SPINE Volume 40, Number 3, pp E161-E167 ©2015, Wolters Kluwer Health, Inc. All rights reserved.
DIAGNOSTICS
Transcranial Magnetic Stimulation in the Diagnosis of Cervical Compressive Myelopathy Comparison With Spinal Cord Evoked Potentials Masahiro Funaba, MD, Tsukasa Kanchiku, MD, PhD, Yasuaki Imajo, MD, PhD, Hidenori Suzuki, MD, PhD, Yuichiro Yoshida, MD, PhD, Norihiro Nishida, MD, PhD, and Toshihiko Taguchi, MD, PhD
Study Design. Single-center retrospective study. Objective. To reveal the characteristic changes in central motor conduction time (CMCT) produced by transcranial magnetic stimulation among the responsible levels of cervical compressive myelopathy (CCM). Summary of Background Data. CMCT is a useful and noninvasive measure for evaluating the central motor pathway. However, a systematic correlation between CMCT findings and the responsible level of CCM has so far not been addressed in a large patient cohort. Method. We measured CMCT in 75 patients with CCM who were determined by intraoperative spinal cord evoked potentials to have a single site of conduction abnormality at the intervertebral level. Twenty-one healthy controls were also evaluated. Motor evoked potentials, compound muscle action potentials, and F wave were recorded from bilateral abductor digiti minimi (ADM) and abductor hallucis (AH) muscles. CMCT was calculated as follows: motor evoked potentials latency − (CMAPs latency + F latency − 1)/2 (ms). Result. The mean values of ADM-CMCT and AH-CMCT at each responsible level were significantly longer than those of normal values (P < 0.01). However, the mean value of ADM-CMCT at the C6–C7 level was markedly shorter than those at the other levels, whereas the mean values of AH-CMCT were not significantly different between each responsible level. We determined that an ADM-CMCT longer than 7.9 ms (mean + 2.5 standard deviation) was abnormal. Using this definition, the sensitivity of ADM-CMCT for CCM was 92% for C3–C4 myelopathy, 95% for C4–C5, 58% for C5–C6, and 9% for C6–C7.
From the Department of Orthopedic Surgery, Yamaguchi University Graduate School of Medicine, Yamaguchi, Japan. Acknowledgment date: July 9, 2014. First revision date: September 24, 2014. Second revision date: October 21, 2014. Acceptance date: October 26, 2014. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Masahiro Funaba, MD, Department of Orthopedic Surgery, Yamaguchi University Graduate School of Medicine, Yamaguchi, Japan; E-mail [email protected] DOI: 10.1097/BRS.0000000000000698 Spine
Conclusion. ADM-CMCT is useful for the screening of CCM rostral to the C5–C6 level. Diagnosis of patients with C6–C7 myelopathy should include assessment of the AH-CMCT. Key words: central motor conduction time, cervical compressive myelopathy, spinal cord evoked potentials, transcranial magnetic stimulation, responsible level. Level of Evidence: 4 Spine 2015;40:E161–E167
C
ervical compressive myelopathy (CCM) is a common disease among middle-aged and elderly people. The patients with CCM are increasing because of the progressive aging of society. Magnetic resonance imaging (MRI) can detect compression of the spinal cord and this plays an important role in the diagnosis of compressive myelopathy. However, MR image often shows compressions in asymptomatic lesions and cannot evaluate spinal cord function.1 Transcranial magnetic stimulation (TMS) can reveal involvement of the corticospinal tract in a noninvasive method.2 Measurement of central motor conduction time (CMCT) is a useful way to assess electrophysiological functioning of the corticospinal tract in patients with CCM and has been widely reported as a noninvasive method for evaluating the central motor pathway.3–7 However, to date there has not been a systematic correlation between CMCT findings and the responsible level of CCM in a large patient cohort. Consequently, the level at which CMCT can detect CCM is still unknown. In previous reports, CMCT measured in hand muscles was shown to be sensitive for the screening of CCM,4–5 but there are no reports evaluating at which level CMCT measured in abductor digiti minimi (ADM) muscle is reliable for screening CCM. We had measured multimodal spinal cord evoked potentials (SCEPs) to diagnose the responsible level of CCM. SCEPs are useful and reliable for investigating the functional integrity of the spinal cord when MR image shows evidence of compression at several levels.8–11 The aim of this study was therefore to evaluate the usefulness and limitations of TMS among the responsible levels. We confirmed the importance of this characteristic for the screening of CCM. www.spinejournal.com
E161
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. SPINE140905_LR E161
08/01/15 2:11 PM
DIAGNOSTICS PATIENTS AND METHODS Patients A total of 75 patients with CCM (44 with cervical spondylotic myelopathy; 7 with cervical disc herniation; and 24 with ossification of longitudinal ligament of cervical spine) were determined by intraoperative SCEPs to have a single site of conduction abnormality at the intervertebral level. All patients had CMCT measured before surgery. The average patient age was 67.3 years (range, 29–86 yr) and all underwent cervical laminoplasty. Written informed consent with the approval of Yamaguchi University Graduate School of medicine was obtained for preoperative MRI investigation and electrophysiological studies in all patients. Patients who fulfilled the criteria given below were included in the study. A diagnosis of myelopathy was established on the basis of the presence of hyper-reflexia, including a positive Hoffmann sign, upper extremity sensory disturbance, and obvious MRI-documented cervical spinal cord compression. Sensory and motor nerve conduction velocities in peripheral nerves were within normal limits. Patients who had peripheral neuropathy, cephalopathy, and thoracic compressive myelopathy were excluded.
Magnetic Resonance Imaging All patients underwent MRI with a 1.5-T imaging system. Sections were 5-mm thick, with a 2-mm gap between intersections. T1-weighted and T2-weighted sagittal and axial images were obtained.
Controls Normal data on TMS (motor evoked potentials; MEPs and CMCT) were obtained from 21 healthy control subjects with matching ages (mean age, 63.5 yr; range, 54–71 yr) and with no signs or symptoms of neurological disease. These individuals were admitted to our hospital to undergo hip or knee joint surgery.
Recording of CMCT All electrophysiological assessments were performed using a Nicolet Viking 4 instrument (Natus medical Incorporated, San Carlos, CA). Self-adhesive surface recording electrodes were placed on target muscles. MEPs were recorded from bilateral ADM and abductor hallucis (AH) muscles. TMS was delivered using the Magstim 200 instrument (The Magstim Company Ltd, Carmarthenshire, UK) with a circular coil having an outer diameter of 140 mm.TMS was applied while the patients exerted isometric voluntary contraction of the target muscles. The coil was held with its center on the Cz position of 10-20 system for recording MEPs from the ADM and moved frontally for recording of MEPs from the AH. TMS intensity was set at 20% above the MEPs threshold. At least 4 consecutive trials were recorded and superimposed. The shortest onset latency of the MEPs was recorded (MEPs latency). Compound muscle action potentials (CMAPs) and F waves were recorded after supramaximal electric stimulation of the ulnar nerve at the wrist and of tibial nerves at the ankle. Sixteen serial responses were obtained and the shortest latency E162
www.spinejournal.com
Transcranial Magnetic Stimulation Study in CCM • Funaba et al
Cerebral cortex CMCT=MEPs latency-PMCT (ms)
C8 motor segment ADM muscle
T1 motor segment
CMCT
PMCT MEPs latency Figure 1. MEPs latency was recorded in the ADM muscle by transcranial magnetic stimulation. The conduction time from the cerebral cortex to the C8 or T1 segment was defined as ADM-CMCT. This was derived by subtracting the PMCT from the MEPs latency. MEPs indicates motor evoked potentials; ADM, abductor digiti minimi; CMCT, central motor conduction time; PMCT, peripheral motor conduction time.
of F waves was measured. Peripheral motor conduction time (PMCT) was calculated as followed: (CMAPs latency + F latency − 1)/2. CMCT was calculated as followed: MEPs latency − PMCT (ms) (Figure 1). The baseline-to-negative peak amplitudes of the m waves and MEPs were measured. All muscle responses were amplified and filtered with a bandpass of 5 to 5000 Hz.
Recording of SCEPs for the Diagnosis of Symptomatic Lesions SCEPs after transcranial electric stimulation (TES-SCEPs) and spinal cord stimulation (spinal-SCEPs) were recorded intraoperatively. TES was delivered as square pulses of 0.2ms duration and at an intensity of 100 mA through needle electrodes (13R25, length: 8 mm, diameter: 0.8 mm; Dantec Dynamics A/S, Skovlunde, Denmark) placed on the skull. The anode was placed 7 cm laterally to the right of the vertex on a line joining the external auditory meatus. The cathode was placed on the opposite side. Spinal-SCEPs were delivered by an epidural catheter electrode (UKG-100-2PM, diameter: 0.8 mm, length: 900 mm; UniqueMedical Co. Ltd, Tokyo, Japan) inserted into the dorsal epidural space from the C7– T1 and T11–T12 interlaminar space. Square wave pulses (0.2-ms duration, 3-Hz rate) were delivered at an intensity of 15 to 20 mA. Prior to surgery, all SCEPs were recorded intraoperatively with recording electrodes (13R25) inserted in the ligamentum flavum at each interlaminar space. A reference electrode was inserted into the subcutaneous tissue in the posterior aspect of the neck for the recording of spinal-SCEPs and TES-SCEPs. All SCEPs signals were amplified and filtered with a band-pass of 20 to 3000 Hz using a standard evoked potential/electromyography machine (Nicolet Viking; Nicolet Biomedical). An average of 40 to 60 TES-SCEPs and 40 to 50 spinal-SCEPs responses were obtained. Two different averaged responses were superimposed and displayed. For both TES-SCEPs and Spinal-SCEPs, intervertebral levels with a marked reduction in the size of February 2015
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. SPINE140905_LR E162
08/01/15 2:11 PM
DIAGNOSTICS
Transcranial Magnetic Stimulation Study in CCM • Funaba et al
TCE-SCEPs
Spinal-SCEPs
C2-3 C3-4 C4-5 C5-6 C6-7 C7-T1
5μV
10μV
1.5ms
1ms
Figure 2. SCEPsobtained from patients with compressive cervical myelopathy. TES-SCEPs and spinal-SCEPs both showed marked attenuation of amplitude at the C4–C5 level, indicating a conduction block at C4–C5. TES-SCEPs indicates spinal cord evoked potentials after transcranial electric stimulation; spinal-SCEPs, spinal cord evoked potentials after spinal cord stimulation.
the negative peak (>50%) were considered to be significant (Figure 2).10–11
Statistical Analysis For TMS examinations, the upper limits for MEPs latency and CMCT were determined as the mean + 2.5 standard deviations (SDs). The t test was used to compare normal and patient data, whereas the Mann-Whitney U test and KruskalWallis test were used for unpaired patient data. All P values less than 0.05 were regarded as statistically significant.
RESULTS The recording of CMCT and SCEPs were performed and success in all 75 patients. The responsible levels that we estimated preoperatively from neurological examination and radiological findings were coincident with the site of conduction block in SCEPs in all patients.
Spinal Cord Evoked Potentials The SCEPs conduction abnormality was localized to the C3– C4 intervertebral level in 25 patients, C4–C5 in 22, C5–C6 in 17, and C6–C7 in 11.
MEPs Latency and CMCT Results for MEPs latencies, PMCT, and CMCT measured from the ADM and AH in normal subjects are shown in Table 1. In addition, result for MEPs latencies and CMCT measured from the ADM and AH in the patients are shown in Table 2. Mean values for CMCT in ADM and AH at each responsible level were significantly longer than the normal values (P < 0.001). However, the mean values for ADMCMCT at the C5–C6 and C6–C7 levels were significantly shorter than those observed at the C3–C4 and C4–C5 levels. The mean value for ADM-CMCT at the C6–C7 level in particular was clearly shorter than at the other levels (Figure 4A). In contrast, the mean values for AH-CMCT Spine
between each responsible level were not significantly different (Figure 4B). The mean value for ADM-MEPs latency was significantly delayed compared with the normal value, except at the C6– C7 level (C3–C4 ∼ C5–C6, P < 0.0001; C6–C7, P = 0.25). The mean value for ADM-MEPs latency at the C6–C7 level in particular was markedly shorter than at the other levels (Figure 3A): (Figure 4C; C6–C7 vs. C3–C4 and C4–C5, P < 0.001; C6–C7 vs. C5–C6, P = 0.01). The mean values for AH-MEPs latency were not significantly different between each responsible level (Figure 3B) (P = 0.43; Figure 4D). The mean values for AH-MEPs latency at each responsible level were significantly delayed compared with the normal values (P < 0.001). The mean values for PMCT in ADM and AH were not significantly different between each responsible level (ADM-PMCT [ms]; C3–C4 14.25 ± 1.26, C4–C5 14.68 ± 1.65, C5–C6 14.49 ± 1.8, C6–C7 14.45 ± 2.11, P = 0.75; AH-PMCT [ms]; and C3–C4 25.9 ± 4.2, C4–C5 25.85 ± 2.7, C5–C6 26.08 ± 1.77, C6–C7 25.42 ± 3.31, P = 0.58).
TABLE 1. Normative Data of MEPs Latency and
Normal Limit of CMCT
ADM Normal limit AH Normal limit
MEPs Latency (ms)
CMCT (ms)
PMCT (ms)
20.3 ± 1.9
5.2 ± 1.1
15.5 ± 1.5
25.1*
7.9*
19.3*
37.9 ± 2.1
12.1 ± 1.5
27.2 ± 2.4
43.2*
15.8*
33.2*
*Mean + 2.5 SD. MEPs indicates motor evoked potentials; CMCT, central motor conduction time; PMCT, peripheral motor conduction time; ADM, abductor digiti minimum; AH, abductor hallucis; SD, standard deviation.
www.spinejournal.com
E163
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. SPINE140905_LR E163
08/01/15 2:11 PM
DIAGNOSTICS
Transcranial Magnetic Stimulation Study in CCM • Funaba et al
TABLE 2. ADM-CMCT, AH-CMCT, ADM-MEPs, and AH-MEPs Latency in 75 Patients With CCM C3–C4 (n = 25)
ADM-CMCT
AH-CMCT
ADM-MEPs
AH-MEPs
Mean ± SD, (ms)
11.65 ± 3.18
20.15 ± 5.07
25.63 ± 3.49
46.07 ± 6.61
2 (8%)
5 (20%)
13 (52%)
9 (36%)
23 (92%)
20 (80%)
12 (48%)
16 (64%)
0
0
0
0
92%
80%
48%
64%
DIAGNOSTICS
Transcranial Magnetic Stimulation in the Diagnosis of Cervical Compressive Myelopathy Comparison With Spinal Cord Evoked Potentials Masahiro Funaba, MD, Tsukasa Kanchiku, MD, PhD, Yasuaki Imajo, MD, PhD, Hidenori Suzuki, MD, PhD, Yuichiro Yoshida, MD, PhD, Norihiro Nishida, MD, PhD, and Toshihiko Taguchi, MD, PhD
Study Design. Single-center retrospective study. Objective. To reveal the characteristic changes in central motor conduction time (CMCT) produced by transcranial magnetic stimulation among the responsible levels of cervical compressive myelopathy (CCM). Summary of Background Data. CMCT is a useful and noninvasive measure for evaluating the central motor pathway. However, a systematic correlation between CMCT findings and the responsible level of CCM has so far not been addressed in a large patient cohort. Method. We measured CMCT in 75 patients with CCM who were determined by intraoperative spinal cord evoked potentials to have a single site of conduction abnormality at the intervertebral level. Twenty-one healthy controls were also evaluated. Motor evoked potentials, compound muscle action potentials, and F wave were recorded from bilateral abductor digiti minimi (ADM) and abductor hallucis (AH) muscles. CMCT was calculated as follows: motor evoked potentials latency − (CMAPs latency + F latency − 1)/2 (ms). Result. The mean values of ADM-CMCT and AH-CMCT at each responsible level were significantly longer than those of normal values (P < 0.01). However, the mean value of ADM-CMCT at the C6–C7 level was markedly shorter than those at the other levels, whereas the mean values of AH-CMCT were not significantly different between each responsible level. We determined that an ADM-CMCT longer than 7.9 ms (mean + 2.5 standard deviation) was abnormal. Using this definition, the sensitivity of ADM-CMCT for CCM was 92% for C3–C4 myelopathy, 95% for C4–C5, 58% for C5–C6, and 9% for C6–C7.
From the Department of Orthopedic Surgery, Yamaguchi University Graduate School of Medicine, Yamaguchi, Japan. Acknowledgment date: July 9, 2014. First revision date: September 24, 2014. Second revision date: October 21, 2014. Acceptance date: October 26, 2014. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Masahiro Funaba, MD, Department of Orthopedic Surgery, Yamaguchi University Graduate School of Medicine, Yamaguchi, Japan; E-mail [email protected] DOI: 10.1097/BRS.0000000000000698 Spine
Conclusion. ADM-CMCT is useful for the screening of CCM rostral to the C5–C6 level. Diagnosis of patients with C6–C7 myelopathy should include assessment of the AH-CMCT. Key words: central motor conduction time, cervical compressive myelopathy, spinal cord evoked potentials, transcranial magnetic stimulation, responsible level. Level of Evidence: 4 Spine 2015;40:E161–E167
C
ervical compressive myelopathy (CCM) is a common disease among middle-aged and elderly people. The patients with CCM are increasing because of the progressive aging of society. Magnetic resonance imaging (MRI) can detect compression of the spinal cord and this plays an important role in the diagnosis of compressive myelopathy. However, MR image often shows compressions in asymptomatic lesions and cannot evaluate spinal cord function.1 Transcranial magnetic stimulation (TMS) can reveal involvement of the corticospinal tract in a noninvasive method.2 Measurement of central motor conduction time (CMCT) is a useful way to assess electrophysiological functioning of the corticospinal tract in patients with CCM and has been widely reported as a noninvasive method for evaluating the central motor pathway.3–7 However, to date there has not been a systematic correlation between CMCT findings and the responsible level of CCM in a large patient cohort. Consequently, the level at which CMCT can detect CCM is still unknown. In previous reports, CMCT measured in hand muscles was shown to be sensitive for the screening of CCM,4–5 but there are no reports evaluating at which level CMCT measured in abductor digiti minimi (ADM) muscle is reliable for screening CCM. We had measured multimodal spinal cord evoked potentials (SCEPs) to diagnose the responsible level of CCM. SCEPs are useful and reliable for investigating the functional integrity of the spinal cord when MR image shows evidence of compression at several levels.8–11 The aim of this study was therefore to evaluate the usefulness and limitations of TMS among the responsible levels. We confirmed the importance of this characteristic for the screening of CCM. www.spinejournal.com
E161
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. SPINE140905_LR E161
08/01/15 2:11 PM
DIAGNOSTICS PATIENTS AND METHODS Patients A total of 75 patients with CCM (44 with cervical spondylotic myelopathy; 7 with cervical disc herniation; and 24 with ossification of longitudinal ligament of cervical spine) were determined by intraoperative SCEPs to have a single site of conduction abnormality at the intervertebral level. All patients had CMCT measured before surgery. The average patient age was 67.3 years (range, 29–86 yr) and all underwent cervical laminoplasty. Written informed consent with the approval of Yamaguchi University Graduate School of medicine was obtained for preoperative MRI investigation and electrophysiological studies in all patients. Patients who fulfilled the criteria given below were included in the study. A diagnosis of myelopathy was established on the basis of the presence of hyper-reflexia, including a positive Hoffmann sign, upper extremity sensory disturbance, and obvious MRI-documented cervical spinal cord compression. Sensory and motor nerve conduction velocities in peripheral nerves were within normal limits. Patients who had peripheral neuropathy, cephalopathy, and thoracic compressive myelopathy were excluded.
Magnetic Resonance Imaging All patients underwent MRI with a 1.5-T imaging system. Sections were 5-mm thick, with a 2-mm gap between intersections. T1-weighted and T2-weighted sagittal and axial images were obtained.
Controls Normal data on TMS (motor evoked potentials; MEPs and CMCT) were obtained from 21 healthy control subjects with matching ages (mean age, 63.5 yr; range, 54–71 yr) and with no signs or symptoms of neurological disease. These individuals were admitted to our hospital to undergo hip or knee joint surgery.
Recording of CMCT All electrophysiological assessments were performed using a Nicolet Viking 4 instrument (Natus medical Incorporated, San Carlos, CA). Self-adhesive surface recording electrodes were placed on target muscles. MEPs were recorded from bilateral ADM and abductor hallucis (AH) muscles. TMS was delivered using the Magstim 200 instrument (The Magstim Company Ltd, Carmarthenshire, UK) with a circular coil having an outer diameter of 140 mm.TMS was applied while the patients exerted isometric voluntary contraction of the target muscles. The coil was held with its center on the Cz position of 10-20 system for recording MEPs from the ADM and moved frontally for recording of MEPs from the AH. TMS intensity was set at 20% above the MEPs threshold. At least 4 consecutive trials were recorded and superimposed. The shortest onset latency of the MEPs was recorded (MEPs latency). Compound muscle action potentials (CMAPs) and F waves were recorded after supramaximal electric stimulation of the ulnar nerve at the wrist and of tibial nerves at the ankle. Sixteen serial responses were obtained and the shortest latency E162
www.spinejournal.com
Transcranial Magnetic Stimulation Study in CCM • Funaba et al
Cerebral cortex CMCT=MEPs latency-PMCT (ms)
C8 motor segment ADM muscle
T1 motor segment
CMCT
PMCT MEPs latency Figure 1. MEPs latency was recorded in the ADM muscle by transcranial magnetic stimulation. The conduction time from the cerebral cortex to the C8 or T1 segment was defined as ADM-CMCT. This was derived by subtracting the PMCT from the MEPs latency. MEPs indicates motor evoked potentials; ADM, abductor digiti minimi; CMCT, central motor conduction time; PMCT, peripheral motor conduction time.
of F waves was measured. Peripheral motor conduction time (PMCT) was calculated as followed: (CMAPs latency + F latency − 1)/2. CMCT was calculated as followed: MEPs latency − PMCT (ms) (Figure 1). The baseline-to-negative peak amplitudes of the m waves and MEPs were measured. All muscle responses were amplified and filtered with a bandpass of 5 to 5000 Hz.
Recording of SCEPs for the Diagnosis of Symptomatic Lesions SCEPs after transcranial electric stimulation (TES-SCEPs) and spinal cord stimulation (spinal-SCEPs) were recorded intraoperatively. TES was delivered as square pulses of 0.2ms duration and at an intensity of 100 mA through needle electrodes (13R25, length: 8 mm, diameter: 0.8 mm; Dantec Dynamics A/S, Skovlunde, Denmark) placed on the skull. The anode was placed 7 cm laterally to the right of the vertex on a line joining the external auditory meatus. The cathode was placed on the opposite side. Spinal-SCEPs were delivered by an epidural catheter electrode (UKG-100-2PM, diameter: 0.8 mm, length: 900 mm; UniqueMedical Co. Ltd, Tokyo, Japan) inserted into the dorsal epidural space from the C7– T1 and T11–T12 interlaminar space. Square wave pulses (0.2-ms duration, 3-Hz rate) were delivered at an intensity of 15 to 20 mA. Prior to surgery, all SCEPs were recorded intraoperatively with recording electrodes (13R25) inserted in the ligamentum flavum at each interlaminar space. A reference electrode was inserted into the subcutaneous tissue in the posterior aspect of the neck for the recording of spinal-SCEPs and TES-SCEPs. All SCEPs signals were amplified and filtered with a band-pass of 20 to 3000 Hz using a standard evoked potential/electromyography machine (Nicolet Viking; Nicolet Biomedical). An average of 40 to 60 TES-SCEPs and 40 to 50 spinal-SCEPs responses were obtained. Two different averaged responses were superimposed and displayed. For both TES-SCEPs and Spinal-SCEPs, intervertebral levels with a marked reduction in the size of February 2015
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. SPINE140905_LR E162
08/01/15 2:11 PM
DIAGNOSTICS
Transcranial Magnetic Stimulation Study in CCM • Funaba et al
TCE-SCEPs
Spinal-SCEPs
C2-3 C3-4 C4-5 C5-6 C6-7 C7-T1
5μV
10μV
1.5ms
1ms
Figure 2. SCEPsobtained from patients with compressive cervical myelopathy. TES-SCEPs and spinal-SCEPs both showed marked attenuation of amplitude at the C4–C5 level, indicating a conduction block at C4–C5. TES-SCEPs indicates spinal cord evoked potentials after transcranial electric stimulation; spinal-SCEPs, spinal cord evoked potentials after spinal cord stimulation.
the negative peak (>50%) were considered to be significant (Figure 2).10–11
Statistical Analysis For TMS examinations, the upper limits for MEPs latency and CMCT were determined as the mean + 2.5 standard deviations (SDs). The t test was used to compare normal and patient data, whereas the Mann-Whitney U test and KruskalWallis test were used for unpaired patient data. All P values less than 0.05 were regarded as statistically significant.
RESULTS The recording of CMCT and SCEPs were performed and success in all 75 patients. The responsible levels that we estimated preoperatively from neurological examination and radiological findings were coincident with the site of conduction block in SCEPs in all patients.
Spinal Cord Evoked Potentials The SCEPs conduction abnormality was localized to the C3– C4 intervertebral level in 25 patients, C4–C5 in 22, C5–C6 in 17, and C6–C7 in 11.
MEPs Latency and CMCT Results for MEPs latencies, PMCT, and CMCT measured from the ADM and AH in normal subjects are shown in Table 1. In addition, result for MEPs latencies and CMCT measured from the ADM and AH in the patients are shown in Table 2. Mean values for CMCT in ADM and AH at each responsible level were significantly longer than the normal values (P < 0.001). However, the mean values for ADMCMCT at the C5–C6 and C6–C7 levels were significantly shorter than those observed at the C3–C4 and C4–C5 levels. The mean value for ADM-CMCT at the C6–C7 level in particular was clearly shorter than at the other levels (Figure 4A). In contrast, the mean values for AH-CMCT Spine
between each responsible level were not significantly different (Figure 4B). The mean value for ADM-MEPs latency was significantly delayed compared with the normal value, except at the C6– C7 level (C3–C4 ∼ C5–C6, P < 0.0001; C6–C7, P = 0.25). The mean value for ADM-MEPs latency at the C6–C7 level in particular was markedly shorter than at the other levels (Figure 3A): (Figure 4C; C6–C7 vs. C3–C4 and C4–C5, P < 0.001; C6–C7 vs. C5–C6, P = 0.01). The mean values for AH-MEPs latency were not significantly different between each responsible level (Figure 3B) (P = 0.43; Figure 4D). The mean values for AH-MEPs latency at each responsible level were significantly delayed compared with the normal values (P < 0.001). The mean values for PMCT in ADM and AH were not significantly different between each responsible level (ADM-PMCT [ms]; C3–C4 14.25 ± 1.26, C4–C5 14.68 ± 1.65, C5–C6 14.49 ± 1.8, C6–C7 14.45 ± 2.11, P = 0.75; AH-PMCT [ms]; and C3–C4 25.9 ± 4.2, C4–C5 25.85 ± 2.7, C5–C6 26.08 ± 1.77, C6–C7 25.42 ± 3.31, P = 0.58).
TABLE 1. Normative Data of MEPs Latency and
Normal Limit of CMCT
ADM Normal limit AH Normal limit
MEPs Latency (ms)
CMCT (ms)
PMCT (ms)
20.3 ± 1.9
5.2 ± 1.1
15.5 ± 1.5
25.1*
7.9*
19.3*
37.9 ± 2.1
12.1 ± 1.5
27.2 ± 2.4
43.2*
15.8*
33.2*
*Mean + 2.5 SD. MEPs indicates motor evoked potentials; CMCT, central motor conduction time; PMCT, peripheral motor conduction time; ADM, abductor digiti minimum; AH, abductor hallucis; SD, standard deviation.
www.spinejournal.com
E163
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. SPINE140905_LR E163
08/01/15 2:11 PM
DIAGNOSTICS
Transcranial Magnetic Stimulation Study in CCM • Funaba et al
TABLE 2. ADM-CMCT, AH-CMCT, ADM-MEPs, and AH-MEPs Latency in 75 Patients With CCM C3–C4 (n = 25)
ADM-CMCT
AH-CMCT
ADM-MEPs
AH-MEPs
Mean ± SD, (ms)
11.65 ± 3.18
20.15 ± 5.07
25.63 ± 3.49
46.07 ± 6.61
2 (8%)
5 (20%)
13 (52%)
9 (36%)
23 (92%)
20 (80%)
12 (48%)
16 (64%)
0
0
0
0
92%
80%
48%
64%
