J Neurosurg Spine 21:210–216, 2014 ©AANS, 2014
Electrophysiological evidence of functional improvement in the corticospinal tract after laminoplasty in patients with cervical compressive myelopathy Clinical article
Kazuyoshi Nakanishi, M.D., Ph.D., Nobuhiro Tanaka, M.D., Ph.D., Naosuke Kamei, M.D., Ph.D., Ryo Ohta, M.D., Ph.D., Yuki Fujioka, M.D., Ph.D., Takeshi Hiramatsu, M.D., Satoshi Ujigo, M.D., and Mitsuo Ochi, M.D., Ph.D. Department of Orthopaedic Surgery, Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima City, Hiroshima, Japan Object. Cervical laminoplasty is a surgical procedure for cervical compressive myelopathy (CCM), and satisfactory outcomes have been reported. However, few reports have examined the pathophysiology of improvements in spinal cord function. The aim of this study was to investigate the variation in central motor conduction time (CMCT) before and after cervical laminoplasty in patients with CCM. Methods. Motor evoked potentials (MEPs) following transcranial magnetic stimulation and compound muscle action potentials (CMAPs) and F-waves following electrical stimulation of the ulnar and tibial nerves at the wrist and ankle were measured from the abductor digiti minimi muscle (ADM) and abductor hallucis muscle (AH) in 42 patients with CCM before and 1 year after cervical laminoplasty. The peripheral conduction time (PCT) was calculated as follows: (latency of CMAPs + latency of F-waves - 1)/2. The CMCT was calculated by subtracting the PCT from the onset latency of the MEPs. The CMCT recovery ratio was defined and calculated as the ratio of CMCT values 1 year after surgery to those before surgery. The CMCT data were analyzed as longer or shorter CMCT between the patients’ right and left ADMs and AHs. The Japanese Orthopaedic Association (JOA) score for cervical myelopathy was obtained as a clinical outcome before and 1 year after surgery. The recovery rate (RR) 1 year after surgery was calculated using the following formula: (postoperative JOA score 1 year after surgery - preoperative JOA score)/(17 - preoperative JOA score) × 100. Correlations among CMCT parameters, patient age, JOA score, and RR were determined. Results. The longer and shorter CMCTs from the ADM (longer, p = 0.000; shorter, p = 0.008) and the longer CMCT from the AH (longer, p = 0.000) before surgery decreased significantly 1 year after surgery; the shorter CMCT from the AH did not significantly differ (shorter, p = 0.078). The mean JOA score before surgery was 10.1 ± 3.0 and improved significantly to 12.9 ± 2.7 at 1 year after surgery (p = 0.000). The mean CMCT recovery ratio and RR were 0.91 ± 0.18 and 0.43 ± 0.27, respectively. The longer/shorter CMCT parameters in the ADM and AH before or 1 year after surgery correlated significantly with the JOA score both before and 1 year after surgery. The CMCT recovery ratio from the longer CMCT in the ADM correlated significantly with the RR (r = -0.390, p = 0.011). There were no significant correlations between age and any CMCT parameters or CMCT recovery ratios. Conclusions. These results suggest that cervical laminoplasty improves corticospinal tract function 1 year after surgery, which may be one of the reasons for the JOA score improvements in patients with CCM. The degree of improvement in corticospinal tract function did not correlate with patient age in this case series. The results demonstrated quantitative evidence of the pathophysiology of functional recovery in the corticospinal tract following cervical laminoplasty in patients with CCM. (http://thejns.org/doi/abs/10.3171/2014.4.SPINE13545)
C
Key Words • motor evoked potentials • central motor conduction time • cervical myelopathy • transcranial magnetic stimulation • laminoplasty • surgical outcome
compressive myelopathy (CCM) is the most commonly acquired cause of spinal cord dysfunction. Myelopathy is the result of chronic seg-
ervical
Abbreviations used in this paper: ADM = abductor digiti minimi muscle; AH = abductor hallucis muscle; CCM = cervical compressive myelopathy; CMAP = compound muscle action potential; CMCT = central motor conduction time; JOA = Japanese Orthopaedic Association; MEP = motor evoked potential; PCT = peripheral conduction time; RR = recovery rate; SCEP = spinal cord evoked potential; TMS = transcranial magnetic stimulation.
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mental compression of the spinal cord due to spondylotic changes, disc herniation, or ossification of the posterior longitudinal ligaments.3 Surgery is usually the treatment of choice for patients with CCM. Cervical laminoplasty is a surgical procedure for CCM, and satisfactory surgical outcomes have been reported.1,6,7,13,29,30 However, few investigators have examined the pathology of CCM or the mechanism of improvements in spinal cord function. Monitoring motor evoked potentials (MEPs) following transcranial magnetic stimulation (TMS) is a noninvasive means of evaluating the electrophysiological function J Neurosurg: Spine / Volume 21 / August 2014
Improvement in CMCT after cervical laminoplasty of the corticospinal tract.9,19 Central motor conduction time (CMCT) can be measured to evaluate corticospinal function in cervical myelopathy.2,10,25,36 In fact, there is an excellent correlation between MRI findings and CMCT in patients with cervical myelopathy.17 Central motor conduction time is more prolonged in patients with more severe cervical spinal cord compression, according to MRI analysis. In addition, CMCT correlates significantly with the results of clinical assessment in patients with cervical myelopathy.33 However, variation in CMCT after decompression surgery in patients with cervical myelopathy has not been described. Therefore, our aim in this study was to investigate the variation in CMCT before and after surgery in patients with CCM.
Methods
Forty-two patients (10 women and 32 men) with CCM who were treated in our department between April 2008 and March 2011 were included in this study. Patients with other brain, thoracic spinal cord, cauda equina, or peripheral nerve disorders, such as diabetic neuropathy, or who exhibited any abnormalities in their sensory or motor peripheral nerve conduction velocities, were excluded. Their mean age was 64 years (range 36–87 years), and their mean height was 161 cm (range 139–179 cm). All patients provided written informed consent prior to initiation of the study. The patients and/or their families were informed that their data would be submitted for publication. This study received approval from the institutional review board of Hiroshima University. Each patient exhibited sensory disturbance in the upper and/or lower limbs and had a spastic gait disturbance. The presence of CCM was confirmed with neurological testing and MRI and was attributable to cervical spondylosis (33 patients), ossification of the posterior longitudinal ligament (6 patients), or cervical disc herniation (3 patients). Compression was detected in the C3–4, C4–5, and/or C5–6 level on MRI. All patients underwent cervical laminoplasty,35 and some exhibited neurological improvement. Orthopedic surgeons who did not perform laminoplasty obtained the Japanese Orthopaedic Association (JOA) score for cervical myelopathy8 as a clinical measure (total of 17 points possible) before surgery and 1 year after surgery. The recovery rate (RR) at the final follow-up was calculated using the following formula: (JOA score at final follow-up - preoperative JOA score)/ (17 - preoperative JOA score) × 100.5 Central motor conduction time was determined as previously described22,23 and was measured for all patients before surgery and 1 year after surgery. Surface recording electrodes were placed bilaterally on the abductor digiti minimi muscle (ADM) and abductor hallucis muscle (AH) using the standard belly-tendon method. Transcranial magnetic stimulation was delivered using a round coil with an outer diameter of 14 cm (model 200, Magstim) whose center was held over the vertex of the cranium when MEP recordings were made from the ADM. Stimulation was applied during a slight voluntary contraction. Recording sensitivity was set at a vertical gain of 0.2 mV/D and a horizontal sweep of 5 msec/D J Neurosurg: Spine / Volume 21 / August 2014
for ADM recordings. Recording sensitivity was set at a vertical gain of 0.1 mV/D and a horizontal sweep of 10 msec/D for AH recordings. A clockwise current in the coil, as viewed from above, was delivered to stimulate the left hemisphere, and a counterclockwise current was used to stimulate the right hemisphere. The magnetic stimulus intensity was set at 20% above the threshold for the MEPs. The coil was then shifted anteriorly when the MEP recordings were made from the AH. The MEPs were recorded more than 10 times, at least 4 reproducible responses were superimposed, and their latencies were measured (Fig. 1). For most trials, a stimulus intensity of 80% was adequate to elicit consistent MEPs of similar morphology. Compound muscle action potentials (CMAPs) and F-waves were recorded following continuous current stimulation at supramaximal intensity (0.2-msec square wave pulses) of the ulnar nerve at the wrist and the tibial nerve at the ankle. None of the patients showed markedly diminished CMAP amplitudes in either the ADM or AH. Thirty-two serial responses were obtained, and the shortest F-wave latency was measured. All muscle responses were recorded using a commercially available electromyography system (Viking IV, Nicolet Biomedical Corp.) after they traversed a bandpass filter of 0.5–2000 Hz. An epoch of 100 msec after stimulation was digitized at a 5-kHz sampling rate. The peripheral conduction time (PCT), excluding the turnaround time at the spinal motor neuron (1 msec), was calculated from the latencies of the CMAPs and F-waves as follows: (latency of CMAPs + latency of F-waves - 1)/2.15 The conduction time from the motor cortex to the spinal motor neurons—that is, the CMCT—was calculated by subtracting the PCT from the onset latency of the MEPs. An examiner blinded to the patient’s history, clinical features, and MRI results performed these measurements. The MEP, PCT, and CMCT data were analyzed on both the right and left sides. In addition, the CMCT data were analyzed as longer or shorter CMCTs between the patients’ right and left ADMs and AHs before surgery. Because a bilateral difference was observed in the symptoms and CMCT values differed between the right and left sides in the patients, the parameters for each longer and shorter side should be respectively analyzed, as done in a previous study.22,23 At follow-up, each longer and shorter CMCT on the same side were compared with the same data from before surgery. The CMCT recovery ratio was defined and calculated as the CMCT values 1 year after surgery divided by those before surgery. Data were compared using the Wilcoxon test for nonparametric statistical analysis, and a p value < 0.05 was considered to be statistically significant. The CMCT ratios were compared using Scheffe’s test with ANOVA among the CMCT recovery ratio from the longer or shorter CMCT in the ADM or AH. Correlations among patient age, JOA score, recovery rate (RR), and CMCT values were estimated using Pearson’s correlation coefficient (r). A correlation was accepted as significant when p < 0.05 and |r| > 0.3. Electrophysiological data are presented as the mean ± standard deviation (range). 211
K. Nakanishi et al.
Fig. 1. Motor evoked potential waveforms recorded from the ADM (A) and AH (B) on both sides. ms = msec.
Results
cantly shorter than those before surgery in both the ADM (right, p = 0.006; left, p = 0.000) and the AH (right, p = 0.001; left, p = 0.006), while there were no significant differences in the PCTs before and after surgery in both the ADM (right, p = 0.231; left, p = 0.722) and the AH (right, p = 0.856; left, p = 0.655; Table 1). The CMCTs detected from the ADM (right, p = 0.010; left, p = 0.000) and the AH (right, p = 0.000; left, p = 0.002) decreased significantly 1 year after surgery. The longer and shorter CMCTs from the ADM (longer, p = 0.000; shorter, p = 0.008) and the longer CMCT from the AH (longer, p =
The MEP latency, PCT, and CMCT values are shown in Tables 1 and 2. All parameters include data from more than 40 patients. The MEP, F-wave, and M-wave could not be recorded from the left ADM in one patient before or 1 year after surgery. The MEP could not be recorded in two other patients from both AHs before surgery. In one of these two patients, F- and M-waves were not detected from either AH before surgery. The MEP latencies 1 year after surgery were signifi-
TABLE 1: Summary of MEP latency, PCT, and CMCT values in the ADM and AH before and 1 year after cervical laminoplasty* MEP Latency ADM Parameter before surgery no. of patients min value max value mean value SD at FU no. of patients min value max value mean value SD p value
PCT AH
CMCT
ADM
AH
ADM
AH
Rt
Lt
Rt
Lt
Rt
Lt
Rt
Lt
Rt
Lt
Rt
Lt
42 19.5 40.3 26.0 4.5
41 19.3 35.9 26.0 4.3
40 36.3 67.1 44.9 6.1
40 37.1 59.3 44.5 5.2
42 12.0 18.7 14.6 1.5
41 12.10 17.6 14.5 1.4
41 21.8 32.0 25.6 2.3
41 21.5 31.7 25.7 2.5
42 5.2 21.6 11.4 3.9
41 4.6 20.3 11.5 3.7
40 13.6 38.5 19.3 4.8
40 13.0 30.5 18.8 3.9
42 34.8 56.4 43.3 4.9 0.001†
42 36.0 55.0 43.3 4.4 0.006†
42 11.0 18.9 14.3 1.4 0.231
41 12.1 19.4 14.6 1.6 0.722
42 21.9 32.4 25.6 2.2 0.856
42 20.8 31.2 25.6 2.4 0.655
42 5.0 19.2 10.3 3.5 0.010§
41 5.2 16.0 9.7 2.7 0.000‡
42 41 18.5 19.8 36.6 32.9 24.6 24.2 4.0 3.4 0.006† 0.000‡
42 42 11.6 12.5 29.4 23.9 17.7 17.7 3.7 3.4 0.000‡ 0.002†
* FU = follow-up. † p < 0.01, compared with before surgery. ‡ p < 0.001, compared with before surgery. § p < 0.05, compared with before surgery.
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Improvement in CMCT after cervical laminoplasty TABLE 2: Summary of CMCT values in and recovery ratios for right and left ADMs and AHs ADM Parameter CMCT before surgery no. of patients min value max value mean value SD at FU no. of patients min value max value mean value SD p value CMCT recovery ratio no. of patients min value max value mean value SD
Longer
AH
Shorter
Longer
Shorter
42 4.6 20.3 10.3 3.3
40 13.7 38.5 20.4 4.5
40 13.0 30.5 17.7 3.8
42 5.0 19.2 10.7 3.5 0.000*
41 5.2 15.4 9.1 2.6 0.008†
42 11.6 29.4 18.3 3.8 0.000*
42 11.8 23.9 17.1 3.2 0.078
42 0.61 1.52 0.86‡ 0.19
40 0.63 1.28 0.90 0.11
41 0.53 1.64 0.94 0.23
40 0.77 1.26 0.97 0.11
42 6.7 21.6 12.7 3.9
* p < 0.001, compared with before surgery. † p < 0.01, compared with before surgery. ‡ p < 0.05, compared with CMCT recovery ratio from the shorter CMCT in the AH.
0.000) before surgery also decreased significantly 1 year after surgery; the shorter CMCT from the AH did not significantly differ (shorter, p = 0.078; Table 2). The mean CMCT recovery ratio for both the ADM and the AH was 0.91 ± 0.18 (range 0.53–1.64). The mean CMCT recovery ratios from the longer and shorter CMCTs in the ADM were 0.86 ± 0.19 (range 0.61–1.52) and 0.90 ± 0.11 (range 0.63–1.28), and those from the longer and shorter CMCTs in the AH were 0.94 ± 0.23 (range 0.53–1.64) and 0.97 ± 0.11 (range 0.77–1.26), respectively. Among these CMCT recovery ratios, the one from the longer CMCT in the ADM shortened significantly, as compared with the one from the shorter CMCT in the AH (p < 0.05). The mean JOA score before surgery was 10.1 ± 3.0 (range 3.5–16.0). Improvements in the JOA score were attained in all patients after surgery. The score improved significantly to 12.9 ± 2.7 (range 7.0–17.0) at 1 year after surgery (p = 0.000). Thus, the mean recovery rate (RR) was 0.43 ± 0.27 (range 0.06–1.00). Patient age correlated significantly with JOA score at 1 year after surgery (r = -0.352, p = 0.022). In contrast, age did not correlate with the JOA score before surgery (r = -261, r = 0.095) or RR (r = -0.204, r = 0.169). The correlations among patient age, JOA score, RR, and CMCT values are shown in Table 3. The longer/shorter CMCT parameters in the ADM and AH before surgery J Neurosurg: Spine / Volume 21 / August 2014
or 1 year after correlated significantly with JOA score both before and 1 year after surgery. The longer CMCT values from the ADM at 1 year after surgery (r = -0.391, p = 0.010) and the CMCT recovery ratio from the longer CMCT in the ADM (r = -0.390, p = 0.011) correlated significantly with the RR. There were no significant correlations between age and any CMCT parameters.
Discussion
Our results show a significant decrease in the CMCT parameters in patients with CCM at 1 year after surgery. The CMCT parameters before or 1 year after surgery correlated significantly with the JOA score both before and 1 year after surgery. The CMCT recovery ratio from the longer CMCT in the ADM significantly correlated with the RR. Central motor conduction time is calculated by subtracting PCT from MEP latency. Thus, the physiology of prolonged CMCT is complex, and only a few reports have noted the mechanism of its occurrence in CCM. Kaneko and colleagues examined CMCT following TMS, as well as spinal cord evoked potentials (SCEPs) following transcranial electric stimulation (TES), in patients with CCM and normal subjects.10 Their results showed that CMCT was prolonged in such patients and that the patients exhibited significant attenuation in their SCEP amplitudes following TES but no significant delay in their SCEP latencies. The authors concluded that impaired temporal summation of multiple descending potentials following TMS produces delays in motor neuron firing that contribute to the prolongation of CMCT. Moreover, a significant correlation between CMCT prolongation and SCEP amplitude attenuation, and no significant correlation between CMCT prolongation and SCEP latency in patients with CCM have been reported.22,23 Thus, corticospinal block is thought to cause CMCT prolongation. Our results showed that functional recovery in the corticospinal tract following cervical laminoplasty in patients with CCM can be quantitatively assessed and that the corticospinal conduction block improvements due to the increase in the number of axons that propagate the evoked potentials were one of the causes of improved JOA scores. The CMCT values did not completely improve to the normal range, which has been reported previously,10,28 and the mean CMCT recovery rate and (JOA score) RR in our series were 0.91 and 0.43, respectively. The data should be important information on the pathophysiology of recovery following surgery. Further, CMCT for the symptomatic side has been shown to correlate significantly with the preoperative JOA score, as well as with the JOA score at 1 year after cervical laminoplasty in patients with CCM.33 In our study, CMCT parameters correlated significantly with the JOA score before and 1 year after surgery, and the CMCT ratio from the longer CMCT in the ADM correlated with the RR, supporting the conclusion that CMCT may be useful in predicting the outcome of surgical treatment, as previously described by Takahashi et al.33 Kawaguchi et al. documented a reduction in JOA scores in 20 patients in a minimum 10-year follow-up of 126 cervical myelopathy patients who underwent cervi213
K. Nakanishi et al. TABLE 3: Correlations among patient age, JOA score, RR, and CMCT values Before Surgery ADM Parameter
Longer
At FU AH
Shorter
no. of patients 42 42 age r 0.240 0.207 p 0.126 0.189 JOA score before surgery r −0.521 −0.532 p 0.000* 0.000* JOA score at FU r −0.400 −0.388 p 0.009‡ 0.011†
ADM
CMCT Recovery Ratio ADM AH
AH
Longer
Shorter
Longer
Shorter
Longer
Shorter
Longer
Shorter
Longer
Shorter
40
40
42
41
42
42
42
40
41
40
−0.094 0.564
0.066 0.684
0.252 0.107
0.284 0.072
−0.023 0.883
0.019 0.905
0.066 0.680
0.134 0.409
0.127 0.428
−0.052 0.750
−0.528 −0.589 0.000* 0.000*
−0.377 −0.338 0.014† 0.031†
−0.598 −0.509 0.000* 0.001‡
0.137 0.388
−0.194 0.231
0.288 0.068
0.212 0.189
−0.444 −0.511 0.004‡ 0.001‡
−0.553 −0.357 0.000* 0.022†
−0.512 −0.387 0.001‡ 0.011†
−0.255 0.103
−0.151 0.353
0.166 0.300
0.224 0.165
−0.391
−0.212
−0.208
−0.111
−0.390
−0.100
0.000
0.134
0.184
0.186
0.484
0.011†
0.539
0.998
0.410
RR r
−0.119
−0.090
−0.150
−0.203
p
0.452
0.569
0.355
0.208
0.010†
* p < 0.001. † p < 0.05. ‡ p < 0.01.
cal laminoplasty.12 They reported that the causes of deterioration were axial spread of ossification of the posterior longitudinal ligament, other spinal lesions, cerebral infarction, and peripheral neuropathy. Central motor conduction time measurements are also a useful tool for detecting functional deterioration of the motor pathway due to thoracic spinal cord compression24 or cerebral infarction,27,31 and the F-wave study can detect a peripheral neuropathy.14,16,26 Consequently, our data should provide important information when a reduced JOA score following surgery is observed and those electrophysiological screenings are implemented, because our study utilized a simple clinical model of cervical myelopathy. To obtain accurate and reliable MEP findings, the patients included in our study had simple spinal cord compressions without any other neural disorders and successfully underwent laminoplasty. Patient age at the time of surgery influences surgical outcome. In previous assessments of surgical outcome in elderly patients with CCM, the results of laminoplasty in elderly patients were worse than those in younger patients.20,29,37 The poor recovery in the elderly patients may be attributable to the age-related decrease of motor neurons and myelinated fibers in the spinal cord. On the other hand, good clinical results have been reported even in elderly patients with myelopathy.34 Moreover, studies have shown no significant differences in RR of the JOA score between elderly and nonelderly patients.11,32 Kawaguchi et al. noted that cervical laminoplasty improves quality of life and activities of daily living even in elderly patients with cervical spondylotic myelopathy.11 Machino et al. reported that the differences in the JOA score before and after surgery were similar among nonelderly (age < 65 214
years), “young-old” (age 65–74 years), and “old-old” (age ≥ 75 years) patient groups, although RR and JOA scores before and after surgery were low in the elderly patients.18 Thus, these authors concluded that elderly patients can have a reasonable recovery after cervical laminoplasty. Suzuki et al. noted that although no significant difference was observed in the RR of the JOA score among groups according to age, the time point at which the JOA score reached a plateau after surgery was significantly later in elderly than in nonelderly patients.32 Surgical outcome, especially in elderly patients with CCM, can be affected by many factors and is still controversial. In the present study, age did not correlate with pre- or postoperative CMCT values or with the CMCT recovery ratio. These results suggest equivalence of function of the compressed corticospinal tract, as well as improvements 1 year after surgery between elderly and nonelderly patients. There were several limitations to our study. Except for the longer CMCT from the ADM at follow-up and the CMCT recovery ratio from the longer CMCT in the ADM, the RR did not completely correlate with the CMCT before surgery, at 1 year after surgery, or the CMCT recovery ratio. Thus, other factors may have influenced the RR in our cases. Central motor conduction time reflects the central motor pathway, and the sensory disturbance was not objectively evaluated. Another limitation was the small number of cases; it was too small to validate the factor that may have influenced the RR. Although few reports provide an objective assessment of corticospinal tract function, Nakamura et al. demonstrated that preoperative diffusion tensor tractography may predict neurological recovery in patients with CCM after laminoplasty.21 As an assessment of sensory disturJ Neurosurg: Spine / Volume 21 / August 2014
Improvement in CMCT after cervical laminoplasty bance, the utility of somatosensory evoked magnetic field dipole measurements by magnetoencephalography has been described.4 The CMCT examination should be used with new methods to identify factors that impact surgical outcome. Moreover, it is unclear how CMCT parameters and the JOA score were affected when other neural disorders were complicated. For example, diabetic neuropathy is a common complication among individuals of an age at which they are susceptible to CCM. Patients with diabetic neuropathy present with numbness in their hands and feet, and the F-wave latency and PCT are prolonged in these patients.14,16,26 Therefore, complicating diabetic neuropathy may affect the JOA score, as well as the electrophysiological results. Further validation of CMCT measurements is required for cases with other complicating neural disorders. CMCT measurements should be developed as a more useful tool that can clarify the pathophysiology and quantitatively assess the functional variation of corticospinal tracts.
Conclusions
In summary, this study suggests that cervical laminoplasty improves corticospinal tract function, which may be one of the reasons for the JOA score improvements in patients with CCM at 1 year after surgery. The degree of CMCT improvement did not correlate with patient age in our series. Our results offer quantitative evidence on the pathophysiology of functional recovery in the corticospinal tract following cervical laminoplasty in patients with CCM. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Supported by the Grants-in-Aid for Scientific Research (Scientific Research C, Research Project Number: 24592198) from Japan Society for the Promotion of Science, Ministry of Health, Labour and Welfare. Author contributions to the study and manuscript preparation include the following. Conception and design: Nakanishi. Acquisition of data: Nakanishi, Kamei, Ohta, Fujioka, Hiramatsu, Ujigo. Analy sis and interpretation of data: Nakanishi. Drafting the article: Naka nishi. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Nakanishi. Statistical analysis: Nakanishi. Study supervision: Ochi. References 1. Chiba K, Ogawa Y, Ishii K, Takaishi H, Nakamura M, Maruiwa H, et al: Long-term results of expansive open-door laminoplasty for cervical myelopathy—average 14-year follow-up study. Spine (Phila Pa 1976) 31:2998–3005, 2006 2. Di Lazzaro V, Restuccia D, Colosimo C, Tonali P: The contribution of magnetic stimulation of the motor cortex to the diagnosis of cervical spondylotic myelopathy. Correlation of central motor conduction to distal and proximal upper limb muscles with clinical and MRI findings. Electroencephalogr Clin Neurophysiol 85:311–320, 1992 3. Fehlings MG, Skaf G: A review of the pathophysiology of cervical spondylotic myelopathy with insights for potential novel mechanisms drawn from traumatic spinal cord injury. Spine (Phila Pa 1976) 23:2730–2737, 1998
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4. Goto T, Tsuyuguchi N, Ohata K, Tsutada T, Hattori H, Shimogawara M, et al: Usefulness of somatosensory evoked magnetic field dipole measurements by magnetoencephalography for assessing spinal cord function. J Neurosurg 96 (1 Suppl):62–67, 2002 5. Hirabayashi K, Miyakawa J, Satomi K, Maruyama T, Wakano K: Operative results and postoperative progression of ossification among patients with ossification of cervical posterior longitudinal ligament. Spine (Phila Pa 1976) 6:354–364, 1981 6. Hirabayashi K, Satomi K: Operative procedure and results of expansive open-door laminoplasty. Spine (Phila Pa 1976) 13:870–876, 1988 7. Itoh T, Tsuji H: Technical improvements and results of laminoplasty for compressive myelopathy in the cervical spine. Spine (Phila Pa 1976) 10:729–736, 1985 8. Japanese Orthopaedic Association: Japanese Orthopaedic Association scoring system for cervical myelopathy. J Jpn Orthop Assoc 68:490–503, 1994 9. Jaskolski DJ, Jarratt JA, Jakubowski J: Clinical evaluation of magnetic stimulation in cervical spondylosis. Br J Neurosurg 3:541–548, 1989 10. Kaneko K, Taguchi T, Morita H, Yonemura H, Fujimoto H, Kawai S: Mechanism of prolonged central motor conduction time in compressive cervical myelopathy. Clin Neurophysiol 112:1035–1040, 2001 11. Kawaguchi Y, Kanamori M, Ishihara H, Ohmori K, Abe Y, Kimura T: Pathomechanism of myelopathy and surgical results of laminoplasty in elderly patients with cervical spondylosis. Spine (Phila Pa 1976) 28:2209–2214, 2003 12. Kawaguchi Y, Kanamori M, Ishihara H, Ohmori K, Nakamura H, Kimura T: Minimum 10-year followup after en bloc cervical laminoplasty. Clin Orthop Relat Res (411):129–139, 2003 13. Kawai S, Sunago K, Doi K, Saika M, Taguchi T: Cervical laminoplasty (Hattori’s method). Procedure and follow-up results. Spine (Phila Pa 1976) 13:1245–1250, 1988 14. Kimura J: F-wave determination in nerve conduction studies. Adv Neurol 39:961–975, 1983 15. Kimura J: Principles and pitfalls of nerve conduction studies. Ann Neurol 16:415–429, 1984 16. Kimura J, Yamada T, Stevland NP: Distal slowing of motor nerve conduction velocity in diabetic polyneuropathy. J Neurol Sci 42:291–302, 1979 17. Lo YL, Chan LL, Lim W, Tan SB, Tan CT, Chen JL, et al: Systematic correlation of transcranial magnetic stimulation and magnetic resonance imaging in cervical spondylotic myelopathy. Spine (Phila Pa 1976) 29:1137–1145, 2004 18. Machino M, Yukawa Y, Hida T, Ito K, Nakashima H, Kanbara S, et al: Can elderly patients recover adequately after laminoplasty?: a comparative study of 520 patients with cervical spondylotic myelopathy. Spine (Phila Pa 1976) 37:667–671, 2012 19. Maertens de Noordhout A, Remacle JM, Pepin JL, Born JD, Delwaide PJ: Magnetic stimulation of the motor cortex in cervical spondylosis. Neurology 41:75–80, 1991 20. Matsuda Y, Shibata T, Oki S, Kawatani Y, Mashima N, Oishi H: Outcomes of surgical treatment for cervical myelopathy in patients more than 75 years of age. Spine (Phila Pa 1976) 24:529–534, 1999 21. Nakamura M, Fujiyoshi K, Tsuji O, Konomi T, Hosogane N, Watanabe K, et al: Clinical significance of diffusion tensor tractography as a predictor of functional recovery after laminoplasty in patients with cervical compressive myelopathy. Clinical article. J Neurosurg Spine 17:147–152, 2012 22. Nakanishi K, Tanaka N, Fujiwara Y, Kamei N, Ochi M: Corticospinal tract conduction block results in the prolongation of central motor conduction time in compressive cervical myelopathy. Clin Neurophysiol 117:623–627, 2006 23. Nakanishi K, Tanaka N, Kamei N, Hamasaki T, Nishida K, Touten Y, et al: Significant correlation between corticospinal
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K. Nakanishi et al. tract conduction block and prolongation of central motor conduction time in compressive cervical myelopathy. J Neurol Sci 256:71–74, 2007 24. Nakanishi K, Tanaka N, Sasaki H, Kamei N, Hamasaki T, Yamada K, et al: Assessment of central motor conduction time in the diagnosis of compressive thoracic myelopathy. Spine (Phila Pa 1976) 35:E1593–E1598, 2010 25. Ofuji A, Kaneko K, Taguchi T, Fuchigami Y, Morita H, Kawai S: New method to measure central motor conduction time using transcranial magnetic stimulation and T-response. J Neurol Sci 160:26–32, 1998 26. Pan H, Jian F, Lin J, Chen N, Zhang C, Zhang Z, et al: F-wave latencies in patients with diabetes mellitus. Muscle Nerve [epub ahead of print], 2013 27. Pennisi G, Alagona G, Rapisarda G, Nicoletti F, Costanzo E, Ferri R, et al: Transcranial magnetic stimulation after pure motor stroke. Clin Neurophysiol 113:1536–1543, 2002 28. Robinson LR, Jantra P, MacLean IC: Central motor conduction times using transcranial stimulation and F wave latencies. Muscle Nerve 11:174–180, 1988 29. Satomi K, Nishu Y, Kohno T, Hirabayashi K: Long-term follow-up studies of open-door expansive laminoplasty for cervical stenotic myelopathy. Spine (Phila Pa 1976) 19:507–510, 1994 30. Seichi A, Takeshita K, Ohishi I, Kawaguchi H, Akune T, Ana mizu Y, et al: Long-term results of double-door laminoplasty for cervical stenotic myelopathy. Spine (Phila Pa 1976) 26:479–487, 2001 31. Sue CM, Yiannikas C, Clouston PD, Lim CL, Graham S: Transcranial cortical stimulation in disorders of the central motor pathways. J Clin Neurosci 4:19–25, 1997 32. Suzuki A, Misawa H, Simogata M, Tsutsumimoto T, Takaoka K, Nakamura H: Recovery process following cervical laminoplasty in patients with cervical compression myelopathy: prospective cohort study. Spine (Phila Pa 1976) 34:2874–2879, 2009
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33. Takahashi J, Hirabayashi H, Hashidate H, Ogihara N, Yama zaki I, Kamimura M, et al: Assessment of cervical myelopathy using transcranial magnetic stimulation and prediction of prognosis after laminoplasty. Spine (Phila Pa 1976) 33:E15– E20, 2008 34. Tanaka N, Nakanishi K, Fujimoto Y, Sasaki H, Kamei N, Hamasaki T, et al: Clinical results of cervical myelopathy in patients older than 80 years of age: evaluation of spinal function with motor evoked potentials. Clinical article. J Neurosurg Spine 11:421–426, 2009 35. Tanaka N, Nakanishi K, Fujimoto Y, Sasaki H, Kamei N, Hamasaki T, et al: Expansive laminoplasty for cervical myelopathy with interconnected porous calcium hydroxyapatite ceramic spacers: comparison with autogenous bone spacers. J Spinal Disord Tech 21:547–552, 2008 36. Tavy DL, Wagner GL, Keunen RW, Wattendorff AR, Hekster RE, Franssen H: Transcranial magnetic stimulation in patients with cervical spondylotic myelopathy: clinical and radiological correlations. Muscle Nerve 17:235–241, 1994 37. Yamazaki T, Yanaka K, Sato H, Uemura K, Tsukada A, Nose T: Cervical spondylotic myelopathy: surgical results and factors affecting outcome with special reference to age differences. Neurosurgery 52:122–126, 2003
Manuscripts submitted June 11, 2013. Accepted April 17, 2014. Please include this information when citing this paper: published online May 23, 2014; DOI: 10.3171/2014.4.SPINE13545. Address correspondence to: Kazuyoshi Nakanishi, M.D., Ph.D., Department of Orthopaedic Surgery, Programs for Applied Biomedicine, Division of Clinical Medical Science, Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minamiku, Hiroshima 734-8551, Japan. email: [email protected].
J Neurosurg: Spine / Volume 21 / August 2014
Electrophysiological evidence of functional improvement in the corticospinal tract after laminoplasty in patients with cervical compressive myelopathy Clinical article
Kazuyoshi Nakanishi, M.D., Ph.D., Nobuhiro Tanaka, M.D., Ph.D., Naosuke Kamei, M.D., Ph.D., Ryo Ohta, M.D., Ph.D., Yuki Fujioka, M.D., Ph.D., Takeshi Hiramatsu, M.D., Satoshi Ujigo, M.D., and Mitsuo Ochi, M.D., Ph.D. Department of Orthopaedic Surgery, Graduate School of Biomedical & Health Sciences, Hiroshima University, Hiroshima City, Hiroshima, Japan Object. Cervical laminoplasty is a surgical procedure for cervical compressive myelopathy (CCM), and satisfactory outcomes have been reported. However, few reports have examined the pathophysiology of improvements in spinal cord function. The aim of this study was to investigate the variation in central motor conduction time (CMCT) before and after cervical laminoplasty in patients with CCM. Methods. Motor evoked potentials (MEPs) following transcranial magnetic stimulation and compound muscle action potentials (CMAPs) and F-waves following electrical stimulation of the ulnar and tibial nerves at the wrist and ankle were measured from the abductor digiti minimi muscle (ADM) and abductor hallucis muscle (AH) in 42 patients with CCM before and 1 year after cervical laminoplasty. The peripheral conduction time (PCT) was calculated as follows: (latency of CMAPs + latency of F-waves - 1)/2. The CMCT was calculated by subtracting the PCT from the onset latency of the MEPs. The CMCT recovery ratio was defined and calculated as the ratio of CMCT values 1 year after surgery to those before surgery. The CMCT data were analyzed as longer or shorter CMCT between the patients’ right and left ADMs and AHs. The Japanese Orthopaedic Association (JOA) score for cervical myelopathy was obtained as a clinical outcome before and 1 year after surgery. The recovery rate (RR) 1 year after surgery was calculated using the following formula: (postoperative JOA score 1 year after surgery - preoperative JOA score)/(17 - preoperative JOA score) × 100. Correlations among CMCT parameters, patient age, JOA score, and RR were determined. Results. The longer and shorter CMCTs from the ADM (longer, p = 0.000; shorter, p = 0.008) and the longer CMCT from the AH (longer, p = 0.000) before surgery decreased significantly 1 year after surgery; the shorter CMCT from the AH did not significantly differ (shorter, p = 0.078). The mean JOA score before surgery was 10.1 ± 3.0 and improved significantly to 12.9 ± 2.7 at 1 year after surgery (p = 0.000). The mean CMCT recovery ratio and RR were 0.91 ± 0.18 and 0.43 ± 0.27, respectively. The longer/shorter CMCT parameters in the ADM and AH before or 1 year after surgery correlated significantly with the JOA score both before and 1 year after surgery. The CMCT recovery ratio from the longer CMCT in the ADM correlated significantly with the RR (r = -0.390, p = 0.011). There were no significant correlations between age and any CMCT parameters or CMCT recovery ratios. Conclusions. These results suggest that cervical laminoplasty improves corticospinal tract function 1 year after surgery, which may be one of the reasons for the JOA score improvements in patients with CCM. The degree of improvement in corticospinal tract function did not correlate with patient age in this case series. The results demonstrated quantitative evidence of the pathophysiology of functional recovery in the corticospinal tract following cervical laminoplasty in patients with CCM. (http://thejns.org/doi/abs/10.3171/2014.4.SPINE13545)
C
Key Words • motor evoked potentials • central motor conduction time • cervical myelopathy • transcranial magnetic stimulation • laminoplasty • surgical outcome
compressive myelopathy (CCM) is the most commonly acquired cause of spinal cord dysfunction. Myelopathy is the result of chronic seg-
ervical
Abbreviations used in this paper: ADM = abductor digiti minimi muscle; AH = abductor hallucis muscle; CCM = cervical compressive myelopathy; CMAP = compound muscle action potential; CMCT = central motor conduction time; JOA = Japanese Orthopaedic Association; MEP = motor evoked potential; PCT = peripheral conduction time; RR = recovery rate; SCEP = spinal cord evoked potential; TMS = transcranial magnetic stimulation.
210
mental compression of the spinal cord due to spondylotic changes, disc herniation, or ossification of the posterior longitudinal ligaments.3 Surgery is usually the treatment of choice for patients with CCM. Cervical laminoplasty is a surgical procedure for CCM, and satisfactory surgical outcomes have been reported.1,6,7,13,29,30 However, few investigators have examined the pathology of CCM or the mechanism of improvements in spinal cord function. Monitoring motor evoked potentials (MEPs) following transcranial magnetic stimulation (TMS) is a noninvasive means of evaluating the electrophysiological function J Neurosurg: Spine / Volume 21 / August 2014
Improvement in CMCT after cervical laminoplasty of the corticospinal tract.9,19 Central motor conduction time (CMCT) can be measured to evaluate corticospinal function in cervical myelopathy.2,10,25,36 In fact, there is an excellent correlation between MRI findings and CMCT in patients with cervical myelopathy.17 Central motor conduction time is more prolonged in patients with more severe cervical spinal cord compression, according to MRI analysis. In addition, CMCT correlates significantly with the results of clinical assessment in patients with cervical myelopathy.33 However, variation in CMCT after decompression surgery in patients with cervical myelopathy has not been described. Therefore, our aim in this study was to investigate the variation in CMCT before and after surgery in patients with CCM.
Methods
Forty-two patients (10 women and 32 men) with CCM who were treated in our department between April 2008 and March 2011 were included in this study. Patients with other brain, thoracic spinal cord, cauda equina, or peripheral nerve disorders, such as diabetic neuropathy, or who exhibited any abnormalities in their sensory or motor peripheral nerve conduction velocities, were excluded. Their mean age was 64 years (range 36–87 years), and their mean height was 161 cm (range 139–179 cm). All patients provided written informed consent prior to initiation of the study. The patients and/or their families were informed that their data would be submitted for publication. This study received approval from the institutional review board of Hiroshima University. Each patient exhibited sensory disturbance in the upper and/or lower limbs and had a spastic gait disturbance. The presence of CCM was confirmed with neurological testing and MRI and was attributable to cervical spondylosis (33 patients), ossification of the posterior longitudinal ligament (6 patients), or cervical disc herniation (3 patients). Compression was detected in the C3–4, C4–5, and/or C5–6 level on MRI. All patients underwent cervical laminoplasty,35 and some exhibited neurological improvement. Orthopedic surgeons who did not perform laminoplasty obtained the Japanese Orthopaedic Association (JOA) score for cervical myelopathy8 as a clinical measure (total of 17 points possible) before surgery and 1 year after surgery. The recovery rate (RR) at the final follow-up was calculated using the following formula: (JOA score at final follow-up - preoperative JOA score)/ (17 - preoperative JOA score) × 100.5 Central motor conduction time was determined as previously described22,23 and was measured for all patients before surgery and 1 year after surgery. Surface recording electrodes were placed bilaterally on the abductor digiti minimi muscle (ADM) and abductor hallucis muscle (AH) using the standard belly-tendon method. Transcranial magnetic stimulation was delivered using a round coil with an outer diameter of 14 cm (model 200, Magstim) whose center was held over the vertex of the cranium when MEP recordings were made from the ADM. Stimulation was applied during a slight voluntary contraction. Recording sensitivity was set at a vertical gain of 0.2 mV/D and a horizontal sweep of 5 msec/D J Neurosurg: Spine / Volume 21 / August 2014
for ADM recordings. Recording sensitivity was set at a vertical gain of 0.1 mV/D and a horizontal sweep of 10 msec/D for AH recordings. A clockwise current in the coil, as viewed from above, was delivered to stimulate the left hemisphere, and a counterclockwise current was used to stimulate the right hemisphere. The magnetic stimulus intensity was set at 20% above the threshold for the MEPs. The coil was then shifted anteriorly when the MEP recordings were made from the AH. The MEPs were recorded more than 10 times, at least 4 reproducible responses were superimposed, and their latencies were measured (Fig. 1). For most trials, a stimulus intensity of 80% was adequate to elicit consistent MEPs of similar morphology. Compound muscle action potentials (CMAPs) and F-waves were recorded following continuous current stimulation at supramaximal intensity (0.2-msec square wave pulses) of the ulnar nerve at the wrist and the tibial nerve at the ankle. None of the patients showed markedly diminished CMAP amplitudes in either the ADM or AH. Thirty-two serial responses were obtained, and the shortest F-wave latency was measured. All muscle responses were recorded using a commercially available electromyography system (Viking IV, Nicolet Biomedical Corp.) after they traversed a bandpass filter of 0.5–2000 Hz. An epoch of 100 msec after stimulation was digitized at a 5-kHz sampling rate. The peripheral conduction time (PCT), excluding the turnaround time at the spinal motor neuron (1 msec), was calculated from the latencies of the CMAPs and F-waves as follows: (latency of CMAPs + latency of F-waves - 1)/2.15 The conduction time from the motor cortex to the spinal motor neurons—that is, the CMCT—was calculated by subtracting the PCT from the onset latency of the MEPs. An examiner blinded to the patient’s history, clinical features, and MRI results performed these measurements. The MEP, PCT, and CMCT data were analyzed on both the right and left sides. In addition, the CMCT data were analyzed as longer or shorter CMCTs between the patients’ right and left ADMs and AHs before surgery. Because a bilateral difference was observed in the symptoms and CMCT values differed between the right and left sides in the patients, the parameters for each longer and shorter side should be respectively analyzed, as done in a previous study.22,23 At follow-up, each longer and shorter CMCT on the same side were compared with the same data from before surgery. The CMCT recovery ratio was defined and calculated as the CMCT values 1 year after surgery divided by those before surgery. Data were compared using the Wilcoxon test for nonparametric statistical analysis, and a p value < 0.05 was considered to be statistically significant. The CMCT ratios were compared using Scheffe’s test with ANOVA among the CMCT recovery ratio from the longer or shorter CMCT in the ADM or AH. Correlations among patient age, JOA score, recovery rate (RR), and CMCT values were estimated using Pearson’s correlation coefficient (r). A correlation was accepted as significant when p < 0.05 and |r| > 0.3. Electrophysiological data are presented as the mean ± standard deviation (range). 211
K. Nakanishi et al.
Fig. 1. Motor evoked potential waveforms recorded from the ADM (A) and AH (B) on both sides. ms = msec.
Results
cantly shorter than those before surgery in both the ADM (right, p = 0.006; left, p = 0.000) and the AH (right, p = 0.001; left, p = 0.006), while there were no significant differences in the PCTs before and after surgery in both the ADM (right, p = 0.231; left, p = 0.722) and the AH (right, p = 0.856; left, p = 0.655; Table 1). The CMCTs detected from the ADM (right, p = 0.010; left, p = 0.000) and the AH (right, p = 0.000; left, p = 0.002) decreased significantly 1 year after surgery. The longer and shorter CMCTs from the ADM (longer, p = 0.000; shorter, p = 0.008) and the longer CMCT from the AH (longer, p =
The MEP latency, PCT, and CMCT values are shown in Tables 1 and 2. All parameters include data from more than 40 patients. The MEP, F-wave, and M-wave could not be recorded from the left ADM in one patient before or 1 year after surgery. The MEP could not be recorded in two other patients from both AHs before surgery. In one of these two patients, F- and M-waves were not detected from either AH before surgery. The MEP latencies 1 year after surgery were signifi-
TABLE 1: Summary of MEP latency, PCT, and CMCT values in the ADM and AH before and 1 year after cervical laminoplasty* MEP Latency ADM Parameter before surgery no. of patients min value max value mean value SD at FU no. of patients min value max value mean value SD p value
PCT AH
CMCT
ADM
AH
ADM
AH
Rt
Lt
Rt
Lt
Rt
Lt
Rt
Lt
Rt
Lt
Rt
Lt
42 19.5 40.3 26.0 4.5
41 19.3 35.9 26.0 4.3
40 36.3 67.1 44.9 6.1
40 37.1 59.3 44.5 5.2
42 12.0 18.7 14.6 1.5
41 12.10 17.6 14.5 1.4
41 21.8 32.0 25.6 2.3
41 21.5 31.7 25.7 2.5
42 5.2 21.6 11.4 3.9
41 4.6 20.3 11.5 3.7
40 13.6 38.5 19.3 4.8
40 13.0 30.5 18.8 3.9
42 34.8 56.4 43.3 4.9 0.001†
42 36.0 55.0 43.3 4.4 0.006†
42 11.0 18.9 14.3 1.4 0.231
41 12.1 19.4 14.6 1.6 0.722
42 21.9 32.4 25.6 2.2 0.856
42 20.8 31.2 25.6 2.4 0.655
42 5.0 19.2 10.3 3.5 0.010§
41 5.2 16.0 9.7 2.7 0.000‡
42 41 18.5 19.8 36.6 32.9 24.6 24.2 4.0 3.4 0.006† 0.000‡
42 42 11.6 12.5 29.4 23.9 17.7 17.7 3.7 3.4 0.000‡ 0.002†
* FU = follow-up. † p < 0.01, compared with before surgery. ‡ p < 0.001, compared with before surgery. § p < 0.05, compared with before surgery.
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J Neurosurg: Spine / Volume 21 / August 2014
Improvement in CMCT after cervical laminoplasty TABLE 2: Summary of CMCT values in and recovery ratios for right and left ADMs and AHs ADM Parameter CMCT before surgery no. of patients min value max value mean value SD at FU no. of patients min value max value mean value SD p value CMCT recovery ratio no. of patients min value max value mean value SD
Longer
AH
Shorter
Longer
Shorter
42 4.6 20.3 10.3 3.3
40 13.7 38.5 20.4 4.5
40 13.0 30.5 17.7 3.8
42 5.0 19.2 10.7 3.5 0.000*
41 5.2 15.4 9.1 2.6 0.008†
42 11.6 29.4 18.3 3.8 0.000*
42 11.8 23.9 17.1 3.2 0.078
42 0.61 1.52 0.86‡ 0.19
40 0.63 1.28 0.90 0.11
41 0.53 1.64 0.94 0.23
40 0.77 1.26 0.97 0.11
42 6.7 21.6 12.7 3.9
* p < 0.001, compared with before surgery. † p < 0.01, compared with before surgery. ‡ p < 0.05, compared with CMCT recovery ratio from the shorter CMCT in the AH.
0.000) before surgery also decreased significantly 1 year after surgery; the shorter CMCT from the AH did not significantly differ (shorter, p = 0.078; Table 2). The mean CMCT recovery ratio for both the ADM and the AH was 0.91 ± 0.18 (range 0.53–1.64). The mean CMCT recovery ratios from the longer and shorter CMCTs in the ADM were 0.86 ± 0.19 (range 0.61–1.52) and 0.90 ± 0.11 (range 0.63–1.28), and those from the longer and shorter CMCTs in the AH were 0.94 ± 0.23 (range 0.53–1.64) and 0.97 ± 0.11 (range 0.77–1.26), respectively. Among these CMCT recovery ratios, the one from the longer CMCT in the ADM shortened significantly, as compared with the one from the shorter CMCT in the AH (p < 0.05). The mean JOA score before surgery was 10.1 ± 3.0 (range 3.5–16.0). Improvements in the JOA score were attained in all patients after surgery. The score improved significantly to 12.9 ± 2.7 (range 7.0–17.0) at 1 year after surgery (p = 0.000). Thus, the mean recovery rate (RR) was 0.43 ± 0.27 (range 0.06–1.00). Patient age correlated significantly with JOA score at 1 year after surgery (r = -0.352, p = 0.022). In contrast, age did not correlate with the JOA score before surgery (r = -261, r = 0.095) or RR (r = -0.204, r = 0.169). The correlations among patient age, JOA score, RR, and CMCT values are shown in Table 3. The longer/shorter CMCT parameters in the ADM and AH before surgery J Neurosurg: Spine / Volume 21 / August 2014
or 1 year after correlated significantly with JOA score both before and 1 year after surgery. The longer CMCT values from the ADM at 1 year after surgery (r = -0.391, p = 0.010) and the CMCT recovery ratio from the longer CMCT in the ADM (r = -0.390, p = 0.011) correlated significantly with the RR. There were no significant correlations between age and any CMCT parameters.
Discussion
Our results show a significant decrease in the CMCT parameters in patients with CCM at 1 year after surgery. The CMCT parameters before or 1 year after surgery correlated significantly with the JOA score both before and 1 year after surgery. The CMCT recovery ratio from the longer CMCT in the ADM significantly correlated with the RR. Central motor conduction time is calculated by subtracting PCT from MEP latency. Thus, the physiology of prolonged CMCT is complex, and only a few reports have noted the mechanism of its occurrence in CCM. Kaneko and colleagues examined CMCT following TMS, as well as spinal cord evoked potentials (SCEPs) following transcranial electric stimulation (TES), in patients with CCM and normal subjects.10 Their results showed that CMCT was prolonged in such patients and that the patients exhibited significant attenuation in their SCEP amplitudes following TES but no significant delay in their SCEP latencies. The authors concluded that impaired temporal summation of multiple descending potentials following TMS produces delays in motor neuron firing that contribute to the prolongation of CMCT. Moreover, a significant correlation between CMCT prolongation and SCEP amplitude attenuation, and no significant correlation between CMCT prolongation and SCEP latency in patients with CCM have been reported.22,23 Thus, corticospinal block is thought to cause CMCT prolongation. Our results showed that functional recovery in the corticospinal tract following cervical laminoplasty in patients with CCM can be quantitatively assessed and that the corticospinal conduction block improvements due to the increase in the number of axons that propagate the evoked potentials were one of the causes of improved JOA scores. The CMCT values did not completely improve to the normal range, which has been reported previously,10,28 and the mean CMCT recovery rate and (JOA score) RR in our series were 0.91 and 0.43, respectively. The data should be important information on the pathophysiology of recovery following surgery. Further, CMCT for the symptomatic side has been shown to correlate significantly with the preoperative JOA score, as well as with the JOA score at 1 year after cervical laminoplasty in patients with CCM.33 In our study, CMCT parameters correlated significantly with the JOA score before and 1 year after surgery, and the CMCT ratio from the longer CMCT in the ADM correlated with the RR, supporting the conclusion that CMCT may be useful in predicting the outcome of surgical treatment, as previously described by Takahashi et al.33 Kawaguchi et al. documented a reduction in JOA scores in 20 patients in a minimum 10-year follow-up of 126 cervical myelopathy patients who underwent cervi213
K. Nakanishi et al. TABLE 3: Correlations among patient age, JOA score, RR, and CMCT values Before Surgery ADM Parameter
Longer
At FU AH
Shorter
no. of patients 42 42 age r 0.240 0.207 p 0.126 0.189 JOA score before surgery r −0.521 −0.532 p 0.000* 0.000* JOA score at FU r −0.400 −0.388 p 0.009‡ 0.011†
ADM
CMCT Recovery Ratio ADM AH
AH
Longer
Shorter
Longer
Shorter
Longer
Shorter
Longer
Shorter
Longer
Shorter
40
40
42
41
42
42
42
40
41
40
−0.094 0.564
0.066 0.684
0.252 0.107
0.284 0.072
−0.023 0.883
0.019 0.905
0.066 0.680
0.134 0.409
0.127 0.428
−0.052 0.750
−0.528 −0.589 0.000* 0.000*
−0.377 −0.338 0.014† 0.031†
−0.598 −0.509 0.000* 0.001‡
0.137 0.388
−0.194 0.231
0.288 0.068
0.212 0.189
−0.444 −0.511 0.004‡ 0.001‡
−0.553 −0.357 0.000* 0.022†
−0.512 −0.387 0.001‡ 0.011†
−0.255 0.103
−0.151 0.353
0.166 0.300
0.224 0.165
−0.391
−0.212
−0.208
−0.111
−0.390
−0.100
0.000
0.134
0.184
0.186
0.484
0.011†
0.539
0.998
0.410
RR r
−0.119
−0.090
−0.150
−0.203
p
0.452
0.569
0.355
0.208
0.010†
* p < 0.001. † p < 0.05. ‡ p < 0.01.
cal laminoplasty.12 They reported that the causes of deterioration were axial spread of ossification of the posterior longitudinal ligament, other spinal lesions, cerebral infarction, and peripheral neuropathy. Central motor conduction time measurements are also a useful tool for detecting functional deterioration of the motor pathway due to thoracic spinal cord compression24 or cerebral infarction,27,31 and the F-wave study can detect a peripheral neuropathy.14,16,26 Consequently, our data should provide important information when a reduced JOA score following surgery is observed and those electrophysiological screenings are implemented, because our study utilized a simple clinical model of cervical myelopathy. To obtain accurate and reliable MEP findings, the patients included in our study had simple spinal cord compressions without any other neural disorders and successfully underwent laminoplasty. Patient age at the time of surgery influences surgical outcome. In previous assessments of surgical outcome in elderly patients with CCM, the results of laminoplasty in elderly patients were worse than those in younger patients.20,29,37 The poor recovery in the elderly patients may be attributable to the age-related decrease of motor neurons and myelinated fibers in the spinal cord. On the other hand, good clinical results have been reported even in elderly patients with myelopathy.34 Moreover, studies have shown no significant differences in RR of the JOA score between elderly and nonelderly patients.11,32 Kawaguchi et al. noted that cervical laminoplasty improves quality of life and activities of daily living even in elderly patients with cervical spondylotic myelopathy.11 Machino et al. reported that the differences in the JOA score before and after surgery were similar among nonelderly (age < 65 214
years), “young-old” (age 65–74 years), and “old-old” (age ≥ 75 years) patient groups, although RR and JOA scores before and after surgery were low in the elderly patients.18 Thus, these authors concluded that elderly patients can have a reasonable recovery after cervical laminoplasty. Suzuki et al. noted that although no significant difference was observed in the RR of the JOA score among groups according to age, the time point at which the JOA score reached a plateau after surgery was significantly later in elderly than in nonelderly patients.32 Surgical outcome, especially in elderly patients with CCM, can be affected by many factors and is still controversial. In the present study, age did not correlate with pre- or postoperative CMCT values or with the CMCT recovery ratio. These results suggest equivalence of function of the compressed corticospinal tract, as well as improvements 1 year after surgery between elderly and nonelderly patients. There were several limitations to our study. Except for the longer CMCT from the ADM at follow-up and the CMCT recovery ratio from the longer CMCT in the ADM, the RR did not completely correlate with the CMCT before surgery, at 1 year after surgery, or the CMCT recovery ratio. Thus, other factors may have influenced the RR in our cases. Central motor conduction time reflects the central motor pathway, and the sensory disturbance was not objectively evaluated. Another limitation was the small number of cases; it was too small to validate the factor that may have influenced the RR. Although few reports provide an objective assessment of corticospinal tract function, Nakamura et al. demonstrated that preoperative diffusion tensor tractography may predict neurological recovery in patients with CCM after laminoplasty.21 As an assessment of sensory disturJ Neurosurg: Spine / Volume 21 / August 2014
Improvement in CMCT after cervical laminoplasty bance, the utility of somatosensory evoked magnetic field dipole measurements by magnetoencephalography has been described.4 The CMCT examination should be used with new methods to identify factors that impact surgical outcome. Moreover, it is unclear how CMCT parameters and the JOA score were affected when other neural disorders were complicated. For example, diabetic neuropathy is a common complication among individuals of an age at which they are susceptible to CCM. Patients with diabetic neuropathy present with numbness in their hands and feet, and the F-wave latency and PCT are prolonged in these patients.14,16,26 Therefore, complicating diabetic neuropathy may affect the JOA score, as well as the electrophysiological results. Further validation of CMCT measurements is required for cases with other complicating neural disorders. CMCT measurements should be developed as a more useful tool that can clarify the pathophysiology and quantitatively assess the functional variation of corticospinal tracts.
Conclusions
In summary, this study suggests that cervical laminoplasty improves corticospinal tract function, which may be one of the reasons for the JOA score improvements in patients with CCM at 1 year after surgery. The degree of CMCT improvement did not correlate with patient age in our series. Our results offer quantitative evidence on the pathophysiology of functional recovery in the corticospinal tract following cervical laminoplasty in patients with CCM. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Supported by the Grants-in-Aid for Scientific Research (Scientific Research C, Research Project Number: 24592198) from Japan Society for the Promotion of Science, Ministry of Health, Labour and Welfare. Author contributions to the study and manuscript preparation include the following. Conception and design: Nakanishi. Acquisition of data: Nakanishi, Kamei, Ohta, Fujioka, Hiramatsu, Ujigo. Analy sis and interpretation of data: Nakanishi. Drafting the article: Naka nishi. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Nakanishi. Statistical analysis: Nakanishi. Study supervision: Ochi. References 1. Chiba K, Ogawa Y, Ishii K, Takaishi H, Nakamura M, Maruiwa H, et al: Long-term results of expansive open-door laminoplasty for cervical myelopathy—average 14-year follow-up study. Spine (Phila Pa 1976) 31:2998–3005, 2006 2. Di Lazzaro V, Restuccia D, Colosimo C, Tonali P: The contribution of magnetic stimulation of the motor cortex to the diagnosis of cervical spondylotic myelopathy. Correlation of central motor conduction to distal and proximal upper limb muscles with clinical and MRI findings. Electroencephalogr Clin Neurophysiol 85:311–320, 1992 3. Fehlings MG, Skaf G: A review of the pathophysiology of cervical spondylotic myelopathy with insights for potential novel mechanisms drawn from traumatic spinal cord injury. Spine (Phila Pa 1976) 23:2730–2737, 1998
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Manuscripts submitted June 11, 2013. Accepted April 17, 2014. Please include this information when citing this paper: published online May 23, 2014; DOI: 10.3171/2014.4.SPINE13545. Address correspondence to: Kazuyoshi Nakanishi, M.D., Ph.D., Department of Orthopaedic Surgery, Programs for Applied Biomedicine, Division of Clinical Medical Science, Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minamiku, Hiroshima 734-8551, Japan. email: [email protected].
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