INTRODUCTION
Recently, intraoperative neurophysiological monitoring (IONM) has been actively implemented to prevent neural damage during spinal surgeries2,6,14,22). In particular, in high-risk procedures such as deformity correction surgery and spinal tumor surgery, the application of intraoperative motor evoked potentials (MEP) is considered essential28). Despite debates regarding its utility and cost-effectiveness, intraoperative MEP monitoring is routinely used, even in decompressive surgery for cervical compressive myelopathy (CCM)3,5).
Intraoperative MEP monitoring has focused on detecting decreased changes with high specificity for predicting postoperative neurological deficit in spine surgery20). During IONM, an increase of 10% in latencies or a decrease of more than 50% in amplitude in intraoperative MEP is considered as a warning sign of cord damage or additional cord compression7,11,15,17).
Recent studies have reported the potential of increased changes in intraoperative MEP after cord decompression in CCM as a predictor for postoperative neurological outcome19,24,25). However, a clear understanding of this is still lacking, and prospective studies are limited7).
The objective of this prospective study was to investigate the relationship between the immediate improvement in intraoperative MEP after cord decompression in patients with CCM and their functional outcomes, exploring the possibility of the intraoperative MEP being a prognostic indicator. In addition, the preoperative factors associated with the immediate improvement of MEP were also investigated.
MATERIALS AND METHODS
This prospective study was conducted on 54 patients who underwent surgery for CCM from April 2021 to January 2023. The inclusion criteria were patients aged 19 or older with clear cord compression and cord signal changes on preoperative magnetic resonance imaging (MRI), confirmed cervical myelopathy on preoperative neurophysiological tests, and the presence of one or more symptoms of myelopathy. Exclusion criteria included thoracic and upper lumbar spine disorders not involving the cervical spine, acute cervical spinal cord injury due to trauma rather than chronic degenerative diseases, myelopathy caused by extradural or intradural tumors or compressive lesions, other neurological disorders such as Parkinson's disease that may limit evaluation, and significant medical history that could impair the assessment of symptoms of cervical myelopathy, such as stroke or pediatric paralysis. This prospective study protocol was approved by the Institutional Review Board (IRB) of our hospital (IRB No. 2106-029-104), and all patients provided written informed consent.
Among the 54 patients, those whose MEP amplitude measured less than 30 µV before decompression were ultimately excluded from the study. This criterion was established because MEP values below 30 µV are considered unreliable due to significant variations in ratio values caused by minor changes in MEP26). These fluctuations can make insignificant absolute increases appear as meaningful advancements in the ratio results of MEP. Consequently, based on this criterion, 16 patients were excluded, leaving 38 patients in the final analysis. The mean age of the patients was 65.82 years, with 30 males and 8 females. The pathologies of CCM included herniated cervical disc in 15 cases, cervical spondylotic myelopathy (CSM) in 15 cases, and ossification of the posterior longitudinal ligament in 8 cases8).
The 38 patients were classified into three groups based on changes in MEP amplitude during surgery: the slightly decreased MEP group (where the amplitude decreased but by less than 50%), the slightly increased MEP group (where it increased but by less than 50%), and the significantly increased MEP group (where it increased by 50% or more). There were no patients with a significant decrease in MEP amplitude of 50% or more during surgery.
First, the preoperative characteristics and intraoperative MEP changes among the three groups were compared. The preoperative characteristics include age, sex, symptom duration, surgical level, surgical approach, Torg-Pavlov ratio, space available for the cord, cord compression ratio, signal intensity grade, preoperative modified Japanese Orthopaedic Association (mJOA) score based on patient’s medical records, preoperative computed tomography, and MRI. Second, functional outcomes on postoperative days (PODs) 7 and 28 were compared among the three groups. Finally, the correlation between the increase in MEP amplitude during surgery and the extent of improvement in functional outcomes was investigated.
1. MEP Monitoring Protocol and Measurement of Pre- and Post- Decompression MEP Amplitude
IONM was performed in all patients, including the combined monitoring of MEP, somatosensory evoked potentials (SSEP), and electromyography as a standard procedure. The transcranial MEP (TcMEP) monitoring protocol was as follows21): TcMEPs were elicited using transcranial electrode stimulation with the NIM-Eclipse monitoring system version 3.5.353 (Medtronic XOMED Inc., Memphis, TN, USA). Transcranial electrical stimulation was administered by placing an anode (2-cm silver disc) at the C3-4 position according to the 10 to 20 electrode system. A train of 6 pulses, each with a duration of 50 microseconds and an interval of 2 milliseconds, was delivered. Stimulus intensity was initially set at 200 V and gradually increased to 999 V to establish a baseline response. Muscle MEPs were recorded using needle electrodes in four extremities, including the abductor hallucis muscle. The time base was 100 milliseconds, and the filter band pass was 100 to 5,000 Hz.
The measurement of intraoperative pre-decompressive MEP amplitude was conducted at specific time points. These included: (1) between 30 min to one hr after anesthesia induction, when the effects of muscle relaxants had dissipated, and when train-of-four (TOF) stimulation showed four or more points; and (2) after muscle and soft tissue dissection before the initiation of discectomy or bone working. Measurements were taken twice at one-min intervals, and the average of these two measurements was considered the recorded value. Post-decompressive MEP amplitude measurements were taken immediately after the completion of the main procedure for cord decompression, such as discectomy or laminoplasty. This measurement was taken when TOF stimulation showed four or more points. Similar to the pre-decompressive measurements, two readings were taken at one-minute intervals, and the average value was recorded. When measuring MEP amplitude, the stimulus intensity remained the same before and after decompression. Only the more reliable MEP amplitude among those of both abductor hallucis muscles was used as the measurement value for analysis.
2. Anesthesia
General anesthesia was induced by total intravenous anesthesia with propofol (100-150 µg/kg/min) and remifentanil (1 µg/kg), avoiding bolus injections whenever possible. A muscle relaxant such as rocuronium was administered only once to facilitate intubation. Mean blood pressure was maintained above 90 mmHg.
3. Functional Outcome Assessment
The evaluation of the neurological status of patients was conducted using the mJOA score, which is commonly employed in cervical myelopathy10,12). Assessments were performed on the day before surgery, on POD 7, and during outpatient visits on POD 28. Two spine surgeons independently measured the mJOA scores consecutively and reached a consensus on the final score.
The degree of neurological recovery after surgery was assessed using the recovery rate (RR) of the mJOA score (%) and the absolute improvement (AI) of the mJOA score. The RR of the mJOA score was calculated using the Hirabayashi formula9,16,23,29): RR = ([Postoperative mJOA score - Preoperative mJOA score] / [18 - Preoperative mJOA score]) * 100 (%), AI = (Postoperative mJOA score) - (Preoperative mJOA score).
4. Statistical Analysis
Continuous variables were presented with mean and standard deviation or median and interquartile range, while categorical variables were presented as frequency and percentage. The Kruskal-Wallis test was performed to compare continuous variables between the groups, while Fisher's exact test was used for categorical variables. To compare the post-operative states at 7 and 28 days based on the pre-operative mJOA score, the Wilcoxon signed rank sum test was performed. The Jonckheere-Terpstra test was used for trend analysis of the mJOA scores at preoperative, postoperative 1 week, and postoperative 1-month intervals. All statistical analyses were performed using the R software (version 4.3.3; The R Foundation for Statistical Computing, Vienna, Austria). The significance level was set at 0.05.
RESULTS
The preoperative characteristics and intraoperative MEP changes in each patient group are presented in Table 1. Out of a total of 38 patients, 14 (36.8%) were in the slightly decreased MEP group, 12 (31.6%) in the slightly increased MEP group, and 12 (31.6%) in the significantly increased MEP group. There were no statistically significant differences among the subgroups in terms of age, sex, symptom duration, surgical level, surgical approach, type of disease, severity of cord compression, and cord signal grade. The mean preoperative mJOA scores were 14.14 ± 2.48, 12.75 ± 1.86, and 10.83 ± 4.32, respectively. Although it was not statistically significant, there was a tendency for the significantly increased MEP group to show a lower preoperative mJOA score (p=0.063).
The mean pre-decompressive MEP amplitudes were 514.36 ± 407.87, 394.17 ± 312.75, and 152.46 ± 179.37 µV, respectively. Notably, the significantly increased group exhibited a relatively low pre-decompressive MEP amplitude, with a statistically significant difference observed among the three groups (p=0.009). Post-decompressive MEP amplitudes were 475.86 ± 395.75, 460.00 ± 352.53, and 472.58 ± 303.69 µV, respectively, with no statistical difference found among the three groups.
In Table 2, the RR and AI of mJOA scores were documented. Overall, patients' mean mJOA scores improved from 12.66 ± 3.27 to 14.24 ± 2.77 at POD 7 and 14.66 ± 2.71 at POD 28, demonstrating statistically significant improvement. In the slightly decreased MEP group, the RR was 27.98 ± 32.29% at POD 7 and 11.61 ± 69.84% at POD 28, with significant improvement at POD 7 (p=0.010) but not at POD 28 (p=0.200). The AI was 0.79 ± 0.80 at POD 7, showing statistical significance, but not at POD 28 (p=0.010 and p=0.100, respectively). In the slightly increased MEP group, the RRs were 23.75 ± 28.36% and 28.47 ± 43.38% at POD 7 and POD 28, respectively, with significant improvement at POD 7 (p=0.040). The AI was 1.00 ± 1.21 at POD 7 and 1.08 ± 1.88 at POD 28, demonstrating statistical significance at POD 7 (p=0.030). In the significantly increased MEP group, the RR was 41.06 ± 32.01% at POD 7 and 59.78 ± 34.52% at POD 28, both showing statistically significant improvement (p=0.009 and p=0.006). The AI was 3.08 ± 2.07 at POD 7 and 4.33 ± 2.54 at POD 28, with statistical significance observed at both time points (p=0.009 and p=0.006).
The relationship between the increase in MEP amplitude after decompression and the improvement of functional neurological outcomes is presented in Table 3 and Fig. 1, 2. On POD 7, there was no statistically significant difference in RR among the three groups (p=0.376), but a statistically significant difference in AI was observed among the groups (p=0.010). Additionally, there was a statistically significant trend indicating that greater improvement in MEP amplitude was associated with an increase in AI (p=0.005). On POD 28, both RR and AI showed statistically significant differences among the three groups (p=0.044 and p=0.010). Furthermore, there was a statistically significant trend indicating that greater improvement in MEP amplitude was associated with greater improvements in both RR and AI (p=0.010, p<0.001).
DISCUSSION
Our prospective study investigated the relationship between intraoperative increases in MEP amplitude following decompressive surgery and the subsequent functional neurological outcomes in patients with CCM, as well as its related preoperative factors.
The preoperative characteristics among the three groups—those with slightly decreased, slightly increased, and significantly increased MEPs—were similar, with no statistically significant differences in age, sex, symptom duration, surgical level, surgical approach, type of disease, severity of cord compression, and cord signal grade. This homogeneity suggests that the observed differences in outcomes are likely attributable to the changes in MEPs rather than underlying patient or surgical factors. Interestingly, while the mean preoperative mJOA scores tended to be lower in the significantly increased MEP group, this trend did not reach statistical significance. In particular, baseline MEP amplitude was significantly different among the three groups. The significantly increased MEP group showed low baseline MEP amplitudes with an average of 152.46 µV. This could indicate a potential correlation between baseline MEP amplitudes and neurological function before surgery4,13). The post-decompressive MEP values for the three groups were 475.86, 460.00, and 472.58, respectively, showing no statistical difference. This may indicate that in cases where the baseline MEP is low, there is a higher likelihood of an amplitude increase of over 50%. In addition, the results imply that the magnitude of intraoperative MEP changes might be more predictive of functional recovery than absolute post-decompressive values.
Overall, patients exhibited significant improvements in mJOA scores at POD 7 and POD 28, indicating successful decompressive surgery. However, there were differences in RR and mJOA score improvement among the three groups. In the slightly decreased MEP group, significant improvements in the mJOA score were noted at POD 7 but not at POD 28, suggesting an initial recovery that plateaus over time. The slightly increased MEP group also showed significant improvements in mJOA scores at POD 7 but not at POD 28, highlighting a similar pattern to the slightly decreased MEP group. The significantly increased MEP group demonstrated consistent and significant improvements at both POD 7 and POD 28, indicating a robust and continuous recovery process. These results suggest a positive impact of increased intraoperative MEP on postoperative functional outcomes.
Regarding the relationship between MEP response and functional outcomes, the study suggests a potential association between intraoperative MEP amplitude increase and postoperative improvement in mJOA scores. Especially, it demonstrated a significant association with the RR at POD 28 and the AI of mJOA at POD 7 and 28. These findings suggest that changes in MEP amplitudes may be a reliable indicator for predicting post-operative neurological improvement. Notably, at POD 28, the relationship between intraoperative MEP change and RR and AI of mJOA score became more apparent. This underscores the importance of intraoperative MEP monitoring as an indicator of mid-term functional outcomes rather than immediate functional outcome.
There have been several studies on the relationship between MEP signal improvement during surgery for CCM and postoperative outcomes1,18,27).
Wang et al.27) were the first to suggest the correlation between intraoperative MEP signal improvement and postoperative neurological outcomes in CCM patients. Among 59 patients, they reported that 21 showed an average 140% improvement in MEP, correlating with a 59% improvement in mJOA score immediately and at six months post-surgery. However, this study was retrospective and did not provide baseline MEP amplitudes for the control group27).
Similarly, Park et al.18) reported MEP amplitude improvement in 11 out of 29 CCM patients, with those showing improvement having higher improvements in American Spinal Injury Association motor score and Korean version of Modified Barthel Index at one month post-surgery compared to those without MEP improvement, though no difference was seen at six months. This study was also retrospective with a relatively small sample size of 29 patients18).
Akbari et al.1) conducted the first prospective study on the relationship between intraoperative MEP increases and postoperative neurological outcomes in 28 CCM patients. They found increased MEP changes in 9 patients and reported a significant improvement in mJOA grade compared to those without changes 6 months after surgery. However, they did not demonstrate pre-decompressive MEP amplitudes for patients, and the sample size was relatively small1).
On the other hand, intraoperative SSEP monitoring during surgery may help predict positive neurological outcomes post-surgery. However, in the case of CSM, intraoperative SSEP monitoring does not reflect motor function and has several limitations, such as response time. Thus, there are currently no studies that use SSEP improvement alone to predict prognosis. Future studies could explore the combined application of SSEP with MEP.
Our study has also several limitations. First, it is not a controlled study with 3 groups; there are differences in pre-decompressive MEP amplitude among patient groups. However, our results suggest that a significant increase in MEP amplitude is more likely to occur in patients with a low baseline MEP amplitude, distinguishing our study from others. Second, the sample size among different groups is small, and only mid-term outcomes were investigated, not long-term outcomes. Despite these limitations, as the largest prospective study including the most patients, it holds significance. Future research should aim to validate these results in larger, multicenter cohorts and explore the underlying mechanisms driving the relationship between MEP changes and neurological recovery. Additionally, long-term follow-up beyond 1 year could provide a more comprehensive understanding of the sustained impacts of decompressive surgery on neurological function.
CONLUCSION
Our prospective study underscores the prognostic value of intraoperative increases in MEP amplitude following decompression for CCM in predicting postoperative neurological outcomes, particularly in patients with lower baseline MEP amplitudes. Greater improvements in MEP amplitudes correlate with more significant functional recovery. These findings highlight the importance of MEP monitoring as a valuable intraoperative tool for optimizing surgical strategies and predicting postoperative neurological recovery in patients with CCM.
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