Reported here are the electrodiagnostic findings in a patient with myasthenia gravis who had dysarthria, dysphagia, and dyspnea. The use of repetitive nerve stimulation and single fiber electromyography studies for the evaluation of patients suspected of myasthenia gravis is reviewed. Key words: myasthenia gravis single fiber EMG repetitive nerve stimulation MUSCLE & NERVE 14:391-397 1991

AAEM CASE REPORT #3: MYASTHENIA GRAVIS CHARLES K. JABLECKI. MD

Myasthenia gravis (MG) is an autoimmune disorder caused by antibodies directed at the acetylcholine receptors (AChR) of skeletal muscle. The development of an assay of serum for AChR antibodies was a major advance in the diagnosis of MG. Circulating ACh receptor antibodies, however, are not detectable in all patients with MG. Electrodiagnostic studies, in particular repetitive nerve stimulation (RNS) and single fiber electromyography (SFEMG), remain the most sensitive and reliable tests for the diagnosis and management of MG. CLINICAL HISTORY

A 55-year-old man was referred for evaluation of dysarthria, dysphagia, and dyspnea. Eighteen months earlier, for the first time, he noted transient difficulty chewing and swallowing. These symptoms developed during a period of environmental stress, and as the stress resolved, the symptoms improved over a period of a few months. Six months before his evaluation, he noted the return of difficulty with chewing, swallowing, and, in ad-

From the Department of Neurology, University of California at San Diego, San Diego, California This publication is a revision of AAEE Case Report #3: Myasthenia Gravis, originally published in June 1981 Address reprint requests to American Association of Electrodiagnostic Medicine (formerly the American Association of Electromyography and Electrodiagnosis), 21 Second Street S W , Suite 306, Rochester, MN 55902 CCC 0148-639X1911050391-07 $04 00 0 1991 Charles J Jablecki, MD Published by John Wiley & Sons, Inc

AAEM Case Report #3: Myasthenia Gravis

dition, slight slurring of his speech. Four months before his evaluation, he noted shortness of breath with customary exercise. One month before, he noted difficulty holding his head up for a prolonged period of time. All of these symptoms were improved by rest and worsened with prolonged activity. Throughout the illness, he was not aware of ptosis, diplopia, weakness of the arms or legs, paresthesias in the face, hands, feet, f'asciculations, cramps, or cutaneous rash. CLINICAL EXAMINATION

The patient's eye movements were full, without complaint of diplopia, and there was no ptosis even with prolonged upward gaze. There was moderate bilateral facial muscle weakness, with difficulty closing the eyelids tightly, pursing the lips to whistle, and holding air in the cheeks. There was weakness of tongue protrusion without atrophy or fasciculations. He had normal movement of the palate, normal gag reflex, absence of jaw jerk, and normal sensation on the face. The neck extensors were moderately weak, and the neck flexors of normal strength. He had normal strength in the shoulder girdle, upper arm and forearm muscles, but moderate weakness without atrophy of the intrinsic hand muscles bilaterally. There was normal strength of the hip girdle, thigh and foreleg muscles, and the patient had no difficulty squatting on either leg, rising from a chair, hopping, or walking on his toes or heels. The muscle stretch reflexes in the arms and legs were easily elicited, but there was no Hoffmann sign or Babinski sign. Sensation to light touch,

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pin, position, and vibration were normal in the hands and feet. The maximum inspiratory force, measured with a hand-held inspirometer, was 45 cm of water, about 40% of normal. T h e initial differential diagnosis of the symmetrical muscle weakness affecting the muscles of facial expression, tongue, neck extensors, and intrinsic hand muscles, included a disorder of neuromuscular transmission, a myopathy, and a motor neuron disorder. T h e absence of pathologic reflexes, atrophy, and fasciculations made motor neuron disease (amyotrophic lateral sclerosis) unlikely. The diagnosis of a disorder of neuromuscular transmission (MC;) was suggested by the results of edrophonium (Tensilon) tests. T o conduct the tests, 1 mg, 3 mg, and 5 mg of edrophonium and normal saline were given intravenously, successively, in a double-blind fashion, until a response was noted. There was no response to the placebo, but edrophonium of 3 mg improved the strength of neck extensors and intrinsic hand muscles. T h e effect began about 30 seconds after the injection and lasted about one minute. LABORATORY TESTS

T h e following laboratory studies were normal: sedimentation rate, creatinine kinase, antinuclear antibodies, free thyroxin, and serum A C h R antibody titer. There was no evidence of thymoma on a computerized tomographic scan of the chest. ELECTROPHYSIOLOGIC EVALUATION

The median and ulnar sensory conduction studies were performed with pairs of 5-mm disc surface recording electrodes 3.5 cm apart, and secured over the respective nerves above the wrist crease. The digits (index: median, little finger: ulnar) were stimulated with surface ring electrodes. The peak latency and amplitude were measured. The conduction distances were 13 cm and 11 cm for the median and ulnar sensory studies, respectively. For the niotor conduction studies, the conipound muscle action potentials (CMAPs) (Mwaves) of the abductor digiti minimi, abductor pollicis brevis, and nasalis muscles were recorded with 5-mm tin disc surface electrodes fastened over the motor points (active electrodes) and the reference electrodes over the tendons of the muscles. The hand was immobilized by wrapping the extended fingers and thumb with gauze which was secured with adhesive tape. A hand-held stimulator probe with cathode distal delivered supramaxMethods.

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imal stimuli (50% greater than maximal stimulus) to the ulnar and median nerves at the wrist and elbow and the facial nerve just anterior to the mastoid process. T h e sweep speed and the gain were chosen so that the negative phases of the CMAPs were displayed in their entirety and appear at least 2 divisions high. For all motor studies, measurements were made of the amplitude (base to negative peak) of the CMAPs and the distal latencies. In addition, for the median and ulnar nerves, the minimum F wave latency of 10 responses with wrist stimulation and the conduction velocity in the forearm were computed. Repetitive nerve stimulation (RNS) of the motor nerves (5 stimuli at 2 Hz) was done first on the rested muscles. Records of the CMAPs elicited by the trains of stimuli were made.5 The decrement was calculated for each train as the difference between the lowest amplitude C M A P of the train of stimuli and the amplitude of the first C M A P expressed as a percentage of the amplitude of the first CMAP. If a decrement was noted, the train of 5 stimuli was repeated to verify the findings. The muscle was then exercised by brief (10 seconds) maximum voluntary contraction, and the train of stimuli was repeated 3 seconds after exercise was completed to test for facilitation (repair of the decrement and/or an increment). An increment after exercise was calculated as the ratio of the amplitude of the first C M A P after exercise to the amplitude of the first C M A P of the rested muscle. T h e RNS then was repeated 1 minute, 2 minutes, 3 minutes, and 4 minutes after 1 minute of sustained maximal voluntary contraction. A concentric needle electrode (recording surface area of 0.07 mm2) was used to study the spontaneous and voluntary activities of muscles. Individual motor unit action potentials (MUAPs) were activated at low rates (5 Hz) and isolated with a sweep trigger and delay line to study the stability of configuration with consecutive discharges. T h e initial median and ulnar sensory and motor conduction studies arid the facial motor conduction studies were normal (Table 1). The median, ulnar, and facial nerves were chosen for the RNS studies because the facial and intrinsic hand muscles were clinically weak. Those results are shown in 'Table 2. T h e RNS of the ulnar nerve was normal. A significant (greater than 10%) decrement was seen in the rested median and facial innervated muscles (Figure 1). After a brief (10 seconds) maximal voluntary contraction, the decrement was eliminated in the abductor pollicis

Results.

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Table 1. Initial sensory and motor conduction studies Nerve Ulnar (sensory) Median (sensory) Ulnar (motor) Median [motor) Facial [motor)

Amplitude*

Latencyt

10 F V 15 p.V 9.0 mV 10.0 mV 1.8 mV

2.8 ms 3.2 ms 3.0 ms 3.5 ms 3.0 ms

Conduction velocity

F wave minimum latency

31 ms 31 ms

-

'Amplitude of negative phase of CMAP for motor studies. peak-to-peak amplitude of sensory nerve action potential jOnset latency of CMAP for motor studies, peak iatency of negative phase for sensory nerve action potential

brevis and reduced in the facial muscle. KNS performed 2 minutes after the end of 1 minute of exercise demonstrated a greater decrement for both muscles; these decrements were again reduced when stimulation was carried out 3 seconds after brief (10 seconds) of maximal voluntary contraction. NO significant increment of the CMAP (> 1.40) was seen for any of the 3 nerves tested; the values were 1.00, 1.03, and 1.10 for the ulnar, median, and facial motor nerves, respectively. Concentric needle electromyography (CNEMG) of the weak orbicularis oris, midcervical paraspinal muscles, and intrinsic hand muscles demonstrated rapid recruitment of MUAPs which were short duration, polyphasic, and showed variation of configuration with consecutive discharges. CNEMG examination of strong muscles (deltoid, biceps, triceps, extensor digitorum communis, and pronator teres) showed normal MUAP activity. There was no abnormal spontaneous activity; in particular, neither fibrillation potentials nor fasciculation potentials were seen in any of the muscles examined by CNEMG.

IMPRESSION

The electrophysiologic studies were compatible with a disorder of neuromuscular transmission of the kind seen in MG. SFEMG studies were not performed because the abnormalities noted with the RNS and CNEMG studies were sufficient to confirm the clinical diagnosis of MG and to provide a basis for subsequent evaluation of therapy. CLINICAL COURSE

T h e patient was treated for 1 month with pyridostigmine (Mestinon), 60 to 120 mg, 3 to 4 times a day, but he was dissatisfied with the results. Prednisone, 40 mgld, was added and was well tolerated. Over the next few months, the patient noted improvement of his dysarthria, dysphagia, dyspnea, and neck- and hand-muscle weakness. This improvement was verified by the clinical examination 3 months after starting prednisone and was confirmed with RNS studies. The pyridostigmine was held for 24 hours before performing the RNS study (Table 2). The pyridostigmine was not restarted, and the prednisone dosage was gradually reduced to 30 mg every other day over the next 2 months. On that dosage, the patient indi-

~~~

Table 2. Serial repetitive nerve stimulation studies Decrement

Rest (%)

3s (Yo)

2-3 min (YO)

Ulnar Median Facial

9.0 mV 10.0 mV 1.8 mV

0 10 19

0 0

0 15 25

Median Facial

After 3 months treatment with prednisone 3 0 5 13.0 mV 2.0 mV 10 0 13

Median Facial

After 5 months treatment with prednisone 12.0 mV 0 0 0 1.8 mV 0 0 0

Nerve

m J;Y

2 ms

+

Jim"

Is

+

FIGURE 1. Consecutive CMAPs (M waves) recorded from the nasalis muscle with surface electrodes, with facial nerve stimulation at a rate of 2is (from another patient). The display on the left permits measurements of the negative phases of the CMAPs and the display on the right permits measurement of the peak-topeak amplitudes of the CMAPs.

AAEM Case Report #3. Myasthenia Gravis

After exercise

InLtial CMAP amplitude

4

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cated his symptoms had completely resolved, and the RNS studies verified the clinical observations (Table 2). The patient has remained asymptomatic on 30 mg prednisone on alternate days for the past year. DISCUSSION

In 1976, Lindstrom reported the presence of antibodies to acetylcholine receptors (AChR) in serum of patients with MG.'" The presence of serum antibodies to AChR has proved to be a highly specific test for MG.'" Elevated AChR antibody levels have been observed in only a few other clinical situations: penicillamine-induced myasthenia2'; ALS patients after treatment with snake venom" ; some elderly patients with other autoimmune diseasesy5; and first degree relatives of myasthenia gravis pat i e n t ~ . ~Although " elevated serum AChK antibody titers are highly specific for MG, there is a significant number of false negative results. Seybold (1983) reported the frequency of elevation of AChR antibodies in patients with generalized and ocular MG at 8 1% and 5 1 %, respectively."' Of all the studies available to confirm a clinical diagnosis of MG, the electrodiagnostic studies are most frequently abnormal."3:'" This case report emphasizes the value of performing electrodiagnostic studies to confirm the diagnosis of MG in myasthenics for whom the serum level of AChR antibodies is normal. Furthermore, if a patient has weakness of' a muscle that lends itself to evaluation by RNS studies, confirmation of the clinical diagnosis can be obtained during the initial evaluation, whereas laboratories may require 1 to 2 weeks to process a serum antibody study. Finally, because electrodiagnostic studies correlate better than serum AChR antibody titers with the distribution and severity of weakness in myasthenia, electrodiagnostic studies performed at the onset of the illness can provide valuable objective baseline information to determine whether the treatment is effectively improving neuromuscular transmis-

ion.^^ A decrernenting motor response to RNS is not unique to myasthenia gravis. A decrementing response has been described in other disorders of neuromuscular trarismission'",""-patients with monone~ropathy,"~ polyneuropathy,"' polyradiculopathy, rapidly progressive motor neuron disorders,2231.98 and myopathies with rr~yotonia.'."~ For this reason, it is important to perform a complete electrophysiologic examination to interpret the significance of the decr-ementing response. Sensory nerve conduction studies and motor con-

'

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AAEM Case Report # 3 Myasthenla G r a m

duction studies with measurement of the initial amplitude of the CMAP, distal latency, limb conduction velocity, and F wave latency are conveniently done before the RNS is begun. The CNEMG examination to evaluate spontaneous insertion and voluntary activity is conveniently done after the RNS is completed. With the results of the sensory and motor conduction studies and CNEMG examination, it is usually possible to determine the probable basis for a decrementing motor response with RNS. 'The physiologic basis for elecctrophysiologic abnormalities in MG will now be reviewed. Studies of curarized nerve- muscle preparation in vitro have shown that the amplitude of the muscle endplate potential (EPP) is not constant (see review by Nastuk, 1974).?" Normally, there is a progressive decrease in the EPP with RNS at slow rates (2-3 Hz). T h e rate of decrease of the EPP is less with RNS immediately after brief exercise. This phenomenon is termed post-activation fucilitation and lasts only a few seconds after a short period of strong voluntary contraction or tetanic nerve stimulation. However, if the train of nerve stimuli is delivered a few minutes after intense neuromuscular activity, the amplitude of the initial EPP is less and the rate of decrease is greater than in the rested preparation. The latter phenomenon is termed post-activation exhuustion. The genesis of this phenomenon is not well understood but it probably represents an interplay between availability of acetylcholine for release and alteration in the reactivity of the acetylcholine receptor in the postsynaptic membrane. Neuromuscular transmission is not affected in a normal subject by the changes in the EPP amplitude described above; the muscle EPP is more than sufficient to reach the threshold necessary to generate a muscle action potential. In other words, normally there is a 3- to 4-fold margin of safety in the process of neuromuscular transmission"'; however, if a disease has reduced the margin of safety of neuromuscular transmission sufficiently, not every nerve impulse may generate a muscle EPP sufficient to activate its muscle fiber. The margin of safety of' neuromuscular transmission may fall in a presynaptic disorder because of impaired release of acetylcholine; it may fall in a postsynaptic disorder because of a reduction in the number or reactivity of acetylcholine receptors. Repetitive nerve stimulation (KNS) reveals disorders of neuromuscular transmission based on the physiology described above. RNS is a tech-

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nique in which a train of stimuli is delivered to a motor nerve and the response, either electrical (CMAP) or mechanical (force), is recorded. T h e mechanical and electrical responses usually parallel each other. When the nerve which innervates a normal rested muscle is stimulated supramaximally at a rate of 2-3 Hz with a train of 4-5 stimuli, the amplitude and area under the CMAPs are constant. T h e sum of the electrical activity of the muscle fibers may be better represented by the area under the negative phase of the CMAP than by the peak-to-peak amplitude of the CMAP.3" Whichever technique is used, control studies should be done to establish the range of normality. In most laboratories, a 10% or greater reduction of the amplitude or area is abnormal and is termed a decrementing response. In MG, most of the decrement in the CMAPs occurs with the first 3 stimuli (Figure 1). The pattern most commonly seen with RNS of a weak muscle in a patient with MG is the following: a decrementing response in the rested muscle, repair of the decrement immediately after brief (10 second) maximum voluntary contraction, and an increased decrement with RNS 2-3 minutes after 30-60 seconds of maximum voluntary contraction. Demonstration of this pattern allows one to be certain that the decrement is a pathologic finding and not a technical artifact due to movement or submaximal nerve stim~lation.'~ It is also possible to demonstrate a decrementing response in the clinically strong muscles of an MG patient if one uses the stimulation sequence described above in conjunction with heat. The limb is warmed to 34%-36"C, and then the RNS is performed. The weakening effect of increased temperature on myasthenic muscles has been described in detail by Simpson (1975)."3T h e physiologic basis for temperature-dependent weakness is a reduction in the margin of safety for neuromuscular transmission. At a higher physiologic temperature, there is more rapid depletion of acetylcholine from presynaptic terminals, decreased sensitivity of the acetylcholine receptors, and reduced half-life of acetylcholine due to enhanced cholinesterase activity in the postsynaptic membrane." In patients with MG, RNS of proximal nerves is 2-3 times more effective for demonstrating a decrement than distal nerves.24 Proximal nerves commonly stimulated include the musculocutaneous, axillary, spinal accessory, and facial nerves. Spinal accessory nerve stimulation has been reported to be less painful and to have a yield as

AAEM Case Report #3: Myasthenia Gravis

great as facial nerve stimulation.") Axillary and musculocutaneous nerve stimulation is often poorly tolerated because of pain and so is usually left for last in the investigative process. Ideally, one would like to demonstrate a decrementing response with at least 2 nerves in a suspected myasthenic to confirm the diagnosis. CNEMG of weak muscles of patients affected by MG fre uently shows variation of MUAP configuration.' This MUAP variation is not seen in normal muscle, but it may be seen in disorders other than primary defects of neuromuscular transmission; eg, motor neuron disease, and recently reinnervated muscles in patients with polyneuropathies. The MUAP variation is due to blocking of individual single-muscle fiber components of the MUAP.36 In disorders of neuromuscular transmission, these phenomena are caused by the reduction of the margin of safety and the attendant failure of the EPP to reach threshold. In addition to the variation of configuration of MUAPs, frequent failure of neuromuscular transmission may result in the occurrence of short duration, low amplitude MUAPs. T h e presence of these small MUAPs combined with rapid recruitment in weak muscles may lead to the erroneous conclusion that the weakness is due to a myopathy. In this situation, ENS studies help distinguish between a disorder of the neuromuscular transmission and a myopathy.16 Single fiber electromyography (SFEMG), has permitted microphysiologic studies of motor units in the clinical 1aborato1-y.~~ T h e time interval between two action potentials from two muscle fibers belonging to the same motor unit shows slight variability called "jitter."9 In normal muscles, jitter in individual single fiber pairs is of the order of 10 to 60 ps. In muscles of patients with MG, the jitter is typically increased27x36 (See Figure 2). SFEMG provides an attractive alternative to two other procedures that may permit one to find a decrementing response in hand muscles of MG patients when initial RNS studies are normal: is~ h e m i a ' . ' ~and regional curare. l 4 Both tests can be cumbersome and cause considerable discomfort, and the regional curare test is potentially hazardous. Sanders and Howard (1986) reported the results of SFEMG studies in 416 patients with MG.28 They found that 92% of the patients showed abnormal jitter in the extensor digitorum communis (EDC) (MCD > 34 ps and/or 10% of potential pairs with jitter >55 ps). Most of the false negative studies were in ocular MG patients where 22%

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FIGURE 2. Potential pair recorded in EDC by single fiber electromyography (from another patient) shows increased jitter (85 CLS)'

showed normal jitter in the EDC; the incidence of normal jitter was decreased to 8% if a facial muscle (frontalis, orbicularis oculi, or orbicularis oris) was tested. Sanders and Howardyx compared the diagnostic sensitivity of SFEMG jitter measurements to ischemic KNS in patients with MG. Both jitter measurements and RNS are more frequently abnormal in proximal muscles compared with distal muscles in early o r mild myasthenia gravis. RNS of ischemic nerves to hand muscles was only slightly more sensitive than RNS of nerves to proximal muscles and only 60% as sensitive as SFEMG jitter measurements in the EDC. Whereas SFEMG showed increased jitter in at least one of two muscles (EDC, frontalis) in 92%, a decrementing response was noted in at least one muscle in only 48% of 220 patients with MG with RNS of the spinal accessory nerve, axillary nerve, o r musculocutaneous nerve. T h u s SFEMG is the most sensitive electrophysiologic test for myasthenia gravis."" Abnormal SFEMG jitter is also seen in a variety of disorders of neuromuscular transmission, as well as in disorders of motor neurons, peripheral nerves, and some myopathies? For this reason, it is recommended that sensory and motor nerve conduction studies, RNS studies, -and CNEMG studies be performed to interpret the significance of SFEMG abnormalities. Although SFEMG is more sensitive than RNS, RNS remains the mainstay for the initial electrodiagnostic evaluation of MG. When a decrement in two muscles is present with KNS, SFEMG is not

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AAEM Case Report #3. Myasthenia G r a m

necessary for diagnosis. However, because SFEMG is more likely to demonstrate an abnormality of neuromuscular transmission, SFEMG is performed as the initial electrodiagnostic test for MG in some laboratories.29 This approach is most successful in patients with mild o r primarily ocular symptoms. If abnormal jitter is documented, KNS is then performed to quantitate the percentage of facilitation after exercise to determine if the disorder of neuromuscular transmission is presynaptic (MG) o r postsynaptic. It is possible with either RNS or SFEMG to demonstrate abnormal neuromuscular transmission in clinically strong muscle of patients with MC,. This is one advantage of electrodiagnostic studies over an edrophoniuni (Tensilon) test, which requires evaluation of a weak muscle. If there is mild to moderate weakness of a muscle d u e to MG, one should be able to demonstrate a decrementing response (KNS) o r increased jitter (SFEMG). Failure to do so implies that MG is not the primary cause of the niuscle weakness."."" Other tests that permit quantification of cranial muscle fatigue and improvement with anticholinesterase medication (edrophonium) are the Lancaster red-green test of ocular mobility and a test for stapedial reflex fatigue. T h e r e is a controversy as to whether the 1,ancaster red-green test really adds objective information, a position supported by Seybold:" and questioned by D a r ~ f f . ~ Recently a disorder of ocular motility responsive to endrophonium a n d caused by a brainstem glioma has been reported.x In a small series, the stapedial reflex test was slightly less sensitive than SFEMG studies, but with the advantage of being less uncomfortable. lXT h e Lancaster red-green test is reported as similar in sensitivity to SFEMG studies of proximal muscles, but only one test o r the other may be positive in a n i n d i ~ i d u a l . Con'~ firmation of the diagnosis reportedly has been achieved in 95% of patients with mild MG with normal RNS studies by the combination of SFEMG studies of the proximal muscles, assay of serum for AChK antibodies, and the Lancaster red-green test. l 7 I n summary, during the last few years there have been major advances in the understanding of the pathophysiology of MG. These advances have led to a reevaluation of the role of electrodiagnostic studies for the diagnosis and management of MG. Electrodiagnostic studies remain the first choice for immediate, reliable, objective results that can be correlated directly with the underlying pathophysiology of weakness in MG. Further-

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more, electrodiagnostic studies simultaneously permit identification of other disorders that can

mimic MG, as well as provide objective parameters to use to monitor the effectiveness of therapy.

REFERENCES 1. Bernstein LP, Antel JP: Motorneuron Disease: DecremenVal responses to repetitive nerve stimulation. NeuroloSy 198 l ; 3 1204-207. 2. Brown JC: Muscle weakness after rest in myotonic disorders: An electrophysiological study. J Neurol Neurosu,rg Pcychiatry 1974;37:1336- 1342. 3 . Cruz-Martinez A, Ferrer MT, Diez-Tejedor E, et al: Diagnostic yield of single fiber electromyography and other electrophysiological techniques in myasthenia gravis: Electromyographic automatic analysis of the voluntary and repetitive nerve stimulation. Electromyog?- Clin Neurophyszol 1982;22:377-393. 4. Daroff KB: T h e office tensilon test for ocular myasthenia gravis. Airh Neurol 1986;43:843-844. 5. Daube J : Minimonograph #8. Electro)p/iy.sio~o~r~c Testing for Disorders of the Neurornusculur Junctzon. Rochester, Minnesota, American Association of Electromyography and Electrodiagnosis, 1978. 6. Denys E: Minimonograph #14. The Role (4 ‘l’ernpmzture in Ekctromyogruphy. Rochester, Minnesota, American Association of Electromyography and Electrodiagnosis, 1980. 7. Desmedt JE, Borenstein S: Double-step nerve stimulation test for myasthenic block: Sensitization of post-activation exhaustion by ischemia. Ann Neurul 1977; 1:55-64. 8. Dirr LY, Donofiro PD, Patton J F , Troost B‘I.: A false-posirive endrophonium test in a patient with a brain stem glioma. Nturol 1989;39:865-867. 9. Ekstedt J , Nilsson G, Stalherg E: Calculation of electromyographic jitter. J Nrurol Nrurosurg P.\ychzuhy 1974; 37:526-539. 10. Gilchrist JM, Sanders DB: Double-step repetitive stimulation in myasthenia gravis. Muscle N e r w 1987; 10:233-237. 11. Gilchrist J M , Sanders DB: Myasthenic U-shaped decrement in multifocal cervical radiculopathy. Muscle Nrivr 1989;12:69-66. 12. Harvey AM, Masland RL: A method for the study of neuromuscular transmission in human subjects. Bull Johns Hopk Hosp 1941;68:81-93. 13. Heilbronn E, Lefvert AK, Stalberg E: Acetylcholine receptor antibodies in the diagnosis of human and experimental myasthenia gravis. Muscle Nerve 1978; 1:427-431. 14. Horowitz SH, Sivak M. T h e regional curare test and electrophysiological diagnosis of myasthenia gravis: Further studies. Muscle Nerve 1978; 1:432-434. 15. Jablecki CK: Electrodiagnostic evaluation of patients with myasthenia gravis and related disorders. Nturologzc Clinzcs 1985;3:557-572. 16. Jablecki CK: Myopathies, in Brown W, Bolton C (eds): Clinical Electromyyqaphy, ed 1. Boston, Butterworths, 1987, pp 384-390. 17. Kelley J J J r , Daube JR, Lennon VA, et al: T h e laboratory diagnosis of mild myasthenia gravis. Ann Neurol 1982;l2:238-242. 18. Kramer LI), Ruth RA, J o h n s ME, et al: A comparison of stapedial reflex fatigue with repetitive stimulation and single-fiber EMG in myasthenia gravis. Ann Neurol 1981;9:531-536. 19. Lindstrom J , Seybold M, Lennon V , Whittingham S, Duane D: Antibody to acetylcholine receptor in myasthenia

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gravis: Prevalence, clinical correlated diagnostic value. NeuroloLgy1976;26: 1054- 1059. 20. Miglietta OE: Myasthenic-like response in patients with neuropathy. Am J Phys Med 1971;50: 1- 16. 21. Mittag T W , (:aroscio J : False-positive initnunoassay for acetylcholine receptor antibody in amyotrophic lateral sclerosis. N Engl J Med 1980;302:868. 22. Mulder DW, Lambert EH, Eaton LAM: Myasthenic syndrome in patients with amyotr-ophic later-al sclerosis. N e w ?‘(J/OLQ 1959;9:627-63 1. 23. Nastuk W: Neuromuscular transmission. in Mountcastle V (ed): Medzcul P/iy.\i010,g~,ed 13. St. Louis, C V Moshy C o , 1974, p p 151- 181. 24. Ozdeniir C, Young R: T h e results to be expected from electrical testing in the diagnosis o f myasthenia gravis. A m N Y Acnd Sci 1976;274:103-222. 25. Kobb SA, Vincent A, Newsorn-Davis,J, et al: Clinical pathological, HLA antigen and immunologic evidence for disease heterogeneity in myasthenia gravis. Brain 1980; 103:579-601. 26. Russel AS, Lindstrom J M : Penicillarnine induced tnyasthenia gravis associated with antibodies to acetylcholine receptor. Neurology 1978;28:847-849. 27. Sanders DB, Howard JF, J o h n s T R : Single fiber electromyography in myasthenia gravis. A ~ c , u ~ - u ~ o1979; ~~v 29:68-76. 28. Sanders DB, Howard JF: AAEE Minimonograph #25: Single-fiber electromyography in myasthenia gravis. Mzrsck N e w t 1986;0:800-819. 29. Sanders DB. T h e electrodiagnosis of myasthenia gravis. Ann N Y Acad Scz 1987;505:539-556. 30. Schumm F, Stohr M : Accessory nerve stimulation in the asP 147sessment of myasthenia gravis. Mu.sc-lr N ~ I 1984;7: 151. 31. Seybold ME: Myasthenia gravis: A clinical and basic science review. JAMA 1983;250:2516-2521. 32. Seybold ME: T h e office tensilon test for ocular myasthenia gravis. Arch Neurol 1986;43:842-843. 3 3 . Simpson J : Myasthenia gravis and myasthenic syndrome, in Walton J (ed): Disor-d~r5uf Voluntmy M u d , ed 3 . Edinburgh, Churchill Livingstone, 1974, p p 65?-692. 34. Singer PA, Lin JTY: Decremental response in carpal tuiinel syndrome (abstract). Muscle Nerve 1982;5:566. 35. Stalberg E, ‘l‘rontelj J : Single Fibre Electromyography. Old Woking, Surrey, England, Mirvalle Press, 1979, pp 1-244. 36. Stalberg E. Clinical electrophysiology in myasthenia gravis. J Neurol Neurosurg Psychiatry 1980;43:622-633. 37. Streih EW. AAEE Minimonograph #27: Differential diagnosis o f myotonic syndromes. Muscle Neive 1987;10:603615. 38. Subramony SH, Mitsomoto H , Mishra SK: Motor neuropathy associated with a facilitating myasthenia syndrome. Musrle Nerve 1986;9:64-68. 39. Swift ‘IR: Disorders of neuromuscular transmission other than myasthenia gravis. Muscle Nerve 1981;4:334-353. 40. Vincent A, Newsom-Davis J : Acetylcholine receptor antibody as a diagnostic test for myasthenia gravis: Results in 153 validated cases and 1967 diagnostic assays. 1 Nturol Neurosurg Psyrchiatry 1985;48: 1246- 1252.

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AAEM case report #3: myasthenia gravis.

Reported here are the electrodiagnostic findings in a patient with myasthenia gravis who had dysarthria, dysphagia, and dyspnea. The use of repetitive...
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