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Nonpoliovirus Poliomyelitis Simulating Guillain-Barré Syndrome
Kenneth C. Gorson, MD;
Allan H. Ropper, MD
Arch Neurol. 2001;58:1460-1464.
ABSTRACT
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Background Paralytic poliomyelitis due to the wild-type poliovirus has been eradicated
in the United States because of effective immunization programs. In the postvaccination
era, most cases are caused by other RNA viruses, such as coxsackievirus or
echovirus. The condition usually begins with a fever and upper respiratory
tract or gastrointestinal tract symptoms that progress to a "paralytic" phase
characterized by limb weakness, areflexia, and, occasionally, respiratory
failure that superficially resemble Guillain-Barré syndrome.
Objective To describe 2 patients with nonpoliovirus poliomyelitis and highlight
the findings on magnetic resonance imaging of the spinal cord to distinguish
these cases from variants of Guillain-Barré syndrome.
Design and Setting Case series from an academic medical center.
Patients Following a viral illness, the patients, aged 35 and 50 years, had painless,
progressive, asymmetrical weakness in the arms followed by respiratory failure
in one patient, and generalized limb weakness in the other patient, reaching
a nadir in 1 week. Both patients had fevers but no signs of meningitis at
onset. Tendon reflexes were absent or reduced in affected regions. The cerebrospinal
fluid findings were as follows: mononuclear leukocyte counts of 100 000
cells/mm3 and 700 000 cells/mm3, respectively,
and the protein level was above 10 g/dL in both patients. Compound muscle
action potential amplitudes were reduced in some nerves with active denervation
in clinically affected muscles, and F-responses were absent but there were
no other demyelinating features. Magnetic resonance imaging showed discrete
T2-weighted signal changes of the ventral horns of the spinal cord, and one
had elevated coxsackievirus titers in the serum. There was little recovery
and significant atrophy in weak muscles after 3 years.
Conclusions The poliomyelitis syndrome still occurs in adults in developed countries.
It has superficial similarities to a motor axonal variant of Guillain-Barré
syndrome but can be distinguished by clinical, cerebrospinal fluid, and, perhaps
specifically, magnetic resonance imaging characteristics.
INTRODUCTION
PARALYTIC poliomyelitis currently results most often from oral polio
vaccination rather than from the wild-type poliovirus, although the latter
still plagues developing countries.1, 2
In the United States, nonvaccine-related cases have been caused by other RNA
viruses, such as coxsackievirus, echovirus, and other enteroviruses.3 The illness usually begins with a fever and upper
respiratory tract or gastrointestinal tract symptoms that progress to a "paralytic"
phase characterized by flaccid, asymmetrical limb weakness, areflexia, and
occasionally, respiratory failure, superficially resembling Guillain-Barré
syndrome (GBS).4, 5 We describe
2 patients with nonpoliovirus poliomyelitis initially diagnosed as having
GBS; in addition to fever and cerebrospinal fluid (CSF) pleocytosis, abnormalities
on magnetic resonance imaging (MRI) of the spinal cord helped distinguish
these cases from the acute motor axonal variant of GBS.
REPORT OF CASES
CASE 1
A 35-year-old man had acute, painless, progressive weakness of the right
hand over 1 day. Within 4 days, the entire right arm was virtually paralyzed
and the left arm became weak. Several days later, the weakness had progressed
to cause bibrachial paralysis and respiratory failure requiring ventilatory
assistance. There were no sensory symptoms, and his cranial nerves, sphincter
function, and legs were unaffected. He had a mild frontal headache and diffuse
arthralgias during the preceding week, without fever or diarrhea. He had received
polio vaccinations as a child, had no contact with recently vaccinated infants
or children, and had not traveled outside the country.
There was a low-grade fever (temperature, 37.8°C) but no meningism.
His mentation, cranial nerves, and legs were normal, but mild weakness was
present in the neck extensor muscles. The right arm and hand, and left deltoid,
infraspinatus, and supraspinatus were paralyzed. There was 3/5 power (Medical
Research Council scale) in the left biceps and triceps, and 4+/5 strength
in the left hand. Sensation was normal. The triceps tendon reflex was trace
and the biceps and brachioradialis reflexes were absent bilaterally. Reflexes
in the legs were normal.
The CSF showed a mononuclear leukocyte count of 100 000 cells/mm3 (56% lymphocytes, 44% neutrophils), a protein level of 10.7 g/dL,
and normal glucose concentration. Results of the complete blood cell count;
liver, kidney, and thyroid function studies; erythrocyte sedimentation rate;
and serum rapid plasma reagin test; human immunodeficiency virus and Lyme
disease titers, and anti-GM1 antibody titers were normal or negative. Bacterial
cultures of the blood, CSF, urine, and sputum were negative for organisms.
Results of urine porphyrin screening were normal. The patient was tentatively
diagnosed as having a variant of GBS and was treated at a local hospital.
There was no immediate improvement in the patient's condition after treatment
with intravenous corticosteroids, plasma exchange, and intravenous immune
globulin, and he was referred to our facility.
Electrodiagnostic studies were performed at our institution 6 weeks
after presentation. The right median compound muscle action potential amplitude
was 0.40 mV (reference range, >4.0 mV); conduction velocity, 58 m/s (reference
range, >50 m/s); distal latency, 5.8 milliseconds (reference range, <4.4
milliseconds); and F-response, absent. The ulnar compound muscle action potential
amplitude was absent, and the peroneal motor potential was normal. The right
median, ulnar, and sural sensory nerve action potentials were normal. Findings
from needle electromyographic examination showed widespread active and chronic
denervation with absent or greatly reduced recruitment in the muscles of the
upper limbs, cervical, and thoracic paraspinal region (Table 1). An MRI of the cervical spine showed an abnormal signal
within the ventral gray matter of the spinal cord (Figure 1).
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Electromyographic Findings for Patient 1*
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Figure 1. Patient 1. A, Sagittal T2-weighted
image of the cervical spinal cord demonstrating an abnormal linear high-signal
lesion in the spinal cord (arrowhead). B, Axial T2-weighted image. Note the
abnormal signal within the ventral gray matter of the cervical spinal cord
(arrowhead).
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He was weaned slowly from the mechanical ventilator over 3 weeks. At
30 months, the patient's right arm remained paralyzed with severe atrophy
of the shoulder girdle, forearm, and hand muscles. The left shoulder girdle
also remained paralyzed with moderate weakness of other left arm and hand
muscles.
CASE 2
A 50-year-old man had a 3-day history of urinary retention, abdominal
cramping, diarrhea, and chills without fever, followed by leg weakness. Within
several days he became lethargic and developed arm weakness. He had received
polio vaccinations as a child, had no contact with recently vaccinated infants
or children, and was not immunodeficient.
He was febrile (temperature, 38.4°C), drowsy and inattentive, dysarthric,
and had a reduced gag reflex; other cranial nerve responses were normal. There
was generalized weakness with 4/5 power in the arm and intrinsic hand muscles,
2/5 strength in the hip muscles, bilateral foot drop (0/5 tibialis anterior),
generalized areflexia except for +1 right biceps reflex, and normal sensation.
Forced vital capacity was 2.1 L (<50% of predicted). He was diagnosed as
having acute GBS and referred to our institution for treatment.
Results of routine laboratory study findings were normal except for
an erythrocyte sedimentation rate of 100 mm/h. The following serological study
findings were also normal or negative: immunofixation, rapid plasma reagin,
cold aggluttins, human immunodeficiency virus, hepatitis B and C virus, Epstein-Barr
virus, Lyme disease, Mycoplasma pneumoniae, Rickettsia, herpes simplex virus 1 and 2 titers, and anti-GM1
antibody titers. Stool culture and serum titers for Campylobacter
jejuni were negative for organisms. Urine porphyrin screening test
results were normal. The CSF findings were as follows: a mononuclear leukocyte
count of 695 000 cells/mm3 (91% lymphocytes, 9% neutrophils),
a protein level of 10.8 g/dL, and a normal glucose level. Bacterial, fungal,
and mycobacterium tuberculosis cultures of the CSF were negative for organisms.
A second lumbar puncture performed 1 week later showed a mononuclear leukocyte
count of 120 000 cells/mm3 (98% lymphocytes, 2% monocytes),
a protein level of 26.1 g/dL, and a glucose level of 0.7 g/dL (3.9 mmol/L).
Oligoclonal bands were not detected and CSF Lyme titer and rapid plasma reagin
results also were negative. Cerebrospinal fluid viral titers, including Epstein-Barr
virus; herpes simplex virus 1 and 2; cytomegalovirus; varicella zoster virus;
coxsackievirus types B1, B2, B3, B4, B5, and B6; echovirus types 4, 9, 11,
and 30; and poliovirus types 1, 2, and 3 were not detected; however, serum
viral titers of coxsackievirus type B4 were elevated (1:256), suggesting recent
infection. Modified barium-swallow esophagogram demonstrated moderate pharyngeal-phase
dysphagia with aspiration of thin liquids.
Four weeks after presentation electrodiagnostic studies showed an ulnar
compound muscle action potential amplitude of 2.6 mV (reference range, >6.0
mV) with a normal conduction velocity and distal latency. The ulnar F-response
was absent. The tibial compound muscle action potential amplitude was 4.6
mV (reference range, >4.0 mV); conduction velocity, 39 m/s (reference range,
>40 m/s), and distal latency, 4.5 milliseconds (reference range, <5.9 milliseconds).
The tibial F-response and H-reflex were absent. The ulnar and sural sensory
nerve action potentials were normal. Findings from a needle electromyographic
examination showed fibrillation potentials, modest reinnervation changes (+1
duration, amplitude, and phases), and reduced recruitment patterns in proximal
and distal muscles of the left arm and leg. Magnetic resonance imaging showed
slight enlargement of the spinal cord in the cervical and thoracic regions
with discrete signal changes within the gray matter (Figure 2).
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Figure 2. Patient 2. A, Sagittal T2-weighted
image of the cervical spinal cord demonstrating an abnormal signal in the
spinal cord (arrowhead). B, Axial T2-weighted image. The abnormal signal restricted
to the anterior horns is characteristic of poliomyelitis (arrowhead).
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He was treated with broad-spectrum antibiotic agents and acyclovir and
his mental status improved over several days, but the weakness remained unchanged
during the hospitalization. There was slow improvement in his condition and
after 20 months his arm, hand, and hip girdle muscles were normal but the
foot drop was unchanged. Deep tendon reflexes were normal except for absent
Achilles reflexes bilaterally. He could walk with leg braces.
COMMENT
Our patients had acute, rapidly progressive regional or generalized
weakness that followed an infectious prodrome and simulated the acute motor
axonal neuropathy variant of GBS. Findings from electrodiagnostic studies
demonstrated a pure motor axonopathy indistinguishable from abnormalities
that have been observed in cases of acute motor axonal neuropathy.6 Although our patients were initially misdiagnosed
as having a motor variant of GBS, the fever, short latent period, and CSF
pleocytosis suggested an acute infectious process, and with the MRI findings
were characteristic of poliomyelitis.3, 5, 7, 8, 9, 10, 11, 12
The prodrome of paralytic poliomyelitis consists of malaise, headache,
fever, myalgias and muscle stiffness, and sore throat that last a few days
before progressing to the paralytic phase. Our second patient displayed other
salient prodromal features such as mental status changes, irritability, and
restlessness, reflecting aseptic meningitis. Weakness peaks rapidly over several
days in most cases, rarely evolving in a saltatory fashion over 1 week or
longer. In contrast to GBS, weakness occurs at the height of the fever and
generally does not progress after the fever subsides. An asymmetrical, flaccid
paralysis develops in most patients, typically affecting proximal more than
distal muscles. The legs are involved more often than the arms and differential
involvement of muscles within a limb is common, but complete paralysis of
an affected limb is unusual. In contrast, in 1 of our patients the illness
began asymmetrically in the arms and rapidly evolved into a symmetrical pattern,
and the other patient had a symmetrical distribution of weakness from the
outset, similar to another study.5 Oropharyngeal
muscles are affected in 10% to 15% of cases, and mechanical ventilatory failure
occurs when the intercostal muscles and diaphragm also are affected, similar
to 1 of our patients. Fasciculations may be prominent early in the illness
but are usually transient and were not noted in either of our cases. Deep,
aching muscle pain, indistinguishable from what occurs in some cases of GBS,
is common as weakness progresses. Muscle atrophy develops within a few weeks
of onset and usually is permanent. Reflexes are reduced in the clinically
affected limbs. Although some patients complain of paresthesias early in the
illness, objective sensory loss is not present.
Vaccine-associated poliomyelitis has been linked to poliovirus type
3 and is extraordinarily rare.13 It generally
occurs within 30 days of immunization with a relative risk of infection of
0.02 to 0.04 cases per 1 million doses of oral poliovirus vaccine.3, 13 However, coxsackieviruses groups A
and B, echovirus, and other viruses are the main causes of sporadic, nonpoliovirus
poliomyelitis and produce a paralytic syndrome indistinguishable from poliovirus.3, 14 Schellinger et al15
recently described 6 patients with a poliomyelitislike illness following a
tick bite and presumed infection with flavivirus, causing an unusual form
of central European encephalitis. Recognition that a suspected poliovirus
infection is due to another virus is invariably retrospective, based on negative
acute and convalescent poliovirus titers or culture, or raised titers of the
offending virus.
Although poliomyelitis is a common cause of acute flaccid paralysis
in many countries around the world, GBS and its variants remain the most common
cause of rapidly progressive generalized weakness in the United States and
Europe.4 For example, Busby and Donaghy16 recently described 4 patients with an acute, bibrachial,
motor predominant neuropathy that was considered a regional variant of GBS,
like one of our cases and similar to others that have been reported with cervico-pharyngeal-brachial
involvement.4 A pure motor variant of GBS was
observed in 18% of cases in one large series,17
but the figure is closer to 3% in our experience.4
These cases are characterized by distally predominant weakness, areflexia,
lack of sensory symptoms or signs, sparing of cranial nerves, an early clinical
nadir, higher than usual rates of raised anti-GM1 or anti–GalNAc-GD1a
antibody titers, and preceding C jejuni infection.17, 18 These cases may be clinically similar
to Chinese patients who had the acute motor axonal neuropathy variant, but
demyelinating changes detected by electromyographic studies are more frequent
in the former group.17, 18 In contrast
to the other well-described pattern of axonal GBS, acute motor sensory axonal
neuropathy, our patients lacked sensory symptoms or findings, electrically
inexcitable motor and sensory nerves, and acellular CSF characteristic of
acute motor sensory axonal neuropathy.19 In
addition to pure motor variants of GBS, rare disorders such as lead poisoning,20 acute fulminant myasthenia gravis, diphtheritic neuropathy,
and tick paralysis are the other major diagnostic considerations in patients
with acute flaccid paralysis.
A useful finding in our cases was the striking T2-weighted signal changes
observed within the gray matter of the spinal cord on MRI, corroborating a
disorder of the anterior horn cell rather than the ventral roots or motor
nerves. In addition to the marked CSF pleocytosis, the MRI abnormalities excluded
a motor variant of GBS. The appearance of abnormal signal in the gray matter
of the spinal cord may not be specific but is characteristic of the anatomical
distribution of poliomyelitis, in contrast to nerve root enhancement, a common
MRI abnormality in patients with GBS.21 The
changes on MRI in poliomyelitis likely reflect edema, perivascular and intraparenchymal
inflammation, gliosis, neuronophagia, or anterior horn cell loss, and identical
MRI abnormalities, mostly in children, have been described in the literature.3, 7, 8, 9, 10, 11, 12, 22
The lack of recovery and substantial residual weakness suggest irreversible
damage of the anterior horn cells in our cases, in contrast to the usually
favorable recovery of most patients with GBS.
Nonpoliovirus poliomyelitis is a rare cause of acute flaccid paralysis
and usually can be differentiated from typical GBS by an active, infectious
prodromal phase, inflammatory CSF profile, and lack of sensory features and
demyelinating abnormalities on electromyography. In ambiguous cases, MRI of
the spinal cord may further distinguish these cases from motor variants of
GBS.
AUTHOR INFORMATION
Accepted for publication April 20, 2001.
Presented in part at the 125th Annual Meeting of American Neurological
Association, Boston, Mass, October 17, 2000.
From the Neurology Service, St Elizabeth's Medical Center, Tufts University
School of Medicine, Boston, Mass.
Corresponding author: Kenneth C. Gorson, MD, Division of Neurology,
St Elizabeth's Medical Center, 736 Cambridge St, Boston, MA 02135 (e-mail:
KGorson{at}aol.com).
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