~~~
~~~~
An adult male with C-7quadriplegia developed neck pain. Axillary F central latencies were prolonged, and MRI showed a syrinx extending to C-1. After shunting, F latencies normalized. At subsequent follow-up, a rostra1 syrinx persisted by magnetic resonance imaging (MRI); motor evoked potential (MEP) latencies were prolonged but F latencies were normal. Later, the syrinx was less distended by MRI, MEPs normalized, and strength improved. We discuss the electrophysiologic methods available for diagnosing and monitoring posttraumatic syringomyelia. 0 1992 John Wiley & Sons, Inc.
Key words: posttraumatic syringomyelia motor evoked potentials electrodiagnosis spinal cord injury MUSCLE 81 NERVE 15:755-760 1992
AAEM CASE REPORT #24: ELECTRODIAGNOSIS IN POSTTRAUMATIC SYRINGOMYELIA JAMES W. LITTLE, MD, PhD, and LAWRENCE R. ROBINSON, MD
Months to years following traumatic spinal cord injury (SCI), a fluid-filled cyst can insidiously develop within the spinal cord. Posttraumatic syringomyelia (PTS) is a form of noncommunicating syringomyelia; the one or more syrinx cavities are not in continuity with the central canal, but rather develop within the gray matter of the cord.5 As one or more cysts of PTS enlarge, patients may experience ascending myelopathy with resulting new neurologic impairment above the level of the original spinal cord injury, or below, if the initial cord injury was incomplete. T w o to 5% of patients with traumatic SCI will develop clinically significant PTS.22230 Many more are likely to have cystic changes in the spinal cord on magnetic resonance imaging (MRI).l 6 Symptoms and signs of PTS can be subtle, and clinical diagnosis is often difficult. While MRI is sensitive for the diagnosis of PTS, it can also reveal common cystic changes that are not functionally sig-
From the Department of Rehabilitation Medicine, University of Washington School of Medicine, Seattle, Washington (Drs. Little and Robinson) and V.A. Medical Center, Seattle, Washington (Dr Little). Acknowledgment: This work was supported by the Rehabilitation Research and Development Service of the Department of Veterans Affairs and the Spinal Cord Research Foundation of the Paralyzed Veterans of America. Address reprint requests to American Association of Electrodiagnostic Medicine, 21 Second Street SW, Suite 306, Rochester, MN 55902 Accepted for publication December 7, 1991 01992 James W. Little, MD, PhD, and Lawrence R. Robinson, MD. Published by John Wiley & Sons, Inc CCC 0148-639W921070755-06$04.00 0 1992 John Wiley & Sons, Inc.
AAEM Case Report #24: Posttraumatic Syringornyelia
nificant.16 Moreover, MRI may fail to resolve changes that are small anatomically but which affect functionally important intact tracts in the spinal cord. Recurrence of cysts after surgical shunting is common,3,22,26,30 yet difficult to assess over time using MRI. It is in this context that electrodiagnosis often plays an important role in the management of patients with PTS. Upper extremity F waves, somatosensory evoked potentials (SEPs), transcortical motor evoked potentials ((MEPs), and needle electromyography (EMG) can be abnormal in PTS, and are potentially useful methods for assessing spinal cord function. CASE REPORT
A 43-year-old male, who had sustained C7 quadriplegia 17 years previously, presented with neck pain radiating into the right arm. The pain was described as sharp, shooting, and progressively more intense over the prior 4 years. It was aggravated by push-ups on wheelchair armrests and by shoulder flexion with extended elbows. Past medical history was significant for his previously mentioned quadriplegia, which was due to C-5 to C-6 vertebral dislocation from a diving accident. Subsequent to this injury, the patient underwent an anterior bony cervical fushion. Five years prior to this admission, there was progressive pain and sensory loss in the upper extremities. PTS was suspected and the patient underwent a C-4 to C-7 laminectomy with syringosubarachnoid shunt placement at C-7, with relief of pain but no improvement in sensation.
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The physical examination at the time of this admission was consistent with motor complete C-7 quadriplegia; an asymmetry of elbow extension strength with the right 515 and left 3/5 was found, and was reported by the patient as having been present since the original SCT. Sensation t o light touch was preserved in the C-8 derniatome and above, and was absent below. Pin-prick sensation
was preserved over the face but was impaired in C-2 to C-4 dermatomes and absent in C-5 and below. Muscle stretch reflexes were absent in the upper extremities. MRI revealed a syrinx extending from the lower cervical cord to the medulla (Fig. la). Needle EMG was performed with a monopolar or concentric needle electrode focusing on mus-
B C FIGURE 1. MRI of posttraumatic syrinx, preshunting and postshunting. Magnetic resonance imaging, T1 -weighted images: (a) preshunting; (b) 12 months postshunting, and (c) 28 months postshunting. Preshunting the syrinx extends caudally to at least the rostral C-5 vertebral body and, at 12 months postshunting, it ends at the mid-C-4 body, suggesting successful shunting of only the caudal portion of the syrinx. At 28 months, there is less distention of the syrinx on MRI than at 12 months postshunting; the anterior-posterior diameter of the syrinx is 0.39 versus 0.56 (as a proportion of the anterior-posterior diameter of the C-2 vertebral body). Also at 28 months, the rostral border of the syrinx is pointed, again suggesting loss of distention versus its rounded, distended appearance at 12 months.
756
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cles near the level of the patient's original SCI. Nerve conduction studies were performed in a standard manner with surface recording and stimulation.' For F-wave latency determination, the shortest latency of more than 10 responses was used. Axillary F central latency (AxFCL) was determined according to the method of Wu and colleagues.31 AxFCL is the shortest F latency to 20 wrist stimulations minus the M latency to axillary stimulation at 25 cm from the sternal notch. This measurement eliminates distal slowing (e.g., from entrapment neuropathy) as a potential source of F-latency prolongation. MEPs were obtained with magnetic stimulation of the motor cortex using a Cadwel MES-10 stimulator. Recording was over biceps and triceps bilaterally. T o measure the peripheral conduction time, magnetic stimulation was performed over the cervical spine. Central motor conduction time (CMCT) was determined by subtracting the shortest cervical spine onset latency from the shortest scalp to muscle onset latency; electromagnetic scalp stimulation was performed without and with facilitation by slight voluntary recruitment of the muscle and the shortest latency used for the CMCT calculation. In our laboratory, the upper limit of normal for CMCT to biceps is 8.0 ms. We do not yet have enough data to establish a valid normal limit for CMCT to triceps, but in our experience the CMCT to this muscle is longer than that to biceps, consistent with the longer neural pathway. At the time of the initial presentation, monopolar needle EMG of the biceps brachii and extensor carpi radialis longus bilaterally revealed normal insertional activity, no abnormal spontaneous activity, and normal motor unit action potentials (MUAPs) and interference pattern. The first dorsal interosseous had no abnormal spontaneous activity and no voluntary MUAPs. Nerve conduction studies revealed normal median and ulnar motor distal latencies and M-wave amplitudes. Motor conduction velocities were all normal except for a left ulnar motor velocity of 44 m/s. Bilateral median and right ulnar antidromic sensory nerve potentials demonstrated mildly prolonged distal latencies (4.0 to 4.4 ms) and normal amplitudes (15 to 40 pV). AxFCLs were asymmetrically prolonged: left median 14.9 ms, right median 13.3 ms, left ulnar 11.8 ms, right ulnar 14.5 ms; the normal range is reported as 8.8 to 13.6 ms (3 SD). The F-latency range was normal for the median and ulnar nerves to wrist stim~lation.'~ Because of persistent symptoms, the patient underwent placement of a syringopleural shunt.
AAEM Case Report #24: Posttraumatic Syringornyelia
At the time of surgery, the cervical cord was noted to be bulging. With the syringostomy incision, fluid under high pressure projected up several feet. F waves were repeated 24 hours after surgery. A notable reduction in AxFCL was recorded from the left median and right ulnar nerves; the left median AxFCL decreased from 14.9 to 10.8 ms, and the right ulnar decreased from 14.5 to 10.4 ms (Fig. 2). Pain improved postoperatively, but strength, tendon reflexes, and sensory level did not change. One year after shunting, the patient had persistent, though less intense, neck and upper extremity pain. Repeat MRI revealed collapse of the syrinx in the lower cervical cord but its persistence rostrally (Fig. Ib). Axillary F central latencies remained within normal limits; however, these studies reflect function of the lower cervical cord at the C-8 to T-1 level. Concentric needle EMG now revealed giant MUAPs and a discrete interference pattern in the right biceps and extensor carpi radialis longus, and in the triceps bilaterally. Minimal abnormal spontaneous activity was noted in the right biceps only. At 20 months postshunting, CMCTs to the left biceps (8.6 ms left, 7.7 ms right) were prolonged and longer than those to the triceps (7.7 ms left, 6.7 ms right); this was unusual, because the upper motoneuron pathways supplying the triceps are longer than those for biceps. 'These results were considered consistent with a high cervical syrinx. Because of potential risks from further surgical procedures and because upper extremity strength was improving by myometry, additional shunting was not attempted at this time. T h e patient was sent home and advised to avoid strenuous physical activity. At 28 months after shunting, the patient reported a gradual improvement in symptoms. Repeat MEPs demonstrated a reduction in CMCTs: left biceps 6.0 ms, right biceps 7.4 ms, left triceps 6.5 ms, right triceps 5.1 ms. MRI showed less distention of the syrinx (Fig. Ic). Between 12 and 28 months postshunting, as MRI and CMCTs improved, maximal isometric strength by myometry increased from 3.3 to 11.2 lbs. in the right elbow extensors, 19.2 to 24.4 lbs in the right wrist extensors, and from 2.7 to 5.1 Ibs. in the left elbow extensors; it was unchanged in the left wrist extensors. DISCUSSION
T h e clinical presentation of p?'S can often be subtle and nonspecific, thus delaying diagnosis. As-
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I
FIGURE 2. F waves preshunting and postshunting. F waves to right ulnar nerve stimulation at the wrist and recording over the hypothenar muscles are shown preshunting (upper) and 24 hours postshunting (lower). Note the marked reduction in F-wave latency postshunting.
ceridirig loss of muscle stretch reflexes arid pinprick sensation are probably the most commoli presenting signs22~"0 of YTS and were seen in this patient. It is often difficult, however, to separate PTS-related signs and symptoms from those due to the original SC1 or due to superimposed entrapment neuropathies, common after SCI. 1224 Pain is not unusual after SCI and is often attributed to musculoskeletal disorders or to the SCI itself. Changes in muscle strength are not readily detected by manual muscle testing, especially in muscles already affected by the SCI. When weakness is present, it is often ascribed to disuse. 'Thus, the history and physical examination are not sufhciently sensitive or specific to diagnose and monitor PTS. Needle EMG is also not sensitive for detecting P'rS. Positive sharp waves and fibrillations are un-
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AAEM Case Report #24: Posttraumatic Syringomyelia
, a similar lack common in progressive PTS10"'322. of muscle membrane instability has been re orted in syringomyelia not associated with SCI."'" 'lhis has been attributed to slow niotoneuron loss with reinnervation by spared motoneurons2"; alternatively, McCornas and colleagues'9 has suggested that sick motoneurons may have "silent" synapses with neuromuscular transmission impaired but with the neurotrophic effect of motor axons on muscle preserved. A n y spontaneous activity that is observed may be as readily attributable to the prior SCl as to an enlarging syrinx. As seen in this patient, motor unit action potentials tend to be of large amplitude, long duration, and polyphasic in muscles clinically affected by PTS or other syringomyelia. 1,2232"Single fiber EMG (SFEMG) reveals increased fiber densities and frequent impulse blocking; increased fi-
El
".'
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her densities and impulse blocking are particularly prominent in patients with recent clinical progression of their syringomyelia.23 Taken together, the EMG observations suggest that gradual loss of anterior horn cells with compensatory collateral sprouting by spared motoneurons contributes to the pathophysiology of syringomyelia. Nevertheless, serial quantitative EMG studies would likely be necessary to distinguish changes in MUAP morphology due to PTS from those due to the original SCI. Conventional nerve conduction studies are often normal in patients with PTS. Preserved sensory nerve action potentials are a well-known electrodiagnostic feature of syringomyelia, l 3 due to the preganglionic nature of the lesion; they were well preserved in this patient. The compound muscle action potential (CMAP) might be expected to show a decreased amplitude if sufficient loss of motoneurons occurs at the appropriate segmental level. This would likely be a late change, because compensatory sprouting would be expected to accommodate for slow motoneuron loss. Peripheral nerve conduction studies may be helpful, however, to detect entra ment neuropathies which are common after SCI.', There is some evidence to suggest patients with syringom elia are especially susceptible to entrapments, lO,lff118,29 possi-
!
bly due to the "double crush syndrome"27 or loss of protective nociceptive sensation due to the syrinx. The unilateral slowing of ulnar motor conduction seen in our patient is consistent with a superimposed ulnar neuropathy. Motor unit counting might allow quantitative follow-up of patients with PTS over time. While this technique has been reported predominantly in small hand or foot muscles,6 a more recent method has been described for obtaining estimates of motor-unit number from large proximal muscles.' Loss of motoneurons has been demonstrated with aging' and in motoneuron disease.*' Serial motor-unit counting in muscles immediately rostral to the SCI may be a sensitive way to detect an enlarging syrinx, despite compensatory motor axon sprouting that preserves CMAP amplitude. The sensitivity of this technique for diagnosing and monitoring PTS remains to be determined. F-wave responses appear to be a sensitive indicator for detecting and monitoring PTS' 1,20,*2 Rossier and colleagues" noted prolonged F-wave latencies in 9 of 9 patients with PTS; in 4 of 5 , F waves improved postshunting. Pieoglou-Harmoussi and colleagues" demonstrated prolonged F-wave latencies in 16 of 22 cases of syringomyelia
AAEM Case Report #24: Posttraurnatic Syringornyelia
from various causes. Prolongation in F-wave latencies likely reflects slowing at the anterior horn cell, because peripheral conduction is usually normal. Our patient had clearly prolonged AxFCLs before shunting, which returned to normal withint 24 hours after shunting, supporting the hypothesis that F responses may be quite sensitive to the degree of compression from the cyst. Unfortunately, F-wave responses can usually only be obtained from C-8 to T-1 segments and are not available for examining upper cervical levels. In our patient, after shunting, the syrinx persisted rostral to this level and F waves were normal. Somatosensory evoked potentials (SEPs) may be abnormal in PTS, and recent interest has focused on subcortical potentials. Anderson and colleagues* reported normal median SEP scalp responses in 9 of 9 patients with syringomyelia; however, they did find abnormally small or absent cervical potentials and prolonged central sensory conduction times in 6 of these 9 patients. Jabbari and colleagues1' found abnormal median andlor posterior tibia1 SEPs in 72% (16 of 22) of patients with syringomyelia of various causes; 10 showed absence of one or more cervical or cortical potentials, and 7 showed slowed central sensory conduction times. Mean transverse diameter of the syrinx by MRI was significantly larger in patients with abnormal SEPs (16.2 mm) than in those with normal SEPs (7.5 mm). Postoperative SEPs were performed in 8 patients and did not reflect the postoperative clinical course. Others have reported loss of the N-13 to P-13 cervical potential but preservation of the P14 far-field potential in syringomyelia. 12,28 Thus, SEP abnormalities are consistent with the anatomic origin of the PTS cyst in the gray matter of the cord.5 The relative sensitivity of SEPs for diagnosing PTS and its usefulness in monitoring the status of a syrinx postshunting remain to be determined. MEPs may be one of the more useful electrophysiologic methods for detecting and following PTS over time. A recent case report has demonstrated prolongation of CMCTs in a patient with PTS followed b significant improvement 2 weeks after shunting? Prolonged CMCT has been reported in a case of nontraumatic syringomyelia,8 but not in 2 other cases4 In the patient reported here, CMCTs were mildly prolonged to the left biceps and demonstrated a curious reversal of latency, with CMC'Ts to biceps longer than those to triceps at the time of the enlarged rostral cervical syrinx. This finding implicates the anterior horn cell or spinal interneurons as the site of conduc-
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tion delay rather than descending motor tracts; such slowing may be based on the same mechanism as prolongation of F-wave latencies, where delay is thought to occur at the motoneuron cell body in the gray matter. After conservative management, our patient's syrinx was decreased on MRI, all CMCTs were shortened, and his upper extremity strength was improved. In contrast to F waves, MEPs are avialable at most segmental levels and, thus, can evaluate rostra1 cervical segments. In summary, electrodiagnostic methods can play an important role in the management of patients with PTS. F-wave analysis, MEPs, and perhaps SEPs and motor unit counting allow early detection of PTS and assessment of spinal cord function over time. They are particularly useful when tested serially for distinguishing neurologic compromise due to an enlarging syrinx from that of the initial SCI and from common associated peripheral nerve entrapments. These methods are also useful for detecting a recurrent syrinx after shunting.
REFERENCES 1. Aljure J , Eltorai I, Bradley WE, et al: Carpal tunnel syn-
drome in paraplegic patients. P a r a p l e p 1985;23:182. 2. Anderson NE, Frith RW, Synek V: Somatosensory evoked potentials in syringomyelia. J Neurol Neurosurg Psychiatry 1986;49:1407- 1410. 3. Barbaro NM, Wilson CB, Guntin PH, Edwards MSR: Surgical treatment of syringomyelia: Favorable results with syringopleural shunting. J Neurosurg 1984;61:531-538. 4. Barker AT, Freeston II., Jalinous R, Jarratt ]A: Magnetic stimulation in clinical practice, in Rossini PM, Marsden CD (eds): Nun-Invasive Stimulation of Brain and Spinal Cord. New York, AR Liss, 1988, p p 231-241. 5. Barnett HJM, Jousse AT: Posttraumatic syringomyelia (cystic myelopathy), in Viiiken PJ, Bruyn GW (eds): Handbook of Clinical A'eurology. Amsterdam, North Holland, 1976, VOI 26, pp 113- 157. 6. Brown WF: Quantitative assessment of the outpatient of' muscles and motor unit estimates, in Brown WF (ed): The Physiologicul and Technical Ba.~ihof Electromyography. Boston, Butterworths, 1984; pp 257-286. 7. Brown WF, Strong MJ, Snow R: Methods for estimating numbers of motor units in biceps-brachialis muscles and losses of motor units with aging. Muscle Nerve 1988;11:423-432. 8 . Caramia MD, Zarola F, Spadaro M, Pardal AM, Bernardi G: Neurophysiologic testing of the central impulse propagation characteristics in patients with sensorimotor disorders, in Rossini PM, Marsden CD (eds): Nun-Inuasive Stimulation of Brain and Spinal Cord. New York, AR Liss, 1988, pp 193-206. 9. DeLisa JA, Mackenzie K, Baran EM: Manual of Neme Con-
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duction Velocity and Somatosensory Evoked Potentials (2 Ed). New York, Raven Press, 1987. 10. DiBenedetto M, Rossier AB: Electrodiagnosis in post-traumatic syringomyelia. Paraplegza 1977;14:286-295. 11. Dyro FM, Rossier AB: Electrodiagnostic abnormalities in 15 patients with post-traumatic syringomyelia: pre- and post-operative studies. Paraplegza 1985;23:233-242. 12. Emerson RG, Pedlcy '1.A: Effect of cervical spinal cord lesions on early components of the median nerve somatosensory evoked potential. NeuroloLgy 1986;36:20-26. 13. Fincham RW, Cape CA: Sensory nerve conduction in syringoniyelia. Neurology (Minneap) 1968;18:200-201. 14. Fisher MA: F response latency determination. Muscle Nenie 1982;5:730-734. 15. Glatzel W, Gruner JU: Results of electromyographical and electroneurographica1 investigations concerning syringomyelia. Eur Neurol 1976;14:60-67. 16. Hussey RW, Ha CY, Ujjay M, Lipper M, Kubota R: Prospective study of the occurrence rate of post-traumatic cystic degeneration of the spinal cord utilizing magnetic resonance imaging. J Am Para Soc 1990; 13: 16. 17. Jabbari B, Geyer C, Gunderson C, Chu A, Brophy J , McBurney JW, Jonas B: Somatosensory evoked potentials and magnetic resoiiaiice imaging in syringomyelia. Electroencephalogr Clin Neurophysiol 1990;77 :277 - 285. 18. ,Jacobi HM, Krott HM: Ulnarisparesen bei Syringomyelze. Nervenarzt 1975;46:68-72. 19. McComas AJ, Uptori ARM, Jorgenscn PB: Serial studies of sick motoneurons: T h e silent synapses. Excerpta Medica Znt Congr Series 1975;360:84-90. 20. Pieoglou-Harmoussi S, Fawcett PRW, Howel D, Barwick DD: F-responses in syringomyelia. J Neurol Sci 1986;75:293-304. 21. Robinson LR, Little JW: Motor evoked potentials reflect spinal cord function in post-traumatic syringomyelia. Am .J Phys Med Rehabil 199 1 ;69:307-3 10. 22. Rossier AB, Foo D, Shillito 1 , Dyro FM: Posttraumatic cervical syringomyelia: Incidence, clinical presentation, electrophysiological studies, syrinx protein and results of conservative arid operative treatment. Brain 1985;108:439461. 23. Schwartz M, Stalberg E, Swash M: Pattern of segmental motor involvement in syringornyelia: A single fibre EMG study. J Neurol Neurosurg Psychiatry 1980;43:150- 155. 24. Stefaniwsky L, Bilowit DS, Prasad SS: Reduced motor conduction velocity of the ulnar nerve in spinal cord injured patients. Paraplegza 1980;18:21-24. 25. Strong MJ, Brown WF, Hudson A.J, Snow R: Motor unit estimates in the biceps-brachialis in amyotrophic lateral sclerosis. Mu.tcle Nerve 1988;11:415-422. 26. 'l'ator C, Bricena C: Treatment of syringomyelia with a syringosuharachnoid shunt. Can J Neurol Sci 1988;15:48-57. 27. Upton ARM, McComas A,J:The double crush in nerve elltrapment syndromes. Lancet 1973;2:359. 28. Urasaki E, Nada S, Kadoya D, Matsuzaki H, Yakota A, Matsuoka S: Absence of spinal N13-Pl3 and normal scalp far-field P I 4 in a patient with syringomyelia. Electroencephalogr Clin Neurophysiol 1988;7 1 :400-404. 29. Veilleux M, Stevens JC: Syringomyelia: Electrophysiologic aspects. Muscle Nerve 1987; 10:449-458. 30. Vernon JD, Silver JR, Ohry A: Post-traumatic syringomyeha. Paraplegaa 1982;20:339- 364. 31. Wu Y , Kunz JRM, Putnam T, Stratigos JS: Axillary F central latency: Simple electrodiagnostic technique for proximal neuropathy. Arch Phys Med Rehabil 1983;64:117- 120.
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~~~~
An adult male with C-7quadriplegia developed neck pain. Axillary F central latencies were prolonged, and MRI showed a syrinx extending to C-1. After shunting, F latencies normalized. At subsequent follow-up, a rostra1 syrinx persisted by magnetic resonance imaging (MRI); motor evoked potential (MEP) latencies were prolonged but F latencies were normal. Later, the syrinx was less distended by MRI, MEPs normalized, and strength improved. We discuss the electrophysiologic methods available for diagnosing and monitoring posttraumatic syringomyelia. 0 1992 John Wiley & Sons, Inc.
Key words: posttraumatic syringomyelia motor evoked potentials electrodiagnosis spinal cord injury MUSCLE 81 NERVE 15:755-760 1992
AAEM CASE REPORT #24: ELECTRODIAGNOSIS IN POSTTRAUMATIC SYRINGOMYELIA JAMES W. LITTLE, MD, PhD, and LAWRENCE R. ROBINSON, MD
Months to years following traumatic spinal cord injury (SCI), a fluid-filled cyst can insidiously develop within the spinal cord. Posttraumatic syringomyelia (PTS) is a form of noncommunicating syringomyelia; the one or more syrinx cavities are not in continuity with the central canal, but rather develop within the gray matter of the cord.5 As one or more cysts of PTS enlarge, patients may experience ascending myelopathy with resulting new neurologic impairment above the level of the original spinal cord injury, or below, if the initial cord injury was incomplete. T w o to 5% of patients with traumatic SCI will develop clinically significant PTS.22230 Many more are likely to have cystic changes in the spinal cord on magnetic resonance imaging (MRI).l 6 Symptoms and signs of PTS can be subtle, and clinical diagnosis is often difficult. While MRI is sensitive for the diagnosis of PTS, it can also reveal common cystic changes that are not functionally sig-
From the Department of Rehabilitation Medicine, University of Washington School of Medicine, Seattle, Washington (Drs. Little and Robinson) and V.A. Medical Center, Seattle, Washington (Dr Little). Acknowledgment: This work was supported by the Rehabilitation Research and Development Service of the Department of Veterans Affairs and the Spinal Cord Research Foundation of the Paralyzed Veterans of America. Address reprint requests to American Association of Electrodiagnostic Medicine, 21 Second Street SW, Suite 306, Rochester, MN 55902 Accepted for publication December 7, 1991 01992 James W. Little, MD, PhD, and Lawrence R. Robinson, MD. Published by John Wiley & Sons, Inc CCC 0148-639W921070755-06$04.00 0 1992 John Wiley & Sons, Inc.
AAEM Case Report #24: Posttraumatic Syringornyelia
nificant.16 Moreover, MRI may fail to resolve changes that are small anatomically but which affect functionally important intact tracts in the spinal cord. Recurrence of cysts after surgical shunting is common,3,22,26,30 yet difficult to assess over time using MRI. It is in this context that electrodiagnosis often plays an important role in the management of patients with PTS. Upper extremity F waves, somatosensory evoked potentials (SEPs), transcortical motor evoked potentials ((MEPs), and needle electromyography (EMG) can be abnormal in PTS, and are potentially useful methods for assessing spinal cord function. CASE REPORT
A 43-year-old male, who had sustained C7 quadriplegia 17 years previously, presented with neck pain radiating into the right arm. The pain was described as sharp, shooting, and progressively more intense over the prior 4 years. It was aggravated by push-ups on wheelchair armrests and by shoulder flexion with extended elbows. Past medical history was significant for his previously mentioned quadriplegia, which was due to C-5 to C-6 vertebral dislocation from a diving accident. Subsequent to this injury, the patient underwent an anterior bony cervical fushion. Five years prior to this admission, there was progressive pain and sensory loss in the upper extremities. PTS was suspected and the patient underwent a C-4 to C-7 laminectomy with syringosubarachnoid shunt placement at C-7, with relief of pain but no improvement in sensation.
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The physical examination at the time of this admission was consistent with motor complete C-7 quadriplegia; an asymmetry of elbow extension strength with the right 515 and left 3/5 was found, and was reported by the patient as having been present since the original SCT. Sensation t o light touch was preserved in the C-8 derniatome and above, and was absent below. Pin-prick sensation
was preserved over the face but was impaired in C-2 to C-4 dermatomes and absent in C-5 and below. Muscle stretch reflexes were absent in the upper extremities. MRI revealed a syrinx extending from the lower cervical cord to the medulla (Fig. la). Needle EMG was performed with a monopolar or concentric needle electrode focusing on mus-
B C FIGURE 1. MRI of posttraumatic syrinx, preshunting and postshunting. Magnetic resonance imaging, T1 -weighted images: (a) preshunting; (b) 12 months postshunting, and (c) 28 months postshunting. Preshunting the syrinx extends caudally to at least the rostral C-5 vertebral body and, at 12 months postshunting, it ends at the mid-C-4 body, suggesting successful shunting of only the caudal portion of the syrinx. At 28 months, there is less distention of the syrinx on MRI than at 12 months postshunting; the anterior-posterior diameter of the syrinx is 0.39 versus 0.56 (as a proportion of the anterior-posterior diameter of the C-2 vertebral body). Also at 28 months, the rostral border of the syrinx is pointed, again suggesting loss of distention versus its rounded, distended appearance at 12 months.
756
AAEM Case Report #24: Posttraumatic Syringomyelia
MUSCLE & NERVE
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cles near the level of the patient's original SCI. Nerve conduction studies were performed in a standard manner with surface recording and stimulation.' For F-wave latency determination, the shortest latency of more than 10 responses was used. Axillary F central latency (AxFCL) was determined according to the method of Wu and colleagues.31 AxFCL is the shortest F latency to 20 wrist stimulations minus the M latency to axillary stimulation at 25 cm from the sternal notch. This measurement eliminates distal slowing (e.g., from entrapment neuropathy) as a potential source of F-latency prolongation. MEPs were obtained with magnetic stimulation of the motor cortex using a Cadwel MES-10 stimulator. Recording was over biceps and triceps bilaterally. T o measure the peripheral conduction time, magnetic stimulation was performed over the cervical spine. Central motor conduction time (CMCT) was determined by subtracting the shortest cervical spine onset latency from the shortest scalp to muscle onset latency; electromagnetic scalp stimulation was performed without and with facilitation by slight voluntary recruitment of the muscle and the shortest latency used for the CMCT calculation. In our laboratory, the upper limit of normal for CMCT to biceps is 8.0 ms. We do not yet have enough data to establish a valid normal limit for CMCT to triceps, but in our experience the CMCT to this muscle is longer than that to biceps, consistent with the longer neural pathway. At the time of the initial presentation, monopolar needle EMG of the biceps brachii and extensor carpi radialis longus bilaterally revealed normal insertional activity, no abnormal spontaneous activity, and normal motor unit action potentials (MUAPs) and interference pattern. The first dorsal interosseous had no abnormal spontaneous activity and no voluntary MUAPs. Nerve conduction studies revealed normal median and ulnar motor distal latencies and M-wave amplitudes. Motor conduction velocities were all normal except for a left ulnar motor velocity of 44 m/s. Bilateral median and right ulnar antidromic sensory nerve potentials demonstrated mildly prolonged distal latencies (4.0 to 4.4 ms) and normal amplitudes (15 to 40 pV). AxFCLs were asymmetrically prolonged: left median 14.9 ms, right median 13.3 ms, left ulnar 11.8 ms, right ulnar 14.5 ms; the normal range is reported as 8.8 to 13.6 ms (3 SD). The F-latency range was normal for the median and ulnar nerves to wrist stim~lation.'~ Because of persistent symptoms, the patient underwent placement of a syringopleural shunt.
AAEM Case Report #24: Posttraumatic Syringornyelia
At the time of surgery, the cervical cord was noted to be bulging. With the syringostomy incision, fluid under high pressure projected up several feet. F waves were repeated 24 hours after surgery. A notable reduction in AxFCL was recorded from the left median and right ulnar nerves; the left median AxFCL decreased from 14.9 to 10.8 ms, and the right ulnar decreased from 14.5 to 10.4 ms (Fig. 2). Pain improved postoperatively, but strength, tendon reflexes, and sensory level did not change. One year after shunting, the patient had persistent, though less intense, neck and upper extremity pain. Repeat MRI revealed collapse of the syrinx in the lower cervical cord but its persistence rostrally (Fig. Ib). Axillary F central latencies remained within normal limits; however, these studies reflect function of the lower cervical cord at the C-8 to T-1 level. Concentric needle EMG now revealed giant MUAPs and a discrete interference pattern in the right biceps and extensor carpi radialis longus, and in the triceps bilaterally. Minimal abnormal spontaneous activity was noted in the right biceps only. At 20 months postshunting, CMCTs to the left biceps (8.6 ms left, 7.7 ms right) were prolonged and longer than those to the triceps (7.7 ms left, 6.7 ms right); this was unusual, because the upper motoneuron pathways supplying the triceps are longer than those for biceps. 'These results were considered consistent with a high cervical syrinx. Because of potential risks from further surgical procedures and because upper extremity strength was improving by myometry, additional shunting was not attempted at this time. T h e patient was sent home and advised to avoid strenuous physical activity. At 28 months after shunting, the patient reported a gradual improvement in symptoms. Repeat MEPs demonstrated a reduction in CMCTs: left biceps 6.0 ms, right biceps 7.4 ms, left triceps 6.5 ms, right triceps 5.1 ms. MRI showed less distention of the syrinx (Fig. Ic). Between 12 and 28 months postshunting, as MRI and CMCTs improved, maximal isometric strength by myometry increased from 3.3 to 11.2 lbs. in the right elbow extensors, 19.2 to 24.4 lbs in the right wrist extensors, and from 2.7 to 5.1 Ibs. in the left elbow extensors; it was unchanged in the left wrist extensors. DISCUSSION
T h e clinical presentation of p?'S can often be subtle and nonspecific, thus delaying diagnosis. As-
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I
FIGURE 2. F waves preshunting and postshunting. F waves to right ulnar nerve stimulation at the wrist and recording over the hypothenar muscles are shown preshunting (upper) and 24 hours postshunting (lower). Note the marked reduction in F-wave latency postshunting.
ceridirig loss of muscle stretch reflexes arid pinprick sensation are probably the most commoli presenting signs22~"0 of YTS and were seen in this patient. It is often difficult, however, to separate PTS-related signs and symptoms from those due to the original SC1 or due to superimposed entrapment neuropathies, common after SCI. 1224 Pain is not unusual after SCI and is often attributed to musculoskeletal disorders or to the SCI itself. Changes in muscle strength are not readily detected by manual muscle testing, especially in muscles already affected by the SCI. When weakness is present, it is often ascribed to disuse. 'Thus, the history and physical examination are not sufhciently sensitive or specific to diagnose and monitor PTS. Needle EMG is also not sensitive for detecting P'rS. Positive sharp waves and fibrillations are un-
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AAEM Case Report #24: Posttraumatic Syringomyelia
, a similar lack common in progressive PTS10"'322. of muscle membrane instability has been re orted in syringomyelia not associated with SCI."'" 'lhis has been attributed to slow niotoneuron loss with reinnervation by spared motoneurons2"; alternatively, McCornas and colleagues'9 has suggested that sick motoneurons may have "silent" synapses with neuromuscular transmission impaired but with the neurotrophic effect of motor axons on muscle preserved. A n y spontaneous activity that is observed may be as readily attributable to the prior SCl as to an enlarging syrinx. As seen in this patient, motor unit action potentials tend to be of large amplitude, long duration, and polyphasic in muscles clinically affected by PTS or other syringomyelia. 1,2232"Single fiber EMG (SFEMG) reveals increased fiber densities and frequent impulse blocking; increased fi-
El
".'
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her densities and impulse blocking are particularly prominent in patients with recent clinical progression of their syringomyelia.23 Taken together, the EMG observations suggest that gradual loss of anterior horn cells with compensatory collateral sprouting by spared motoneurons contributes to the pathophysiology of syringomyelia. Nevertheless, serial quantitative EMG studies would likely be necessary to distinguish changes in MUAP morphology due to PTS from those due to the original SCI. Conventional nerve conduction studies are often normal in patients with PTS. Preserved sensory nerve action potentials are a well-known electrodiagnostic feature of syringomyelia, l 3 due to the preganglionic nature of the lesion; they were well preserved in this patient. The compound muscle action potential (CMAP) might be expected to show a decreased amplitude if sufficient loss of motoneurons occurs at the appropriate segmental level. This would likely be a late change, because compensatory sprouting would be expected to accommodate for slow motoneuron loss. Peripheral nerve conduction studies may be helpful, however, to detect entra ment neuropathies which are common after SCI.', There is some evidence to suggest patients with syringom elia are especially susceptible to entrapments, lO,lff118,29 possi-
!
bly due to the "double crush syndrome"27 or loss of protective nociceptive sensation due to the syrinx. The unilateral slowing of ulnar motor conduction seen in our patient is consistent with a superimposed ulnar neuropathy. Motor unit counting might allow quantitative follow-up of patients with PTS over time. While this technique has been reported predominantly in small hand or foot muscles,6 a more recent method has been described for obtaining estimates of motor-unit number from large proximal muscles.' Loss of motoneurons has been demonstrated with aging' and in motoneuron disease.*' Serial motor-unit counting in muscles immediately rostral to the SCI may be a sensitive way to detect an enlarging syrinx, despite compensatory motor axon sprouting that preserves CMAP amplitude. The sensitivity of this technique for diagnosing and monitoring PTS remains to be determined. F-wave responses appear to be a sensitive indicator for detecting and monitoring PTS' 1,20,*2 Rossier and colleagues" noted prolonged F-wave latencies in 9 of 9 patients with PTS; in 4 of 5 , F waves improved postshunting. Pieoglou-Harmoussi and colleagues" demonstrated prolonged F-wave latencies in 16 of 22 cases of syringomyelia
AAEM Case Report #24: Posttraurnatic Syringornyelia
from various causes. Prolongation in F-wave latencies likely reflects slowing at the anterior horn cell, because peripheral conduction is usually normal. Our patient had clearly prolonged AxFCLs before shunting, which returned to normal withint 24 hours after shunting, supporting the hypothesis that F responses may be quite sensitive to the degree of compression from the cyst. Unfortunately, F-wave responses can usually only be obtained from C-8 to T-1 segments and are not available for examining upper cervical levels. In our patient, after shunting, the syrinx persisted rostral to this level and F waves were normal. Somatosensory evoked potentials (SEPs) may be abnormal in PTS, and recent interest has focused on subcortical potentials. Anderson and colleagues* reported normal median SEP scalp responses in 9 of 9 patients with syringomyelia; however, they did find abnormally small or absent cervical potentials and prolonged central sensory conduction times in 6 of these 9 patients. Jabbari and colleagues1' found abnormal median andlor posterior tibia1 SEPs in 72% (16 of 22) of patients with syringomyelia of various causes; 10 showed absence of one or more cervical or cortical potentials, and 7 showed slowed central sensory conduction times. Mean transverse diameter of the syrinx by MRI was significantly larger in patients with abnormal SEPs (16.2 mm) than in those with normal SEPs (7.5 mm). Postoperative SEPs were performed in 8 patients and did not reflect the postoperative clinical course. Others have reported loss of the N-13 to P-13 cervical potential but preservation of the P14 far-field potential in syringomyelia. 12,28 Thus, SEP abnormalities are consistent with the anatomic origin of the PTS cyst in the gray matter of the cord.5 The relative sensitivity of SEPs for diagnosing PTS and its usefulness in monitoring the status of a syrinx postshunting remain to be determined. MEPs may be one of the more useful electrophysiologic methods for detecting and following PTS over time. A recent case report has demonstrated prolongation of CMCTs in a patient with PTS followed b significant improvement 2 weeks after shunting? Prolonged CMCT has been reported in a case of nontraumatic syringomyelia,8 but not in 2 other cases4 In the patient reported here, CMCTs were mildly prolonged to the left biceps and demonstrated a curious reversal of latency, with CMC'Ts to biceps longer than those to triceps at the time of the enlarged rostral cervical syrinx. This finding implicates the anterior horn cell or spinal interneurons as the site of conduc-
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tion delay rather than descending motor tracts; such slowing may be based on the same mechanism as prolongation of F-wave latencies, where delay is thought to occur at the motoneuron cell body in the gray matter. After conservative management, our patient's syrinx was decreased on MRI, all CMCTs were shortened, and his upper extremity strength was improved. In contrast to F waves, MEPs are avialable at most segmental levels and, thus, can evaluate rostra1 cervical segments. In summary, electrodiagnostic methods can play an important role in the management of patients with PTS. F-wave analysis, MEPs, and perhaps SEPs and motor unit counting allow early detection of PTS and assessment of spinal cord function over time. They are particularly useful when tested serially for distinguishing neurologic compromise due to an enlarging syrinx from that of the initial SCI and from common associated peripheral nerve entrapments. These methods are also useful for detecting a recurrent syrinx after shunting.
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