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Neurol Med Chir (Tokyo) 41, 494¿498, 2001
Isolated Abducens Nerve Paresis Associated
With Incomplete Horner's Syndrome Caused
by Petrous Apex Fracture
—Case Report and Anatomical Study—
M. Faik OZVEREN, Koichi UCHIDA*, Fatih S. EROL, Murat T. TIFTIKCI,
Bengu COBANOGLU**, and Takeshi KAWASE*
Departments of Neurosurgery and **Pathology, Firat University Medical School, Elazig, Turkey;
*Department of Neurosurgery, Keio University School of Medicine, Tokyo
Abstract
A 17-year-old male presented with a wound on the right temporal region, oozing hemorrhagic necrotic
brain tissue and cerebrospinal fluid, following a fall. Computed tomography showed temporoparietal
and petrous apex fractures on the right. Neurological examination revealed abducens nerve paresis,
ptosis, and myosis on the right side. The patient was treated surgically for the removal of the free bony
fragments at the fracture site and to close the dural tear. The abducens nerve paresis, ptosis, and myosis
persisted at the 3rd monthly postoperative follow-up examination. The anatomy of the abducens nerve
at the petroclival region was studied in four cadaveric heads. Two silicone-injected heads were used for
microsurgical dissections and two for histological sections. The abducens nerve has three different angulations in the petroclival region, located at the dural entrance porus, the petrous apex, and the lateral
wall of the cavernous segment of the internal carotid artery. The abducens nerve had fine anastomoses
with the trigeminal nerve and the periarterial sympathetic plexus. There were fibrous connections extending inside the venous space of the petroclival area. The abducens nerve seems to be vulnerable to
damage in the petroclival region, either directly by trauma to its dural porus and petrous apex or indirectly by stretching of the nerve through the nervous and/or fibrous connections. Concurrent functional
loss of the abducens nerve and the periarterial sympathetic plexus clinically manifested as incomplete
Horner's syndrome in our patient.
Key words: abducens nerve,
sympathetic plexus
incomplete Horner's syndrome,
Introduction
condition and a cadaveric anatomy study of the abducens nerve in the petroclival region to investigate
the mechanism of injury leading to isolated abducens nerve paresis and incomplete Horner's syndrome.
The incidence of traumatic unilateral abducens
nerve palsy is 1% to 2.7% in patients with head trauma.15) Both severe head traumas and severe cervical
traumas can lead to abducens nerve palsy.2) The low
incidence of abducens nerve palsy among patients
with severe cervical and head trauma may be attributed to the low survival rate after the traumatic
episode.2) Stretching of the abducens nerve at the petrous apex and dural entrance porus may be the
mechanism of injury.2,9,14)
However, abducens nerve palsy has never been associated with incomplete Horner's syndrome caused
by petrous apex fracture. We report a case of this
Received
January 17, 2001;
Accepted
petrous apex fracture,
Case Report
A 17-year-old male was admitted to the emergency
unit of Firat University Hospital, Department of
Neurosurgery, following a fall from a height of 7
meters. He had a scalp hematoma of 10-cm diameter
in the right temporoparietal region. There was an
8-cm vertical wound 1 cm behind the auricle. There
was no lateralization finding, but a slight amount of
hemorrhagic necrotic brain and cerebrospinal fluid
oozed out of the wound. He also had otorrhagia
July 19, 2001
494
Abducens Nerve Paresis and Petrous Apex Fracture
through the right external ear meatus. The Glasgow
Coma Scale score was 12 points. The patient complained of diplopia. Neurological examination revealed lateral gaze restriction, myosis, and ptosis on
the right side (Fig. 1). Computed tomography revealed diastatic fracture of the posterior part of the
right temporal bone, a fracture in the right temporal
region, a fracture in the lateral wall of the right side
of the sphenoid sinus, and a bony fragment at the
right petrous apex (Fig. 2).
Surgery was performed 7 hours after the trauma
under emergency conditions. The upper edge of the
wound was extended to the right frontal region of
the scalp to form a temporoparietal scalp flap. A
dural tear extended from the temporal region to the
border of the transverse sinus on the right side under the fracture. There was a small tear on the upper
side of the sinus. The dural tear was repaired with a
periosteal graft, and the sinus bleeding was stopped
by the periosteal graft and a tissue sealant. Free bony
fragments were also removed during the operation.
The patient awakened with preoperative findings
of diplopia on right lateral gaze, and myosis and ptosis on the right side on the postoperative first day.
The Glasgow Coma Scale score increased to 15
points. There was no sweating abnormality on either
side of the face. However, his complaints persisted
at the 3rd monthly follow-up examination.
495
Fig. 1
Photograph of the patient showing right
lateral gaze restriction, slight ptosis, and
myosis in the right eye indicating abducens
nerve paresis and sympathetic plexus involvement.
Fig. 2
Computed tomography scan showing diastatic fracture of the posterior part of the
temporal bone, fracture of the lateral wall of
the sphenoid sinus, and the bony fragment
at the petrous apex (arrow).
Anatomical Study
I. Materials and methods
Four adult fresh cadaveric heads, 65 to 80 years of
age, were used. The coagulated blood remnants in
the vessels were removed with isotonic NaCl in two
heads, then both the common carotid and vertebral
arteries, and internal jugular veins were perfused
with colored silicone; red for arteries and blue for
veins. The skull vaults and the brains were removed
and the heads were preserved in 10% formalin solution. Both petroclival areas were dissected under an
OPMI MD surgical microscope (Carl Zeiss Co. Ltd.,
Berlin, Germany). Contax 167 M camera (Kyocera
Co. Ltd., Tokyo) was used for photographic
documentation. The petroclival dura mater was dissected and partially removed to expose the structures in this space, protecting the part around the abducens nerve dural entrance porus.
Both the common carotid and vertebral arteries,
and internal jugular veins of two fresh cadaver
heads were perfused with 10% formalin in 0.1 M
phosphate buffered solution (pH 7.4) for histological
examination. The heads were kept in the same fixative solution for 10 days. The calvarium and the
brains were removed. The dura mater around the
Neurol Med Chir (Tokyo) 41, October, 2001
petroclival region covering the cranial base was
carefully lifted away including all the membranous,
nervous, and ligamentous structures. Right and left
sides were separately embedded in paraffin after
processing in a graded ethanol series from 70% to
100%, and serial sections of 5-mm thickness were
made. The sections were stained with hematoxylineosin and Masson-trichrome stains and observed
under the light microscope.
II. Results
The abducens nerve follows three different routes
in its course through the petroclival region. The ab-
496
M. F. Ozveren et al.
ducens nerve runs laterally from its exit point in the
brainstem until piercing the dura mater. At first, its
direction changes medially at the dural entrance porus, forming the first angulation; then laterally at the
petrous apex, forming the second angulation. The
third angulation occurs at the tangential passing of
the lateral wall of the cavernous segment of the internal carotid artery (ICA). The round shape of the
abducens nerve flattens vertically at the third angulation point where the abducens nerve anastomoses
with the periarterial sympathetic plexus surrounding the ICA (Fig. 3). The abducens nerve is covered
by arachnoid membrane and dura mater between
the dural entrance porus and the third angulation
point (Fig. 4). The dural sleeve of the abducens nerve
becomes thinner, and transforms into a semitransparent membrane around this area. This transformation point is located where the lateral wall of the
cavernous segment of the ICA tangentially approaches the medial wall of Meckel's cave just before the third angulation. Fine anastomoses between
the abducens and trigeminal nerves were observed
at this location (Fig. 5). There were fibrous trabeculations extending between the layers of dura mater
which were attached to the membranous coverages
of the trigeminal and abducens nerves, the periarterial sympathetic plexus, and the external layer of
the ICA (Fig. 5).
Fig. 3
Photomicrograph showing flattening of the
abducens nerve (VI) on the lateral wall of
the cavernous segment of the internal
carotid artery (star), at the anastomosis with
the sympathetic plexus fibers (arrowheads).
arrow: inferolateral trunk, double arrow:
meningohypophysial trunk, II: optic nerve,
III: oculomotor nerve, V2: second branch of
the trigeminal nerve.
Discussion
The abducens nerve may be damaged directly by
bony fragments caused by the skull base fracture.
However, the mechanism of abducens nerve paresis
in severe head or cervical trauma without fracture is
controversial. The petrosphenoidal ligament acts as
a contusion point of the abducens nerve in upward
and posterior displacement of the brain in cervical
spine fracture cases.12) However, this mechanism
Fig. 4
Photomicrograph showing the abducens
nerve (VI) has fibrous (arrowheads) and
neural (double arrow) connections with the
internal carotid artery (white star) and
trigeminal nerve (V). black stars: venous
spaces, S: sympathetic nerve. Massontrichrome stain, ×40.
Fig. 5
Photomicrograph showing the dural layer
(D) and arachnoid membrane (arrowhead)
covered the abducens nerve (VI). HE stain,
×40.
Neurol Med Chir (Tokyo) 41, October, 2001
Abducens Nerve Paresis and Petrous Apex Fracture
has been rejected because the abducens nerve is fixed downward below the petrosphenoidal ligament
by the dura mater and the apex of the petrous
pyramid.14) The petrosphenoidal ligament constitutes a bridge between the petrous apex and the
dorsum sellae under the petroclival dura mater. According to our dissection findings, a second layer of
the petroclival dura mater apparently fixes the abducens nerve between the petrosphenoidal ligament
and the petrous apex. Therefore, we suggest that
direct damage of the abducens nerve by the
petrosphenoidal ligament is not the mechanism of
injury as previously stated.14)
Cerebrospinal fluid suspends the brain and the
spinal cord in a watery medium and cushions the
central nervous system from external forces applied
to the skull or vertebral column. The brain weighs
only 50 g when floating in the cerebrospinal fluid.3)
However, a transfer of high velocity to the brain by
the sudden acceleration of the head in severe trauma
causes the rupture of vessels and nerve fibers.6) Considering the movement of the brain in the skull, both
abducens nerves may be stretched downward by a
linear acceleration in the midsagittal plane during
an impact.14) Then, the nerve is compressed against
the petrous apex, resulting in injury. Two points
may be the site of abducens nerve damage in cases of
traumatic bilateral abducens nerve palsy, the dural
entrance porus and the petrous apex.2) Vectorial
analysis of the flexion and extension forces in cervical injuries demonstrated that there was a consistent
vertical component in both types of injuries.17) This
finding indicates an upward movement of the brain
in cervical trauma leading to functional loss of the
nerve at the dural entrance porus of the abducens
nerve. In our opinion, the rigid structure formed by
borders of the dural entrance porus is significant, especially in cervical trauma, because of the upward
movement of the brain. On the other hand, since the
abducens nerve crosses the petrous apex, acute
downward displacement of the brain may compress
and injure the nerve at this location.
The right temporoparietal fracture indicated the
site of the impact in our patient. The brain definitely
moved upwards and right and then downwards in
the skull. The dural entrance porus of the abducens
nerve acted as a fulcrum in the upward movement,
and the nerve stretched at the petrous apex in the
downward movement. We believe that the isolated
abducens nerve paresis was caused by injury at the
two locations mentioned above. The presence of petrous apex fracture specifically suggests direct
damage of the nerve. Incomplete Horner's syndrome indicates definite damage of the periarterial
sympathetic plexus at the third angulation point.
Neurol Med Chir (Tokyo) 41, October, 2001
497
Based on our anatomical dissections, damage of the
abducens nerve is quite possible due to the anastomosis of the abducens nerve with the periarterial
sympathetic plexus at the third angulation point.
Abducens nerve has three angulations in the
petroclival region, at the dural entrance porus,
petrous apex, and the lateral wall of the cavernous
segment of the ICA.16,18) The dural sleeve of the abducens nerve, which protects the nerve from venous
blood, becomes thinner at the end of the petrous
apex and the abducens nerve anastomoses with the
periarterial sympathetic plexus on the lateral wall of
the cavernous segment of the ICA, where the last angulation is located.9,16,18) The sympathetic connections to the abducens nerve were studied in detail,
finding that the connecting fibers must process
some of the functions absent in Horner's syndrome.10,11) Abducens nerve paresis and Horner's
syndrome can be caused by intracavernous aneurysm and petrous apex tumors, but the sweating
function, which is another component of Horner's
syndrome, was not mentioned.5,13) However, involvement of the periarterial sympathetic plexus in the
dissection of ICA present as incomplete Horner's
syndrome, which is characterized with ptosis and
myosis but not anhydrosis, due to sparing of the external carotid plexus, which innervates the facial
sweat glands.1) Similarly, the absence of anhydrosis
in our case indicates incomplete Horner's syndrome.
The results of our anatomical study indicate that
the abducens nerve may be tethered by the periarterial sympathetic nerve fibers during the strong
sudden backward stretching of the nerve. The
anastomoses between the abducens nerve and the
trigeminal nerve were weaker than those with the
periarterial sympathetic plexus. Therefore, their
effect during entrapment may be slight. On the other
hand, the use of long electrodes through the foramen
ovale was considered responsible for the abducens
nerve palsy complication during treatment for
trigeminal neuralgia.7) In our opinion, the abducens
nerve palsy complication during the rhizolysis
procedure provides more evidence for the connections between the abducens and trigeminal nerves
and implies the tethering of the abducens nerve by
these structures.
Two types of connective tissue occur inside the
cavernous sinus; adipose tissue and a network of
collagenous sheaths.8) The fibrous trabeculations extending between the two dural leaves limit the
venous space of the petroclival region as well as suspend the arteries.4,8) The petrosphenoidal ligament is
the largest of the fibrous trabeculations at the
petroclival region and forms a ligament between the
M. F. Ozveren et al.
498
petrous apex and the dorsum sellae including the
posterior clinoid process supporting the posterior
petroclinoid fold. These trabeculations fix the dural
sleeve between the dural entrance porus and the
petrous apex, and thin membranous coverage of the
abducens nerve at the third angulation point. Therefore, the fibrous trabeculations form another tethering structure of the abducens nerve.
In our case, the direct injury was the main
mechanism of abducens nerve paresis, inflicted by
the bony fragment at the petrous apex. However, the
association of incomplete Horner's syndrome indicates damage to the periarterial sympathetic nerve
fibers through the nervous and/or fibrous connections between these two structures. Based on our
anatomical dissections and histological findings, we
suggest that the fixation of the abducens nerve by
the periarterial sympathetic plexus and fibrous
trabeculations may form another mechanism of
nerve damage.
In conclusion, the three angulation points of the
abducens nerve in the petroclival region are critical
locations where the nerve is highly vulnerable to
damage. Association of incomplete Horner's syndrome with abducens nerve paresis suggests the involvement of the periarterial sympathetic plexus
surrounding the ICA. Although the origin of abducens nerve paresis seems to be a direct bony injury
in our patient, these indirect mechanisms may also
be involved.
5)
6)
7)
8)
9)
10)
11)
12)
13)
14)
Acknowledgment
15)
We thank to Professor Sadakazu Aiso (Department
of Anatomy, Keio University School of Medicine)
for his support in the anatomical part of this study.
16)
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Address reprint requests to: M. Faik Ozveren, M.D., Firat
Universitesi, Tip Fakultesi, Arastirma Hastanesi,
Norosirurji Anabilim Dali, Elazig 23200, Turkey.
Neurol Med Chir (Tokyo) 41, October, 2001