biochemical analysis of the ischemic extremity. J Vasc Surg 1986;3:411-420. 16. Keller U, Oberhansli R, Huber P, et al. Phosphocreatine content and intracellular pH of calf muscle measured by phosphorus NMR spectroscopy in occlusive arterial disease of the legs. Eur J Clin Invest 1985;15:382-388. 17. Meyer RA. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol 1988;254:C548-C553.
18. Miller RG, Carson PJ, Moussavi RS, Green AT, Baker AJ, Weiner M W . F a t i g u e a n d myalgia i n AIDS p a t i e n t s . Neurology 1991;41:1603-1607. 19. Engle AG, Banker BQ. Myology: basic and clinical. New York: McGraw-Hill, 1986:848. 20. Sweeney HL, Kushmerick MJ, Mabuchi K, S r e t e r FA, Gergely J. Myosin alkali light chain and heavy chain variations correlate with altered shortening velocity of isolated skeletal muscle fibers. J Biol Chem 1988;263:9034-9039.
Electrophysiologic changes in lumbar spinal cord after cervical cord injury Mindy L. Aisen, MD; William Brown, MD, FRCP (C); and Michael Rubin, MD, FRCP (C)
Article abstract-Spontaneous activity on the EMG examination is traditionally ascribed to disease of the lower motor neuron when present in muscles well below the level of para- or quadriplegia despite the absence of any detectable peripheral nerve injury. It is uncertain whether it reflects transient paralysis of transmission (related to clinical spinal shock) or irreversible postsynaptic damage. We performed serial EMG studies of lower extremities and paraspinal muscles on eight young, previously healthy adults, commencing 2 t o 9 weeks after acute cervical cord injury. All had stimulated single-fiber EMG (SFEMG) studies at 6-month intervals t o determine whether irreversible postsynaptic damage of the anterior horn cell had occurred. MRI and nerve conduction excluded patients with evidence of distal cord injury or peripheral neuropathy. All patients had spontaneous activity in all muscles tested, persisting after spinal shock had resolved. Jitter was present on SFEMG in three of eight patients 6 months after injury. Four of five patients retested 12 months after injury had abnormal jitter, including three who initially had normal SFEMG studies. We conclude that there is electrophysiologic evidence of trans-synaptic distal cord dysfunction following acute spinal cord injury. SFEMG studies suggest that anterior horn cell dropout occurs during the 1st year after injury. NEUROLOGY 1992;42:623-626
Spontaneous activity (SA) in the form of fibrillation potentials (FP) and positive sharp waves (PSW) as seen on EMG examination is traditionally ascribed to disease of the lower motor neuron, which extends from the anterior horn cell in the ventral horn to distal muscle.' However, SA occurs i n disease apparently limited t o the upper motor neuron2-11 and in muscles well below the level of a lesion causing para- or quadriplegia despite the absence of any detectable peripheral nerve The frequency, prognostic implications, and etiology of this abnormal finding have not been thoroughly elucidated. Prior studies have not followed the time course of EMG abnormalities and have not defined the relationship of EMG changes to clinical weakness,
spasticity, and ultimate improvement. In addition, they have not addressed the pathophysiology of these apparent caudal effects of rostra1 cord trauma. At present, it is not known whether the EMG changes reflect transient paralysis of transmission (related to clinical spinal shock) o r irreversible postsynaptic damage. We undertook t h e present study to gain a n understanding of the evolution of EMG changes in subacute cervical spinal cord injury by performing serial EMG studies while chronicling ongoing changes in neurologic examination as patients progressed from spinal shock to the spastic phase. The integrity of anterior horn cells caudal to the lesion site was assessed with stimulated single-fiber EMG (SFEMG) at 6-month intervals.
From The Burke Rehabilitation Center (Dr. Aisen), Cornell University Medical College, White Plains, NY; the Division of Neurology (Dr. Brown), University Hospital, London, ON, Canada; and the Department of Neurology (Dr. Rubin). The New York Hospital, Cornell University Medical College, New York, NY. Supported by a grant from the American Paralysis Association. Received May 21, 1991. Accepted for publication in final form August 21, 1991 Address correspondence and reprint requests to Dr. Mindy L. Aisen, The Burke Rehabilitation Center, Cornell University Medical College, 785 Mamaroneck Avenue, White Plains, NY 10605.
March 1992 NEUROLOGY 42 623
’able.Spontaneous activity in paraspinal (PS)and lower extremity (LE) muscles Weeks postinjury Pt no.
Clinical
1
25 yo fall C6-7 sensory complete
2
23 yo diving injury C-6 sensory complete
3
16 yo motor vehicle accident c-7 sensory complete
4
16 yo diving injury c-4 sensory complete
5
19 yo gunshot wound T-1 sensory complete
6
17 yo diving injury c-7 sensory incomplete
7
8
0-4_
~
PS LE
2+
1+
s=o
PS LE
9-11 . PS LE
1+ 3+ S = l
o+ 2+ s=1
2+ 2+ s=2
3+ 3+ s=3
0 1+ s=1
0 1+ S=l
16-20
PS LE
PS LE
1+
1+
s = 2:l:
4+
3+
s=o
0
0
s=o
3+
1+
s=o
2+
0
s =I:>
4+ 3+ S=l
3+
2+
2+ 1+ s=2
1+
o+
s=l
o+ 1+ s=l:’: s = 2”
4+
3+
s=o
2+ s=2
2+
Methods. Eight patients meeting inclusion criteria were sequentially selected upon admission to The Burke Spinal Cord Injury Inpatient Service; clinical characteristics are summarized in the table. All were previously healthy young adults (ages 16 t o 30 years) admitted from rehabilitation 2 t o 9 weeks after traumatic cervical spinal cord injury; patient 3 was the only female studied. All had complete motor paralysis at the time of entry. Patients with evidence of lower limb or lumbar trauma were excluded. The experimental protocol was approved by The Burke Rehabilitation Center Committee for Human Rights i n Research, and written consent was obtained from all participants. To document the integrity of the peripheral nervous system below the level of the lesion, all had normal superficial peroneal conduction
1+
1+
s = 3“
6mos
12 mos
0
Normal
Jitter
1+
0
Normal
Normal
2+
2+
Normal
Jitter
Jitter
Jitter
Jitter
s = 3”
s =1“
1+ 2+ S=l”
0 0 s=2*
2+ 3+ S=l
2+
3+
Normal
0
0
Normal
s=1
s = 3s: -
t
1+ 3+
s=3:+
Single-fiber EMG
0
s = 3*
t 1+ 3+
21-28 PS LE
s = 2“
S=l
Spontaneous activity guide O+ = No positive wavesifibrillation. 1+ = Positive waves/fibrillation a t one site. 2+ = Positive waves/fibrillation occasionally present a t 22 sites. 3+ = Positive wavedfibrillation a t most sites. 4+ =Abundant positive waves/fibrillation a t all sites.
624 NEUROLOGY 42 March 1992
12-15
~~~
1+ 2+
30 yo skiing accident c-5 sensory incomplete 27 yo diving injury C-6 sensory incomplete
_ 5-8 _
o+
1+ s=3*
Jitter
1+ 1+
s = 3”
Spasticity scores ( S ) 0 = Flaccid areflexia. 1 = No increase in tone. 2 = Slight increase in tone, giving a “catch” when limb moved. 3 = More marked increase, but affected part easily flexed. 4 = Passive movement difficult. 5 = Rigid in flexion or extension.
Jitter
*Treated with baclofen. ? Motor recovery.
velocities. Six had normal peroneal somatosensory evoked potentials (stimulating a t the knee and recording over lumbar and midthoracic cord). Patient 5 had no cord potential, a finding in 2% of controls in our laboratory, and patient 7 refused evoked potential study. All patients had MRI studies of cervical, thoracic, and lumbar spine t o exclude the possibility of structural cord disease extending below injury level. Although patients 3 and 6 had evidence of L3-4 disk degeneration, no abnormality of cord or cauda equina was noted in any patient. EMG studies of bilateral T-12 and L-5 paraspinal muscles and of right vastus lateralis, anterior tibialis, biceps femoris, and medial gastrocnemius muscles were performed during the 1st week after admission t o Burke, and repeated at approximately 3-week intervals. EMG
changes were graded according to criteria established by Kimura.' Physical examination was performed immediately before EMG to grade motor power (0 to 5 ) , reflex changes, and spasticity (Ashworth scoreI2). Stimulated SFEMG was performed by percutaneously stimulating the peroneal nerve and recording jitter at a single neuromuscular junction, adapting previously described methods.13 The deep peroneal nerve was stimulated at the neck of the fibula using constant-current stimuli at a frequency of 10 Hz, and single-fiber potentials were recorded by a single-fiber needle placed in the anterior tibialis muscle. In stimulated SFEMG, normal jitter is defined as the square root of the normal value seen in conventional single-fiber studies (560 psec for the tibialis anterior muscle). SFEMG was considered abnormal if jitter exceeding this value was present a t two (or more) of 20 sites. SFEMG was performed a t 6 and 12 months after injury.
Results. As seen in the table, all patients had persistent and widespread SA involving muscles of the trunk and legs; EMG changes are designated a s paraspinal (PS) or lower extremity (LE), including vastus lateralis, biceps femoris, anterior tibialis, and medial gastrocnemius. Two patients initially studied 4 weeks after injury had EMG changes. Patient 6 was first studied 2 weeks after injury, a t which time no PSW or FP were seen; 3 weeks later, PSW and FP developed. Although the extent of FP and PSW in PS as opposed to LE musculature varied within individuals, overall axial and appendicular involvement were equivalent. The degree of PSW and FP gradually rose, then fell over time after injury, peaking in 9 to 11 weeks after injury and resolving in most cases by 28 weeks after injury. The presence of FP and PSW did not correlate with clinical state, as shown in the table, in all but patient 6. FP and PSW were present during the spinal shock phase and persisted during the spastic phase. There w a s no a p p a r e n t relationship between degree of F P and PSW and severity of spasticity or severity of cord injury (ie, FP and PSW were noted in patients regardless of sensory function) in seven patients, all of whom had persistent complete motor paralysis. Patient 6, however, developed substantial voluntary motor control during the 12th week after injury, at which time EMG abnormalities abated. SFEMG was normal in five of eight patients 6 months after injury; patients 4,7, and 8 had abnormal jitter at that time. These patients suffered from the anatomically highest structural and functional cord injuries in the group, although they differed clinically in degree of spasticity and sensory loss. Five patients were retested 12 months after injury, and four of five had abnormal jitter, including three who initially had normal SFEMG studies. Discussion. In this study, all patients had diffuse and widespread FP and PSW in lumbosacral-innervated muscles. These p a t i e n t s had cervical myelopathy and no clinical, other electrophysiolog-
ic, or radiographic evidence of distal cord or lower motor neuron pathology. An appreciation of the association between EMG changes a n d upper motor neuron disease, and an understanding of the abnormal SA in muscles supplied by spinal cord substantially caudal to the area of injury, is clinically important. Physicians should not attribute this finding t o focal radiculopathy, which could then lead to unnecessary diagnostic or surgical procedures. Another major finding was t h e presence of abnormal jitter on SFEMG in six patients, developing in three patients 6 to 12 months after injury. As reinnervation occurs, recorded action potentials become increasingly complex, and jitter commonly develops. Progressive trans-synaptic degeneration of motor neurons occurring in the lumbar spinal cord following cervical injury is a potential explanation for the observed subacute signs of denervation (PSW, FP) and chronic signs of reinnervation (jitter). PSW and FP are nonspecific abnormalities that occur in disease of muscle,14neuromuscular junction,15 a n d a n t e r i o r horn ce11,16 b u t EMG is employed as a tool for recognizing partial denervation. SA is not associated with disuse atrophy.' The mechanism by which SA develops has not been fully elucidated. There is evidence that denervation hypersensitivity to acetylcholine plays a n important role in its de~elopment,'~ although other data conflict with this hypothesis.18 Another theory invokes a specific trophic effect of peripheral nerve on m u ~ c 1 e . lThese ~ observations have led t o the widely accepted clinical tenet that SA is a sign of disease of the lower motor neuron. However, several studies have demonstrated the presence of PSW and FP in disease apparently limited to the upper motor neuron, both in ~ t r o k and e ~ in ~ ~myelop~ ~ a thy. 6-1 Goldkamp2 studied 116 stroke patients and found PSW and FP in almost 70%. The peak incidence occurred 4 to 4% weeks after the acute event, with greater PSW and FP in the upper than lower extremities, suggesting a cerebral pattern. These abnormalities were present despite normal nerve conduction studies. Rosen et a16found PSW and FP in six of seven patients studied during spinal shock, which largely resolved after the spastic phase developed, suggesting that during spinal shock, functional depression of the anterior horn cell occurred, and that anterior horn cells recovered when spinal shock resolved. However, Van Alphen et a17 found actual anterior horn cell loss well below the site of spinal injury at postmortem in three quadriplegic patients, and Brown et alRdemonstrated that hemisection of the macaque spinal cord in the thoracic region resulted in a 20% loss of anterior horn cells in the lumbosacral cord. These findings may indicate that anterior horn cell degeneration and dropout is the source of SA after cord transection. Other investigator^^-^^ have found that PSW and March 1992 NEUROLOGY 42 625
F P a r e not confined to t h e spinal shock phase. Subsequent studies20-22 indicated that PSW and FP develop by 3 weeks after injury a n d gradually resolve over time. B r a n d s t a t e r a n d Dinsdale" raised the possibility t h a t SA below the level of injury may be due to spinal cord trauma over a significant longitudinal segment of cord, and in no s t u d y w a s t h i s i d e a objectively a d d r e s s e d . Furthermore, examination of differences in prognosis between patients who do or do not have PSW and FP has not been performed. I n o u r s t u d y , e i g h t of e i g h t p a t i e n t s w i t h myelopathy and no identifiable pathology of lower motor neuron had persistent and diffuse PSW and FP in lumbosacral-innervated musculature. I n most patients, PSW a n d FP appeared within 6 weeks of injury, peaked 9 to 11 weeks after injury, and resolved by 28 weeks after injury. This time course is essentially that which is seen following acute axonotmesis and subsequent reinnervation. There was no clear relationship between resolution of the spinal shock phase and EMG abnormalities, arguing against a transient dysfunctional neuronal state as the etiology for SA. The degree of PSW and FP did not correlate with axon length. A low degree of PSW and FP may signify a better prognosis for motor recovery, as seen in patient 6. Six patients developed abnormal jitter by 12 months after injury. The time course and degree of SFEMG abnormality bore no relationship to earlier EMG changes. This finding may signify evolving motor neuron dropout and collateral reinnervation and in vivo confirmation of the pathologic findings of Van Alphen et al' and Brown et al.8 It raises the possibility that lower motor neuron EMG findings in upper motor neuron disease are due to distant neuronal degeneration, as it provides evidence of reinnervation and reorganization of the motor unit during the chronic phase. Further investigation to define this phenomenon and to establish etiologic factors is required to understand the pathophysiology and prognosis of spinal cord injury lesions and to plan strategies for intervention.
Refe.rences 1. Kimura J . Electrodiagnosis in diseases of nerve and muscle: principles and practice. 2nd ed. Philadelphia: F.A. Davis, 1989.
626 NEUROLOGY 42 March 1992
2. Goldkamp 0. Electromyography and nerve conduction studies in 116 patients with hemiplegia. Arch Phys Med Rehabil 1967;48:59-63. 3. Chokroverty S, Medina J. Electrophysiological s t u d y of hemiplegia: motor nerve conduction velocity, brachial plexus latency a n d EMG. Arch Neurol 1978;35:360-363. 4. Bhala RP. Electromyographic evidence of lower motor neuron involvement in hemiplegia. Arch P h y s Med Rehabil 1969;50:632-637. 5. Brown WF, Snow R. Denervation in hemiplegic muscles. Stroke 1990;21:1700-1704. 6. Rosen JS, Lerner IM, Rosenthal AM. Electromyography in spinal cord injury. Arch Phys Med Rehabil 1969;50:271-273. 7. Van Alphen HA, Lammers H J , Walder HAD. On remarkable reaction of motor neurons of lumbosacral region after traumatic transection in man. Neurochirurgia (Stuttg) 1962;8:328-330. 8 Brown WF, Milner-Brown HS, Ball M, Girvin JP. Control of t h e m o t o r c o r t e x o n s p i n a l m o t o n e u r o n e s i n m a n . In: Desmedt J E , ed. Cerebral motor control in man: long loop mechanisms. Progress in clinical neurophysiology, vol. 4. Basel: Karger, 1978:246-262. 9 Nyboer V J , J o h n s o n H E . Electromyographic findings in lower extremities of patients with traumatic quadriplegia. Arch Phys Med Rehabil 1971;52:256-259. 10. O'Hare VM, Abbot GH. EMG evidence of lower motor neuron injury i n cervical spinal cord injury. Proc Ann Con Spinal Cord Inj Center 1967;17:25-35. 11. Spielholz NI, Sell GH, Goodgold J, Rusk HA, Greens SK. Electrophysiologic s t u d i e s in p a t i e n t s with s p i n a l cord lesions. Arch Phys Med Rehabil 1972;53:558-562. 12. Ashworth B. Preliminary trial of carisoprodol i n multiple sclerosis. Practitioner 1964;192:540-542, 13. J a b r e JF, Chirico-Post J, Weiner M. Stimulation single fiber EMG in myasthenia gravis. Muscle Nerve 1989;12:38-42. 14. Buchthal F, Rosenfalck P. Spontaneous electrical activity of h u m a n m u s c l e . E l e c t r o e n c e p h a l o g r Clin Neurophysiol 1966;20:321-336. 15. Peterson I, Broman AM. Electromyographic findings in a case of botulism. Nard Med 1961;65:259-261. 16. Johnson EW, Guyton J D , Olson KJ. Motor nerve conduction velocity studies in poliomyelitis. Arch Phys Med Rehabil 1960;41:185-190. 17. Thesleff S. Supersensitivity of skeletal muscle produced by botulinum toxin. J Physiol (Land) 1960;151:598-607. 18. Miled R. The acetylcholine sensitivity of frog muscle fibers after complete a n d partial denervation. J Physiol ( L a n d ) 1960;151:1-23. 19. Goodgold J, Eberstein A. Electrodiagnosis of neuromuscular disease, 3rd ed. Baltimore: Williams & Wilkins, 1983. 20. Taylor RG, K e w a l r a m a n i LS, Fowler WM. Electromyographic findings in lower extremities of patients with high spinal cord injury. Arch Phys Med Rehabil 1974;55:16-23. 21. Onkelinx A, Chantraine A. Electromyographic study of paraplegic patients. Elcctroniyogr Clin Neurophysiol 1975;15:7181. 22. Brandstater ME, Dinsdale SM. Electrophvsiological studies in t h e assessment of spinal cord lesions-. Arch Phys Med Rehabil 1976;57:70-74.
Electrophysiologic changes in lumbar spinal cord after cervical cord injury Mindy L. Aisen, William Brown and Michael Rubin Neurology 1992;42;623 DOI 10.1212/WNL.42.3.623 This information is current as of March 1, 1992 Updated Information & Services
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Neurology ® is the official journal of the American Academy of Neurology. Published continuously since 1951, it is now a weekly with 48 issues per year. Copyright © 1992 by AAN Enterprises, Inc.. All rights reserved. Print ISSN: 0028-3878. Online ISSN: 1526-632X.
18. Miller RG, Carson PJ, Moussavi RS, Green AT, Baker AJ, Weiner M W . F a t i g u e a n d myalgia i n AIDS p a t i e n t s . Neurology 1991;41:1603-1607. 19. Engle AG, Banker BQ. Myology: basic and clinical. New York: McGraw-Hill, 1986:848. 20. Sweeney HL, Kushmerick MJ, Mabuchi K, S r e t e r FA, Gergely J. Myosin alkali light chain and heavy chain variations correlate with altered shortening velocity of isolated skeletal muscle fibers. J Biol Chem 1988;263:9034-9039.
Electrophysiologic changes in lumbar spinal cord after cervical cord injury Mindy L. Aisen, MD; William Brown, MD, FRCP (C); and Michael Rubin, MD, FRCP (C)
Article abstract-Spontaneous activity on the EMG examination is traditionally ascribed to disease of the lower motor neuron when present in muscles well below the level of para- or quadriplegia despite the absence of any detectable peripheral nerve injury. It is uncertain whether it reflects transient paralysis of transmission (related to clinical spinal shock) or irreversible postsynaptic damage. We performed serial EMG studies of lower extremities and paraspinal muscles on eight young, previously healthy adults, commencing 2 t o 9 weeks after acute cervical cord injury. All had stimulated single-fiber EMG (SFEMG) studies at 6-month intervals t o determine whether irreversible postsynaptic damage of the anterior horn cell had occurred. MRI and nerve conduction excluded patients with evidence of distal cord injury or peripheral neuropathy. All patients had spontaneous activity in all muscles tested, persisting after spinal shock had resolved. Jitter was present on SFEMG in three of eight patients 6 months after injury. Four of five patients retested 12 months after injury had abnormal jitter, including three who initially had normal SFEMG studies. We conclude that there is electrophysiologic evidence of trans-synaptic distal cord dysfunction following acute spinal cord injury. SFEMG studies suggest that anterior horn cell dropout occurs during the 1st year after injury. NEUROLOGY 1992;42:623-626
Spontaneous activity (SA) in the form of fibrillation potentials (FP) and positive sharp waves (PSW) as seen on EMG examination is traditionally ascribed to disease of the lower motor neuron, which extends from the anterior horn cell in the ventral horn to distal muscle.' However, SA occurs i n disease apparently limited t o the upper motor neuron2-11 and in muscles well below the level of a lesion causing para- or quadriplegia despite the absence of any detectable peripheral nerve The frequency, prognostic implications, and etiology of this abnormal finding have not been thoroughly elucidated. Prior studies have not followed the time course of EMG abnormalities and have not defined the relationship of EMG changes to clinical weakness,
spasticity, and ultimate improvement. In addition, they have not addressed the pathophysiology of these apparent caudal effects of rostra1 cord trauma. At present, it is not known whether the EMG changes reflect transient paralysis of transmission (related to clinical spinal shock) o r irreversible postsynaptic damage. We undertook t h e present study to gain a n understanding of the evolution of EMG changes in subacute cervical spinal cord injury by performing serial EMG studies while chronicling ongoing changes in neurologic examination as patients progressed from spinal shock to the spastic phase. The integrity of anterior horn cells caudal to the lesion site was assessed with stimulated single-fiber EMG (SFEMG) at 6-month intervals.
From The Burke Rehabilitation Center (Dr. Aisen), Cornell University Medical College, White Plains, NY; the Division of Neurology (Dr. Brown), University Hospital, London, ON, Canada; and the Department of Neurology (Dr. Rubin). The New York Hospital, Cornell University Medical College, New York, NY. Supported by a grant from the American Paralysis Association. Received May 21, 1991. Accepted for publication in final form August 21, 1991 Address correspondence and reprint requests to Dr. Mindy L. Aisen, The Burke Rehabilitation Center, Cornell University Medical College, 785 Mamaroneck Avenue, White Plains, NY 10605.
March 1992 NEUROLOGY 42 623
’able.Spontaneous activity in paraspinal (PS)and lower extremity (LE) muscles Weeks postinjury Pt no.
Clinical
1
25 yo fall C6-7 sensory complete
2
23 yo diving injury C-6 sensory complete
3
16 yo motor vehicle accident c-7 sensory complete
4
16 yo diving injury c-4 sensory complete
5
19 yo gunshot wound T-1 sensory complete
6
17 yo diving injury c-7 sensory incomplete
7
8
0-4_
~
PS LE
2+
1+
s=o
PS LE
9-11 . PS LE
1+ 3+ S = l
o+ 2+ s=1
2+ 2+ s=2
3+ 3+ s=3
0 1+ s=1
0 1+ S=l
16-20
PS LE
PS LE
1+
1+
s = 2:l:
4+
3+
s=o
0
0
s=o
3+
1+
s=o
2+
0
s =I:>
4+ 3+ S=l
3+
2+
2+ 1+ s=2
1+
o+
s=l
o+ 1+ s=l:’: s = 2”
4+
3+
s=o
2+ s=2
2+
Methods. Eight patients meeting inclusion criteria were sequentially selected upon admission to The Burke Spinal Cord Injury Inpatient Service; clinical characteristics are summarized in the table. All were previously healthy young adults (ages 16 t o 30 years) admitted from rehabilitation 2 t o 9 weeks after traumatic cervical spinal cord injury; patient 3 was the only female studied. All had complete motor paralysis at the time of entry. Patients with evidence of lower limb or lumbar trauma were excluded. The experimental protocol was approved by The Burke Rehabilitation Center Committee for Human Rights i n Research, and written consent was obtained from all participants. To document the integrity of the peripheral nervous system below the level of the lesion, all had normal superficial peroneal conduction
1+
1+
s = 3“
6mos
12 mos
0
Normal
Jitter
1+
0
Normal
Normal
2+
2+
Normal
Jitter
Jitter
Jitter
Jitter
s = 3”
s =1“
1+ 2+ S=l”
0 0 s=2*
2+ 3+ S=l
2+
3+
Normal
0
0
Normal
s=1
s = 3s: -
t
1+ 3+
s=3:+
Single-fiber EMG
0
s = 3*
t 1+ 3+
21-28 PS LE
s = 2“
S=l
Spontaneous activity guide O+ = No positive wavesifibrillation. 1+ = Positive waves/fibrillation a t one site. 2+ = Positive waves/fibrillation occasionally present a t 22 sites. 3+ = Positive wavedfibrillation a t most sites. 4+ =Abundant positive waves/fibrillation a t all sites.
624 NEUROLOGY 42 March 1992
12-15
~~~
1+ 2+
30 yo skiing accident c-5 sensory incomplete 27 yo diving injury C-6 sensory incomplete
_ 5-8 _
o+
1+ s=3*
Jitter
1+ 1+
s = 3”
Spasticity scores ( S ) 0 = Flaccid areflexia. 1 = No increase in tone. 2 = Slight increase in tone, giving a “catch” when limb moved. 3 = More marked increase, but affected part easily flexed. 4 = Passive movement difficult. 5 = Rigid in flexion or extension.
Jitter
*Treated with baclofen. ? Motor recovery.
velocities. Six had normal peroneal somatosensory evoked potentials (stimulating a t the knee and recording over lumbar and midthoracic cord). Patient 5 had no cord potential, a finding in 2% of controls in our laboratory, and patient 7 refused evoked potential study. All patients had MRI studies of cervical, thoracic, and lumbar spine t o exclude the possibility of structural cord disease extending below injury level. Although patients 3 and 6 had evidence of L3-4 disk degeneration, no abnormality of cord or cauda equina was noted in any patient. EMG studies of bilateral T-12 and L-5 paraspinal muscles and of right vastus lateralis, anterior tibialis, biceps femoris, and medial gastrocnemius muscles were performed during the 1st week after admission t o Burke, and repeated at approximately 3-week intervals. EMG
changes were graded according to criteria established by Kimura.' Physical examination was performed immediately before EMG to grade motor power (0 to 5 ) , reflex changes, and spasticity (Ashworth scoreI2). Stimulated SFEMG was performed by percutaneously stimulating the peroneal nerve and recording jitter at a single neuromuscular junction, adapting previously described methods.13 The deep peroneal nerve was stimulated at the neck of the fibula using constant-current stimuli at a frequency of 10 Hz, and single-fiber potentials were recorded by a single-fiber needle placed in the anterior tibialis muscle. In stimulated SFEMG, normal jitter is defined as the square root of the normal value seen in conventional single-fiber studies (560 psec for the tibialis anterior muscle). SFEMG was considered abnormal if jitter exceeding this value was present a t two (or more) of 20 sites. SFEMG was performed a t 6 and 12 months after injury.
Results. As seen in the table, all patients had persistent and widespread SA involving muscles of the trunk and legs; EMG changes are designated a s paraspinal (PS) or lower extremity (LE), including vastus lateralis, biceps femoris, anterior tibialis, and medial gastrocnemius. Two patients initially studied 4 weeks after injury had EMG changes. Patient 6 was first studied 2 weeks after injury, a t which time no PSW or FP were seen; 3 weeks later, PSW and FP developed. Although the extent of FP and PSW in PS as opposed to LE musculature varied within individuals, overall axial and appendicular involvement were equivalent. The degree of PSW and FP gradually rose, then fell over time after injury, peaking in 9 to 11 weeks after injury and resolving in most cases by 28 weeks after injury. The presence of FP and PSW did not correlate with clinical state, as shown in the table, in all but patient 6. FP and PSW were present during the spinal shock phase and persisted during the spastic phase. There w a s no a p p a r e n t relationship between degree of F P and PSW and severity of spasticity or severity of cord injury (ie, FP and PSW were noted in patients regardless of sensory function) in seven patients, all of whom had persistent complete motor paralysis. Patient 6, however, developed substantial voluntary motor control during the 12th week after injury, at which time EMG abnormalities abated. SFEMG was normal in five of eight patients 6 months after injury; patients 4,7, and 8 had abnormal jitter at that time. These patients suffered from the anatomically highest structural and functional cord injuries in the group, although they differed clinically in degree of spasticity and sensory loss. Five patients were retested 12 months after injury, and four of five had abnormal jitter, including three who initially had normal SFEMG studies. Discussion. In this study, all patients had diffuse and widespread FP and PSW in lumbosacral-innervated muscles. These p a t i e n t s had cervical myelopathy and no clinical, other electrophysiolog-
ic, or radiographic evidence of distal cord or lower motor neuron pathology. An appreciation of the association between EMG changes a n d upper motor neuron disease, and an understanding of the abnormal SA in muscles supplied by spinal cord substantially caudal to the area of injury, is clinically important. Physicians should not attribute this finding t o focal radiculopathy, which could then lead to unnecessary diagnostic or surgical procedures. Another major finding was t h e presence of abnormal jitter on SFEMG in six patients, developing in three patients 6 to 12 months after injury. As reinnervation occurs, recorded action potentials become increasingly complex, and jitter commonly develops. Progressive trans-synaptic degeneration of motor neurons occurring in the lumbar spinal cord following cervical injury is a potential explanation for the observed subacute signs of denervation (PSW, FP) and chronic signs of reinnervation (jitter). PSW and FP are nonspecific abnormalities that occur in disease of muscle,14neuromuscular junction,15 a n d a n t e r i o r horn ce11,16 b u t EMG is employed as a tool for recognizing partial denervation. SA is not associated with disuse atrophy.' The mechanism by which SA develops has not been fully elucidated. There is evidence that denervation hypersensitivity to acetylcholine plays a n important role in its de~elopment,'~ although other data conflict with this hypothesis.18 Another theory invokes a specific trophic effect of peripheral nerve on m u ~ c 1 e . lThese ~ observations have led t o the widely accepted clinical tenet that SA is a sign of disease of the lower motor neuron. However, several studies have demonstrated the presence of PSW and FP in disease apparently limited to the upper motor neuron, both in ~ t r o k and e ~ in ~ ~myelop~ ~ a thy. 6-1 Goldkamp2 studied 116 stroke patients and found PSW and FP in almost 70%. The peak incidence occurred 4 to 4% weeks after the acute event, with greater PSW and FP in the upper than lower extremities, suggesting a cerebral pattern. These abnormalities were present despite normal nerve conduction studies. Rosen et a16found PSW and FP in six of seven patients studied during spinal shock, which largely resolved after the spastic phase developed, suggesting that during spinal shock, functional depression of the anterior horn cell occurred, and that anterior horn cells recovered when spinal shock resolved. However, Van Alphen et a17 found actual anterior horn cell loss well below the site of spinal injury at postmortem in three quadriplegic patients, and Brown et alRdemonstrated that hemisection of the macaque spinal cord in the thoracic region resulted in a 20% loss of anterior horn cells in the lumbosacral cord. These findings may indicate that anterior horn cell degeneration and dropout is the source of SA after cord transection. Other investigator^^-^^ have found that PSW and March 1992 NEUROLOGY 42 625
F P a r e not confined to t h e spinal shock phase. Subsequent studies20-22 indicated that PSW and FP develop by 3 weeks after injury a n d gradually resolve over time. B r a n d s t a t e r a n d Dinsdale" raised the possibility t h a t SA below the level of injury may be due to spinal cord trauma over a significant longitudinal segment of cord, and in no s t u d y w a s t h i s i d e a objectively a d d r e s s e d . Furthermore, examination of differences in prognosis between patients who do or do not have PSW and FP has not been performed. I n o u r s t u d y , e i g h t of e i g h t p a t i e n t s w i t h myelopathy and no identifiable pathology of lower motor neuron had persistent and diffuse PSW and FP in lumbosacral-innervated musculature. I n most patients, PSW a n d FP appeared within 6 weeks of injury, peaked 9 to 11 weeks after injury, and resolved by 28 weeks after injury. This time course is essentially that which is seen following acute axonotmesis and subsequent reinnervation. There was no clear relationship between resolution of the spinal shock phase and EMG abnormalities, arguing against a transient dysfunctional neuronal state as the etiology for SA. The degree of PSW and FP did not correlate with axon length. A low degree of PSW and FP may signify a better prognosis for motor recovery, as seen in patient 6. Six patients developed abnormal jitter by 12 months after injury. The time course and degree of SFEMG abnormality bore no relationship to earlier EMG changes. This finding may signify evolving motor neuron dropout and collateral reinnervation and in vivo confirmation of the pathologic findings of Van Alphen et al' and Brown et al.8 It raises the possibility that lower motor neuron EMG findings in upper motor neuron disease are due to distant neuronal degeneration, as it provides evidence of reinnervation and reorganization of the motor unit during the chronic phase. Further investigation to define this phenomenon and to establish etiologic factors is required to understand the pathophysiology and prognosis of spinal cord injury lesions and to plan strategies for intervention.
Refe.rences 1. Kimura J . Electrodiagnosis in diseases of nerve and muscle: principles and practice. 2nd ed. Philadelphia: F.A. Davis, 1989.
626 NEUROLOGY 42 March 1992
2. Goldkamp 0. Electromyography and nerve conduction studies in 116 patients with hemiplegia. Arch Phys Med Rehabil 1967;48:59-63. 3. Chokroverty S, Medina J. Electrophysiological s t u d y of hemiplegia: motor nerve conduction velocity, brachial plexus latency a n d EMG. Arch Neurol 1978;35:360-363. 4. Bhala RP. Electromyographic evidence of lower motor neuron involvement in hemiplegia. Arch P h y s Med Rehabil 1969;50:632-637. 5. Brown WF, Snow R. Denervation in hemiplegic muscles. Stroke 1990;21:1700-1704. 6. Rosen JS, Lerner IM, Rosenthal AM. Electromyography in spinal cord injury. Arch Phys Med Rehabil 1969;50:271-273. 7. Van Alphen HA, Lammers H J , Walder HAD. On remarkable reaction of motor neurons of lumbosacral region after traumatic transection in man. Neurochirurgia (Stuttg) 1962;8:328-330. 8 Brown WF, Milner-Brown HS, Ball M, Girvin JP. Control of t h e m o t o r c o r t e x o n s p i n a l m o t o n e u r o n e s i n m a n . In: Desmedt J E , ed. Cerebral motor control in man: long loop mechanisms. Progress in clinical neurophysiology, vol. 4. Basel: Karger, 1978:246-262. 9 Nyboer V J , J o h n s o n H E . Electromyographic findings in lower extremities of patients with traumatic quadriplegia. Arch Phys Med Rehabil 1971;52:256-259. 10. O'Hare VM, Abbot GH. EMG evidence of lower motor neuron injury i n cervical spinal cord injury. Proc Ann Con Spinal Cord Inj Center 1967;17:25-35. 11. Spielholz NI, Sell GH, Goodgold J, Rusk HA, Greens SK. Electrophysiologic s t u d i e s in p a t i e n t s with s p i n a l cord lesions. Arch Phys Med Rehabil 1972;53:558-562. 12. Ashworth B. Preliminary trial of carisoprodol i n multiple sclerosis. Practitioner 1964;192:540-542, 13. J a b r e JF, Chirico-Post J, Weiner M. Stimulation single fiber EMG in myasthenia gravis. Muscle Nerve 1989;12:38-42. 14. Buchthal F, Rosenfalck P. Spontaneous electrical activity of h u m a n m u s c l e . E l e c t r o e n c e p h a l o g r Clin Neurophysiol 1966;20:321-336. 15. Peterson I, Broman AM. Electromyographic findings in a case of botulism. Nard Med 1961;65:259-261. 16. Johnson EW, Guyton J D , Olson KJ. Motor nerve conduction velocity studies in poliomyelitis. Arch Phys Med Rehabil 1960;41:185-190. 17. Thesleff S. Supersensitivity of skeletal muscle produced by botulinum toxin. J Physiol (Land) 1960;151:598-607. 18. Miled R. The acetylcholine sensitivity of frog muscle fibers after complete a n d partial denervation. J Physiol ( L a n d ) 1960;151:1-23. 19. Goodgold J, Eberstein A. Electrodiagnosis of neuromuscular disease, 3rd ed. Baltimore: Williams & Wilkins, 1983. 20. Taylor RG, K e w a l r a m a n i LS, Fowler WM. Electromyographic findings in lower extremities of patients with high spinal cord injury. Arch Phys Med Rehabil 1974;55:16-23. 21. Onkelinx A, Chantraine A. Electromyographic study of paraplegic patients. Elcctroniyogr Clin Neurophysiol 1975;15:7181. 22. Brandstater ME, Dinsdale SM. Electrophvsiological studies in t h e assessment of spinal cord lesions-. Arch Phys Med Rehabil 1976;57:70-74.
Electrophysiologic changes in lumbar spinal cord after cervical cord injury Mindy L. Aisen, William Brown and Michael Rubin Neurology 1992;42;623 DOI 10.1212/WNL.42.3.623 This information is current as of March 1, 1992 Updated Information & Services
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Neurology ® is the official journal of the American Academy of Neurology. Published continuously since 1951, it is now a weekly with 48 issues per year. Copyright © 1992 by AAN Enterprises, Inc.. All rights reserved. Print ISSN: 0028-3878. Online ISSN: 1526-632X.
