Download The Hip and the Neuromuscular Physician From EDX to

The Hip and the Neuromuscular Physician
From EDX to Coxa Saltans
Keith A. J. Sequeira MD
Thomas A. Miller, MD
Timothy J. Doherty, MD
Timothy P. Carey, MD
Douglas C. Ross, MD
2009 COURSE D
AANEM 56th Annual Meeting
San Diego, California
Copyright © October 2009
American Association of Neuromuscular & Electrodiagnostic Medicine
2621 Superior Drive NW
Rochester, MN 55901
Printed by Johnson Printing Company, Inc.
ii
The Hip and the Neuromuscular Physician
From EDX to Coxa Saltans
Faculty
Timothy Carey, MD, FRCS(C)
Thomas A. Miller, BSc, MD, FRCP(C)
Associate Professor
University of Western Ontario
London, Ontario, Canada
Associate Professor
Schulich School of Medicine and Dentistry
Department of Physical Medicine & Rehabilitation
University of Western Ontario
St. Joseph’s Health Care/Mount Hope
London, Ontario, Canada
Dr. Carey is a graduate of the University of Ottawa school of medicine and
also completed his orthopaedic residency there after a year internship at
the Toronto East General hospital. Two years of fellowship training in paediatric orthopaedic surgery followed at the Childrens Hospital of Eastern
Ontario and the Shriners Hospital, Tampa Unit. Dr. Carey has been on
staff at the London Health Sciences Centre since 1995 and is currently an
associate professor at the University of Western Ontario (UWO), program
director of the orthopaedic residency training program UWO, and chief
of paediatric orthopaedics division. His clinical interests include spinal
deformity, cerebral palsy, and limb lengthening.
Timothy J. Doherty, MD, PhD, FRCP(C)
Dr. Miller is a graduate of Queen’s University and trained in physical medicine and rehabilitation at the University of Ottawa. He then performed
a fellowship in clinical neurophysiology at the University of New South
Wales, Australia. He is the medical director of the musculoskeletal rehabilitation program, director of the electrodiagnostic laboratory, the consultant
physiatrist with the Hand and Upper Limb Centre, and co-director of the
Peripheral Nerve Clinic, St. Joseph’s Health Centre, London, Canada. Tom
is an associate professor in the Schulich School of Medicine and Dentistry
at the University of Western Ontario. Dr Miller is currently the president
of the Canadian Association of Physical Medicine and Rehabilitation.
Associate Professor
Departments of Clinical Neurological Sciences and Rehabilitation Medicine
The Schulich School of Medicine and Dentistry
University of Western Ontario
London, Ontario, Canada
Dr. Doherty is an associate professor in the Departments of Clinical
Neurological Sciences and Physical Medicine and Rehabilitation at the
University of Western Ontario in London, Ontario. In 2005, he was
named Canada Research Chair in Neuromuscular Function in Health,
Aging, and Disease. He is a consultant physiatrist and clinical neurophysiologist at London Health Sciences Centre. Dr. Doherty is the author
of over 60 peer-reviewed papers. His research focuses on the examination of the motor system and motor units in health, aging, and disease.
Additionally, his research is aimed at understanding the physiological basis
of impairment in the motor system and rehabilitation interventions to
limit disability.
No one involved in the planning of this CME activity had any relevant financial
relationships to disclose. Authors/faculty have nothing to disclose.
Course Chair: David Bryan Shuster, MD
The ideas and opinions expressed in this publication are solely those of the specific authors and
do not necessarily represent those of the AANEM.
iii
Douglas C Ross, MD, MEd, FRCS(C)
Keith Sequeira, MD, FRCP(C)
Chair, Division of Plastic Surgery
Co-Director, Peripheral Nerve Clinic
Schulich School of Medicine and Dentistry
University of Western Ontario
London, Ontario, Canada
Associate Director
Regional Spinal Cord and Brain Injury Rehabilitation
Parkwood Hospital
London, Ontario, Canada
Dr. Ross is a graduate of the University of British Columbia (BSc, MD).
He also holds a Masters of Education from the Ontario Institute for
Studies in Education at the University of Toronto. He completed his
plastic surgery training at the University of Toronto followed by two years
of fellowship training in hand and microsurgery at Toronto, and hand
surgery in Louisville, Kentucky. He has been a faculty member at the
University of Western Ontario (UWO) since 1992. Dr. Ross is chair of
the Division of Plastic Surgery at UWO, a staff member at the Hand &
Upper Limb Centre at St. Joseph's Health Centre, and co-director of the
Peripheral Nerve Clinic in London. He serves as secretary of the Canadian
Society for Surgery of the Hand and is a member of the American Society
for Surgery of the Hand, the American Society for Peripheral Nerve, and
the American Society for Reconstructive Microsurgery. His clinical interests include upper extremity surgery, reconstructive microsurgery and peripheral nerve surgery. He also has a strong interest in surgical education.
Dr. Sequeira is a graduate of the University of Toronto and completed his
residency at the Albany Medical Center in New York where he was chief
resident during his final year. He completed a fellowship in electrodiagnostic and sports medicine at Michigan State University. Dr. Sequeira is currently the associate director of the Regional Spinal Cord and Brain Injury
Rehabilitation Programs at Parkwood Hospital in London, Ontario. He
holds an appointment at the University of Western Ontario as an associate
professor and residency program director in the Department of Physical
Medicine & Rehabilitation. He is the director of the undergraduate musculoskeletal curriculum at the Schulich School of Medicine at the University
of Western Ontario. He runs a spasticity clinic at Parkwood Hospital and
is actively involved in spinal cord and brain injury research, medical school
education and has been in active practice for over 10 years.
iv
iv
Practice Management
AANEM Course
Please be aware that some of the medical devices or pharmaceuticals discussed in this handout may not be cleared by the FDA
or cleared by the FDA for the specific use described by the authors and are “off-label” (i.e., a use not described on the product’s
label). “Off-label” devices or pharmaceuticals may be used if, in the judgement of the treating physician, such use is medically indicated to treat a patient’s condition. Information regarding the FDA clearance status of a particular device or pharmaceutical may
be obtained by reading the product’s package labeling, by contacting a sales representative or legal counsel of the manufacturer
of the device or pharmaceutical, or by contacting the FDA at 1-800-638-2041.
v
The Hip and the Neuromuscular Physician
From EDX to Coxa Saltans
Contents
Faculty
ii
Objectives
v
Course Committee
vi
Three Important Musculoskeletal Conditions Involving the Groin and Buttock: Femoroacetabular Impingement,
“Sports Hernia”, and Trochanteric Bursal Pain Syndrome
1
The Diagnosis and Management of Piriformis Syndrome: Myths and Facts
9
Keith Sequeira, MD, FRCP(C); Douglas D.R. Naudie, MD, FRCS(C)
Thomas A Miller, M.D. FRCP(C); Douglas C Ross, MD, MEd, FRCS(C)
Lumbosacral Plexopathy: The Clinical and Electrodiagnostic Spectrum
19
Neuromuscular Disease and the Hip: An Orthopedic Perspective
25
Evaluation and Surgical Treatment of Neurologic Injuries Around the Hip
33
Timothy J. Doherty, MD, PhD
Timothy P. Carey, MD, FRCS(C)
Douglas C. Ross, MD, MEd, FRCS(C); Thomas A. Miller, MD, FRCP(C)
O b j e c t i v e s — After attending this session, participants will be able to (1) distinguish and contrast presentations of musculoskeletal
hip and pelvic pain for the clinical EDX physician, (2) summarize the myth and facts about piriformis syndrome, (3) develop a clinical
and EDX approach to lumbosacral plexopathy, (4) demonstrate and recognize orthopedic treatment options for the hip, pelvis, and lower
limb in neuromuscular disease, and (5) appreciate the surgical treatment options in nerve injury including “neurotization” for lower-limb
nerve injuries.
P r e r e q u i s i t e — This course is designed as an educational opportunity for physicians.
A c c r e d i tat i o n S tat e m e n t — The AANEM is accredited by the Accreditation Council for Continuing Medical Education
to provide continuing medical education (CME) for physicians.
CME C r e d i t — The AANEM designates this activity for a maximum of 3.25 hours in AMA PRA Category 1 Credit(s).TM If
purchased, the AANEM designates this activity for 2 AMA PRA Category 1 Credit(s).TM This educational event is approved as an
Accredited Group Learning Activity under Section 1 of the Framework of Continuing Professional Development (CPD) options for the
Maintenance of Certification Program of the Royal College of Physicians and Surgeons of Canada. Each physician should claim only
those hours of credit he or she actually spent in the educational activity. CME for this course is available 10/09 - 10/12.
vi
AANEM Course
2008-2009 AANEM COURSE COMMITTEE
Anthony E. Chiodo, MD, Chair
Ann Arbor, Michigan
Shawn J. Bird, MD
Philadelphia, Pennsylvania
Mazen M. Dimachkie, MD
Kansas City, Kansas
Gary L. Branch, DO
Dewitt, Michigan
John E. Hartmann, MD
Augusta, Georgia
John E. Chapin, MD
Walla Walla, Washington
David Bryan Shuster, MD
Dayton, Ohio
2008-2009 AANEM PRESIDENT
Michael T. Andary, MD, MS
East Lansing, Michigan
Benjamin S. Warfel, II, MD
Lancaster, Pennsylvania
AANEM Course
Practice Management
1
Three Important Musculoskeletal
Conditions Involving the Groin
and Buttock: Femoroacetabular
Impingement, “Sports Hernia”, and
Trochanteric Bursal Pain Syndrome
Keith Sequeira MD, FRCP(C)
Douglas D.R. Naudie, MD, FRCS(C)
Department of Physical Medicine and Rehabilitation
University of Western Ontario
London, Ontario, Canada
Department of Orthopedic Surgery
University of Western Ontario
London, Ontario, Canada
INTRODUCTION
Hip and groin injuries only account for 2-4% of all adult athletic
injuries, but are a significant cause of morbidity.1-6 The complexity
of the anatomy and the numerous structures (e.g., muscles, abdominal contents, nerves, cartilage) often make it a challenge to confirm
diagnosis; in approximately 30% of cases, it remains unclear.5,7 The
differential diagnoses include: muscle strain, tendonitis, apophysitis, fracture (stress, avulsion, trauma related), bursitis (trochanteric,
ischial), iliotibial band syndrome, labral tear, femoroacetabular
impingement, snapping hip syndrome, osteitis pubis, degenerative
disease, peripheral nerve injury, and sports hernia.5,8
edge of the acetabulum and outlines the periphery. It ends at the
inferior part of the acetabulum and is innervated by numerous
sensory nerve endings mediating deep sensation, pressure, and
pain.9-12 The labrum has several contact surfaces, which articulate
with the femoral head, acetabulum, and joint capsule. It is composed of thick cartilage (type I collagen), mostly arranged in parallel to the acetabular rim. Approximately the outer one-third of the
hip labrum is vascular.9,10
This manuscript focuses on three important non-neurological
causes of groin and buttock pain in young patients. It discusses the
clinical features, diagnosis, treatment, and prognosis for femoroacetabular impingement (FAI), sports hernia (SH), and trochanteric
bursitis (Table 1).
The labrum serves many functions. It deepens the socket, increases
surface area, distributes load, and reduces articular stress.8-12 Its
most important role is to improve stability of the joint by distributing pressure, especially during motion.8,10 The labrum also helps to
seal the joint, maintaining fluid and hydrostatic pressure within it.
It reduces the forces that would otherwise be applied to the articular cartilage of the joint. Because the labrum is deeply innervated,
a tear can result in pain as well as early joint deterioration (osteoarthritis) and destabilization.8-14
FEMOROACETABULAR IMPINGEMENT
Description
Anatomy
FAI is a hip disorder characterized by impaired joint clearance
between the femoral head/neck and acetabulum. Two types have
been described: femoral cause (CAM) and acetabular cause (pincer)
impingement.8-11,13-18
The ball and socket hip joint consists of the femoral head and
acetabulum. The articular surface of the acetabulum is a dense
cartilage (type II collagen) that also covers most of the femoral
head.8.10,11 The acetabular labrum is a fibrocartilaginous structure
similar to that in the shoulder. The labrum is attached to the bony
CAM impingement is caused by an abnormality of the anterolateral femoral head-neck junction8,10,13-15,19-25 that manifests as
2
Three Important Musculoskeletal Conditions Involving the Groin and Buttock
AANEM Course
Table 1
Conditions
Important Neurological
Differential Diagnosis
Distinguishing Features
Helpful Imaging
Treatment
FAI
Femoral Acetabular
Impingement
Ilioinguinal neuropathy,
L1-2 radiculopathy,
Obturator Neuropathy
Age 30-45; Groin pain (no swelling);
Anterior impingement on exam;
typically no neurologic symptoms.
X-ray (AP, cross table lateral)head/neck offset; MRI/MRA
(labral, cartilage deficiencies).
Conservative Tx often
poor; surgical treatment
better short-term; long-term
prognosis with surgery
uncertain.
SH
Ilioinguinal neuropathy,
Age varies; Groin pain (occ asional
Genitofemoral Neuropathy, swelling); pain w/ resisted groin
testing/stretching; typically no neuro
L1-2 radiculopathy,
logic symptoms. Pubic tubercle tender;
Obturator Neuropathy
subtle swelling/tender inguinal ring
Imaging to rule out other
causes, not to confirm Dx.
(e.g., ultrasound hernia, or
MRI
Conservative Tx often
poor; surgical helps with
diagnosis and treatment.
Age varies; pain to palpate lateral
buttock; worse with standing or lying
on affected side; associated w/tingling
in L5/S1 distribution.
Physical exam most useful;
imaging to rule out other
causes; inflammation not
typically seen.
Sports Hernia
GTPS
Greater Trochanteric
Bursitis
L5/S1 radiculopathy, spinal
stenosis, SI Dysfunction
Piriformis Syndrome,
Sciatic Neuropathy
osteitis pubis
Conservative Tx (NSAIDs,
physiotherapy, avoid
exacerbating factors);
corticosteroid injections
helpful; surgery rarely.
MRI = magnetic resonance imaging; MRA = magnetic resonance angiography; NSAIDs = nonsteroidal antiinflammatory drugs
insufficient anterolateral concavity. The shape of the femoral head
(aspherical) promotes extra contact between the femoral head/
neck and acetabulum. The extra stress on the adjacent cartilage
results in excess compressive force and injury to the labrum or
adjacent condral surface. CAM impingement typically presents in
males, with onset of symptoms between 30 and 39 years of age.1315
Any deformity of the femoral head or neck or decreased head/
neck concavity (“offset”) can result in CAM impingement; these
include femoral neck retroversion, Legg-Calvé-Perthes disease,
and slipped capital femoral epiphysis, or malunited femoral
neck fractures.
Pincer impingement happens when overcoverage of the femoral
head by the acetabulum8,10,13-15,19-25 causes contact between the
labrum and femoral neck, compressing the labrum during physiologic hip motion. Forces are spread to the labrum and underlying cartilage, extending to the lip of the acetabulum. Over time,
chronic impingement leads to excess bone growth at the base of the
labrum.16,17 Repetitive loading eventually causes the labrum to fail
and become symptomatic. Pincer impingement most often presents
in females between the ages of 40 and 49, with groin pain after
activity.13-15 Predisposing factors include a retroverted acetabulum
or coxa profunda.17
Clinical Presentation
Previously, labral tears were thought to occur developmentally
or via high force/trauma.13,14 However, data show that abnormal
contact between the femoral head/neck and acetabulum causes FAI,
and can lead to labral tears and cartilaginous injuries.13,14 Damage
to the hip labrum is one purported mechanism for the development
of early hip degenerative disease.13-17 The femoral head and hip
joint have the least bony anterior support, and rely on the labrum,
ligaments, and joint capsule for stability.8,10,11,12 Because much of
the labrum is avascular, it is unclear if labral tears heal spontaneously.
Originally described by Ganz and colleagues in 2001,14 FAI is now a
recognized cause of hip pain and osteoarthritis in young adults. The
typical age of patients is 30 to 50 years, with a slight preponderance of males.13-18 FAI often presents insidiously with groin pain.
Patients are usually active and/or athletic, and frequently there is
no inciting trauma or event. Although the condition is often radiographically bilateral, symptoms are typically unilateral.13-18
The pain associated with this condition is sharp or dull, and usually
located in the groin. Aggravating factors include running, pivoting,
walking, and flexion activities, such as climbing stairs, getting up
from a seated position, and prolonged sitting. Rest and frequent
position changes alleviate discomfort. The initial pain is mild, but
gradually progresses to moderate or severe levels. Growing intensity
limits participation in sports and other activities. Patients often
note that they periodically limp during symptoms, exertion, and
toward the end of more intense activity.
Diagnosis
Physical examination shows reduced active and passive (may be
pain related) hip flexion. Patients often have a slightly antalgic gait.
Data suggest that the hip anterior impingement test is generally
the most sensitive and specific examination technique.10,13-15 With
the patient in a supine position, the hip is passively flexed to 90
degrees as the examiner adducts the leg and gently rotates the hip
internally. Limitation of movement and pain at the end of range are
important positive signs. Most patients (95%) with this condition
have a positive finding.10,13-15 In a recent study, the involved side
revealed 9° less hip flexion, 3 degrees less adduction, and 4 degrees
less internal rotation.15
AANEM Course
The Hip and the Neuromuscular Physician From EDX to Coxa Saltans
Flexion Abduction External Rotation (FABER) testing also often
reveals groin pain on the side being moved. To test for posterior impingement, the patient lies in a supine position while the examined
leg is allowed into extension off the side of the table. The clinician
provides external rotation of the hip as it is extending. A positive
test produces pain in the groin during this motion. This test is far
less sensitive than the anterior impingement test for FAI.13-15
Studies indicate that the labrum takes on some weight-bearing load
at the end range of motion, with excess or repetitive force causing
injury.8,11,12 Patients with FAI are often involved in athletics requiring hip flexion and/or rotation. Typical sports include hockey, tennis,
martial arts, weight lifting, soccer, horse riding, and dance. All of these
require frequent, and at times, forceful hip external rotation.13-17
Misdiagnoses are common; it takes an average of 2 years9,10 before
FAI is identified. In one recent study, 20-25% of athletes with
groin pain and 55% of patients with mechanical hip pain of
unknown cause were eventually found to have a labral hip tear and
a diagnosis of FAI.9,10
Investigations
The diagnosis is mostly made on history and physical examination. However, there are imaging findings that help support one’s
conclusions.17,24,26,27 Hip X-rays are the first and most important
diagnostic tool. Anterior-posterior pelvic radiographs will confirm
retroversion or coxa profunda (pincer impingement).17,24,26,27
Examination of the femoral head-neck is essential. Femoral headneck offset measures the difference between the widest diameter
of the femoral head and the most prominent part of the femoral
neck.13,14 Reduced offset can result in CAM impingement . Lateral
and cross-table lateral views are also essential, and provide additional information regarding femoral head sphericity and headneck relationship.13,14,24,26,27 It is important to notify the radiologist
of your suspicion as findings are often subtle.
Computed tomography imaging can assess the bony architecture of the hip, and is useful for diagnosing CAM lesions, and if
needed, surgical planning. It should be used with caution given its
limited utility and high radiation exposure compared to magnetic
resonance imaging (MRI). The latter, and especially magnetic resonance arthrography (MRA) (gadolinium), are useful in the workup
of FAI and assessment of the labrum and articular cartilage.26,27
MRA distends the joint and separates the various articular structures, allowing visualization of the cartilage and labrum. MRA can
localize head-neck offset, labral tears, and cartilage lesions.26,27 If
the abnormality of the head-neck is not found, and only the labral/
cartilage lesions are treated, the underlying cause will be missed and
the problem will recur.
Conservative Treatment
Nonsurgical treatment should always be considered first. This
includes activity modification and/or stopping the precipitating
3
sport, at least temporarily. Often this is difficult as many patients
are competitive athletes who do not want to stop. They need to
be made aware of the long-term consequences of the condition if
allowed to persist untreated, i.e., degenerative disease.
A course of physiotherapy to target the tight and weak muscles is
typically a good initial treatment. Stretching the hip flexors and
strengthening the core muscles and glutei can be helpful. A short
course of nonsteroidal anti-inflammatory drugs (NSAIDs) or other
pain medication can often help control pain and allow patients to
take full advantage of therapy. A diagnostic and therapeutic injection
(guided with ultrasound or fluoroscopy) with anesthetic/cortisone
may help.20,21 If this reduces the pain, it provides confirmation that
the hip joint is the problem. The pain control achieved with such
an injection may allow increased therapy and further improvement.
Alterations of lower extremity mechanics (i.e., foot/shoe orthotics)
can help correct leg length discrepancies or malalignments.
Surgical Treatment
Open and arthroscopic treatments have been described. The open
procedure involves dislocation of the hip, careful preservation
of the hip`s blood supply, and treatment directed to the pathology.18,20,22 It typically involves some form of femoral osteoplasty
(removal of the impinging `bump`) and debridement/repair of the
labrum and articular cartilage. Very good short-term improvements
have been noted in symptoms, function, and return to activity/
sport.18,22 Long-term outcomes are still unknown.
SPORTS HERNIA VERSUS ADDUCTOR STRAIN
Anatomy/Description
SH is a nonspecific diagnosis that refers to groin pain in an athlete
related to a weakness of the posterior inguinal wall,28-49 and relates
to an abnormality of the internal or external abdominal oblique
muscles, inguinal ligament, or conjoined tendon.28-31 It typically
results in a loss of inguinal canal integrity without a clinically detectable hernia.28-30 Imbalance between the adductor and abdominal muscle strength/pull may also lead to this condition.31,36,40,46
For instance, repetitive or extreme forces applied by the adductor
muscles may injure the internal oblique and/or transversalis fascia
attachments to the inguinal ligament. In men, the internal oblique
muscle forms the cremaster and spermatic fascia, which may be
why these injuries cause scrotal and testicular pain.11, 28
Clinical Presentation
Patients often present with insidious groin pain that gradually
worsens. Increases in intra-abdominal pressure (e.g.,situps, cough,
sneeze) or vigorous hip/leg activity (e.g., kicking a ball, pivoting)
worsen the pain. In fact, reproduction of groin pain during the
sporting activity is important to make this diagnosis.30,31,42-45,48,49
Symptoms typically improve with rest but recur with activity.
4
Three Important Musculoskeletal Conditions Involving the Groin and Buttock
Diagnosis/Investigations
Four abnormalities are generally found on examination: (1) inguinal canal tenderness; (2) dilated superficial inguinal ring; (3)
pubic tubercle tenderness; and (4) hip adductor origin tenderness.29-31,36,37 The most important physical examination findings
are pubic tubercle tenderness and an inguinal floor tear that may be
palpable, causing pain in the external inguinal ring. Unfortunately,
these findings are not specific for SH.
SH is a nonspecific diagnosis made on clinical grounds. It is difficult
to differentiate it from a muscle strain of the rectus abdominus and
adductor group. There is no test that definitively confirms the presence of a SH. Although dynamic ultrasound has shown promise (as
the patient strains, a bulge is noted at the superficial inguinal ring),
the findings are subtle and extremely operator dependent.28,29,30,39
Testing is done to rule out other causes for the pain (e.g., MRI to
rule out muscle tear, bone scan for osteitis pubis).
Pain on palpation in the adductor musculature and with resisted
hip adduction suggests an adductor strain. Unfortunately, herniography (injecting contrast into the peritoneal cavity) has a high false
positive rate and cannot be reliably trusted to diagnose a SH.28,38,39
Although there are numerous helpful signs/tests, none confirm this
diagnosis. Often, it can only be determined at the time of surgery.
In spite of all investigations to date, there is no consensus as to what
constitutes a SH, and it remains a diagnosis of exclusion.
Conservative Treatment
Conservative treatment (e.g., 6 to 8 weeks of rest, activity modification, medications, physiotherapy) is often disappointing.29-33,41-45
Biomechanical abnormalities (leg length discrepancies, muscle
imbalances, and leg/foot malalignments) need to be ruled out or
treated. If needed, physiotherapy and the use of suitable foot/shoe
orthotics can address these issues. An adequate trial of therapy
should involve strengthening of the core, pelvic, and adductor
muscles. The biomechanics of the sport being performed should
also be assessed and errors in technique that predispose to injury
should be corrected.
Therapy should focus on correcting imbalances between the hip and
abdominal muscles and on endurance, coordination, and flexibility
of the trunk and upper leg musculature.41 Transient improvement
occurs when trigger activities are avoided, but pain often returns
when the inciting maneuver is performed. Attempts to return to
sport should be considered once the patient is pain-free. Injection
treatment (corticosteroid, prolotherapy) directed to the adductor
origin can temporarily relieve pain.29-34 However, literature on the
results of injections for sport hernias is sparse.
Surgical Treatment
SHs, unlike most cases of groin pain, rarely improve long-term
without surgical treatment. Surgery for this condition has a good
success rate (60-90% symptom relief and return to sport).29-33,46,49
AANEM Course
The most common finding is posterior inguinal wall insufficiency
that creates an occult hernia, not noticeable on physical examination.29,40,42,49 Open or laparoscopic herniorrhaphy with mesh
reinforcement has good success rates.49 The goal of surgery is
generally to reinforce the abdominal muscles and/or fascia around
the inguinal ligament (similar to other inguinal hernia surgeries). Additionally, a portion of the adductor muscle origin can be
released to restore the balance between these muscles and the abdominal group. Postoperative care involves walking with a gradual
progression to jogging by 3 to 4 weeks, as pain allows. Cutting activities should be slowly introduced at 2 to 3 months, as tolerated.
Rehabilitation after laparoscopic techniques generally progresses
faster than with open procedures. If patients receive appropriate
postoperative treatment, a return to full activities is often possible
within 3 to 4 months.
Differential Diagnosis
Adductor strain is the most common cause of groin pain in athletes.34,39,41,43 It is often seen in those involved in soccer or sports
requiring pivoting (e.g., squash, hockey, tennis). The proximal
musculotendinous junction of the adductor longus and/or gracilis
is typically involved.39,41 An MRI can help rule out a muscle or
tendon tear. If a tear is present, a period of relative rest is necessary. A thorough biomechanical evaluation is needed, similar to
treatment of a SH. Acute management should attempt to reduce
pain and swelling with rest, ice, and compression. This should
be followed by physiotherapy to restore range of motion, reduce
pain, increase strength, and eventually begin active sport-specific
training and return to competition. NSAIDs and corticosteroid
injections are often used, but the literature is unclear about their efficacy.29-31,44-47 Anecdotal evidence supports alternative treatments
like acupuncture, mobilization, transcutaneous electrical nerve
stimulation, and liniments, but additional studies on their efficacy
are needed.31-34
GREATER TROCHANTERIC PAIN SYNDROME
Anatomy/Description
Bursae, fluid-filled sacs that cushion bony regions and adjacent soft
tissue structures, are abundant in the lateral hip region. The two
major ones are the subgluteus maximus and subgluteus medius
bursae.11,50,51 The former, located superficial to the gluteus medius
tendon and deep to the tensor fascia latae and gluteus maximus
muscles, is the biggest bursa. It contributes most to greater trochanteric pain syndrome (GTPS).50-57 The gluteus minimus bursa,
located cephalad and ventral to others, is relatively minor. The
varied anatomy, number, and location of these bursae create a variable clinical presentation for GTPS.
The gluteus medius and minimus muscles/tendons play an important role in GTPS. Inflammation, irritation, and/or minor tears in
the musculotendinous regions present with localized pain in the
lateral hip region. Secondary inflammation of the adjacent bursae
AANEM Course
The Hip and the Neuromuscular Physician From EDX to Coxa Saltans
may occur, but bursitis is not typically the primary pathology.52
Bursitis tends to result from repetitive microtrauma between adjacent surfaces, muscle dysfunction, or tightness that causes abnormal
movement mechanics or muscle overuse. In a retrospective review
of MRIs in 24 patients with lateral hip pain, most had gluteus
medius abnormalities (minor tears). Bursitis was uncommon.55
Clinical Presentation
GTPS usually presents with insidious lateral hip and buttock
pain. Exacerbating factors include lying down on the affected
side, prolonged standing, and transitioning from sitting to standing.50,51 Running, walking on uneven terrain, cutting activities, and
climbing stairs often provoke symptoms. Pain frequently radiates
along the lateral thigh to the knee. Numbness, tingling, and frank
weakness are not typically associated with GTPS. The physical
examination is normal except for pain and tenderness localized to
the posterolateral hip region and the origin of the gluteus medius
tendon. Pain can be reproduced with resisted abduction and external rotation. In general, however, the physical exam is nonspecific
and not well-correlated with imaging findings.50-57
Diagnosis/Investigations
This diagnosis pertains to pain along the lateral buttock and hip
region. It typically affects 10-25% of individuals over the age of
50, but can also afflict young athletes, especially those susceptible
to buttock and leg muscle tightness (e.g., runners).50,51 Although
previously known as trochanteric bursitis, the condition typically
lacks frank clinical or pathological inflammation.52 In addition,
numerous bursae in the lateral hip region are potential contributors
to this condition.50-53
Numerous risk factors are associated with the development of
GTPS. These include: obesity, female gender, low back pain, hip/
knee/lumbar degenerative disease, age >50, and iliotibial band
(ITB) tightness.50,51,53-57 It is often confused with myofascial
buttock pain, spinal pathology, and degenerative joint disease.
Conservative Treatment
Most cases of GTPS resolve spontaneously with conservative treatment. NSAIDs, relative rest, ice massage, weight loss, and behavior
modification (avoiding lying on the affected side, limiting climbing
and other precipitating factors) may speed recovery and improve
pain. Physiotherapy aimed at restoring normal biomechanics of
the hip and buttock region, core muscle strengthening, and lower
extremity flexibility training can also help.50,51,56,57
If conservative care fails to resolve the pain, injections may be
considered.58-63 Although no placebo-controlled trials have been
completed, prospective studies suggest improvements in pain with
cortisone/anesthetic up to 6 months postinjection.55 Repeat injections, once the initial one wears off, are also effective. Thus far,
5
fluoroscopically guided injections have not been shown to work
better than landmark guided ones.59,61 This likely relates to the
numerous bursae involved and the myotendinous rather than inflammatory nature of the problem.55,59,61 Given the varied etiology
of GTPS, peribursal injections are more likely to go into the soft
tissue structures, where the problem lies.
Corticosteroid injections are a safe, simple, and effective treatment for GTPS.58-63 Injections are used to treat the condition,
provide pain relief, enhance participation in therapy, and confirm
the diagnosis. Elevations of blood sugar have been reported up
to 21 days post- injection.64-66 Thus, care needs to be taken with
diabetic patients, especially with peribursal or soft tissue injections;
The most common complications postinjection involve increased
pain in the injected area (2-10%).64-66 Less common complications
include fat and skin atrophy (1%), infection (0.1%), and tendon
rupture (especially involving the Achilles tendon and plantar
fascia – 0.1%).65-67
Little evidence supports the efficacy of one steroid preparation
over another. Injectable steroids improve pain and inflammation
by reducing synovial blood flow and the inflammatory response.60
Insoluble steroids have a longer duration of action and higher
incidence of cutaneous side effects. The least soluble are triamcinolone hexacetonide, followed by triamcinolone acetonide.60
Methylprednisolone acetate is moderately soluble and is the most
commonly used injectable steroid in North America. In a recent
review from the United Kingdom, it was recommended for large
joints.60 Betamethasone has a high solubility and shorter duration
of action, and may be better for soft tissue injections, such as the
trochanteric bursal region.60 Duration and onset of action of anesthetics vary. Bupivacaine has a 30 minute onset of action and 9
hour duration. Lidocaine has a 1-2 minute onset of action and 1
hour duration.60
Surgical Treatment
Refractory GTPS can also be treated surgically. Prospective shortterm studies show that bursectomy and ITB release can improve
pain in such cases.50,55,56 Long-term studies on GTPS and surgical
outcomes are needed.
SUMMARY
Hip and groin pain is a common complaint in young athletes.
In this article, we discussed the clinical presentation, diagnosis,
treatment, and prognosis for FAI, SH, and GTPS. As with many
musculoskeletal disorders, the history and physical examination are
vital to differentiate between the various causes. Investigations are
used to confirm clinical findings and rule out alternate sources of
symptomology.
FAI is a relatively new diagnosis that presents with groin pain in the
young adult population. It is under-recognized and without a gold
standard test. FAI is characterized by reduced clearance between the
6
Three Important Musculoskeletal Conditions Involving the Groin and Buttock
femoral head/neck and the acetabulum, resulting in an “impingement syndrome.” It is diagnosed by history and physical examination, supported with imaging findings. As our knowledge of this
condition and hip anatomy/biomechanics improve, so will our
ability to recognize it and utilize additional imaging (MRA, MRI)
to diagnosis it. FAI is associated with premature hip osteoarthritis
in young adults. Thus, it is important to be aware of this and to
know that early identification and treatment may delay onset and
progression in this population.
SH is a nonspecific diagnosis that is not a “true hernia.” Most
conventional tests are normal; clinical features, diagnostic criteria,
and physical examination findings are nonspecific. It is mostly a
diagnosis of exclusion. Subtle findings of posterior inguinal wall
insufficiency are often found during surgery; in addition, SH often
responds favorably to surgical treatment and repair.
GTPS pertains to pain in the lateral buttock in the area of the
trochanteric bursa. Pain increases with lying on the affected side,
walking, and standing. There is no definitive diagnostic test for this
condition. One of its hallmarks is response to conservative treatment, including relative rest, activity modification, corticosteroid
injections, physiotherapy, and NSAIDs. In rare instances, surgical treatment (bursectomy, ITB release) is needed. In such cases,
surgery helps, at least in the short- term.
REFERENCES
1. Keogh MJ, Batt M. A Review of Femoroacetabular Impingement in
Athletes. Sports Med. 2008;38:863-878.
2. Caudill P, Nyland J, Smith C, Yerasimides J, Lach J. Sports hernias: a
systematic literature review. Br J Sports Med. 2008;42:954-964.
3. Kluin J, den Hoed PT, van Linschoten R. Endoscopic evaluation and treatment of groin pain in the athlete. Am J Sports Med.
2004;32:944-949.
4. Gilmore OJA. Groin pain in the soccer athlete: fact, fiction and treatment. Clin Sports Med. 1998;17:787-793.
5. Morelli V, Smith V. Groin injuries in Athletes. Am Fam Phys.
2001;64:1405-1415.
6. Karlsson J, Sward L, Kalebo P, Thomee R. Chronic groin injuries in
athletes. Recommendation for treatment and rehabilitation. Sports
Med. 1994;17:141-148.
7. Roos HP. Hip pain in sport. Sports Med Arthroscopy Rev. 1997;5:292300.
8. Groh M, Herrera J. A comprehensive review of hip labral tears. Curr
Rev Musculoskel Med. 2009.
9. Bharam S. Labral tears, extra-articular injuries, and hip arthroscopy in
the athlete. Clin Sports Med. 2006;25:279-292.
10. Keogh M, Batt M. A review of femoroacetabular impingement in
athletes. Sports Med. 2008;38:863-878.
11. Standring S (editor). Gray’s Anatomy. 39th edition. London: Churchill
Livingstone, 2004.
12. Leunig M, Beck M, Woo A. Acetabular rim degeneration: a constant
finding in the aged hip. Clin Orthop Relat Res. 2003;413:201-207.
13. Hart E, Metkar U, Rebello G, Grottkau B. Femoroacetabular
impingement in adolescents and young adults. Orthop Nurse.
2009;28:117-124.
AANEM Course
14. Ito K, Minka MA 2nd, Leunig M, Werlen S, Ganz R. Femoroacetabular
impingement and the cam-effect. A MRI-based quantitative anatomical study of the femoral head-neck offset. J Bone Joint Surg Br. 2001
Mar;83:171-6.
15. Beaule P, Allen D, Clohisy J, Schoenecker P Leunig M. The young
adult with hip impingement: deciding on the optimal intervention.
AAOS Instructional Course Lectures. 2009;58:213-222.
16. Clohisy J, Knaus E, Hunt D, Lesher J, Harris-Hayes M, Prather H.
Clinical presentation of patients with symptomatic anterior hip impingement. Clin Orthop Relat Res. 2009;467:638-644.
17. Bathala E, Bancroft L, Peterson J, Ortiguera C. Radiology case study.
Femoroacetabular impingement. Orthopedics. 2007;30:1061-1064.
18. Ganz R, Parvizi J, Beck M, Leunig M, Notzli H, Siebenrock K.
Femoroacetabular impingement: A cause for osteoarthritis of the
hip. Clin Orthop Relat Res. 2003;417:112-120.
19. Parvizi J, Ganz R. Femoroacetabular Impingement. Semin
Arthroplasty. 2005;16:33-37.
20. Philippon M, Maxwell R, Johnston T. Clinical presentation of femoroacetabular impingement. Knee Surg Sports Traumatol Arthrosc.
2007;15:1041-1047.
21. Robertson W, Kadrmas W, Kelly B. Arthroscopic management of
labral tears in the hip: a systematic review. Clin Orthop Relat Res.
2007;455:88-92.
22. Burnett S, Della Rocca G, Prather H. Clinical presentation of patients with tears of the acetabular labrum. J Bone Joint Surg Am.
2006;88:1448-1457.
23. Fitzgerald R. Acetabular labrum tears: diagnosis and treatment. Clin
Orthop. 1995;311:60-68.
24. Tannast M, Siebenrock K, Anderson S. Femoroacetabular
Impingement: Radiographic Diagnosis-What the Radiologist should
know. American Journal of Radiology. 2007;188:1540-1552.
25. Hickman J, Peters C. Hip pain in the young adult: diagnosis and treatment of disorders of the acetabular labrum and acetabular dysplasia.
Am J Orthop. 2001;30:459-467.
26. James S, Ali K, Malara F. MRI findings of femoroacetabular impingement. AJR Am J Roent. 2006;187:1412-1419.
27. Eijer H, Mahomed M, Ganz R. Crosstable lateral radiograph for
screening of an anterior femoral head-neck offset in patients with
femoroacetabular impingement. Hip Int. 2001;11:37-41.
28. Short C, Zoga A, Kavanagh E, Meyers W. Anatomy, Pathology and
MRI Findings in the Sports Hernia. Semin Musculoskelet Radiol.
2008;12:54-61.
29. Caudill P, Nyland J, Smith C, Yerasimides J, Lach J. Sports hernias: a
systematic literature review. Br J Sports Med. 2008;42:954-964.
30. Morelli V, Smith V. Groin Injuries in Athletes. Am Fam Physician.
2001;64:1405-1415.
31. Morelli V, Espinosa L. Groin injuries and groin pain in athletes: Part
2. Primary Care: Clinics in Office Practice. 2005;32:185-200.
32. Chung L, O’Dwyer PJ. Treatment of asymptomatic inguinal hernias.
Surgeon. 2007;5:95-100.
33. Nam A, Brody F. Management and Therapy for Sports Hernia. J Am
Coll Surg. 2008;206:154-164.
34. Harmon K. Evaluation of groin pain in athletes. Curr Sports Med
Rep.. 2007;6:354-361.
35. Van Hanswijck de Jonge P, Lloyd A, Horsfall L, Tan R, O’Dwyer PJ.
The measurement of chronic pain and health-related quality of life
following inguinal hernia repair: a review of the literature. Hernia.
2008;12:561-569.
36. Farber A, Wilckens J. Sports Hernia: Diagnosis and Therapeutic
Approach. J Am Acad Orthop Surg. 2007;15:507-514.
37. Moeller J. Sportsman’s hernia. Curr Sports Med Rep. 2007;6:111114.
AANEM Course
The Hip and the Neuromuscular Physician From EDX to Coxa Saltans
38. Omar I, Zoga A, Kavanagh E et al. Athletic Pubalgia and
“Sports Hernia”:Optimal MR Imaging Technique and Findings.
Radiographics. 2008;28:1415-1438.
39. Robinson P, Barron DA, Parsons W, et al. Adductor-related groin
pain in athletes: Correlation of MR imaging with clinical findings.
Skeletal Radiol. 2004;33:451-457.
40. Fon LJ, Spence RA. Sportsman’s hernia. Br J Surg. 2000;87:5445552.
41. Holmich P, Uhrskou P, Ulnits L, et al. Effectiveness of active physical
training as treatment for long-standing adductor-related groin pain in
athletes: Randomised trial. Lancet. 1999;353:439-443.
42. Swan KG, Wolcott M. The athletic hernia. A systematic review. Clin
Orthop. 2006;455:78-87.
43. Schilders E, Bilsmil Q, Robinson P, et al. Adductor related groin pain
in competitive athletes. J Bone Joint Surg Am. 2007;89:2173-2178.
44. Macintyre J, Johson C, Schroeder EL. Groin pain in athletes. Curr
Sports Med Rep. 2006;5:293-299.
45. Paluska SA. An overview of hip injuries in running. Sports Med.
2005;35:991-1014.
46. Leblanc KE, LeBlanc KA. Groin pain in athletes. Hernia. 2003;7:6871.
47. Joesting DR. Diagnosis and treatment of sportsman’s hernia. Curr
Sports Med Rep. 2002;1:121-124.
48. Nicholas SJ, Tyler TF. Adductor muscle strains in sport. Sports Med.
2002;32:339-344.
49. Neumayer L, Giobbie-Hurder A, Jonasson O, et al. Open mesh
versus laparoscopic mesh repair of inguinal hernia. N Engl J Med.
2004;350:1819-1827.
50. Williams B, Cohen S. Greater Trochanteric Pain Syndrome: A
Review of Anatomy, Diagnosis and Treatment. Anesth Analag.
2009;108:1662-1670.
51. Segal NA, Felson DT, Torner JC, Zhu Y, Curtis JR, Niu J, Nevitt MC.
Greater trochanteric pain syndrome: epidemiology and associated
factors. Arch Phys Med Rehabil. 2007;88:988-992.
52. Silva F, Adams T, Feinstein J, Arroyo R. Trochanteric bursitis: refuting the myth of inflammation. J Clin Rheum. 2008;14:82-86.
53. Tortolani P, Carbone J, Quartararo L. Greater trochanteric pain
syndrome in patients referred to orthopaedic spine specialists. Spine.
2002;2:251-254.
7
54. Sayegh F, Potoupnis M, Kapetanos G. Greater trochanter bursitis
pain syndrome in females with chronic low back pain and sciatica.
Acta Ortop Belg. 2004;70:423-428.
55. Shbeeb MI, Matteson EL. Trochanteric bursitis (greater trochanter
pain syndrome). Mayo Clin Proc. 1996;71:565-569.
56. Lievense A, Bierma-Zeinstra S, Schouten B, Bohnen A, Verhaar j,
Koes B. Prognosis of trochanteric pain in primary care. Br J Ben
Pract 2005;55:199-204. [Au: correct journal name?]
57. Anderson K, Strickland SM, Warren R. Hip and groin injuries in
athletes. Am J Sports Med. 2001;29:521-533.
58. Shbeeb M, O’Duffy J, Michet C, O’Fallon W, Matteson E. Evaluation
of glucocorticosteroid injection for the treatment of trochanteric
bursitis. J Rheumatol. 1996;23:2104-2106.
59. Cohen S, Narvaez J, Lebovits A, Stojanovic M. Corticosteroid injections for trochanteric bursitis: is fluoroscopy necessary? A pilot study.
Br J Anaesth. 2005;94:100-106.
60. Stephens M, Beutler A, O’Connor F. Musculoskeletal injections: a
review of the evidence. Am Fam Physician. 2008;78:971-977.
61. Hall S, Buchbinder R. Do imaging methods that guide needle placement improve outcome? Ann Rheum Dis. 2004;63:1007-1008.
62. Cardone D, Tallia A. Diagnostic and therapeutic injection of the hip
and knee. Am Fam Physician. 2003;67:2147-2152.
63. Foley B, Christopher T. Injection therapy of bursitis and tendinitis.
Clin Proc in Emerg Med, 4th Ed. Phil, PA 2004:1020-1040.
64. O’Connor F. Common injections in sports medicine: general principles and specific techniques. O’Connor F (ed). Sports Medicine:
Just the Facts. New York NY;2005:426-433.
65. Courtney P, Doherty M. Joint aspiration and injection. Best Pract
Clin Res Rheumatol. 2005;19:345-369.
66. Gray R, Gottleib N. Intra-articular corticosteroids. An updated assessment. Clin Orthop Relat Res. 1983;177:235-263.
67. Acevedo J, Beskin J. Complications of plantar fascia rupture associated with corticosteroid injection. Foot Ankle Int. 1998;19:91-97.
8
AANEM Course
9
The Diagnosis and Management of
Piriformis Syndrome:
Myths and Facts
Thomas A Miller, MD, FRCP(C)
Douglas C Ross, MD, MEd, FRCS(C)
Departments of Physical Medicine and
Rehabilitation and Surgery
Schulich School of Medicine and Dentistry,
University of Western Ontario
London, Ontario Canada
Chair, Division of Plastic Surgery
Co-Director, Peripheral Nerve Clinic
Schulich School of Medicine and Dentistry
University of Western Ontario
London, Ontario, Canada
INTRODUCTION
Though several discrepant definitions exist, to purists, piriformis
syndrome (PS) is best defined as a neuromuscular disorder that is
presumed to occur when the sciatic nerve is compressed or otherwise irritated by the piriformis muscle as it passes through the
sciatic notch. Some have subdivided PS into primary and secondary forms.1,2 Primary PS comprises those cases in which sciatic
nerve root entrapment occurs because of some abnormality within
the muscle itself, as in anomalous anatomy or hypertrophy of the
muscle and/or nerve. Secondary PS usually caused by direct, blunt
trauma to the piriformis muscle. The sciatic nerve entrapment
that results produces a constellation of symptoms that can include
pain, tingling and numbness in the affected buttock and along the
ipsilateral sensory distribution of the sciatic nerve, combined with
focal tenderness directly over the muscle, deep in the sciatic notch,
and worsening of symptoms with certain provocative tests.3 In
this way, it has been likened to other nerve entrapment syndromes
like carpal tunnel syndrome (CTS) and entrapment involving the
ulnar, peroneal, and tibial nerve at the elbow, knee and ankle,
respectively.4 However, unlike these other syndromes that have
gained broad acceptance among clinicians and researchers alike, PS
is mired in controversy. While some believe that cases of true piriformis induced entrapment are rare but do exist, 5-9 others, though
perhaps not questioning the patient’s symptoms, express sincere
scepticism regarding the piriformis’ causative role10 and the use
of invasive injections and surgical procedures to treat it.9 There is
debate as to whether the syndrome is best categorized as an entrap-
ment11 or a myofascial pain disorder.12 This manuscript claims to
explore the various sources of controversy, addressing issues of PS
from both perspectives as they relate to the diagnosis and management of this condition.
MAGNITUDE OF THE PROBLEM
The term “sciatica” has been in existence since at least 1450,13 and
generally refers to a set of symptoms, which includes pain, that are
believed to be caused by general compression and/or irritation of
one of five nerve roots that give rise to the sciatic nerve, or by compression or irritation of the sciatic nerve itself. Characteristically,
patients complain of pain in their lower back, as well as pain into
their buttock, and/or various parts of the leg and foot on the affected side. In addition to potentially severe pain, patients may
report unilateral numbness, muscular weakness, and difficulty
moving or controlling their lower extremity, symptoms not unlike
those claimed for PS. This, in addition to the lack of a gold standard diagnostic test to either confirm or refute the existence of
piriformis induced sciatic nerve entrapment, leads to considerable
difficulties estimating both the incidence and prevalence of PS, per
se. Filler and associates3,4 have pointed out that roughly 1.5 million
magnetic resonance imaging (MRI) scans are performed for sciatica
annually in the United States, and that only 200,000 of these patients obtain relief from surgical procedures to relieve spinal root
pressure, implying that many of the remaining patients have PS. In
fact, in one study,3 magnetic resonance neurography (MRN) and
10
The Diagnosis and Management of Piriformis Syndrome
interventional MRI were utilized in 239 consecutive patients with
sciatica who had failed to respond to traditional treatment, and the
authors ultimately attributed more than two-thirds of these cases to
PS (67.8%), based on diagnostic criteria which included response
to local piriformis injection but not spinal injection (i.e., disc, facet
and/or root). Furthermore, MR-guided injection of a local anesthetic into the piriformis muscle produced relief in almost 85% of
the presumed PS patients, with 15% obtaining relief lasting more
than 8 months; and piriformis surgery performed on 62 patients
resulted in either a good or excellent outcome in 80%.
Several other estimates of the percentage of patients with lower
back and/or buttock pain with PS named as a cause of their
symptoms have been on the order of 5 to 8%,14-20 although some
have claimed a much lower percentage; in fact, suggesting that
entrapment caused by the piriformis muscle is quite rare,5,7-9 and
that the symptoms attributed to PS are caused by nerve impingement from some other structures, or are totally removed from any
impingement at all. One survey that supports the rarity of PS is a
retrospective review that examined 1293 cases of lower back pain
treated at an orthopedic back pain clinic over a 12-year period, in
which the incidence of PS was determined to be 0.33%.21 Clearly,
differences in how PS is defined could have played a major role
in these conflicting prevalence estimates. Stewart,8 for example,
claims that the term is being used to denote four clinically distinct
entities: (1) damage to the sciatic nerve by lesions in the vicinity of
the piriformis muscle, (e.g., hematomas and aneurisms) (2) compressive damage to the proximal sciatic nerve by the piriformis
muscle, usually because of some anatomic anomaly; (3) damage
to the sciatic nerve by the piriformis muscle and adjacent tissue
from trauma and scarring, which was termed post-traumatic PS,
corresponding to the secondary PS mentioned previously; and (4)
chronic buttock pain with no evidence of sciatic nerve damage.
Stewart then argues that the first and fourth definitions should
be excluded. Unquestionably, the number of these entities one
encapsulates within the definition of PS would influence both
its incidence/prevalence and the requirements for its diagnosis,
both generically and in the individual patient. In terms of the
latter issue, Stewart8 further recommends that patients meet five
criteria prior to being assigned the second of his four piriformis
definitions: symptoms and signs of sciatic nerve damage; electrophysiologic evidence of sciatic nerve damage in the absence of any
abnormalities in paraspinal muscles by electromyography (EMG);
imaging of the pelvis/lumbosacral spine that demonstrates no
other pathology; surgical evidence consistent with piriformismuscle induced nerve entrapment; and relief of symptoms postsurgical decompression, though he accepts the potential that
chronic patients may not improve. As will become evident in
further exploration, few patients meet these five criteria.
There seems to be relatively little debate at the individual level
as to why many of the patients ascribed the diagnosis of PS
suffer significantly, their disability largely secondary to pain that
can severely restrict walking or even sitting. Additionally, many
patients see several physicians and undergo years of waiting and
expensive diagnostic imaging before a definitive diagnosis either
is made, or they stop seeking explanations. For example, in one
AANEM Course
clinical trial of botulinum toxin (BTX) injections, the average
duration of symptoms prior to inclusion in the trial was 39
months, ranging from 16 months to 7 years.22 During this time,
patients may undergo lengthy trials of misdirected and fruitless
therapy, injections, and even surgery. Consequently, it behoves
physicians to (1) determine if, other than in very rare instances,
piriformis-induced nerve entrapment truly is a cause of sciaticalike symptoms and, if so, how commonly; (2) name and/or define
PS in such a way that it can be uniformly accepted, recognized
and appropriately treated, as well as studied in clinical trials that
generate results that are comparable between studies and can
be generalized to a clearly defined population of patients; (3)
identify sensitive and specific markers of disease, potentially a
gold standard diagnostic test, but more likely a set of validated
and universally applicable classification criteria; and (4) identify
effective treatments through appropriate random, controlled and
blinded clinical trials.
CONTROVERSY BEHIND PS
The controversy that surrounds PS does not just exist within
the scientific community; it also affects daily clinical practice,
as evidenced by widely discrepant estimates of its incidence in
various settings. Further evidence of the effect of this controversy
at the healthcare delivery level stems from a survey that was conducted by Silver and Leadbetter.10 Questionnaires were mailed
to a random sample of 75 United States physiatrists, and of that
sample, 29 responded (39%). Of these, only 72% were confident
that PS was a legitimate diagnosis; moreover, reasonably similar
percentages of physiatrists felt that the disorder was over diagnosed (55%) and under diagnosed (38%). On the other hand,
the major controversies belying PS do not appear to be centered
on whether or not these patients have true pain, but rather on
what the source of that pain is and how it is best identified and
treated.
Recent debate on the pros and cons of PS as a legitimate entity
has included opinion papers and letters drafted by several different authors, addressing a host of different issues.4,5,7-9,23,24 Even
the most adamant critics seem to accept the possibility that an
occasional patient experiences piriformis induced sciatic nerve
root entrapment,7-9 as in the case of a 40-year-old patient whose
MRI scan demonstrated an anomalous sacral attachment of the
piriformis muscle, whose piriformis was enlarged and compressing
the S2 nerve root upon surgical exploration, and whose symptoms
resolved immediately post operatively, leaving the patient pain free
through at least 5 years of follow up.25 Similarly, Sayson and associates26 described a patient with sciatica who responded poorly
to epidural steroid injection and only transiently to piriformis
injection; but in whom subsequent surgical exploration of the
sciatic nerve revealed a constricting band of fascia around the nerve,
and the piriformis muscle lying anterior to the nerve. Arguments
against the syndrome being more than just a rarity largely are
defined in Table 1.
AANEM Course
The Hip and the Neuromuscular Physician From EDX to Coxa Saltans
Table 1 Arguments against piriformis syndrome
(1) A lack of convincing evidence that the piriformis is anything more
than a rare to very rare cause of sciatic nerve entrapment8;
(2) The evidence that exists suggesting otherwise is based upon flawed
studies and/or reasoning8,9;
(3) Studies on cadavers as well as patients who have undergone surgery
for other reasons have demonstrated that piriformis induced sciatic nerve
compression is either uncommon or highly non specific 1,16;
(4) Electrophysiologic and imaging studies suggesting pathology
generally are nonspecific and, consequently, potentially misleading9;
(5) Numerous other causes of the symptoms are at least as likely5,7-9,27;
(6) The label “piriformis syndrome” is misleading and should be
changed to a more general term that does not implicate any particular
anatomic structure5,7,8; and
(7) Injections and surgical manipulations of the piriformis muscle
are being performed too commonly and usually without adequate
justification.
On the flip side, arguments for the syndrome being more than just
a rarity largely are defined in Table 2.
Table 2 Arguments for Piriformis Syndrome
(1) Piriformis syndrome is a reasonable explanation for a significant
proportion of the patients with sciatic like symptoms whose pain is not
explained by other, more accepted diagnoses4,23;
The sciatic nerve generally lies on the ventral aspect of the piriformis muscle, but considerable variation exists, with the S2 and
S3 nerve roots especially documented to pass through the muscle
in some symptomatic patients,48 and in a sizeable percentage of
asymptomatic live controls33 and cadavers.31,49 Due to its location
within the sciatic notch and relative to the sacral nerve roots, symptoms classically include buttock pain with radiation into the ipsilateral thigh and leg.50 This pain often is exacerbated by prolonged
sitting, walking, walking up inclines, and other movements.50
Symptoms other than skeletal pain include paresthesias and motor
weakness, as well as dyspareunia in women, abdominal, pelvic and
inguinal pain, and pain with bowel movements.2 Generally, they
do not include urinary or bowel dysfunction, other than a possible
increase in pain while passing stool.
On physical examination, patients are typically tender in the sciatic
notch area and are focally tender on the ipsilateral side on rectal
examination. In addition, a variety of provocative tests have been
developed to stretch the piriformis, thereby increasing its compressive effect upon whatever nerve roots are being entrapped. The first
such test to be ascribed specifically to PS is the Lasègue test, mentioned in 1947, when Robinson28 proposed a set of six criteria for
what he labeled pyriformis syndrome. These criteria, which were
based entirely upon his clinical experience, rather than any formal
study, and are listed in Table 3.
Table 3 Criteria for PS
(2) The anatomic location of the piriformis muscle corresponds
precisely with the area of focal tenderness observed in these
patients4,23,28;
(1) A history of buttock trauma;
(3) The course of the muscle relative to the sacral nerve roots explains
the results of a host of provocative tests that are often positive in these
patients3,23,29-33;
(3) Acute exacerbation of the pain with lifting, with moderate relief
provided by traction;
(4) A variety of imaging and neurodiagnostic tests now confirm the
presence of piriformis pathology4,23,25,29,30,32,34-36; and
(5) A positive Lasègue sign; and
(5) Numerous patients have responded well to either focal
injections12,16-18,22,30,37-44 or surgical manipulation45,46 of the piriformis, thereby
implicating it as the cause of symptoms in those cases.
Management of PS patients, including the clinical history and examination, and the use of diagnostic testing including electrophysiology, and treatment will be further discussed and these arguments
and counter arguments will come into play once again.
CLINICAL FINDINGS
Understanding the manifestations of piriformis-induced entrapment requires some familiarity with the anatomy of the muscle
and surrounding structures. The piriformis muscle originates on
the ventrolateral aspect of the sacrum at levels S2 through S4, and
inserts into the piriform fossa of the greater trochanter.47 It is innervated by a nerve that is of S1 and S2 segmental origin. Its main
functions are to externally rotate the thigh, and to abduct the thigh
when the hip is flexed,2,15,47 though it also can be a weak hip flexor.
11
(2) Pain in the region of the sacroiliac joint that causes difficulty walking;
(4) A palpable, sausage shaped mass over the piriformis muscle;
(6) Possible gluteal atrophy.
As stated earlier, the various symptoms attributed to PS are problematic in that they all are nonspecific and are commonly reported
in patients with other causes of lower back, buttock, and sciatic
like pain. The same can be said of various physical findings that
have been reported in these patients (Table 4). Tenderness in the
buttock, even into the area of the sciatic notch, can be referred
from the lumbosacral spine or sacroiliac joint, or can be the result
of irritation of several different muscles within the pelvis. Rectal
tenderness can be caused by something as simple and unrelated
as compression of an internal hemorrhoid. Pain with external
rotation of the hip is a common manifestation of early arthritis.
All the various named signs (Lasègue, Freiburg, Pace, and Beatty)
are nonspecific, not particularly sensitive, and are often absent in
patients otherwise diagnosed with PS.8,9 Even during attempts by
Fishman and associates30 to validate criteria for PS, many patients
who responded to focal injections and, hence, were ultimately
diagnosed with PS, exhibited only two of the three criteria used
by the investigators to screen for the diagnosis. Broadhurst and as-
12
The Diagnosis and Management of Piriformis Syndrome
sociates51 attempted to correlate various symptoms and signs of PS
with piriformis muscle morphology, as determined by ultrasound
(US), and found that the odds of abnormal morphology was as
high as 10.8 for the symptom of buttock pain walking up inclines,
with a sensitivity of 95%; however, five of every eight patients with
normal morphology also reported this symptom, for a specificity of
just 38%. The odds ratios, sensitivity and specificity for pain with
needling of the muscle, pain referred to the thigh, and pain with
resisted abduction were 10.8, 95%, and 25%; 5.3, 80% and 57%;
and 2.6, 95% and 13%, respectively.
Consequently, it appears that symptoms and physical signs alone
are inadequate in establishing the diagnosis of PS as a distinct clinical entity and in establishing the diagnosis in the individual patient.
Both require the addition of diagnostic testing and/or a response to
disease specific treatments.
Table 4 Signs of Piriformis Syndrome
(1) Deep focal tenderness over the sciatic notch2,27,45,52
(2) Ipsilateral rectal tenderness (patient often exclaims that for the first
time, someone has found his/her pain)53
(3) Palpable mass in the ipsilateral buttock2,28
(4) Antalgic gait2
(5) Traction of the affected limb reduces pain2,28
(6) Ipsilateral lower extremity
weakness2,16,24,54,55
(7) Positive Freiberg sign (pain with passive internal rotation of the
hip)2,56
(8) Positive Lasègue sign (localized pain over the sciatic notch,
especially when the hip is flexed and knee extended)2,28
(9) Positive Pace sign (pain and weakness on resisted abduction
external rotation of the hip)2,24,45,53
(10)Positive FAIR sign (pain reproduced when the hip is flexed,
adducted and internally rotated)
(11)Positive piriformis sign (patient externally rotates the affected hip
when lying supine)2,52
(12)Positive Beatty test (abduction of affected lower extremity when
lying on the contralateral side recreates sciatic symptoms)2,57
(13)Limited internal rotation of the affected hip2
(14)Gluteal trophy in chronic cases2,28 – question disuse atrophy
(15)Persistent sacral rotation toward the contralateral side with
compensatory lumbar rotation2
FAIR = hip flexed, adducted, and internally rotated
DIAGNOSTIC IMAGING
Although there is relatively little debate as to their use in ruling
out certain other causes of sciatic pain like radiculopathy, there is
controversy in determining the value of using a variety of imaging
modalities to document or confirm the presence of piriformis
related nerve root entrapment.
In terms of diagnostic (as opposed to therapeutic guidance)
imaging, investigators have primarily reported on the use of MRI
AANEM Course
and MRN, though a single report on nuclear scintigraphy in a
single patient described uptake in the distribution of the piriformis
muscle on the symptomatic side after the administration of 20 mCi
of Tc-99m methylene diphosphonate.58 Computed tomography
(CT) scans were not found to be helpful by Benson and Schutzer
in their study of post-traumatic PS,45 but both contrast CT and
MRI were helpful in identifying an enlarged piriformis muscle
in a 27-year-old woman with several classic symptoms and signs
that included severe rectal and pelvic tenderness, as well as positive
Freiberg, Pace, and Lasègue signs; injection of 10ml of 1% lidocaine and 10mg of triamcinolone acetonide produced immediate
and complete relief.59
The largest study assessing the potential utility of MRI in diagnosing PS was an imaging survey to assess piriformis muscle appearance and its relationship to sacral nerve roots in 100 patients who
did not have PS.33 Because both sides were assessed, 200 piriformis
muscles and sciatic nerves were viewed. Considerable variability
was found in the size of the muscles and the nerve root courses.
Almost one in five subjects had greater than 3mm of asymmetry in
the size of their piriformis muscles, with a maximum of 8mm; and
the percentage of nerve roots that traversed the muscle was < 1%
for S1, but 95% and 97% for S2 and S3, respectively. The S4 root
was located below the muscle in 95% of cases.
Reports supporting the diagnostic use of standard MRI in patients
diagnosed with PS are limited to the single patient described
above,59 who underwent CT and MRI testing, as well as three
further single case reports, involving a 40-year-old man,25 and, 30-35
and 27-year-old women59. In the first single case,58 MRI revealed an
anomalous sacral attachment, with accessory muscle fibers crossing
over the S2 nerve root; surgical exploration revealed S2 compression, which was surgically released via resection of approximately
1 cm of the piriformis tendon near its insertion into the piriformis
fossa, resulting in total resolution of pain through 5 years of follow
up. In the second case,35 MRI revealed asymmetrical enlargement
of the piriformis on the symptomatic side, accompanied by anterior
displacement of the sciatic nerve. Interestingly, plain radiographs
revealed thoracolumbar rotoscoliosis, which was also felt to contribute to the patient’s pain and was a major focus of physiotherapy;
ultimately, this woman experienced resolution of her symptoms
after 3 months of conservative treatment. The final patient59 had
evidence of ipsilateral piriformis muscle enlargement documented
both by CT and MRI. In a fourth single case report,26 MRI was
normal, even though surgical exploration of the sciatic nerve revealed a constricting band of fascia around the nerve, as well as the
piriformis muscle lying anterior to the nerve. This absence of MRI
findings is consistent with a lack of findings reported by Barton50 in
a series of four patients, despite piriformis-related pathology identified on surgical exploration in some of them.
MRN is a relatively new technique that has been specifically developed to enhance the imaging of nerves.3,34,60 Filler and associates34
have defined it as “…tissue-selective imaging directed at identifying
and evaluating characteristics of nerve morphology: internal fascicular pattern, longitudinal variations in signal intensity and calibre,
and connections and relations to other nerves or plexuses.” Its
ability to identify peripheral nerve pathology has been documented
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
at numerous body sites, including neck, back, pelvis, and extremities.34 The only study on the usefulness of MRN in PS has been the
Filler and associates3 study of 239 patients with sciatica-like pain in
whom standard diagnostics and therapy failed to yield any satisfactory recovery; as stated earlier, 67% of this number were deemed to
have piriformis-induced sciatic nerve root entrapment, based upon
the appearance of diagnostic images, the patient’s response to guided
injections, or both. The authors concluded not only that MRN was
a useful tool for establishing a diagnosis and aiding in the monitoring of treatment effects in PS, but that the results validate PS as a
true clinical entity. Tiele disagrees with both conclusions,9 arguing
that Filler’s study was flawed on several counts, including the lack
of adequate information to rule out other diagnoses, a potential for
contamination from other treatments, and problems with the issues
of magic angle effect61 and echo times. In rebuttal, Filler4 points
out that magic angle effects only occur when echo times less than
40 ms are used, whereas MRN studies generally utilize echo times
between 70 and 100 ms; and that the immediate and dramatic
response to targeted injections of patients ascribed a diagnosis of
piriformis in the noted study makes it extremely unlikely that other
diagnoses or treatments exerted a substantial effect. Finally, in one
subsequent study in which all other pathologies that might explain
sciatic pain were ruled out prior to patient enrollment, by MRI
and electrophysiologic studies, guided injections of BTX-B again
yielded fair to excellent results in 19 of 20 patients.18
DIAGNOSTIC ELECTROPHYSIOLOGIC STUDIES
As opposed to the relative dearth of evidence supporting the diagnostic use of most imaging modalities in PS, there is support for
electrophysiologic testing. The main advantage of EMG testing is
its ability to assist with the differential diagnosis. Perhaps the first to
report using EMG to diagnose piriformis was Kipervas, in 1976.62
In the English language literature, Synek36 was the first to write
about using electrophysiologic studies for this purpose, after reporting in 1987 about the detection of short-latency somatosensory
evoked potentials in four patients, one of whom had PS; the other
three patients had spondylopathic cervical radiculopathy, meralgia
paraesthetica, and allodynia secondary to a femoral nerve injury.
Benson and Schutzer45 noted abnormal EMG findings in the distribution of the inferior gluteal nerve, and the tibial and peroneal
divisions of the sciatic nerve in 6 of 8 patients who later went on
to have adhesions identified between the piriformis muscle, sciatic
nerve, and the roof of the greater sciatic notch, and suggested that
these findings demonstrated extra pelvic compression of the sciatic
nerve. No specific needle EMG or further information regarding
their EMG findings was provided in the paper.
In 1990, Chang and Lien reported on their comparison of EMG
versus spinal nerve stimulation in patients with L5 or S1 radiculopathies. They found that in 17 patients with objective clinical
evidence of radiculopathy, including a neurological deficit, EMG
was abnormal in 10 (59%), whereas amplitude and area differences
on spinal nerve stimulation were noted in 16 (94%) and 12 (71%),
respectively.63 More recently, Chang and associates64 measured
motor nerve conduction velocity, using magnetic stimulation in
the sciatic nerve in patients who met all three criteria for diag-
13
nosis proposed by Fisher (sciatica or gluteal pain in the flexed,
adducted, and internally rotated [FAIR] position; focal tenderness
in the sciatic notch; and a positive Lasègue sign), and detected significant slowing of motor nerve conduction velocity in the gluteal
component of the L5 root (L5 root to gluteal fold) versus healthy
control subjects. There was no difference in compound muscle
action potential amplitude recording from the tibialias anterior or
gastrocnemius muscles.
Specifically looking at the use of electrodiagnostic (EDX) testing
in patients with PS during a positive provocative test, and using
an epidural electrode positioned at S3-4, Nakamura and associates32 recorded action potentials from the cauda equina in two
patients with PS symptoms, with the hip and knee fully extended,
the hip flexed, and then the hip both flexed and internally rotated
to stretch the piriformis muscle and increase its compressive effect
upon the sciatic nerve. They detected roughly a 30% decrease in
amplitude in the piriformis stretch position on the symptomatic
side, versus just a 10% decrease in the other two hip positions or
on the contralateral side. Similarly, Fishman and associates29 has
documented significant prolongation of both the posterior tibial
and peroneal H reflexes in symptomatic patients whose hip is in the
FAIR position, and noted that more than a three standard deviation
increase was 83% specific for the condition, when clinical criteria
and response to treatment were used to define it. Interestingly, the
results of these last two studies concur with the results of a study on
10 cadavers,31 in which the FAIR or piriformis "stretch" position
was found to result in the infra piriformis foramen becoming narrower, the sciatic nerve closer to the ischial spine of the hip, and the
angle between the sciatic nerve and the transverse plane increased.
However, as Tiel9 and Stewart8 have both pointed out, there is an
inherent dilemma of tautology using treatment response as the standard for diagnosis, given the absence of any way to reliably confirm
the diagnosis of PS; in essence, it creates a self-fulfilling and highly
convenient prophesy: patients who get better had the condition we
thought they had. On the other hand, this is not so different than
the situation that exists for any disorder for which there is no “gold
standard” for diagnosis, like systemic lupus erythematosus (SLE),
for which a set of diagnostic criteria are required. Moreover, as
Filler4 argues, the dramatic and prolonged response seen in the majority of such patients treated by guided injection, who had failed
all prior attempts at treatment, strongly implicates the piriformis as
being involved in the mechanism of pain in some way.
TREATMENT OF PS
The absence of a widely accepted operative definition of PS, and
the significant controversy over how common or rare the condition
is makes it even more difficult than usual to compare different
treatment modalities in its management. Traditional wisdom is that
many, but certainly not all patients with PS respond to conservative
management that largely consists of anti inflammatory medications, like non steroidal anti inflammatory drugs (NSAIDs), and
physiotherapy. However, the percentage of patients that require
more “aggressive” treatment, like injections, is difficult to ascertain,
because some authors include injections under the umbrella of
14
Management
The Diagnosis andPractice
Management
of Piriformis Syndrome
conservative management while others do not. In addition, the
exact nature of the physiotherapy to which patients might respond
is elusive, because of the muscle’s position deep within the buttocks, where it can be neither easily palpated nor manipulated. It is
beyond the scope of this paper to describe the various conservative
strategies used. Suffice it to say that stretching the piriformis muscle
is a primary objective of the therapy, and only two papers describe
such therapy in any detail, one written by a physiotherapist65 and
the other by an osteopathic physician(2); neither author referenced
any actual data to support their conclusions regarding the effectiveness of physiotherapy.
A common adjunct to NSAIDs and physiotherapy is a local injection, which can consist of a local anaesthetic alone, steroid alone,
both, or more recently, BTX. In one study (30), the combination
of physiotherapy and a local injection (1.5mL 2% lidocaine +
20mg triamcinolone acetonide in 0.5mL) resulted in 79% of 353
patients who had met at least two of three criteria for PS experiencing at least a 50% reduction in pain lasting over an average of
16 months follow up. Others have reported success with various
injections, but the doses and methods of administration have
varied. A few have attempted blind injections30,41. Others have
performed injections guided by imaging alone, using modalities
like CT,17 MRN,3 US,14,43,66 and fluoroscopy.16,37,44 In the majority
of studies, however, injections have been guided by EMG,18,30,38,39
nerve stimulation,14,16,37,38 or a combination of modalities, invariably incorporating imaging plus EMG, nerve stimulation, or
both.12,14,22,37,40 Unfortunately, the only report comparing different
modalities to guide injections was one designed to compare the accuracy of US versus fluoroscopic guidance to inject 20 piriformis
muscles in 10 cadavers.67 In this study, two different-colored latex
dyes were used; US was found to be superior, with subsequent
dissection revealing the injected dye in 19 of 20 muscles injected
via US, but only 6 of 20 muscles injected via fluoroscopy. To date,
no one has compared injections guided by imaging alone, versus
nerve studies alone, versus both, but such a study certainly seems
warranted. Although the combination of fluoroscopy plus EMG or
nerve stimulation has seemed most popular,3,22,37,38,40 the combination of US plus nerve stimulation may be particularly attractive for
several reasons that include the ability to perform the procedure
using two relatively portable and low cost devices, in the absence of
any radiographic exposure.14 However, to date, this latter combination remains untested.
Besides the usual questions related to the efficacy and safety of
treatment, questions have arisen with respect to the use of local
anaesthetics and injected steroids include: Why does a local anaesthetic produce anything more than a very transient benefit? What
inflammation is the steroid treating? And how can anyone be sure
that it is PS that is being treated, versus nerve irritation caused by
some other muscle or other structure within the sciatic notch? With
respect to the latter, North and associates68 studied the sensitivity
and specificity of several different local anaesthetic blocks in 33
patients with sciatica that had been attributed to spinal disease, and
found both sensitivity and specificity to be less than 40% in almost
all instances. However, their injections were not guided. Several
subsequent studies specifically addressing PS management have
AANEM Course
Course
AANEM
examined the use of guided injections, and the results have been
generally encouraging.
In terms of prolonged pain relief, some of the most encouraging results are from the use of BTX, usually type A. BTX-A is a
150_kD single chain polypeptide that is produced by Clostridium
botulinum.44 Although its existence has been recognized for centuries, it has only been since the late 1970s that it has been considered for therapeutic purposes, and only since 1989 that the United
States Food and Drug Administration has approved its clinical use.
Its approved use was initially restricted to the treatment of strabismus, blepharo spasm, and hemifacial spasm. Over the past decade,
however, its use has grown exponentially, and it is now being used
for a much wider spectrum of conditions, including chronic pain
disorders (i.e., cervical dystonia, myofascial pain, chronic low back
pain), and focal tendonopathies (i.e., tennis elbow, and PS).69 In
chronic pain conditions, BTX presumably works by breaking the
muscle spasm or subsequently the pain cycle, affording the patient
a window of opportunity for traditional conservative measures to
have a greater beneficial impact;69 but several studies suggest that a
direct antinociceptive effect distinct from any reduction in muscle
spasm may be at play.70 Again, the major benefit of BTX compared
with standard therapies appears to be the prolonged duration of the
response.12,71 In one study, CT-guided injections of BTX-A versus
methylprednisolone were compared in 40 patients (20 per treatment arm). Both treatments resulted in a decrease in pain baseline
at 30 days follow up; the beneficial effect of the steroid, but not
the BTX-A, was lost by 60 days, a between-drug difference that was
statistically significant. Other comparative studies of BTX versus
control vehicle, using both parallel and crossover group designs,
have also demonstrated a beneficial effect of both BTX-A17,22,37,38,72
and BTX-B.18,39 Therefore, there is some support for the use of
BTX in the treatment paradigm.
As a final measure, should all other treatment options fail, surgery
is sometimes used in the treatment of PS patients, often sectioning the muscle to reduce or eliminate its contact with the effected
sciatic nerve root(s).45,46,73 Debate rages as to the legitimacy and effectiveness of surgery on the piriformis muscle, spurred once again
by questions as to whether or not the piriformis muscle actually
is the source of symptoms. Critics site one case of failed surgical
decompression73 in a 44-year-old woman whose serial electrophysiological tests, plain radiographs, MRIs of the pelvis and lumbar
spine, and CT myelograms all were interpreted as normal; who
had failed to obtain any lasting relief from NSAIDs, physiotherapy,
and multiple caudal, piriformis, sciatic, and S1 nerve root blocks;
and who now was being treated chronically with sustained release
morphine and paroxetene. However, straight-leg raising and diagnostic maneuvers designed to detect PS, produced buttock pain
only. No mention was made of whether or not the patient had pain
elsewhere, had any evidence of a chronic generalized pain condition
like fibromyalgia, or any history of drug or alcohol dependency or
addiction. Consequently, the value of this case as disproving PS, or
of the value of surgical intervention must be considered zero.
Instead, the major concern for proponents of surgery must be the
relative lack of data supporting it, limited to two small published
studies. Benson and colleagues45 described their results of 15 opera-
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
tions in 14 patients (one with bilateral symptoms) with sciatica, who
had failed to respond to all other measures, and whose symptoms
had started following blunt trauma to their buttock. Eight of 14
patients underwent preoperative EMG, which revealed extra pelvic
compression of the sciatic nerve in 6. Details of the electrophysiological assessment were superficial. At the time of surgery, all had
adhesions between the piriformis muscle, sciatic nerve, and the roof
of the sciatic notch, which were resected. Eleven “excellent” and 4
“good” results were attained across the 15 procedures. Meanwhile,
Dezawa and associates46 reported their results performing arthroscopic release of the piriformis in eight limbs in six patients
who met at least five of the nine criteria the authors themselves
had established, and who had failed conservative treatment over 6
months. All eight procedures achieved “good results”, but further
details were not provided. Otherwise, the literature contains only
isolated reports of success, typically in patients who were among
larger series of patients receiving injections, and who had achieved
less than satisfactory long-term resolution of their pain.
CONCLUSIONS
PS faces controversy on almost all fronts. Can the piriformis muscle
entrap the sciatic nerve or its individual roots? There is convincing
evidence that this does occur on occasion, but how commonly
this transpires remains open to debate, largely because there are no
agreed upon and scientifically validated diagnostic or classification
criteria. As opposed to what some critics may require, it is not necessary to have a “gold standard” for diagnosis, which is also lacking
for many well-accepted clinical entities, like rheumatoid arthritis,
SLE, and even CTS. A set of clinical criteria that provide reasonable
assurance of accuracy is necessary, by means of achieving at least
80% sensitivity and specificity. To date, such criteria do not exist.
Controversy exists in which symptoms and signs are most characteristic, essentially because of their uniform nonspecificity; but
highly sensitive and specific single symptoms or signs, again, are
not necessary, so long as criteria exist that combine them and
achieve adequate specificity and sensitivity. The same is true of
imaging and EDX tests, though MRN has improved our ability to
visualize nerves in live patients; and EDX tests that demonstrate
ipsilateral slowing of nerve transmission during physical maneuvers
that are presumed to increase piriformis pressure upon the nerve,
like the FAIR test, certainly support the diagnosis, both generically
and in the individual patient.
As for treatment, some level of controversy will always exist regarding the effectiveness of any treatment that cannot be administered in
a totally double-blinded way, as with many facets of physiotherapy
and various surgical procedures. However, injections can generally
be blinded; and, to date, controlled. Double-blinded studies have
shown that active injections are better than shams in the treatment
of these patients. Guided administration of these injections has
helped investigators to see what they are injecting, and these studies
demonstrate superiority of active versus sham treatment. Moreover,
though it remains possible that local anesthetics delivered into the
sciatic notch might alter pain even if that pain originates further
upstream, it is more difficult to imagine how the same could be said
15
of a targeted and guided injection of BTX. Therefore, future investigators should use guided injections of BTX into the piriformis
muscle as a “gold standard” proxy while generating and testing
diagnostic criteria for this condition, so that reasonable assurances
as to the diagnosis can be achieved in the individual patient prior
to this expensive and somewhat invasive procedure.
Finally, from the perspective of the EDX physician, clearly there is
a role for EMG, nerve conduction studies, and nerve stimulation in
the diagnosis and management of this condition, though the specifics and magnitude of that role warrants further testing within the
confines of formal comparative clinical trials. Presently, it appears
that the most important aspect of EDX testing is in ruling out more
common conditions and evaluating the differential diagnosis (e.g.,
peroneal entrapment at the fibular neck, an L 5 radiculopathy, or
a sciatic nerve palsy).
Reference
1. Windisch G, Braun EM, Anderhuber F. Piriformis muscle: clinical
anatomy and consideration of the piriformis syndrome. Surg Radiol
Anat 2007 Feb;29(1):37-45.
2. Boyajian-O'Neill LA, McClain RL, Coleman MK, Thomas PP.
Diagnosis and management of piriformis syndrome: an osteopathic
approach. J Am Osteopath Assoc 2008 Nov;108(11):657-64.
3. Filler AG, Haynes J, Jordan SE, Prager J, Villablanca JP, Farahani K,
et al. Sciatica of nondisc origin and piriformis syndrome: diagnosis
by magnetic resonance neurography and interventional magnetic
resonance imaging with outcome study of resulting treatment. J
Neurosurg Spine 2005 Feb;2(2):99-115.
4. Filler AG. Piriformis and related entrapment syndromes: diagnosis &
management. Neurosurg Clin N Am 2008 Oct;19(4):609-22, vii.
5. Read MT. The "piriformis syndrome"--myth or reality? Br J Sports
Med 2002 Feb;36(1):76.
6. Jroundi L, El QA, Chakir N, El Hassani MR, Jiddane M. [The piriformis syndrome: a rare cause of non discogenic sciatica. A case
report]. J Radiol 2003 Jun;84(6):715-7.
7. McCrory P. The "piriformis syndrome"--myth or reality? Br J Sports
Med 2001 Aug;35(4):209-10.
8. Stewart JD. The piriformis syndrome is overdiagnosed. Muscle
Nerve 2003 Nov;28(5):644-6.
9. Tiel RL. Piriformis and related entrapment syndromes: myth &
fallacy. Neurosurg Clin N Am 2008 Oct;19(4):623-7, vii.
10. Silver JK, Leadbetter WB. Piriformis syndrome: assessment of current
practice and literature review. Orthopedics 1998 Oct;21(10):1133-5.
11. Parziale JR, Hudgins TH, Fishman LM. The piriformis syndrome.
Am J Orthop 1996 Dec;25(12):819-23.
12. Porta M. A comparative trial of botulinum toxin type A and methylprednisolone for the treatment of myofascial pain syndrome and
pain from chronic muscle spasm. Pain 2000;85((1-2)):101-5.
13. Oxford English Dictionary, 2nd Edition. Oxford University Press;
1450.
14. Huerto AP, Yeo SN, Ho KY. Piriformis muscle injection using ultrasonography and motor stimulation--report of a technique. Pain
Physician 2007;10(5):687-90.
15. Papadopoulos EC, Khan SN. Piriformis syndrome and low back
pain: a new classification and review of the literature. Orthop Clin
North Am 2004 Jan;35(1):65-71.
16
Management
The Diagnosis andPractice
Management
of Piriformis Syndrome
16. Benzon HT, Katz JA, Benzon HA, Iqbal MS. Piriformis syndrome:
anatomic considerations, a new injection technique, and a review of
the literature. Anesthesiology 2003 Jun;98(6):1442-8.
17. Fanucci E, Masala S, Sodani G, Varrucciu V, Romagnoli A, Squillaci
E, et al. CT-guided injection of botulinic toxin for percutaneous
therapy of piriformis muscle syndrome with preliminary MRI results
about denervative process. Eur Radiol 2001;11(12):2543-8.
18. Lang AM. Botulinum toxin type B in piriformis syndrome. Am J
Phys Med Rehabil 2004 Mar;83(3):198-202.
19. Rodrigue T, Hardy RW. Diagnosis and treatment of piriformis syndrome. Neurosurg Clin N Am 2001 Apr;12(2):311-9.
20. Hallin RP. Sciatic pain and the piriformis muscle. Postgrad Med
1983;74(2):69-72.
21. Bernard TNJr, Kirkaldy-Willis WH. Recognizing specific characteristics of nonspecific low back pain. Clin Orthop Relat Res
1987;217:266-80.
22. Childers MK, Wilson DJ, Gnatz SM, Conway RR, Sherman AK.
Botulinum Toxin Type A Use in Piriformis Muscle Syndrome A
Pilot. Am J Phys Med Rehabil 2002;81(10):751-9.
23. Fishman LM, Schaefer MP. The piriformis syndrome is underdiagnosed. Muscle Nerve 2003 Nov;28(5):646-9.
24. Foster MR. Clinical trials for piriformis syndrome. Orthopedics 1999
Jun;22(6):561, 569.
25. Lee EY, Margherita AJ, Gierada DS, Narra VR. MRI of piriformis
syndrome. AJR Am J Roentgenol 2004 Jul;183(1):63-4.
26. Sayson SC, Ducey JP, Maybrey JB, Wesley RL, Vermilion D. Sciatic
entrapment neuropathy associated with an anomalous piriformis
muscle. Pain 1994 Oct;59(1):149-52.
27. McCrory P, Bell S. Nerve entrapment syndromes as a cause of pain
in the hip, groin and buttock. Sports Med 1999;27(4):261-74.
28. Robinson D. Pyriformis syndrome in relation to sciatic pain. Am J
Surg 1947;73:355-8.
29. Fishman LM, Zybert PA. Electrophysiologic evidence of piriformis
syndrome. Arch Phys Med Rehabil 1992 Apr;73(4):359-64.
30. Fishman LM, Dombi GW, Michaelsen C, Ringel S, Rozbruch J, Rosner
B, et al. Piriformis syndrome: diagnosis, treatment, and outcome--a
10-year study. Arch Phys Med Rehabil 2002 Mar;83(3):295-301.
31. Guvencer M, Akyer P, Iyem C, Tetik S, Naderi S. Anatomic considerations and the relationship between the piriformis muscle and the
sciatic nerve. Surg Radiol Anat 2008 Aug;30(6):467-74.
32. Nakamura H, Seki M, Konishi S, Yamano Y, Takaoka K. Piriformis
syndrome diagnosed by cauda equina action potentials: report of two
cases. Spine 2003 Jan 15;28(2):E37-E40.
33. Russell JM, Kransdorf MJ, Bancroft LW, Peterson JJ, Berquist TH,
Bridges MD. Magnetic resonance imaging of the sacral plexus and
piriformis muscles. Skeletal Radiol 2008 Aug;37(8):709-13.
34. Filler AG, Kliot M, Howe FA, Hayes CE, Saunders DE, Goodkin
R, et al. Application of magnetic resonance neurography in the
evaluation of patients with peripheral nerve pathology. J Neurosurg
1996;85(2):299-309.
35. Rossi P, Cardinali P, Serrao M, Parisi L, Bianco F, De BS. Magnetic
resonance imaging findings in piriformis syndrome: a case report.
Arch Phys Med Rehabil 2001 Apr;82(4):519-21.
36. Synek V. Short latency somatosensory evoked potentials in patients with painful dysaesthesias in peripheral nerve lesions. Pain
1987;29(1):49-58.
37. Betts A. Combined Fluoroscopic and Nerve Stimulator Technique for
Injection of the Piriformis Muscle. Pain Physician 2004;7:279-81.
38. Fishman LM, Anderson C, Rosner B. BOTOX and physical therapy
in the treatment of piriformis syndrome. Am J Phys Med Rehabil
2002 Dec;81(12):936-42.
39. Fishman LM, Konnoth C, Rozner B. Botulinum neurotoxin type B
and physical therapy in the treatment of piriformis syndrome: a dosefinding study. Am J Phys Med Rehabil 2004 Jan;83(1):42-50.
AANEM Course
Course
AANEM
40. Fishman SM, Caneris OA, Bandman TB, Audette JF, Borsook D.
Injection of the piriformis muscle by fluoroscopic and electromyographic guidance. Reg Anesth Pain Med 1998 Nov;23(6):554-9.
41. Mullin V, de RM. Caudal steroid injection for treatment of piriformis
syndrome. Anesth Analg 1990 Dec;71(6):705-7.
42. Mullin V, de RM, Quint D. Mechanism of action caudal steroids for
piriformis syndrome. Anesth Analg 1998 Mar;86(3):680.
43. Reus M, de Dios BJ, Vazquez V, Redondo MV, Alonso J. Piriformis
syndrome: a simple technique for US-guided infiltration of the perisciatic nerve. Preliminary results. Eur Radiol 2008 Mar;18(3):616-20.
44. Bennett JD, Miller TA, Richards RS. The use of Botox in interventional radiology. Tech Vasc Interv Radiol 2006 Mar;9(1):36-9.
45. Benson ER, Schutzer SF. Posttraumatic piriformis syndrome: diagnosis and results of operative treatment. J Bone Joint Surg Am 1999
Jul;81(7):941-9.
46. Dezawa A, Kusano S, Miki H. Arthroscopic release of the piriformis
muscle under local anesthesia for piriformis syndrome. Arthroscopy
2003 May;19(5):554-7.
47. Gray's Anatomy. The anatomical basis of clinical practice. Amsterdam:
Elsevier; 2005.
48. Pecina HI, Boric I, Smoljanovic T, Duvancic D, Pecina M. Surgical
evaluation of magnetic resonance imaging findings in pririformis
muscle syndrome. Skeletal Radiol 2008;37:1019-23.
49. Pecina M. Contribution to the etiological explanation of the piriformis syndrome. Acta Anat (Basel) 1979;105(2):181-7.
50. Barton PM. Piriformis syndrome: a rational approach to management. Pain 1991 Dec;47(3):345-52.
51. Broadhurst NA, Simmons DN, Bond MJ. Piriformis syndrome:
Correlation of muscle morphology with symptoms and signs. Arch
Phys Med Rehabil 2004 Dec;85(12):2036-9.
52. Foster MR. Piriformis syndrome. Orthopedics 2002 Aug;25(8):821-5.
53. Pace JB, Nagle D. Piriform syndrome. West J Med 1976;124(6):435-9.
54. Papadopoulos EC, Korres DS, Papachristou G, Efstathopoulos N.
Piriformis syndrome. Orthopedics 2004 Aug;27(8):797, 799.
55. Steiner C, Staubs C, Ganon M, Buhlinger C. Piriformis syndrome:
pathogenesis, diagnosis, and treatment. J Am Osteopath Assoc 1987
Apr;87(4):318-23.
56. Freiburg A, Vinkle T. Sciatica and the sacro-iliac joint. J Bone Joint
Surg 1934;16:126-36.
57. Beatty RA. The piriformis muscle syndrome: a simple diagnostic
maneuver. Neurosurgery 1994 Mar;34(3):512-4.
58. Karl RDJr, Yedinak MA, Hartshorne ME, Cawthon MA, Bauman
JM, Howard WH, et al. Scintigraphic appearance of the piriformis
muscle syndrome. Clin Nucl Med 1985;10(5):361-3.
59. Jankiewicz JJ, Hennrikus WL, Houkom JA. The appearance of the
piriformis muscle syndrome in computed tomography and magnetic
resonance imaging. A case report and review of the literature. Clin
Orthop Relat Res 1991 Jan;(262):205-9.
60. Filler AG, Maravilla KR, Tsuruda JS. MR neurography and muscle
MR imaging for image diagnosis of disorders affecting the peripheral
nerves and musculature. Neurol Clin 2004;22(3):643-82.
61. Bydder M, Rahal A, Fullerton GD, Bydder GM. The magic angle
effect: a source of artifact, determinant of image contrast, and technique for imaging. J Magn Reson Imaging 2007;25(2):290-300.
62. Kipervas IP, Ivanov LA, Urikh EA, Pakhomov SK. [Clinicoelectromyographic characteristics of piriform muscle syndromes].
Zh Nevropatol Psikhiatr Im S S Korsakova 1976 Sep;76(9):1289-92.
63. Chang C-W, Lien I-N. Spinal nerve stimulation in the diagnosis of lumbosacral radiculopathy. Am J Phys Med Rehabil 1990;69(6):318-22.
64. Chang CW, Shieh SF, Li CM, Wu WT, Chang KF. Measurement of
motor nerve conduction velocity of the sciatic nerve in patients with
piriformis syndrome: a magnetic stimulation study. Arch Phys Med
Rehabil 2006 Oct;87(10):1371-5.
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
65. Keskula DR, Tamburello M. Conservative Management of Piriformis
Syndrome. J Athl Train 1992;27(2):102-10.
66. Smith J, Hurdle MF, Locketz AJ, Wisniewski SJ. Ultrasound-guided
piriformis injection: technique description and verification. Arch
Phys Med Rehabil 2006;87(12):1664-7.
67. Finnoff JT, Hurdle MF, Smith J. Accuracy of ultrasound-guided
versus fluoroscopically guided contrast-controlled piriformis injections: a cadaveric study. J Ultrasound Med 2008;27(8):1157-63.
68. North RB, Kidd DH, Zahurak M, Piantadosi S. Specificity of diagnostic nerve blocks: a prospective, randomized study of sciatica due
to lumbosacral spine disease. Pain 1996;65(1):77-85.
69. Jeynes LC, Gauci CA. Evidence for the use of botulinum toxin in
the chronic pain setting--a review of the literature. Pain Pract 2008
Jul;8(4):269-76.
17
70. Monnier G, Tatu L, Fabrice M. New indications for botulinum toxin
in rheumatology. Joint Bone Spine 2006;73(667):671.
71. Raj PP. Botulinum toxin therapy in pain management. Anesthesiol
Clin North Amer 2003;21(4):715-31.
72. Yoon SJ, Ho J, Kang HY, Lee SH, Kim KI, Shin WG, et al. Low-dose
botulinum toxin type A for the treatment of refractory piriformis
syndrome. Pharmacotherapy 2007 May;27(5):657-65.
73. Spinner RJ, Thomas NM, Kline DG. Failure of surgical decompression for a presumed case of piriformis syndrome. Case report. J
Neurosurg 2001 Apr;94(4):652-4.
18
Practice Management
18
AANEM Course
Course
AANEM
AANEM Course
Practice Management
19
Lumbosacral Plexopathy: The Clinical
and Electrodiagnostic Spectrum
Timothy J. Doherty, MD, PhD
Associate Professor and Canada Research Chair in Neuromuscular Function in Health, Aging, and Disease
Departments of Clinical Neurological Sciences and Physical Medicine & Rehabilitation
Schulich School of Medicine and Dentistry
The University of Western Ontario
London, Ontario, Canada
INTRODUCTION
The clinical and electrodiagnostic (EDX) evaluations of lumbosacral (LS) plexopathies are often complex, even for the experienced clinician. LS plexus lesions are less common than brachial
plexus lesions and vary considerably in their presentations, depending on which components of the plexus are involved. The EDX assessment can be challenging because of difficulty performing motor
nerve conduction studies (NCSs) for many of the proximal nerves
and muscles involved (e.g., obturator to adductors), and an inability to obtain standard sensory nerve action potentials (SNAPs) for
many of the sensory branches involved. Like brachial plexopathies,
a LS plexus lesion should be considered when the clinical and EDX
features cannot be explained by a lesion of a single nerve root (e.g.,
radiculopathy) or a single peripheral nerve lesion (e.g., femoral or
sciatic mononeuropathy). This manuscript will review the anatomical, clinical, and EDX features of LS plexopathies.
femoral and lateral femoral cutaneous nerves. The lumbar plexus
communicates with the sacral plexus via the LS trunk (or cord).
The LS trunk is formed primarily by the L5 root, with a smaller
contribution from the L4 root. The LS trunk travels a relatively
long distance in close contact with the ala of the sacrum, which is
in close proximity to the sacroiliac joint. The LS trunk is protected
through much of its course by the psoas muscle, except at its terminal portion near the pelvic brim, where it is in close contact to
bone. There it is joined by the S1 nerve root to form the sciatic
nerve. The sacral plexus is formed by the anterior rami of spinal
nerves L4 – S3. The anterior division forms the tibial portion of the
sciatic nerve and gives rise to its peroneal component. The superior
(L4 – S1) and inferior (L5 – S2) gluteal nerves arise from the posterior division of the sacral plexus. The posterior cutaneous nerve
of the thigh arises from the anterior divisions of S1 – S3.
ANATOMICAL CONSIDERATIONS
CLINICAL FEATURES OF LS PLEXOPATHY
The LS plexus can be anatomically divided into the lumbar plexus
and sacral plexus (Figure 1). The lumbar plexus is comprised of
the anterior rami of the L1 – L4 roots and lies within the posterior
portion of the psoas muscle. The anterior rami of the L2 – L4 roots
divide into anterior and posterior divisions. The anterior divisions
form the obturator (L2 – L4), genitofemoral (L1, L2), iliohypogastric, and ilioinguinal (L1) nerves. The posterior division forms the
LS plexus disorders typically present with features of motor and
sensory deficits in the territories of multiple peripheral nerves
or multiple nerve root territories. Pain is often a predominant
feature.
Lumbar plexus disorders cause deficits in the distribution of the
iliohypogastric, genitofemoral, ilioinguinal, femoral, and obturator nerves. These may result in weakness of hip flexion, knee
20
Management
Lumbosacral Plexopathy:Practice
The Clinical
and Electrodiagnostic Spectrum
AANEM Course
Course
AANEM
EDX FEATURES OF LS PLEXOPATHY
EDX of LS plexus disorders can be challenging and perplexing for
even the experienced electromyographer (Table 1). In comparison to the brachial plexus, the anatomy of the LS plexus makes it
difficult to perform motor NCSs to some of the more proximal
muscles. Additionally, sensory NCSs are not feasible in many
cases (e.g., ilioinguinal nerve, posterior cutaneous nerve of the
thigh). Nonetheless, carefully planned and executed EDX studies
combined with thorough clinical assessment can usually localize
the lesion.
LS plexus lesions tend to be lumped into a single entity. However,
as outlined in the previous sections, it is usually more practical to
approach these problems as lumbar plexus or sacral plexus lesions.
Lumbar plexus problems must be distinguished from root lesions
of the L1 – L4 root, or isolated lesions of the femoral or obturator
nerves. Sacral plexus lesions must be distinguished from L5 or S1
root lesions, sciatic nerve injury, or mononeuropathies of the peroneal, and less commonly, tibial nerves.
Motor NCSs of the peroneal nerve to extensor digitorum brevis
and the anterolateral muscles, as well as tibial motor studies to the
gastrocnemius muscles and adductor hallucis are useful. These will
often show amplitude reduction with involvement of the lumbar
trunk and sacral plexus. Because foot drop is often a prominent
clinical feature of patients with possible sacral plexus lesions, it is
important to examine for the presence of conduction block across
the fibular head; this indicates a peroneal mononeuropahy.
Figure 1 Anatomy of the lumbosacral plexus.
(From WH Hollingshead. Anatomy for Surgeons. Vol 2. The Back and
Limbs. New York: Harper and Row, 1969.)
n = nerve
extension, and thigh adduction. Sensory deficits may occur over
the lower abdomen, inguinal region, the medial lower leg (saphenous nerve territory), and the anterior, lateral, and medial thigh,
The patellar reflex may be reduced or absent. Patients will complain
of the leg giving way when standing or walking (due to knee extensor weakness), walk with knee hyperextension, and have difficulty
getting in and out of bed or a car (due to hip flexor weakness).
Sacral plexus disorders produce deficits within the distribution of
the gluteal, tibial, and peroneal nerves. These result in weakness of
hip extension and abduction, knee flexors, ankle dorsi- and plantar
flexors, and the extensors and flexors of the toes. Sensory deficits
may occur over the posterior thigh, anterolateral and posterior
lower leg, and the plantar and dorsal aspects of the foot. The ankle
jerk may be reduced or absent. One important key to sacral plexus
lesions is weakness in the distribution of both the gluteal and sciatic
nerves. This is particularly so when both L5 and S1 innervated
muscles are involved, making a single root lesion less likely.
Femoral motor studies (we usually record over the vastus medialis) will reveal amplitude reduction for lumbar plexus disorders.
Demonstration of conduction block is often challenging in the
femoral nerve as it is difficult to perform supramaximal percutaneous stimulation proximal to the region of demyelination. Side-toside comparisons of compound muscle action potentials are very
useful for grading severity and prognosis.
Sensory NCSs for the superficial peroneal, sural, and saphenous
nerves are helpful as amplitude reduction indicates a lesion at
or distal to the dorsal root ganglion; these responses are usually
normal in the presence of root disease. This author and colleagues
routinely perform sensory studies of the lateral femoral cutaneous
nerve and use near nerve recording with a monopolar electrode.
These studies are most useful in diagnosing a lateral femoral nerve
lesion, or so called meralgia paresthetica. Again, side-to-side comparisons are routinely made.
Carefully planned needle electromyography (EMG) is often the
key to sorting out these disorders. In the case of axonal injuries,
it is typically necessary to delay needle studies for 10-14 days to
ensure that spontaneous activity will be present. For lumbar plexus
disorders, it is necessary to study the quadriceps, adductors, and
iliopsoas to rule out a femoral or obturator mononeuropathy.
Examination of the upper lumbar paraspinals is also useful, as
denervation indicates root disease. In sacral plexus disorders, it is
important to sample muscle in the peroneal and tibial components
of the sciatic nerve.
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
For patients presenting with foot drop, denervation in tibialis posterior or flexor digitorum, and short head of biceps femoris, indicate involvement outside the peroneal distribution. Denervation in
the gluteal muscles indicates involvement outside the sciatic nerve.
In some cases, it can be challenging to sort out an LS plexus lesion
from an L5 root lesion; both have prominent weakness in the L5
myotome. The presence of paraspinal denervation goes against a
plexus lesion, while reduction or absence of the superficial peroneal
sensory response indicates a more peripheral lesion. Caveats to
these guidelines apply to frequent involvement of the roots as well
in diabetic LS plexopathy.
COMPRESSIVE DISORDERS
Hemorrhage
Retroperitoneal hemorrhage is a common and sometimes overlooked cause of LS plexopathy. Large hematomas within the psoas
muscle lead to diffuse compression of the lumbar plexus with
involvement of both the femoral and obturator nerves. More
commonly, the intrapelvic component of the femoral nerve is compressed by smaller haematomas within the indistensible fascia of
the iliacis muscle.6 This leads to an isolated femoral lesion. These
usually occur in the setting of therapeutic anticoagulation, but can
also be seen with clotting disorders, leaking aneurysms, or trauma.
Patients typically present with acute onset of lower abdominal
and groin pain with referral into the thigh. Weaknesses of hip
flexion and knee extension as well as sensory deficits occur shortly
thereafter. Patients may adopt a posture of hip flexion and external rotation to reduce the severe pain. There is usually an associated drop in the hematocrit, and computed tomography (CT) of
the abdomen and pelvis will reveal the hematoma. Treatment is
normally conservative, with management of pain, reversal of anticoagulation, and transfusion. Outcomes are variable, with most
21
patients experiencing partial recovery; the extent depends on the
degree of axonal injury.
Neoplastic LS Plexopathy
Neoplastic LS plexopathies are relatively uncommon. They occur
as a result of direct invasion or external compression of the plexus
by a tumor.10,9 Pain, in association with weakness and sensory loss,
is the most typical presenting feature. The most common tumors
associated with LS plexopathy include: colorectal, lymphoma, genitourinary, breast and lung carcinoma, as well as a range of sarcomas.
Both CT and magnetic resonance imaging (MRI) are useful in
the evaluation of suspected cases.14 However, MRI may be more
useful in visualizing the neural structures.14 Treatment is specific to
the underlying malignancy. It often involves chemo- and radiation
therapy, with surgery in some cases. Pain control usually requires
narcotics. The addition of gabapentin, pregabalin, or tricyclics is
often helpful.
Pregancy and Post-partum
Compressive LS plexopathy can develop during late gestation, but
symptoms usually manifest during labor, with pain in the sciatic
distribution and the development of foot drop a few hours postpartum.1 Young, primagravidae women of short stature are most
susceptible.7 The usual mechanism of LS plexopathy is direct pressure of the fetal head against the plexus as it descends into the pelvis
during the second stage of labor. The peroneal component of the
sciatic nerve is most commonly affected, with weakness of ankle
dorsiflexion and eversion as well as sensory loss over the dorsum of
the foot. Peroneal motor studies reveal decreased amplitudes with
no block across the fibular head. The peroneal SNAP is absent or
decreased. Needle studies performed 10 to 14 days post-partum
will reveal denervation in peroneal innervated muscles as well as
Table 1 Muscles and sensory nerves to consider for electrodiagnostic evaluation of lumbosacral plexopathy
Spinal Root
Muscle
Motor Nerve
Lumbar plexus
L3/L4
Adductor longus
Obturator
Iliopsoas
Femoral
Saphenous
Vastus
Femoral
Saphenous
Sacral plexus
L5
Tensor Fascia
Superior Gluteal
Gluteus Medius
Superior Gluteal
Tibialis Anterior
Peroneal
Superficial Peroneal
Peroneus Longus
Peroneal
Superficial Peroneal
Tibialis Posterior
Tibial
Gluteus Maximus
Inferior Gluteal
Biceps Femoris (long)
Sciatic (tibial)
Sural
Biceps Femoris (short)
Sciatic (peroneal)
Sural
Gastrocnemius
Tibial
Sural
S1
Sensory Nerve
22
Management
Lumbosacral Plexopathy:Practice
The Clinical
and Electrodiagnostic Spectrum
short head of biceps femoris, with sparing of gluteal muscles and
paraspinals.7 Prognosis is usually good, with most patients gradually recovering over the course of 3 to 4 months.
AANEM Course
Course
AANEM
Trauma
In both DLRP and LRP, the cerebrospinal fluid will reveal elevated
protein. This provides evidence that the disease process is proximal
at the level of the spinal roots. Some patients will have elevated
erythrocyte sedimentation rate, positive rheumatoid factor, positive
antinuclear antibody test, or other indicators of immune mediated
disorders.5
Traumatic lesions of the LS plexus are far less common than
traumatic brachial plexopathy. The most typical causes are motor
vehicle accidents and severe falls that result in fractures of the pelvic
ring or sacrum.12 The entire LS plexus may be involved, but the
sacral plexus is more commonly affected with predominant involvement of the gluteal nerves and peroneal component of the sciatic
nerve. This relates to the proximity of these fibers to the sacrum
and sacroiliac joint.12 Clinical examination is often difficult in
these patients due to pain and orthopaedic injury. This makes EDX
assessment essential to characterize the extent of neurological involvement and provide prognosis. Treatment is usually conservative
unless there is the possibility of removing a compressive mass.
Some authors have proposed two subtypes of patients with
DLRP—those with EDX evidence of a more generalized diabetic
peripheral neuropathy, and those without it.13 However, a large
community-based cohort study of diabetics did not support this
hypothesis. Most patients who developed DLRP had not been diabetic long enough to develop a distal symmetric diabetic polyneuropathy.2 In addition, the occurrence of diabetic polyneuropathy
is highly associated with diabetic retinopathy and nephropathy, and
the majority of patients who developed DLRP had neither of those.
Thus, it is likely that those with DLPR and a polyneuropathy
simply reflect the end of the spectrum with more severe underlying
disease rather than a specific subgroup.5
Vascular Disease
Compression of the LS plexus can occur as a result of expansion of
iliac or hypogastric artery aneurysms. A slowly leaking abdominal
aortic aneurysm may lead to accumulation of a large retroperitoneal
hematoma that results in LS plexopathy.8 Back and leg pain with
the presence of a pulsatile mass in the abdomen are features of this
syndrome. CT scan of the abdomen and pelvis will confirm the
presence of the hematoma and aneurysm and allow for urgent surgical assessment and treatment.
NONCOMPRESSIVE DISORDERS
Diabetic LS Radiculoplexopathy
Diabetic LS radiculoplexopathy (DLRP), often referred to as diabetic amyotrophy or proximal diabetic neuropathy, is a relatively
common disorder usually seen in older men and women. It often
results in severe impairment and disability that affects 1-2% of
diabetics (typically, Type II).5 Nondiabetic LRP is a more recently
recognized condition,3 with clinical features and etiology that
appear very similar to DLRP.5 Both DLRP and LRP typically
present with severe, acute onset of lower-limb pain and weakness.
Frequently, these occur in concert with a large concomitant weight
loss. In many cases, affected patients have not been diabetic for a
long period of time.
Symptoms are usually unilateral and involve proximal lower limb
segments, such as the hip flexors and knee extensors. They may
spread more distally, and to the contralateral side over a few days.
While pain, often requiring narcotic analgesia, is the most severe
initial manifestation, weakness typically develops in the first few
days as well. Often, it has severe effects not only on the hip flexors
and knee extensors, but also the more distal muscles, including the
ankle plantar and dorsiflexors. Gait aids or wheelchairs are often
required for mobility.
The EDX features of DLRP and LRP are very similar. Needle
EMG reveals axonal injury or denervation in affected muscles in
multiple nerve territories, often with severe loss of recruitment implying substantive loss of axons. Motor and sensory action potential amplitudes are often reduced, with only mild slowing of nerve
conduction velocities. Paraspinal denervation is typically present in
both DLRP and LRP (29 of 30 patients in one series).3
Earlier studies suggested that the pathophsyiology of DLRP was
diabetes-induced vasculopathy. More recent investigation, however,
provides strong evidence that DLRP, and similarly, LRP, are caused
by an immune-mediated attack and microvasculitis of nerve.3,5
Given that both of these disorders are potentially immune mediated, early initiation of immunotherapy may limit the extent of
disease.
Some evidence from small open cohort studies suggests that immunotherapy (intravenous immunoglobulin, prednisone) may be of
benefit.11 One open-label trial of weekly intravenous infusions of
methlyprednisolone for 11 patients with LRP reported marked improvement in pain and weakness.4 However, there was no control
group, and LRP tends to improve in most untreated patients.
Without evidence from controlled trials, most clinicians reserve
immunotherapy for those most severely affected.
Given that axonal loss is the mechanism, the time course of recovery is typically many months.5 In the author’s experience, most
of these patients do well if provided with supportive treatment,
followed by appropriate physical therapy in the form of resistance
exercise and gait retraining.
REFERENCES
1. Alsever JD. Lumbosacral plexopathy after gynecologic surgery:
case report and review of the literature. Am J Obstet Gynecol
1996;174:1769-1777; discussion 1777-1768.
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
2. Dyck PJ, Kratz KM, Karnes JL, Litchy WJ, Klein R, Pach JM, Wilson
DM, O'Brien PC, Melton LJ, 3rd, Service FJ. The prevalence by
staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester
Diabetic Neuropathy Study. Neurology 1993;43:817-824.
3. Dyck PJ, Norell JE, Dyck PJ. Non-diabetic lumbosacral radiculoplexus neuropathy: natural history, outcome and comparison with
the diabetic variety. Brain 2001;124:1197-1207.
4. Dyck PJ, Norell JE, Dyck PJ. Methylprednisolone may improve lumbosacral radiculoplexus neuropathy. Can J Neurol Sci 2001;28:224227.
5. Dyck PJ, Windebank AJ. Diabetic and nondiabetic lumbosacral
radiculoplexus neuropathies: new insights into pathophysiology and
treatment. Muscle Nerve 2002;25:477-491.
6. Emery S, Ochoa J. Lumbar plexus neuropathy resulting from retroperitoneal hemorrhage. Muscle Nerve 1978;1:330-334.
7. Feasby TE, Burton SR, Hahn AF. Obstetrical lumbosacral plexus
injury. Muscle Nerve 1992;15:937-940.
23
8. Fletcher HS, Frankel J. Ruptured abdominal aneurysms presenting
with unilateral peripheral neuropathy. Surgery 1976;79:120-121.
9. Jaeckle KA, Young DF, Foley KM. The natural history of lumbosacral plexopathy in cancer. Neurology 1985;35:8-15.
10. Jaeckle KA. Nerve plexus metastases. Neurol Clin 1991;9:857-866.
11. Krendel DA, Costigan DA, Hopkins LC. Successful treatment of
neuropathies in patients with diabetes mellitus. Archives of neurology 1995;52:1053-1061.
12. Stoehr M. Traumatic and postoperative lesions of the lumbosacral
plexus. Arch Neurol 1978;35:757-760.
13. Subramony SH, Wilbourn AJ. Diabetic proximal neuropathy. Clinical
and electromyographic studies. J Neurol Sci 1982;53:293-304.
14. Taylor BV, Kimmel DW, Krecke KN, Cascino TL. Magnetic resonance imaging in cancer-related lumbosacral plexopathy. Mayo Clin
Proc 1997;72:823-829.
24
Practice Management
24
AANEM Course
Course
AANEM
AANEM Course
Practice Management
25
Neuromuscular Disease and the Hip:
An Orthopedic Perspective
Timothy P. Carey, MD, FRC(C)
Associate Professor
Department of Orthopedic Surgery
University of Western Ontario
London, Ontario, Canada
INTRODUCTION
By definition, neuromuscular disease involves an alteration in
the normal function of musculotendinous units, and can lead to
secondary effects on the skeletal system. The hip is commonly affected. Muscle imbalance due to disease can alter forces across the
joint, eventually leading to subluxation or dislocation, with subsequent development of painful degenerative arthritis. Management
of the hip in patients with neuromuscular disease involves awareness of potential pathology, preventative measures, appropriate
surveillance, and an array of reconstructive techniques to address
the varied and often challenging situations encountered.5
This manuscript brings an orthopedic perspective to neuromuscular
diseases of the hip. It covers clinical considerations, identifies conditions associated with increased and decreased muscle tone; and reviews
the assessment, treatment, and management of hip pathologies.
issues secondary to muscle imbalance around the hip. Degenerative
changes from aging are not directly related to neuromuscular condition, but their management can be complicated or compromised
by muscle imbalance.
The multiple neuromuscular conditions that can affect the hip can
be classified into two broad categories: those involving spasticity,
and those with a flaccid-type paralysis. In children, examples of
the former include cerebral palsy (CP) and brain and spinal cord
injury; in adults, they include cerebrovascular accidents, Parkinson’s
disease, and acquired brain and spinal cord injury. Conditions with
decreased muscle tone or flaccidity include myelomeningocele,
polyneuropathies, and myopathies. Poliomyelitis, although rare, is
a classic example.
OVERVIEW
Patients with a neuromuscular hip disease may need treatment for
two general reasons: the disease process (e.g., CP or myelomeningocele) has led to dysplasia of the hip, which in turn, has evolved into
degenerative arthritis; or the degenerative joint disease has developed
independently of the neurologic disease (e.g., Parkinson’s disease).
Knowing age of onset can help physicians anticipate clinical issues
they may encounter in patients with hip disorders. Neuromuscular
disease leading to muscle imbalance around a child’s developing
hip will alter normal forces transmitted to the changing skeleton,
and affect growth and development. Frequently, the result is progressive dysplasia and subluxation of the hip joint, culminating in
accelerated degenerative changes in the femoral head and distortion
of the acetabular anatomy.1 Adult onset conditions do not lead to
dysplastic changes, but can result in contractures and functional
In the child with hip dysplasia, efforts are typically directed at
restoring normal anatomy and normalizing soft tissue balance and
muscle forces early, before irreversible degenerative changes to the
articular cartilage develop. Treatment ranges from bracing and tone
reduction to soft tissue releases and femoral and pelvic osteotomies.
In the adult with degenerative changes, reconstructive options
include total joint arthroplasty in addition to osteotomies. Salvage
procedures can include joint excision, soft tissue releases, and arthrodesis, but all are associated with functional compromise.12
26
Practice
Management
Neuromuscular Disease
and the
Hip: An Orthopedic Perspective
EVALUATION
Assessment of hip pathology begins with a focused history and physical examination. Ambulatory patients require a visual gait analysis,
measurement of joint range of motion (ROM), contractures, and
evaluation of muscle strength and tone. Tools, such as the modified
Ashworth or Tardieu scores, are often used to quantify the degree of
spasticity.7,6 Imaging of the hip with plain anterior-posterior (AP) and
lateral radiographs is routine. AP pelvic views allow comparison with
the contra-lateral hip. Indications for additional imaging depend on
the clinical scenario. Additional information on bony dysplasia can
be obtained with special views, such as the false profile view of the acetabulum. Cross-sectional imaging with computed tomography scans
can help delineate more complex changes in the bony anatomy.27
3-D computed gait analysis has evolved significantly since its introduction as a research tool, and is now routinely performed at most
centers that deal with children who have CP. Advantages include a
multimodal approach with video recording, kinematic and kinetic
data, electromyography (EMG), and energy consumption measurements. Costs of the computer hardware and software have decreased
significantly, but a useful gait laboratory requires sufficient investment in physical resources and, most importantly, trained staff.13,22
CONDITIONS ASSOCIATED WITH INCREASED MUSCLE
TONE
AANEM Course
Course
AANEM
Deformities of the hip joint in patients with CP produce pain and
prevent ambulation. In the most profoundly affected, they can
also interfere with sitting ability and hygiene. The most common
pattern of muscle imbalance results in the hip adductors and flexors
overpowering the hip abductors and extensors, leading to progressive “uncovering” of the hip as measured by Reimer’s migration
index (Figure 1).29,17
This can eventually progress to frank dislocation of the hip joint.
Frequently, patterns of asymmetric tone lead to “windswept” posturing
of the lower limbs, with severe adduction of one hip with abduction of
the contralateral side. This is often associated with pelvic obliquity and
scoliosis. Early surgical treatment during childhood consists of muscle
releases to obtain balance and early femoral varus rotation or acetabular osteotomies for containment of the femoral head. Without early
surgical intervention, the uncovered femoral capital epiphysis becomes
deformed from the tremendous pressures generated by the overlying capsule and spastic abductor muscles, leading to painful arthritic
changes in adolescents and adults (Figures 2A and 2B).
In adults, the aim of treatment is to prevent contractures that lead
to hip subluxation or dislocation. With end-stage arthritis, treatment
goals are to eradicate pain in the affected arthritic joint and preserve
motion, if possible. Surgical options include resection/interposition
arthroplasty, arthrodesis, and total hip replacement arthroplasty.
Treatments
CP
The incidence of hip subluxation/dislocation in children with CP
ranges from 2-75%.34,31,32 Hip dislocation/subluxation with severe
or total body involvement is more common. Recent literature shows
a direct correlation between the incidence of hip displacement (subluxation to dislocation) and functional level measured by the Gross
Motor Function Classification System.34 Recommended hip surveillance schedules for children with CP are shown in Table 1.43
Proximal Femoral Resection Interposition Arthroplasty
Resection of the femoral head and neck is used to treat end-stage
arthritis in the dislocated hip. Interposition of local soft tissue
between the acetabulum and the remaining femur prevents impingement and subsequent pain. The procedure is reserved for
patients who are unable to walk and whose functional needs might
Table 1 Recommended hip surveillance schedules for children with cerebral palsy
Gross Motor Function Functional Description
Classification System
Recommended Surveillance
Level I
Walks without limitations
Clinical and x-ray 12-24 months; clinical at 3, 6 years
Level II
Walks with Limitations
Clinical and x-ray 12-24 months; repeat q12 months until MP stable; ages 5, 10
years
Level III
Walks using a Hand-Held Mobility Device
Clinical and x-ray 12-24 months;repeat q 6 months until MP stable; repeat q 12
months until age 7; if MP stable, review prepuberty, follow until skeletal maturity
Level IV
Self-Mobility with Limitations; May use
Powered Mobility
Clinical and x-ray 12-24 months; repeat q 6 months until MP stable; repeat q 12
months until age 7; if stable, review prepuberty, follow until skeletal maturity – if
scoliosis or pelvic obliquity present, follow q 6 months until skeletal maturity
Level V
Transported in a Manual Wheelchair
Clinical and x-ray 12-24 months;repeat q 6 months until age 7; if stable, review
q 12 months until skeletal maturity – if scoliosis or pelvic obliquity present,
follow q 6 months until skeletal maturity
MP = migration percentage
Wynter and colleagues. Consensus Statement on Hip Surveillance for Children with Cerebral Palsy: Australian Standards of Care. 2008
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
27
Figure 2A Management with botulinum toxin and hip abduction
orthosis.
Figure 1 Deformities of the hip joint in patients with cerebral palsy. The
most common pattern of muscle imbalance results in the hip adductors and
flexors overpowering the hip abductors and extensors, leading to progressive “uncovering” of the hip.
include improved hygiene and ease of positioning. Although good
results have been reported in terms of pain relief, significant complications are not uncommon. Heterotopic bone formation at the
surgical site is the most problematic effect.
In our series, only half of parents and caretakers would recommend
the procedure to others. Most centers have moved away from it.
Subtrochanteric valgus osteotomy (+/- femoral head resection)
is more commonly performed to relieve pain while maintaining
some stability of the leg. This limits shortening and decreases the
incidence of proximal migration and heterotopic bone formation
(Figure 3).4,42
Hip Arthrodesis
A subluxed hip makes arthrodesis is a poor choice for most patients
with severe painful arthritis. The majority are nonambulatory and have
significant musculoskeletal involvement. They often have scoliosis and
contralateral hip pathology. These conditions preclude any compensatory movements to accommodate the arthrodesed hip, as occurs in
otherwise healthy patients with unilateral hip disease. For these and
other reasons, the procedure is rarely performed in CP patients.12,30
Total Hip Arthroplasty
The clinical success of total hip arthroplasty for painful degenerative arthritis is well-documented in the literature. Many large series
include a small number of patients with neuromuscular issues, and
Figure 2B Progressive hip subluxation with development of erosive
changes superolaterally as seen in subsequent radiographs.
in general, good results can be expected even in this patient population. However, those with CP present many significant challenges
that need to be addressed.
Careful selection of appropriate candidates is of paramount importance. The concerns with total hip arthroplasty (THA) include
the patient's age (patients are usually young), the abnormal muscle
strength, the spasticity and contractures that are often present,
and poor compliance with postoperative regimens. Indications for
performing a total hip replacement in the spastic patient usually
include the following:
•
Hip pain refractory to medication;
•
Decreased function in standing, limited sitting, and dif
ficulty with perineal hygiene; and
•
The potential for standing or walking, transfer ability, or
upright sitting in a wheelchair.
28
Practice
Management
Neuromuscular Disease
and the
Hip: An Orthopedic Perspective
AANEM Course
Course
AANEM
authors recommend hemiarthroplasty or THA for treatment of hip
fractures.16
In 1988, Staeheli and colleagues investigated treatment of femoral
neck fractures (Garden III and IV) in patients with Parkinson’s
Disease. They reported high rates of complications at 6 months
(mostly urinary tract infections and pneumonias) and a high mortality rate (20%) after 50 hemiarthroplasties in 49 patients. Despite
these outcomes, functional results were good: 80% of the survivors
could walk. The authors attributed the positive result to rapid
postoperative mobilization of patients and the release of contracted
adductor muscles at the time of surgery.35
Figure 3 Severe degenerative changes secondary to paralytic hip dis-
location treated with femoral head and neck resection and subtrochanteric
osteotomy
Contraindications include active or previous hip joint infection,
poor general medical condition, insufficient bone stock, and
limited functional goals. The literature is relatively sparse, but
case series demonstrate acceptable results. Complications, such as
increased incidence of heterotopic ossification, dislocation, and
loosening are more frequent in patients with CP compared to those
without it.
Patients with CP require extensive preoperative planning. The
surgery is technically challenging, and modular or custom components are often required. Nonetheless, THA is a valuable option.
Incapacitating pain can be relieved and function improved in the
majority of patients. Longevity of the implant can also be expected
(>95% at 10 years).
Surgeons should pay attention to adductor spasticity that might need
an adductor tenotomy at the time of implantation. Modification
of surgical technique to favor stability over ROM, and the use of
constrained components may afford protection from instability. If
instability is a concern intraoperatively, postoperative support with a
hip abduction orthosis or even a hip spica cast may be needed.40,9,8
Parkinson’s Disease
The prevalence of Parkinson’s disease in the general population
older than 60 years of age is 1%. The incidence rate is 20.5 persons
per 100,000, with concomitant dementia 3 times more frequent
than in a control group.28,26 Current medical management effectively controls tremors, rigidity, and akinesia. Degenerative arthritis
of hips may occur through natural processes or after hip fractures.
The literature on the treatment of hip fractures in patients with
Parkinson’s disease is extensive. Regardless of fracture type, morbidity and mortality are high, with pneumonia the most frequent
complication. Patients treated with surgery have better functional
results and improved quality of life. However, standard internal
fixation techniques have a high failure rate. Due to the often
compromised medical status of this patient population, many
THA performed for fracture or degenerative arthritis has similar
results. Restoration of motion and pain relief is good, but the
complication rate is high compared to primary THA in an agematched non-Parkinson’s population. Significant increase in function and decrease in pain is seen at 1 year postoperatively, but
function continues to deteriorate with time. This is evidenced by
an increased use of gait aids and a decrease in walking distance. The
decline is mostly due to progression of the underlying Parkinson’s
disease, as neurological deterioration appears to parallel decreasing
functional scores.41
Although THA in Parkinson’s patients can be quite successful,
careful preoperative assessment is necessary to optimize surgical
results. In particular, screening for low-grade or asymptomatic infections is necessary to decrease the rate of this common complication. As with the CP patient, operative techniques often need to be
modified to deal with preexisting soft tissue contractures and bone
quality issues. Ultimately function is determined by progression of
the neurological disease.
Spasticity Due to Brain/Spinal Cord Injury
Hip joint contractures are a frequent complication in adult onset
spasticity caused by brain or upper spinal cord injury. Additionally,
heterotopic ossification around the hip can decrease ROM significantly in patients with brain injury. Prevention of fixed contractures is of paramount importance, and early management with an
aggressive physical therapy program of ROM exercises. Additional
modalities include tone reduction measures, such as botulinum
toxin or phenol injections.
Surgery plays a small role in these situations, but it offers another
option if limb position doesn’t improve over time, and contractures
interfere with sitting, hygiene, or achieving full rehabilitation potential. Generally, adduction and flexion contractures are the most
significant problems, and soft tissue releases can help to restore
ROM. Again, physical therapy is an integral part of the treatment
to maintain gains achieved with surgery. In select cases, postoperative bracing may be used.
In head injuries, significant heterotopic ossification will occasionally cause loss of joint ROM. This condition often responds well
to surgical excision and therapy, but careful timing is required, and
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
operations are not usually performed until there is evidence of a
maturing of the heterotopic bone.
THA is occasionally indicated in elderly patients with spasticity, usually secondary to stroke. As in the other cases, acceptable
results with respect to pain relief and mobility can be achieved.
Contractures can be dealt with at the time of surgery, and care must
be taken to ensure stability of the prosthesis.21 A higher incidence
of heterotopic ossification postoperatively has been reported in this
patient population; prophylactic treatment with low-dose radiation
is often recommended.18,15,39
CONDITIONS ASSOCIATED WITH DECREASED
MUSCLE TONE
Poliomyelitis
Poliomyelitis, although rarely seen in the modern era due to vaccination programs, is a classic example of pure flaccid paralysis. The
result of a viral infection targeting the anterior horn cells, permanent muscle paralysis occurs in varying anatomical distributions.
After the acute phase of the illness, treatment is aimed at addressing
the effects of the paralysis on the locomotor system.
Although the disease is static, there can be deterioration in aging
polio victims, a condition known as post-polio syndrome (PPS).
Primary criteria necessary for the diagnosis of PPS are a history of
paralytic poliomyelitis, partial or complete recovery of neurological
function followed by a period of stability (usually several decades),
persistent new muscle weakness or abnormal muscle fatigability,
and the exclusion of other causes of new symptoms.38
Orthopedic treatment of the manifestations of poliomyelitis is
rarely indicated. Physiotherapy and orthotic management are the
mainstays of treatment. However, patients with significant complications may require surgical intervention. Those who did not have
adequate medical attention during childhood can have residual
deformities. These will occasionally require tendon transfers and
boney reconstructive work. Surgery to address limb length discrepancies and joint arthrodeses for severely unstable joints are other
common procedures.
Specific deformities involving the hip occur when the flexors and
adductors overpower the weaker abductors and extensors, causing
hip subluxation, and occasionally, dislocation. In the young child,
coxa valga and excessive femoral anteversion contribute to the development of the hip instability. Significant hip abduction contracture can also uncover the hip on the “high” side. In this situation,
release of the abductors, as recommended by Eberle, may result in
reduction just by leveling the pelvis.14 When surgical treatment is
indicated for a subluxed hip, muscle transfers must be considered to
address the muscle imbalance at the root of the hip problem. Boney
reconstruction that doesn’t address the contractures and imbalance
is less likely to be successful.24,33
29
Myelomeningocele
The management of children with myelomeningocele has evolved
over the years. Early closure of the spinal defect, aggressive shunting
of hydrocephalus, and improved management of renal disease have
increased lifespan and quality of life.
Involvement of the lower extremities is classified on the basis of
the lowest functioning intact nerve root, or neurosegmental level.
These generally determine not only the patient's ability to walk,
but also the risk of developing hip instability. High-level involvement, such as thoracic or high lumbar levels, rarely results in hip
instability; these patients are wheelchair ambulators. Those with an
L2 level only walk with braces and crutches, and generally become
wheelchair-bound by their adolescent years.
L3 and L4 level children have good quadriceps and the potential
to be community ambulators, although they may require orthotics.
Their prognosis improves if hamstring activity is also present. The
incidence of hip subluxation is greatest in patients with lesions at
these levels because hip flexors and adductors remain intact and hip
extensors and abductors are absent or weak. Patients at an L5 or
sacral level rarely develop significant hip pathology.11,3
Surgical reduction of dislocated hips in myelomeningocele is unnecessary for patients with neurosegmental levels of L2 and higher.
Successful maintenance of the reduction is difficult, and the presence of a dislocation does not affect ambulation, pain, or quality of
life. Indications for surgery in the mid lumbar level child are still
controversial. The surgical reconstruction can be challenging; soft
tissue contractures and bony deformities need to be corrected; and
muscle transfers to address the absent abductor function are typically recommended.37
Still, recurrence of dislocation is not uncommon, and stiffness,
wound breakdown, and fractures have all been reported. Except
for a small improvement in energy expenditure in gait, studies in
operative and nonoperative cohorts fail to show a significant benefit
in quality of life.25,36
Hereditary Motor Sensory Neuropathies
Charcot-Marie-Tooth (CMT) disease is the most common form
of heritable peripheral neuropathy, with a prevalence estimated
at 1 in 2500. Two types are recognized. Type 1 (demyelinating),
the more common form, affects 60-80% of the CMT population;
Type 2 (axonal) affects 20-40% of patients. Clinically, the disease
is characterized by distal limb weakness that affects both extrinsic
and intrinsic musculature in the lower limbs. Sensory deficits and
areflexia are also seen.
The muscle weakness can gradually produce secondary deformities in the musculoskeletal system. The most common are cavovarus foot deformities. Often progressive, these are aggravated by
the weakness of ankle dorsiflexion due to extrinsic involvement.
Management includes use of foot orthotics and ankle foot orthoses
(AFOs). Surgical intervention is aimed at correcting deformities
and muscle imbalance by tendon transfers.19,20
30
Practice
Management
Neuromuscular Disease
and the
Hip: An Orthopedic Perspective
Hip dysplasia is a problem that occurs more frequently than previously thought. Kumar and colleagues first reported the association
between CMT and hip dysplasia in 1985. Since then, numerous
studies have addressed this issue.23 One series found a prevalence
rate of 8.1%, with radiographic abnormalities in a higher proportion of patients.10 Hips in children with CMT are normal at birth,
but progressive weakness from the neuropathy affects the hip extensors and abductors, leading to a more shallow acetabulum and a
valgus, anteverted femoral neck. Hip subluxation is subsequent to
these changes (Figure 4).
Figure 4 Hips in children with CMT are normal at birth, but progressive
weakness from the neuropathy affects the hip extensors and abductors, leading to a more shallow acetabulum and a valgus, anteverted
femoral neck. Hip subluxation is subsequent to these changes.
CMT= Charcot Marie Tooth disease
Hip dysplasia can be asymptomatic. As with CP patients, regular
surveillance should be instituted. The natural history of hip disease
in CMT is not yet defined, but a baseline AP pelvis film is suggested
when the diagnosis is made, with follow-up films every other year
during skeletal immaturity. If dysplasia exists, as defined by established
radiographic criteria, there are no effective nonsurgical options.
Surgical intervention requires correction of both the acetabular deficiencies and restoration of more normal proximal femoral anatomy.
Patients with CMT may be more sensitive to pressure or stretch of
peripheral nerves, and this should be taken into account when planning surgical treatment. Early mobilization to prevent aggravation of
weakness is also important in postoperative rehabilitation.2
SUMMARY
Numerous neuromuscular conditions can affect the normal development and function of the hip joint. A useful approach to
hip pathology categorizes the underlying neurological disease into
spastic or flaccid paralysis, and pediatric or adult onset. Within this
framework, specific approaches to hip pathology can be developed
and incorporated into the overall management of patients.
AANEM Course
Course
AANEM
REFERENCES
1. Bagg MR, Farber J, Miller F. Long-term follow-up of hip subluxation
in cerebral palsy patients. J Pediatr Orthop 1993;13:32-36.
2. Bamford NS, White KK, Robinett SA, Otto RK, Gospe SM, Jr.
Neuromuscular hip dysplasia in Charcot-Marie-Tooth disease type
1A. Dev Med Child Neurol 2009;51:408-411.
3. Bartonek A, Saraste H. Factors influencing ambulation in myelomeningocele: a cross-sectional study. Dev Med Child Neurol
2001;43:253-260.
4. Baxter MP, D'Astous JL. Proximal femoral resection-interposition
arthroplasty: salvage hip surgery for the severely disabled child with
cerebral palsy. J Pediatr Orthop 1986;6:681-685.
5. Bleck EE. The hip in cerebral palsy. Orthop Clin North Am
1980;11:79-104.
6. Bohannon RW, Smith MB. Interrater reliability of a modified
Ashworth scale of muscle spasticity. Phys Ther 1987;67:206-207.
7. Boyd RN, Hays RM. Outcome measurement of effectiveness of
botulinum toxin type A in children with cerebral palsy: an ICIDH-2
approach. Eur J Neurol 2001;8 Suppl 5:167-177.
8. Buly RL, Huo M, Root L, Binzer T, Wilson PD, Jr. Total hip arthroplasty in cerebral palsy. Long-term follow-up results. Clin Orthop
Relat Res 1993:148-153.
9. Cabanela ME, Weber M. Total hip arthroplasty in patients with neuromuscular disease. Instr Course Lect 2000;49:163-168.
10. Chan G, Bowen JR, Kumar SJ. Evaluation and treatment of hip
dysplasia in Charcot-Marie-Tooth disease. Orthop Clin North Am
2006;37:203-209, vii.
11. Correll J, Parsch K. Myelomeningocele--still a challenge for the orthopaedic paediatric surgeon. J Pediatr Orthop B 2000;9:141-142.
12. de Moraes Barros Fucs PM, Svartman C, de Assumpcao RM,
Kertzman PF. Treatment of the painful chronically dislocated
and subluxated hip in cerebral palsy with hip arthrodesis. J Pediatr
Orthop 2003;23:529-534.
13. Dobson F, Morris ME, Baker R, Graham HK. Gait classification
in children with cerebral palsy: a systematic review. Gait Posture
2007;25:140-152.
14. Eberle CF. Pelvic obliquity and the unstable hip after poliomyelitis. J
Bone Joint Surg Br 1982;64:300-304.
15. Ebinger T, Roesch M, Kiefer H, Kinzl L, Schulte M. Influence
of etiology in heterotopic bone formation of the hip. J Trauma
2000;48:1058-1062.
16. Eventov I, Moreno M, Geller E, Tardiman R, Salama R. Hip fractures in patients with Parkinson's syndrome. J Trauma 1983;23:98101.
17. Faraj S, Atherton WG, Stott NS. Inter- and intra-measurer error in
the measurement of Reimers' hip migration percentage. J Bone Joint
Surg Br 2004;86:434-437.
18. Gardner MJ, Ong BC, Liporace F, Koval KJ. Orthopedic issues after
cerebrovascular accident. Am J Orthop 2002;31:559-568.
19. Houlden H, Reilly MM. Molecular genetics of autosomal-dominant
demyelinating Charcot-Marie-Tooth disease. Neuromolecular Med
2006;8:43-62.
20. Houlden H, Charlton P, Singh D. Neurology and orthopaedics. J
Neurol Neurosurg Psychiatry 2007;78:224-232.
21. Kaliyaperumal K, Sathappan SS, Peng LY. Total hip arthroplasty for
ankylosed hip secondary to heterotopic ossification. J Arthroplasty
2008;23:470-475.
22. Keenan WN, Rodda J, Wolfe R, Roberts S, Borton DC, Graham HK.
The static examination of children and young adults with cerebral
palsy in the gait analysis laboratory: technique and observer agreement. J Pediatr Orthop B 2004;13:1-8.
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
23. Kumar SJ, Marks HG, Bowen JR, MacEwen GD. Hip dysplasia
associated with Charcot-Marie-Tooth disease in the older child and
adolescent. J Pediatr Orthop 1985;5:511-514.
24. Lau JH, Parker JC, Hsu LC, Leong JC. Paralytic hip instability in
poliomyelitis. J Bone Joint Surg Br 1986;68:528-533.
25. Lorente Molto FJ, Martinez Garrido I. Retrospective review of L3
myelomeningocele in three age groups: should posterolateral iliopsoas transfer still be indicated to stabilize the hip? J Pediatr Orthop
B 2005;14:177-184.
26. Nataraj A, Rajput AH. Parkinson's disease, stroke, and related epidemiology. Mov Disord 2005;20:1476-1480.
27. Parrott J, Boyd RN, Dobson F, Lancaster A, Love S, Oates J, Wolfe
R, Nattrass GR, Graham HK. Hip displacement in spastic cerebral
palsy: repeatability of radiologic measurement. J Pediatr Orthop
2002;22:660-667.
28. Rajput AH, Birdi S. Epidemiology of Parkinson's disease.
Parkinsonism Relat Disord 1997;3:175-186.
29. Reimers J. The stability of the hip in children. A radiological study of
the results of muscle surgery in cerebral palsy. Acta Orthop Scand
Suppl 1980;184:1-100.
30. Root L, Goss JR, Mendes J. The treatment of the painful hip in cerebral palsy by total hip replacement or hip arthrodesis. J Bone Joint
Surg Am 1986;68:590-598.
31. Scrutton D, Baird G. Hip dysplasia in cerebral palsy. Dev Med Child
Neurol 1993;35:1028-1030.
32. Scrutton D, Baird G, Smeeton N. Hip dysplasia in bilateral cerebral
palsy: incidence and natural history in children aged 18 months to 5
years. Dev Med Child Neurol 2001;43:586-600.
33. Shahcheraghi GH, Javid M. Abductor paralysis and external oblique
transfer. J Pediatr Orthop 2000;20:380-382.
31
34. Soo B, Howard JJ, Boyd RN, Reid SM, Lanigan A, Wolfe R,
Reddihough D, Graham HK. Hip displacement in cerebral palsy. J
Bone Joint Surg Am 2006;88:121-129.
35. Staeheli JW, Frassica FJ, Sim FH. Prosthetic replacement of the
femoral head for fracture of the femoral neck in patients who have
Parkinson disease. J Bone Joint Surg Am 1988;70:565-568.
36. Swaroop VT, Dias LS. Strategies of hip management in myelomeningocele: to do or not to do. Hip Int 2009;19 Suppl 6:S53-55.
37. Tosi LL, Buck BD, Nason SS, McKay DW. Dislocation of hip in
myelomeningocele. The McKay hip stabilization. J Bone Joint Surg
Am 1996;78:664-673.
38. Trojan DA, Cashman NR. Post-poliomyelitis syndrome. Muscle
Nerve 2005;31:6-19.
39. Vanden Bossche L, Vanderstraeten G. Heterotopic ossification: a
review. J Rehabil Med 2005;37:129-136.
40. Weber M, Cabanela ME. Total hip arthroplasty in patients with cerebral palsy. Orthopedics 1999;22:425-427.
41. Weber M, Cabanela ME, Sim FH, Frassica FJ, Harmsen WS. Total
hip replacement in patients with Parkinson's disease. Int Orthop
2002;26:66-68.
42. Widmann RF, Do TT, Doyle SM, Burke SW, Root L. Resection
arthroplasty of the hip for patients with cerebral palsy: an outcome
study. J Pediatr Orthop 1999;19:805-810.
43. Wynter M, Gibson,N.,Kentish,M.,Love, S.C.,Thomason,P.,Graham,
H.K. Consensus Statement on Hip Surveillance for Children with
Cerebral Palsy. 2008.
32
Practice Management
32
AANEM Course
Course
AANEM
AANEM Course
Course
Practice Management
33
Evaluation and Surgical Treatment of
Neurologic Injuries Around the Hip
Douglas C. Ross, MD, MEd, FRCS(C)
Thomas A. Miller, MD, FRCP(C)
Chair, Division of Plastic Surgery
Co-Director, Peripheral Nerve Clinic
Schulich School of Medicine and Dentistry
University of Western Ontario
London, Ontario, Canada
Departments of Physical Medicine and
Rehabilitation and Surgery
Schulich School of Medicine and Dentistry,
University of Western Ontario
London, Ontario Canada
INTRODUCTION
The hip joint is surrounded by multiple neural and vascular structures that are susceptible to both traumatic and iatrogenic injuries.
These may cause extremely disabling motor or sensory dysfunction.
Appropriate management includes imaging and electrodiagnostic
(EDX) studies to determine which injuries will spontaneously
recover, and which may benefit from intervention.
This manuscript describes the anatomy of the hip joint, the causes
of specific nerve injuries, how they present, and effective evaluation and diagnostic techniques. It also covers recommendations
for intervention, treatment options, and prognoses for the various
types of injuries.
ANATOMY
The hip joint is surrounded by multiple major motor nerves (sciatic,
superior gluteal, inferior gluteal, femoral, and obturator) and multiple sensory nerves (lateral femoral cutaneous, ilioinguinal, iliohypogastric, and genitofemoral). Each of these are at risk from either
trauma or various medical interventions. Knowledge of the relevant
anatomy assists in appropriate diagnosis and treatment.
The sciatic nerve arises from the L4 to S3 nerve roots and exits
the pelvis through the greater sciatic foramen. It passes under the
piriformis muscle and over the other external rotators of the hip to
the gluteus maximus muscle. Computed tomographic (CT) studies
demonstrate that the sciatic nerve lies less than a centimeter from
the posterior column of the pelvis adjacent to the acetabulum35
(Figure 1). The intraneural anatomy of the sciatic nerve contains
distinct peroneal and tibial divisions, with the former more susceptible to injury.12
The superior gluteal nerve arises separately from the L4 to S1
nerve roots and exits the pelvis through the greater sciatic foramen
along with the sciatic nerve before supplying gluteus medius,
gluteus minimus, and tensor fascia lata. Surprisingly high rates
of superior gluteal nerve palsy have been reported with lateral approaches to the hip,22 but modifying the surgical approach protects
the nerve.9
The femoral nerve arises from the L3 to L4 nerve roots and travels
on the ventral surface of the iliopsoas muscle. It enters the femoral
triangle as it passes beneath the inguinal ligament. At this point, the
nerve is almost directly anterior to the hip joint, and at risk during
anterior or anterolateral approaches to the hip, particularly from
retractor placement.
The obturator nerve arises from the L2 to L4 nerve roots and leaves
the pelvis through the obturator foramen. It then innervates the
adductors of the medial thigh. Of the major motor nerves around
the hip, it is the one that receives the fewest injuries.
34
Practice Management
Evaluation and Surgical Treatment
of Neurologic Injuries Around the Hip
AANEM Course
Course
AANEM
Figure 1 Cross-section at level of femoral head demonstrating key neural relationships to hip. M = Muscle
SPECIFIC NERVE INJURIES
Superficial sensory nerves
The sensory nerves that arise from the T12 to L2 roots provide
sensation to the inguinal region and the ventral surface of the thigh
(Figure 2). All are at risk from various surgical interventions. The
ilioinguinal, iliohypogastric, and genitofemoral nerves are at particular
risk during inguinal hernia repairs, particularly when prosthetic mesh is
used.2 Other causes include blunt and postappendectomy trauma.23
Patients present with symptoms consistent with a Type II complex
regional pain syndrome. Burning neuropathic pain is common and
is frequently positional. Some patients experience worse pain with
hip extension; others when they sit. Sexual dysfunction secondary
to cutaneous hypersensitivity is common. Physical examination
reveals hypersensitivity and allodynia in the distribution of one or
more of the three nerves. A positive Tinel sign may be elicited at
the particular site of injury, but significant overlap of the sensory
territory of these nerves makes it difficult to be certain which of the
nerves is causing the symptoms (Figure 3).
In general, imaging studies do not help assess the causes of pain.
Diagnostic nerve blocks with electromyography (EMG) guidance
help localize the cause of pain, and for some patients, may alleviate
it.33 Other nonoperative therapies, such as gabapentin or pregabalin,
may also help.
Operative treatment mirrors that of painful neuromas in other anatomic locations. Proximal neurectomy alone risks regrowth of regenerating axons into adjacent cutaneous areas. Burying the resected nerve
Figure 2 Anatomy of superficial sensory nerves ventral to hip.
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
35
Yuen and colleagues37 reviewed the EDX features of 100 sciatic
nerve injuries and found a surprisingly high frequency of normal
sural and peroneal sensory nerve action potentials (SNAPs) despite
the presence of postganglionic sciatic nerve injury. Thus, normal
SNAPs “do not necessarily exclude sciatic neuropathy.” One important take home point in this retrospective analysis deals with the
importance of contralateral limb studies.
Only 18 of the 27 normal sural reports had comparisons with
the contralateral sural SNAP (65 abnormal of 92 studies).37 This
further emphasizes the importance of bilateral sensory studies to
look for sensory axonal involvement in nerve injury. In addition,
this study found that the compound motor action potentialof the
extensor digitorum brevis was the best predictor for prognosis.
The peripheral nerve surgeon seeks the following information from
the EDX physician: (1) nature of the lesion (neuropraxic versus
axontemetic); (2) localization of the lesion; (3) associated nerve
injuries; and (4) evidence of recovery. (Table 1)
Table 1 Key information peripheral nerve surgeon requires from
electromyographer.
1. Is the injury neuropraxic or axontemetic?
2. Where is the injury anatomically (localization)?
3. Are there other associated nerve injuries (are possible nerve
transfer options injured)?
4. Is there evidence of recovery?
Figure 3 Cutaneous distribution of sensory nerves demonstrating
overlap.
end into muscle “satisfies” the regenerating nerves,25 and is preferred.
Surgical options include a so-called “triple neurectomy” through an
anterior2 or retroperitoneal approach via a flank incision.8
Amid2 reported that out of 100 patients, 80% experienced complete pain relief from an anterior approach triple neurectomy, but
follow-up was short. This outcome still mirrors our own experience.
In summary, patients who continue to experience significant and
disabling pain despite a reasonable trial of nonoperative therapy,
should be considered for surgical treatment.
Sciatic Nerve Injuries
The sciatic nerve is the one most often injured. The relative tethering
of the peroneal nerve at the fibular neck renders the peroneal division
more susceptible to traction injury. Axonotmetic injuries of the sciatic
nerve have a poor prognosis due to the significant distance from injury
site to motor end-plates and sensory receptors.37 Common mechanisms include gluteal injection, hip dislocation, as well as iatrogenic
damage after surgery for actetabular fractures or total hip arthroplasty.
Cross-sectional imaging and EDX testing to evaluate sciatic nerve
injury are advocated. They’re also complementary.3,28
Distinguishing neuropraxic from axonotmetic lesions allows the
surgeon to inform the patient about prognosis as well as the
potential need (in the case of axonal injuries) for surgery. It is
also useful in planning follow-up since axonal injuries not only
require closer scrutiny, but also decisions on intervention by 4 to
6 months postinjury. Sciatic nerve injuries frequently present as
peroneal nerve deficits, making localization of the lesion crucial.
In a systematic review, Marciniak and colleagues28 concluded
that motor nerve conduction studies (NCSs)—particularly across
the fibular neck—were useful to assess and localize peroneal
nerve palsies.
Looking for associated neuromuscular deficits can help localize
sciatic nerve injury and plan reconstructive surgery; for instance,
transfer of the tibialis posterior tendon for persistent peroneal nerve
palsies requires assurance that the tibialis posterior as well as other
plantar flexors are functioning normally. In addition, the technique
of nerve transfers, which has “exploded” in upper extremity nerve
reconstruction, is likely to become more popular in lower extremity
nerve reconstruction.
For example, branches to the lateral head of the gastrocnemius may
be transferred to injured branches of the peroneal nerve (Ross, unpublished data, 2009). Therefore, the surgeon requires assurance
that potential donor nerve branches of the tibial nerve are functioning normally. Finally, recovery on EMG testing predates that from
36
Practice Management
Evaluation and Surgical Treatment
of Neurologic Injuries Around the Hip
the clinical examination by several months. This is also very useful
when considering surgery.
Injection Injuries
Injection injuries are common, particularly in children.34 Severity
is highly dependent on the injected agent. Cephalosporins produce
relatively mild injury while some steroid agents, such as hydrocortisone, produce severe damage.26 Children who are born prematurely or have medical conditions requiring intensive care are at
higher risk.30 The typical presentation is that of a foot drop with or
without an accompanying pain syndrome. In the perinatal period,
this may be misdiagnosed as either congenital club foot or spinal
cord dysfunction.
A paucity of literature documents the natural history of these injuries, making definitive recommendations about observation versus
intervention difficult. Several authors have advocated surgical intervention34,31 if spontaneous recovery does not occur. Senes and
colleagues31 found that EDX testing helped identify less clinically
obvious tibial nerve involvement, thereby confirming the level of
involvement at the sciatic nerve rather than more distally at the the
common peroneal nerve.
Of 17 children with sciatic nerve palsies secondary to injection
injuries, 3 recovered spontaneously within a few months. Of the
remaining 14, 5 were referred more than 2 years after injury and
underwent reconstructive procedures, such as tendon transfers, but
no nerve surgery. Thus, 9 children underwent nerve surgery, most
commonly neurolysis.
The most important predictor of outcome was time from injury
to intervention. Of the 5 children treated less than 6 months
postinjury, 4 achieved Medical Research Council (MRC) grade 4
or higher, whereas only 1 of the 4 children treated after 6 months
did so. The other 3 achieved MRC grades of 1 or 0. The authors,
and most peripheral nerve surgeons, advocate exploration if there
is no significant clinical or electrophysiologic evidence of recovery
by 4 months postinjury.
Injuries Associated With Hip Trauma
The sciatic nerve may be injured from trauma or iatrogenically
during treatment of hip trauma.17,18,10,20 The frequency of sciatic
nerve injury from hip dislocations varies among series, but is approximately 10% in adults and 5% in children.10 It is thought that
the incidence is lower in children because dislocation is often associated with low-energy trauma whereas adults’ injuries are typically
high-energy (i.e., motor vehicle accidents). As is typical in many
sciatic nerve injuries, the peroneal division is more commonly
injured. Unlike the tibial division, the tethering of the peroneal
nerve at the fibular neck may render it less able to dissipate the
stretch forces incurred at the moment of injury.
The frequency of primary sciatic nerve injury is also related to the
pattern of hip injury, with the highest incidence in dislocations as-
AANEM Course
Course
AANEM
sociated with fractures of the posterior wall and/or column of the
acetabulum.20 In addition, the length of time that the hip remains
dislocated may affect outcomes. Hillyard and Fox18 reviewed 106
patients with hip dislocations and sciatic nerve dysfunction and
found that increasing periods of dislocation correlated with both a
higher incidence and greater severity of sciatic nerve injury.
Sciatic nerve injury may also occur during operative treatment of
hip injuries. Reasons include retractor or hardware placement, and
prolonged hip flexion and/or knee extension (placing greater tension
on the nerve).20 Some authors advocate intraoperative somatosensory
evoked potential monitoring to lessen the incidence of nerve injuries.29
Others, however, suggest that such monitoring is ineffective.17
Finally, sciatic nerve dysfunction may occur sometime after injury
and operative treatment secondary to heterotopic ossification
(HO).1,27 Incidence increases with associated closed head injuries,
complex fracture patterns, and postoperative hematoma formation.
Both indomethacin and low-dose radiation have been used for
prophylaxis against HO.5,6
Assessment of these injuries includes clinical examination, imaging,
and EDX testing. Symptoms may mimic a radicular pattern with
buttock pain, sensory disturbances in the sciatic nerve distribution,
and motor deficits with a predominance in the peroneal division.
Imaging may include plain films, CT, and magnetic resonance
imaging (MRI). Plain films may be helpful in identifying HO,
errant hardware, and fracture fragments that can potentially
impinge on the nerve.
CT scanning more precisely identifies HO location, more fully
defines the posterior acetabular wall and columns, and assesses for
possible confounding spinal pathology. MRI may be compromised
by metal artifacts, but helps assess spinal pathology, in particular.
EDX testing may be extremely helpful as stated previously.
Findings from the literature that describe the natural history of
these lesions are mixed. Epstein14 found that 60% of sciatic nerve
injuries associated with posterior fracture-dislocations “fully recovered." In a more detailed study, Fassler and colleagues16 reported
on 14 post-trauma patients with sciatic nerve injuries, with particular attention to the severity of initial injury and prognosis. Those
who presented with a “mild” peroneal palsy had a good prognosis,
typically with mild permanent sensory deficits and no motor deficits. Of 10 patients with initially severe peroneal deficits alone or
in combination with tibial deficits, only one recovered with a MRC
grade > 3.
A relative paucity of literature exists on outcomes of surgical interventions after hip trauma. Isaak and colleagues21 reported on 10
patients with sciatic nerve palsies after acetabular trauma. All sciatic
nerves were released; none were grafted. Every patient reported
improvement in sensory symptoms, including pain, but only 4 of 7
with motor deficits improved.
Benson and Schutzer4 found good results after piriformis release
and sciatic neurolysis (n=14), although all patients were injured
by low energy, blunt trauma. Precise indications for surgical inter-
AANEM Course
The Hip and the Neuromuscular
Practice Physician
Management
From EDX to Coxa Saltans
vention are not available due to small patient numbers. However,
a reasonable guideline for those with significant neuropathic pain,
parasthesia, and/or motor deficits is a lack of progressive recovery
at 6 months postinjury.
Injuries Associated With Total Hip Arthroplasty
Nerve injuries occur in 1-2% of total hip arthroplasty (THA)
procedures; more than 90% of these involve the sciatic nerve.12
Factors that increase the risk of sciatic nerve injury include revision
arthroplasty (rate 3-8%) and procedures for congenital hip dysplasia (rate 5.8%).32 Mechanisms of injury include direct mechanical
trauma from retractors, cautery, and reamers; also mechanisms specific to THA, such as cement extrusion and/or heating. Excessive
limb lengthening can also cause injury. In addition, sciatic nerve
dysfunction may occur years after THA secondary to inflammation
caused by wear debris from the prosthesis.11
The recurring pattern of a predominance of injury to the peroneal
division of the nerve is seen once again (>90% of all injuries32).
Although the diagnosis is typically made on clinical grounds, this
may underestimate the frequency of injury. Weale and colleagues36
prospectively studied 42 patients undergoing primary THA.
Although all were asymptomatic postoperatively,4 had denervation
potentials on EMG testing. Foot drop as well as neuropathic pain
were common symptoms. Precise cause of injury is often unclear,
but if clinical examination and/or imaging suggest reversible causes,
such as hematoma or cement extrusion, early exploration is warranted, and the prognosis is good.15
Factors that predict a poor prognosis include severe neuropathic
pain or complete lesions involving both the tibial and peroneal
divisions. Schmalzreid and colleagues32 examined patients at a
minimum of two years postinjury; 19% were normal, 64% had
a mild persistent deficit, and 17% had a major persistent deficit.
Farrell and colleagues15 cautioned that, “The majority of nerve injuries, whether complete or incomplete, never fully resolved.”
Few papers have examined the role of nerve exploration/reconstruction in the context of THA. In a large, heterogeneous group of
patients with sciatic nerve injuries from various causes, Kline and
colleagues24 reported on 13 patients with sciatic nerve dysfunction
after THA. Nine underwent exploration and were treated with
either neurolysis (4 of 9 ) or grafting. Recovery was good for the
tibial division in both groups (MRC grade >3 in 3 of 4 with neurolysis, and 3 of 5 with grafting), but the prognosis was poor for
the peroneal division, with only 1 of 9 recovering useful function.
If there is no evidence of recovery at 4 to 6 months postinjury,
most peripheral nerve surgeons support exploration of sciatic nerve
injuries associated with hip trauma.
Nerve Injuries Associated With Hip Arthroscopy
Hip arthroscopy is a new and increasingly popular treatment for hip
pathology, such as femeroacetabular impingement.7 Complications
are uncommon. In a review by Ilizaliturri,19 nerve injuries occurred
37
in 0.9-2% of cases. Injury is typically due to traction on the joint
(required for arthroscopic access) and surrounding structures, and
the perineal post used for countertraction. The most commonly
injured nerves are the perineal and pudendal, followed by the sciatic
and femoral. Fortunately, virtually all injuries are neuropraxic, and
therefore, resolve spontaneously. Indications for nerve exploration
are similar to those outlined above for other kinds of injuries.
OTHER MOTOR NEUROPATHIES
Although much less common than sciatic nerve injuries, both
the femoral and obturator nerves may be injured after trauma or
surgery. Farrell and colleagues15 noted that only 3 of 47 injuries
post THA involved the femoral nerve; none involved the obturator.
The superior gluteal nerve may also be injured in isolation after
antegrade femoral nailing for fractures as well as after THA.13 The
small numbers in these studies make it is difficult to extrapolate
findings for these less common neuropathies. Recommendations
for exploration mirror those for THA and hip trauma.
SUMMARY
Nerve injuries around the hip are relatively uncommon, but disabling when they occur. Appropriate evaluation requires clinical
examination, imaging, and electrodiagnostic testing. Surgical assessment and intervention should be considered for nerve deficits
that persist longer than 4 to 6 months postinjury.
REFERENCES
1. Abayev B, Ha E, Cruise C. A sciatic nerve lesion secondary to compression by a heterotopic ossification in the hip and thigh region--an
electrodiagnostic approach. Neurologist. 2005;11(3):184-6.
2. Amid PK. Causes, prevention, and surgical treatment of postherniorrhaphy neuropathic inguinodynia: Triple neurectomy with proximal end implantation. Hernia. 2004;8: 343–349.
3. Bendszus M, Wessig C, Reiners K, Bartsch AJ, Solymosi L,
Koltzenberg M. MR imaging in the differential diagnosis of neurogenic foot drop. Am J Neuroradiol 2003;24:1283–1289.
4. Benson ER, Schutzer SF. Posttraumatic piriformis syndrome: diagnosis and results of operative treatment. J Bone Joint Surg Am.
1999;81(7):941-9.
5. Blokhuis TJ, Frölke JP. Is radiation superior to indomethacin to
prevent heterotopic ossification in acetabular fractures?: a systematic
review. Clin Orthop Relat Res. 2009;467(2):526-30.
6. Burd TA, Lowry KJ, Anglen JO. Indomethacin compared with localized irradiation for the prevention of heterotopic ossification following surgical treatment of acetabular fractures. J Bone Joint Surg Am
2001;83-A:1783–1788.
7. Byrd JW. Hip arthroscopy. J Am Acad Orthop Surg. 2006;14:433–
444.
8. Choi PD, Nath R, Mackinnon SE. Iatrogenic injury to the ilioinguinal
and iliohypogastric nerves in the groin: a case report, diagnosis, and
management. Ann Plast Surg. 1996;37(1):60-5.
9. Comstock C, Imrie S, Goodman SB. A clinical and radiographic
study of the "safe area" using the direct lateral approach for total hip
arthroplasty. J Arthroplasty. 1994;9(5):527-31.
38
Practice Management
Evaluation and Surgical Treatment
of Neurologic Injuries Around the Hip
10. Cornwall R, Radomisli TE. Nerve injury in traumatic dislocation of
the hip. . Clin Orthop Relat Res. 2000;377:84-91.
11. Crawford JR, Van Rensburg L, Marx C. Compression of the sciatic
nerve by wear debris following total hip replacement: A report of
three cases. J Bone Joint Surg Br 2003;85:1178-80.
12. DeHart MM, Riley LH. Nerve injuries in total hip arthroplasty. J Am
Acad Orthop Surg 1999;7:101-111.
13. Donofrio PD, Bird SJ, Assimos DG, Mathes DD. Iatrogenic superior
gluteal mononeuropathy. Muscle Nerve. 1998;21(12):1794-1799.
14. Epstein HC. Posterior fracture–dislocations of the hip: long-term
follow-up. J Bone Joint Surg Am 1974;56:1103–1127.
15. Farrell CM, Springer BD, Haidukewych GJ, Morrey BF. Motor nerve
palsy following primary total hip arthroplasty. J Bone Joint Surg Am
2005;87:2619-25.
16. Fassler PR, Swiontkowski MF, Kilroy AW. Injury of the sciatic
nerve associated with acetabular fracture. J Bone Joint Surg Am
1993;75:1157–1166.
17. Haidukewych GJ, Scaduto J, Herscovici D, Sanders RW, DiPasquale
T. Iatrogenic nerve injury in acetabular fracture surgery: A comparison of monitored and unmonitored procedures. J Orthop Trauma
2002;6(5):297–301.
18. Hillyard RF, Fox J. Sciatic nerve injuries associated with traumatic
posterior hip dislocations. Am J Emerg Med 2003;21:545-548.
19. Ilizaliturri VM. Complications of arthroscopic femoroacetabular impingement treatment: A review. Clin Orthop Relat Res
2009;467:760–768.
20. Issack PS, MD, Helfet DL. Sciatic nerve injury associated with acetabular fractures. HSS J 2009;5: 12–18.
21. Issack PS, Toro JB, Buly RL, Helfet DL. Sciatic nerve release following
fracture or reconstructive surgery of the acetabulum. J Bone Joint
Surg Am. 2007;89(7):1432-7.
AANEM Course
Course
AANEM
22. Jacobs LG, Buxton RA. The course of the superior gluteal nerve in
the lateral approach to the hip.. J Bone Joint Surg Am. 1989;71:123943.
23. Kim DH, Murovic JA, Tiel RL, Kline DG. Surgical management of 33
ilioinguinal and iliohypogastric neuralgias at Louisiana State University
Health Sciences Center. Neurosurgery. 2005;56(5):1013-20.
24. Kline DG, Kim D, Midha R, Harsh C, Tiel R. Management and
results of sciatic nerve injuries: a 24-year experience J Neurosurg.
1998;89(1):13-23.
25. Mackinnon SE, Dellon AL, Hudson AR, Hunter DA. Alteration of
neuroma formation by manipulation of neural environment. Plast
Reconstr Surg 1985;76:345-51.
26. Mackinnon SE, Hudson AR, Gentili F, Kline DG, Hunter D.
Peripheral nerve injection injury with steroid agents. Plast Reconstr
Surg. 1982;69(3):482-90.
27. Manidakis N, Kanakaris NK, Nikolaou VS, Giannoudis PV. Early
palsy of the sciatic nerve due to heterotopic ossification after surgery
for fracture of the posterior wall of the acetabulum. J Bone Joint
Surg Br. 2009;91(2):253-7.
28. Marciniak C, Armon C, Wilson J, Miller R. Practice parameter: Utility
of electrodiagnostic techniques in evaluating patients with suspected
peroneal neuropathy: An evidence-based review. Muscle Nerve
2005;31: 520–527.
29. Middlebrooks ES, Sims SH, Kellam JF(1997) Incidence of sciatic
nerve injury in operatively treated acetabular fractures without
somatosensory evoked potential monitoring. J Orthop Trauma
1997;11:327–329.
30. Ramos-Fernandez JM, Oliete-Garcia FM, Roldan-Aparicio S,
Kirchschlanger E, Barrio-Nicolas A. Neonatal sciatic palsy: Etiology
and outcome of 21 cases. Rev Neurol 1998;26:752–755.
31. Senes FM, Campus R, Becchetti F, Catena N. Sciatic nerve injection
palsy in the child: Early microsurgical treatment and long-term result.
Microsurgery. 2009; March 20 (Epub ahead of print).
Critical Care
Charles F. Bolton, MD, FRCP(C)
Simon Podnar, MD, DSc
Andrea J. Boon, MD
Ted M. Burns, MD
Shawn J. Bird, MD
2009 COURSE E
AANEM 56th Annual Meeting
San Diego, California
Copyright © October 2009
American Association of Neuromuscular & Electrodiagnostic Medicine
2621 Superior Drive NW
Rochester, MN 55901
Printed by Johnson Printing Company, Inc.
ii
Critical Care
Faculty
Shawn J. Bird, MD
Andrea J. Boon, MD
Associate Professor
Director, Electromyography Laboratory
Department of Neurology
University of Pennsylvania
Philadelphia, Pennsylvania
Department of Physical Medicine and Rehabilitation
Mayo Clinic College of Medicine
Rochester, Minnesota
Dr. Bird is director of the EMG laboratory and clinical neurophysiology
fellowship program, as well as the Muscular Dystrophy Association and
myasthenia gravis clinics at the University of Pennsylvania. He is an associate professor of neurology at the University of Pennsylvania. He received
his undergraduate degrees in electrical engineering and biology from
Cornell University. He attended medical school at the Johns Hopkins
University School of Medicine. He completed his neurology residency
and fellowship training in neuromuscular disease and electrodiagnostic
medicine at the University of Pennsylvania. He is an active member of
the AANEM, is currently on the AANEM’s Course Committee, and has
served on the Journal, Special Interest, and Historical Committees. He
is a member of the American Academy of Neurology and the American
Neurological Association. His main research interests include neuromuscular disorders associated with critical illness, immune-mediated neuropathies and myasthenia gravis.
Dr. Boon graduated from medical school in New Zealand before completing
her residency in physical medicine and rehabilitation (PMR), followed by a
fellowship in clinical neurophysiology at the Mayo Clinic, Rochester, MN.
She has been on staff at Mayo since 2000, with a joint appointment as assistant professor in the Departments of PMR and Neurology, Mayo Clinic
College of Medicine. Dr. Boon has introduced diagnostic ultrasound into
the clinical and academic practice of the Mayo EMG lab, where over 12,000
patients undergo testing annually. Her current research focus is in this area,
in addition to her musculoskeletal practice where she has been investigating
the role of botulinum toxin in painful musculoskeletal disorders. Dr. Boon is
a member of the Continuing Medical Education committee of the AAPMR
and the Professional Practice committee of the AANEM, as well as serving
as the AANEM CPT advisor and the AANEM alternate RUC advisor to
the AMA.
Charles F. Bolton, MD, FRCP(C)
Faculty
Department of Medicine Division of Neurology
Queen’s University
Kingston, Ontario, Canada
Dr. Bolton was born in Outlook, Saskatchewan, Canada. He received his
medical degree from Queen’s University and trained in neurology at the
University Hospital, Saskatoon, Saskatchewan, Canada, and at the Mayo
Clinic. While at the Mayo Clinic, he studied neuromuscular disease
under Dr. Peter Dyck, and electromyography under Dr. Edward Lambert.
Dr. Bolton has had academic appointments at the Universities of
Saskatchewan and Western Ontario, at the Mayo Clinic, and currently at
Queen’s University. He also recently received the AANEM Distinguished
Physician Award. His special interests are investigations of neuromuscular
problems in the intensive care unit, and of neuromuscular respiratory
insufficiency.
No one involved in the planning of this CME activity had any relevant financial
relationships to disclose. Authors/faculty have nothing to disclose.
Course Chair: Shawn J. Bird, MD
The ideas and opinions expressed in this publication are solely those of the specific authors and
do not necessarily represent those of the AANEM.
iii
Ted M. Burns, MD
Simon Podnar, MD, DSc
Associate Professor
Department of Neurology
University of Virginia
Charlottesville, Virginia
Division of Neurology
Institute of Clinical Neurophysiology
University Medical Center
Ljubljana, Slovenia
Dr. Burns is an associate professor of neurology at the University of Virginia
in Charlottesville. He graduated from Kansas University Medical School and
completed his neurology residency at the University of Virginia (UVA). He
later completed 1-year fellowships in electromyography/neuromuscular diseases at UVA, and peripheral nerve diseases at the Mayo Clinic in Rochester,
Minnesota. He is board certified in neurology, clinical neurophysiology,
and electromyography. Dr. Burns is the director of the EMG laboratory at
UVA, director of the UVA neurology residency program, and director of the
UVA clinical neurophysiology fellowship program. He is the editor of the
weekly podcast for Neurology. He is also the editor of the AANEM’s Nerve
and Muscle Junction podcasts. He is a member of the AANEM’s Continuing
Medical Education committee and also a member of the American Board
of Psychiatry and Neurology’s (ABPN) Neurology Clinical Neurophysiology
committee, and the ABPN Neurology Recertification and Maintenance of
Certification committee.
Dr. Podnar graduated in 1992 from the University of Ljubljana Medical
School, in Ljubljana, Slovenia. In 1996 and 2002 he received his
masters, and the doctorate degrees. Since April 2001 he has worked as
a neurologist and clinical neurophysiologist at The Institute of Clinical
Neurophysiology in Ljubljana, Slovenia. His main interests are uroneurology, quantitative EMG and respiratory neurophysiology. He is co-author
of 10 chapters, and is the first author on over 50 papers in peer reviewed,
Science Citation Index cited journals. He is on the editorial board of
Muscle & Nerve, and regularly reviews papers for several other journals,
including Clinical Neurophysiology, European Journal of Neurology, Journal
of Neurology, and Neurosurgery & Psychiatry. He has been an invited speaker
at neurologic, clinical neurophysiologic, and urologic meetings in Europe
and North America. Since 2004 he has been president of the section for
clinical neurophysiology of the Slovenian medical society.
iv
iv
Sports Related Neuromuscular Disorders
Please be aware that some of the medical devices or pharmaceuticals discussed in this handout may not be cleared by the FDA
or cleared by the FDA for the specific use described by the authors and are “off-label” (i.e., a use not described on the product’s
label). “Off-label” devices or pharmaceuticals may be used if, in the judgement of the treating physician, such use is medically indicated to treat a patient’s condition. Information regarding the FDA clearance status of a particular device or pharmaceutical may
be obtained by reading the product’s package labeling, by contacting a sales representative or legal counsel of the manufacturer
of the device or pharmaceutical, or by contacting the FDA at 1-800-638-2041.
v
Critical Care
Contents
Faculty
ii
Objectives
v
Course Committee
vi
Electrophysiologic Approach to Neuromuscular Weakness in the Intensive Care Unit
1
Charles F. Bolton, MD, FRCP(C)
Phrenic Nerve Conduction Studies
Simon Podnar MD, DSc
5
Needle Electromyography of the Diaphragm
11
Myasthenia Gravis – Management of Myasthenic Crisis and Perioperative Care 15
Critical Illness Polyneuropathy and Critical Illness Myopathy
21
Andrea J. Boon, MD, C. Michel Harper, MD
Ted M. Burns, MD, Vern C. Juel, MD
Shawn J. Bird, MD
O b j e c t i v e s — Neuromuscular disorders are a common cause of prolonged weakness and failure to wean from mechanical ventilation.
Participants will learn (1) up-to-date information on various electrophysiologic techniques used to assess patients with neuromuscular respiratory failure, (2) current approaches to the management of myasthenic crisis, and (3) the recognition of critical illness polyneuropathy and critical
illness myopathy.
P r e r e q u i s i t e — This course is designed as an educational opportunity for physicians.
A c c r e d i tat i o n S tat e m e n t — The AANEM is accredited by the Accreditation Council for Continuing Medical Education
to provide continuing medical education (CME) for physicians.
CME C r e d i t — The AANEM designates this activity for a maximum of 3.25 hours in AMA PRA Category 1 Credit(s).TM If
purchased, the AANEM designates this activity for 2 AMA PRA Category 1 Credit(s).TM This educational event is approved as an
Accredited Group Learning Activity under Section 1 of the Framework of Continuing Professional Development (CPD) options for the
Maintenance of Certification Program of the Royal College of Physicians and Surgeons of Canada. Each physician should claim only
those hours of credit he or she actually spent in the educational activity. CME for this course is available 10/09 - 10/12.
vi
2008-2009 AANEM COURSE COMMITTEE
Anthony E. Chiodo, MD, Chair
Ann Arbor, Michigan
Shawn J. Bird, MD
Philadelphia, Pennsylvania
Mazen M. Dimachkie, MD
Kansas City, Kansas
Gary L. Branch, DO
Dewitt, Michigan
John E. Hartmann, MD
Augusta, Georgia
John E. Chapin, MD
Walla Walla, Washington
David Bryan Shuster, MD
Dayton, Ohio
2008-2009 AANEM PRESIDENT
Michael T. Andary, MD, MS
East Lansing, Michigan
Benjamin S. Warfel, II, MD
Lancaster, Pennsylvania
1
Electrophysiologic Approach to
Neuromuscular Weakness in the
Intensive Care Unit
Charles F. Bolton, MD, FRCP(C)
Division of Neurology
Queen’s University
Kingston, Ontario, Canada
INTRODUCTION
An electrophysiological approach to neuromuscular (NM) weakness
in the intensive care unit (ICU) may be time consuming. It involves
comprehensive clinical and electrophysiological assessment, as well
as other studies when indicated.1,2 There are two main reasons for
NM consultations in the ICU. One reason is the unexplained difficulty in weaning patients from the ventilator after cardiac and
pulmonary causes have been excluded. The second reason involves
observed limb weakness and reduced deep tendon reflexes.
Appropriate arrangements should be made in advance with the
ICU staff. Information on the patient’s history and physical examination, possible diagnoses, main treatments including use of NM
blocking agents and steroids, and ventilator settings should be obtained. The best time for the bedside clinical and electrophysiological assessment should be indicated. Additionally, the patient should
be on the least amount of sedation. Knowledgeable members of the
ICU staff including a nurse, resident, and a respiratory technologist
should be available.
There are two main categories to be considered in the differential
diagnosis which will be discussed.
Conditions developing acutely before
admission to the ICU
In this scenario, the respiratory muscles are predominantly involved
and an NM condition has not been previously considered. The
patient presents to the emergency room in acute respiratory failure.
An endotrachial tube is inserted, the patient is placed on a ventila-
tor, and continues to be managed thereafter in the ICU. After acute
cardiac and pulmonary conditions have been addressed, a consultation from an electrodiagnostic (EDX) physician is requested
because an NM problem is suspected.
In this acutely developing situation, clinical signs may be confusing. The differential diagnosis should be approached systematically,
and the relevant conditions should be eliminated.
Brain
Somatosensory evoked potentials (SEPs) are valuable in determining the severity of encephalopathy, particularly anoxic ischemic
encephalopathy. Severe trauma or metabolic toxic illnesses affecting
the brain may interfere with respiration though a lack of central
drive to the extent that endotracheal intubation and mechanical
ventilation are required. The results of limb conduction studies
and phrenic nerve conduction studies (NCSs) are normal. A needle
electromyography (EMG) of limb muscles shows an absence of or a
decrease in the number of motor unit action potentials (MUAPs).
The pattern of firing of MUAPs in the diaphragm is abnormal. For
example, Cheyne-Stokes respiration indicates diffuse disturbance of
the central hemispheres.
Spinal Cord
In acute disorders of the high cervical spinal cord, the traditional
signs of localized spinal cord disease such as compression resulting from neoplasm, infection, or acute transverse myelitis may be
2
Electrophysiologic Approach to Neuromuscular Weakness in the Intensive Care Unit
absent. Hyperreflexia is usually abolished by spinal shock, with the
sensory level difficult to determine, particularly in high cervical
lesions. Thus, magnetic resonance imaging (MRI) of the spinal
cord on an emergency basis is often necessary.
In motor NCSs, the amplitude of compound muscle action potentials (CMAPs) is decreased due to anterior horn cell disease
when the injury occurred at least 5 days earlier. When sensory
conduction is normal and clinical sensory loss is present, the
lesion is proximal to the dorsal root ganglion, usually indicating
myelopathy. Needle EMG abnormalities appear after a 10 to 20
day interval, depending on the distance between the muscle and
the site of injury along the nerve. The pattern of needle EMG
signs of denervation should assist in localizing the segmental
level, in determining whether it is unilateral or bilateral, and
in providing a rough estimation of the number of segments
involved, although the results may not be precise due to the
considerable overlap of innervation, particularly of the paraspinal muscles.
If the high cervical spinal cord is damaged, the results of motor and
sensory NCSs of limb nerves are normal. Because the phrenic nerves
arise from spinal segments C3 - C5, the amplitude of CMAPs from
the diaphragm may be considerably reduced or absent, although
latency is relatively preserved. Needle EMG shows an absence of
or a decreased number of MUAPS. Muscles innervated by the
involved high cervical segments demonstrate fibrillation potentials
and positive sharp waves 2 weeks after the lesion occurs. To confirm
the localization further, needle EMG of the cervical paraspinal and
the shoulder muscles supplied predominantly by C4 should also
show evidence of denervation.
In lesions of the lower cervical spinal cord, respiratory difficulty
is the result of upper motor neuron (MN) weakness of chest wall
muscles. Thus, the findings of phrenic NCSs and needle EMG of
the diaphragm are normal. However, there is a relative lack of firing
of MUAPs from chest wall muscles, and fibrillation potentials and
positive sharp waves are not present.
Motor Neuron Disease
Amyotrophic lateral sclerosis may be initially misdiagnosed as severe
respiratory insufficiency. The typical combined upper and lower MN
signs of hyporeflexia or hyperreflexia, muscle wasting and fasciculations, atrophy, and fasciculations of the tongue may not be obvious.
Electrophysiological studies, including phrenic NCSs and needle
EMG of the chest wall, diaphragm, and the limb muscles, often
suggest the diagnosis. However, it still may be necessary to proceed
with MRI studies. Atypical MN disease, such as motor neuropathy
with multifocal conduction block, should be excluded.
Acute Polyneuropathy
Acute polyneuropathy is suspected in the presence of muscle weakness, hyporeflexia, distal sensory loss, and the absence of upper
AANEM Course
MN signs or bladder dysfunction, but these signs may not always
be obvious. Bladder dysfunction and extensor plantar responses are
seen occasionally in Guillain-Barré syndrome (GBS).
In an acute inflammatory demyelinating polyneuropathy such
as GBS, the electrophysiological features are those indicating
demyelination of peripheral nerve. In the initial stages, conduction velocities may be decreased only mildly, but the diagnosis is
suggested by the prolongation or absence of F waves, evidence
of conduction block, and an absence of abnormal spontaneous
activity in muscle, with the remaining MUAPs firing rapidly.
Thus, even within hours after onset, the findings often strongly
suggest GBS. Phrenic NCSs and needle EMG of the diaphragm
are particularly valuable in establishing the type and severity of
the involvement of the phrenic nerve and diaphragm. Serial electrophysiological studies that follow the course of treatment, such
as plasmapheresis and hyperimmune globulin are valuable. In
the author’s experience, symptomatic improvement may precede
electrophysiological improvement.
Variants of GBS are primarily axonal, rather than demyelinating.
Most, but not all of them are likely to have Campylobacter jejuni
as the factor precipitating the immune mediated polyneuropathy. Positive results on serological testing or stool culture for C.
jejuni may be the earliest evidence of these axonal variants.
The acute axonal form of GBS (acute motor and sensory axonal
neuropathy) presents with a rapidly developing paralysis that
reaches completion within hours and requires early admission to
the ICU and full ventilatory assistance. Although the severity of
the condition varies, all muscles of the body, including cranial, eye,
and papillary muscles, may be completely paralyzed. Therefore, it
clinically simulates the syndrome of brain death, but the electroencephalogram (EEG) is relatively normal. All peripheral nerves may
be unresponsive to electrical stimulation.
In acute paralytic syndromes of children and young adults
with acute motor axonal neuropathy, symmetrical ascending
weakness develops over days, sensation is normal, deep tendon
reflexes are often preserved, and the concentration of protein in
the cerebrospinal fluid is increased. The amplitude of CMAPs
is reduced, but the latency is normal. Sensory conduction is
normal. Respiratory paralysis may be significant. Good recovery
eventually occurs.
Other polyneuropathies such as acute porphyria, Lyme disease, or
human immunodeficiency virus infection should be considered.
Chronic Polyneuropathies
Chronic polyneuropathies may evolve as rapidly developing respiratory insufficiency. Although rare, this situation may occur in
chronic inflammatory demyelinating polyneuropathy and diabetic
polyneuropathy. The typical clinical and electrophysiological signs
should be noted, and phrenic NCSs and needle EMG of the diaphragm should be performed.
AANEM Course
Critical Care
Neuromuscular Transmission Defects
Initially, both myasthenia gravis (MG) and Lambert-Eaton myasthenic syndrome (LEMS) may present with respiratory insufficiency.
In MG, this appears to be a syndrome. Levels of acetylcholine antibodies are normal, but muscle-specific tyrosine kinase-seropositive
antibodies may be abnormal. LEMS, hyocalcemia, hypermagnesemia,
and wound botulism may also be identified electrophysiologically. In
organophosphate poisoning, a repetitive discharge appearing after a
single electrical shock to a peripheral nerve is diagnostic.
Myopathies
Myopathies do not usually pose a difficult diagnostic problem
because the diagnosis is usually evident, having been established
previously in chronic cases such as muscular dystrophy. However,
respiratory muscles are occasionally involved, and these patients
may require intubation and admission to the ICU. In acute myopathies, such as necrotizing myopathy with myoglobinuria, the
diagnosis is evident due to the high levels of creatine phosphokinase
(CPK) and, at times, myoglobinuria.
Conditions Developing After Admission to the
ICU
1. Critical illness polyneuropathy (CIP) occurs commonly
and manifests as flaccid limbs and respiratory weakness.
Electrophysiologically, the findings are consistent with an axonal
motor and sensory polyneuropathy. The duration of the CMAP
is normal, and there is a response on direct muscle stimulation.
The CPK is near normal. Muscle biopsy reveals atrophy of both
type I and type II fibers. The prognosis is variable.
2. NM transmission defects commonly occur following the
use of NM blocking agents. There are flaccid limbs and respiratory weakness. Repetitive nerve stimulation shows the
typical post synaptic defect. Creatine kinase (CK) is normal,
as is the muscle biopsy. Prognosis is good.
3. Critical illness myopathy (CIM) can be subdivided into
several different types.
Thick filament myosin loss has the distinctive feature of a deficiency
of thick filament myosin on muscle biopsy. This occurs commonly
in patients who have been treated with NM blocking agents and steroids, but are often septic as well. The limbs are flaccid and there is
a respiratory weakness. EMG may show a myopathic pattern. There
is mild elevation in the CK. The duration of the CMAP is increased,
and there is an equally reduced response in amplitude on both stimulation of nerve and direct stimulation of muscle. Prognosis is good.
Rhabdomyolysis occurs rarely, and is likely a complication of sepsis
or a variety of medications used in the ICU. The limbs are flaccid
and there may be respiratory insufficiency. Electrophysiological
findings are near normal. The CK is markedly elevated and myo-
3
globinuria is possible. Like the electrophysiological studies, the
muscle biopsy may be near normal. The prognosis is good.
Necrotizing myopathy of intensive care is rare and presents as
severe flaccid weakness with myoglobinuria. Electrophysiology is
consistent with a very severe myopathy. CK is markedly elevated
and there is myoglobinuria. Muscle biopsy shows marked necrosis.
The prognosis tends to be poor.
Diffuse (cahectic) myopathy occurs commonly in patients who
have been recumbent for long periods in the ICU. Weakness and
wasting of muscle may be considerable. However, electrophysiological studies are normal, as is serum CK. Muscle biopsy is normal or
reveals type II fiber atrophy. The prognosis is good.
Combined polyneuropathy and myopathy is likely a common occurrence with the proportion of each depending on a variety of
factors. The limbs are flaccid and there is respiratory weakness.
Electrophysiological studies indicate a combined polyneuropathy
and myopathy. The CK is variably elevated. Muscle biopsy often
shows a mixture of denervation, necrosis, and atrophy of either type
I or type II fibers, or both. The prognosis is variable.
Mononeuropathies
A variety of mononeuropathies and plexopathies may occur in isolation or coexist with CIP and CIM. These may occur as a result of nerve
compression from prolonged recumbency, direct trauma, ischemia, or
hemorrhagic compression, complicating anticoagulant therapy. One or
both phrenic nerves may be damaged by mechanical trauma in major
accidents, following surgery, or trauma of a thermal nature, as in the
application of ice during cardiac surgery, or induction of heat in the
procedure of radio frequency ablation for auricular fibrillation.
Clinical Assessment
A reasonably comprehensive neurological assessment can be performed, especially if the patient is under minimal sedation and
there is little evidence of septic encephalopathy. With the patient
receiving only a pressure support of 9 cm H2O, the strength
and pattern of respiratory muscles from central drive can then
be accurately observed, including paradoxical respiration from
severe paralysis of both diaphragms. The accuracy of sensory
testing will depend on the degree of patient alertness and level
of cooperation.
Protocol for Electrophysiological Studies
1. Record skin temperatures.
2. Perform needle EMG of chest wall muscles and diaphragm.
This can be performed under the condition of least sedation and on a pressure support of only 9 cm H2O so there
is maximum possible central drive. In conditions of difficult
4
Electrophysiologic Approach to Neuromuscular Weakness in the Intensive Care Unit
access to the diaphragm (e.g., edema or obesity), an ultrasound-guided technique may be helpful.3 Needle EMG of
limb muscles should also be performed at this time.
3. Administer an intravenous narcotic for the remainder of the
studies, as the tests can be quite uncomfortable, especially in
patients who have GBS.
4. Perform pherenic nerve, motor, and sensory conduction
tests of limb nerves. In addition to observing any reductions
in the CMAP, a possible increase in duration is an important
sign of CIM.
5. Perform repetitive nerve stimulation to investigate for
defects in NM transmission. While the patient is under narcotic sedation, these tests can be performed at slow and rapid
rates of stimulation with reasonable comfort and can be used
to investigate for pre synaptic and post synaptic defects in NM
transmission.4
Other Tests of Neuromuscular Investigation in the ICU
If there is any possibility that acute respiratory insufficiency is based
on cervical myelopathy, MRI scans of the cervical area should be
performed before electrophysiological studies. Computed tomog-
AANEM Course
raphy, head scans, EEG, and SEPs may be necessary. If after all the
above investigations have been explored there is still uncertainty,
muscle biopsy is often quite helpful in a prognosis. For example,
in acute rhabdomyolysis, despite severe muscle weakness and very
high levels of CK, if the muscle biopsy is relatively normal, it
harbors a good prognosis. On the other hand, massive necrosis of
muscle may indicate a poor prognosis. Since open biopsy of muscle
may be difficult to arrange in ICU patients, needle biopsy may be
worthwhile.5
References
1. Bolton CF. Neuromuscular manifestations of critical illness. Muscle
& Nerve 2005;32:140-163.
2. Gorson KC. Approach to neuromuscular disorders in the intensive
care unit. Neurocritic Care 2005;3:195-212.
3. Boon AJ, Alsharif KI, Harper C, Smith J. Ultrasound-guided needle
EMG of the diaphragm: technique description and case report.
Muscle & Nerve 2008;38:1623-1626.
4. Rich MM, Bird SJ, Raps EC, et al. Direct muscle stimulation in acute
quadriplegic myopathy. Muscle & Nerve 1997;20:665-673.
5. Kendra LD, Nicole MN, Keith-Rokosh JA, Hammond RR.
Percutaneous muscle biopsies: review of 900 consecutive cases at
London Health Sciences Centre. Canadian Journal of Neurol. Sc.
2009;36:201-206.
5
Phrenic Nerve Conduction Studies
Simon Podnar MD, DSc
Division of Neurology
Institute of Clinical Neurophysiology
University Medical Center Ljubljana
Ljubljana, Slovenia
TECHNIQUE
Phrenic nerve conduction studies (NCSs) have been used for a
number of years in the evaluation of patients with respiratory
failure due to suspected neuromuscular (NM) disorders. The
first phrenic NCSs were performed by Heinbecker and associates
in 1936 using specimens obtained from operations or harvested
from cadavers.1 Later, “in vivo” studies were also performed,
using invasive recording electrodes (either esophageal or needle
electrodes inserted through the chest).1 However, the modern
era of phrenic NCSs began in 1967 with the publication of
Newsom Davis’ work.1 Davis demonstrated the clinical feasibility and utility of surface electrodes for recording the diaphragm
compound muscle action potential (CMAP) on phrenic nerve
stimulation. A pair of surface electrodes that were separated for
5 cm and positioned at the antero-lateral chest in the eighth or
ninth intercostal space were used.1 In these early studies, the
phrenic nerve was stimulated at the upper margin of the thyroid
cartilage behind the posterior border of the sternocleidomastoid
(SCM) muscle.1
Seventeen years later, another important contribution to phrenic
nerve conduction techniques was provided by Markand and
colleagues.2 A similar stimulation technique was used, but it
involved exploring recording montage in detail. Using a remote
reference (knee), it was discovered that a surface electrode placed
at the ipsilateral seventh intercostal space produced a higher
amplitude electropositive response, and that a surface electrode
placed at the xiphoid process generated a minimal amplitude electronegative response. Simultaneous recordings from the xiphoid
process (G1), and the ipsilateral seventh intercostal space (G2) resulted in summation of opposite polarity activity, and in a higher
amplitude electronegative response similar to typical CMAP, as
recorded from distal limb muscles.2
In a 1992 study, Swenson and Rubenstein further refined the position of recording electrodes.3 Using electrode arrays, they found
the maximal phrenic nerve CMAP amplitude at the intersection
of the anterior axilary line and the transverse plain through the
xyphoid. The researchers also mapped out the “motor point” area
of the diaphragm for the phrenic NCS.
The technique that is most widely used today in phrenic nerve
studies was established in 1995 by Chen and asssociates.4 They
discovered that phrenic nerve stimulation in the supraclavicular
fossa just above the clavicle is easier than stimulation at the level
of the upper margin of the thyroid cartilage, which had been used
before. Furthermore, use of a recording montage similar to that
used by Markand and colleagues was suggested, but instead of
counting intercostals spaces, the G1 electrode was placed 5 cm
above the tip of the xiphoid process, and the G2 electrode was
placed 16 cm from G1 on the rib cage margin, ipsilateral to the
phrenic nerve stimulation. In using this approach, the G2 in most
subjects was at the level of the seventh intercostal space, which
made G2 electrode positioning much easier, particularly in obese
subjects.4
Since the publication of that article in 1995, only small changes
in technique were suggested in 2008 by Resman-Gašperšič and
Podnar.5 Instead of phrenic nerve stimulation at the posterior
border of the SCM muscle, these authors proposed stimulation between both heads of the SCM muscle. It had been their
experience that stimulation at the posterior border of the SCM
muscle often resulted in difficulties obtaining a well formed and
6
Phrenic Nerve Conduction Studies
AANEM Course
reproducible supramaximal diaphragm CMAP. When using stimulation at the posterior border of the SCM muscle, concomitant
brachial plexus stimulation had proven to be a problem reported
by others as well.1-4,6
electrode and stimulation at higher levels in the neck, instead of
in the supraclavicular fossa. These differences in optimal position
of stimulation electrodes are likely due to anatomical variability
in phrenic nerve course.
The authors’ current approach is very similar to that described
by Bolton. It includes phrenic nerve stimulation in the supraclavicular fossa just above the clavicle with the anode above the
cathode. First, stimulation between both heads of the SCM
muscle (Figure 1) is attempted. Both heads of the SCM muscle
become more prominent when the subject flexes the neck for a
moment during stimulation electrode positioning. During stimulation, firm pressure of a bipolar stimulating electrode is applied
using lateral inclination pointing beneath the SCM muscle.5
Stimulation strength is continually increased, and no attention is
given to breathing. When amplitude stops increasing, in spite of
an increase in stimulation strength, voltage is increased another
20% to ensure a supramaximal stimulation strength. This usually
occurs at 70 to 90 mA with 0.1 ms pulse duration.5 Again, five
responses are recorded at the supramaximal stimulation strength,
and the breathing cycle is disregarded. The highest amplitude and
artifact-free CMAP is used as the result.7 If supramaximal stimulation response is not obtained at 100 mA, other stimulation electrode positions are used. These include the posterior border of the
SCM muscle with anterior inclination of the bipolar stimulating
Two disposable, self-adhesive disc electrodes are used for recording; the G1 electrode is fixed on the sternum 5 cm above the
xyphoid process tip, and the G2 electrode is placed ipsilaterally to the stimulation electrode 16 cm from G1 along the rib
cage border (Figure 1).4 The distance between both electrodes
is fixed and should only be proportionally reduced in small
children to the approximate location of the anterior axillary
line. The ground electrode is usually fixed to the middle of
the sternum.
The setting of the electromyography (EMG) machine is the
same as for other NCSs (filters 2 Hz to 10 kHz). However, the
amplitude is usually set at 200 µV, and latency is set to 3 ms per
division.
Bilateral studies are performed in all subjects. At supramaximal
stimulation strength, phrenic nerve CMAP onset latency (ms),
peak latency (ms), amplitude (mV), duration (ms), and area of
the negative phase (mVms) are measured.5
PHRENIC NERVE CMAP PARAMETERS: UTILITY AND
CONFIDENCE INTERVALS
The most regularly used CMAP parameters are onset latency and
amplitude. Exact confidence intervals for these two parameters
vary somewhat between different studies (Table 1).
CMAP onset latency has a well-established role in phrenic NCSs,
and is most useful in the detection of phrenic nerve demyelination.1,2,6 It was found to correlate with the subjects’ age4,8 and
height.5 However, as seen in patients with hereditary demyelinating polyneuropathies (e.g., Charcot-Marie-Tooth 1A, Figure 2),
latency poorly correlates with respiratory function. Therefore, it
can be regarded as a surrogate marker of neuropathy. In general,
longer latencies were reported in studies that used phrenic nerve
stimulation at the upper level of thyroid cartilage1,2,6 than in
studies that used stimulation in the supraclavicular fossa (in
Table 1 non-standard and standard, respectively).4,5,8,9 Using
the latter stimulation site, latencies > 8.0 ms can be regarded
as prolonged.5
Figure 1 Position of stimulation and recording electrodes for phrenic
nerve conduction studies. Stimulation electrodes (shown on subject’s
right) are positioned between the sternal and clavicular heads of the
sternocleidomastoid muscle (shown schematically on subjects’ left),
cathode being distal to anode. The position of the recording electrodes
is as described by Chen and colleagues (G1 5 cm above xiphoid
process, and G2 ipsilateral to stimulation 16 cm infero-laterally from
G1 over the chest margin).4 In addition, positions for electromyographic
(EMG) needle electrode insertions into the diaphragm are also shown
on the subject’s left side.5
In contrast, amplitude is very useful in assessing phrenic nerve
function (Figure 3), and is usually regarded as the main CMAP
parameter in phrenic NCSs. It is particularly helpful in the detection of neuronal or axonal lesions.2 However, the variability
among the results of previous studies is even larger (Table 1).
This may be primarily due to technical reasons (i.e., differences in stimulation efficiency and in recording montage).
Stimulation at the posterior border of the SCM muscle is not
likely always supramaximal, due to concomitant brachial plexus
stimulation. With a slightly more medial position in the supra-
AANEM Course
Critical Care 7
Table 1 Published reference intervals for phrenic nerve conduction
studies.
Reference
N
Technique
Latency
Amplitude
(mean ± SD;
upper limit)
(mean ± SD;
lower limit)
1
18 Non-standard 7.7±0.80; 9.3
0.16 - 0.50;-
2
50 Non-standard L: 7.74±0.76; 9,26
L: 0.77±0.22; 0.33
6
32 Non-standard 7.4±0.9; 9,2
0.51±0.12; 0.26
3
20 Non-standard L: 6.72±1.15; 9,02
L: 0.55±0.24;
0.065
7
?
4
9
8
50 Non-standard L: 6.81±0.75; 8.31
L: 0.40±0.18; 0.02
5
29 Standard
1.00±0.27; 0.46
R: 7.77±0.77; 9,31 R: 0.79±0.19; 0.41
R: 6.87±1.37; 9,61 R: 0.50±0.19; 0.12
Standard
6.3±0.8; 7,9
0.60±0.14; 0.32
25 Standard
6.54±0.77; 8.08
0.66±0.20; 0.26
35 Standard
6.1±0.7; 7.5
0.67±0.16; 0.35
6.55±0.69; 7.93
Figure 2 Phrenic nerve compound muscle action potentials (CMAP)
recorded in a 67-year-old man with genetically confirmed Charcot-MarieTooth 1A, and without respiratory symptoms. Note normally shaped CMAPs
(lower limit of normal for amplitude: 0.46 mV; left: 1.0 mV, and right: 0.9
mV) with extremely prolonged onset latency (upper limit of normal: 8.0 ms;
left: 18.0 ms, and right: 21.1 ms). No spontaneous denervation activity,
normal firing pattern, and normal quantitative motor unit action potential
parameters were found on the diaphragm electromyography.
The lower and upper normative (cut-off) limits were calculated as mean ± 2 SD - for
amplitude lower limit, because study data do not enable us to calculate this value.
Non-standard and standard techniques are as described in the “Technique” portion
of this text; SD = standard deviation.
clavicular fossa between both heads of the SCM muscle, amplitudes < 0.46 mV can be regarded as pathologic. The CMAP
amplitude is larger in men than in women, a result possibly due
to larger diaphragm muscle bulk in subjects with larger chest
circumference. A correlation of phrenic nerve CMAP amplitude with subjects’ age was found in some studies, 8 but not
in others. 5
Amplitude becomes larger during inspiration, which can be
recognized as more peaked traces. 5 Several explanations for
this observation have been discussed. The flattening of the diaphragm during inspiration increases the angle that the moving
dipole subtends at the recording electrode, which, according
to the theory of volume conduction, would result in increased
CMAP amplitude. 4 Shortening (shorter path) and thickening (faster conduction) of muscle fibers during contraction
(inspiration), both of which shorten the conduction time
along the diaphragm muscle fibers, could also contribute to
this variance. 5 Similarly, the lower right phrenic nerve CMAP
amplitude during inspiration might be explained by the higher
position of the diaphragm dome (smaller angle, longer and
thinner muscle fibers) on that side due to the subjacent liver.
No such difference was observed during expiration.5 The explanation is further complicated by the fact that both recording electrodes (G1 and G2) used in phrenic nerve CMAPs
are active. 2
Due to lower sensitivity to the respiratory cycle, and no differences between the left and right sides, the CMAP area was
proposed to be used instead of amplitude.5 However, the clinical
utility of phrenic nerve CMAP area is not yet well established.
Figure 3 Low amplitude phrenic nerve compound muscle action poten-
tials (CMAPs) (lower limit of normal: 0.46 mV; left: 0.1 mV, and right: 0.1
mV) recorded in a 78-year-old man with unexplained respiratory failure.
Patient was examined in a neurological intensive care unit where he was
intubated and mechanically ventilated. Onset latencies were normal on the
right (6.5 ms), and slightly prolonged on the left (10.3 ms; upper limit of
normal: 8.0 ms). Profuse spontaneous denervation activity, reduced firing
pattern, and relatively normal quantitative motor unit potential parameters
were found on the diaphragm electromyography. Clinical findings and
results of other electrodiagnostic studies were consistent with rapidly
progressive amyotrophic lateral sclerosis with poor collateral reinervation.
Note high amplitude electrocardiogram artifact on a second trace from the
right phrenic nerve.
By recording several responses and taking the largest amplitude
reproducible CMAP response, respiratory variation is probably of
minor importance, because traditionally, CMAP is taken during
inspiration.
Several investigators also reported CMAP duration, a parameter
useful to assess decreases in muscle fiber conduction velocity described in critical illness myopathy, and CMAP dispersion often
found in segmental demyelination. However, no data supports
use of this parameter.
8
Phrenic Nerve Conduction Studies
Using a rectangular pulse of 0.1 ms duration, CMAPs usually
appear at a stimulation strength of less than 50 mA in most
control subjects. None of them require stimulation with more
than 85 mA to record the maximal amplitude CMAP.4,5 However,
in extremely obese patients (body mass index > 40 kg/m2) with
short, thick necks, stronger stimulation strengths (longer pulse
durations) are often needed to record supramaximal amplitude CMAPs.2 Higher response thresholds are usually observed
in men.5
In addition to normative data for absolute values, normative data
for interside differences are also available.5 Although the value is
currently unclear, they are expected to be particularly useful in patients with asymmetric or unilateral phrenic nerve involvement.
INDICATIONS
Phrenic NCSs have several indications. When used with needle
EMG of the diaphragm, these studies are useful in evaluating
patients with respiratory failure due to suspected NM disorders.
However, in contrast to needle EMG of the diaphragm, phrenic
NCSs are noninvasive. They can also be safely performed in intensive care unit (ICU) patients with catheters in the supra and
infra clavicular fossae, as well as in those with implanted cardiac
devices.10
AANEM Course
Such patients will most often note reduced exercise tolerance
and report difficulties in the ability to lay flat. These complaints
often lead to a referral to a pulmologist and a chest x-ray will
be ordered, which may demonstrate the elevation of either a
single diaphragm leaf or both leaves. This is confirmed by poor
movement of the diaphragm on chest fluoroscopy or ultrasound
study. The most common localization of the lesion in this group
is the phrenic nerve itself. These disorders may be confined to
the phrenic nerve unilaterally (Figure 4), or bilaterally. However,
they may also be evident in other parts of the peripheral nervous
system. In some of these patients, systemic lupus erythematosus
(SLE), Lyme disease, and Herpes zoster (Martić V., personal
communication) can be diagnosed. In those with severe neck
and shoulder pain following infection, surgery, or vaccination, a
diagnosis of neuralgic amyotrophy is usually made (Figure 4).11
Phrenic nerves were affected in 7 of 99 consecutive patients with
neuralgic amyotrophy,12 but isolated phrenic nerve involvement
was reported only a few times in this condition.11 However, painless (bilateral) isolated phrenic neuropathy has been proposed as a
distinctive entity,13 a shared opinion among others as well13-15 In
some of these patients, other concomitant autoimmune disorders
such as myasthenia gravis16 and SLE suggest an immunological
Nevertheless, in most of these patients, phrenic NCSs are probably even more useful than needle EMG of the diaphragm. Normal
amplitude phrenic nerve CMAP virtually excludes the important
lesion of the phrenic nerve or diaphragm. Needle EMG of the
diaphragm is useful only in patients with nonrecordable or very
low amplitude phrenic nerve CMAPs. In this situation, it may not
only confirm the phrenic NCS findings, but also provide data in
regards to severity, mechanism, time course, and collateral reinnervation. Therefore, phrenic NCSs can and should be performed
even by electrodiagnostic (EDX) physicians who are not accustomed to performing needle EMG of the diaphragm.
In general, referrals to respiratory EDX studies can be divided
into several groups. The first group includes patients with known
NM conditions where respiratory failure is either expected (e.g.,
amyotrophic lateral sclerosis [ALS]) or possible (e.g., different
myopathies,9 Guillain-Barré syndrome (GBS),6 chronic inflammatory neuropathy ) along the disease course. It is often useful to
follow these patients using regular respiratory EDX studies along
with pulmonary function tests in order to be prepared for the
occurrence of respiratory failure, and treat it in a timely manner.
Although needle EMG of the diaphragm will provide more detailed information, phrenic NCSs alone will usually demonstrate
the severity of NM involvement of the peripheral respiratory
system. CMAP amplitude is particularly useful in this respect,
and is expected to fall steadily in progressive diseases (e.g., ALS)
along with failing respiratory function.
The second group consists of patients with minor respiratory
symptoms and signs of partial restrictive respiratory failure.
Figure 4 Phrenic nerve compound muscle action potentials (CMAP) recorded in a 49-year-old women with breathlessness on minor effort and on
laying on the left flank. She reported severe pain on the right side of the
neck before onset of respiratory symptoms. She had normal chest x-ray
just before onset of pain, and highly elevated right diaphragm leaf 4 weeks
after onset of pain. The first study was performed at 5 months(left study),
and the second was at 15 months after the onset of pain(right study). Note
absent responses from the right on the first study (lower limit of normal amplitude: 0.46 mV; left: 0.7 mV, and right: no response), that partially recovered on the second study (left: 0.6 mV, and right: 0.4 mV). Onset latencies
were normal on the left (6.0 ms), and slightly prolonged on the right on the
second study (9.4 ms; upper limit of normal: 8.0 ms). Profuse spontaneous
denervation activity and severely reduced firing patterns were found on
the right diaphragm electromyography on the first examination, but were
remarkably improved on the second. Clinical findings and results of other
electrodiagnostic studies were consistent with isolated, almost complete
axonal lesion of the right phrenic nerve with good recovery in 15 months.
Findings are probably consistent with diagnosis of neuralgic amyotrophy
confined to the right phrenic nerve.
AANEM Course
Critical Care
Table 2. Reference intervals for phrenic nerve conduction studies
obtained in 29 normal volunteers.5
Parameter
Mean±SD
L/U limits
5th/95th
Response threshold (mA)
32.41±12.02
8.38/56.45
15/48
Maximal response (mA)
55.86±13.76
28.34/83.39
37/83
Onset latency (ms)
6.55±0.69
5.18/7.92
5.53/7.72
Peak latency (ms)
12.89±1.25
10.39/15.39
11.08/14.94
Amplitude (mV)
1.00±0.27
0.46/1.54
0.66/1.46
Duration (ms)
14.99±3.14
8.70/21.28
11.18/20.25
Area (mVms)
8.23±1.91
4.40/12.05
5.58/11.31
L/U – lower/upper limits obtained after mathematical transformations; 5th/95th –
5th/95th percentile limits. Clinically more relevant limits are underlined.
basis for this disorder. A patient was seen by this author with
severe idiopathic thrombocytopenic purpure and bilateral phrenic
nerve lesion presenting soon after laparoscopic splenectomy
(Podnar, unpublished personal data). In some patients, other
diagnoses could have been made if the presentation occurred
earlier in the disease course. Presentations may also occur soon
after surgery, a trigger cause of phrenic nerve lesions (e.g., cardiac
or thoracic surgery). Phrenic nerve lesions in these patients may
be unilateral or even bilateral, and their prognosis depends on the
exact mechanism of the nerve lesion (i.e., traction or compression
versus section). Similarly, in nonsurgical patients, some phrenic
nerves will recover, while others will not. In general, the prognosis is slower and worse than in typical neuralgic amyotrophy.11
Phrenic nerve CMAP amplitude will often be very useful in these
patients to confirm presence and the extent of the phrenic nerve
injury. Interestingly, in some patients, bilateral phrenic nerve
lesions will be demonstrated in imaging studies even when only a
unilateral lesion was suspected.15
The last group is comprised of ICU patients. Some will be admitted to the ICU due to restrictive respiratory failure of unknown
cause. Many of these patients have ALS, which occasionally presents with respiratory failure (Figure 3).17 Other patients from this
group may have severe neuropathies (e.g., GBS, porphyria), myelopathies, or encephalopathies. Phrenic NCSs will be very useful
in these patients to differentiate between lower and upper motor
neuron lesions. Additional EDX studies performed in other
regions will be helpful in revealing the extent and mechanism of
disease process. Severe respiratory failure that requires admittance
to the ICU may also be observed in patients with isolated, usually
bilateral, phrenic nerve lesions due to the mentioned etiologies,
particularly if their respiratory function is compromised for other
reasons. The other important group includes patients that need
phrenic NCS at some point and are admitted to the ICU due to
severe medical or surgical conditions, of which respiratory failure
is not the leading component. Respiratory failure will often
become obvious at the moment an attending physician would
expect them to be weaned from the mechanical ventilator. This
typically occurs when such patients become alert and responsive.
9
Characteristically, these patients have a tendency to move their
limbs poorly, a result of diseased muscle or nerve. These conditions are referred to as critical illness myopathy or neuropathy,
respectively. They are supposedly caused by systemic inflammatory response that accompanies severe illness (e.g., sepsis, multiorgan failure, etc). Although a diagnosis can often be made by
limb NCSs and limb muscle needle EMG, due to the importance
of respiratory function in this clinical situation, phrenic NCSs
should also be considered.
Furthermore, phrenic NCSs may be also used in patients with
high cervical spinal cord lesions to identify candidates for phrenic
nerve or diaphragmatic pacing. For these patients, mechanical
ventilation via a tracheostomy is a standard therapy. Potential
problems associated with the use of mechanical ventilation
include high cost, risk of infection, tracheal injury, and equipment malfunction. Pneumonia remains the most common cause
of death after spinal cord injury. A demonstration of normal or
near normal amplitude phrenic nerve CMAPs can serve as a useful
indicator of viable phrenic motor neurons that are needed for this
type of treatment.18
CONCLUSION
Phrenic NCS is an established technique that is not only fast
and easy to perform, but can provide important information
in patients with suspected NM causes of restrictive respiratory
failure. Additionally, it can usually be effectively applied in ICU
patients.
Acknowledgements: The writing was supported by the Republic
of Slovenia Research Agency, Grant No. J3 7899.
REFERENCES
1. Newsom Davis J. Phrenic nerve conduction in man. J Neurol
Neurosurg Psychiatry 1967;30:420-426.
2. Markand ON, Kincaid JC, Pourmand RA, Moorthy SS, King RD,
Mahomed Y, et al. Electrophysiologic evaluation of diaphragm by
transcutaneous phrenic nerve stimulation. Neurology 1984;34:604614.
3. Swenson MR, Rubenstein RS. Phrenic nerve conduction studies.
Muscle Nerve 1992;15:597-603.
4. Chen R, Collins S, Remtulla H, Parkes A, Bolton CF. Phrenic nerve
conduction study in normal subjects. Muscle Nerve 1995;18:330335.
5. Resman-Gasperšič A, Podnar S. Phrenic nerve conduction studies:
technical aspects and normative data. Muscle Nerve 2008;37:36-41.
6. Gourie-Devi M, Ganapathy GR. Phrenic nerve conduction time in
Guillain-Barré syndrome. J Neurol Neurosurg Psychiatry 1985;48:245249.
7. Bolton CF. Clinical neurophysiology of the respiratory system.
Muscle Nerve 1993;16:809-818.
8. Imai T, Yuasa H, Kato Y, Matsumoto H. Aging of phrenic nerve
conduction in the elderly. Clin Neurophysiol 2005;116:2560-2564.
10
Phrenic Nerve Conduction Studies
9. Zifko UA, Hahn AF, Remtulla H, George CF, Wihlidal W, Bolton
CF. Central and peripheral respiratory electrophysiological studies in
myotonic dystrophy. Brain 1996;119:1911-1922.
10. Schoeck AP, Mellion ML, Gilchrist JM, Christian FV. Safety of nerve
conduction studies in patients with implanted cardiac devices. Muscle
Nerve 2007;35:521-524.
11. Lahrmann H, Grisold W, Authier FJ, Zifko UA. Neuralgic amyotrophy with phrenic nerve involvement. Muscle Nerve 1999;22:437442.
12. Tsairis P, Dyck PJ, Mulder DW. Natural history of brachial plexus
neuropathy. Report on 99 patients. Arch Neurol 1972;27:109-117.
13. Lin PT, Andersson PB, Distad BJ, Barohn RJ, Cho SC, So YT, et al.
Bilateral isolated phrenic neuropathy causing painless bilateral diaphragmatic paralysis. Neurology 2005;65:1499-1501.
14. Valls-Sole J, Solans M. Idiopathic bilateral diaphragmatic paralysis.
Muscle Nerve 2002;25:619-623.
15. Kumar N, Folger WN, Bolton CF. Dyspnea as the predominant
manifestation of bilateral phrenic neuropathy. Mayo Clin Proc
2004;79:1563-1565.
AANEM Course
16. Valadas A, de Carvalho M. Myasthenia gravis and respiratory failure
related to phrenic nerve lesion. Muscle Nerve 2008;38:1340-1341.
17. Spitzer AR, Giancarlo T, Maher L, Awerbuch G, Bowles A.
Neuromuscular causes of prolonged ventilator dependency. Muscle
Nerve 1992;15:682-686.
18. Alshekhlee A, Onders RP, Syed TU, Elmo M, Katirji B. Phrenic
nerve conduction studies in spinal cord injury: applications for diaphragmatic pacing. Muscle Nerve 2008;38:1546-1552.
11
Needle Electromyography of
the Diaphragm
Andrea J. Boon, MD
C. Michel Harper, MD
Assistant Professor of Physical Medicine and
Rehabilitation
Assistant Professor of Neurology
Mayo Clinic College of Medicine
Rochester, Minnesota
Professor of Neurology
Mayo Clinic College of Medicine
Rochester, Minnesota
NEEDLE ELECTROMYOGRAPHY OF THE DIAPHRAGM
Indications
Needle electromyography (EMG) of the diaphragm is a useful
electrophysiologic technique in patients presenting with unexplained dyspnea or failure to wean from the ventilator. Underlying
etiologies include lack of central drive (such as in high spinal cord
injury or encephalopathy), anterior horn cell or nerve root disease
(at C3 - C5 levels), polyneuropathy (including critical illness polyneuropathy and Guillain-Barré syndrome), myasthenia gravis or
other disorders of neuromuscular transmission, myopathy (including critical illness myopathy), and phrenic neuropathy (which may
be traumatic, compressive, or inflammatory such as in Parsonage
Turner syndrome).
Needle EMG can provide important information regarding the underlying pathophysiology. It can assist in differentiating between
neuropathic, myopathic, and central disorders, as well as prognostic
information regarding potential for meaningful recovery, that may
not be elicited on clinical grounds alone. Although the diaphragm
is an inherently high-risk muscle to examine due to nearby vital
structures (liver, spleen, colon and lung), when performed with appropriate technique, the actual risk appears to be quite low.
is a musculotendinous structure that receives its motor innervation from the phrenic nerves (C3 - C5) and its sensory supply
from the phrenic, intercostal (T5 - T11), and subcostal (T12)
nerves. The muscular part of the diaphragm lies peripherally, with
fibers converging radially onto a central tendon. It is fixed to the
thoracic cage and superior lumbar vertebrae, allowing only the
central portion to move. The costal part of the diaphragm consists
of wide muscular slips attaching to the costal cartilages and ribs
(forming a dome on either side). The muscle contracts (the domes
flatten) during inspiration, then relaxes during expiration. Based
on anatomical studies, there is at least 1.5 cm between the pleural
reflection and the lower costal cartilage upon which the diaphragm
inserts,1 and with quiet inspiration, the lung does not descend to
enter the pleural space.
Technique
Anatomy
Several techniques for needle EMG of the diaphragm have been
described, including two which approach the muscle from the
abdominal wall, advancing the needle rostrally beneath the costal
margin, towards the diaphragm.5,7 However, both can be technically difficult, particularly in more obese patients, and may require
a long needle to reach the diaphragm. More recently, Bolton and
colleagues have described a technique initially reported by Koepke
which is technically very feasible and has been demonstrated in a
cadaveric study to be safer than the abdominal approach.1,4,6
It is important to understand the anatomy and normal function of
the diaphragm prior to attempting needle EMG. The diaphragm
This technique involves insertion of the EMG needle just above the
costal margin at any interspace between the medial clavicular line
12
Needle Electromyography of the Diaphragm and the anterior axillary line (Figure 1). The interspace chosen is
based on palpation and examiner preference, as in some cases cartilage may bridge the interspace, making needle insertion difficult,
and another interspace must be chosen. The needle is inserted as far
medially and caudally within the chosen interspace as possible. The
angle of entry is perpendicular to the chest wall, with the needle
passing first through skin and subcutaneous tissue before encountering the external oblique or rectus abdominus muscle, followed
by external and internal intercostal muscles, and finally passing in
to the diaphragm (Figure 2).
At rest, the intercostal muscles should be fairly quiet; however, they
can be easily activated with vigorous inspiration, forced expiration
such as coughing, or slight twisting of the chest wall. Entry in to
the diaphragm is signaled by bursts of motor unit action potentials
(MUAPs) firing with each inspiration. This can be accentuated by
asking the patient to sniff quickly in through the nose. Small redirections of the needle may be required to achieve complete entry of the
needle into the diaphragm; however, if motor units are initially heard
to fire with inspiration, but are no longer audible with further advancement of the needle, this suggests the diaphragm has been completely traversed and the needle should be withdrawn and redirected.
MUAPs in the diaphragm are typically shorter in duration, have lower
amplitude, and are more numerous than MUAPs in the intercostal or
limb muscles.
Risks
Prior to attempting needle EMG of the diaphragm, it is prudent
to discuss the potential risks with the patient, to obtain informed consent (either written informed consent or verbal
consent documented in the EMG report), and to instruct the
patient to notify the electrodiagnostic (EDX) medicine physi-
Figure 1 Insertion points for diaphragmatic needle electromyography
examination are marked by an X. The needle is inserted just above the
costal margin between the medial clavicular line and the anterior axillary
line. The needle is inserted as far medially and caudally within the chosen
interspace as possible and the lowest interspace that can be entered is
targeted.
AANEM Course
cian if they feel a deep aching or very sharp pain any time
after the intercostal muscles have been entered, as this may
represent penetration of the pleura or peritoneum. Chiodo and
associates performed a cadaveric study evaluating three different techniques of needle insertion, just lateral to the xiphoid
process,5 beneath the costal margin at the anterior axillary line,7
and through the sixth, seventh, and eighth intercostal spaces at
the anterior axillary line.1,6 This was a small study with only 10
needle insertions per technique and was performed in cadavers (in which the diaphragm is elevated, similar to a paralyzed
diaphragm). The authors reported a 100% success rate with
insertions above and below the seventh rib (Bolton’s technique),
and only 50% accuracy with the other approaches.4 They also
documented “dangers” (inadvertent placement in a vital structure), of which 71% occurred on the right side (predominantly
liver penetration). There were no cases of pleura or lung penetration reported. The authors concluded that needle insertion
superior to the eighth rib in the anterior axillary line is the safest
approach and that needle EMG should be avoided in patients
with coagulopathy (particularly on the right side due to risk of
liver penetration).
Bolton reported a series of 49 cases with no pneumothorax, and
based on a telephone survey, two cases of pneumothorax in over 1000
needle examinations of the diaphragm, both in patients with severe
chronic obstructive pulmonary disease (COPD).1,2 Anecdotally, this
is a low-risk procedure, and pneumothorax is more commonly seen
after examination of chest wall muscles (such as serratus anterior,
rhomboid) than after examination of the diaphragm. However, this
may in part reflect the greater number of chest wall muscles that are
examined in a particular laboratory in addition to the relative experience of the EDX medicine physician.
Figure 2 Anatomy of needle electromyography (EMG) of the diaphragm.
The angle of needle entry is perpendicular to the chest wall, with the
needle passing first through skin and subcutaneous tissue before encountering the external oblique or rectus abdominus muscle, followed by the
intercostal muscles, and finally passing in to the diaphragm. The pleural
reflection is usually at least 1.5 cm rostral to the lower costal margin.
AANEM Course
Critical Care
ULTRASOUND-GUIDED NEEDLE EMG OF THE
DIAPHRAGM
Rationale
Ultrasound (US) imaging provides excellent direct and real
time visualization of soft tissues. It provides details about anatomic landmarks, fascial planes, and neurovascular structures
adjacent to the intended target. With recent advances in technology, high-quality US machines are affordable and portable, and
have subsequently become more widely available for a variety
of clinical applications. For the past several years, the use of
US imaging has been integrated into a number of aspects of
daily clinical and academic practice in a large, tertiary referral
EMG laboratory.
Although Bolton’s described technique is relatively safe and technically feasible, in certain cases, such localization is not always
possible or may be inaccurate based on anatomical landmarks (i.e.,
when the diaphragm is completely paralyzed or very atrophic, in
obese patients, in patients with altered anatomy, or in patients with
severe obstructive pulmonary disease with hyperinflated lungs).
For this reason, the use of diagnostic US has been introduced
to help localize the diaphragm. By providing direct visualization
during needle placement, this enhances the safety and accuracy
of the examination and may also provide additional information
regarding diaphragmatic function which cannot be elicited on the
basis of needle EMG alone. Many of the benefits of complementary US in the assessment of respiratory failure were highlighted
in a recent case report in which US enabled physicians to evaluate
whether the diaphragm was actually contracting during phrenic
nerve conduction studies and whether there was any volitional
activation of the diaphragm with the ventilator turned off. In
addition, it provided real time visualization of needle placement
into the diaphragm and allowed for detection of any associated
bleeding in a patient on warfarin with an international normalized
ratio of 4.1.3
Technique
US examination of the diaphragm can be easily performed at the
bedside using a portable machine. Depending on the US system utilized, depths of up to 10 cm can be visualized using a linear probe
at frequencies of 8 to 12 Hz. (In larger adults, a curvilinear transducer may be necessary to adequately image the diaphragm). The
seventh, eighth, and ninth ribs in the region of the anterior axillary
line are identified, and the probe is initially placed perpendicular to
the ribs, centered over the eighth intercostal space. Each rib is easily
identified by the bright signal generated at the bony cortex, and the
acoustic shadowing deep to it. Subcutaneous tissue lies superficial
to the ribs, and two layers of intercostal muscle bridge the space
between any two adjacent ribs. Deep to the ribs, the diaphragm can be
visualized (Figure 3a).
The muscle layers are easily recognized by their location and
appearance. Longitudinally, muscles have a mixed echogenic
appearance, consisting of hypoechoic (dark) muscle fibers sepa-
13
rated by hyperechoic (bright) fibroadipose septae (perimysium).
Transversely, the mixed echogenicity pattern of muscle produces a
“starry night” appearance. The diaphragm is typically identified by
its deep location, curved geometry, and muscular echotexture. In
addition, the diaphragm will thicken during inspiration as a result
of muscular contraction unless severely atrophic, in which case it
will appear as a very thin strip beneath the intercostal muscles and
may not move with inspiration.
In the region of the lower intercostal spaces, the liver on the right
and the spleen on the left can be visualized deep to the diaphragm
and appear as homogeneous, low-intensity structures punctuated
by occasional blood vessels (Figure 3). However, when the patient
inhales deeply, the pleura and lung will enter into the field of view;
the lung will appear as a bright high-intensity shadow coming in
from above and displacing the diaphragm and underlying liver or
spleen (Figure 3b).
After initial identification of the anatomy perpendicular to the long
axis of the ribs, the transducer is then turned parallel to the ribs
overlying the intercostal space. Typically, the seventh intercostal
space is initially evaluated, but other spaces are subsequently evaluated as necessary to identify the space that will provide the best
visualization of the diaphragm, where the muscle is thickest, with
minimal encroachment of the pleural space and or lung. Under
real-time US guidance, the needle can be inserted either parallel or
perpendicular to the long axis of the transducer. A personal preference is to insert the needle parallel to the transducer (long axis
approach), providing direct visualization of the needle throughout
the examination (Figure 3b) while simultaneously monitoring the
pleural space descending in to the field of view as the patient takes
in a deep inspiration. The scanning depth and transducer frequency
should be adjusted to allow the highest frequency to be used that
will allow visualization at a sufficient depth to see the pleura. If a
short axis approach is used, caution must be exercised to stop advancing the needle as soon as the bright tip of the needle is identified on US, as the appearances of the needle tip and the shaft (i.e.,
the tip has moved beyond the plane of the US beam) are nearly
indistinguishable.
Applications
US is utilized on a regular basis when examining the diaphragm.
Even in relatively uncomplicated cases, US can easily identify the rib
space that provides the best view of the diaphragm, without pleural
or lung encroachment. In addition, the depth of needle penetration
necessary to reach the diaphragm can be quickly gauged. This is
also helpful when attempting a nonguided approach.
It is particularly helpful in more challenging cases, such as larger
patients where ribs may be more difficult to palpate, patients with
altered anatomy where landmarks cannot be relied upon for accurate guidance, patients with COPD and associated hyperinflation
of the lungs, patients on anticoagulation or with coagulopathy who
would otherwise not be candidates for needle EMG, and patients
with severe atrophy or denervation of the diaphragm where the
normal sound of MUAP firing cannot be relied upon to guide
14
Needle Electromyography of the Diaphragm AANEM Course
needle placement. US imaging not only provides information
on the proximity of nearby vital structures, but also allows the
EDX physician to assess the quality and degree of motion of the
diaphragm, both with respiration and in response to phrenic nerve
stimulation.
REFERENCES
1. Bolton CF, Grand'Maison F, Parkes A, Shkrum M. Needle electromyography of the diaphragm. Muscle Nerve 1992;15:678-681.
2. Bolton CF, Chen R, Wijdicks EFM, Zifko UA. Neurology of
Breathing. Philadelphia: Elsevier Inc.; 2004.
3. Boon AJ, Alsharif KI, Harper CM, Smith J. Ultrasound-guided
needle EMG of the diaphragm: technique description and case
report. Muscle & Nerve 2008;38:1623-1626.
4. Chiodo A, Goodmurphy C, Haig A. Diaphragm needle placement
techniques evaluated in cadaveric specimens. Arch Phys Med Rehabil
2006;87:1150-1152.
5. Goodgold J, editor. Anatomical Correlates of Clinical
Electromyography. 2nd ed. Baltimore: Williams and Wilkins; 1984.
p.41
6. Koepke GH, Smith EM, Murphy AJ, Dickinson DG. Sequence
of action of the diaphragm and intercostal muscles during respiration. I. Inspiration. Archives of Physical Medicine & Rehabilitation
1958;39:426-430.
7. Saadeh PB, Crisafulli CF, Sosner J, Wolf E. Needle electromyography
of the diaphragm: a new technique. Muscle Nerve 1993;16:15-20.
Figure 3 Ultrasound guided needle electromyography of the diaphragm.
3(A): The transducer is initially placed perpendicular to the ribs, and the
different layers of tissue are identified: subcutaneous tissue (SC), two
layers of intercostal muscles (IC) spanning the ribs, diaphragm (D), and
pleura (P) which is just coming in to the field of view with inspiration. 3(B):
The transducer is then aligned parallel to the ribs, overlying the intercostal
space. As the patient takes a deep inspiration, the bright shadow of the
lung is seen coming into the field of view from the superolateral direction,
displacing the diaphragm and underlying liver. 3(C): The needle is inserted parallel to the long axis of the transducer under real time ultrasound
guidance until the needle tip (arrow) enters the diaphragm. The left side
of the image is cephalad.
15
Myasthenia Gravis – Management of
Myasthenic Crisis and Perioperative Care
Ted M. Burns, MD
Vern C. Juel, MD
Associate Professor of Neurology
Department of Neurology
University of Virginia
Charlottesville, Virginia
Associate Professor of Neurology
Duke University
Department of Medicine
Durham, North Carolina
Introduction
Myasthenic crisis is defined as myasthenic weakness leading to
respiratory failure requiring intubation and mechanical ventilation
or delayed postoperative extubation for more than 24 hours due
to myasthenic weakness.6,23 Approximately 15-20% of myasthenia
gravis (MG) patients experience crisis at some time during the
course of their disease. Respiratory failure caused by myasthenic
weakness has historically represented the “gravis” of MG, with
60-80% mortality reported in the first half of the 20th century.4,47
With advances in critical care and treatment, myasthenic crisis
mortality rates have dropped to < 5%.2,48
Although the diagnosis of MG is often known at the time of myasthenic crisis, some undiagnosed patients may develop crisis in
the setting of medical illnesses or surgical procedures. When such
undiagnosed patients present with respiratory failure associated
with extraocular and bulbar weakness, the differential diagnosis
might include Guillain-Barré syndrome, tick paralysis, botulism,
Lambert-Eaton myasthenic syndrome, organophosphate intoxication, and brainstem ischemia. A clinical diagnosis of MG may be
supported by edrophonium testing; by electrophysiological studies,
including repetitive nerve stimulation studies and single-fiber electromyography; and by acetylcholine receptor and muscle-specific
receptor tyrosine kinase (MuSK) antibody testing.23
This manuscript explores the critical muscles, clinical manifestations, and management of patients with myasthenic respiratory
failure. It also focuses on risk factors, complications, weaning
criteria, and perioperative care.
CRITICAL MUSCLES INVOLVED IN MYASTHENIC
VENTILATORY FAILURE
Respiratory failure in myasthenic crisis develops from critical
weakness involving respiratory muscles, upper airway muscles, or
both muscle groups. Respiratory muscles of inspiration include
the diaphragm and external intercostals, with the scalene and sternocleidomastoid muscles acting as accessory inspiratory muscles.
Exhalation in quiet breathing occurs with passive recoil of the
lungs, and may be augmented by contractions of the abdominal
muscles and the internal intercostals. Vital capacity and negative
inspiratory force are ventilatory indices that reflect the strength of
inspiratory muscles. Positive expiratory force measurements reflect
the strength of expiratory muscles. Compared with vital capacity,
maximal inspiratory and expiratory force measurements may be
more sensitive indices of respiratory muscle function in patients
with MG.23, 33
CLINICAL MANIFESTATIONS OF EVOLVING MYASTHENIC
CRISIS
Patients experiencing an MG exacerbation leading to crisis can deteriorate quickly, and thus, warrant close observation. For example,
68% of patients in one series (44 patients with 63 crises) needed
mechanical ventilation within 1 to 3 days of the start of deterioration. This illustrates the importance of closely monitoring patients
at risk.7
16
Myasthenia Gravis – Management of Myasthenic Crisis and Perioperative Care
A focused history and examination that assess ventilatory status and
the muscles of the head and neck region are essential.23 Features
of impending myasthenic crisis include severe bulbar weakness,
increased respiratory rate due to decreased tidal volumes, marginal
vital capacity (i.e., less than 20 mL/kg), weak cough with difficulty
clearing secretions, and paradoxical breathing while supine. Serial
vital capacity measurements and peak inspiratory and expiratory
pressures are customarily used to monitor ventilatory capacity in
impending crisis.
To establish the timing of intubation, the “40/30/20” guide
(vital capacity < 20mL/kg; peak inspiratory pressure < -30 cm
H20; peak expiratory pressure < 40 cm H20) may be helpful.8
Results must be compared to prior readings to identify trends,
and they must also be placed in the proper clinical context.
These indices have notable limitations; for example, when there
is significant bulbar weakness, measurements may be limited by
difficulty sealing the lips around the spirometer mouthpiece or
by an inability to seal the nasopharynx. Furthermore, vital capacity measurements may not reliably predict respiratory failure
in MG.41
Other indicators that suggest the need for intubation include
evidence of fatigue with increasing tachypnea and declining tidal
volumes, hypoxemia despite supplemental oxygen administration,
hypercapnea, and difficulty with secretions. Many patients initially
maintain partial pressure of carbon dioxide in the blood (PaCO2)
in the range of 35 mm Hg because of a subjective sense of dyspnea
with low tidal volume, or because of hypoxia from atelectasis and
increasing dead space. When the PaCO2 begins to rise in this
setting, respiratory failure may be imminent.22,48
Patients with features of impending crisis should be admitted to an
intensive care unit and monitored closely.39 Patients should receive
nothing by mouth to prevent aspiration. In acute respiratory failure
due to myasthenic crisis, noninvasive mechanical ventilation with
bi-level positive pressure ventilation (BiPAP) may circumvent the
need for intubation in myasthenic patients who have not developed
overt hypercapnea (PaCO2 > 50 mm Hg).38
Bulbar manifestations usually accompany respiratory weakness due
to MG, and patients will often have flaccid dysarthria, dysphagia,
and chewing fatigue.48 They may exhibit facial weakness with
difficulty holding air within the cheeks. Jaw closure is sometimes
weak. Tongue weakness may be assessed with protrusion of the
tongue into each cheek. Neck muscle weakness is a very common
accompaniment of crisis. For example, of the 73 episodes of myasthenic crisis at Columbia Presbyterian Medical Center from
1983 to 1994, 92% of patients had neck weakness at the time
of intubation.48
Very rarely, vocal cord abductor paralysis may cause laryngeal
obstruction with associated stridor.9,44 When upper airway dysfunction due to oropharyngeal and laryngeal muscle weakness
compromises respiration, tidal volume and vital capacity may be
deceptively normal. Direct laryngoscopy may be useful to demon-
AANEM Course
strate vocal cord paralysis when bulbar myasthenic findings are not
otherwise overt.9
RESPIRATORY MANAGEMENT OF THE PATIENT IN
MYASTHENIC CRISIS
Nasotracheal tubes are more comfortable than orotracheal tubes,
therefore nasotracheal intubation is preferred. Mechanical ventilation is started using intermittent mandatory ventilation (IMV) or
a synchronized IMV mode with additional positive end-expiratory
pressure or pressure support to reduce alveolar collapse and atelectasis.23 The duration of ventilator requirement is often relatively
prolonged in myasthenic crisis, with most patients requiring mechanical ventilation for nearly 2 weeks.43
Predictors of prolonged intubation (> 2 weeks) include preintubation serum bicarbonate ≥ 30 mg/dL, vital capacity < 25 mL/
kg within 6 days of initial intubation, and age over 50 years.48
For patients requiring more than 2 weeks of mechanical ventilation, a tracheostomy should be considered; the procedure decreases the risk of tracheolaryngeal injury related to prolonged
intubation, facilitates suctioning of oropharyngeal secretions,
reduces dead space, and is often more comfortable for chronically
ventilated patients.31
Aggressive respiratory treatment—including suctioning, intermittent positive-pressure breathing, bronchodilator treatments, sighs,
and chest physiotherapy—may reduce prolonged respiratory complications of atelectasis and pneumonia, and shorten periods of
mechanical ventilation and intensive care.49
RISK FACTORS AND PRECIPITATING FACTORS OF
MYESTHENIC CRISIS
Approximately 15-20% of MG patients experience a crisis; of
these, an estimated 33% will have a second episode.7,43,48 Risk
factors are shorter duration of disease, history of previous crisis,
thymoma, and anti-MuSK antibodies. Crisis usually occurs early
in the disease course.7,40,48 For example, a recent case series from
Columbia Presbyterian Medical Center reported a mean interval
between symptom onset and myasthenic crisis of 8 months (range
0 to 22 years);48 53% of patients experienced the first crisis within
1 year of symptom onset, and 21% during the second year. Other
series show longer intervals. A series in Leipzig, Germany, found a
mean interval of 37 months (range 0 to 18 years).
The prevalence of thymoma is greater in MG patients who experience
crisis than in those who do not. For example, approximately one-third
of patients in the Columbia Presbyterian cohort had thymoma—a
figure higher than the overall prevalence of 10-15% in MG.48 Patients
with anti-MuSK antibodies may also have a higher risk of crisis.35,50
The most common identifiable precipitants of myasthenic crises
are infection, aspiration, change in medication (e.g., tapering immunosuppressants), and surgery.7,40,43,45,48,49 Bacterial pneumonia,
AANEM Course
Critical Care
for example, was a precipitant in 16% of cases in the Columbia
Presbyterian cohort; viral and bacterial upper respiratory infections
were identified in another 14%.48 Other noteworthy precipitating
factors include sepsis and pregnancy.
Corticosteroid-related exacerbations of MG may follow initial treatment with steroids and result in transiently increased myasthenic
weakness. Increased weakness usually begins within 1 to 2 weeks
after beginning drug therapy and lasts up to 1 week before strength
improves. Patients at highest risk are those with more severe bulbar
and generalized MG. Those with marginal respiratory or bulbar
muscle function may lapse into crisis after starting steroids and
should be observed carefully for the first 2 weeks.
Excessive dosing of cholinesterase inhibitors, such as pyridostigmine, can potentially increase weakness due to depolarization
blockade at functionally compromised neuromuscular junctions in
MG. The muscarinic effects of cholinesterase inhibitors may also
increase oropharyngeal and bronchopulmonary secretions that can
obstruct the airway and be aspirated.23 With limited therapeutic
options before the widespread use of immunotherapy, some patients in myasthenic crisis experienced a “cholinergic crisis” due to
excessive dosing of cholinesterase inhibitors.
In addition to weakness indistinguishable from the underlying myasthenic crisis, signs of cholinergic crisis include muscle fasciculations, miosis, excessive lacrimation, salivation, bronchial secretions,
abdominal cramping, diarrhea, diaphoresis, and bradycardia.
Cholinergic crisis is now rare.48 It is common practice to avoid
repeated dose escalations of cholinesterase inhibitors in impending
myasthenic crisis and to discontinue the use of cholinesterase inhibitors following intubation. These approaches reduce muscarinic
complications and facilitate an uncontaminated observation of the
response to immune modulation with plasma exchange (PEX) or
intravenous immunoglobulin (IVIg). Table 1 lists some commonly
prescribed drugs that can exacerbate MG.
TREATING MYASTHEIC WEAKNESS, INCLUDING
MYASTHEIC CRISIS
PEX is an effective short-term treatment for myasthenic crisis, and is
used to prepare symptomatic MG patients for surgery.3,7,11,16,27,36,37,48
For patients in crisis, many centers perform a series of 5 to 6 exchanges of 2-3 L every other day. Fewer exchanges (e.g., 3) are
typically prescribed for surgery preparation. Onset of improvement
varies, but generally begins within 2 to 3 days. Improvement in
strength following PEX is only temporary and lasts several weeks
at best unless an immune suppressant agent is used. Many of the
complications of PEX (e.g., venous thrombosis, infection, and
pneumothorax) are associated with large-bore central venous catheters or with the large volume shifts that occur during procedures
(e.g., hypotension, bradycardia, and congestive heart failure).
IVIg is an alternative short-term immunomodulating treatment
for myasthenic exacerbations or crises. It is also used for surgi-
17
Table 1
Drugs that worsen myasthenic weakness
Neuromuscular blocking agents
Antibiotics
Aminoglycosides, particularly gentamycin
Macrolides, particularly erythromycin and azithromycin
Cardiovascular agents
Beta-blockers
Calcium channel blockers
Procainamide
Quinidine
Quinine
Corticosteroids
Magnesium salts
Antacids, laxatives, intravenous tocolytics
Iodinated contrast agents
D-Penicillamine
cal preparation in patients who are poor candidates for PEX due
to vascular access problems or septicemia.14,20 A randomized,
controlled trial of IVIg at 1.2 or 2.0 gm/kg over 2 to 5 days in
myasthenic exacerbations and crises demonstrated comparable efficacy, but the sample size was relatively small.14 In a retrospective
multicenter study of myasthenic crisis, PEX facilitated extubation
at 2 weeks and improved 1-month functional outcome more than
IVIg.37 In both studies however, patients treated with PEX experienced a higher rate of cardiovascular and infectious complications.
Treatment failures with IVIg that subsequently responded to PEX
have been reported.46
Chronic, oral immunosuppressant medications (e.g., azathioprine)
do not produce improved strength for weeks to months after a
therapeutic dosage is reached; they are therefore ineffective for
the acute treatment of myasthenic crisis or exacerbation. Chronic
immunosuppression, on the other hand, will decrease the likelihood of recurrence of crisis.24,42 A center in Hungary, for instance,
treated myasthenic crisis patients with corticosteroids only during
their intensive care unit stay. After 1997, however, patients were
started on azathioprine and prednisolone at the time of their
crisis. Both oral medications were continued after hospitalization
until pharmacological remission. Prednisolone was then gradually
tapered. This practice of daily oral immunosuppression during and
following myasthenic crisis dramatically reduced the rate of recurrent crisis from 74% to 19%.42
Cholinesterase inhibitors treat symptoms of MG but do not alter
the autoimmune attack of the postsynaptic acetylcholine receptor
complex. For this reason, and because of their potential for increased
weakness due to depolarization blockade and more secretions, they
are generally discontinued upon intubation.8,23 After several days,
when patients exhibit a definite response to immune modulation
(PEX or IVIg), enteral pyridostigmine may be restarted at a low
18
Myasthenia Gravis – Management of Myasthenic Crisis and Perioperative Care dose (30 mg q 8 hours) to treat symptoms. In all assessments of
myasthenic patients approaching or experiencing crisis, the time of
the assessment in relation to the last dose of cholinesterase inhibitor should be noted, since this may affect the measured strength or
ventilatory index.23
COMPLICATIONS OF MYASTHENIC CRISIS
The main causes of mortality in myasthenic crisis are medical complications associated with the crisis itself and its treatment.2,7,15,48
Fever, pneumonia, atelectasis, diarrhea, bronchitis, depression,
and anemia requiring transfusion are relatively common complications.7,28, 48 Sepsis and cardiac arrhythmias or failure are particularly
serious complications during crisis.2,7,48 Hospital mortality rates in
MG crisis are approximately 5%.2,7,45,48
Patients with crisis and fever should be evaluated with appropriate
chest imaging and cultures for infections, particularly bronchopulmonary. Aggressive respiratory treatment may reduce prolonged
complications of atelectasis and pneumonia, and shorten periods
of mechanical ventilation and intensive care.49 Because Clostridium
difficile enterocolitis is a complication of broad-spectrum antibiotic
therapy, caution regarding antibiotic treatment should be exercised
in the absence of documented infection. Medications that may
increase myasthenic weakness (Table 1) should be discontinued
and avoided.19
WEANING CRITERIA
After patients exhibit a clear trend of improved respiratory muscle
strength (i.e., negative inspiratory force greater than 20 cm H2O,
positive expiratory force greater than 40 cm H2O, vital capacity
greater than 10 mL/kg), weaning trials should begin.31,32 The initial
goal should be to eliminate mandatory ventilations, then to reduce
the amount of pressure support by about 2 cm H2O every 3 hours,
as tolerated.
The weaning trial should end if patients develop signs of respiratory
fatigue, including shallow, rapid respirations, diaphoresis, tachycardia, or agitation. Intubated myasthenic patients with significant
residual bulbar weakness may exhibit favorable respiratory parameters (vital capacity, negative inspiratory force, positive expiratory
force) but retain the potential for significant upper airway dysfunction when the stenting effect of the nasotracheal or orotracheal
tube ends upon extubation.23,43 For this reason, clinical assessment
of surrogate bulbar muscles is as important as respiratory parameters. It has been proposed that extubation can be attempted when
patients are breathing comfortably, do not become fatigued, have
a force vital capacity ≥ 15 mL/kg, and have a negative inspiratory
force of ≥ -20 cm H20.49
A recent study from the Mayo Clinic found that male gender, previous crisis, atelectasis, and intubation for more than 10 days were all
associated with failure to extubate.43 Reintubation after extubation
is relatively common following crisis.43,40 In the Mayo Clinic study,
AANEM Course
26% of extubated MG patients required reintubation. In these patients, the need for reintubation could be predicted based on lower
pH and vital capacities at the time of extubation, BiPAP use after
extubation, and atelectasis.43 In another series, extubation failure
occurred 27% of the time.40 Median time to reintubation was 36
hours. Older age, atelectasis, and pneumonia were associated with
extubation failure.
PERIOPERATIVE CARE
Myasthenic crises may occur in the context of surgical procedures
and manifest as prolonged postoperative intubation. Prior to the
common use of preoperative PEX, for example, nearly one-third of
myasthenic patients undergoing transsternal thymectomy required
supported ventilation for 3 days or more postoperatively.51 In a
later series, 37 of 51 transcervical-transsternal “maximal” thymectomy patients received preoperative plasmapheresis to optimize
clinical status; approximately 25% of them needed postoperative
ventilatory support for 6 hours or longer.34
Patients with preoperative respiratory and oropharyngeal weakness, whether overt or masked by cholinesterase inhibitors, are at
particularly high risk for postoperative respiratory complications.21
Risk factors for postsurgical (especially post-thymectomy) extended
ventilation vary among case series. This is due, in part, to different
pre- and perioperative management, surgical techniques, and MG
disease severities. Taken together, however, studies indicate that
poor preoperative respiratory condition (e.g., pulmonary function
test performance) and disease (e.g., bulbar) status17,18,29,34,51 signify
increased the risk for extended ventilation.
Preoperative PEX in patients with bulbar and generalized myasthenia
has reduced postoperative time on mechanical ventilation and in the
intensive care unit.12 In a study of thymectomy patients with an
undetectable level of myastheic weakness, PEX treatment prior to
surgery eliminated the need for postoperative ventilation or reintubation and reduced the mean length of hospital stay to 5 days.10 IVIg
has also been used to prepare patients for thymectomy, although the
time to maximal response varies (range 3 to 19 days).20
To prevent delayed postoperative extubation or reintubation, PEX
(or IVIg) should be performed in patients with respiratory, bulbar,
or generalized weakness prior to surgery. For patients who are poor
PEX candidates due to difficult vascular access, IVIg may achieve
a similar improvement in strength. When in doubt, preoperative
pulmonary function testing may help document the function of
respiratory and upper airway muscles. This author typically performs 3 to 5 preoperative PEX treatments in patients with bulbar
or generalized weakness, or with abnormal pulmonary function
studies relating to MG.
The last PEX should ideally be performed 24 to 48 hours prior
to surgery to allow for repletion of coagulation factors and more
time for the treatment effects of PEX to take hold. Cholinesterase
inhibitors should be tapered concurrently so that true myasthenic
weakness is not masked and the risk for cardiac arrhythmias relat-
AANEM Course
Critical Care
ing to vagal effects is minimized.21 With adequate preoperative
PEX preparation, use of cholinesterase inhibitors and associated
cholinergic risks may be eliminated. Post-thymectomy pain control
and ventilatory function may be improved by administration of
epidural morphine.26
A number of anesthesia-related considerations are specific to
MG. In brief, MG patients generally demonstrate relative resistance to depolarizing neuromuscular blockers (e.g., succinylcholine) and sensitivity to nondepolarizing neuromuscular blockers
(e.g., vecuronium, atracurium).5,13,25 Long-acting nondepolarizing
muscle relaxants, such as pancuronium should be avoided.1,13 Many
inhaled anesthetic agents, such as isoflurane and sevoflurance, cause
neuromuscular junction depression that can magnify weakness in
patients with MG.1,30 Asymptomatic MG patients (e.g., in remission) can also demonstrate sensitivity to nondepolarizing agents
and volatile anesthetics.13, 30
SUMMARY
The outlook for myasthenic patients experiencing crisis has improved markedly over the past half century. With timely recognition, respiratory support, and appropriate immunotherapy, those
experiencing crisis or undergoing surgical procedures should incur
minimal morbidity and mortality.23
REFERENCES
1. Abel M, Eisenkraft JB. Anesthetic implications of myasthenia gravis. Mt
Sinai J Medicine 2002;69:31-37.
2. Alshekhlee A, Miles JD, Katirji B, Preston DC, Kaminski H. Incidence
and mortality rates of myasthenia gravis and myasthenic crisis in US
hospitals. Neurology 2009;72:1548-1554.
3. Antozzi C, Gemma M, Regi B, et al. A short plasma exchange protocol
is effective in severe myasthenia gravis. J Neurol 1991;238:103-107
4. Ashworth B, Hunter AR. Respiratory failure in myasthenia gravis. Proc
Roy Soc Med 1971;64:489
5. Baraka A, Taha S, Yazbeck V, Rizkallah P. Vecuronium block in the
myasthenic patient. Anaesthesia 1993;48:588-590.
6. Bedlack RS, Sanders DB. On the concept of myasthenic crisis. J Clin
Neuromuscul Dis 2002;4:40-42
7. Berrouschot J, Baumann I, Kalischewski P, Sterker M, Schneider D.
Therapy of myasthenic crisis. Crit Care Med 1997;25:1228-1235
8. Chaudhuri A, Behan PO. Myasthenic crisis. QJM 2009;102:97-107.
9. Cridge PB, Allegra J, Gerhard H. Myasthenic crisis presenting as isolated vocal cord paralysis. Am J Emerg Med 2000;18:232-233
10. Cumming WJK, Hudgson P. The role of plasma phoresis in preparing patients with myasthenia for thymectomy. Muscle Nerve
1986;9:S155
11. Dau PC, Lindstrom JM, Cassel CK, et al. Plasmapheresis and immunosuppressive durg therapy in myasthenia gravis. New Engl J Med
1977;297:1134-1140
12. d’Empaire G, Hoaglin DC, Perlo VP, et al. Effect of prethymectomy
plasma exchange on postoperative respiratory function in myasthenia
gravis. J Thorac Cardiovasc Surg 1985;89:592-596
13. Enoki T, Naito Y, Hirokawa Y, et al. Marked sensitivity to pancuronium in a patient without clinical manifestations of myasthenia
gravis. Anesth Analg 1989;69:840-842.
19
14. Gajdos P, Chevret S, Clair B, Tranchant C, Chastang C, Myasthenia
Gravis Clinical Study Group. Clinical trial of plasma exchange and
high-dose intravenous immunoglobulin in myasthenia gravis. Ann
Neurol 1997;41:789-796
15. Gracey DR, Divertie MB, Howard FM. Mechanical ventilation for respiratory failure in myasthenia gravis. Mayo Clin Proc 1983;597-602
16. Gracey DR, Howard FM, Divertie MB. Plasmapheresis in the treatment of ventilator-dependent myasthenia gravis patients: report of
four cases. Chest 1984;8:739-743
17. Gracey DR, Divertie MB, Howard FM Jr, Payne WS. Postoperative
respiratory care after transsternal thymectomy in myasthenia gravis.
A 3-year experience in 53 patients. Chest 1984;86:67-71.
18. Grant RP, Jenkins LC. Prediction of the need for postoperative mechanical ventilation in myasthenia gravis: thymectomy compared to
other surgical procedures. Can Anaesth Soc J 1982;29:112-116.
19. Howard JF. Adverse drug effects on neuromuscular transmission.
Semin Neurol 1990;10:89-102
20. Huang C-S, Hsu H-S, Kao K-P, Huang M-H, Huang B-S. Intravenous
immunoglobulin in the preparation of thymectomy for myasthenia
gravis. Acta Neurol Scand 2003;60:1805-1810
21. Jaretzki A, Aarli JA, Kaminski HJ, Phillips LH, Sanders DB.
Preoperative preparation of patients with myasthenia gravis forestalls
postoperative respiratory complications after thymectomy. Ann
Thorac Surg 2003;1068
22. Juel VC, Bleck TP. Neuromuscular disorders in critical care. In:
Shoemaker WC, Ayers SM, Grenvik ANA, Holbrook PR, eds.
Textbook of Critical Care, Fourth Edition. New York: WB Saunders;
2000:1886-1894
23. Juel VC. Myasthenia gravis: management of myasthenic crisis and
perioperative care. Semin Neurol 2004;24:75-81.
24. Juel VC. Myasthenic crisis: smoother sailing ahead. Eur J Neurol
2009;16:775-776.
25. Kim JM, Mangold J. Sensitivity to both vecuronium and neostigmine in
a sero-negative myasthenic patient. Br J Anaesth 1989;63:497-500.
26. Kirsch JR, Diringer MN, Borel CO, et al. Preoperative lumbar epidural
morphine improves postoperative analgesia and ventilatory function
after transsternal thymectomy in patients with myasthenia gravis.
Crit Care Med 1991;19:1474-1479
27. Kornfield P, Ambinder EP, Papatestas AE, Bender AN, Genkins
G. Plasmapheresis in myasthenia gravis: controlled study. Lancet
1979;2(8143):629
28. Lacomis D. Myasthenic crisis. Neurocrit Care 2005;03:189-194.
29. Leventhal SR, Orkin FK, Hirsh RA. Prediction of the need for postoperative mechanical ventilation in myasthenia gravis. Anesthesiology
1980;53:26-30
30. Lumb AB, Calder I. ‘Cured’ myasthenia gravis and neuromuscular
blockaded. Anaesthesia 1989;44:828-830.
31. Mayer SA, Thomas CE. Therapy of myasthenic crisis [Letter]. Crit
Care Med 1997;25:1136
32. Mayer SA. Intensive care of the myasthenic patient. Neurology
1997;48(Suppl 5):S70-S75
33. Mier-Jedrzejowicz AK, Brophy C, Green M. Respiratory muscle function in myasthenia gravis. Am Rev Respir Dis 1988;138:867-873
34. Naguib M, El Dawlatly AA, Ashour M, Bamgboye EA. Multivariate
determinants of the need for postoperative ventilation in myasthenia
gravis. Can J Anaesth 1996;43:1006-1013.
35. Nemoto Y, Kuwabara S, Misawa S, et al. Patterns and severity of neuromuscular transmission failure in seronegative myasthenia gravis. J
Neurol Neurosurg Psych 2005;76:714-718.
36. Pinching AJ, Peters DK. Remission of myasthenia gravis following
plasma exchange. Lancet 1976;2(8000):1373-1376
20
Myasthenia Gravis – Management of Myasthenic Crisis and Perioperative Care
37. Qureshi AI, Choundry MA, Akbar MS, et al. Plasma exchange
versus intravenous immunoglobulin treatment in myasthenic crisis.
Neurology 1999;52:629-632
38. Rabinstein A, Wijdicks EFM. BiPAP in acute respiratory failure due to
myasthenic crisis may prevent intubation. Neurology 2002;1647-1649
39. Rabinstein AA, Wijdicks EFM. Warning signs of imminent respiratory failure in neurological patients. Semin Neurol 2003;23:97-104
40. Rabeinstein A, Mueller-Kronast N. Risk of extubation failure in patients with myasthenic crisis. Neurocrit Care 2005;03:213-315.
41. Rieder P, Louis M, Jolliet P, Chevrolet JC. The repeated measurement
of vital capacity is a poor predictor of the need for mechanical ventilation in myasthenia gravis. Int Care Med 1995;21:663-668
42. Rózsa C, Mikor A, Kasa K, Illes Z, Komoly S. Long-term effects of
combined immunosuppressive treatment on myasthenic crisis. Eur J
Neurol 2009;16:796-800.
43. Seneviratne J, Mandrekar J, Wijdicks EFM, Rabinstein AA. Predictors of
extubation failure in myasthenic crisis. Arch Neurol 2008;65:929-933.
44. Schmidt-Nowara WW, Marder EJ, Feil PA. Respiratory failure in myasthenia gravis due to vocal cord paresis. Arch Neurol 1984;41:567-568
45. Soleimani A, Moayyeri A, Akhondzadeh S, Sadatsafavi M, Shalmani
HT, Soltanzadeh A. Frequency of myasthenic crisis in relation to
thymectomy in generalized myasthenia gravis: A 17-year experience.
BMC Neurol 2004;4:1-6.
AANEM Course
46. Stricker RB, Kwiatkowska BJ, Habis JA, Kiprov DD. Myasthenic
crisis: response to plasmapheresis following failure of intravenous
gamma-globulin. Arch Neurol 1993;50:837-840
47. Tether JE. Management of myasthenic and cholinergic crises. Am J
Med 1955;19:740-742
48. Thomas CE, Mayer SA, Gungor Y, et al. Myasthenic crisis: clinical
features, mortality, complications, and risk factors for prolonged
intubation. Neurology 1997;48:1253-1260
49. Varelas PN, Chua HC, Natterman J, et al. Ventilatory care in myasthenia gravis crisis: assessing the baseline adverse event rate. Crit Care
Med 2002;30:2663-2668
50. Wolfe GI, Trivedi JR, Oh SJ. Clinical review of muscle-specific tyrosine
kinase-antibody positive myasthenia gravis. J Clin Neuromuscul Dis
2007;8:217-224.
51. Younger DS, Braun NMT, Jaretzki A, Penn AS, Lovelace RE.
Myasthenia gravis: determinants for independent ventilation after
transsternal thymectomy. Neurology 1984;34:336-340
21
Critical Illness Polyneuropathy and
Critical Illness Myopathy
Shawn J. Bird, MD
Department of Neurology
Director, Electromyography and Neurodiagnostic Labs
University of Pennsylvania
Philadelphia, Pennsylvania
Introduction
The development of severe, acquired neuromuscular (NM) weakness
is common in the intensive care unit (ICU). The two syndromes
that account for the vast majority of cases of acquired weakness in
the ICU are critical illness polyneuropathy (CIP) and an acute myopathy, critical illness myopathy (CIM). These disorders contribute
significantly to prolonged ventilator dependence, as well increased
morbidity, costs, and persistent neurologic deficits. The mean increase in ventilator days is 11.6 days in a patient with one of these
disorders as compared to those without CIP or CIM.13
There are numerous potential causes of NM weakness in the
ICU. They are generally separated into disorders that produce
weakness severe enough to result in ICU care, such as myasthenia
gravis or the Guillain-Barré syndrome. These disorders should be
differentiated from disorders that develop as a consequence of
critical illness, CIP, and CIM. In the ICU setting, considerations
of acquired weakness should also include severe hypokalemia, hypermagnesemia, or prolonged NM blockade. The latter should be
considered in those who have received nondepolarizing NM blocking agents, particularly if there is renal or hepatic disease where the
active metabolites may persist.4
sis period and half (50%) of those developed CIP, CIM, or features
of both, most by day 14 of illness. Of those affected, 10% were
found to have CIP, 10% had CIM, and 80% had both.
Stevens and colleagues performed a systematic review of 24 studies
(19 prospective) of critically ill patients who developed CIP and/or
CIM.27 Most of these studies avoided the problem of distinguishing between the two disorders (see below) by combining them as
an endpoint. Of the total 1421 patients included in the studies,
655 (46%) developed CIP, CIM, or both.
INCIDENCE AND RISK FACTORS
Three large prospective studies (61 to 95 patients each) have
examined risk factors in critically ill patients for the development of NM weakness.2,14,15 The studies concur that measures of
illness severity (Acute Physiology and Chronic Health Evaluation
(APACHE) III score, presence of systemic inflammatory response
syndrome [SIRS], or organ failure assessment scores) correlate with
the development of CIP/CIM. The likelihood of developing CIP
and/or CIM is strongly influenced by the severity of illness. For
those with a high APACHE III score (>85) and those with the
presence of sepsis at the time of study entry (day four of mechanical ventilation), the probability of developing CIP/CIM by 30 days
was 72%. This compares to only 8% in patients with low APACHE
III scores (<70) and no sepsis.15 This is almost a 10-fold higher risk
in severely ill patients.
In general, the incidence of CIP and/or CIM appears to be about
50% in patients who are critically ill in the ICU for more than a
week.14,15,19,23,27,31 This has been demonstrated in small, single-site
prospective studies, as well as larger multicenter studies. Khan and
colleagues recently conducted a prospective cohort study of patients
with severe sepsis in the ICU.18 Twenty patients survived the analy-
The causative association between high-dose corticosteroids, nondepolarizing NM blocking agents (NMBAs), and sedative drugs
like propofol with acquired ICU weakness, particularly for CIM, is
likely but not established. The first reports of CIM were in patients
with status asthmaticus treated with high dose corticosteroids and
NMBAs. Many of the early reports of critically ill patients with
22
Critical Illness Polyneuropathy and Critical Illness Myopathy
severe CIM emphasized the prodromal use of corticosteroids and
NMBAs.12,17 However, the results from prospective trials have
been inconsistent. Of the reports that detailed this information,
there was no significant univariate association with corticosteroids, NMBAs, midazolam, or aminoglycosides.27 Multivariable
analysis identified a relationship between corticosteroids and CIP/
CIM in one of the two studies that addressed this. In this study,
the use of corticosteroids was a significant risk factor (Operations
Room [OR] 14.9).14 Similarly, one of three studies that performed
multivariable analysis showed an association of CIP/CIM with
NMBAs (OR 16.32).16 The studies that did not show an association were limited, due to the relatively small number of patients
included that had received substantial doses of corticosteroids and/
or NMBAs.
DIFFERENTIATING CIP AND CIM
There is a large cohort of patients in the ICU who have clinical
and electrodiagnostic (EDX) features common to both disorders.
These patients are not as easily classified as purely CIP or CIM.4,5
The clinical presentation of both disorders is dominated by limb
weakness that develops in the ICU, usually accompanied by a delay
in weaning the patient from mechanical ventilation.
On electrophysiologic examination, one typically finds features
common to both disorders. This includes reduced compound
muscle action potential (CMAP) amplitudes on nerve conduction studies (NCSs) and the presence of fibrillation potentials on
needle electromyography (EMG) examination. Sensory NCSs are
often hampered by technical factors (limb edema and electrical
noise from the ICU equipment), or the sensory responses may be
low amplitude due to preexisting neuropathies. Furthermore, the
assessment of motor unit action potential (MUAP) morphology
and recruitment is often limited by the patient’s encephalopathy
or sedation. Direct muscle stimulation and measures of the CMAP
duration may be helpful in identifying CIM, but specific diagnostic
criteria for these techniques have not been formally established. Of
course, establishing the presence of CIM by direct muscle timulation or prolonged CMAP amplitudes does not address the presence
or absence of CIP. Despite the limitations in differentiating CIM
from CIP, suggested criteria have been proposed (Tables 1 and 2).
In addition to the technical considerations that may limit
these studies, the risk factors for the two disorders overlap
and many patients have a variable combination of both disorders.5,18 Nonetheless, the recognition that the cause of acquired limb weakness and failure to wean in the ICU is due
to CIP, CIM, or a combination of both, is helpful to the
ICU staff.
CIP
A sensory motor axonal neuropathy commonly develops in the
ICU. This was first described by Bolton and colleagues8 who gave
it the name critical illness polyneuropathy, or CIP. They described
AANEM Course
a cohort of patients who, during a period of critical illness with
sepsis and multiorgan failure, developed a severe sensory motor
neuropathy. CIP was convincingly shown to be a distal sensory
and motor axonal neuropathy that could be differentiated from the
Guillain-Barré syndrome on electrophysiologic and morphologic
studies. The clinical, electrophysiologic, and pathologic features
have been detailed by Bolton and collegues.7,9,10,31-33 In the setting
of critical illness, these characteristics define a distinctive form of
acute polyneuropathy.
Clinical features
The clinical features of CIP are similar to other length dependent
neuropathies with distally predominant limb weakness and reduced
reflexes. Difficulty weaning the patient from mechanical ventilation
due to phrenic nerve involvement is common, and is often the
first recognized manifestation of CIP. Muscle atrophy isn’t usually
present until the second or third month of illness, and it parallels
the degree of axonal loss. Sensory loss is usually present distally,
but is difficult to demonstrate. These patients often have coexistent septic encephalopathy or are sedated in the ICU, limiting the
sensory examination that is dependent upon patient responses.
Cranial nerve involvement in CIP is rare and should suggest the
presence of another NM disorder.
An early, illustrative prospective study detailed 43 ICU patients
who had sepsis and multiple organ failure.31 The patients were in
the ICU for a mean of 28 days when evaluated and diagnosed
with septic encephalopathy. Thirty-five percent had clinical findings consistent with neuropathy, defined as distal weakness and
hyporeflexia, or as an inability to wean from the respirator. More
than half (70%) had electrophysiologic evidence of an axonal neuropathy. Only half of those patients survived the ICU stay. Of
Table 1 Suggested diagnostic criteria for critical illness
polyneuropathy7
1. The patient is critically ill (sepsis and multi organ failure, SIRS)
2. Difficulty weaning the patient from mechanical ventilator support
after non neuromuscular causes, such as cardiac and pulmonary
disease, have been excluded
3. Possible limb weakness
4. Electrophysiologic evidence of an axonal sensory and motor
neuropathy
5. Under the appropriate clinical circumstances, other causes of
acute neuropathy should be excluded (i.e., porphyria, acute
massive intoxications from arsenic or thallium, fulminant
vasculitis, etc.)
SIRS = systemic inflammatory response syndrome
AANEM Course
Critical Care
the survivors, the course of recovery followed that expected of
an acute axonal neuropathy.
The prognosis for recovery from CIP is variable, although it is
good for most patients. As with other acute nerve injuries, recovery
depends on the severity of axonal loss and the distance over which
nerve regeneration must occur. Patients who have had only mild to
moderate axonal loss recovered fully over months as a result of collateral sprouting from remaining motor neurons. Those with severe
axonal loss due to CIP may take longer to recover. In these patients,
permanent distal sensory and motor deficits may occur, although
deficits severe enough to preclude ambulation are uncommon.31,32
Electrophysiologic Features
Electrophysiologic studies of CIP are those of an axonal neuropathy.7,9,10,32,33 NCSs are characterized by reduced sensory and motor
response amplitudes. There are no features that suggest demyelination. In
general, conduction velocities and distal motor latencies are not significantly affected. Repetitive nerve stimulation studies of NM transmission
are normal, unless there is persistent pharmacologic NM blockade.
Table 2
myopathy*20
Suggested diagnostic criteria for critical illness
1. The patient has had a variable combination of non-depolarizing
neuromuscular blocking agents, high dose corticosteroids,
and sepsis
2. Clinical features (one or both)
a.
Limb weakness is present
b.
Difficulty weaning the patient from mechanical ventilator
support, and cardiac and pulmonary causes have
been excluded
3. Electrophysiologic studies
a.
Reduced motor responses (CMAP amplitudes < 80% lower
limit of normal in two or more nerve without conduction
block)
b.
Normal repetitive nerve stimulation studies
c.
Needle EMG with short duration, low amplitude motor
unit potentials with early full or normal recruitment, with or
without fibrillation potentials
d.
Demonstration of muscle inexcitability with direct muscle
stimulation techniques
e.
Prolonged CMAP durations (> 9.0 ms)
4. Muscle biopsy that demonstrates myopathy with myosin loss
* For the clinical diagnosis of CIM, patients should have features 1 and 2, 3a and
3b, and one of the following three – 3c, 3d, 3e, or 4.
CIM = critical illness myopathy; CMAP = compound muscle action potentials
EMG = electromyography; SIRS = systemic inflammatory response syndrome
23
Needle EMG examination of limb muscle is often notable for
abnormal spontaneous activity (fibrillation potentials and positive
sharp waves) with the muscle at rest. The degree of abnormal spontaneous activity varies from nothing detectable to profuse. With
voluntary muscle activation of significantly weak muscles, MUAPs
are recruited with an increased recruitment ratio. These needle
EMG findings are consistent with acute denervation.
In those with severe CIP, phrenic NCSs are often absent and
needle EMG examination of the diaphragm can demonstrate
denervation.32
Pathologic Features and Pathophysiology
Sural nerve biopsy and postmortem autopsy studies in patients
with CIP show features of an acute axonal neuropathy. The pathology is consistent with axonal degeneration of both sensory and
motor nerve fibers, with no evidence of significant inflammation
or of primary demyelination.7,8,33
The pathogenesis of CIP is uncertain. Prospective studies have
not supported a causative role of pharmacologic agents.27 No
specific toxin, infectious agents, or nutritional deficiencies have
been identified in CIP. Cytokines and free radicals associated with
SIRS may adversely affect the nerve microcirculation, producing
endoneurial hypoxia and distal axonal degeneration.7 This view
is supported by the finding that critically ill patients with high
APACHE III scores and SIRS are most prone to the development
of CIP.
Sepsis activates humoral responses locally in tissues as antigen
presenting cells that produce pro-inflammatory cytokines such
as tumor necrosis factor, interleukin1, and free radicals. These
interact with adhesion molecules on platelets and endothelial cells
producing platelet fibrin aggregates that reduce capillary flow.
Cytokines released in sepsis have histamine like effects that increase microvascular permeability and produce endoneurial edema.
This may result in endoneurial hypoxia. In addition, an increase
in local tissue nitric oxide may cause arteriolar dilatation, further
reducing capillary flow. The microvascular structures of nerve lack
auto regulation, which may make it particularly vulnerable to
deleterious effects.7
CIM
Clinical Features
As with CIP, the clinical presentation of CIM is that of limb and
respiratory muscle weakness that develops acutely, but is often
difficult to recognize early in the course of disease due to coexistent encephalopathy, sedation, or both. The weakness varies from
mild to complete quadriplegia. The weakness is not in a strictly
length related pattern where distal muscles are weakest, a pattern
typical of CIP and most neuropathies. In patients with CIM,
there is usually as much proximal limb weakness as there is distal.
24
Critical Illness Polyneuropathy and Critical Illness Myopathy
Respiratory muscles are frequently involved, delaying weaning
from mechanical ventilation. Failure to wean from mechanical
ventilation may be the first recognized manifestation. Neck flexor
or facial muscle weakness may be present, but the presence of
ophthalmoparesis should suggest the existence of another disorder.
Sensation is spared, but often cannot be clinically evaluated in an
encephalopathic, sedated, and intubated patient. As with other
myopathies, reflexes are decreased in parallel with the decrease
in strength.
Laboratory and Pathologic Features
The serum creatine kinase (CK) is elevated in less than half of the
reported patients, and is usually only mild.4 One prospective study
in patients with severe sepsis found the mean CK at day 7 was 365
(range 128 to 1397; normal < 250).18
A spectrum of pathological findings, mostly such nonspecific
abnormalities such as myofiber size variability or atrophy (especially of type 2 fibers), are found in CIM. Lymphocytic inflammation and significant muscle fiber necrosis is not seen. Muscle
biopsy may show a characteristic patchy loss of myosin thick
filaments. This is the hallmark pathologic finding of CIM and
has led some to call this disorder “thick filament myopathy.”12
This characteristic pathologic finding of myosin loss can be seen
in up to 50% of those with CIM.21 Even though the diagnosis
of CIM may be strongly supported by such pathological findings, muscle biopsy is invasive and is not routinely performed for
diagnostic confirmation.
Electrophysiology
Motor NCSs in patients with CIM differ from those found
in most myopathies. The motor response CMAP amplitudes
are reduced, or even absent, when recording from distal limb
muscles.5,21,24,25 The motor response amplitudes generally increase during clinical recovery of strength. In many patients,
the CMAP durations are abnormally prolonged (see below).
There is preservation of sensory nerve action potential amplitudes, unless there is coexistent CIP or preexistent neuropathy.
Sensory and motor response conduction velocities, as well as
distal motor and F-wave latencies, are normal. Repetitive nerve
stimulation studies do not show an abnormality of NM transmission.
On EMG examination, abnormal spontaneous activity in the
form of fibrillation potentials and positive sharp waves, is variably present. It is not infrequently seen, but is generally sparse.
Reduced insertional activity may be seen in patients with severe
weakness and markedly reduced CMAP amplitudes, another
feature of reduced muscle membrane inexcitability. 5 With
voluntary muscle activation of significantly weak muscles, one
generally sees small amplitude, short duration MUAPs with an
early recruitment pattern.
AANEM Course
Muscle Membrane Electrical Inexcitability - Direct Muscle
Stimulation
There are several features that are unique to this CIM. The myopathy develops in the setting of critical illness and there are features
that are unlike most other myopathies. The presence of severe
weakness (often quadriplegia) are absent or markedly reduced.
CMAP amplitudes are difficult to reconcile with normal CK values
and minimally abnormal muscle pathology. An acquired disorder
of muscle membrane inexcitability would fit these observations.
There are several lines of evidence indicating that muscle membrane inexcitability plays a role in CIM. These include:
1.
2.
3.
4.
5.
Absent or reduced responses with direct electrical
stimulation of muscle.3,22,24,25,30
Increased CMAP durations.1,26
Muscle fiber conduction velocity is slowed.1,30
All features improve with clinical recovery.1,6
Animal models of these disorders.5,28
Muscle membrane inexcitability can be demonstrated by direct
stimulation of muscle in patients with severe CIM.3,22,24,25,30 In
contrast, muscle is easily excitable by this technique in patients
with CIP and other acute and chronic neuropathies. The muscles
most commonly studied are the tibialis anterior (TA) and the
biceps. In this technique, the peroneal nerve is stimulated at the
fibular head and the CMAP is recorded from the TA muscle. The
stimulating and recording locations for the nerve evoked CMAP
are the same as those used with routine NCS techniques. However,
the active recording electrodes are either a 12 mm subcutaneous
stainless steel electrode, or a concentric needle EMG electrode inserted near the end-plate. Most favor the latter electrode. The direct
muscle stimulation CMAP is performed with the same recording
locations and electrodes. The muscle is directly stimulated with a
monopolar EMG electrode 2 to 5 cm distal to the active recording
electrode away from the endplate region.
This is a semi-quantitative technique without well established
normative values. Using this technique, an absent direct muscle
stimulation CMAP is strongly supportive of CIM. When a direct
muscle stimulation CMAP can be obtained, an amplitude from
the tibialis anterior of less than 2mV with subcutaneous recording
electrodes, or 3 mV with a concentric needle recording electrode
is also consistent with CIM (Bird, personal communication,
2009).25,30 This technique is not helpful in differentiating mild or
moderate myopathy from normal, where there is a relatively preserved direct muscle stimulation CMAP amplitude. Serial studies
using this technique in patients with CIM have shown recovery of
muscle membrane excitability as strength improves and an increase
in CMAP rise.4
Prolonged CMAP duration
An interesting observation in many patients with CIM is that the
CMAP duration is significantly increased, concomitant with a drop
in amplitude.11 During recovery of strength, the CMAP amplitude
AANEM Course
Critical Care
increases and the CMAP duration shortens, with no change in the
distal motor latency.6
Park and colleagues26 reported the first series detailing prolonged
CMAP durations in clinically defined CIM. This retrospective
review of nine patients reported a prolonged distal CMAP duration
in all of the motor nerves studied. For example, the median nerve
distal CMAP durations ranged from 9.2 to 21.4 ms (normal < 7.2
ms). A larger study of 32 patients with CIM also noted prolonged
CMAP durations.1 They found a mean median nerve CMAP
duration of 9.0 ms. This was abnormal (abnormal > 6.8 ms) in
72% of nerves. Similarly, the mean tibial CMAP duration was 9.4
ms. This was abnormal (> 6.2 ms) in 63% of the nerves studied.
However, in this study, only the medial and tibial motor nerves
were studied.
Increased CMAP durations are frequently seen in demyelinating
neuropathies as well.29 However, both groups1,26 have indicated
that there are important differences in the prolonged CMAP durations seen in CIM and demyelinating neuropathies, such as CIDP.
In CIM, the durations of the distal and proximal CMAP are the
same. In many patients with demyelinating neuropathy, the CMAP
with proximal stimulation is considerably longer than the distal
CMAP, reflecting abnormal proximal to distal temporal dispersion. In CIM, other features of demyelination are also absent. The
distal motor latencies are normal and the conduction velocities
are normal or minimally reduced (not less than 80% lower limit
of normal).
Pathophysiology
The mechanism involved in the development of CIM is likely
multifactorial.4,5 The use of nondepolarizing NM blocking agents
and corticosteroids may result in myosin loss and changes in
other structural proteins. Inactivity and sepsis can increase the
ubiquitin proteasomal mediated proteolysis induced by corticosteroids. The up regulation of corticosteroid receptors due to
immobilization, sedation, or NMBAs may increase muscle fiber
susceptibility to the myotoxic effects of steroids. Sepsis may alter
the muscle bioenergetic machinery with unknown deleterious
effects. Impaired muscle membrane excitability probably plays a
more significant role in producing weakness in the acute stage.
Muscle membrane inexcitability is likely due to abnormal sodium
channel inactivation.28
References
1. Allen DC, Arunachalam R, Mills KR. Critical illness myopathy: further
evidence from muscle-fiber excitability studies of an acquired channelopathy. Muscle Nerve 2008;37:14-22.
2. Bednarik J, Vondracek P, Dusek L, et al.Risk factors for critical illness
polyneuromyopathy. J Neurol 2005;252:343-351.
3. Bednarik J, Lukas Z, Vondracek P. Critical illness polyneuromyopathy:
the electrophysiological components of a complex entity. Intensive
Care Med 2003; 29:1505-1514.
25
4. Bird SJ. Critical care: myopathies and disorders of neuromuscular
transmission. In: Brown WF, Bolton CF, Aminoff MJ, editors.
Neuromuscular Function and Disease. Philadelphia: Harcourt-Brace;
2002: p 1507-1520.
5. Bird SJ, Rich MM. Critical illness myopathy and polyneuropathy. Curr
Neurol Neurosci Rep 2002;2:527-533.
6. Bird SJ. Critical care myopathies. In Stalberg E, editor. Clinical
Neurophysiology of Disorders of Muscle and Neuromuscular
Junction. Amsterdam: Elsevier, 2003, p 565-582.
7. Bolton CF. Neuromuscular manifestations of critical illness. Muscle
Nerve 2005;32:140-163.
8. Bolton CF, Gilbert JJ, Hahn AF, Sibbald WJ. Polyneuropathy in critically
ill patients. J Neurol Neurosurg Psychiatry 1984;47:1223-1231.
9. Bolton CF. Electrophysiologic studies of critically ill patients. Muscle
Nerve 1987;10:129-135.
10. Bolton CF, Young GB, Zochodne DW. The neurologic complications
of sepsis. Ann Neurol 1993;33:94-100.
11. Bolton CF. Evidence of neuromuscular dysfunction in the early
stages of the systemic inflammatory syndrome. Intensive Care Med
2000;26:1179-1180.
12. Danon MJ, Carpenter S. Myopathy with thick filament (myosin) loss
following prolonged paralysis with vecuronium during steroid treatment. Muscle Nerve 1991;14:1131-1139.
13. De Jonghe B, Bastuji-Garin S, Sharshar T, et al. Does ICU-acquired
paresis lengthen weaning from mechanical ventilation? Intensive Care
Med 2004;30: 1117-1121.
14. De Jonghe B, Sharshar T, Lefaucher JP, et al. Paresis acquired in
the intensive care unit: a prospective multicenter study. JAMA
2002;288:2859-2867.
15. De Letter MC, Schmitz PI, Visser LH, et al. Risk factors for the development of polyneuropathy and myopathy in critically ill patients. Crit
Care Med 2001;29:2281-2286.
16. Garnacho-Montero J, Amaya-Villar R, Garcia-Garmendia JL, et al.
Effect of critical illness polyneuropathy on the withdrawal from
mechanical ventilation and the length of stay in septic patients. Crit
Care Med 2005;33:349-354.
17. Hirano M, Ott BR, Raps EC, et al. Acute quadriplegic myopathy: a
complication of treatment with steroids, nondepolarizing blocking
agents, or both. Neurology 1992;42: 2082-2087.
18. Khan J, Harrison TB, Rich MM, Moss M. Early development of critical illness myopathy and neuropathy in patients with severe sepsis.
Neurology 2006;67:1421-1425.
19. Lacomis D, Petrella JT, Giuliani MJ. Causes of neuromuscular weakness in the intensive care unit: a study of ninety-two patients. Muscle
Nerve 1998;21:610-617.
20. Lacomis D, Zochodne DW, Bird SJ. Critical illness myopathy: what’s in
a name? Muscle Nerve 2000;23:1767-1772.
21. Lacomis D, Giuliani MJ, Van Cott A, Kramer DJ. Acute myopathy of
intensive care: clinical, electromyographic, and pathological aspects.
Ann Neurol 1996;40:645-654.
22. Lefaucher J-P, Nordine T, Rodriguez P, Brouchard L. Origin of ICU
acquired paresis determined by direct muscle stimulation. J Neurol
Neurosurg Psychiatry 2006;77:500-506.
23. Leijten FSS, Harinck-De Weerd JE, Poortvliet DCJ, De Weerd
AW. Critical illness polyneuropathy in multiple organ dysfunction
syndrome and weaning from the ventilator. Intensive Care Med
1996;22:856-861.
24. Rich MM, Bird SJ, Raps EC, et al. Direct muscle stimulation in acute
quadriplegic myopathy. Muscle Nerve 1997;0:665-673.
25. Rich MM, Teener JW, Raps EC, et al. Muscle is electrically inexcitable
in acute quadriplegic myopathy. Neurology 1996;6:731-736.
26
Critical Illness Polyneuropathy and Critical Illness Myopathy
26. Park EJ, Nishida T, Sufit RL, Minieka MM. Prolonged compound
muscle action potential duration in critical illness myopathy. J Clin
Neuromusc Dis 2004;5:176-183.
27. Stevens RD, Dowdy DW, Michaels RK et al. Neuromuscular dysfunction acquired in critical illness: a systematic review. Intensive Care
Med 2007;33:1876-1891.
28. Teener JW, Rich MM. Dysregulation of sodium channel gating in critical illness myopathy. J Muscle Res Cell Motil 2006;7:291-296.
29. Thaisetthawatkul P, Logigian EL, Herrmann DN. Dispersion of the
distal compound muscle action potential as a diagnostic criterion
for chronic inflammatory demyelinating polyneuropathy. Neurology
2002;59:1526-1532.
AANEM Course
30. Trojaborg W, Weimer LH, Hays AP. Electrophysiologic studies in
critical illness associated weakness: myopathy or neuropathy – a reappraisal. Clin Neurophysiol 2001;12:1586-1593.
31. Witt NJ, Zochodne DW, Bolton CF, et al. Peripheral nerve function in
sepsis and multiple organ failure. Chest 1991;9:176-184.
32. Zifko U, Zipko H, Bolton CF. Clinical and electrophysiological findings in critical illness polyneuropathy. J Neurol Sci 1998;59:186-198.
33. Zochodne DW, Bolton CF, Wells GA, et al. Critical illness polyneuropathy. Brain 1987;10:819-842.