Somatosensory evoked potentials (SEPs) and motor evoked potentials (MEPs) to transcranial and spinal stimulation from upper and lower limb muscles were elicited in 13 patients with syringomyelia. Seven had an associated Chiari type I anomaly. Diagnosis was confirmed by MRI. In 5 cases, SEPs and MEPs were performed before and after surgical treatment. Prolonged central motor conduction times or absent motor responses in upper or lower limbs were found in most patients. The greatest number of abnormalities was disclosed by measurement of CMCT followed by SEPs after tibia1 nerve stimulation. Two of 5 cases undergoing surgery improved clinically and showed reduction in CMCT after surgical treatment. Our study shows that MEPs were useful in the evaluation of neurophysiological status in syringomyelia patients, helping to estimate anterolateral spinal cord function. Key words: magnetic stimulation MEPs SEPs syringomyelia MUSCLE 81 NERVE 15:993-1001 1992
SEPS AND CNS MAGNETIC STIMULATION IN SYRINGOMYELIA MARTIN A. NOGUES, MD, ANA M A R ~ APARDAL, MD, MARCEL0 MERELLO, MD, and MIGUEL A. MIGUEL, MD
T h e corticospinal pathways are frequently involved in syringomyelia, and it is not uncommon to find early pyramidal signs in the lower limbs.9 This pyramidal tract dysfunction is the main cause of motor disability. Descending motor pathways may also be constricted at the cervicomedullary junction by an associated Chiari type I malformation. Transcranial magnetic stimulation of the motor cortex enables conduction in the central motor pathways to be studied readily in health and disMotor evoked potentials (MEPS) elicited by brain stimuli can be recorded rapidly and without discomfort.2 Abnormalities of central motor conduction time (CMCT) by this technique have been demonstrated in a variety of conditions such as motor neuron disease, degenerative ataxic diso r d e r ~and , ~ multiple sclerosis,’ among others. So
From the lnstituto de lnvestigaciones Neurol6gicas Ra61 Carea (Fleni). Buenos Aires, Argentina (Drs. Nogues and Merello); and Centro de Neurofisiologia Clinica y Terapia Fisica, Buenos Aires, Argentina (Drs. Pardal and Miguel). Acknowledgments. The authors are greatly indebted to Dr. Nicholas Murray for his helpful opinlon and suggestions for improving the manuscript. Address reprint requests to Dr. Martin A. Nogues, Fleni, Ayacucho 2166, 1112 Buenos Aires, Argentina. Accepted for publication November 1 , 1991 CCC 0148-639x1921090993-09 $04.00 0 1992 John Wiley & Sons, Inc.
SEPs and MEPs in Syringomyelia
far, few cases of syrin omyelia have been evaluated by this procedure.?$ In this study, we have correlated findings from motor studies with neurological signs and alteration in somatosensory evoked potentials (SEPs) in a series of syringomyelia patients. MATERIALS AND METHODS
Thirteen patients with syringomyelia, 6 females and 7 males, ages ranging from 19 to 53 years (mean 37.4 years), were studied. All had a classic syringomyelic syndrome with dissociated sensory loss, wasting, and weakness in upper limbs and a variable degree of spasticity in lower limbs. In 6, there was a bilateral Babinski sign, and 2 other patients showed a unilateral extensor plantar response. In the remaining 5 patients there was variable spasticity manifested by either increased tone or hyperreflexia. Joint position sense was impaired in all 4 limbs in one case, and in one or two limbs in 5 other patients. The integrity of the peripheral nerves was determined from normal nerve conduction studies. Associated radiological findings were a basilar impression in 1 case, and a Chiari type I anomaly in 7 cases. These diagnoses were confirmed by MRI scanning. Five patients underwent surgery, and a follow-up clinical and electrophysiological evaluation was performed 3 months postsurgery. Surgical treatment consisted of a syringosubarachnoid shunt (case 9), a foramen magnum decompression and ventricu-
Patients.
MUSCLE & NERVE
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993
loperitoneal shunt (cases 2 and lo), or a syringoperitoneal shunt (cases 12 and 13). T h e control group comprised 10 healthy subjects, 4 males and 6 females, ages 17 to 67 years (mean 43.7 years). Motor Evoked Potentials (MEPs). MEPs were recorded using a magnetic stimulator (Dantec) consisting of a high-energy capacitor bank which discharged transient 150 ks pulses via an electronic switching device into a circular coil (inner and outer diameters were 3 and 13 cm, respectively). The coil was placed in contact with the skin of the right or left scalp, roughly overlying the motor area of the hand (about 7 cm lateral to Cz and 1 to 2 cm in front of the Cz-earlobe line) and foot muscles (2 cm anterior to the vertex). T h e coil was moved over the scalp until optimal motor responses were localized. Stimulation intensity was expressed as a percentage of the maximal output delivered by the stimulator (2.5 T). In most cases, the threshold level was 40% to 45% of the stimulator output for upper limbs and 70% to 75% for lower limbs. To elicit reproducible MEPs during voluntary contraction, stimulus strength was increased 20% above threshold value. Recordings were obtained from surface electrodes on abductor pollicis brevis (APB) and flexor hallucis in all patients. In 2 cases, latencies to deltoid muscles were also measured. The patient was instructed to exert gentle voluntary contraction of the target muscle. Stimulation was repeated until two consecutive reproducible motor responses were obtained, and the shortest latency was used for analysis. T o separate the peripheral component from the total cortex-muscle time, we placed the coil just lateral to the spine, as close as possible to the exit foramina.' Central motor conduction time (CMCT) was calculated as the difference between the latency at cortical and spinal stimulation sites. Latencies and CMCTs were considered abnormal whenever they exceeded normal values by 2.5 SD.
Median nerves were recorded via needle electrodes on the Erb's point, on the seventh cervical spine process, and on the scalp positions overlying the sensory area for the hand (C3 and C4). A cephalic midfrontal (Fz) reference was used for all leads. The median nerve was stimulated at the wrist using 0.2-ms square-wave electrical pulses. The cathode electrode was positioned 2 cm proximal to the anode. Stimulus intensity was adjusted to produce a Somatosensory Evoked Potentials (SEPs).
994
SEPs and MEPs in Syringomyelia
visible twitch of the hallux without causing discomfort. Stimulus rate was 4/s. The tibial nerve was stimulated at the ankle, and evoked responses were recorded 2 cm posterior to the vertex and referred to Fz. At least 1024 responses were averaged with a 30-Hz to 1.5-Hz bandpass. T o confirm SEP reproducibility, each measurement was carried out at least twice. Latencies were measured to the peaks of the negative potentials and considered abnormal when they exceeded mean normal values by 3 SD. RESULTS
Ten of 13 patients had a prolonged CMCT on one (n = 4) or both sides ( n = 6) (Table 1). Two of the latter were the more severely handicapped (cases 12 and 13), and 1 (case 2) had an associated Chiari malformation. In case 11, no reproducible response could be elicited on one side, and the other side showed a slightly prolonged CMCT (10.5 ms). Mean total latency value after scalp stimulation and recording from APB muscle in controls was 21.5 ms (SD 1.56), whereas the CMCT was 8.5 ms (SD 0.36). While there was a tendency for the most affected patients to show more prolonged latencies, the magnitude of the delay seemed unrelated to the presence of a Chiari malformation or to clinical status. Stimulation at the cervical level elicited reproducible responses on both sides in all patients. Mildly prolonged latencies were observed in 2 patients (bilateral!y in l ) without entrapment neuropathies, in 1 patient (case 8) with gross cervical radiculopathy (Fig. l), and in 2 patients with a Chiari anomaly (cases 5 and 10). Recordings from foot muscles after scalp stimulation elicited normal MEPs on both sides in the 4 patients with mildest clinical symptoms, and in case 12. Conversely, MEPs could not be elicited from either foot in 2 severely disabled patients (cases 11 and 13). When obtainable, MEPs to foot muscles showed latencies within normal range. Figures 2 and 3 illustrate pre- and postoperative MEP recordings in a patient with syringomyelia (case 10).
MEP Studies.
Median and tibial nerve SEPs were performed bilaterally in all patients. Recordings were compared with normative data obtained from the 10 healthy subjects. Mean value for scalp N,, latency was 19.5 ms (SD 0.66); for N,, to N,, interpeak latency, 5.78 ms (SD 0.44); and for P,, after tibial nerve stimulation, 40.0 ms (SD 2.24). Eight of the 13 cases showed an abnormal central SEP Studies.
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Table 1. Motor evoked potentials. ~~
Motor conduction time (rns) Thenar Cervical Height
Pt. #
Surgery
R
Scalp L
CMCT L
R
R
Hallux L
-
R
L
38.0 34.0 NE 40.5 39.0 40.0 40.0 43.4 41 .O
38.8 35.0 34.8 36.1 42.0 41 .O 40.0 47.3 45.0 46.0 44.0 36.0 37.5
~
1.73 1.67
1 2
1.67 1.69 1.70 1.60 1.70 1.70 1.71 10
1.54
11 12
1.52 1.58
13
1.70
Control group: Mean
SD Mean
+ 2.5 SD
No Pre Post No No No No No No Pre Post Pre Post No Pre Post Pre Post
12.9 11.0 13.4 11.7 14.0 16.0 13.3 18.0 15.0 15.0 14.0 12.5 12.5 10.5 14.0 14.0 12.0 12.0
12.95 0.87 15.12
12.6 11.4 11.8 12.2 14.0 14.5 13.2 17.3 15.0 15.0 13.5 11.0 12.5 13.0 12.5 14.0 12.5 14.0
22.9 21.2 23.0 20.7 22.5 22.2 21.2 25.3 25.0 25.0 28.0 20.0 20.0 -
28.5 25.0 23.0 23.5
21.9 22.0 21.4 19.4 25.0 25.0 19.8 25.9 25.0 26.0 25.0 23.0 22.0 23.5 25.0 25.5 26.0 28.0
21.50 1.56 25.4
10.0 10.2 9.6 9.0 7.5 6.2 7.9 7.3 10.0 10.0 14.0 7.5 7.5 -
14.5 11.0 11.0 11.5
9.3 10.6 9.6 7.2 11.0 10.5 6.6 8.6 10.0 11.0 11.5 12.0 9.5 10.5 12.5 11.5 13.5 14.0
8.50 0.36 9.4
-
39.9 -
40.0 -
-
32.5
30.0 41 .O
-
-
-
46.0
40.5 4.04 50.6
FIGURE 1. MRI scan of case 8. Note the coexistence of a cervical syrinx with cervical spondylosis and narrow canal.
SEPs and MEPs in Syringomyelia
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995
MAGNETIC TCS RECORDED FROM RlCHT APB
lODmV MAGNETIC CERVICAL RECORDED FROM x RIGHT APB
-
I2 6m s e
I MAGNETICTCS
I
MAGNETIC CERVICAL RECORDED FROM LEFT APE
FIGURE 2. Preoperative MEPs to magnetic stimulation in case 10. Recording from thenar muscles. CMCT is prolonged on the left side (12.0 ms).
conduction time (CCT) either unilaterally or bilaterally. Four patients showed abnormal latencies or a rionobtainable cervical N after median nerve stimulation. In the 2 most severely affected cases, potentials could not be recorded at least in one side. Similar findings were observed with scalp N2(,. Two of the 3 most affected patients showed a lack of N,, on one side, and the third patient showed a bilateral latency prolongation. N,,, latencies after tibial nerve stimulation was normal in only 4 cases. Latencies were prolonged or responses unobtainable bilaterally in 4 patients, and unilaterally in 3. Measurement of CMCT showed the highest sensitivity (61.5% of abnormal sides) followed by SEPs after tibial nerve stimulation (38.4% of abnormal sides).
996
SEPs and MEPs in Syringomyelia
Comparison between Pre- and Postoperative Findings. Table 1 shows the magnitude of change in
pre- versus postoperative MEP latencies, while Figure 4 shows CMCT values in normal subjects 1 week apart, and in patients before and after surgery. Postoperative changes were found in one or more neurophysiological parameters. One patient that worsened after surgery (case 4) showed weakness of the right limbs that closely correlated with increased right CMCT. Three patients who showed clinical improvement after surgery, also showed significant MEP changes (Figure 5). Two of them (cases 10 and 12) showed a significant reduction in CMCT after a shunting procedure. Furthermore, in cases 10 and 13, who had no preoperative recordable lower-limb MEPs, a lower limb MEP could be recorded from one foot (with latencies of 40 and 46 ms, respectively, after sur-
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MAONETIC TCS RECORDED FROM RIOHT APB 5 msec
10 m n c
MAONETIC CERVICAL RIGHT APE
5 mpc
MAGNETIC TCS RECORDED FROM LEFT APB
5 mscc
MAONETIC CERVICAL RECORDED FROM LEFT APB 12.6 mnc
FIGURE 3. Postoperative MEPs to magnetic stimulation in case 10: recording from thenar muscles. Note CMCT normalization on the left side to 9.5 ms.
gery). In the remaining cases, there was no strict relationship between neurological and MEP changes. In fact, improvement or deterioration of some neurophysiological parameters did not always correlate with objective changes in neurological examination. For example, a previously present lower-limb MEP because unrecordable in cases 2 and 12 after surgery, despite subjective improvement and reduction in CMCT (not significant in case 2). In case 12, SEPs, previously absent, became measurable after surgery due to the appearance of cervical and scalp potentials on stimulation of the left median and posterior tibia1 nerves.
DISCUSSION
This study showed that MEPs provided a useful tool to measure the involvement of descending motor tracts in syringomyelia. A central latency was calculated by subtracting the MEP latencies at
SEPs and MEPs in Syringomyelia
two stimulation sites. By this method, we were able to demonstrate abnormalities in 10 cases, with significant improvement in CMCT after surgical treatment in 2 patients. T h e absence of MEPs to a magnetic transcranial stimulation of maximal intensity was a frequent finding in severely affected patients, and might be related to desynchronization of the descending volley or to either conduction failure owing to corticospinal tract compression or degeneration, lowered spinal motor neuron excitability, or enhanced presynaptic inhibition of corticospinal terminals within the Motor descending pathways might have been affected in these patients for several reasons. In cases of Chiari malformation, the cervicomedullary junction may be constricted by the ectopic tonsils protruding through the foramen magnum.9 At certain spinal cord levels, the entire grey matter may be replaced by the cavity. Although the white matter resists extension of the syrinx, in
MUSCLE & NERVE
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997
CMCT 15.0
141
1s.a
11.1
11.1
1O.(
01
8.’
I ’
g
10 R
x-
-- - -
-X
10 R
L 1
2
FIGURE 4. Reproducibility of CMCT in 13 normal sides 1 week apart (1 and 2: first and second study). On the right side, preoperative and postoperative results (Preop.- Postop.); R: right side; L: left side. Number indicates case. Observe dramatic change in some patients pattern after surgery.
advanced cases the syrinx may occupy most of the cross-section of the spinal cord. Vascular alterations, such as hyalinized and thickened blood vessel walls, edema, and occasional hemorrhages are often observed around the cavity, while degeneration of the ascending and descending tracts of the spinal cord may also be present in advanced cases, particularly in pyramidal and spinocerebellar tracts, as well as in dorsal columns.6 Alternatively, the abnormalities described may be explained by clefts in the medulla,’ although there was no such evidence at MRI scanning. There have been several reports on somatosensory evoked potentials (SEPs) in syringomyelia. 1.5,10,1 l , l 4 The most commonly described abnormalities are reduced amplitude of scalp responses after tibial nerve stimulation; reduced or absent cervical evoked responses after median and especially, ulnar stimulation; and prolonged CCT, particularly in cases with an associated craniovertebral anomaly. Latencies are usually within normal range or only slightly prolonged.
998
SEPs and MEPs in Syringomyelia
Findings are mostly nonspecific, and standard evoked potentials may be entirely normal. Veilleux and Stevens14 have shown a significant correlation between the clinical evidence of proprioceptive sensory deficit in lower limbs and abnormal tibial nerve SEPs in syringomyelia patients. In a detailed study, Restuccia and Mauguiere, l o found absent or reduced cervical N,, and preserved scalp Pi4 and N,, in 83% of median nerves in syringomyelia patients. The dissociated loss of the cervical N,, was considered the most relevant SEP feature in syringomyelia. Our SEP findings are similar to those described by other authors. ‘*14 SEPs after tibial nerve stimulation were the most frequently affected. In median nerve SEPs, latency prolongation of the NI4 and N,,, were observed in the same patients. Since we used a cephalic reference, the “cervical” N,, measured in this study may had a nonspinal com onent generated above the foramen magnum.‘The low sensitivity of SEPs in our patients may be due to the fact that amplitude was
MUSCLE & NERVE
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A FIGURE 5. Case 10. (a) Preoperative MRI scan: note the Chiari malformation and cervical hydromyelia. (b) Postoperative MRI scan: note the disappearance of the cavity.
SEPs and MEPs in Syringomyelia
MUSCLE 8. NERVE
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999
B FIGURE 5 (continued)
not considered in the analysis. Sensitivity may be enhanced by using SEPs after ulnar nerve stimulation,' expanded recording montage^,^ noncephalic references,' or amplitude analysis. In summary, we have found abnormal CMCTs in the early stages of the condition, even when patients were able to carry on their normal life, and siens " were limited to u m e r limbs. T h e combination of SEps and M E P ~may improve objective quantification of functional status of the spinal cord in syringomyelia. ,
1000
I
SEPs and MEPs in Syringomyelia
REFERENCES 1. Anderson NE, Frith RW, Synek VM: Somatosensory evoked potentials in syringomyelia. J Neurol Neurosurg Psychiutqr 1986;49:1407- 1410. 2. Barker A T , Freeston JL, Jahnous R, Jarrat JA: Clinical evaluation of conduction time measurement in central motor oathwavs usine magnetic stimulation of the human brai;. Lancit 1986;;: 132;- 1326. 3. Caramia M, Zarola F, Spddaro M, Pardal AM: Neurophysiologic testing of the central impulse propagation characteristics in patients with sensorimotor disorders, in Rossini P, Marsden CD (eds): Non-tnvasive Stimulation of Brain and
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Spinal Cord: Fundamentals and Clinical Applications. New York, Liss, 1988. 4. Claus D, Harding AE, Hess CW, Mills KR, Murray NMF: Central motor conduction in degenerative ataxic disorders: A magnetic stimulation study. J Neurol Neurosurg Psychiatry 1988;51:790-795. 5. Emerson RJ, Pedley TA: Effect of cervical spine cord lesions on early component of the median nerve somatosensory evoked potential. Neurology (NY) 1986;36:20- 26. 6 . Greenfield JG: Malformations of the nervous system, in Blackwood W, Corsellis JAN (eds): Greenfield's Neuropathology (3rd ed). London, Arnold, 1976. 7. Hess CW, Murray NMF, Mills KR: Measurement of central motor conduction in multiple sclerosis by magnetic brain stimulation. Lancet 1986;ii:355-358. 8. Mauguiere F, Ibariez V: The dissociation of early SEP components in lesions of the cervicomedullary junction: A cue for routine interpretation of abnormal cervical responses to median nerve stimulation. Electroencephalogr Clin Neurophysiol 1985;62:406-420. 9. Nogues MA: Syringomyelia and syringobulbia, in Myrianthopoulus NC (ed): Handbook of Clinical Neurology: Malformations. Amsterdam, Elsevier, 1987, vol 6.
SEPs and MEPs in Syringomyelia
10. Restuccia D, Mauguiere F: The contribution of median nerve SEPs in the functional assessment of the cervical spinal cord in syringomyelia. Brain 1991;114:361-379. 1 1 . Riffel B, Stohr M, Petruch F, Ebensperger H, Schenglmann K: Somatosensory evoked potentials following tibia1 nerve stimulation in multiple sclerosis and space-occupying spinal cord diseases, in Courjon J, Mauguiere F, Revol M (eds): Clinical Applications of Evoked Potentials in Neurology. New York, Raven Press, 1982, pp 493-500. 12. Rothwell JC, Day BL, Thompson PD, Dick JPR, Marsden CD: Some experiences of technique for stimulation of the human cerebral motor cortex through the scalp. Neurosurgery 1987;20:156-163. 13. Thompson PD, Day BL, Rothwell JC, Dick JPR, Cowan JMA, Asselman P, Griffin GB, Sheehy MP, Marsden CD: The interpretation of electromyographic responses to electrical stimulation of the motor cortex in diseases of the upper motor neur0n.J Neural Sci 1987;80:91- 110. 14. Veilleux M, Stevens C: Syringomyelia: Electrophysiological aspects. Muscle Nerve 1987; 10:449-458.
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SEPS AND CNS MAGNETIC STIMULATION IN SYRINGOMYELIA MARTIN A. NOGUES, MD, ANA M A R ~ APARDAL, MD, MARCEL0 MERELLO, MD, and MIGUEL A. MIGUEL, MD
T h e corticospinal pathways are frequently involved in syringomyelia, and it is not uncommon to find early pyramidal signs in the lower limbs.9 This pyramidal tract dysfunction is the main cause of motor disability. Descending motor pathways may also be constricted at the cervicomedullary junction by an associated Chiari type I malformation. Transcranial magnetic stimulation of the motor cortex enables conduction in the central motor pathways to be studied readily in health and disMotor evoked potentials (MEPS) elicited by brain stimuli can be recorded rapidly and without discomfort.2 Abnormalities of central motor conduction time (CMCT) by this technique have been demonstrated in a variety of conditions such as motor neuron disease, degenerative ataxic diso r d e r ~and , ~ multiple sclerosis,’ among others. So
From the lnstituto de lnvestigaciones Neurol6gicas Ra61 Carea (Fleni). Buenos Aires, Argentina (Drs. Nogues and Merello); and Centro de Neurofisiologia Clinica y Terapia Fisica, Buenos Aires, Argentina (Drs. Pardal and Miguel). Acknowledgments. The authors are greatly indebted to Dr. Nicholas Murray for his helpful opinlon and suggestions for improving the manuscript. Address reprint requests to Dr. Martin A. Nogues, Fleni, Ayacucho 2166, 1112 Buenos Aires, Argentina. Accepted for publication November 1 , 1991 CCC 0148-639x1921090993-09 $04.00 0 1992 John Wiley & Sons, Inc.
SEPs and MEPs in Syringomyelia
far, few cases of syrin omyelia have been evaluated by this procedure.?$ In this study, we have correlated findings from motor studies with neurological signs and alteration in somatosensory evoked potentials (SEPs) in a series of syringomyelia patients. MATERIALS AND METHODS
Thirteen patients with syringomyelia, 6 females and 7 males, ages ranging from 19 to 53 years (mean 37.4 years), were studied. All had a classic syringomyelic syndrome with dissociated sensory loss, wasting, and weakness in upper limbs and a variable degree of spasticity in lower limbs. In 6, there was a bilateral Babinski sign, and 2 other patients showed a unilateral extensor plantar response. In the remaining 5 patients there was variable spasticity manifested by either increased tone or hyperreflexia. Joint position sense was impaired in all 4 limbs in one case, and in one or two limbs in 5 other patients. The integrity of the peripheral nerves was determined from normal nerve conduction studies. Associated radiological findings were a basilar impression in 1 case, and a Chiari type I anomaly in 7 cases. These diagnoses were confirmed by MRI scanning. Five patients underwent surgery, and a follow-up clinical and electrophysiological evaluation was performed 3 months postsurgery. Surgical treatment consisted of a syringosubarachnoid shunt (case 9), a foramen magnum decompression and ventricu-
Patients.
MUSCLE & NERVE
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993
loperitoneal shunt (cases 2 and lo), or a syringoperitoneal shunt (cases 12 and 13). T h e control group comprised 10 healthy subjects, 4 males and 6 females, ages 17 to 67 years (mean 43.7 years). Motor Evoked Potentials (MEPs). MEPs were recorded using a magnetic stimulator (Dantec) consisting of a high-energy capacitor bank which discharged transient 150 ks pulses via an electronic switching device into a circular coil (inner and outer diameters were 3 and 13 cm, respectively). The coil was placed in contact with the skin of the right or left scalp, roughly overlying the motor area of the hand (about 7 cm lateral to Cz and 1 to 2 cm in front of the Cz-earlobe line) and foot muscles (2 cm anterior to the vertex). T h e coil was moved over the scalp until optimal motor responses were localized. Stimulation intensity was expressed as a percentage of the maximal output delivered by the stimulator (2.5 T). In most cases, the threshold level was 40% to 45% of the stimulator output for upper limbs and 70% to 75% for lower limbs. To elicit reproducible MEPs during voluntary contraction, stimulus strength was increased 20% above threshold value. Recordings were obtained from surface electrodes on abductor pollicis brevis (APB) and flexor hallucis in all patients. In 2 cases, latencies to deltoid muscles were also measured. The patient was instructed to exert gentle voluntary contraction of the target muscle. Stimulation was repeated until two consecutive reproducible motor responses were obtained, and the shortest latency was used for analysis. T o separate the peripheral component from the total cortex-muscle time, we placed the coil just lateral to the spine, as close as possible to the exit foramina.' Central motor conduction time (CMCT) was calculated as the difference between the latency at cortical and spinal stimulation sites. Latencies and CMCTs were considered abnormal whenever they exceeded normal values by 2.5 SD.
Median nerves were recorded via needle electrodes on the Erb's point, on the seventh cervical spine process, and on the scalp positions overlying the sensory area for the hand (C3 and C4). A cephalic midfrontal (Fz) reference was used for all leads. The median nerve was stimulated at the wrist using 0.2-ms square-wave electrical pulses. The cathode electrode was positioned 2 cm proximal to the anode. Stimulus intensity was adjusted to produce a Somatosensory Evoked Potentials (SEPs).
994
SEPs and MEPs in Syringomyelia
visible twitch of the hallux without causing discomfort. Stimulus rate was 4/s. The tibial nerve was stimulated at the ankle, and evoked responses were recorded 2 cm posterior to the vertex and referred to Fz. At least 1024 responses were averaged with a 30-Hz to 1.5-Hz bandpass. T o confirm SEP reproducibility, each measurement was carried out at least twice. Latencies were measured to the peaks of the negative potentials and considered abnormal when they exceeded mean normal values by 3 SD. RESULTS
Ten of 13 patients had a prolonged CMCT on one (n = 4) or both sides ( n = 6) (Table 1). Two of the latter were the more severely handicapped (cases 12 and 13), and 1 (case 2) had an associated Chiari malformation. In case 11, no reproducible response could be elicited on one side, and the other side showed a slightly prolonged CMCT (10.5 ms). Mean total latency value after scalp stimulation and recording from APB muscle in controls was 21.5 ms (SD 1.56), whereas the CMCT was 8.5 ms (SD 0.36). While there was a tendency for the most affected patients to show more prolonged latencies, the magnitude of the delay seemed unrelated to the presence of a Chiari malformation or to clinical status. Stimulation at the cervical level elicited reproducible responses on both sides in all patients. Mildly prolonged latencies were observed in 2 patients (bilateral!y in l ) without entrapment neuropathies, in 1 patient (case 8) with gross cervical radiculopathy (Fig. l), and in 2 patients with a Chiari anomaly (cases 5 and 10). Recordings from foot muscles after scalp stimulation elicited normal MEPs on both sides in the 4 patients with mildest clinical symptoms, and in case 12. Conversely, MEPs could not be elicited from either foot in 2 severely disabled patients (cases 11 and 13). When obtainable, MEPs to foot muscles showed latencies within normal range. Figures 2 and 3 illustrate pre- and postoperative MEP recordings in a patient with syringomyelia (case 10).
MEP Studies.
Median and tibial nerve SEPs were performed bilaterally in all patients. Recordings were compared with normative data obtained from the 10 healthy subjects. Mean value for scalp N,, latency was 19.5 ms (SD 0.66); for N,, to N,, interpeak latency, 5.78 ms (SD 0.44); and for P,, after tibial nerve stimulation, 40.0 ms (SD 2.24). Eight of the 13 cases showed an abnormal central SEP Studies.
MUSCLE & NERVE
September 1992
Table 1. Motor evoked potentials. ~~
Motor conduction time (rns) Thenar Cervical Height
Pt. #
Surgery
R
Scalp L
CMCT L
R
R
Hallux L
-
R
L
38.0 34.0 NE 40.5 39.0 40.0 40.0 43.4 41 .O
38.8 35.0 34.8 36.1 42.0 41 .O 40.0 47.3 45.0 46.0 44.0 36.0 37.5
~
1.73 1.67
1 2
1.67 1.69 1.70 1.60 1.70 1.70 1.71 10
1.54
11 12
1.52 1.58
13
1.70
Control group: Mean
SD Mean
+ 2.5 SD
No Pre Post No No No No No No Pre Post Pre Post No Pre Post Pre Post
12.9 11.0 13.4 11.7 14.0 16.0 13.3 18.0 15.0 15.0 14.0 12.5 12.5 10.5 14.0 14.0 12.0 12.0
12.95 0.87 15.12
12.6 11.4 11.8 12.2 14.0 14.5 13.2 17.3 15.0 15.0 13.5 11.0 12.5 13.0 12.5 14.0 12.5 14.0
22.9 21.2 23.0 20.7 22.5 22.2 21.2 25.3 25.0 25.0 28.0 20.0 20.0 -
28.5 25.0 23.0 23.5
21.9 22.0 21.4 19.4 25.0 25.0 19.8 25.9 25.0 26.0 25.0 23.0 22.0 23.5 25.0 25.5 26.0 28.0
21.50 1.56 25.4
10.0 10.2 9.6 9.0 7.5 6.2 7.9 7.3 10.0 10.0 14.0 7.5 7.5 -
14.5 11.0 11.0 11.5
9.3 10.6 9.6 7.2 11.0 10.5 6.6 8.6 10.0 11.0 11.5 12.0 9.5 10.5 12.5 11.5 13.5 14.0
8.50 0.36 9.4
-
39.9 -
40.0 -
-
32.5
30.0 41 .O
-
-
-
46.0
40.5 4.04 50.6
FIGURE 1. MRI scan of case 8. Note the coexistence of a cervical syrinx with cervical spondylosis and narrow canal.
SEPs and MEPs in Syringomyelia
MUSCLE & NERVE
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995
MAGNETIC TCS RECORDED FROM RlCHT APB
lODmV MAGNETIC CERVICAL RECORDED FROM x RIGHT APB
-
I2 6m s e
I MAGNETICTCS
I
MAGNETIC CERVICAL RECORDED FROM LEFT APE
FIGURE 2. Preoperative MEPs to magnetic stimulation in case 10. Recording from thenar muscles. CMCT is prolonged on the left side (12.0 ms).
conduction time (CCT) either unilaterally or bilaterally. Four patients showed abnormal latencies or a rionobtainable cervical N after median nerve stimulation. In the 2 most severely affected cases, potentials could not be recorded at least in one side. Similar findings were observed with scalp N2(,. Two of the 3 most affected patients showed a lack of N,, on one side, and the third patient showed a bilateral latency prolongation. N,,, latencies after tibial nerve stimulation was normal in only 4 cases. Latencies were prolonged or responses unobtainable bilaterally in 4 patients, and unilaterally in 3. Measurement of CMCT showed the highest sensitivity (61.5% of abnormal sides) followed by SEPs after tibial nerve stimulation (38.4% of abnormal sides).
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SEPs and MEPs in Syringomyelia
Comparison between Pre- and Postoperative Findings. Table 1 shows the magnitude of change in
pre- versus postoperative MEP latencies, while Figure 4 shows CMCT values in normal subjects 1 week apart, and in patients before and after surgery. Postoperative changes were found in one or more neurophysiological parameters. One patient that worsened after surgery (case 4) showed weakness of the right limbs that closely correlated with increased right CMCT. Three patients who showed clinical improvement after surgery, also showed significant MEP changes (Figure 5). Two of them (cases 10 and 12) showed a significant reduction in CMCT after a shunting procedure. Furthermore, in cases 10 and 13, who had no preoperative recordable lower-limb MEPs, a lower limb MEP could be recorded from one foot (with latencies of 40 and 46 ms, respectively, after sur-
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MAONETIC TCS RECORDED FROM RIOHT APB 5 msec
10 m n c
MAONETIC CERVICAL RIGHT APE
5 mpc
MAGNETIC TCS RECORDED FROM LEFT APB
5 mscc
MAONETIC CERVICAL RECORDED FROM LEFT APB 12.6 mnc
FIGURE 3. Postoperative MEPs to magnetic stimulation in case 10: recording from thenar muscles. Note CMCT normalization on the left side to 9.5 ms.
gery). In the remaining cases, there was no strict relationship between neurological and MEP changes. In fact, improvement or deterioration of some neurophysiological parameters did not always correlate with objective changes in neurological examination. For example, a previously present lower-limb MEP because unrecordable in cases 2 and 12 after surgery, despite subjective improvement and reduction in CMCT (not significant in case 2). In case 12, SEPs, previously absent, became measurable after surgery due to the appearance of cervical and scalp potentials on stimulation of the left median and posterior tibia1 nerves.
DISCUSSION
This study showed that MEPs provided a useful tool to measure the involvement of descending motor tracts in syringomyelia. A central latency was calculated by subtracting the MEP latencies at
SEPs and MEPs in Syringomyelia
two stimulation sites. By this method, we were able to demonstrate abnormalities in 10 cases, with significant improvement in CMCT after surgical treatment in 2 patients. T h e absence of MEPs to a magnetic transcranial stimulation of maximal intensity was a frequent finding in severely affected patients, and might be related to desynchronization of the descending volley or to either conduction failure owing to corticospinal tract compression or degeneration, lowered spinal motor neuron excitability, or enhanced presynaptic inhibition of corticospinal terminals within the Motor descending pathways might have been affected in these patients for several reasons. In cases of Chiari malformation, the cervicomedullary junction may be constricted by the ectopic tonsils protruding through the foramen magnum.9 At certain spinal cord levels, the entire grey matter may be replaced by the cavity. Although the white matter resists extension of the syrinx, in
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CMCT 15.0
141
1s.a
11.1
11.1
1O.(
01
8.’
I ’
g
10 R
x-
-- - -
-X
10 R
L 1
2
FIGURE 4. Reproducibility of CMCT in 13 normal sides 1 week apart (1 and 2: first and second study). On the right side, preoperative and postoperative results (Preop.- Postop.); R: right side; L: left side. Number indicates case. Observe dramatic change in some patients pattern after surgery.
advanced cases the syrinx may occupy most of the cross-section of the spinal cord. Vascular alterations, such as hyalinized and thickened blood vessel walls, edema, and occasional hemorrhages are often observed around the cavity, while degeneration of the ascending and descending tracts of the spinal cord may also be present in advanced cases, particularly in pyramidal and spinocerebellar tracts, as well as in dorsal columns.6 Alternatively, the abnormalities described may be explained by clefts in the medulla,’ although there was no such evidence at MRI scanning. There have been several reports on somatosensory evoked potentials (SEPs) in syringomyelia. 1.5,10,1 l , l 4 The most commonly described abnormalities are reduced amplitude of scalp responses after tibial nerve stimulation; reduced or absent cervical evoked responses after median and especially, ulnar stimulation; and prolonged CCT, particularly in cases with an associated craniovertebral anomaly. Latencies are usually within normal range or only slightly prolonged.
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SEPs and MEPs in Syringomyelia
Findings are mostly nonspecific, and standard evoked potentials may be entirely normal. Veilleux and Stevens14 have shown a significant correlation between the clinical evidence of proprioceptive sensory deficit in lower limbs and abnormal tibial nerve SEPs in syringomyelia patients. In a detailed study, Restuccia and Mauguiere, l o found absent or reduced cervical N,, and preserved scalp Pi4 and N,, in 83% of median nerves in syringomyelia patients. The dissociated loss of the cervical N,, was considered the most relevant SEP feature in syringomyelia. Our SEP findings are similar to those described by other authors. ‘*14 SEPs after tibial nerve stimulation were the most frequently affected. In median nerve SEPs, latency prolongation of the NI4 and N,,, were observed in the same patients. Since we used a cephalic reference, the “cervical” N,, measured in this study may had a nonspinal com onent generated above the foramen magnum.‘The low sensitivity of SEPs in our patients may be due to the fact that amplitude was
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A FIGURE 5. Case 10. (a) Preoperative MRI scan: note the Chiari malformation and cervical hydromyelia. (b) Postoperative MRI scan: note the disappearance of the cavity.
SEPs and MEPs in Syringomyelia
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B FIGURE 5 (continued)
not considered in the analysis. Sensitivity may be enhanced by using SEPs after ulnar nerve stimulation,' expanded recording montage^,^ noncephalic references,' or amplitude analysis. In summary, we have found abnormal CMCTs in the early stages of the condition, even when patients were able to carry on their normal life, and siens " were limited to u m e r limbs. T h e combination of SEps and M E P ~may improve objective quantification of functional status of the spinal cord in syringomyelia. ,
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I
SEPs and MEPs in Syringomyelia
REFERENCES 1. Anderson NE, Frith RW, Synek VM: Somatosensory evoked potentials in syringomyelia. J Neurol Neurosurg Psychiutqr 1986;49:1407- 1410. 2. Barker A T , Freeston JL, Jahnous R, Jarrat JA: Clinical evaluation of conduction time measurement in central motor oathwavs usine magnetic stimulation of the human brai;. Lancit 1986;;: 132;- 1326. 3. Caramia M, Zarola F, Spddaro M, Pardal AM: Neurophysiologic testing of the central impulse propagation characteristics in patients with sensorimotor disorders, in Rossini P, Marsden CD (eds): Non-tnvasive Stimulation of Brain and
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Spinal Cord: Fundamentals and Clinical Applications. New York, Liss, 1988. 4. Claus D, Harding AE, Hess CW, Mills KR, Murray NMF: Central motor conduction in degenerative ataxic disorders: A magnetic stimulation study. J Neurol Neurosurg Psychiatry 1988;51:790-795. 5. Emerson RJ, Pedley TA: Effect of cervical spine cord lesions on early component of the median nerve somatosensory evoked potential. Neurology (NY) 1986;36:20- 26. 6 . Greenfield JG: Malformations of the nervous system, in Blackwood W, Corsellis JAN (eds): Greenfield's Neuropathology (3rd ed). London, Arnold, 1976. 7. Hess CW, Murray NMF, Mills KR: Measurement of central motor conduction in multiple sclerosis by magnetic brain stimulation. Lancet 1986;ii:355-358. 8. Mauguiere F, Ibariez V: The dissociation of early SEP components in lesions of the cervicomedullary junction: A cue for routine interpretation of abnormal cervical responses to median nerve stimulation. Electroencephalogr Clin Neurophysiol 1985;62:406-420. 9. Nogues MA: Syringomyelia and syringobulbia, in Myrianthopoulus NC (ed): Handbook of Clinical Neurology: Malformations. Amsterdam, Elsevier, 1987, vol 6.
SEPs and MEPs in Syringomyelia
10. Restuccia D, Mauguiere F: The contribution of median nerve SEPs in the functional assessment of the cervical spinal cord in syringomyelia. Brain 1991;114:361-379. 1 1 . Riffel B, Stohr M, Petruch F, Ebensperger H, Schenglmann K: Somatosensory evoked potentials following tibia1 nerve stimulation in multiple sclerosis and space-occupying spinal cord diseases, in Courjon J, Mauguiere F, Revol M (eds): Clinical Applications of Evoked Potentials in Neurology. New York, Raven Press, 1982, pp 493-500. 12. Rothwell JC, Day BL, Thompson PD, Dick JPR, Marsden CD: Some experiences of technique for stimulation of the human cerebral motor cortex through the scalp. Neurosurgery 1987;20:156-163. 13. Thompson PD, Day BL, Rothwell JC, Dick JPR, Cowan JMA, Asselman P, Griffin GB, Sheehy MP, Marsden CD: The interpretation of electromyographic responses to electrical stimulation of the motor cortex in diseases of the upper motor neur0n.J Neural Sci 1987;80:91- 110. 14. Veilleux M, Stevens C: Syringomyelia: Electrophysiological aspects. Muscle Nerve 1987; 10:449-458.
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