic dystrophy usually
become apparent in adolescents or young adults, detailed questioning often documents symptoms during the first decade of
life, and the disease can, at times, affect infants and young children distinctly.127 For the ophthalmologist, a characteristic facial
appearance (facial diplegia, triangular-shaped mouth, and slack
jaw) and weak orbicularis function typically without ptosis suggests the possibility of myotonic dystrophy in a young child.
Bilateral facial weakness is the most characteristic feature of
early-onset myotonic dystrophy and is frequently misdiagnosed
as Möbius syndrome (see following section). With increasing
age, the more familiar facial appearance of myotonic dystrophy
(narrow, expressionless, “hatchet” face with hollowing of cheeks
and temples) evolves because wasting of the facial muscles
occurs, and ptosis becomes far more common.
PROMM, PDM, and DM2 are also autosomal dominant
myotonic dystrophy without the CTG repeat expansion at the
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DM1 locus. PROMM and PDM predominantly involve proximal
muscles, and DM2 involves distal muscles. All three have been
linked to chromosome 3q21.3 and may be various phenotypes
of the same disease. These patients also develop posterior subcapsular cataracts with onset before 50 years of age. They do not
exhibit ophthalmoplegia, however.320
CLINICAL ASSESSMENT
Bilateral iridescent and posterior cortical lens opacities are
useful for establishing a clinical diagnosis27; they may be identified in young children but are often not seen until the teenage
years. Clear electroretinographic abnormalities with normalappearing fundi may be observed early on,69 and a subgroup of
patients demonstrate visual loss and observable pigmentary
retinopathy later in the course of the disease. Additional ophthalmic signs are listed in Table 12-9.37 A negative family history
does not exclude the diagnosis because a parent with myotonic
dystrophy may be affected so mildly as to be unaware of it.374
Careful evaluation of the parents can therefore prove helpful.
Beside the slit lamp examination for cataracts, other primary
diagnostic tests include DNA testing for an enlarged CTG
repeat, examination for muscle and nonmuscle manifestations,
and EMG for subclinical myotonia. Secondary tests include
serum creatinine kinase, which is often mildly elevated in
TABLE 12-9. Ophthalmic Manifestations of Myotonic Dystrophy.
Structure
Findings
Eyelids
Ptosis; myotonic lag (due to delayed relaxation of levator);
orbicularis weakness; myotonic closure (due to delayed
relaxation of orbicularis)
Motility
Slow saccades with full ductions and versions; myotonia induced
by Bell’s reflex, convergence, or eccentric gaze; partial to
complete ophthalmoplegia (usually symmetrical)
Globe
Cataracts (subcapsular polychromatophilic opacities; posterior
cortical spokes; posterior subcapsular plaques; mature
cataracts); short depigmented ciliary processes; hypotony; iris
neovascular tufts (resulting in spontaneous hyphema); keratitis
sicca; macular and peripheral retinal pigmentary degeneration;
miotic, sluggishly reacting pupils
Miscellaneous
Decreased ERG responses; elevated dark-adaptation thresholds;
generalized constriction of visual fields
Source: From Ref. 37, with permission.
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handbook of pediatric strabismus and amblyopia
diseased individuals, and muscle biopsy, which frequently shows
an increase in central nuclei, fiber atrophy, and ringed fibers.
INHERITANCE
The interesting feature of this disease is that when it is passed
on from one generation to the next in autosomal dominant
fashion, the severity of disease increases. The phenomenon of
progressive earlier onset and greater severity of disease is termed
anticipation; this is particularly true for cases of female transmission, which can lead to the congenital cases of the disease.
Increased severity in the subsequent generations is associated
with increased expansion of the CTG repeats.303
DM1 gene has been mapped to chromosome 19q13.3. DM2,
PROMM, and PDM have all been linked to chromosome 3q21.3,
but the gene defect(s) has not yet been identified.320
SYSTEMIC ASSOCIATIONS
In addition to facial diplegia, infants frequently demonstrate
hypotonia, delayed motor and intellectual development, feeding
difficulties, neonatal respiratory distress, and talipes.192 In
adults, diabetes, pituitary dysfunction, widespread involvement
of the smooth muscle of the gastrointestinal tract, premature
balding, and gonadal atrophy may all be seen.
TREATMENT AND PROGNOSIS
Comprehensive medical care of patients with myotonic dystrophy is essential. Prompt intervention may become necessary at
any time because of associated, potentially life-threatening,
cardiac conduction defects. Periodic EKGs are obtained to detect
heart block, which may require a pacemaker. Drugs such as procainamide, quinine, and propranolol are avoided in patients with
cardiac involvement. Endocrinological management is necessary for those patients who also have diabetes or pituitary
dysfunction.
Prostheses may be used for foot and hand weakness. Myotonia may be moderately reduced with mexiletine and tocainide,
which have been found to be more effective than phenytoin and
dysopyramide.
Any strabismus surgery for myotonic dystrophy patients is
approached with caution because of the potential for friable and
atrophic extraocular muscles.306 Also any ptosis surgery risks
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489
corneal exposure due to lack of Bell’s phenomenon in the setting
of ophthalmoplegia.
Life expectancy is reduced particularly in the case of early
onset disease and proximal muscle involvement. The high mortality rate is due to an increase in deaths from respiratory diseases, cardiovascular diseases, and neoplasms, as well as sudden
deaths from cardiac arrhythmias.320
Möbius Syndrome
Möbius328,329 designated congenital, bilateral sixth and seventh
nerve palsies as central features of what has come to be known
as Möbius’ syndrome, but subsequent clinical and pathological
observations reveal greater complexity. It has become clear that
the eponym has been applied to a heterogeneous group of congenital neuromuscular disorders that produce facial weakness in
some combination with a variety of other findings (Table 12-10).
It has been suggested that the term sequence is more appropriate because a sequence defines a cascade of secondary events
after an embryonic insult from heterogeneous causes.325
Clinical Features and Systemic Associations
Typically, a short time after birth, an affected infant demonstrates difficulty feeding because of poor sucking and little, if
TABLE 12-10. Manifestations of Möbius Syndrome.
System
Findings
Cardinal features
Partial or complete facial paralysis, usually bilateral (may be
unilateral)203,324
Straight eyes, esotropia, or exotropia with no horizontal
movements and preserved vertical movements324,407,461; total
ophthalmoplegia206,324,464; cocontraction of horizontal recti61
Unilateral or bilateral palsy of cranial nerves V, VIII, IX, X, or
XII42,475; autism325
Abnormal tongue; bifid uvula; cleft lip/palate; micrognathia,
microstomia; external ear defects324,325
Syndactyly; brachydactyly; absent or supranumerary digits;
arthrogryposis multiplex congenital; talipes; absence of
hands or feet324,325,409,461
Mental retardation325; congenital heart defects; absent sternal
head of the pectoralis major (second major component of
the Poland anomaly)324,325; rib defects; Klippel–Feil anomaly;
neuroradiologic cerebellar hypoplasia51,190; hypogonadotropic
hypogonadism with or without anosmia362,422
Ocular motor
Neurological
Orofacial
Musculoskeletal
Miscellaneous
490
handbook of pediatric strabismus and amblyopia
any, facial expression, as a result of the involvement of cranial
nerves IX and XII in addition to VII. Generally, horizontal eye
movements are clearly abnormal, and vertical eye movements
are preserved. If convergence is intact and used for crossfixation, the ocular motility pattern may resemble that produced by bilateral sixth nerve palsies. On occasion, vertical eye
movements may also be affected or total ophthalmoplegia
may occur. Crocodile tears, micrognathia, dental anomalies,
cleft palate, facial asymmetry, limb malformations, Poland’s
syndrome, epilepsy, mental retardation, and autism may be
present.325
Etiology
Fifteen autopsied cases have been classified into four groups
based on neuropathological findings in the brainstem.489 Group
I demonstrated absence or hypoplasia of relevant cranial nerve
nuclei; group II, in addition to neuronal loss, showed evidence
of neuronal degeneration suggesting peripheral nerve injury;
group III, in addition to neuronal loss and neuronal generation,
had frank necrosis of the tegmentum of the lower pons; group
IV revealed no abnormalities in the brainstem and may represent a purely myopathic disorder. Cases of facio-scapulohumeral muscular dystrophy and congenital centronuclear
(myotubular) myopathy that clinically mimic Möbius syndrome would also presumably belong to group IV.189,199
A number of investigators have speculated that disruption
of the vascular system causes hypoxia of vulnerable tissues
between 4 and 7 weeks gestation.190,294,396 It has been proposed
that Möbius syndrome, the Poland anomaly, and the
Klippel–Feil defect all result from a transient interruption during
the sixth week of gestation in the development of the subclavian artery and its branches, including the basilar, vertebral, and
internal thoracic arteries, which supply the brain, neck, pectoral
muscles, and upper limbs; in addition, in Möbius syndrome, the
primitive trigeminal artery that supplies the hindbrain during
fetal life may regress before the establishment of adequate perfusion from the vertebral or basilar artery and thereby disturb
development of the cranial nerve nuclei.48 Such a mechanism
would be consistent with the brainstem necrosis seen in group
III Möbius’ syndrome patients but would not account for the
findings in groups I and II.
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491
Inheritance
As might be expected, most reported cases have been sporadic,
and the sexes are affected with equal frequency. At least five
families with Möbius’ syndrome have been reported without
any one consistent chromosomal defect.206,283,325,531 Chromosomal translocations (1;13 and 1;11), chromosome 13q12.2 deletion, and linkage to chromosome 3q21–22 have been reported by
previous authors. The recurrence risk to siblings of isolated
cases with these three manifestations appears to be less than
2%.42
Treatment and Prognosis
Depending on the severity and types of malformations, the treatment will vary.325 Initially, sucking problems often require modification in type of bottle used. If lid lag is present from seventh
nerve palsy, lubricants are necessary. Refractive errors, amblyopia, and strabismus often need attention.
Maximal medial rectus recessions with or without vertical
displacement have been shown to suffice in some cases,466,516
whereas
others
have
advocated
horizontal
recessresections321,346,490 or vertical muscle transposition.206,470
Because of the lack of facial expression, parents and children
may have psychological difficulty with bonding and social
communication. Plastic surgeries do exist that can improve
facial movement.81,543 Finally, helping families cope by contacting others through a national organization, such as the Möbius
Syndrome Foundation, is also important and appreciated, as is
the case for other diseases or syndromes mentioned in this
chapter.
References
1. Abdul-Rahim AS, et al. Cryptogenic oculomotor nerve palsy. The
need for repeated neuroimaging studies. Arch Ophthalmol 1989;
107(3):387–390.
2. Afifi AK, et al. Recurrent lateral rectus palsy in childhood. Pediatr
Neurol 1990;6(5):315–318.
3. Afifi AK, Bell WE, Menezes AH. Etiology of lateral rectus palsy in
infancy and childhood. J Child Neurol 1992;7(3):295–299.
4. Afifi AK, Bell WE. Tests for juvenile myasthenia gravis: comparative
diagnostic yield and prediction of outcome. J Child Neurol 1993;
8(4):403–411.
492
handbook of pediatric strabismus and amblyopia
5. Aguirre-Aquino BI, Rogers DG, Traboulsi EI. A patient with de
Morsier and Duane syndromes. J Am Assoc Pediatr Ophthalmol
Strabismus 2000;4(4):243–245.
6. Ahn JC, Hoyt WF, Hoyt CS. Tonic upgaze in infancy. A report of
three cases. Arch Ophthalmol 1989;107(1):57–58.
7. Aicardi J, et al. Ataxia-ocular motor apraxia: a syndrome mimicking
ataxia-telangiectasia. Ann Neurol 1988;24(4):497–502.
8. Al-Din AN, et al. Brainstem encephalitis and the syndrome of Miller
Fisher: a clinical study. Brain 1982;105(pt 3):481–495.
9. Aldrich MS, Beck RW, Albers JW. Familial recurrent Bell’s palsy with
ocular motor palsies. Neurology 1987;37(8):1369–1371.
10. Aleksic S, et al. Congenital ophthalmoplegia in oculoauriculovertebral dysplasia-hemifacial microsomia (Goldenhar–Gorlin syndrome).
A clinicopathologic study and review of the literature. Neurology
1976;26(7):638–644.
11. Alfano J. Spasm of fixation. Am J Ophthalmol 1955;40:724–725.
12. Alvarez F, et al. Nervous and ocular disorders in children with
cholestasis and vitamin A and E deficiencies. Hepatology 1983;3(3):
410–414.
13. Amit R, Benezra D. Oculomotor ophthalmoplegic migraine in an
infant. Headache 1987;27(7):390–391.
14. Anastasopoulos D, et al. Abnormalities of ocular motility in
myotonic dystrophy. Brain 1996;119(pt 6):1923–1932.
15. Andrews PI, Massey JM, Sanders DB. Acetylcholine receptor antibodies in juvenile myasthenia gravis. Neurology 1993;43(5):977–982.
16. Andrews PI, et al. Race, sex, and puberty influence onset, severity,
and outcome in juvenile myasthenia gravis. Neurology 1994;44(7):
1208–1214.
17. Angelini L, et al. Hallervorden–Spatz disease: clinical and MRI study
of 11 cases diagnosed in life. J Neurol 1992;239(8):417–425.
18. Anlar B, et al. Myasthenia gravis in childhood. Acta Paediatr
1996;85(7):838–842.
19. Anlar B. Juvenile myasthenia: diagnosis and treatment. Paediatr
Drugs 2000;2(3):161–169.
20. Appukuttan B, et al. Localization of a gene for Duane retraction
syndrome to chromosome 2q31. Am J Hum Genet 1999;65(6):1639–
1646.
21. Araie M, Ozawa T, Awaya Y. A case of congenital ocular motor
apraxia with cerebellospinal degeneration. Jpn J Ophthalmol 1977;
21:355–365.
22. Armstrong MW, Mountain RE, Murray JA. Treatment of facial synkinesis and facial asymmetry with botulinum toxin type A following
facial nerve palsy. Clin Otolaryngol 1996;21(1):15–20.
23. Arnold AC, et al. Internuclear ophthalmoplegia in the Chiari type II
malformation. Neurology 1990;40(12):1850–1864.
24. Aroichane M, Repka MX. Outcome of sixth nerve palsy or paresis
in young children. J Pediatr Ophthalmol Strabismus 1995;32(3):152–
156.
chapter
12:
ocular motility disorders
493
25. Asbury AK, Arnason BG, Adams RD. The inflammatory lesion in
idiopathic polyneuritis. Its role in pathogenesis. Medicine (Baltim)
1969;48(3):173–215.
26. Aseff AJ, Munoz M. Outcome of surgery for superior oblique palsy
with contracture of ipsilateral superior rectus treated by superior
rectus recession. Binoc Vs Strabismus Q 1998;13(3):177–180.
27. Ashizawa T, et al. Diagnostic value of ophthalmologic findings in
myotonic dystrophy: comparison with risks calculated by haplotype
analysis of closely linked restriction fragment length polymorphisms. Am J Med Genet 1992;42(1):55–60.
28. Astle WF, Rosenbaum AL. Familial congenital fourth cranial nerve
palsy. Arch Ophthalmol 1985;103(4):532–535.
29. Astle WF, Miller SJ. Acute comitant esotropia: a sign of intracranial
disease. Can J Ophthalmol 1994;29(3):151–154.
30. Atwal AJ, Smith BH, Dickenson ES. Letter: Pseudo-internuclear ophthalmoplegia in polyneuritis. Arch Neurol 1976;33(6):457.
31. Avanzini G, et al. Oculomotor disorders in Huntington’s chorea.
J Neurol Neurosurg Psychiatry 1979;42(7):581–589.
32. Averbuch-Heller L, Leigh RJ. Eye movements. Curr Opin Neurol
1996;9(1):26–31.
33. Awan K. Duane’s retraction syndrome and hypertelorism. J Pediatr
Ophthalmol Strabismus 1975;12:100–102.
34. Awan K. Flocculi iridis and retraction syndrome: their coexistence
and associated ocular anomalies. J Pediatr Ophthalmol Strabismus
1975;12:246–254.
35. Awan KJ. Association of ocular, cervical, and cardiac malformations.
Ann Ophthalmol 1977;9(8):1001–1011.
36. Awaya Y, Sugie H, Fukuyama Y. A hereditary variant of spinocerebellar degeneration associated with choreoathetosis and ocular
motor apraxia of early onset. Acta Paediatr Jpn 1986;28:271–272.
37. Babel J. Ophthalmological aspects of myotonic dystrophy. In: Huber
A, Klein D (eds) Neurogenetics and neuro-ophthalmology. Amsterdam: Elsevier/North Holland, 1981.
38. Bachynski BN, et al. Hyperglycemic acidotic coma and death in
Kearns–Sayre syndrome. Ophthalmology 1986;93(3):391–396.
39. Bailey PBD, Ducy PC. Intracranial tumors in infancy and childhood.
Chicago: University of Chicago Press, 1939.
40. Bailey TD, et al. Ophthalmoplegic migraine. J Clin Neuroophthalmol 1984;4(4):225–228.
41. Balkan R, Hoyt CS. Associated neurologic abnormalities in
congenital third nerve palsies. Am J Ophthalmol 1984;97(3):315–
319.
42. Baraitser M. Genetics of Mobius syndrome. J Med Genet 1977;14(6):
415–417.
43. Barlow C. Headaches and migraine in childhood. Philadelphia:
Lippincott, 1984.
44. Barsoum–Homsy M. Congenital double elevator palsy. J Pediatr
Ophthalmol Strabismus 1983;20(5):185–191.
494
handbook of pediatric strabismus and amblyopia
45. Bartkowski SB, et al. Marcus Gunn jaw-winking phenomenon: management and results of treatment in 19 patients. J Craniomaxillofac
Surg 1999;27(1):25–29.
46. Barton JJ. Quantitative ocular tests for myasthenia gravis: a comparative review with detection theory analysis. J Neurol Sci 1998;
155(1):104–114.
47. Barton JJ, Fouladvand M. Ocular aspects of myasthenia gravis. Semin
Neurol 2000;20(1):7–20.
48. Bavinck JN, Weaver DD. Subclavian artery supply disruption
sequence: hypothesis of a vascular etiology for Poland, Klippel–Feil,
and Mobius anomalies. Am J Med Genet 1986;23(4):903–918.
49. Beck RW, Meckler RJ. Internuclear ophthalmoplegia after head
trauma. Ann Ophthalmol 1981;13(6):671–675.
50. Becker WJ, Watters GV, Humphreys P. Fisher syndrome in childhood.
Neurology 1981;31(5):555–560.
51. Beerbower J, et al. Radiographic findings in Moebius and Moebius-like
syndromes. AJNR Am J Neuroradiol 1986;7(2):364–365.
52. Bell JA, Fielder AR, Viney S. Congenital double elevator palsy in
identical twins. J Clin Neuroophthalmol 1990;10(1):32–34.
53. Benson P. Transient unilateral external rectus muscle in newborn
infants. Br Med J 1962;1:1054–1055.
54. Berenberg RA, et al. Lumping or splitting? “Ophthalmoplegia-plus”
or Kearns–Sayre syndrome? Ann Neurol 1977;1(1):37–54.
55. Betz R, et al. Children with ocular motor apraxia type Cogan carry
deletions in the gene (NPHP1) for juvenile nephronophthisis. J
Pediatr 2000;136(6):828–831.
56. Beutler E, Grabowski G. Gaucher disease. In: Scriver C, et al (eds)
The metabolic and molecular bases of inherited disease. New York:
McGraw-Hill, 1995:2641–2670.
57. Beyer–Machule C, et al. The Marcus–Gunn phenomenon: a review
of 80 cases (an update). Orbit 1985;4:15–19.
58. Biedner B, Geltman C, Rothkoff L. Bilateral Duane’s syndrome associated with crocodile tears. J Pediatr Ophthalmol Strabismus 1979;
16(2):113–114.
59. Bielschowsky A. Lectures on motor anomalies of the eyes. II. Paralysis
of individual muscles. Arch Ophthalmol 1935;13:33–59.
60. Bixenman WW, von Noorden GK. Benign recurrent VI nerve
palsy in childhood. J Pediatr Ophthalmol Strabismus 1981;18(3):
29–34.
61. Blodi FC. Electromyographic evidence for supranuclear gaze palsies.
Trans Ophthalmol Soc UK 1970;90:451–469.
62. Bloom JN, Graviss ER, Mardelli PG. A magnetic resonance imaging
study of the upshoot-downshoot phenomenon of Duane’s retraction
syndrome. Am J Ophthalmol 1991;111(5):548–554.
63. Bodensteiner JB, et al. Macrocerebellum: neuroimaging and clinical
features of a newly recognized condition. J Child Neurol 1997;12(6):
365–368.
chapter
12:
ocular motility disorders
495
64. Bodziner RA, Singer W, Hedges TR. Bilateral internuclear ophthalmoplegia in meningoencephalitis. Dev Med Child Neurol 1983;
25(6):819–820.
65. Boger WP, et al. Recurrent isolated sixth nerve palsy in children. Ann
Ophthalmol 1984;16(3):237–238, 240–244.
66. Boghen D, et al. Primary aberrant third nerve regeneration. Ann
Neurol 1979;6(5):415–418.
67. Borchert MS, et al. Congenital ocular motor apraxia in twins. Findings with magnetic resonance imaging. J Clin Neuroophthalmol
1987;7(2):104–107.
68. Bowen J, Daltner C, Troost B. The treatment of ocular myasthenia
with plasmapheresis: three case reports. Neuro-Ophthalmology
1986;6:109–112.
69. Breningstall GN, Smith SA, Purple RL. Electroretinography in the
evaluation of childhood myotonic dystrophy. Pediatr Neurol 1985;
1(4):238–241.
70. Bresolin N, et al. Clinical and biochemical correlations in mitochondrial myopathies treated with coenzyme Q10. Neurology 1988;
38(6):892–899.
71. Brodsky MC, Frenkel RE, Spoor TC. Familial intracranial aneurysm
presenting as a subtle stable third nerve palsy. Case report. Arch
Ophthalmol 1988;106(2):173.
72. Brodsky MC, Pollock SC, Buckley EG. Neural misdirection in congenital ocular fibrosis syndrome: implications and pathogenesis. J
Pediatr Ophthalmol Strabismus 1989;26(4):159–161.
73. Brodsky MC. Hereditary external ophthalmoplegia synergistic divergence, jaw winking, and oculocutaneous hypopigmentation: a congenital fibrosis syndrome caused by deficient innervation to
extraocular muscles. Ophthalmology 1998;105(4):717–725.
74. Buckley SA, Elston JS. Surgical treatment of supranuclear and internuclear ocular motility disorders. Eye 1997;11(pt 3):377–380.
75. Burian H, Miller J. Comitant convergent strabismus with acute
onset. Am J Ophthalmol 1968;45:55–64.
76. Butler T. Third nerve paralysis after mumps and chicken-pox. Br
Med J 1930;1:1095.
77. Butler T. Ocular paralysis after mumps. Br Med J 1937;1:752–
753.
78. Caccavale A, Mignemi L. Acute onset of a bilateral areflexical mydriasis in Miller–Fisher syndrome: a rare neuro-ophthalmologic disease.
J Neuroophthalmol 2000;20(1):61–62.
79. Calabrese G, et al. Detection of an insertion deletion of region
8q13–q21.2 in a patient with Duane syndrome: implications for
mapping and cloning a Duane gene. Eur J Hum Genet 1998;6(3):
187–193.
80. Calvert P. Personal communication, 2001.
81. Carr MM, Ross DA, Zuker RM. Cranial nerve defects in congenital
facial palsy. J Otolaryngol 1996;26(2):80–87.
496
handbook of pediatric strabismus and amblyopia
82. Carroll JE, et al. Depressed ventilatory response in oculocraniosomatic neuromuscular disease. Neurology 1976;26(2):140–146.
83. Cassidy L, Taylor D, Harris C. Abnormal supranuclear eye movements in the child: a practical guide to examination and interpretation. Surv Ophthalmol 2000;44(6):479–506.
84. Catalano RA, Sax RD, Krohel GB. Unilateral internuclear ophthalmoplegia after head trauma. Am J Ophthalmol 1986;101(4):491–493.
85. Catalano RA, et al. Asymmetry in congenital ocular motor apraxia.
Can J Ophthalmol 1988;23(7):318–321.
86. Chan CC, Sogg RL, Steinman L. Isolated oculomotor palsy after
measles immunization. Am J Ophthalmol 1980;89(3):446–448.
87. Chan TK, Demer JL. Clinical features of congenital absence of the
superior oblique muscle as demonstrated by orbital imaging. J Am
Assoc Pediatr Ophthalmol Strabismus 1999;3(3):143–150.
88. Charles R, et al. Myocardial ultrastructure and the development of
atrioventricular block in Kearns–Sayre syndrome. Circulation 1981;
63(1):214–219.
89. Chattha AS, Delong GF. Sylvian aqueduct syndrome as a sign of
acute obstructive hydrocephalus in children. J Neurol Neurosurg
Psychiatry 1975;38(3):288–296.
90. Christodoulou K, et al. Mapping of the familial infantile myasthenia (congenital myasthenic syndrome type Ia) gene to chromosome
17p with evidence of genetic homogeneity. Hum Mol Genet 1997;
6(4):635–640.
91. Christoff N. A clinicopathologic study of vertical eye movements.
Arch Neurol 1974;31(1):1–8.
92. Chu BC, et al. MRI of the brain in the Kearns–Sayre syndrome: report
of four cases and a review. Neuroradiology 1999;41(10):759–764.
93. Ciafaloni E, et al. Mycophenolate mofetil for myasthenia gravis: an
open-label pilot study. Neurology 2001;56(1):97–99.
94. Clausen N, Andersson P, Tommerup N. Familial occurrence
of neuroblastoma, von Recklinghausen’s neurofibromatosis,
Hirschsprung’s agangliosis and jaw-winking syndrome. Acta Paediatr Scand 1989;78(5):736–741.
95. Cogan D. Neurology of the ocular muscles. Springfield: Thomas, 1948.
96. Cogan D. A type of congenital ocular motor apraxia presenting jerky
head movement. Trans Am Acad Ophthalmol Otolaryngol 1952;
56:853–862.
97. Cogan D, et al. A long-term follow-up of congenital ocular motor
apraxia: case report. Neuroophthalmology 1980;1:145–147.
98. Cogan DG. Congenital ocular motor apraxia. Can J Ophthalmol
1966;1(4):253–260.
99. Cogan DG. Internuclear ophthalmoplegia, typical and atypical. Arch
Ophthalmol 1970;84(5):583–589.
100. Cogan DG, et al. Ocular motor signs in some metabolic diseases.
Arch Ophthalmol 1981;99(10):1802–1808.
101. Cooper J, et al. Accommodative and vergence findings in ocular
myasthenia: a case analysis. J Neuroophthalmol 2000;20(1):5–11.
chapter
12:
ocular motility disorders
497
102. Coppeto JR, Lessell S. Dorsal midbrain syndrome from giant
aneurysm of the posterior fossa: report of two cases. Neurology
1983;33(6):732–736.
103. Couchot J, et al. Guillain–Barre syndrome following varicella. Nouv
Presse Med 1978;7(1):47.
104. Coulter DL, Allen RJ. Abrupt neurological deterioration in children
with Kearns–Sayre syndrome. Arch Neurol 1981;38(4):247–250.
105. Cox TA, Wurster JB, Godfrey WA. Primary aberrant oculomotor
regeneration due to intracranial aneurysm. Arch Neurol 1979;36(9):
570–571.
106. Cross HE, Pfaffenbach DD. Duane’s retraction syndrome and associated congenital malformations. Am J Ophthalmol 1972;73(3):442–450.
107. Cruysberg J, et al. Bilateral Duane’s syndrome associated with congenital panhypopituitarism. Neuro-Ophthalmology 1986;3:165–168.
108. Cruysberg J, Huygen P. Congenital monocular adduction palsy
with synergistic divergence diagnosed in a young infant. NeuroOphthalmology 1990;10:253–256.
109. Cruysberg JR, et al. Congenital adduction palsy and synergistic
divergence: a clinical and electro-oculographic study. Br J Ophthalmol 1989;73(1):68–75.
110. Cuneo HMRC. Brain tumors of childhood. Springfield: Thomas, 1952.
111. Currie J, Lubin JH, Lessell S. Chronic isolated abducens paresis from
tumors at the base of the brain. Arch Neurol 1983;40(4):226–229.
112. Dagi LR, Chrousos GA, Cogan DC. Spasm of the near reflex associated with organic disease. Am J Ophthalmol 1987;103(4):582–585.
113. Daroff R, Hoyt W. Supranuclear disorders of ocular control systems
in man: clinical, anatomical, and physiological correlations. In:
Bach-y-Rita P, Collins C, Hyde J (eds) The control of eye movements.
New York: Academic Press, 1971.
114. Daroff RB, et al. Spongiform encephalopathy with chronic progressive external ophthalmoplegia. Central ophthalmoplegia mimicking
ocular myopathy. Neurology 1966;16(2):161–169.
115. Davidson JL, Rosenbaum AL, McCall LC. Strabismus surgery in
patients with myasthenia. J Pediatr Ophthalmol Strabismus 1993;
30(5):292–295.
116. Davis TL, Lavin PJ. Pseudo one-and-a-half syndrome with ocular
myasthenia. Neurology 1989;39(11):1553.
117. De Graaf J, Cats H, deJager A. Gradenigo’s syndrome: a rare complication of otitis media. Clin Neurol Neurosurg 1988;90:237–239.
118. de la Monte SM, et al. Keyhole aqueduct syndrome. Arch Neurol
1986;43(9):926–929.
119. Dehaene I, et al. Guillain–Barre syndrome with ophthalmoplegia:
clinicopathologic study of the central and peripheral nervous
systems, including the oculomotor nerves. Neurology 1986;36(6):
851–854.
120. Denslow GT, Sims M. Duane’s retraction syndrome associated with
optic nerve hypoplasia. J Pediatr Ophthalmol Strabismus 1980;17(1):
26–28.
498
handbook of pediatric strabismus and amblyopia
121. Derakhshan I, Lotfi J, Kaufman B. Ophthalmoplegia, ataxia and
hyporeflexia (Fisher’s syndrome). With a midbrain lesion demonstrated by CT scanning. Eur Neurol 1979;18(6):361–366.
122. DeRespinis PA, et al. Duane’s retraction syndrome. Surv Ophthalmol 1993;38(3):257–288.
123. Di Costanzo A, et al. Relative sparing of extraocular muscles in
myotonic dystrophy: an electrooculographic study. Acta Neurol
Scand 1997;95(3):158–163.
124. Diamond GR, et al. Variations in extraocular muscle number and
structure in craniofacial dysostosis. Am J Ophthalmol 1980;90(3):
416–418.
125. Diamond S, Schear HE, Leeds MF. Pseudo-internuclear oculomotor
ophthalmoplegia secondary to Guillain–Barre polyneuronitis simulating myasthenia gravis in a air transport pilot. Aviat Space Environ
Med 1975;46(2):204–207.
126. Discepola MJ, et al. Autosomal recessive Duane’s retraction syndrome. Can J Ophthalmol 1987;22(7):384–386.
127. Dodge P, et al. Myotonic dystrophy in infancy and childhood.
Pediatrics 1965;35:3–19.
128. Donahue SP, Lavin PJ, Hamed LM. Tonic ocular tilt reaction simulating a superior oblique palsy: diagnostic confusion with the 3-step
test. Arch Ophthalmol 1999;117(3):347–352.
129. Donaldson MD, et al. Familial juvenile nephronophthisis, Jeune’s
syndrome, and associated disorders. Arch Dis Child 1985;60(5):426–
434.
130. Drachman D. Myasthenia gravis: immunobiology of a receptor disorder. Trends Neurosci 1983;6:446–450.
131. Drachman DA. Ophthalmoplegia plus. The neurodegenerative disorders associated with progressive external ophthalmoplegia. Arch
Neurol 1968;18(6):654–674.
132. Duffner PK, et al. Survival of children with brain tumors: SEER
Program, 1973–1980. Neurology 1986;36(5):597–601.
133. Durkan GP, et al. Recurrent painless oculomotor palsy in children.
A variant of ophthalmoplegic migraine? Headache 1981;21(2):58–62.
134. Dyken P. Extraocular myotonia in families with dystrophia myotonica. Neurology 1966;16:738–740.
135. Ebner R. Angiography for IIIrd nerve palsy in children. J Clin
Neuroophthalmol 1990;10(2):154–155.
136. Echaniz-Laguna A, et al. The Miller Fisher syndrome: neurophysiological and MRI evidence of both peripheral and central origin in one
case. J Neurol 2000;247(12):980–982.
137. Eda I, et al. Computed tomography in congenital ocular motor
apraxia. Neuroradiology 1984;26(5):359–362.
138. Edis RH, Mastaglia FL. Vertical gaze palsy in barbiturate intoxication. Br Med J 1977;1(6054):144.
139. Egger J, Lake BD, Wilson J. Mitochondrial cytopathy. A multisystem
disorder with ragged red fibres on muscle biopsy. Arch Dis Child
1981;56(10):741–752.
chapter
12:
ocular motility disorders
499
140. Egger J, Wilson J. Mitochondrial inheritance in a mitochondrially
mediated disease. N Engl J Med 1983;309(3):142–146.
141. Elizan TS, et al. Syndrome of acute idiopathic ophthalmoplegia with
ataxia and areflexia. Neurology 1971;21(3):281–292.
142. Ellis FD, et al. Extraocular muscle responses to orbital cooling (ice
test) for ocular myasthenia gravis diagnosis. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(5):271–281.
143. Emre M, Henn V. Central eye movement disorder in a case of
myotonic dystrophy. Neuro-Ophthalmology 1985;5:21–25.
144. Engel A, et al. Molecular basis of congenital myasthenic syndromes:
mutations in the acetylcholine receptor. Neuroscientist 1998;4:185–
194.
145. Engel AG, et al. A newly recognized congenital myasthenic syndrome attributed to a prolonged open time of the acetylcholineinduced ion channel. Ann Neurol 1982;11(6):553–569.
146. Engel AG. Congenital myasthenic syndromes. J Child Neurol 1988;
3(4):233–246.
147. Eustace P, et al. Congenital ocular motor apraxia: an inability to
unlock the vestibulo-ocular reflex. Neuro-Ophthalmology 1994;4:
167–174.
148. Evans JC, et al. Confirmation of linkage of Duane’s syndrome and
refinement of the disease locus to an 8.8-cM interval on chromosome 2q31. Hum Genet 2000;106(6):636–638.
149. Evoli A, et al. Ocular myasthenia: diagnostic and therapeutic problems. Acta Neurol Scand 1988;77(1):31–35.
150. Evoli A, et al. Therapeutic options in ocular myasthenia gravis.
Neuromusc Disord 2001;11(2):208–216.
151. Fenichel GM. Clinical syndromes of myasthenia in infancy and
childhood. A review. Arch Neurol 1978;35(2):97–103.
152. Fernandez E, et al. Oculomotor nerve regeneration in rats. Functional, histological, and neuroanatomical studies. J Neurosurg 1987;
67(3):428–437.
153. Fielder AR, et al. Congenital ocular motor apraxia. Trans Ophthalmol Soc UK 1986;105(pt 5):589–598.
154. Fink JK, et al. Clinical spectrum of Niemann–Pick disease type C.
Neurology 1989;39(8):1040–1049.
155. Fisher C. An unusual variant of acute idiopathic polyneuritis (syndrome of ophthalmoplegia, ataxia, and areflexia). N Engl J Med
1956;255:57–65.
156. Flynn JT, et al. Hyperglycemic acidotic coma and death in Kearns–
Sayre syndrome. Trans Am Ophthalmol Soc 1985;83:131–161.
157. Fox A. Angiography for third nerve palsy in children. J Clin
Neuroophthalmol 1989;9:37–38.
158. Gabianelli EB, Klingele TB, Burde RM. Acute oculomotor nerve
palsy in childhood. Is arteriography necessary? J Clin Neuroophthalmol 1989;9(1):33–36.
159. Galetta SL, Smith JL. Chronic isolated sixth nerve palsies. Arch
Neurol 1989;46(1):79–82.
500
handbook of pediatric strabismus and amblyopia
160. Gallastegui J, et al. Cardiac involvement in the Kearns–Sayre syndrome. Am J Cardiol 1987;60(4):385–388.
161. Gay A, Brodkey J, Miller J. Convergence retraction nystagmus. Arch
Ophthalmol 1963;70:456–461.
162. Gentile M, et al. COACH syndrome: report of two brothers with congenital hepatic fibrosis, cerebellar vermis hypoplasia, oligophrenia,
ataxia, and mental retardation. Am J Med Genet 1996;64(3):514–520.
163. Giroud M, et al. Miller–Fisher syndrome and pontine abnormalities
on MRI: a case report. J Neurol 1990;237(8):489–490.
164. Gittinger JW Jr, Sokol S. The visual-evoked potential in the diagnosis of congenital ocular motor apraxia. Am J Ophthalmol 1982;
93(6):700–703.
165. Gittinger JW Jr, Hughes JP, Suran EL. Medial orbital wall blow-out
fracture producing an acquired retraction syndrome. J Clin Neuroophthalmol 1986;6(3):153–156.
166. Glaser J, Bachynski B. Infranuclear disorders of eye movement. In:
Glaser J (ed) Neuroophthalmology. Philadelphia: Lippincott, 1990.
167. Glaser JS. Myasthenic pseudo-internuclear ophthalmoplegia. Arch
Ophthalmol 1966;75(3):363–366.
168. Glover AT, Powe LK. Ocular motor apraxia and neurofibromatosis.
Arch Ophthalmol 1985;103(6):763.
169. Gobin MH. Surgical management of Duane’s syndrome. Br J
Ophthalmol 1974;58(3):301–306.
170. Goldman HD, Nelson LB. Acute acquired comitant esotropia. Ann
Ophthalmol 1985;17(12):777–778.
171. Goldstein JH, Sacks DB. Bilateral Duane’s syndrome. J Pediatr Ophthalmol 1977;14(1):12–17.
172. Goldstein JH, Schneekloth BB. Spasm of the near reflex: a spectrum
of anomalies. Surv Ophthalmol 1996;40(4):269–278.
173. Golnik KC, et al. An ice test for the diagnosis of myasthenia gravis.
Ophthalmology 1999;106(7):1282–1286.
174. Gonatas NK. A generalized disorder of nervous system, skeletal
muscle and heart resembling Refsum’s disease and Hurler’s syndrome. II. Ultrastructure. Am J Med 1967;42(2):169–178.
175. Good WV, et al. Bilateral congenital oculomotor nerve palsy in a
child with brain anomalies. Am J Ophthalmol 1991;111(5):555–558.
176. Goodman CR, Chabner E, Guyton DL. Should early strabismus
surgery be performed for ocular torticollis to prevent facial asymmetry? J Pediatr Ophthalmol Strabismus 1995;32(3):162–166.
177. Gourdeau A, et al. Central ocular motor abnormalities in Duane’s
retraction syndrome. Arch Ophthalmol 1981;99(10):1809–1810.
178. Graeber MB, Muller U. Recent developments in the molecular genetics of mitochondrial disorders. J Neurol Sci 1998;153(2):251–263.
179. Green SH. Polyradiculitis (Landry–Guillain–Barre syndrome)
with total external ophthalmoplegia: encephalo-myelo-radiculoneuropathy. Dev Med Child Neurol 1976;18(3):369–373.
180. Greer M, Schotland M. Myasthenia gravis in the newborn. Pediatrics
1960;26:101–108.
chapter
12:
ocular motility disorders
501
181. Gresty M, Ell J. Normal modes of head and eye coordination and
the symptomatology of their disorders. In: Lennestrand G, Zee D,
Keller E (eds) Functional basis of ocular motility disorders. New
York: Pergamon, 1982;391–405.
182. Griffin JF, Wray SH, Anderson DP. Misdiagnosis of spasm of the near
reflex. Neurology 1976;26(11):1018–1020.
183. Grob D, et al. The course of myasthenia gravis and therapies affecting outcome. Ann NY Acad Sci 1987;505:472–499.
184. Grose C, et al. Primary Epstein–Barr virus infections in acute neurologic diseases. N Engl J Med 1975;292(8):392–395.
185. Gross-Tsur V, et al. Oculomotor apraxia: the presenting sign of
Gaucher disease. Pediatr Neurol 1090;5(2):128–129.
186. Grunnet ML, Lubow M. Ascending polyneuritis and ophthalmoplegia. Am J Ophthalmol 1972;74(6):1155–1160.
187. Hamed LM, Dennehy PJ, Lingua RW. Synergistic divergence and jawwinking phenomenon. J Pediatr Ophthalmol Strabismus 1990;27(2):
88–90.
188. Hamed LM, et al. Synergistic divergence: saccadic velocity analysis
and surgical results. J Pediatr Ophthalmol Strabismus 1992;29(1):
30–37.
189. Hanson PA, Rowland LP. Mobius syndrome and facioscapulohumeral muscular dystrophy. Arch Neurol 1971;24(1):31–39.
190. Harbord MG, et al. Moebius’ syndrome with unilateral cerebellar
hypoplasia. J Med Genet 1989;26(9):579–582.
191. Harley RD. Paralytic strabismus in children. Etiologic incidence and
management of the third, fourth, and sixth nerve palsies. Ophthalmology 1980;87(1):24–43.
192. Harper P. Myotonic dystrophy in infancy and childhood. In:
Myotonic dystrophy. London: Saunders, 1989.
193. Harrad RA, Graham CM, Collin JR. Amblyopia and strabismus in
congenital ptosis. Eye 1988;2(pt 6):625–627.
194. Harris C, Taylor D, Velodi A. Eye movement recording in type
3 Gaucher disease: a preliminary report. Mol Med Ther 1997;5:7–
10.
195. Harris CM, et al. Intermittent horizontal saccade failure (‘ocular
motor apraxia’) in children. Br J Ophthalmol 1996;80(2):151–158.
196. Harris CM, et al. Familial congenital saccade initiation failure and
isolated cerebellar vermis hypoplasia. Dev Med Child Neurol 1998;
40(11):775–779.
197. Harris CM, Taylor DS, Vellodi A. Ocular motor abnormalities in
Gaucher disease. Neuropediatrics 1999;30(6):289–293.
198. Harris DJ Jr, et al. Familial congenital superior oblique palsy. Ophthalmology 1986;93(1):88–90.
199. Heckmatt JZ, et al. Congenital centronuclear (myotubular) myopathy. A clinical, pathological and genetic study in eight children.
Brain 1985;108(pt 4):941–964.
200. Hedges TR III, et al. Botulin ophthalmoplegia. Clinical and oculographic observations. Arch Ophthalmol 1983;101(2):211–213.
502
handbook of pediatric strabismus and amblyopia
201. Helveston EM, Giangiacomo JG, Ellis FD. Congenital absence of the
superior oblique tendon. Trans Am Ophthalmol Soc 1981;79:123–
135.
202. Helveston EM, et al. Surgical treatment of superior oblique palsy.
Trans Am Ophthalmol Soc 1996;94:315–328.
203. Henderson J. The congenital facial diplegia syndrome. Clinical features, pathology, and aetiology. Brain 1939;62:381–403.
204. Hepler RS, Hoyt WF, Loeffler JD. Paradoxical synkinetic levator
inhibition and excitation. An electromyographic study of unilateral
oculopalpebral and bilateral mandibulopalpebral (Marcus Gunn)
synkineses in a 74-year-old man. Arch Neurol 1968;18(4):416–424.
205. Hertle R. Diagnosis of isolated cyclovertical muscle overaction using
a modification of the Parks’ Three-Step Test. Strabismus 1993;1:
107–120.
206. Hicks A. Congenital paralysis of lateral rotators of the eyes with
paralysis of muscles of face. Arch Ophthalmol 1943;30:38–42.
207. Hofmann RJ. Monozygotic twins concordant for bilateral Duane’s
retraction syndrome. Am J Ophthalmol 1985;99(5):563–566.
208. Holmes JM, Cronin CM. Duane syndrome associated with oculocutaneous albinism. J Pediatr Ophthalmol Strabismus 1992;28(1):32–
34.
209. Holmes JM, et al. Pediatric third, fourth, and sixth nerve palsies: a
population-based study. Am J Ophthalmol 1999;127(4):388–392.
210. Holtz SJ. Congenital ocular anomalies associated with Duane’s
retraction syndrome, the nervus of Ota, and axial anisometropia. Am
J Ophthalmol 1974;77(5):729–731.
211. Holzman AE, et al. Duane’s retraction syndrome in the fetal alcohol
syndrome. Am J Ophthalmol 1990;110(5):565.
212. Honda Y, Yoshioka M. Duane’s retraction syndrome associated with
muscular dystrophy. J Pediatr Ophthalmol Strabismus 1978;15(3):
157–159.
213. Hotchkiss MG, et al. Bilateral Duane’s retraction syndrome. A
clinical-pathologic case report. Arch Ophthalmol 1980;98(5):870–
874.
214. Hoyt CS, Billson FA, Alpins N. The supranuclear disturbances of
gaze in kernicterus. Ann Ophthalmol 1978;10(11):1487–1492.
215. Hoyt CS, Mousel DK, Weber AA. Transient supranuclear disturbances of gaze in healthy neonates. Am J Ophthalmol 1980;89(5):
708–713.
216. Hoyt WF, Nachtigaller H. Anomalies of ocular motor nerves.
Neuroanatomic correlates of paradoxical innervation in Duane’s
syndrome and related congenital ocular motor disorders. Am J
Ophthalmol 1965;60(3):443–448.
217. Huber A. Electrophysiology of the retraction syndromes. Br J Ophthalmol 1974;58(3):293–300.
218. Huber A. Botulinum A toxin injections as a new treatment of
blepharospasm and strabismus. In: Satoshi I (ed) Highlights in
neurophthalmology. Proceedings of the sixth meeting of the
chapter
219.
220.
221.
222.
223.
224.
225.
226.
227.
228.
229.
230.
231.
232.
233.
234.
235.
12:
ocular motility disorders
503
International Neurophthalmology Society. Amsterdam: Aeolus
Press, 1897.
Hughes J, et al. Congenital vertical ocular motor apraxia. J Clin
Neuroophthalmol 1985;5:153–157.
Hung TP. A polio-like syndrome in adults following acute hemorrhagic conjunctivitis. Int J Neurol 1981;15(3–4):266–278.
Hunt JM, et al. A post-docking role for synaptobrevin in synaptic
vesicle fusion. Neuron 1994;12(6):1269–1279.
Hurko O, et al. Heteroplasmy in chronic external ophthalmoplegia:
clinical and molecular observations. Pediatr Res 1990;28(5):542–
548.
Iannaccone ST, et al. Familial progressive external ophthalmoplegia
and ragged-red fibers. Neurology 1974;24(11):1033–1038.
Imes R, Monteiro M, Hoyt W. Ophthalmoplegic migraine with proximal posterior cerebral artery vascular anomaly. J Clin Neuroophthalmol 1984;4:221–223.
Ing EB, et al. Oculomotor nerve palsies in children. J Pediatr Ophthalmol Strabismus 1992;29(6):331–336.
Inocencio F, Ballecer R. Tuberculosis granuloma in the midbrain
causing wall-eyed bilateral internuclear ophthalmoplegia (Webino).
J Clin Neuroophthalmol 1985;5:31–35.
Inoue A, Koh C, Iwahashi T. Detection of serum anticerebellar antibodies in patients with Miller Fisher syndrome. Eur Neurol 1999;
42(4):230–234.
Inoue N, Izumi K, Mawatar S. Congenital ocular motor apraxia and
cerebellar degeneration: report of two cases. Jpn J Clin Neurol 1971;
11:855–861.
Isenberg S, Urist MJ. Clinical observations in 101 consecutive
patients with Duane’s retraction syndrome. Am J Ophthalmol 1977;
84(3):419–425.
Isenberg S, Blechman B. Marcus Gunn jaw winking and Duane’s
retraction syndrome. J Pediatr Ophthalmol Strabismus 1983;20(6):
235–237.
Jamal GA, et al. Myotonic dystrophy. A reassessment by conventional and more recently introduced neurophysiological techniques.
Brain 1986;109(pt 6):1279–1296.
Jamal GA, Ballantyne JP. The localization of the lesion in patients
with acute ophthalmoplegia, ataxia and areflexia (Miller Fisher syndrome). A serial multimodal neurophysiological study. Brain 1988;
111(pt 1):95–114.
James RH. Induction agent sensitivity and ophthalmoplegia plus.
Anaesthesia 1986;41(2):216.
Jampolsky A. Surgical leashes and reverse leashes in strabismus surgical management. In: Symposium on strabismus. Transactions of
the New Orleans Academy of Ophthalmology. St. Louis: Mosby,
1978.
Jan JE, et al. Speech, cognition, and imaging studies in congenital
ocular motor apraxia. Dev Med Child Neurol 1998;40(2):95–99.
504
handbook of pediatric strabismus and amblyopia
236. Jankowicz E, et al. Familial progressive external ophthalmoplegia
with abnormal muscle mitochondria. Eur Neurol 1977;15(6):318–
324.
237. Jay WM, Hoyt CS. Abnormal brain stem auditory-evoked potentials
in Stilling–Turk–Duane retraction syndrome. Am J Ophthalmol
1980;89(6):814–818.
238. Jimura T, et al. A case of synergistic divergence associated
with Horner’s syndrome. Folia Ophthalmol Jpn 1983;34:477–
480.
239. Johnson LN, Pack WL. Transient oculomotor nerve misdirection
in a case of pituitary tumor with hemorrhage. Case report. Arch
Ophthalmol 1988;106(5):584–585.
240. Johnson RO, Clay SA, Arnon SS. Diagnosis and management of
infant botulism. Am J Dis Child 1979;133(6):586–593.
241. Jones HR Jr. Guillain–Barre syndrome: perspectives with infants and
children. Semin Pediatr Neurol 2000;7(2):91–102.
242. Jordan D, Miller D, Anderson R. Acquired oculomotor-abducens
synkinesis. Can J Ophthalmol 1990;25:148–151.
243. Kaminski HJ, et al. Why are eye muscles frequently involved in
myasthenia gravis? Neurology 1990;40(11):1663–1669.
244. Kaminski HJ, Kusner LL, Block CH. Expression of acetylcholine
receptor isoforms at extraocular muscle endplates. Investig Ophthalmol Vis Sci 37(2):345–351.
245. Karpati H, et al. The Kearns–Shy syndrome: a multisystem disease
with mitochondrial abnormality demonstrated in skeletal muscle
and skin. J Neurol Sci 1973;19:133–151.
246. Katiyar BC, et al. Adult polio-like syndrome following enterovirus
70 conjunctivitis (natural history of the disease). Acta Neurol Scand
1983;67(5):263–274.
247. Kaufman LW, Folk ER, Miller MT. Monozygotic twins discordant for
Duane’s retraction syndrome. Case report. Arch Ophthalmol
1989;107(3):324–325.
248. Kawano K, Fujita S. Duane’s retraction syndrome associated with
morning glory syndrome. J Pediatr Ophthalmol Strabismus 1981;
18(1):51–54.
249. Keane J. Upward gaze paralysis as the initial sign of Fisher’s syndrome. Arch Neurol 1982;32:781–782.
250. Keane JR, Hoyt WF. Myasthenic (vertical) nystagmus. Verification
by edrophonium tonography. JAMA 212(7):1209–1210.
251. Keane JR, Davis RL. Pretectal syndrome with metastatic malignant
melanoma to the posterior commissure. Am J Ophthalmol 1976;
82(6):910–914.
252. Keane JR. Neuro-ophthalmic signs and symptoms of hysteria.
Neurology 1982;32(7):757–762.
253. Keane JR. Acute bilateral ophthalmoplegia: 60 cases. Neurology
1986;36(2):279–281.
254. Keane JR. Traumatic internuclear ophthalmoplegia. J Clin Neuroophthalmol 1987;7(3):165–166.
chapter
12:
ocular motility disorders
505
255. Keane JR. The pretectal syndrome: 206 patients. Neurology 1990;
40(4):684–690.
256. Kearns T, Sayre G. Retinitis pigmentosa, external ophthalmoplegia,
and complete heart block. Arch Ophthalmol 1958;60:280–289.
257. Keith CG. Oculomotor nerve palsy in childhood. Aust N Z J
Ophthalmol 1987;15(3):181–184.
258. Khodadoust AA, von Noorden GK. Bilateral vertical retraction syndrome. A family study. Arch Ophthalmol 1967;78(5):606–612.
259. Khwarg SI, et al. Management of moderate-to-severe Marcus-Gunn
jaw-winking ptosis. Ophthalmology 1999;106(6):1191–1196.
260. Kiloh L, Nevin S. Progressive dystrophy of the ocular muscles (ocular
myopathy). Brain 1951;74:115–143.
261. Kirkham TH. Cervico-oculo-acusticus syndrome with pseudo-papilloedema. Arch Dis Child 1969;44(236):504–508.
262. Kirkham TH. Duane’s syndrome and familial perceptive deafness. Br
J Ophthalmol 1969;53(5):335–339.
263. Kirkham TH. Duane’s retraction syndrome and cleft palate. Am J
Ophthalmol 1970;70(2):209–212.
264. Kirkham TH. Inheritance of Duane’s syndrome. Br J Ophthalmol
1970;54(5):323–329.
265. Kirkham TH, Kamin DF. Slow saccadic eye movements in Wilson’s
disease. J Neurol Neurosurg Psychiatry 1974;37(2):191–194.
266. Kivlin JD, Lundergan MK. Acquired retraction syndrome associated
with orbital metastasis. J Pediatr Ophthalmol Strabismus 1985;
22(3):109–112.
267. Knox DL, Clark DB, Schuster FF. Benigh VI nerve palsies in children.
Pediatrics 1967;40(4):560–564.
268. Kodsi S. Marcus Gunn jaw winking with trigemino-abducens
synkinesis. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(5):
316–317.
269. Kodsi SR, Younge BR. Acquired oculomotor, trochlear, and abducent
cranial nerve palsies in pediatric patients. Am J Ophthalmol 1992;
114(5):568–574.
270. Koeppen AH, Hans MB. Supranuclear ophthalmoplegia in olivopontocerebellar degeneration. Neurology 1976;26(8):764–768.
271. Kommerell GBM. A new type of Duane’s syndrome: twitch abduction on attempted upgaze and V-incomitance due to misinnervation
of the lateral rectus by superior rectus neurons. Neuro-Ophthalmology 1986;6:159–164.
272. Kommerell G, et al. Oculomotor palsy with cyclic spasms: electromyographic and electron microscopic evidence of chronic peripheral neuronal involvement. Neuro-Ophthalmology 1988;8:9–21.
273. Kompf D, Christen H. Isolated abducens nerve palsy preceding infectious mononucleosis. Neuro-Ophthalmology 1984;4:101–105.
274. Kraft S, Scott W. Masked bilateral superior oblique palsy. Clinical features and diagnosis. J Pediatr Ophthalmol 1986;23:264–272.
275. Kraft S. A surgical approach for Duane syndrome. J Pediatr
Ophthalmol Strabismus 1988;25:119–130.
506
handbook of pediatric strabismus and amblyopia
276. Kraft SP, O’Donoghue EP, Roarty JD. Improvement of compensatory
head postures after strabismus surgery. Ophthalmology 1992;99(8):
1301–1308.
277. Krohel GB. Blepharoptosis after traumatic third-nerve palsies. Am J
Ophthalmol 1979;88(3 pt 2):598–601.
278. Kubis KC, et al. The ice test versus the rest test in myasthenia gravis.
Ophthalmology 2000;107(11):1995–1998.
279. Kuncl R, Hoffman P. Myopathies and disorders of neuromuscular
transmission. In: Miller N, Newman N (eds) Walsh & Hoyt’s
clinical neuro-ophthalmology. Baltimore: Williams & Wilkins,
1998.
280. Kushner BJ. The diagnosis and treatment of bilateral masked superior oblique palsy. Am J Ophthalmol 1988;105(2):186–194.
281. Kushner BJ. Errors in the three-step test in the diagnosis of vertical
strabismus. Ophthalmology 1989;96(1):127–132.
282. Lambert SR, et al. Joubert syndrome. Arch Ophthalmol 1989;107(5):
709–713.
283. Lammens M, et al. Neuropathological findings in Moebius syndrome. Clin Genet 1998;54(2):136–141.
284. Lavy T, et al. Electrophysiological and eye-movement abnormalities
in children with the Bardet–Biedl syndrome. J Pediatr Ophthalmol
Strabismus 1995;32(6):364–367.
285. Lebensohn J. Parinaud’s syndrome. From obstetric trauma with
recovery. Am J Ophthalmol 1955;40:738–740.
286. Lee J, Flynn JT. Bilateral superior oblique palsies. Br J Ophthalmol
1985;69(7):508–513.
287. Lee MS, et al. Sixth nerve palsies in children. Pediatr Neurol
1999;20(1):49–52.
288. Leigh RJ, Zee DS. The neurology of eye movements, 3rd edn.
Philadelphia: Davis, 1999.
289. Lepore FE, Glaser JS. Misdirection revisited. A critical appraisal of
acquired oculomotor nerve synkinesis. Arch Ophthalmol 1980;
98(12):2206–2209.
290. Lessell S, Coppeto J, Samet S. Ophthalmoplegia in myotonic dystrophy. Am J Ophthalmol 1971;71(6):1231–1235.
291. Leung AK. Transient sixth cranial nerve palsy in newborn infants.
Br J Clin Pract 1987;41(4):717–718.
292. Lindstrom JM, et al. Antibody to acetylcholine receptor in myasthenia gravis. Prevalence, clinical correlates, and diagnostic value.
Neurology 1976;26(11):1054–1059.
293. Lingua R, Walkoner F. Use of the posterior fixation suture in type I
Duane syndrome. J Ocul Ther Surg 1985;4:107–111.
294. Lipson AH, et al. Moebius syndrome: animal model–human correlations and evidence for a brainstem vascular etiology. Teratology
1989;40(4):339–350.
295. Loewenfeld IE, Thompson HS. Oculomotor paresis with cyclic
spasms. A critical review of the literature and a new case. Surv
Ophthalmol 1975;20(2):81–124.
chapter
12:
ocular motility disorders
507
296. Lubkin V. The inverse Marcus Gunn phenomenon. An electromyographic contribution. Arch Neurol 1978;35(4):249.
297. Lueder GT, et al. Vertical strabismus resulting from an anomalous
extraocular muscle. J Am Assoc Pediatr Ophthalmol Strabismus
1998;2(2):126–128.
298. Lyle D. A discussion of ocular motor apraxia with a case presentation. Trans Am Ophthalmol Soc 1961;59:274–285.
299. Lyness RW, et al. Histological appearances of the levator palpebrae
superioris muscle in the Marcus Gunn phenomenon. Br J Ophthalmol 1988;72(2):104–109.
300. MacDonald AL, Crawford JS, Smith DR. Duane’s retraction
syndrome: an evaluation of the sensory status. Can J Ophthalmol
1974;9(4):458–462.
301. MacLennan C, et al. Acetylcholine receptor expression in human
extraocular muscles and their susceptibility to myasthenia gravis.
Ann Neurol 1997;41(4):423–431.
302. Magoon E. The use of botulinum injection as an alternative to
surgery. Contemp Ophthalmic Forum 1987;5:222.
303. Mahadevan M, et al. Myotonic dystrophy mutation: an unstable
CTG repeat in the 3 untranslated region of the gene. Science 1992;
255(5049):1253–1255.
304. Mankodi A, et al. Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 2000;289(5485):1769–1773.
305. Manson JI. Ocular motor apraxia in childhood. Proc Aust Assoc
Neurol 1973;10(0):27–29.
306. Marshman WE, Adams GG, Cree I. Extraocular muscle surgery in
myotonic dystrophy. J Pediatr Ophthalmol Strabismus 1998;35(3):
169–171.
307. Marshman WE, et al. Congenital anomalies in patients with Duane
retraction syndrome and their relatives. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(2):106–109.
308. Maruo T, et al. Duane’s syndrome. Jpn J Ophthalmol 1979;23:453–
468.
309. Marzetti G, Midulla M, Balducci L. Monolateral paralysis of the 3rd
pair of cranial nerves due to A9 Coxsackie virus. Minerva Pediatr
1968;20(18):943–947.
310. Matteuci P. I difetti congenit di abduzione con particolare rifuardo
all patogenesi. Rass Ital Ottal 1946;15:345–380.
311. McGettrick P, Eustace P. The w.e.b.i.n.o. syndrome. NeuroOphthalmology 1985;5:109–115.
312. McGovern ST, Crompton JL, Ingham PN. Trigemino-abducens synkinesis: an unusual case of aberrant regeneration. Aust N Z J Ophthalmol 1986;14(3):275–279.
313. Mehkri IA, et al. Double vision in a child. Surv Ophthalmol
1999;44(1):45–51; discussion 51–52.
314. Meienberg O, Ryffel E. Supranuclear eye movement disorders in
Fisher’s syndrome of ophthalmoplegia, ataxia, and areflexia. Report
of a case and literature review. Arch Neurol 1983;40(7):402–405.
508
handbook of pediatric strabismus and amblyopia
315. Meienberg O. Lesion site in Fisher’s syndrome. Arch Neurol 1984;
41(3):250–251.
316. Meire F, et al. Waardenburg syndrome, Hirschsprung megacolon, and
Marcus Gunn ptosis. Am J Med Genet 1987;27(3):683–686.
317. Mellinger J, Gomez M. Agenesis of the cranial nerves. In: Vinken P,
Bruyn G (eds) Handbook of clinical neurology. New York: Elsevier,
1977.
318. Melmed C, Karpati G, Carpenter S. Experimental mitochondrial
myopathy produced by in vivo uncoupling of oxidative phosphorylation. J Neurol Sci 1975;26(3):305–318.
319. Meola G. Myotonic dystrophies. Curr Opin Neurol 2000;13(5):519–
525.
320. Meola G. Clinical and genetic heterogeneity in myotonic dystrophies. Muscle Nerve 2000;23(12):1789–1799.
321. Merz M, Wojtowicz S. The Mobius syndrome. Report of electromyographic examinations in two cases. Am J Ophthalmol 1967;
63(4):837–840.
322. Metz HS, Scott AB, Scott WE. Horizontal saccadic velocities in
Duane’s syndrome. Am J Ophthalmol 1975;80(5):901–906.
323. Miller MT, et al. Superior oblique palsy presenting in late childhood.
Am J Ophthalmol 1970;70(2):212–214.
324. Miller MT, et al. Mobius and Mobius-like syndromes (TTV-OFM,
OMLH). J Pediatr Ophthalmol Strabismus 1989;26(4):176–188.
325. Miller MT, Stromland K. The Mobius sequence: a relook. J Am Assoc
Pediatr Ophthalmol Strabismus 1999;3(4):199–208.
326. Miller NR. Solitary oculomotor nerve palsy in childhood. Am J
Ophthalmol 1977;83(1):106–111.
327. Millichap J, Dodge P. Diagnosis and treatment of myasthenia gravis
in infancy, childhood, and adolescence: a study of 51 patients.
Neurology 1960;10:1007–1014.
328. Möbius P. Uber angeborene doppelseitige Abducens-FacialisLahmung. Munch Med Wochenschr 1888;35:91–108.
329. Möbius P. Uber infantilen Kernschwund. Munch Med Wochenschr
1892;39:17–21.
330. Mohan K, et al. Treatment of congenital adduction palsy with
synergistic divergence. J Pediatr Ophthalmol Strabismus 1998;35(3):
149–152.
331. Molarte AB, Rosenbaum AL. Vertical rectus muscle transposition
surgery for Duane’s syndrome. J Pediatr Ophthalmol Strabismus
1990;27(4):171–177.
332. Moore AT, Taylor DS. A syndrome of congenital retinal dystrophy
and saccade palsy—a subset of Leber’s amaurosis. Br J Ophthalmol
1984;68(6):421–431.
333. Moore LD, Feldon SE, Liu SK. Infrared oculography of Duane’s
retraction syndrome (type 1). Arch Ophthalmol 1988;106(7):943–946.
334. Moraes CT, et al. Mitochondrial DNA deletions in progressive external ophthalmoplegia and Kearns–Sayre syndrome. N Engl J Med
1989;320(20):1293–1299.
chapter
12:
ocular motility disorders
509
335. Morimoto T, et al. A case of a rapidly progressive central nervous
system disorder manifesting as a pallidal posture and ocular motor
apraxia. Brain Dev 1985;7(4):449–453.
336. Mounsey JP, et al. Skeletal muscle sodium channel gating in mice
deficient in myotonic dystrophy protein kinase. Hum Mol Genet
2000;9(15):2313–2320.
337. Movaghar M, Slavin ML. Effect of local heat versus ice on blepharoptosis resulting from ocular myasthenia. Ophthalmology 2000;
107(12):2209–2214.
338. Muchnick RS, Aston SJ, Rees TD. Ocular manifestations and treatment of hemifacial atrophy. Am J Ophthalmol 1979;88(5):889–897.
339. Mudgil AV, Repka MX. Ophthalmologic outcome after third cranial
nerve palsy or paresis in childhood. J Am Assoc Pediatr Ophthalmol
Strabismus 1999;3(1):2–8.
340. Mullaney P, et al. The natural history and ophthalmic involvement
in childhood myasthenia gravis at the hospital for sick children.
Ophthalmology 2000;107(3):504–510.
341. Mullie MA, et al. The retinal manifestations of mitochondrial
myopathy. A study of 22 cases. Arch Ophthalmol 1985;103(12):1825–
1830.
342. Muri RM, Meienberg O. The clinical spectrum of internuclear
ophthalmoplegia in multiple sclerosis. Arch Neurol 1985;42(9):851–
855.
343. Murray R, Steven P. Congenital levator and lateral rectus muscle
associated reflex. Neuro-Ophthalmology 1986;6:29–31.
344. Namba T, Brown SB, Grob D. Neonatal myasthenia gravis: report of
two cases and review of the literature. Pediatrics 1970;45(3):488–504.
345. Narbona J, Crisci CD, Villa I. Familial congenital ocular motor
apraxia and immune deficiency. Arch Neurol 1980;37(5):325.
346. Neimann N, et al. Mobius’ syndrome associated with atrophic
myopathy. Ann Med Nancy 1965;4:1084–1092.
347. Nellhaus G. Isolated oculomotor nerve palsy in infectious mononucleosis. A report of an unusual case and review of the literature. Neurology 1966;16(2):221–224.
348. Nelson LB. Severe adduction deficiency following a large medial
rectus recession in Duane’s retraction syndrome. Arch Ophthalmol
1986;104(6):859–862.
349. Nelson S, Kline L. Acquired trigemino-abducens synkinesis. J Clin
Neuroophthalmol 1990;10:111–114.
350. Nemet P, Ehrlich D, Lazar M. Benign abducens palsy in varicella.
Am J Ophthalmol 1974;78(5):859.
351. Nemet P, Ron S. Ocular saccades in Duane’s syndrome. Br J Ophthalmol 1978;62(8):528–532.
352. Nishizaki T, et al. Bilateral internuclear ophthalmoplegia due to
hydrocephalus: a case report. Neurosurgery 1985;17(5):822–825.
353. Noel LP, Clarke WN. Adduction deficiency following medial recti
recession in Duane’s retraction syndrome. Case report. Arch Ophthalmol 1987;105(4):465.
510
handbook of pediatric strabismus and amblyopia
354. Oda K, Shibasaki H. Antigenic difference of acetylcholine receptor
between single and multiple form endplates of human extraocular
muscle. Brain Res 1988;449(1–2):337–340.
355. O’Day J, Billson F, King J. Ophthalmoplegic migraine and aberrant
regeneration of the oculomotor nerve. Br J Ophthalmol 1980;64(7):
534–536.
356. Oesterle CS, et al. Eye bobbing associated with jaw movement. Ophthalmology 1982;89(1):63–67.
357. Ogasahara S, et al. Improvement of abnormal pyruvate metabolism
and cardiac conduction defect with coenzyme Q10 in Kearns–Sayre
syndrome. Neurology 1985;35(3):372–377.
358. Ogasahara S, et al. Treatment of Kearns–Sayre syndrome with coenzyme Q10. Neurology 1986;36(1):45–53.
359. Ogasahara S, et al. Muscle coenzyme Q deficiency in familial mitochondrial encephalomyopathy. Proc Natl Acad Sci USA 1989;
86(7):2379–2382.
360. Ohtsuki H, et al. Strabismus surgery in ocular myasthenia gravis.
Ophthalmologica 1996;210(2):95–100.
361. Okihiro MM, et al. Duane syndrome and congenital upper-limb
anomalies. A familial occurrence. Arch Neurol 1977;34(3):174–
179.
362. Olson WH, et al. Moebius syndrome. Lower motor neuron involvement and hypogonadotrophic hypogonadism. Neurology 1970;20(10):
1002–1008.
363. O’Malley ER, Helveston EM, Ellis FD. Duane’s retraction syndrome—plus. J Pediatr Ophthalmol Strabismus 1982;19(3):161–
165.
364. Oohira A, Goto K, Ozawa T. Slow saccades in myogenic and peripheral neurogenic ophthalmoplegia. Late ocular myopathy in myotonic
dystrophy. Neuro-Ophthalmology 1985;5:117–123.
365. Oosterhuis HJ. The ocular signs and symptoms of myasthenia gravis.
Doc Ophthalmol 1982;52(3–4):363–378.
366. Osher RH, et al. Neuro-ophthalmological complications of enlargement of the third ventricle. Br J Ophthalmol 1978;62(8):536–542.
367. Osher RH, Schatz NJ, Duane TD. Acquired orbital retraction syndrome. Arch Ophthalmol 1980;98(10):1798–1802.
368. Ouhabi H, et al. Bilateral optic neuritis and ponto-mesencephalic
involvement shown by MRI in Miller–Fisher syndrome. Rev Neurol
(Paris) 1998;154(11):780–782.
369. Ozawa T, Naito M, Takasu T. Disorder of saccadic eye movement
in cerebellar degeneration. Jpn J Ophthalmol 1974;18:363–380.
370. Parks M. Isolated cyclovertical muscle palsy. Arch Ophthalmol
1958;60:1027–1035.
371. Pasik P, Pasik T, Bender MB. The pretectal syndrome in monkeys. I.
Disturbances of gaze and body posture. Brain 1969;92(3):521–534.
372. Pasik T, Pasik P, Bender MB. The pretectal syndrome in monkeys.
II. Spontaneous and induced nystagmus, and “lightning” eye movements. Brain 1969;92(4):871–884.
chapter
12:
ocular motility disorders
511
373. Paysee EA, Coats DK, Plager DA. Facial asymmetry and tendon
laxity in superior oblique palsy. J Pediatr Ophthalmol Strabismus
1995;32(3):158–161.
374. Pearse RG, Howeler CJ. Neonatal form of dystrophia myotonica.
Five cases in preterm babies and a review of earlier reports. Arch Dis
Child 1979;54(5):331–338.
375. Pebbenito R, Cracco J. Congenital ocular motor apraxia. Clin Paediatr 1988;27:27–31.
376. Pesando P, Nuzzi G, Maraini G. Vertical retraction syndrome. Ophthalmologica 1978;177(5):254–259.
377. Pfaffenbach DD, Cross HE, Kearns TP. Congenital anomalies in
Duane’s retraction syndrome. Arch Ophthalmol 1972;88(6):635–639.
378. Phillips MS, Stewart S, Anderson JR. Neuropathological findings in
Miller Fisher syndrome. J Neurol Neurosurg Psychiatry 1984;47(5):
492–495.
379. Pieroni D. Goldenhar’s syndrome associated with Duane’s retraction
syndrome. J Pediatr Ophthalmol Strabismus 1969;6:16–18.
380. Pierrot–Deseilligny C, Gautier JC, Loron P. Acquired ocular motor
apraxia due to bilateral frontoparietal infarcts. Ann Neurol
1988;23(2):199–202.
381. Plager DA. Tendon laxity in superior oblique palsy. Ophthalmology
1992;99(7):1032–1038.
382. Polak PE, Zijlstra F, Roelandt JR. Indications for pacemaker implantation in the Kearns–Sayre syndrome. Eur Heart J 1989;10(3):
281–282.
383. Pollard ZF. Aneurysm causing third nerve palsy in a 15-year-old boy.
Arch Ophthalmol 1988;106(12):1647–1648.
384. Pollard ZF. Bilateral superior oblique muscle palsy associated with
Apert’s syndrome. Am J Ophthalmol 1988;106(3):337–340.
385. Pollard ZF. Accommodative esotropia after ocular and head injury.
Am J Ophthalmol 1990;109(2):195–198.
386. Poppen JL, Marino R Jr. Pinealomas and tumors of the posterior
portion of the third ventricle. J Neurosurg 1968;28(4):357–364.
387. Prasad P, Nair S. Congenital ocular motor apraxia: sporadic and
familial. Support for natural resolution. J Neuroophthalmol 1994;
14(2):102–104.
388. Pressman SH, Scott WE. Surgical treatment of Duane’s syndrome.
Ophthalmology 1986;93(1):29–38.
389. Pruksacholawit K, Ishikawa S. Atypical retraction syndrome: a case
study. J Pediatr Ophthalmol Strabismus 1976;13:215–220.
390. Putterman AM. Botulinum toxin injections in the treatment of
seventh nerve misdirection. Am J Ophthalmol 1990;110(2):205–206.
391. Raab EL. Clinical features of Duane’s syndrome. J Pediatr Ophthalmol Strabismus 1986;23(2):64–68.
392. Ramon Y, Cajal S. Degeneration and regeneration of the nervous
system. London: Oxford University Press, 1928.
393. Ramsay J, Taylor D. Congenital crocodile tears: a key to the aetiology of Duane’s syndrome. Br J Ophthalmol 1980;64(7):518–522.
512
handbook of pediatric strabismus and amblyopia
394. Rana PV, Wadia RS. The Marin–Amat syndrome: an unusual facial
synkinesia. J Neurol Neurosurg Psychiatry 1985;48(9):939–941.
395. Rappaport L, et al. Concurrence of congenital ocular motor apraxia
and other motor problems: an expanded syndrome. Dev Med Child
Neurol 1987;29(1):85–90.
396. Raroque HG Jr, Hershewe GL, Snyder RD. Mobius syndrome and
transposition of the great vessels. Neurology 1988;38(12):1894–1895.
397. Rating D, et al. 4-Hydroxybutyric aciduria: a new inborn error of
metabolism. I. Clinical review. J Inherit Metab Dis 1984;7(suppl
1):90–92.
398. Redding FK. Familial congenital ocular motor apraxia. Neurology
1970;20(4):405.
399. Reinecke RD, Thompson WE. Childhood recurrent idiopathic paralysis of the lateral rectus. Ann Ophthalmol 1981;13(9):1037–1039.
400. Reisner SH, et al. Transient lateral rectus muscle paresis in the
newborn infant. J Pediatr 1971;78(3):461–465.
401. Ricker K. Myotonic dystrophy and proximal myotonic myopathy.
J Neurol 1999;246(5):334–338.
402. Ro A, et al. Duane’s retraction syndrome: southwestern Ontario
experience. Can J Ophthalmol 1989;24(5):200–203.
403. Ro A, et al. Auditory function in Duane’s retraction syndrome. Am
J Ophthalmol 1990;109(1):75–78.
404. Roberts NK, Perloff JK, Kark RA. Cardiac conduction in the
Kearns–Sayre syndrome (a neuromuscular disorder associated with
progressive external ophthalmoplegia and pigmentary retinopathy).
Report of 2 cases and review of 17 published cases. Am J Cardiol
1979;44(7):1396–1400.
405. Robertson DM, Hines JD, Rucker CW. Acquired sixth-nerve paresis
in children. Arch Ophthalmol 1970;83(5):574–579.
406. Robertson WC, Chun RW, Kornguth SE. Familial infantile myasthenia. Arch Neurol 1980;37(2):117–119.
407. Rodrigues–Alves C, Caldeira J. Moebius’ syndrome: a case report
with multiple congenital anomalies. J Pediatr Ophthalmol Strabismus 1975;12:103–106.
408. Rodriguez M, et al. Myasthenia gravis in children: long-term followup. Ann Neurol 1983;13(5):504–510.
409. Rogers GL, Hatch GF Jr, Gray I. Mobius syndrome and limb abnormalities. J Pediatr Ophthalmol 1977;4(3):134–138.
410. Rogers GL, Bremer DL. Surgical treatment of the upshoot and downshoot in Duanes’ retraction syndrome. Ophthalmology 1984;91(11):
1380–1383.
411. Roggenkamper P, et al. Orbicular synkinesis after facial paralysis:
treatment with botulinum toxin. Doc Ophthalmol 1994;86(4):395–
402.
412. Rollinson RD, Fenichel GM. Relapsing ocular myasthenia. Neurology 1981;31(3):325–326.
413. Ropper A, Wijdicks E, Truax B. Guillain–Barre syndrome. Philadelphia: Davis, 1991.
chapter
12:
ocular motility disorders
513
414. Ropper AH. The CNS in Guillain–Barre syndrome. Arch Neurol
1983;40(7):397–398.
415. Ropper AH. Unusual clinical variants and signs in Guillain–Barre
syndrome. Arch Neurol 1986;43(11):1150–1152.
416. Ropper AH. Three patients with Fisher’s syndrome and normal MRI.
Neurology 1988;38(10):1630–1631.
417. Rosenberg ML, Wilson E. Congenital ocular motor apraxia without
head thrusts. J Clin Neuroophthalmol 1987;7(1):26–28.
418. Roses AD, Appel SH. Protein kinase activity in erythrocyte ghosts
of patients with myotonic muscular dystrophy. Proc Natl Acad Sci
USA 1973;70(6):1855–1859.
419. Rothner AD. The migraine syndrome in children and adolescents.
Pediatr Neurol 1986;2(3):121–126.
420. Rowland LP. Molecular genetics, pseudogenetics, and clinical neurology. The Robert Wartenberg lecture. Neurology 1983;33(9):1179–
1195.
421. Rozen S, et al. Marfanoid hypermobility syndrome associated with
Duane’s retraction syndrome. Ann Ophthalmol 1983;15(9):862–864.
422. Rubinstein AE, et al. Moebius syndrome in Kallmann syndrome.
Arch Neurol 1975;32(7):480–482.
423. Rush J, Shafrin F. Ocular myasthenia presenting as superior oblique
weakness. J Clin Neuroophthalmol 1982;2:125–127.
424. Rush JA, Younge BR. Paralysis of cranial nerves III, IV, and VI. Cause
and prognosis in 1,000 cases. Arch Ophthalmol 1981;99(1):76–79.
425. Saavedra J, et al. A cold test for myasthenia gravis. Neurology
1979;29(7):1075.
426. Sakalas R, et al. Chronic sixth nerve palsy. An initial sign of
basisphenoid tumors. Arch Ophthalmol 1975;93(3):186–190.
427. Sano K. Trigemino-ocular synkineses. Neurologia 1959;1:29–51.
428. Saraux H, Laroche L, Lacombe H. Congenital horizontal gaze paralysis and ear dysplasia in a boy with Duane’s retraction syndrome and
seventh nerve palsy. Ophthalmologica 1984;188(4):208–211.
429. Sargent MA, Poskitt KJ, Jan JE. Congenital ocular motor apraxia:
imaging findings. AJNR Am J Neuroradiol 1997;18(10):1915–1922.
430. Sarkies NJ, Sanders MD. Convergence spasm. Trans Ophthalmol Soc
UK 1985;104(pt 7):782–786.
431. Sarnat HB, McGarry JD, Lewis JE Jr. Effective treatment of infantile
myasthenia gravis by combined prednisone and thymectomy. Neurology 1977;27(6):550–553.
432. Sato M. Magnetic resonance imaging and tendon anomaly associated
with congenital superior oblique palsy. Am J Ophthalmol 1999;
127(4):379–387.
433. Scassellat-Sforzolini G. Una sindroma molto rare: diffeto congenito
monolaterale della elevazione con retrazione del globe. Riv Otoneurooftalmol 1958;33:431–439.
434. Schapira AH, Thomas PK. A case of recurrent idiopathic ophthalmoplegic neuropathy (Miller Fisher syndrome). J Neurol Neurosurg
Psychiatry 1986;49(4):463–464.
514
handbook of pediatric strabismus and amblyopia
435. Scharf J, Zonis S. Benign abducens palsy in children. J Pediatr Ophthalmol 1975;12:165.
436. Schatz NJ, Savino PJ, Corbett JJ. Primary aberrant aculomotor regeneration. A sign of intracavernous meningioma. Arch Neurol
1977;34(1):29–32.
437. Schmidt D. Prognosis of ocular myasthenia in childhood. NeuroOphthalmology 1983;3:117–124.
438. Schneck L, et al. Ophthalmoplegia plus with morphological and
chemical studies of cerebellar and muscle tissue. J Neurol Sci
1973;19(1):37–44.
439. Schraeder PL, Cohen MM, Goldman W. Bilateral internuclear ophthalmoplegia associated with fourth ventricular epidermoid tumor.
Case report. J Neurosurg 1981;54(3):403–405.
440. Schumacher-Feero LA, et al. Third cranial nerve palsy in children.
Am J Ophthalmol 1999;128(2):216–221.
441. Schumm F, et al. Thymectomy in patients with pure ocular symptoms. J Neurol Neurosurg Psychiatry 1985;48:332–337.
442. Scott A. Botulinum toxin treatment for strabismus. Am Orthop J
1985;35:28.
443. Scott AB, Wong GY. Duane’s syndrome. An electromyographic
study. Arch Ophthalmol 1971;87(2):140–147.
444. Scott AB, Kraft SP. Botulinum toxin injection in the management of
lateral rectus paresis. Ophthalmology 1985;92(5):676–683.
445. Seaber J, Nashold B. Comparison of ocular motor effects of unilateral stereotactic midbrain lesions in man. Neuro-Ophthalmology
1980;1:95–99.
446. Sharf B, Hyams S. Oculomotor palsy following varicella. J Pediatr
Ophthalmol 1972;9:245–247.
447. Sharpe JA, Johnston JL. Ocular motor paresis versus apraxia. Ann
Neurol 1989;25(2):209–210.
448. Shauly Y, Weissman A, Meyer E. Ocular and systemic characteristics of Duane syndrome. J Pediatr Ophthalmol Strabismus 1993;
30(3):178–183.
449. Shaunak S, et al. Saccades and smooth pursuit in myotonic dystrophy. J Neurol 1999;246(7):600–606.
450. Shawkat FS, et al. Neuroradiological and eye movement correlates
in children with intermittent saccade failure: “ocular motor
apraxia.” Neuropediatrics 1995;26(6):298–305.
451. Shawkat FS, et al. The role of ERG/VEP and eye movement recordings in children with ocular motor apraxia. Eye 1996;10(pt 1):53–60.
452. Shoffner JM, et al. Spontaneous Kearns–Sayre/chronic external ophthalmoplegia plus syndrome associated with a mitochondrial DNA
deletion: a slip-replication model and metabolic therapy. Proc Natl
Acad Sci USA 1989;86(20):7952–7956.
453. Shulman LM, Gallo BV, Weiner WJ. Acquired abducens-trigeminal
synkinesis. Neurology 1998;50(5):1507–1508.
454. Sibony PA, Lessell S. Transient oculomotor synkinesis in temporal
arteritis. Arch Neurol 1984;41(1):87–88.
chapter
12:
ocular motility disorders
515
455. Sibony PA, Lessell S, Gittinger JW Jr. Acquired oculomotor synkinesis. Surv Ophthalmol 1984;28(5):382–390.
456. Sibony PA, Evinger C, Lessell S. Retrograde horseradish peroxidase
transport after oculomotor nerve injury. Investig Ophthalmol Vis Sci
1986;27(6):975–980.
457. Simcock PR, Kelleher S, Dunne JA. Neuro-ophthalmic findings in
botulism type B. Eye 1994;8(pt 6):646–648.
458. Simpson LL. The origin, structure, and pharmacological activity of
botulinum toxin. Pharmacol Rev 1981;33(3):155–188.
459. Slavin ML. Gaze palsy associated with viral syndrome. Am J Ophthalmol 1985;100(3):468–473.
460. Slavin ML. Transient comitant esotropia in a child with migraine.
Am J Ophthalmol 1989;107(2):190–191.
461. Smith C. Nuclear and infranuclear ocular motility disorders. In:
Miller N, Newman N (eds) Clinical neuro-ophthalmology. Baltimore: Williams & Wilkins, 1999:1238–1240.
462. Snead OC III, et al. Juvenile myasthenia gravis. Neurology 1980;30(7
pt 1):732–739.
463. Soliven BC, et al. Seronegative myasthenia gravis. Neurology
1988;38(4):514–517.
464. Spatz H, Ullrich O. Klinischer und anatomischer Beitrag zu den
angeborenen Beweglichkeitsdefekten im Hirnnervenbereich. Z
Kinderheilkd 1931;51:579–597.
465. Spielmann A, Richter J. Oculomotor surgery in Parinaud’s syndrome.
Ophtalmologie 1989;3(2):157–159.
466. Spierer A, Barak A. Strabismus surgery in children with Mobius
syndrome. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(1):58–
59.
467. Spiro AJ, et al. A cytochrome-related inherited disorder of the
nervous system and muscle. Arch Neurol 1970;23(2):103–112.
468. Spooner JW, Baloh RW. Eye movement fatigue in myasthenia gravis.
Neurology 1979;29(1):29–33.
469. Stamler J, Nerad J, Keech R. Acquired pseudo-Duane’s retraction
syndrome secondary to acute orbital myositis. Binoc Vision 1989;4:
103–108.
470. Stansbury J. Moebius’s syndrome. Am J Ophthalmol 1952;35:256–
261.
471. Starr A. A disorder of rapid eye movements in Huntington’s chorea.
Brain 1967;90(3):545–564.
472. Steinlin M, et al. Congenital oculomotor apraxia: a neurodevelopmental and neuroradiological study. Neuro-Ophthalmology 1990;10:
27–32.
473. Stell R, et al. Ataxia telangiectasia: a reappraisal of the ocular motor
features and their value in the diagnosis of atypical cases. Mov
Disord 1989;4(4):320–329.
474. Sternberg I, Ronen S, Arnon N. Recurrent, isolated, post-febrile
abducens nerve palsy. J Pediatr Ophthalmol Strabismus 1980;17(5):
323–324.
516
handbook of pediatric strabismus and amblyopia
475. Sudarshan A, Goldie WD. The spectrum of congenital facial diplegia
(Moebius syndrome). Pediatr Neurol 1985;1(3):180–184.
476. Sullivan S. Benign recurrent isolated VI nerve palsy of childhood.
Clin Pediatr 1985;24:160–161.
477. Summers CG, MacDonald JT, Wirtschafter JD. Ocular motor apraxia
associated with intracranial lipoma. J Pediatr Ophthalmol Strabismus 1987;24(5):267–269.
478. Swick HM. Pseudointernuclear ophthalmoplegia in acute idiopathic
polyneuritis (Fisher’s syndrome). Am J Ophthalmol 1974;77(5):725–
728.
479. Sydnor CF, Seaber JH, Buckley EG. Traumatic superior oblique
palsies. Ophthalmology 1982;89(2):134–138.
480. Tamura EE, Hoyt CS. Oculomotor consequences of intraventricular
hemorrhages in premature infants. Arch Ophthalmol 1987;105(4):
533–535.
481. Taylor MJ, Polomeno RC. Further observations on the auditory
brainstem response in Duane’s syndrome. Can J Ophthalmol 1983;
18(5):238–240.
482. Tekkok IH, et al. Bilateral intranuclear ophthalmoplegia associated
with fourth ventricular dermoid tumor. J Clin Neuroophthalmol
1989;9(4):254–257.
483. Teller J, Karmon G, Savir H. Long-term follow-up of traumatic unilateral superior oblique palsy. Ann Ophthalmol 1988;20(11):424–425.
484. Ter Bruggen JP, et al. Disorders of eye movement in myotonic dystrophy. Brain 1990;113(pt 2):463–473.
485. Terranova W, Palumbo JN, Breman JG. Ocular findings in botulism
type B. JAMA 1979;241(5):475–477.
486. Thomas R, et al. Bilateral synergistic divergence. J Pediatr Ophthalmol Strabismus 1993;30(2):122–123.
487. Tjissen C, Goor C, van Woerkom T. Spasm of the near reflex: functional or organic disorder? Neuro-Ophthalmology 1983;3:59–64.
488. Toshniwal P. Demyelinating optic neuropathy with Miller–Fisher
syndrome. The case for overlap syndromes with central and peripheral demyelination. J Neurol 1987;234(5):353–358.
489. Towfighi J, et al. Mobius syndrome. Neuropathologic observations.
Acta Neuropathol (Berl) 1979;48(1):11–17.
490. Traboulsi EI, Maumenee IH. Extraocular muscle aplasia in Moebius
syndrome. J Pediatr Ophthalmol Strabismus 1986;23(3):120–122.
491. Tredici TD, von Noorden GK. Are anisometropia and amblyopia
common in Duane’s syndrome? J Pediatr Ophthalmol Strabismus
1985;22(1):23–25.
492. Tripp JH, et al. Juvenile Gaucher’s disease with horizontal gaze palsy
in three siblings. J Neurol Neurosurg Psychiatry 1977;40(5):470–478.
493. Trobe JD, Glaser JS, Post JD. Meningiomas and aneurysms of the
cavernous sinus. Neuro-ophthalmologic features. Arch Ophthalmol
1978;96(3):457–467.
494. Trobe JD. Cyclodeviation in acquired vertical strabismus. Arch
Ophthalmol 1984;102(5):717–720.
chapter
12:
ocular motility disorders
517
495. Trobe JD. Third nerve palsy and the pupil. Footnotes to the rule.
Arch Ophthalmol 1988;106(5):601–602.
496. Troost BT, et al. Upbeat nystagmus and internuclear ophthalmoplegia with brainstem glioma. Arch Neurol 1980;37(7):453–456.
497. Tsai L, et al. Oculomotor apraxia in a case of Gaucher’s disease with
homozygous T1448C mutation. Chung Hua Min Kuo Hsiao Erh Ko
I Hsueh Hui Tsa Chih 1996;37:52–55.
498. Vajsar J, et al. Arthrogryposis multiplex congenita due to congenital
myasthenic syndrome. Pediatr Neurol 1995;12(3):237–241.
499. Valbuena O, et al. Ataxia telangiectasia: review of 13 new cases. Rev
Neurol 1996;24(125):77–80.
500. Valmaggia C, Zaunbauer W, Gottlob I. Elevation deficit caused by
accessory extraocular muscle. Am J Ophthalmol 1996;121(4):444–
445.
501. Vassella F, Lutschg J, Mumenthaler M. Cogan’s congenital ocular
motor apraxia in two successive generations. Dev Med Child Neurol
1972;14(6):788–796.
502. Velez FG, Clark RA, Demer JL. Facial asymmetry in superior oblique
muscle palsy and pulley heterotopy. J Am Assoc Pediatr Ophthalmol Strabismus 2000;4(4):233–239.
503. Versino M, et al. Lateral gaze synkinesis on downward saccade
attempts with paramedian thalamic and midbrain infarct. J Neurol
Neurosurg Psychiatry 1999;67(5):696–697.
504. Victor DI. The diagnosis of congenital unilateral third-nerve palsy.
Brain 1976;99(4):711–718.
505. Vincent C, et al. A proposed new contiguous gene syndrome on 8q
consists of branchio-oto-renal (BOR) syndrome, Duane syndrome, a
dominant form of hydrocephalus and trapeze aplasia; implications
for the mapping of the BOR gene. Hum Mol Genet 1994;3(10):
1859–1866.
506. Vincent FM, Vincent T. Relapsing Fisher’s syndrome. J Neurol Neurosurg Psychiatry 1986;49(5):604–606.
507. Vivian A, Harris C, Kriss A. Oculomotor signs in infantile Gaucher
disease. Neuro-Ophthalmology 1993;13:151–155.
508. von Ludinghausen M. Bilateral supernumerary rectus muscles of the
orbit. Clin Anat 1998;11(4):271–277.
509. von Ludinghausen M, Miura M, Wurzler N. Variations and anomalies of the human orbital muscles. Surg Radiol Anat 1999;21(1):
69–76.
510. von Noorden GK, Murray E. Up- and downshoot in Duane’s
retraction syndrome. J Pediatr Ophthalmol Strabismus 1986;23(5):
212–215.
511. von Noorden GK. A magnetic resonance imaging study of the
upshoot-downshoot phenomenon of Duane’s retraction syndrome.
Am J Ophthalmol 1991;112(3):358–359.
512. Wadia NH, Swami RK. A new form of heredo-familial spinocerebellar degeneration with slow eye movements (nine families). Brain
1971;94(2):359–374.
518
handbook of pediatric strabismus and amblyopia
513. Wadia NH, et al. A study of the neurological disorder associated with
acute haemorrhagic conjunctivitis due to enterovirus 70. J Neurol
Neurosurg Psychiatry 1983;46(7):599–610.
514. Wagner RS, Caputo AR, Frohman LP. Congenital unilateral adduction deficit with simultaneous abduction. A variant of Duane’s
retraction syndrome. Ophthalmology 1987;94(8):1049–1053.
515. Walsh F, Hoyt W. Clinical neuro-ophthalmology. Baltimore:
Williams & Wilkins, 1969.
516. Waterhouse WJ, Enzenauer RW, Martyak AP. Successful strabismus
surgery in a child with Moebius syndrome. Ann Ophthalmol 1993;
25(8):292–294.
517. Weeks CL, Hamed LM. Treatment of acute comitant esotropia in
Chiari I malformation. Ophthalmology 1999;106(12):2368–2371.
518. Weinacht S, Huber A, Gottlob I. Vertical Duane’s retraction syndrome. Am J Ophthalmol 1996;122(3):447–449.
519. Weinberg DA, Lesser RL, Vollmer TL. Ocular myasthenia: a protean
disorder. Surv Ophthalmol 1994;39(3):169–210.
520. Weintraub MI. External ophthalmoplegia, ataxia, and areflexia complicating acute infectious polyneuritis. Am J Ophthalmol 1977;83(3):
355–357.
521. Welch R. Chicken-pox and the Guillain–Barre syndrome. Arch Dis
Child 1962;37:557–559.
522. Werner DB, Savino PJ, Schatz NJ. Benign recurrent sixth nerve
palsies in childhood. Secondary to immunization or viral illness.
Arch Ophthalmol 1983;101(4):607–608.
523. Whitsel EA, Castillo M, D’Cruz O. Cerebellar vermis and midbrain
dysgenesis in oculomotor apraxia: MR findings. AJNR Am J Neuroradiol 1995;16(suppl 4):831–834.
524. Wieacker P, et al. A new X-linked syndrome with muscle atrophy,
congenital contractures, and oculomotor apraxia. Am J Med Genet
1985;20(4):597–606.
525. Wilcox LM Jr, Gittinger JW Jr, Breinin GM. Congenital adduction
palsy and synergistic divergence. Am J Ophthalmol 1981;91(1):1–7.
526. Williams AS, Hoyt CS. Acute comitant esotropia in children with
brain tumors. Arch Ophthalmol 1989;107(3):376–378.
527. Willison HJ, O’Hanlon GM. The immunopathogenesis of Miller
Fisher syndrome. J Neuroimmunol 1999;100(1–2):3–12.
528. Wilson ME, Hoxie J. Facial asymmetry in superior oblique muscle
palsy. J Pediatr Ophthalmol Strabismus 1993;30(5):315–318.
529. Wilson RS, Landers JH. Anomalous duplication of inferior oblique
muscle. Am J Ophthalmol 1982;93(4):521–522.
530. Wise GA, McQuillen MP. Transient neonatal myasthenia. Clinical
and electromyographic studies. Arch Neurol 1970;22(6):556–565.
531. Wishnick M, et al. Mobius syndrome and limb abnormalities with
dominant inheritance. Ophthalmic Pediatr Genet 1983;2:77–81.
532. Woods CG, Taylor AM. Ataxia telangiectasia in the British Isles: the
clinical and laboratory features of 70 affected individuals. Q J Med
1992;82(298):169–179.
chapter
12:
ocular motility disorders
519
533. Woody R, Reynolds J. Association of bilateral internuclear ophthalmoplegia and myelomeningocele with Arnold–Chiari malformation
type II. J Clin Neuroophthalmol 1985;5:124–126.
534. Woody RC, Blaw ME. Ophthalmoplegic migraine in infancy. Clin
Pediatr (Phila) 1986;25(2):82–84.
535. Wright PW, Strauss GH, Langford MP. Acute hemorrhagic conjunctivitis. Am Fam Physician 1992;45(1):173–178.
536. Wybar K. Disorders of ocular motility in brain stem lesions in children. Ann Ophthalmol 1971;3(6):645–647.
537. Yang MC, et al. Electrooculography and discriminant analysis in
Duane’s syndrome and sixth-cranial-nerve palsy. Graefe’s Arch Clin
Exp Ophthalmol 1991;229(1):52–56.
538. Yeh JH, et al. Miller Fisher syndrome with central involvement: successful treatment with plasmapheresis. Ther Apher 1999;3(1):69–71.
539. Yuki N. Pathogenesis of Guillain–Barre and Miller Fisher syndromes
subsequent to Campylobacter jejuni enteritis. Jpn J Infect Dis
1999;52(3):99–105.
540. Zaret CR, Behrens MM, Eggers HM. Congenital ocular motor apraxia
and brainstem tumor. Arch Ophthalmol 1980;98(2):328–330.
541. Zasorin NL, Yee RD, Baloh RW. Eye-movement abnormalities in
ophthalmoplegia, ataxia, and areflexia (Fisher’s syndrome). Arch
Ophthalmol 1985;103(1):55–58.
542. Zee DS, Yee RD, Singer HS. Congenital ocular motor apraxia. Brain
1977;100(3):581–599.
543. Zuker RM. Facial paralysis in children. Clin Plast Surg 1990;17(1):
95–99.
13
Optical Pearls and Pitfalls
David L. Guyton, Joseph M. Miller, and
Constance E. West
O
ptics and refraction are often thought of as a dry chapter in
ophthalmology, but understanding a few basic principles
enables one to avoid errors and complications when treating
both pediatric and adult strabismic patients.
REFRACTION AND REFRACTIVE ERROR
IN CHILDREN
Retinoscopy need not be limited to preverbal children following
cycloplegia. Dry retinoscopy is useful both in evaluating the
ability to accommodate and in serving as a quick assessment of
the present pair of glasses. To check the present correction, two
free lenses, a 1.50 D and a 2.00 D, are grasped between the
thumb and forefinger of one hand and held in front of the two
eyes. The patient is instructed to look at the distance fixation
target through the 2.00 D lens, thus relaxing accommodation.
The eye being evaluated is then checked with the 1.50 D lens
with the retinoscope on axis for neutrality.
Dynamic retinoscopy, performed to evaluate the effectiveness of accommodation, is performed without free lenses. One
eye of the subject is occluded. A fixation target is held just below
the peephole of the retinoscope, and the subject is instructed to
look first at a distance target, then at a near one. If the subject
is able to focus on the near target, the observer will see neutralization of the retinoscopy reflex. This test is most useful in
assessing the need for bifocal correction in an amblyopic eye. If
the child cannot readily accommodate and neutralize the reflex
at near, even if there is no element of accommodative esotropia,
a reading add should be considered. Performing dynamic
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retinoscopy with both the patient’s eyes open provides a good
screen for anisometropia or sphere imbalance in the glasses.
Cycloplegic refraction is an essential part of the examination of strabismic children and may be effected by several drugs
with different cycloplegic and mydriatic characteristics. The
agents most commonly used by strabismologists are atropine,
cyclopentolate, and tropicamide. Atropine blocks parasympathetic activity by competing with acetylcholine and therefore
prevents contraction of the ciliary muscle and iris sphincter.
Mydriasis is fully developed at 35 to 45 min, while cycloplegia
is not completed until 1 h after instillation of eyedrops. Atropine
has the longest duration of cycloplegia (up to 48 h) and mydriasis (up to several days) of the parasympatholytic drugs. Tropicamide 1% is a short-acting (3–6 h duration) mydriatic with a
rapid onset of cycloplegia (20–30 min). Cyclopentolate, like
tropicamide, is a synthetic parasympatholytic but seems to be a
more effective cycloplegic with peak accommodative paresis
between 25 and 35 min. Its mydriatic action may last for 24 h.
One cannot measure accommodative amplitude, reading adds
cannot be determined, and strabismic deviations are affected
after the administration of cycloplegic agents.
The authors’ preferred practice with children is to anesthetize the conjunctiva with a topical anesthetic, followed by
instillation of 1% cyclopentolate. The anesthetic seems to
lessen the discomfort caused by the cyclopentolate and has
the advantage of increasing its penetration into the anterior
chamber. Cyclomydril (cyclopentolate 0.2% and phenylephrine
hydrochloride 0.5%) or 0.5% cyclopentolate should be used in
neonates and infants. In adults who require a cycloplegic refraction, we use 1% tropicamide because of its shorter duration of
cycloplegia. When adequate cycloplegia cannot be effected in
the office (usually in children with darkly pigmented irises),
prescribe atropine sulfate 1%, one drop in each eye, morning
and evening for 2 days before the next visit. On the day of the
visit, a drop should be instilled in each eye 1 h before the
appointment.
Local allergic (hypersensitivity) reactions manifested by
conjunctivitis, swollen lids, and periocular dermatitis are occasionally seen with atropine administration but rarely, if ever,
with tropicamide or cyclopentolate. All cycloplegic medicines
have potential systemic side effects: flushing, fever, dry skin and
mucous membranes, tachycardia, restlessness, hallucinations,
seizures, and even death, especially in the smallest and most
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lightly pigmented children. Severe reactions are rare but may
require administration of intravenous physostigmine (0.5–
1.0 mg in children, 1–4 mg in adults, administered as a 0.2 mg/ml
solution over at least 2 min). Systemic side effects may be lessened by occluding the canaliculi and preventing absorption by
the nasal mucosa. Special care must be taken when atropine is
given for administration at home, where the dose given is less
controlled than in the office. One 50-␮l drop of 1% atropine
sulfate contains 0.5 mg of atropine, whereas the dose of atropine
in resuscitation of the infant and child is 0.01 to 0.03 mg/kg! Be
particularly careful in small babies and children with heart
disease.
Most neonates (approximately 75%) are hyperopic.2 The
hyperopia is usually symmetrical and less than 4 D.8 It is also
known that the degree of hyperopia usually increases until about
the age of 7 years.1 The increase in hyperopia during early childhood also seems to apply to neonates born myopic and results
in loss of myopia in those neonates born with a small amount
of myopia.5 Thus, the majority of children examined have some
degree of refractive error.
PRESCRIBING GUIDELINES AND
LENS TYPES
Once the refractive error has been determined, a decision must
be made about whether to give the correction. In the absence of
strabismus, the decision as to when to prescribe the correction
must be made based on the magnitude of the error, the patient’s
ability to accommodate, the visual needs of the individual, and
the risk of refractive and/or anisometropic amblyopia. There are
few data regarding who should receive glasses, but some
common sense and general guidelines are helpful.
Myopic children should receive correction when their
uncorrected binocular visual acuity is 20/30 or worse. This level
of acuity frequently occurs at 1.50 D in both eyes and is the
threshold to follow for simple, symmetrical myopia. Hyperopia
has no such simple guideline, as there is a tremendous variation
in how children respond to an accommodative demand. Many
children will not accommodate consistently at a level above
5.00 D and will require at least partial correction to allow for
normal visual development. For high hyperopia, which is
usually accompanied by subnormal accommodation, prescribe
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the full hyperopic correction (perhaps cut by 0.50 D), especially
when there is abnormal visual function.
It is a little easier to determine when to prescribe glasses in
the presence of anisometropia. If both eyes are developing
normal visual acuity and normal binocular function is present,
no glasses are given. However, if anisometropic amblyopia is
present (usually in the more ametropic eye), glasses must be prescribed. In anisometropic hyperopic amblyopia, the full correction need not be prescribed so long as the correction is reduced
equally in each eye. In anisometropic myopic amblyopia, the full
correction should be given. Pay careful attention to accommodative abilities when children are forced to fix with an amblyopic eye. A reading add may hasten treatment of the amblyopia
during occlusion or atropine penalization therapy, although this
has not been proven conclusively.
If glasses are to be prescribed for a significant spherical error,
any astigmatic error should be corrected as well. Astigmatic correction is given by itself when the child is not developing normal
visual acuity; this usually occurs with 1.50 D or more of astigmatism. Children readily accept the full cylindrical correction
at the proper axis, and it should be prescribed as such (not always
the case with adults). Strabismus surgery can affect the refractive error, particularly the astigmatic component, and refraction
should be rechecked after strabismus surgery.
In the presence of high refractive errors, it is best to overrefract the individual and then read the resultant correction by
placing both the free lenses and the glasses in a lensometer.
Errors induced by changes in pantoscopic tilt or vertex distance
will be eliminated.
When strabismus coexists with a refractive error or an
abnormal accommodative convergence/accommodation ratio,
the full cycloplegic refraction should be given, adding bifocals if
an esodeviation is still present at near. If alignment is not
attained or maintained with spectacle correction, surgery may
be considered. Bifocals, when used for the treatment of accommodative esotropia with a high accommodative convergence/
accommodation ratio, should be fit high, usually with the top
of the segment bisecting the pupil. Executive-style bifocals are
commonly prescribed, but large, “D”-shaped (flat-top) segments
are frequently less expensive, lighter in weight, and provide adequate field in pediatric patient frames. Progressive style bifocals
have been advocated by some authors,3 but one should remember that the transitional zone is usually 12 mm in vertical extent
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and may render the most powerful part of the segment useless
to pediatric patients. It is often prudent to specify a lens with
high impact resistance (polycarbonate) for monocular and
amblyopic children; special recreation spectacles are particularly
appropriate for this population. Lens coating and filters are
sometimes included in children’s corrective lenses. Ultraviolet
protection should be considered for children with aphakia, lens
implants, or maculopathy and for those children undergoing
atropine penalization. Tinted and photochromic lenses, both of
which are now available in glass or plastic, often provide comfort
for patients with aniridia, ocular albinism, or oculocutaneous
albinism.
THE CORNEAL LIGHT REFLEX
AND STRABISMUS
The corneal light reflex (the first Purkinje–Sanson image) is a
virtual image located 4 mm behind the cornea and may be
thought of as located on an imaginary string connecting the
center of curvature of the cornea with the fixation light. To avoid
errors from parallax in the Hirschberg or Krimsky4 test, the
examiner’s eye must be directly behind the fixation light.
To produce Hirschberg test photographs of strabismic
patients, the electronic flash should be held directly below, or
above, the camera lens, with a fixation object placed between
the flash and the lens. Reflection of the camera flash in the
patient’s glasses can be detected by a handlight before taking the
photograph and avoided by raising the temples, thus increasing
the pantoscopic tilt of the glasses.
MEASUREMENT AND CORRECTION OF
STRABISMIC DEVIATIONS WITH PRISMS
Misalignment of the visual axes may be measured in degrees or
prism diopters (PD). While strabismic deviations are measured
in degrees in Europe, it is more common to quantify them in PD
in the United States. Glass and plastic prisms are made with
nonparallel surfaces that deviate light rays passing through
them. The power of a prism (glass or plastic) in PD () is equal
to the displacement, in centimeters, of a light ray passing
through the prism, measured 100 cm from the prism (Fig. 13-1).
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525
FIGURE 13-1. A 15 prism displaces a light ray 15 cm when measured
100 cm from the plane.
Remember, when converting PD to degrees, that each degree is
not exactly equal to 2 ; the relationship is a trigonometric one
(degrees tan1(/100). For amounts less than 45° (100 ), the
relationship of 2 per degree is roughly correct but, beyond 45°
(100 ), the number of PD per degree increases rapidly without
bounds, rising to an infinite number of PD at 90°.
Variability in strabismus surgery may result, in part, from
incorrect use of prisms when measuring strabismic deviations
preoperatively. Knowledge of these potential errors helps the
ophthalmologist minimize their effects. These errors occur
when prisms are incorrectly positioned or stacked in the same
direction and when measuring deviations through high minus
and high plus lenses.
Ophthalmic prisms are made of either glass or plastic, and
the amount of strabismic deviation neutralized (or produced) by
the prism varies with the position in which it is held. There are
three commonly used positions for holding ophthalmic prisms:
Prentice position, minimum deviation position, and frontal
plane position (Fig. 13-2). Glass prisms are calibrated for use in
the Prentice position, which requires the patient’s line of sight
to strike the rear (or front) surface of the prism at right angles.
Small errors in holding glass prisms may produce large errors in
the amount of deviation neutralized. For example, if the rear
surface of a 40 glass prism is held in the frontal plane rather
than in the Prentice position, the effect is only 32 .9
Plastic prisms and prisms bars are calibrated for use in the
position of minimum deviation and, in this position, the line of
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handbook of pediatric strabismus and amblyopia
FIGURE 13-2. The three common positions for use of ophthalmic prisms
with fixation at a distance: left, Prentice position; center, minimum deviation position; right, frontal plane position at distance (solid lines) and
near (dashed lines). Plastic prisms should be held in the frontal plane position, and glass prisms are calibrated to be held in the Prentice position.
sight makes an equal angle with each of the faces of the prism.
In clinical practice, however, the position of minimum deviation may be difficult to judge. Holding the rear surface of the
prism in the frontal plane of the patient very nearly produces
the minimum deviation for that prism. Note, however, that if
the rear surface of a 40 plastic prism is held in the Prentice
position (a large error in holding a plastic prism) rather than in
the frontal plane, the effect is 72 rather than 40 . Small errors
in holding plastic prisms (in the frontal plane position instead
of the minimum deviation position) produce only small errors
in the amount of deviation neutralized. Thus, plastic prisms are
less prone to position error than glass prisms and are preferable
for this reason.
The common practice of “stacking” two prisms together in
the same direction to measure large deviations (greater than
50 ) may induce large errors. Glass prisms are available to a
maximum of 40 and plastic prisms are available to a maximum
of 50 . Prisms do not add linearly when stacked together in the
same direction and should never be stacked together in that
manner. Even though the rear surface of one of the prisms may
be held in the correct position, the other prism is far from its
calibrated position, and a much greater effect is produced than
anticipated. For instance, a 3 plastic prism added to a 50 plastic prism gives a 58 effect.9 When measuring large deviations, prisms are best held before both eyes, although there is
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527
still some additivity error in doing this. The additivity errors
induced have been tabulated by Thompson and Guyton9 or may
be calculated with a formula. Fortunately, additivity error is not
significant when adding a vertical prism to a horizontal one.
Thus, a vertical and a horizontal prism may be stacked together
with no significant interaction between the two when measuring a combined horizontal and vertical deviation.
When measuring strabismic deviations with a fixation target
at near, the distance from the eye to the prism must be acknowledged. The amount of prism necessary to neutralize a deviation
at near fixation increases as the prism is held farther away from
the eye; this effect may lead to overcorrections when the surgery
is calculated on the basis of the near deviation.10
An additional error may result when measuring strabismic
deviations through glasses, even when prisms are held in the
proper position.7 This error is also present when measuring the
deviation by the Krimsky prism reflex test or subjective
methods. Both lines of sight of a strabismic patient cannot pass
through the optical centers of the respective spectacle lenses;
thus, glasses produce a prismatic change of the deviation as
measured in front of the glasses. This peripheral prismatic effect
begins to become clinically significant with spectacle lenses of
more than 5 D (minus or plus). Minus lenses increase the measured angle of deviation, and plus lenses decrease the measured
angle, whether the deviation is esotropia, exotropia, or hypertropia. The distance deviation is changed by approximately (2.5)
(D)%, where D is the spectacle power. For example, a 10 D
bilateral high myope with 40 of exotropia will measure (2.5)
(10)% more than 40 , or 50 , through the glasses. A helpful
mnemonic is “minus measures more.”
When calculating and prescribing oblique prisms, remember
that prisms add as ordinary vectors, so a horizontal prism may
be combined with a vertical prism and prescribed as a single
prism at an oblique angle. The power and orientation of the
prism may be determined by using a prism nomogram (Fig.
13-3), or by marking off proportional distances from the corner
of a piece of paper, forming two sides of a right triangle. The
third side of the triangle is proportional to the amount of oblique
prism needed, and the orientation can be determined by folding
the paper and measuring the appropriate angle with the protractor on a trial frame. The orientation of the prism base should
be specified in the appropriate meridian, but note that over the
left eye, for example, “base in the 135° meridian” is ambiguous.
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PR
IS
M
RO
T
IO
AT
N
G
AN
LE
FIGURE 13-3. Prism nomograph. To use the nomograph, determine the
amount of vertical and horizontal prism needed to neutralize the deviation and then locate their intersection on the nomograph. The quarter
circle nearest their intersection is the power of the prism to be used.
Locate the intersection of this quarter circle and the amount of vertical
prism determined on prism and cover test. A line drawn through this
point and the origin intersects the prism rotation angle scale and determines the proper orientation of the oblique prism.
The base must be specified either as “base up and in at the 135°
meridian” or as “base down and out in the 135° meridian.” Horizontal, vertical, or oblique prisms may be ground into spectacle correction, or Fresnel Press-On prisms may be applied to
existing lenses.
When one measures incomitant deviations with the prism
and cover test,6 the deviation should always be neutralized with
the prisms placed before each eye in turn. Only the eye not
looking through the prism is truly pointing in the desired direction of gaze during testing. In this case, therefore, the “fixing
eye” must be defined as the eye not looking through the prism;
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the position of the cover makes no difference. Once an incomitant deviation is neutralized with prism(s), no movement of
either eye should be seen on movement of the cover from one
eye to the other, unless a dissociated horizontal or vertical
deviation is also present.
When determining the amount of prism ground into, applied
to, or caused by decentration (intentional or unintentional) of
spectacles, it is important to measure the effective prism in the
part of the lens through which the patient is looking. While the
patient is looking through the spectacles, mark that point with
the edge of a piece of paper tape. Then, measure the amount and
orientation of the prism by placing this mark in the center of
the nosecone of the lensometer.
References
1. Brown EVL. Net average yearly change in refraction of atropinized
eyes from birth to beyond middle age. Arch Ophthalmol 1938;19:
719–734.
2. Cook RC, Glasscock RE. Refractive and ocular findings in the
newborn. Am J Ophthalmol 1951;34:1407–1412.
3. Jacob J-L, Beaulieu Y, Brunet E. Progressive addition lenses in the
management of esotropia with a high accommodation/convergence
ratio. Can J Ophthalmol 1980;15:166–169.
4. Krimsky E. Fixational corneal light reflexes as an aid in binocular
investigation. Arch Ophthalmol 1943;30:505–521.
5. Mohindra I, Held R. Refractions in humans from birth to 5 years. In:
Fledelius HC, Alsbirk PH, Goldschmidt E (eds) Documenta Ophthalmologica Proceeding Series, vol 28. The Hague: Junk, 1981.
6. Repka MX, Kelman S, Guyton DL. Prism measurement of incomitant strabismus. Binoc Vis 1985;1:45–49.
7. Scattergood KD, Brown MH, Guyton DL. Artifacts introduced by
spectacle lenses in the measurement of strabismic deviations. Am J
Ophthalmol 1983;96:439–448.
8. Slataper FJ. Age norms of refraction and vision. Arch Ophthalmol
1950;43:466–481.
9. Thompson JT, Guyton DL. Ophthalmic prisms: measurement errors
and how to minimize them. Ophthalmology 1983;90:204–210.
10. Thompson JT, Guyton DL. Ophthalmic prisms: deviant behavior at
near. Ophthalmology 1985;92:684–690.
Index
A
Abduction
deficits of
in Duane’s syndrome, 356,
357, 358, 359, 361
in infantile/congenital
esotropia, 226, 227
in Möbius syndrome,
364–365
definition of, 27
AC/A ratio. See Accommodative
convergence
Accommodation
in convergence, 99
deficiency of, 280
definition of, 161
normal development of, 7
relationship with convergence,
161
retinoscopic evaluation of,
520–521
Accommodative convergence (AC/A
ratio), 99, 161–164
definition of, 161
in esotropia, 99
in accommodative esotropia,
243, 246–247
in exotropia, 99
in intermittent exotropia, 269,
271, 272, 275
with true divergence excess,
271, 272, 275
measurement of, 161–164
heterophoria method, 161–162
lens gradient method, 161–162,
163–164
Accommodative insufficiency, 280
Accommodative near targets, 3
Active forced-generation test, 169, 170,
171–172
Adduction
deficits of
in Brown’s syndrome, 306,
315, 316
differential diagnosis of, 306,
316
in Duane’s syndrome, 356–357,
358, 359, 360, 361, 362
definition of, 27
Adhesive syndrome, 334
Adie’s pupil, as accommodative
insufficiency cause, 280
Adjustable suture technique,
394–396
Afterimage test, 209–212
Albinism
ocular, congenital exotropia
associated with, 281
oculocutaneous, Duane’s
syndrome-related, 359
Alcohol use, exotropia-inducing effect
of, 266
Alcon Corporation, 17
Allen picture cards, 3, 11, 118, 141
Amblyopia, 108–125
ametropic (bilateral
hypermetropic), 115–116
anisometropic, 114–115
myopic, lens-based correction
of, 523
part-time occlusion therapy
for, 130
astigmatic, 113, 114
bilateral meridional, 116
binocular fixation preference
testing in, 8
classification of, 114
bilateral blurred retinal image,
110, 115–116
strabismic, 84, 110
531
532
index
Amblyopia (Continued)
unilateral pattern distortion,
110, 113, 115
congenital exotropia-related, 281
cortical suppression in, 107, 109
cranial nerve III palsy-related, 442
cranial nerve VI palsy-related, 446
definition of, 108–109
diagnosis of, 7–11, 118–125,
140–141
with fixation testing, 119–122
with vertical prism testing,
122–125
with visual acuity testing, 118
dissociated vertical deviationrelated, 373
Duane’s syndrome-related, 360–361
esotropia associated with, 223
ex anopsia, 109
extrafoveal fixation associated
with, 117
functional, 109
hypermetropic, 114, 115
bilateral, 115–116
intermittent exotropia surgeryrelated, 274
lateral geniculate nucleus (LGN)
in, 110, 111, 190
Marcus Gunn jaw-winking-related,
468–469
monofixation syndrome-related,
182
myopic, 115
occlusion therapy for, effect on
contrast sensitivity, 14
organic, 109
pathology of, 109–110
pattern distortion in, 109
unilateral, 110, 113, 114, 115
prevalence of, 108
prognosis for, 133
reverse
penalization-related, 131
prevention of, 130
stereopsis in, 114
strabismic, 84, 110
testing for, 116
treatment of, 127–133
for clear retinal image, 127,
128
ocular dominance correction
in, 130–133
Amblyoscope, use in haploscopic tests,
204, 205–209
American Optical Hardy-Rand-Rittler
(AO-HRR) plates, 13
Amniotic membrane transplantation,
334
Amputation defects, Möbius syndromerelated, 364
Anencephaly, extraocular muscle
aplasia-related, 365
Anesthesia. See also Sedation
physical examination under, 5
Angiography, of the iris, 59, 60
Angle kappa, 145–149
differentiated from tropias, 149
negative, 147
positive, 146–147, 148
physiological, 149
Anisekonia, 177
Anisometropia
as anisekonia cause, 177
astigmatic, 127, 128
dynamic retinoscopic evaluation
of, 520–521
hypermetropic, 127, 128
lens-based correction of, 523
Marcus Gunn jaw-winking-related,
468–469
myopic, 127, 128
red reflex test in, 128, 129
Anomalous retinal correspondence. See
Retinal correspondence, anomalous
(ARC)
Anteriorization (anterior transposition),
inferior oblique, 45–47, 311–312,
407–410
as dissociated vertical deviation
treatment, 373
graded anteriorization technique of,
47
J-deformity associated with, 46–47,
312, 409, 410
as ocular restriction cause, 46–47,
327
Anterior segment
ischemia of, 59–60, 354, 406
vascular supply to, 58–60
Anterior segment procedures,
medial rectus muscle damage during,
34
Antiacetylcholine drugs, as myasthenia
gravis cause, 470, 471, 475–476
Antiarrhythmic drugs, as myasthenia
gravis cause, 472
Antibiotics, as myasthenia gravis
cause, 472
index
Anticholinesterase drugs, as
myasthenia gravis cause, 472
Anticonvulsant drugs, as myasthenia
gravis cause, 472
Antisaccades, 425
Antisuppression therapy
as diplopia cause, 273
as horror fusionis cause, 189–190
Aphakia, ultraviolet protection in, 524
ARIX gene mutations, 339–340
Arnold-Chiari malformations, 431,
441
Asthenopia
convergence insufficiency-related,
277, 280
intermittent exotropia-related,
267
Astigmatism
bilateral, 116, 127, 128
corneal, 17
lens-based correction of, 523
Atropine, as cycloplegic agent, 18, 19,
172, 244, 521
contraindications to, 18
dosage of, 522
side effects of, 521
use in heart disease patients, 522
Atropine penalization, 130–131, 523
ultraviolet protection during, 524
Autorefractors, 20
Axes of Fick, 61
B
Bagolini striated lens test, 179–180,
181, 184, 185, 190, 202–203
Bell’s palsy, recurrent, 459
Bell’s phenomenon, 4, 16–17, 431
in cranial nerve III palsy, 364
in dorsal midbrain syndrome,
436
in double elevator syndrome, 439
in Kearns-Sayre syndrome, 481,
484–485
in myotonic dystrophy, 486
Bielschowsky head tilt test, 65
Bifocals
for accommodative esotropia,
523–524
for high-accommodative
convergence esotropia, 247
Bifoveal vision (bifixation), 81
Binocular cortical cells, 70
Binocular eye movements, yoke
muscles in, 64
533
Binocular fusion
in Duane’s syndrome, 358, 359
head posturing associated with, 139
in horror fusionis, 188–190
Binocular sensory testing, 139
Binocular vision
definition of, 70
development of, 104–105
cortical suppression-related
abnormality in, 107
infantile esotropia-related
impairment of, 220
motor fusion in, 70, 81–83
sensory fusion in, 70–83
binocular cortical cells in, 70,
71
corresponding retinal points
in, 70–71
definition of, 70
disparate images in, 72
empirical horopter in, 71, 72,
73, 74–75
noncorresponding retinal
points in, 72, 73
Panum’s fusional area in, 72,
73, 74
stereoacuity testing in, 76–80
stereoscopic vision in, 72,
74–75
Vieth-Müller circle in, 71, 72
Blebs, pseudo-Brown’s syndromerelated, 349, 350
Blepharoptosis, congenital fibrosis of
the extraocular muscles-related, 339
Blindness. See also Visual loss/
impairment
unilateral, as sensory esotropia
cause, 261–262
Blinking, “synkinetic,” 433–434
Blink response, normal development of,
7
Blurred vision
convergence insufficiency-related,
277, 280
intermittent exotropia-related, 267
Botulinum toxin, 419–420
as cranial nerve VI palsy
treatment, 446
as intrafacial synkinesis treatment,
469
Botulism, 478–479
Brain lesions. See also Brainstem
tumors; Brain tumors
contrast sensitivity in, 14
534
index
Brainstem
anomalies of, as neural integrator
abnormality cause, 431
lacunar infarcts of, 302
role in eye movements, 430
in saccadic eye movements,
427, 428, 437
Brainstem tumors
as internuclear ophthalmoplegia
cause, 441
as saccade initiation cause, 434
Brain tumors
as cranial nerve VI palsy cause, 352
as esotropia cause, 445
as eye movement disorder cause,
431
as superior oblique paresis cause,
302
Break point, 278
Bridle-effect theory, of Duane’s
syndrome, 147–148
Brown’s syndrome, 312–319
acquired, 312, 314, 315–316
idiopathic, 315, 316
inflammatory, 315, 316
as ocular restriction cause, 326
as “canine tooth syndrome,” 319
classification of, 312, 314
clinical features of, 314–315
congenital (“true”), 312, 313,
314–315, 316–319
as ocular restriction cause, 326
surgical treatment of, 317–319
differentiated from
inferior oblique paresis, 305,
306
monocular elevation deficit
syndrome, 341
primary superior oblique
overaction, 306, 307
etiology of, 312–314
iatrogenic, 303–304, 412, 413
limited elevation in adduction
associated with, 314–315
pseudo-, 327
surgical treatment of, 414, 416
Y-pattern strabismus associated
with, 285
Brückner reflex test, 15, 149–150
in accommodative esotropia, 249
corneal light reflex in, 126, 127
in Duane’s syndrome, 358
in manifest latent nystagmus, 258
red reflex in, 126, 127
C
Calipers, 3
Campylobacter jejuni infections,
457–458, 459
CAM therapy, for amblyopic eyes, 133
Cancer. See also specific types of
cancer
myasthenia gravis associated with,
476
“Canine tooth syndrome,” 319
Capsulopalpebral fascia, 36–37, 38–39
Cataracts
congenital, early detection and
treatment of, 125, 127, 128
effect on red reflex test, 126–127
unilateral
as horror fusionis cause,
188–189
as sensory exotropia cause,
281
Caudal pons, role in saccadic eye
movements, 429, 438
Central fixation, as visual development
milestone, 106–107
Central nervous system
malformations of, saccade
initiation failure associated with,
434
motility disorders of, 423–470
anomalies of innervation,
460–467
internuclear ophthalmoplegia,
440–441
ocular motor cranial nerve
palsies, 442–470
supranuclear disorders,
432–440
Central nervous system depressants,
phoria-inducing effect of, 85
Cerebellitis, as cranial nerve VI palsy
cause, 443
Cerebellum
anomalies of, as neural integrator
abnormality cause, 431
role in eye movements, 430
Cerebral palsy, congenital exotropia
associated with, 281
Check ligaments, 54, 57–58
Chin depression, 373–374, 375
surgical treatment of, 378
Chin elevation, 373–374
Brown’s syndrome-related, 315
monocular deficit syndromerelated, 341
index
Chin elevation (Continued)
ptosis-related, 374, 378–379
surgical treatment of, 378
Chloral hydrate, 4, 5, 17
Chronic progressive external
ophthalmoplegia (CPEO), 482–483
Cianci’s syndrome, 228–231, 232, 237,
256
Ciliary arteries, anterior and posterior,
58–58
in muscle transposition surgery,
404, 406
City University Color Vision Test
(TCU test), 13
Clefts, oral or facial, Möbius syndromerelated, 364
Clinical distance-near relationship, 164
Clostridium botulinum, 478
Club foot, Möbius syndrome-related,
364
Coenzyme Q10, as Kearns-Sayre
syndrome treatment, 484
Cogan’s lid switch sign, 474
Collicular plate sign, 435
Collier’s sign, 436
Color vision assessment, 12–13
Confusion, visual, 81, 177–178
definition of, 349, 351
glaucoma-related, 349, 351
Congenital Esotropia Observational
Study (CEOS), 221–225, 228, 233
Congenital fibrosis of the extraocular
muscles (CFEOM), 339–340
Congenital fibrosis syndrome, 231–232,
237
differentiated from infantile/
congenital esotropia, 219, 220
as ocular restriction cause, 325, 326
Conjunctivitis, acute hemorrhagic,
459–460
Contact lens, occlusive, as amblyopia
treatment, 131
Contour stereoacuity test, 77, 78–80
monocular clues in, 78–79
Contrast dyes, as myasthenia gravis
cause, 472
Contrast sensitivity, assessment of,
13–14
Contrast sensitivity function, 14
Contrast sensitivity threshold, 13–14
Convergence, 82–83
accommodative. See
Accommodative convergence
(AC/A ratio)
535
fusional, 95, 98
tonic, 99
normal amplitude of, 96
proximal or instrument, 100
relationship with
accommodation, 161
interpupillary distance, 161
voluntary, 99
Convergence exercises, for convergence
insufficiency, 278–279
Convergence insufficiency, 277–280
Convergence spasm, 439–440
Cornea, shape of, assessment of, 17
Corneal light reflex, 524
Corneal light reflex test. See
Hirschberg test
Corneal-pupillary axis, angle kappa of,
145–149
Cortical and basal ganglia dysplasia, 339
Cortical suppression
in amblyopia, 107, 109
definition of, 84
as saccadic omission, 30
in sensory adaptations to
strabismus, 178
Worth 4-dot test in, 199
Cover tests, 4, 150–159, 528–529
alternate cover test, 152–153, 154,
157
for cardinal positions of gaze
measurement, 155
cover/uncover test, 149, 150–152,
154
interpretation of, 152, 154
prism alternate cover test, 154
simultaneous prism cover test,
155–157
variable measurements in, 154–155
Cranial nerve(s)
palsies of, 442–460
combined, 456–457
general considerations in,
456–457
paresis of, 323–324
Cranial nerve III
anomalies of, 462–463, 467–468
Marcus Gunn jaw-winking,
468–469
oculomotor synkinesis, 467
vertical retraction syndrome,
467–468
congenital fibrosis of the
extraocular muscles-related
abnormalities of, 340
536
index
Cranial nerve III (Continued)
in Duane’s syndrome, 355, 359
as inferior oblique muscle
innervation, 45
as inferior rectus muscle
innervation, 36
as medial rectus muscle
innervation, 34
palsies of, 362–364, 452–456
amblyopia associated with, 442
congenital, 363–364, 454–455
with cyclic spasms, 455
partial, 453
traumatic, 453, 454, 456
treatment of, 363–364
role in eye movements, 424–425
in supranuclear eye
movements, 427, 428
as superior rectus muscle
innervation, 36
Cranial nerve IV
congenital fibrosis of the
extraocular muscles-related
abnormalities of, 340
palsies of, 446–452
superior oblique, 446–447,
449–450, 451
traumatic, 451–452
role in eye movements, 424–425
in supranuclear eye
movements, 427
as superior oblique muscle
innervation, 42
in traumatic superior oblique
paresis, 299–300
Cranial nerve V, palsies of, 459–460
Cranial nerve VI
agenesis of, as Duane’s syndrome
cause, 355, 356–357
anomalies of, 460–467
in Duane’s syndrome, 460–466
in synergistic divergence,
466–467
immaturity of, as infantile
esotropia cause, 220
nucleus lesions of, 440
palsies of, 101, 443–446
botulinum toxin treatment of,
353–355, 419–420
causes of, 352
congenital, 352
differentiated from infantile/
congenital esotropia, 219,
220
face turning associated with,
375
forced-generation test of, 169,
170
as lateral rectus muscle
weakness cause, 226
lid fissure widening associated
with, 332, 353
Möbius syndrome-related,
364
as paralytic strabismus cause,
352–355
surgical treatment of, 353,
354–355
traumatic, 352–353
paresis of, Faden operation for, 400,
402
role in eye movements, 424–425
in supranuclear eye
movements, 427, 428
Cranial nerve VII
anomalies of, 469–470
in Möbius syndrome, 489–490
palsies of, 459–460
Cranial nerve XI, in Möbius syndrome,
489–490
Cranial nerve XII, in Möbius syndrome,
489–490
Craniofacial anomalies
congenital exotropia associated
with, 281
Möbius syndrome-related,
364
Craniofacial dysostosis, extraocular
muscle aplasia-related, 365
Craniosynostosis, 369
ocular restriction associated with,
325, 327
Cross-fixation, 123
Cianci’s syndrome-related, 228,
230, 231
Crowding phenomenon, 116
Cycloduction, 27, 62
Cyclomydril, 18, 521
Cyclopentolate, as cycloplegic agent,
18, 19, 172, 244, 521
Cyclopentolate test, for atropine
penalization evaluation, 131
Cycloplegia, 17–20
Cycloplegic agents. See also specific
cycloplegic agents
side effects of, 521–522
Cyclotropia, 88
Cysts, of the iris, 253–254
index
D
Demerol, 4
Denver Developmental Scale, 2
Depth perception, monocular, 80–81
Dermoids, limbal, 17
Dextroversion, 67
Diabetes mellitus, as superior oblique
paresis cause, 302
Diplopia
acquired strabismus-related, 139,
174–177
antisuppression orthotopic therapyrelated, 273
convergence insufficiency-related,
277
crossed, 75, 177
in anomalous retinal
correspondence, 183, 184
exotropia-associated, 203
head posturing associated with,
378
heterotropia-related, 84
horror fusionis-related, 188–189
intermittent exotropia-related, 267
Miller Fisher syndrome-related,
458
paradoxical, 182, 184
physiological, 73, 75–76
prism-induced, 95
torsional, retinal surgery-related,
348, 349
uncrossed, 75–76, 175, 177
esotropia-associated, 203
Diplopia tests, 190–204
Bagolini striated lens test, 179–180,
181, 184, 185, 190, 202–203
dissociating, 190, 193
Maddox rod test, 88, 165, 167, 190,
204, 301, 302, 307
red filter test, 190, 191, 192,
193–196
vertical prism red filter test, 196,
197, 198
Worth 4-dot test, 190, 196,
199–202
Dissociated horizontal deviation
(DHV), 373
Dissociated vertical deviation (DVD),
370–373
asymmetrical, 370
bilateral, 370, 371, 373
definition of, 370
differentiated from inferior oblique
muscle overaction, 310
537
infantile/congenital esotropiarelated, 225
inferior oblique overaction-related,
312
latent, 370
neurophysiological basis for, 372
primary, 370, 371
relationship with infantile
esotropia surgery, 372–373
treatment of, 373
with superior oblique
weakening procedure, 308
Divergence, 83
fusional, 95
normal amplitude of, 96
as position of rest, 26
Divergence insufficiency, 261
Divergence paresis, cranial nerve VI
palsy-related, 352
“Dog on a leash” eye movement, 169,
171, 328
Doll’s head (oculocephalic) maneuver,
431
for double elevator palsy
evaluation, 439
for infantile esotropia evaluation,
220, 221
for ocular motor cranial nerve
palsy evaluation, 442
Donder’s law, 61–62
Dorsal midbrain syndrome, 435–438
Dorsolateral pontine nuclei (DLPN),
430
Dorsumduction, 27
Double elevator palsy, 316, 340–342,
439
Marcus Gunn jaw-winking-related,
468–469
Double vision. See Diplopia
Duane’s cocontraction syndrome,
355–356
Duane’s syndrome, 355–362, 443
A- and V-pattern strabismus
associated with, 284
adduction deficits associated with,
310, 356–357, 358, 359, 360, 361,
362
bilateral, 359
bridle-effect theory of, 463–464
cause of, 355
cranial nerve IV anomalies
associated with, 460–466
differentiated from infantile/
congenital esotropia, 219, 220
538
index
Duane’s syndrome (Continued)
esotropia associated with, 219
face turning associated with, 375
horizontal rectus muscle
cocontraction in, 32, 34
lateral rectus muscle weakness
associated with, 226
limited adduction associated with,
325, 326
Marcus Gunn jaw-winking-related,
469
medial and lateral rectus muscle
contraction in, 64
suppression associated with, 188
surgical treatment of
for Duane’s syndrome type I,
361
for Duane’s syndrome type III,
361
for globe retraction, 361–362
indications for, 359–361
for upshoot and downshoot
correction, 362
as synergistic divergence, 356, 357,
359
type I, 356, 357, 359
type II, 356, 357
type III, 356, 357, 359
X-pattern strabismus
associated with, 286
unilateral, 359
Y-pattern strabismus associated
with, 285
Ductions, 26–27, 63, 64, 65, 141, 142
forced. See Forced-duction testing
limited, 323
Dysplasia, cortical and basal ganglia,
339
E
Eccentric fixation, 7
amblyopia-related, 117
differentiated from anomalous
retinal correspondence, 184,
186
testing for, 117, 119
E game. See Illiterate E game
Electromyography (EMG), in agonist
and antagonist muscles, 63–64
Electro-oculography (EOG), 169
for cranial nerve VI palsy
evaluation, 171
for horizontal and vertical eye
movement measurement, 328
Empirical horopter, 71, 72, 73, 74–75
in stereoscopic vision, 74–75
Endophthalmitis, red reflex in, 15
Enophthalmos, 24
orbital floor fracture-related, 342
Epicanthal folds, in pseudo-strabismus,
229
Epstein-Barr virus infections, as
Guillain-Barré syndrome risk factor,
457–458
Esophoria, 255
definition of, 86
divergence-based control of, 95
Esotropia, 217–265
accommodative, 243
bifocals for, 523–524
hypermetropic, 243–246
accommodative convergence
(AC/A ratio) in, 99, 243, 246–247
acquired, 243
nonaccommodative, 254–255
acute comitant, 443–444
anomalous retinal correspondence
associated with, 197
binocular vision in, 217
comparison with exotropia, 217
cortical suppression and, 107, 108
cover/uncover test for, 150–151
crossed diplopia associated with,
203
cyclic, 261
definition of, 86
Duane’s syndrome-related, 358,
359
surgical treatment of, 361
duration of, 217
fusional divergence correction of,
217
with high accommodative
convergence (AC/A ratio), 243,
246–247
surgical treatment of, 251–252,
400, 402
Hirschberg test for, 146
incomitant, Faden operation for,
400, 402
infantile accommodative, 228, 245,
254
differentiated from infantile/
congenital esotropia, 219,
220–221
infantile/congenital, 217–243
amblyopia associated with,
223
index
Esotropia (Continued)
botulinum toxin treatment of,
242–243
characterization of, 221–222
Chavasse theory of, 219
Cianci’s syndrome-related,
228–231, 232
clinical assessment of, 226–227
clinical features of, 221
definition of, 217, 226
differential diagnosis of, 219,
220–221
differentiated from infantile
accommodative esotropia,
219, 220–221
etiology of, 219–220
genetic factors in, 227–228
incidence of, 217–218
inferior oblique overactionrelated, 370
large-angle, 218, 221
latent nystagmus associated
with, 225–226
motor abnormalities associated
with, 225
onset of, 221
refractive errors associated
with, 223–225
spontaneous resolution of,
222–223
strabismic amblyopia
associated with, 113, 114
systemic associations of, 226
treatment of, 232–243, 372–373
types of, 228–232
Worth theory of, 219
large-angle, infantile esotropiarelated, 218, 221
Möbius syndrome-related, 364–365
neonatal, 105
with normal retinal
correspondence, 193
nystagmus associated with,
255–260
face turning associated with,
255–256, 257
partially accommodative, 247–251
miotics treatment of, 252–254
surgical treatment of, 251–252
postoperative, 242
in intermittent exotropia
patients, 276–277
prism-based neutralization of, 91,
92, 93
539
prism-induced, 94
refractive, 243
sensory, 261–262
differentiated from infantile/
congenital esotropia, 219
as uncrossed diplopia cause, 175
V-pattern, 450
chin depression associated
with, 376
Ethmoid bone, endoscopic sinus
surgery-related injury to, 365
Excitatory burst neurons (EBNs),
426–427, 429
Excycloduction (extorsion), 27
Excyclotropia (extorsion)
definition of, 88
foveal location in, 89
Exophoria
convergence-based control of,
95
definition of, 86
near, convergence insufficiencyrelated, 277
prism-induced, 96, 97
Exotropia, 86, 87, 266–283
accommodative convergence
(AC/A ratio) in, 99, 269, 271,
272, 275
alternating, 87
A-pattern
chin depression associated
with, 376
treatment of, 287, 288
classification of, 267
comparison with esotropia, 217
congenital, 279, 281
inferior oblique overactionrelated, 370
consecutive, 240
cover/uncover test for, 150–151
craniosynostosis-related, 369
crossed diplopia associated with,
177, 203
definition of, 86
Duane’s syndrome-related, 358,
359
surgical treatment of, 361–362
Hirschberg test for, 146
intermittent, 266–277
A- and V-patterns in, 275–276
accommodative convergence
(AC/A ratio) in, 269, 271,
272, 275
basic, 269
540
index
Exotropia (Continued)
bifoveal fusion in, 267
classification of, 268–272
clinical features of, 266–267
measurement of deviation in,
272–273
natural history of, 267
nonsurgical treatment of, 273
normal, 266
postoperative care for, 276–277
proximal convergence in, 269
pseudodivergence excess in,
269, 270, 274–275
suppression associated with,
188
surgical treatment of, 273–275
tonic divergence excess in,
269, 270–272, 274–275
tonic fusional convergence in,
269
tropia phase increase in,
273–274
X-pattern, 276
Y-pattern, 285
large-angle, X-pattern, 286
left, cranial nerve III palsy-related,
362, 363
neonatal, 105
with normal retinal
correspondence, 193
prism-induced, 92, 95
sensory, 280–281
Extorsion
as excycloduction, 27
as excyclotropia, 88, 89
retinal, 167, 168
Extrafovel fixation, amblyopia-related,
117
Extraocular muscles. See also Oblique
muscles; Rectus muscles
actions of, 27–28
agonists, 27, 63–64
anatomy of, 24, 25, 30–60
oblique muscles, 24, 25, 38–47
rectus muscles, 24, 25, 30–38
antagonists, 27, 63–64
aplasia of, 365, 368, 369
arcs of contact of, 27
congenital absence of, 480
disorders of, 479–480
fascial structures of
pulleys (muscle sleeves),
49–51, 52, 55–56, 58
Tenon’s capsule, 52–58
fibrosis of, 480
field of action of, 28–29
histology of, 48–51
insertion of, 27
length of, 27
muscle fiber types of, 48
global layer (GL), 49, 50, 51
orbital layer (OL), 49, 50, 51,
52, 58
muscle-pulleys (muscle sleeves) of,
49–51, 52, 55–56, 58
abnormal location of, 325, 327
nerve fiber to muscle filer
innervation ratio to, 48
neuromuscular spindles of, 48–49
in ocular positioning, 24–26
origin of, 27
palsy of, definition of, 323
paresis of
causes of, 323–324
definition of, 323
as incomitant strabismus
cause, 100, 101–102
in smooth pursuit versus saccadic
eye movements, 29–30
synergist, 64
tendon length of, 34
yoke muscles
definition of, 67
Hering’s law of, 65–66, 67
Eye alignment, neonatal, 105
Eye examination, pediatric, 1–23
family history in, 2
medical history in, 1–2, 6
physical examination in, 1, 2–20
contrast sensitivity assessment
in, 13–14
dilatation and cycloplegia in,
17–20
external examination in, 6
fundus examination in, 20
intraocular pressure
measurement in, 16–17
keratometry in, 17
physician-patient rapport in,
2–4
pupillary examination in,
15–16
red reflex test in, 14–15
sedation use in, 4–5
slit-lamp examination in, 16
in uncooperative children, 4–5
visual acuity assessments in,
6–14
index
Eye movements, 24–69. See also
Ductions; Saccades; Smooth pursuit;
Vergences
development of, 105–106
limitation of, 325
ocular position, 24–26
range of, evaluation of, 424
reflex, evaluation of, 431
saccadic. See Saccades
supranuclear, 423–440
disorders of, 432–440
physiology and clinical
evaluation of, 424–431
vestibular, 424–425
F
Face turning, 255–256, 257, 373–375
Brown’s syndrome-related, 315
congenital nystagmus-related,
376–378
cranial nerve VI palsy-related, 375
Duane’s syndrome-related, 358,
359, 375
treatment of, 359–360, 361
measurement of, 375
Facial anomalies
congenital superior oblique palsyrelated, 301–302
cranial nerve VI palsy-related,
449–450, 451
Möbius syndrome-related, 490
myotonic dystrophy-related, 486
Facial palsy, Möbius syndrome-related,
364
Faden procedure, 333, 399–402
effect on accommodative
convergence, 333
“Fallen eye,” 297–298
Far distance test, 273
Fat, orbital, 24, 25
entrapment of, 342, 343, 344. See
also Fat adherence
Fat adherence, 56–57, 411
definition of, 334
as ocular restriction cause, 325, 326
retinal surgery-related, 346–347
treatment of, 334–336
Fatigue, visual, intermittent exotropiarelated, 267
Fetal alcohol syndrome, 359
Fibrosis
local anesthetics-related, 325, 326,
343, 345, 346
trochlear, 319
541
Fibrotic bands, congenital. See
Congenital fibrosis syndrome
Fixation
alternating, 120
infantile/congenital esotropiarelated, 224
Worth 4-dot test in, 199–200
normal development of, 7
Fixation preference testing, 8
for amblyopia, 199–122
for infantile/congenital esotropia,
226
for strabismus amblyopia, 10
Fixation reflex, 12
Fixation testing, 4, 6–8. See also
Fixation preference testing
for amblyopia, 119–122
in eccentric fixation, 117, 119,
120
with monocular fixation
testing, 119
with Visuscope, 119
binocular, 6, 7–8
monocular, 6–7, 8
Forced-choice preferential looking (FPL)
test, 9–10
Forced-duction testing, 168, 169, 170,
329–331
in Brown’s syndrome, 315
Forced-generation testing, 331
Forced lid closure test, 431
Four base-out test, 212, 214–216
Fovea
angle kappa of, 145–149
maturation of, 7
Foveal ectopia, 348
Fresnel Press-On prisms, 528
Fundus, examination of, 20, 172
Fusion
diplopia test-related disruption of,
190
with Maddox rod test, 193, 204
with red filter test, 193
with Worth 4-dot test, 193,
196, 200–201
four base-out test for, 212, 214–216
latent strabismus-related
disruption of, 139
Fusional tests, 3
G
Gaucher’s disease, 432, 433
saccade initiation failure associated
with, 432, 433, 434
542
index
Gaze
cardinal positions of, 142
measurement of, 155
positions of, 28
Glasses. See Spectacles
Glaucoma explant surgery, as
strabismus cause, 349–351
Globe retraction
Duane’s syndrome-related, 361–362
Möbius syndrome-related, 364
Goldenhar’s syndrome, 359
Goldmann perimetry, 12
Goniometers, orthopedic, 374–375
Gradenigo’s syndrome, as cranial nerve
VI palsy cause, 352
Graves’ disease/ophthalmology
definition of, 336
inferior rectus muscle recession in,
333–334
management of, 336–338
as ocular restriction cause, 326
Guillain-Barré syndrome
bulbar variant of, 457
cranial nerve palsy associated with,
457–458
differentiated from botulism, 479
infections as risk factor for, 457–458
relationship with Miller Fisher
syndrome, 458–459
H
Haemophilus influenzae infections, 452
Hang-back recession, 393–394, 396
Haploscopic devices, 77–78
Haploscopic tests, 204–212
amblyoscope-based, 204, 205–209
Lancaster Red/Green test, 164–165,
166–267, 204–205
Harada-Ito procedure, 42, 304, 349,
412–413, 451
bilateral, 305
Headaches, migraine. See Migraine
headaches
Head posturing, abnormal, 373–379.
See also Face turning; Head tilt;
Torticollis
as binocular fusion indicator, 139
incomitant strabismus-related,
375–376
nystagmus-related, 379
surgical treatment of, 376–378
Head-thrusting behavior, in saccade
initiation failure (oculomotor
apraxia), 433–434
Head tilt
congenital superior oblique paresisrelated, 301, 302
cranial nerve IV palsy-related, 449,
450, 451
nystagmus-related, 378
traumatic superior oblique paresisrelated, 300
Head tilt test
for differentiation of primary from
secondary inferior oblique
overaction, 310–311
in inferior oblique paresis, 305
in superior oblique overaction, 305
Head trauma
as cranial nerve III palsy cause, 363
as cranial nerve IV palsy cause,
443–444, 451–452
as cranial nerve VI palsy cause, 352
as esotropia cause, 443–444
as inferior oblique palsy cause, 304
as superior oblique paresis cause,
297, 299–300
Heavy eye syndrome, 351
Hering’s law of equal innervation, 144,
474
esotropia neutralization and, 93
hypertropia and, 87
incomitant deviations and, 159
oblique overaction and, 290
primary deviation and, 101
prism-induced vergence and, 95
right amblyopia and, 123
superior oblique paresis and, 295
true hypertropia and, 370
vergence eye movements and, 82,
95
yolk muscles and, 65–66, 298–299
Herpes zoster ophthalmicus, 302
Heterophoria, definition of, 84
Heterophoria method, of
accommodative convergence (AC/A
ratio) measurement, 161–162
Heterotropia, definition of, 84
Hirschberg reflex, 126
Hirschberg test, 144–145, 146, 147, 152
corneal light reflex in, 524
photographic techniques in, 524
Homatropine, as cycloplegic agent, 18,
19
Horizontal rectus muscles. See also
Lateral rectus muscle; Medial rectus
muscle
action of, 27
index
Horizontal rectus muscles (Continued)
anatomy of, 32–35
Duane’s syndrome-related
cocontraction of, 24
transposition of, 403, 407
as A- or V-pattern strabismus
treatment, 287–288, 289
as superior oblique muscle
overaction treatment, 308
Horror fusionis, 188–190
HOTV letters, 11, 14, 118
Hummelsheim procedure, 404, 405,
406, 419
for cranial nerve VI palsy, 353, 354,
355
for medial rectus hypoplasia, 365,
369
for medial rectus muscle injury,
365
modifications of, 354, 406
for monocular elevation deficit
syndrome, 342
Hydrocephalus
dorsal midbrain syndrome
associated with, 436, 438
internuclear ophthalmoplegia
associated with, 441
setting sun sign associated with,
437
Hypermetropia
amblyopia-related, 115–116
bilateral, spectacles use in, 127, 128
infantile/congenital esotropiarelated, 223–224, 225
with overconvergence, as infantile
esotropia cause, 219
Hyperopia
high, lens-based correction of,
522–523
infantile/congenital esotropiarelated, 224–225
in neonates, 522
Hypertropia, 87
bilateral superior oblique paresisrelated, 296, 297
cover/uncover test for, 150–151
dissociated vertical deviationrelated, 370
Hirschberg test for, 146
left, 87–88
diplopic image in, 177
oblique muscle palsy-related,
292–294
prism-induced, 92
543
rectus muscle palsy-related,
292–294
right, 87–88
superior oblique paresis-related,
302–303
true, 370
vertical vergence-based control of,
95
Hypoaccommodation, cranial nerve III
palsy-related, 362
Hypotonia, in saccade initiation failure,
434
Hypotropia, 87
cranial nerve III palsy-related, 362,
363
I
I-ARM acronym, for pediatric screening
examination, 125, 126
Illiterate E game, 11, 14, 118, 141
Image jump, 79, 90, 91
Immunizations
as cranial nerve III palsy cause, 452
as cranial nerve VI palsy cause, 352
Immunosuppressive therapy, for
myasthenia gravis, 476–477
Incycloduction, 27
Incyclotropia, 88
foveal location in, 89
Induced convergence retraction,
435–438
Induced tropia test, 122–125
Infarction, as cranial nerve III palsy
cause, 452
Infections, as Guillain-Barré syndrome
cause, 457–458
Inferior oblique muscle
actions of, 27, 42, 45
anatomic insertion of, 27
anatomic relationship with
inferior rectus muscle, 36–37,
38–39
lateral rectus muscle, 34–35
vertical rectus muscle, 40, 41
anatomy of, 40, 41, 42, 45–47
arc of contact of, 27
field of action of, 28
length of, 27
origin of, 27
palsies of
adduction deficits associated
with, 306, 316
eye movement limitations in,
29
544
index
Inferior oblique muscle (Continued)
pareses of
isolated, 304–305
unilateral, 305–306
pseudo-overaction, 310
tendon length of, 34
weakness of, 439
yoke muscle function of, 66
Inferior oblique muscle overaction,
308–312
with A- or V-pattern strabismus,
288
bilateral asymmetrical, 311
craniosynostosis-related, 369
differentiated from dissociated
vertical deviation, 370
dissociated vertical deviationrelated, 373
infantile/congenital esotropiarelated, 225, 370
intermittent exotropia-related, 275
mimickers of, 310–311
primary, 308–310
differentiated from secondary
inferior oblique overaction,
309–310
V-pattern, 309, 311
Y-pattern, 309–310, 311
superior oblique paresis versus, 299
treatment of. See Inferior oblique
muscle weakening procedures
unilateral asymmetrical, 311
Inferior oblique muscle recession, 311,
391, 407, 408
Inferior oblique muscle weakening
procedures, 311–312, 407–411
anteriorization (anterior
transposition), 45–47, 311–312,
407–410
as dissociated vertical
deviation treatment, 373
graded anteriorization
technique of, 47
J-deformity associated with,
46–47, 312, 409, 410
as ocular restriction cause,
46–47, 327
extirpation-denervation, 407
graded recession-anteriorization,
410–411
myotomy, 407
recession, 311, 391, 407, 408
Inferior rectus muscle
actions of, 27, 36
anatomic insertion of, 27
anatomic relationship with inferior
oblique muscle, 36–37, 38–39
anatomy of, 30, 36–38
fascial connections, 36–37,
38–39
aplasia of, 365, 368
arc of contact of, 27
hypoplasia of, 365, 368
length of, 27
lost, 37
origin of, 27
paresis of, left, 290
tight, double elevator palsy-related,
340, 341
transposition of, 406–407
Inferior rectus muscle recession
lid changes associated with, 37
in thyroid strabismus, 337
Inferior rectus muscle resection, lid
changes associated with, 37
Inflammation, as cranial nerve VI palsy
cause, 443, 446
Infraduction, 27
Infrared eye trackers, 328
Infraversion, 67
Ing, Malcolm, 235
Inhibitional palsy of the contralateral
antagonist, 298–299
Inhibitory burst neurons (IBNs),
426–427, 429
Intermuscular septum, 53, 54
Internuclear ophthalmoplegia, 440–441
Interpupillary distance
effect on stereoacuity, 78
relationship with convergence, 161
Interstitial nucleus of Cajal, lesions of,
372
Intorsion, retinal, 167
Intrafacial synkinesis, 469
Intraocular pressure (IOP)
elevated, 16
ocular restriction-related, 331
measurement of, 16–17
propofol-related decrease in, 4, 5,
17
Iris, vascular supply to, 58–59
Ischemia, of the anterior segment,
59–60, 354, 406
J
J-deformity, 46–47, 312, 409, 410
Jensen procedure, 404, 405
Joubert syndrome, 339
index
K
Kearns-Sayre syndrome, 481–485
chronic progressive external
ophthalmoplegia associated with,
482–484
cranial nerve palsy associated with,
456
Keratometry, 17
Kestenbaum-Anderson-Parks procedure,
376–378
Klippel-Feil syndrome, 359
Koerber-Salus-Elschnig syndrome, 435
Krimsky light reflex test, 149, 150, 227,
524, 527
L
Lancaster Red/Green test, 164–165,
166–167, 204–205
Lateral geniculate nucleus (LGN), in
amblyopia, 110, 111, 113–114, 190
Lateral rectus muscle
actions of, 27, 32
anatomic insertion of, 27
vertical displacement of, 32
anatomic relationship with inferior
oblique muscle, 34–35
anatomy of, 30, 34–35
in anterior segment blood
circulation, 59
arc of contact of, 27, 34
congenital aberrant innervation of,
285
in cranial nerve VI palsy, 354
Duane’s syndrome-related
cocontraction of, 355–356, 357
infraplacement of, 275–276
with intermuscular septum and
check ligaments, 54
“leash effect” of, 286
length of, 27
lost, 34–35
myopic strabismus fixus-related
slippage of, 351
origin of, 27
recession of
as A-pattern strabismus
treatment, 287, 288
bilateral, as intermittent
exotropia treatment, 274–275
ipsilateral, as dissociated
horizontal deviation
treatment, 373
tendon length of, 34
yoke muscle function of, 65, 66
545
LEA figures, 11, 118
Lens gradient method, of
accommodative convergence (AC/A
ratio) measurement, 161–162,
163–164
Lens implants, ultraviolet protection
for, 524
Levator palpebrae, anatomic
relationship with superior rectus
muscle, 36
Levodopa/carbidopa, as amblyopia
treatment, 132
Levoversion, 67
Lid fissure
narrowing of, 24
Duane’s syndrome-related,
356–357
inferior rectus muscle
recession-related, 37
ocular restriction-related, 331
widening of, 24
inferior rectus muscle
recession-related, 37
rectus muscle paresis-related,
331–332
Lidocaine, myotoxic effects of, 343
Lid retraction, in dorsal midbrain
syndrome, 436
Lid speculum, 4
wire, 3
Light occlusion, bilateral, as amblyopia
treatment, 131–132
Light reflex tests, 144–150
angle kappa, 145–149
Brückner test, 15, 126, 127,
149–150, 249, 358
Hirschberg test, 144–145, 146, 147,
152
Krimsky test, 149, 150, 227, 524,
527
Line of sight, angle kappa of, 145–146
Listing’s law, 61–62
Listing’s plane, 61
Local anesthetics, myotoxic effects of,
343, 345–346
Lockwood’s ligament, 37, 38, 39, 45
Long-lead burst neurons (LLBNs), role
in saccadic eye movements, 429
M
Macular degeneration, color vision
assessment in, 12
Maculopathy, ultraviolet protection in,
524
546
index
Maddox rod test, 88, 165, 167, 190, 204
in congenital superior oblique
palsy, 301, 302
double, 165, 167
single, 165
in superior oblique overaction, 307
Marcaine, myotoxic effects of, 343
Marcus Gunn jaw-winking
phenomenon, 341, 468–469
Duane’s syndrome-related, 359
Marin-Amat syndrome, 470
M cells, 373
Measles, as Guillain-Barré syndrome
cause, 457–458
Medial longitudinal fasciculus lesions,
440–441
Medial rectus muscle
actions of, 27, 32, 33
anatomic insertion of, 27
vertical displacement of, 32
anatomy of, 30, 34
arc of contact of, 27
in Cianci’s syndrome, 229, 231
Duane’s syndrome-related
cocontraction of, 355–356
endoscopic sinus surgery-related
injury to, 365, 366–367
in Faden procedure, 400
length of, 27
lost, 56
origin of, 27
tendon length of, 34
tight, Möbius syndrome-related,
364–365
yoke muscle function of, 65, 66
Medial rectus muscle recession,
390–391
bilateral, 304
asymmetrical, 333
as congenital esotropia
treatment, 232–242
as partially accommodative
esotropia treatment, 247–252
right, 332–333
as Möbius syndrome treatment,
365
Medial rectus muscle shortening, right,
396–397
Medulloblastomas, as cranial nerve VI
palsy cause, 443
Megacolon, Hirschsprung, 469
Meningitis
cranial nerve VI palsy associated
with, 352, 443
internuclear ophthalmoplegia
associated with, 441
Mesencephalic-diencephalic junction
lesions, 435
Mesencephalic reticular formation, 430
Micrognathia, Möbius syndromerelated, 364
Microtropias, binocular fixation
preference testing in, 8
Migraine headaches
as esotropia cause, 443–444
ophthalmoplegic, 455–456
Miller Fisher syndrome, 441, 457,
458–459
relapsing, 459
Miotics
as accommodative esotropia
treatment, 252–254
side effects of, 253–254
Misoprostol, as Möbius syndrome risk
factor, 364
Möbius syndrome, 364–365
differentiated from infantile/
congenital esotropia, 219, 220
Monocular depth perception, 80–81
Monocular elevation deficiency, 439
Monocular fixation syndrome. See
Monofixation syndrome (peripheral
fusion)
Monocular vision, development of,
103
Monofixation syndrome (peripheral
fusion), 89, 172–182
amblyoscope testing in, 206
anisometropic amblyopia-related,
114
Bagolini striated lenses test in, 203
cover test in, 152, 154
as ocular restriction cause, 326
primary, 182
Worth 4-dot test in, 200–201
Motility disorders, ocular, 423–519
disorders at the neuromuscular
junction, 470–479
disorders of nerve and muscle, 481
Kearns-Sayre syndrome,
481–485
Möbius syndrome, 489–491
myotonic dystrophy, 485–489
disorders of the central and
peripheral nervous systems,
423–470
anomalies of innervation,
460–467
index
Motility disorders, ocular (Continued)
internuclear ophthalmoplegia,
440–441
ocular motor cranial nerve
palsies, 442–470
supranuclear disorders, 432–440
disorders of the extraocular
muscles, 479–480
Möbius syndrome-related, 364
Motion parallax, 80–81
Motor abnormalities, esotropia
associated with, 225
Motor examination, ocular, 138–173
family history in, 139
goals of, 138
medical history in, 138–139
physical examination in, 139–172
accommodative convergence
measurement in, 161–164
amblyopia assessment/visual
acuity assessment in,
140–141
binocular sensory testing in,
139
clinical distance-near
relationship in, 164
cycloplegic refraction in, 172
ductions and versions in, 140,
141–143
fundus examination in, 172
inspection of patients in, 140
Lancaster Red/Green test in,
164–165, 166–167
ocular deviation
measurements in, 140,
143–160
restriction and paresis tests in,
168–172
sensory tests in, 141
torsion assessment in, 164–168
Motor fusion, 70, 81–83
in binocular vision, 70, 81–83
definition of, 81–82
fusional vergence movements in,
82
phoria-related decrease in, 84, 85
torsional, 88–89
MTI PhotoScreener, 10, 15
Multiple sclerosis
contrast sensitivity in, 14
internuclear ophthalmoplegia
associated with, 441
superior oblique paresis associated
with, 302
547
Mumps, as Guillain-Barré syndrome
cause, 457–458
Muscle pull, mechanical disadvantage
of, 324
Muscle-pulleys (muscle sleeves), of
extraocular muscles, 49–51, 52,
55–56, 58
abnormal location of, 325, 327
Muscle recession procedures, 388–396
adjustable suture technique in,
394–396
hang-back technique in, 393–394,
396
as incomitant strabismus
treatment, 332
inferior oblique, 311, 391, 407, 408
inferior rectus, 37, 337
lateral rectus, 274–275, 287, 288,
373
recession-resection (“R and R”)
procedure, 399
rectus, 388–391
Starling’s length-tension curve in,
388, 389, 390
superior rectus, 36, 373
Muscle shortening procedures, 396–399
plications, 396, 398–399
resections, 332, 396, 397
tucks, 396, 397–398
Muscle transposition procedures,
402–407
anteriorization (anterior
transposition), inferior oblique,
45–47, 311–312, 407–410
as dissociated vertical
deviation treatment, 373
graded anteriorization
technique of, 47
J-deformity associated with,
46–47, 312, 409, 410
as ocular restriction cause,
46–47, 327
complications of, 406
of horizontal rectus muscle, 403,
407
as A- or V-pattern strabismus
treatment, 287–288, 289,
403
as superior oblique muscle
overaction treatment, 308
for rectus muscle palsy, 404–406
complications of, 406
Hummelsheim procedure, 405,
406
548
index
Muscle transposition procedures
(Continued)
Jensen procedure, 404, 405
Knapp procedure, 404, 405
for small vertical deviations, 403
split-tendon
Hummelsheim procedure, 353,
354, 355, 365, 369, 404, 405,
406, 419
Jensen procedure, 404, 405
for torsion, 406–407
of vertical rectus muscles, 345,
406, 407
Muscular dystrophy, facio-scapulohumeral, 490
Myasthenia gravis
autoimmune (acquired), 472–477
congenital, differentiated from
infantile/congenital esotropia,
219, 220
as cranial nerve VI palsy cause,
352
differentiated from internuclear
ophthalmoplegia, 441
Mydriasis
atropine-related, 521
comparison with cycloplegia, 172
cyclopentolate-related, 521
Mydriatic drops, as discomfort cause, 4
Myectomy, of inferior oblique muscle,
311
Myopathies
congenital centronuclear
(myotubular), 490
dysthyroid, 480
proximal myotonic, 485, 486–487,
488
Myopia
alternating, infantile/congenital
esotropia-related, 225
binocular visual acuity in, 522
high, 351
acquired strabismus fixusrelated, 351–352
lens-based correction of, 522
in neonates, 522
Myotonic dystrophy, 485–489
N
Near fixation targets, 3
Near point convergence exercises,
278–279
Near point of convergence (NPC), in
convergence insufficiency, 278
Near reflex, 99
spasm of, 439–440
Near targets, accommodative, 3
Near triad, 430
Neisseria meningitidis infections, 452
Neosynephrine, 172
Nephronophthisis, 435
Neural integrator, 429
definition of, 430
evaluation of, 431
Neuroblastomas, 469
Neurological diseases
as comitant strabismus cause, 100
differentiated from infantile/
congenital esotropia, 219
Neurological evaluation, of acquired
strabismus patients, 139
Neuromuscular blocking agents, as
myasthenia gravis cause, 472
Neuromuscular junction disorders,
470–479
autoimmune (acquired) myasthenia
gravis, 472–477
botulism, 478–479
congenital myasthenic syndrome,
471–472
familial infantile myasthenia
gravis, 470–471
transient neonatal myasthenia,
470
Neuromyopathies, 456–457
Neurons
binocular cortical, 104–105
monocular cortical, 104
Neuropathies
generalized, 457
progressive optic, 12
Niemann-Pick disease, 434
Nucleus reticularis tegmenti pontis
(NRTP), 430
Nystagmus
Cianci’s syndrome-related,
228–229, 231
congenital, esotropia associated
with, 257 258, 259
gaze-evoked, 431, 474
head posturing associated with,
374, 375, 378–379, 379
treatment of, 376–378
head tilt associated with, 378
latent
with cyclovertical movement,
370, 372
esotropia-related, 255–256, 257
index
Nystagmus (Continued)
infantile/congenital esotropiarelated, 225–226
manifest, 257, 258, 378–379
visual acuity testing in, 123,
125
optokinetic (OKN), 8–9, 65. See
also Optokinetic nystagmus
(OKN) drum; Optokinetic
nystagmus (OKN) testing
evaluation of, 429
normal development of, 7
in saccade initiation failure,
432–433
rebound, 431
seesaw, 372
sensory, 115
surgical treatment of, 378
vestibular, evaluation of, 429
Nystagmus compensation (blockage)
syndrome, 259–260
cyclovertical, 372
O
Oblique muscle(s). See also Inferior
oblique muscle; Superior oblique
muscle
actions of, 27–28, 39–40
anatomic relationship with rectus
muscles, 24
anatomy of, 24, 25, 39–47
dysfunction of, 289–319
clinical evaluation of, 289–290
primary overaction of,
differentiated from paresis
Bielschowsky head tilt test for,
290–291, 294
three-step test for, 291, 292–294
retinal surgery-related
displacement of, 347–348
Oblique muscle recessions, 391
Occlusion test
for exotropia measurement, 272
in combination with far
distance test, 273
for intermittent exotropia
measurement, 274–275
for pseudodivergence excess
measurement, 270–271
Occlusion therapy, 3
for amblyopia, 130, 131–132
effect on contrast sensitivity,
14
part-time, for exotropia, 273
549
Ocular deviations, measurement of,
140, 143–160
accommodation targets in, 144
accommodative convergence
(AC/A ratio), 161–164
cover tests for, 4, 150–159, 528–529
alternate cover test, 152–153,
154, 157
for cardinal positions of gaze
measurement, 155
cover/uncover test, 149,
150–152, 154
interpretation of, 152, 154
prism alternate cover test, 154
simultaneous prism cover test,
155–156
variable measurements in,
154–155
incomitant deviations
measurement, 159, 160
light reflex tests, 144–150
angle kappa, 145–149
Brückner reflex test, 149–150
Hirschberg test, 144–145, 146,
147, 152
Krimsky test, 149, 150, 227,
524, 527
methods of, 144
prism-based methods, 143–144
with Snellen letters, 144
Ocular muscle contraction
moment arm in, 388, 389
rotational force in, 388, 389
Ocular tilt reaction, 450
Oculocephalic maneuver. See Doll’s
head (oculocephalic) maneuver
Oculomotor nerve. See Cranial nerve
III
Oculomotor reflexes, 65
Oculomotor synkinesis, 453–454, 467
cranial nerve III palsy-related,
362–363
Omnipause neurons, role in saccadic
eye movements, 429
One and one-half syndrome, 474
Ophthalmoplegia
chronic progressive external,
482–484
generalized neuropathies-related,
457
internuclear, 440–441
Optical pearls and pitfalls, 520–529
Optic nerve, hypoplasia of, 370
Optic nerve, myelination of, 7
550
index
Optokinetic nystagmus (OKN) drum, 7,
9, 30, 65, 169, 328–329
Optokinetic nystagmus (OKN) testing
in congenital fibrosis syndrome,
232
for saccadic eye movement
diagnosis, 30, 226–227, 328–329
for smooth pursuit asymmetry
diagnosis, 106
Optotype testing, 11–12, 141
Oral clefts, Möbius syndrome-related,
364
Orbit
craniosynostosis-related extorsion
of, 369
fractures of, as ocular restriction
cause, 326
Orbital decompression, as Graves’
ophthalmology treatment, 336–337
Orbital floor fractures, as restrictive
strabismus cause, 342–345
Orbital mass, as ocular restriction
cause, 325, 326
Orthophoria, 84–85
Orthostatic reflex, 65
Orthotropia, 84
Otoliths, 425
P
Palpebral fissure, Duane’s syndromerelated narrowing of, 359–360
Palsy. See also Strabismus, paralytic;
specific palsies
definition of, 323
Panum’s fusional area
binasal retinal stimulation within,
76, 77–78
bitemporal retinal stimulation
within, 76–77
in physiological diplopia, 75, 76
Papoose boards, 3, 4
Paramedian pontine reticular
formation, 427, 428, 429, 437
Paresis. See also Strabismus, paralytic;
specific pareses
definition of, 323
diagnostic tests for, 168, 169, 170,
171–172
Parkinson’s disease, as accommodative
insufficiency cause, 280
Parks, Marshall, 334, 416
Parks-Bielschowsky three-step test, 449
Patching. See Occlusion therapy
Patch test. See Occlusion test
Penalization, as amblyopia treatment,
130–131
atropine, 130–131, 523
ultraviolet protection during,
524
optical, 130
Pencil pushups, 279
D-Penicillamine, as myasthenia gravis
cause, 472–473
Perkins tonometer, 16–17
Pertussis, as Guillain-Barré syndrome
cause, 457–458
Peters’ anomaly, bilateral, 115
Pfeiffer syndrome, 369
Phenergan, 4, 5
Phenothiazines, as myasthenia gravis
cause, 472
Phenylephrine, as cycloplegic agent, 18,
19
Phorias
cover/uncover test for, 151
definition of, 84
differentiated from tropias, 204
intermittent, 85
spontaneous manifestation of, 85
Phoria-tropia syndrome, 179
Phospholine iodide, 252–253
side effects of, 253–254
Photophobia, intermittent exotropiarelated, 267
Photoscreening, 10, 15
Physical restraint, of uncooperative
patients, 3, 4
Physostigmine, 18
side effects of, 521
Pinealomas, as dorsal midbrain
syndrome cause, 436
Placido’s disc, 17
Plagiocephaly, congenital superior
oblique palsy-related, 301–302
Plasticity, prolonged visual, 190
Pleoptics, as amblyopia-related
eccentric fixation treatment, 132
Plications, 396, 398–399
Pneumotonometers, 17
Podnar, Gregg, 118
Podnar, Paul, 118
Portal Stimuli System (Haag-Streit), 118
Position, ocular, 24–25
Position of rest, 26
Prader-Willi syndrome, 339
Premature infants
retinopathy in, 147, 148
tonic downgaze in, 439
index
Presbyopia, 280
Pretectal sign, 435
Prism adaptation, 252, 255
Prism alternate cover test, 154
Prism convergence exercises, 278
Prism diopters (PD), 90–91, 524
conversion to degrees, 525
use in fusional vergence amplitude
measurement, 95–96, 98
Prisms, ophthalmic
for ocular deviations measurement,
143–144
for strabismus measurement and
correction, 524–529
additivity error with, 526–527
base-down, 95
base-in, 92, 94, 95–96
base-out, 91–92, 95, 96, 97, 98
base-up, 92, 95
in exotropia, 272
for face turning measurement,
375
in four base-out test, 212,
214–216
Fresnel Press-On, 528
image jump effect of, 79, 90,
91
in incomitant strabismus,
528–529
in Krimsky test, 149, 150
loose, 3
at near fixation, 527
nomograms for, 527, 528
oblique, 527–528
positioning of, 525–526
in simultaneous prism cover
test, 155–157
“stacking” of, 526–527
strabismus-inducing, 92,
94–95, 96
strabismus-neutralizing, 91–92,
93, 528–529
through glasses, 527
Propofol, 4, 5
Proprioceptive eye position control, 99
Proptosis, 24
Graves’ disease-related, 336–337
Prostigmin, 475
Proximal myotonic myopathy, 485,
486–487, 488
Pseudo-Brown’s syndrome, 327, 349
Pseudo-esotropia, 220, 228
differentiated from infantile/
congenital esotropia, 219, 220
551
Pseudo-fovea
in anomalous retinal
correspondence, 182, 183, 184,
185, 186, 202–203, 207–209
in vertical prism red filter test,
196, 197, 198
Pseudointernuclear ophthalmoplegia,
458
Pseudo-strabismus, 229
Pseudotorsion, 62
Ptosis
chin elevation associated with,
374, 378–379
cranial nerve III palsy-related,
362–363, 364
treatment of, 363, 364
myasthenia gravis-related, 473,
474, 475
myotonic dystrophy-related,
488–489
Pulled-in-two syndrome (PITS), 347
Pulleys. See Muscle-pulleys
Pupillary dilation, 17–18, 19
cranial nerve III palsy-related, 362
Pupillary light reactor, normal
development of, 7
Pupils
Adie’s, as accommodative
insufficiency cause, 280
distance between
relationship with convergence,
161
examination of, 4, 15–16
pupillary distance between
effect on stereoacuity, 78
size of, age-related variations in, 15
Purkinje image, first, 144–145
Purkinje-Sanson image, first, 524
Q
Quinine, as myasthenia gravis cause,
472
“Quiver movements,” 474
R
Ragged-red fibers, 482, 487
Random dot stereoacuity test, 79–80
Reading aids
for accommodative insufficiency
patients, 280
for anisometropic myopic
amblyopia patients, 523
Recession procedures. See Muscle
recession procedures
552
index
Recession-resection (“R and R”)
procedure, 399
Rectus muscle(s). See also Lateral
rectus muscle; Medial rectus muscle
anatomic relationship with oblique
muscles, 24
anatomy of, 24, 25, 30–38
forced-duction testing of, 329–331
innervation of, 31
insertion of, 30–31
length of, 31
lost, 55–56, 418–419
in ocular positioning, 24, 25
palsies of
differentiated from ocular
restriction, 325
forced-duction testing in,
329–331
forced-generation testing in,
331
preoperative diagnosis of,
330–331
pseudoinferior, 342, 343
transposition surgery for,
404–406
paresis of, as saccadic eye
movement loss cause, 327
in saccadic eye movements, 30,
327
slipped, 55–56, 418–419
as ineffective muscle pull
cause, 324
retinal surgery-related, 347
surgical procedures on, 388–391
Faden procedure, 399–402
plication, 398–399
recession, 24, 388–392
tightening procedures, as lid
fissure narrowing cause, 24
Red filter test, 190, 191, 192, 193–196
Red reflex test, 4, 14–15, 125, 126–129
Refraction, 19, 20
cycloplegic, 172, 521
effect of eye pigment on, 172
in hypermetropic
accommodative esotropia,
244
for infantile/congenital
esotropia evaluation, 227
Refractive errors
esotropia associated with, 223–225
as head posturing cause, 379
high, lens-based correction of, 523
as strabismus cause, 85
strabismus-related, lens-based
correction of, 523
Resection procedures. See Muscle
resection procedures
Restriction, ocular
causes of, 325–327
definition of, 325
differentiated from paresis, 327–332
test for identification of, 168–171
Retinal correspondence
anomalous (ARC), 117, 182–188
afterimage test of, 209,
210–211, 212
amblyoscope testing in,
207–209
angle of anomaly in, 186, 207
Bagolini striated lenses test in,
202–203
definition of, 182
differentiated from eccentric
fixation, 184, 186
differentiated from normal
retinal correspondence, 193,
196, 197, 198
harmonious, 186, 207–208
paradoxical diplopia associated
with, 183, 184, 187
pseudo-fovea in, 182, 183, 184,
185, 186, 202–203, 207–209
red filter test in, 192, 193
unharmonious, 186, 187,
208–209
normal (NRC)
afterimage test of, 209, 210–211
amblyoscope testing in, 205,
206
Bagolini striated lenses test in,
202, 203
definition of, 182
differentiated from anomalous
retinal correspondence, 193,
196, 197, 198
red filter test in, 191, 193
Retinal image, blurred bilateral,
115–116
Retinal rivalry, 81, 82
Retinal surgery, as strabismus cause,
346–349
Retinopathy of prematurity, positive
kappa angle in, 147, 148
Retinoscopy
dry, 520
dynamic, 520–521
Retinoscopy lens, loose, 3
index
Retrobulbar anesthetic blocks, 42
Rheumatoid arthritis, as Brown’s
syndrome cause, 315, 316
Richmond pseudoisochromatic plates,
13
Rivalry, retinal, 81, 82
Rotation, ocular
limitation of, 325
physiology of, 61–67
cycloduction, 62
Donder’s law of, 61–62
Listing’s law of, 61–62
pseudotorsion, 62
Sherrington’s law of reciprocal
innervation, 63–64
synergist muscles, 64
Rubinstein-Taybi syndrome, 469
S
Saccade initiation failure, 432–435
acquired, 432, 433
congenital, 432, 433
Saccades, 29–30
abnormalities of, 429
amplitude of, 29
command-generated, 425
definition of, 29
evaluation of, 328–329, 425
preoperative, 328
involuntary, 425
memory-guided, 425
in neonates, 7, 105
normal development of, 7
optokinetic nystagmus-based
evaluation of, 30, 226–227
physiology of, 426–429
reflex, 425
elicitation of, 429
smooth pursuit eye movements
versus, 29–30
spontaneous, 425
upward, brainstem pathways in,
437
voluntary, 425
Saccadic omission, 30
Saccadic velocity measurement, 169,
171
for differentiated of restriction
from paresis, 327–329
of lateral rectus muscle function,
354
Schiotz tonometer, 16
Scleral buckling procedure, as
strabismus cause, 346, 347
553
Scotomas
large, Worth 4-dot test in, 200
suppression, 107
Bagolini striated lenses test in,
203
facultative, 180
large-scale strabismus-related,
188, 189
monofixation syndromerelated, 179–182
red filter test in, 194
vectograph examination of,
214
Worth 4-dot test in, 202
Sedation
contraindication in adjustment
suture technique, 396
during intraocular pressure
measurement, 17
during keratometry, 17
during slit-lamp examination, 16
of uncooperative patients, 4
Sedatives, exotropia-inducing effect of,
266
Semicircular canals, 424–425
Sensory adaptations, to strabismus, 85,
174–216
definition of, 174
sensory tests for, 141, 190–216
afterimage test, 209–212
diplopia tests, 190–204
four base-out test, 212,
214–216
haploscopic tests, 204–212
vectographic tests, 212,
213–214
visually immature, 174, 178–190,
178–216
anomalous retinal
correspondence, 182–188
horror fusionis, 188–190
large retinal suppression, 188,
189
monofixation syndrome
(peripheral fusion), 172–182
prolonged visual plasticity, 190
visually mature, 174–178
confusion, 177–178
diplopia, 174–177
Sensory fusion, in binocular vision,
70–83
binocular cortical cells in, 70, 71
corresponding retinal points in,
70–71
554
index
Sensory fusion, in binocular vision
(Continued)
definition of, 70
disparate images in, 72
empirical horopter in, 71, 72, 73,
74–75
noncorresponding retinal points in,
72, 73
Panum’s fusional area in, 72, 73, 74
stereoacuity testing in, 76–80
stereoscopic vision in, 72, 74–75
Vieth-Müller circle in, 71, 72
Sensory tests, 141, 190–216
afterimage test, 209–212
diplopia tests, 190–204
four base-out test, 212, 214–216
haploscopic tests, 204–212
vectographic tests, 212, 213–214
Setting sun sign, 437
Sherrington’s law of reciprocal
innervation, 63–64, 171, 331–332,
352, 391
Silicone frontalis sling procedure, 364
Simultaneous prism cover test,
155–157
Sinus disease, cavernous, as cranial
nerve VI palsy cause, 352
Sinusitis, as Brown’s syndrome cause,
315, 316
Sinus surgery, as medial rectus muscle
injury cause, 365, 366–367
Skiascopy rack, 20
Slip lamps, portable, 3
Slipped muscles, in strabismus surgery,
53, 55–56
Slit lamp examination, 16
Smooth pursuit, 425, 429–430
accurate, as visual development
milestone, 106
in neonates, 7, 105–106
neural pathways for, 429–430
purpose of, 429
saccadic eye movements versus,
29–30
Smooth pursuit asymmetry, 105–106
infantile/congenital esotropiarelated, 106, 225
Snellen acuity, comparison with
contrast acuity, 13
Snellen letters, 11–12, 109
Spectacles
hypermetropic, for infantile/
congenital esotropia correction,
232
for hypermetropic accommodative
esotropia correction, 244–246
indications for prescription of, 127,
128
polarized, as haploscopic devices,
77–78
prescription guidelines for, 522–524
strabismic deviation measurement
through, 527
Spin test, 431, 442
Spiral of Tillaux, 30
Split-tendon lengthening procedure,
superior oblique, 289, 414
Split-tendon transposition procedures
Hummelsheim procedure, 353, 354,
355, 365, 369, 404, 405, 406, 419
Jensen procedure, 404, 405
Squinting
to bright light. See Photophobia
strabismus-related, 84
Starling’s length-tension curve, 388,
389, 390
Stereoacuity
from binocular retinal fields, 75
from central field, 75
high-grade, 81
quantification of, 78
Stereoacuity testing, 76–80
contour, 77, 78–79
random dot, 79–80
Stereopsis
intermittent exotropia surgeryrelated loss of, 274
normal development of, 7
Stereoscopic resolution, 78
Stereoscopic vision, 72, 74–75
Steroids, as myasthenia gravis
treatment, 476–477
Stimulation, active, of amblyopic eyes,
132–133
Strabismus
acquired
as confusion cause, 177–178
prognosis for, 138–139
as amblyopia cause, 109, 110
fixation preference testing for,
119–122
pathophysiologic mechanisms
of, 110, 113
vertical prism testing for,
122–125
angle of, measurement of. See
Ocular deviations, measurement
of
index
Strabismus (Continued)
A-pattern
definition of, 284
ET-pattern, 284
lamba-pattern, 286
treatment of, 287–289
XT-pattern, 284
basic concepts of, 84–102
comitant, 100
botulinum toxin treatment of,
421
surgical treatment of, 391
complex, definition of, 323
congenital
incomitant, large regional
suppression in, 188
prognosis for, 138–139
as cortical suppression cause, 107
cranial nerve III palsy-related, 362,
363
definition of, 84
dissociated, 370–379
distance measurements in, 3
divergent, most common form of,
266
duration of, 138–139
effect on visual development, 103,
107
horizontal, inferior oblique
overaction associated with, 311
idiopathic, 85
incomitant, 100
congenital, large regional
suppression in, 188
definition of, 323
extraocular muscle paresisrelated, 100, 101–102
left lateral rectus paresisrelated, 100, 101
management of, 332–334
right medial rectus recessionrelated, 391
intermittent, as binocular fusion
indicator, 139
large-angle
adjustment suture technique
in, 396
depth perception in, 81
suppression scotomas
associated with, 188, 189
Marcus Gunn jaw-winking-related,
468–469
myasthenia gravis-related, 477
occlusion therapy for, 130
555
paralytic, 85, 352–369
adjustment suture technique
in, 396
aplasia of extraocular musclesrelated, 365–369
cranial nerve III palsy-related,
362–364
cranial nerve IV palsy-related,
362
cranial nerve VI palsy-related,
352–355
craniosynotosis-related, 369
differentiated from restrictive
strabismus, 323–324,
327–332
Duane’s syndrome-related,
355–362
inferior oblique palsy-related,
364
Möbius syndrome-related,
364–365
sinus surgery-related, 365
primary deviation, 442
refractive error-related, 85
restrictive, 85
causes of, 326
congenital fibrosis of the
extraocular muscles -related,
339–340
differentiated from paralytic
strabismus, 323–324,
327–332
double elevator palsy-related,
340–342
fat adherence syndromerelated, 334–336
glaucoma explant surgeryrelated, 349–351
Graves’ ophthalmology-related,
336–338
local anesthetics-related, 343,
345–346
monocular elevation deficit
syndrome-related, 340–342
myopic strabismus fixusrelated, 351–252
orbital floor fracture-related,
342–345
retinal surgery-related, 346–349
in saccade initiation failure, 434,
455
secondary deviation, 442
sensory aspects of. See Sensory
adaptations, to strabismus
556
index
Strabismus (Continued)
small-angle, monofixation
syndrome associated with, 179,
201
as squinting cause, 84
torsional, rectus muscle
transposition surgery for,
406–407
vertical, 87–88
V-pattern
arrow, 285, 286
bilateral superior oblique
paresis-related, 296, 297
craniosynostosis-related, 369
definition of, 284
ET-pattern, 284
treatment of, 287–289
XT-pattern, 284
Y-pattern, 285
Strabismus examination. See Motor
examination, ocular
Strabismus fixus, 232, 339
acquired, 351
myopic, 351–352
Strabismus surgery, 388–422
complications of
slipped or lost rectus muscle,
418–419
stretched insertion scar, 419
effect on astigmatic correction,
523
Faden procedure, 333, 399–402
inferior oblique muscle weakening
procedures, 407–411
anterior transposition, 407–410
extirpation-denervation, 407
graded recessionanteriorization, 410–411
myotomy, 407
recession, 407, 408
muscle recession procedures,
388–396
adjustable suture technique in,
394–396
hang-back technique in,
393–394, 396
as incomitant strabismus
treatment, 332
inferior oblique muscle, 311,
391, 407, 408
inferior rectus muscle, 37, 337
lateral rectus muscle, 274–275,
287, 288, 373
rectus muscle, 388–391
Starling’s length-tension curve
in, 388, 389, 390
muscle shortening procedures,
396–399
plications, 396, 398–399
resections, 396, 397
tucks, 396, 397–398
muscle transposition procedures,
402–407
anteriorization, inferior
oblique, 45–47, 311–312,
327, 407–410
complications of, 406
of horizontal rectus muscle,
287–288, 289, 308, 403, 407
inferior oblique
anteriorization, 45–47,
311–312, 327, 373, 407–410
for rectus muscle palsy,
404–406
for small vertical deviations,
403
for torsion, 406–407
in myotonic dystrophy, 488
recession-resection (“R and R”)
procedure, 399
superior oblique muscle tightening
procedures, 411–414
full-tendon tuck or plication,
413–414
Harada-Ito procedures,
412–413
superior oblique muscle weakening
procedures, 414–418
dissociated vertical deviationexacerbating effect of, 308,
414–418
tenotomy, 415–416
for unilateral inferior oblique
paresis, 305–306
Wright superior oblique
tendon expander, 415,
416–418
Stroke, as dorsal midbrain syndrome
cause, 436, 437
Superior colliculi, 426
Superior oblique muscle
actions of, 27, 40
anatomic insertion of, 27
anatomy of, 40–42
arc of contact of, 27
field of action of, 28, 2