Intraoperative spinal cord monitoring is performed

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1 J Neurosurg Spine 14: , 2011 Factors predicting the feasibility of monitoring lower-limb muscle motor evoked potentials in patients undergoing excision of spinal cord tumors Clinical article Vedantam Rajshekhar, M.Ch., Parthiban Velayutham, Ph.D., Mathew Joseph, M.Ch., and K. Srinivasa Babu, Ph.D. Department of Neurological Sciences, Christian Medical College, Vellore, India Object. This prospective study on intraoperative muscle motor evoked potentials (MMEPs) from lower-limb muscles in patients undergoing surgery for spinal cord tumors was performed to: 1) determine preoperative clinical features that could predict successful recording of lower-limb MMEPs; 2) determine the muscle in the lower limb from which MMEPs could be most consistently obtained; 3) assess the need to monitor more than 1 muscle per limb; and 4) determine the effect of a successful baseline MMEP recording on early postoperative motor outcome. Methods. Of 115 consecutive patients undergoing surgery for spinal cord tumors, 110 were included in this study (44 intramedullary and 66 intradural extramedullary tumors). Muscle MEPs were generated using transcranial electrical stimulation under controlled anesthesia and were recorded from the tibialis anterior, quadriceps, soleus, and external anal sphincter muscles bilaterally. The effect of age ( 20 or > 20 years old), location of the tumor (intramedullary or extramedullary), segmental location of the tumor (cervical, thoracic, or lumbar), duration of symptoms ( 12 or > 12 months), preoperative functional grade (Nurick Grades 0 3 or 4 5), and muscle power (Medical Research Council Grades 0/5 3/5 or 4/5 5/5) on the success rate of obtaining MMEPs was studied using multiple regression analysis. The effect of the ability to monitor MMEPs on motor outcome at discharge from the hospital was also analyzed. Results. The overall success rate for obtaining baseline lower-limb MMEPs was 68.2% (75 of 110 patients). Eighty-nine percent of patients with Nurick Grades 0 3 had successful MMEP recordings. Muscle MEPs could not be obtained in any patient in whom muscle power was 2/5 or less, but were obtained from 91.4% of patients with muscle power of 4/5 or more. Analysis showed that only preoperative Nurick grade (p ) and muscle power (p < ) were significant predictors of the likelihood of obtaining MMEPs. Responses were most consistently obtained from the tibialis anterior muscle (68%), but in the other 32% MMEPs could not be recorded from the tibialis anterior but could be recorded from another muscle. The ability to monitor MMEPs was associated with better motor outcome at discharge from the hospital (p = 0.052). Conclusions. The likelihood of obtaining lower-limb MMEPs is significantly greater in patients with better functional grades and higher motor power. Muscle MEPs are most consistently obtained from the tibialis anterior muscle but other muscles should also be monitored to optimize the chances of obtaining MMEP responses from the lower limbs. (DOI: / SPINE10310) Key Words spinal cord tumor success rate motor evoked potential transcranial electrical stimulation diagnostic and operative techniques Intraoperative spinal cord monitoring is performed using either SSEPs or MEPs. Since it was recognized that changes in intraoperative SSEPs do not necessarily correlate with postoperative motor outcome, 9 MEP monitoring has gained ascendancy in recent years. Motor evoked potentials can be obtained either by epidural recording from the spinal cord during surgery (D wave Abbreviations used in this paper: MEP = motor evoked potential; MMEP = muscle MEP; MRC = Medical Research Council; SSEP = somatosensory evoked potential. and I wave) or from the muscles in the limbs (MMEPs). The D wave and I wave can be elicited by single-pulse stimulating techniques, and the D wave is unaffected by anesthesia. 5,10 Studies have suggested that in situations in which epidural recording can be performed, D waves are more reliable than MMEPs 1 and a 50% drop in the D wave can indicate postoperative deficit. 5,14 Muscle MEPs, however, would require a multipulse stimulation technique to overcome the effect of anesthesia. 6,15 Although D wave recordings are more robust and less influenced by anesthesia, they cannot provide information on the function 748 J Neurosurg: Spine / Volume 14 / June 2011

2 Intraoperative lower-limb motor evoked potentials of specific muscle groups and cannot be recorded below the T-12 level. We preferred to use MMEPs rather than D wave monitoring because more than 20% of our patients had lesions in the thoracolumbar region and eliciting the D wave below the T10 11 spinal cord level is difficult. 5 The success rate of D wave recording is also lower than MMEPs, which therefore should be the preferred method for intraoperative monitoring during spinal cord surgery if only 1 technique is used. Studies have shown that many factors can affect MMEPs such as the technique employed, 9 type of anesthesia, 9 and preoperative clinical status. One of the major impediments to the use of MEP monitoring during spinal cord surgery has been the relatively low success rate of recording these potentials from the lower limbs. There are only a few studies on the effect of preoperative factors such as age, 4,11 functional status of the patient, 4 duration of symptoms, and preoperative motor power on the feasibility of recording intraoperative MMEPs, and none of these is focused on the lower-limb MMEPs. Finally, we correlated the ability to record MMEPs with early postoperative motor outcome. We performed a prospective study of lower-limb MMEPs in patients undergoing surgery for spinal cord tumors to determine the influence of preoperative patient factors on the feasibility of MMEP monitoring. We also studied other aspects of MMEP monitoring such as which muscle in the lower limbs yielded MEPs most consistently, and assessed whether monitoring more than 1 muscle in the lower limbs would enhance the chances of obtaining MMEPs. Methods Patient Population One hundred fifteen consecutive patients undergoing surgery for spinal cord tumors between March 2004 and June 2007 were considered for this prospective study after approval by the institutional review board. Informed written consent was obtained, in their native language, from all patients who were willing to participate in the study. Patients with a history of seizures, head injury, or stroke, and those younger than 10 years of age (due to safety concerns) were excluded from the study. Five patients refused to participate in the study. Of the remaining 110 patients, 44 had intramedullary and 66 had intradural extramedullary tumors. Patient age ranged from 10 to 72 years (mean 36 ± 18 years), and 71 patients were male. J Neurosurg: Spine / Volume 14 / June 2011 Electrophysiology and Transcranial Electrical Stimulation Intraoperative MMEPs were recorded using Viking IV or Endeavor machines (Nicolet Biomedical, Inc.), linked to a D185 stimulator (Digitimer Ltd.) for transcranial electrical stimulation. Transcranial electrical stimulation was delivered by placing an anode (2-cm silver disc) at Cz' (1 cm behind the Cz position) and a cathode at Fpz (electroencephalography electrode system). A train of 5 pulses (each pulse 50-μsec pulse width duration) with a 2-msec time interval between them was termed a sweep. Five such sweeps at 0.7 Hz were delivered and responses were averaged. To establish baseline responses, stimulus intensity was started at 100 V and gradually increased in increments of 10 V. Stimulus intensity was increased until all muscles undergoing monitoring were recruited or until the surgeon warned of patient movement or perceptible paraspinal muscle movement noticeable on the monitor linked to the operating microscope. Stimulus strength was then reduced until no movement was observed. Muscle MEPs were recorded bilaterally from the tibialis anterior, soleus, quadriceps, and external anal sphincter muscles. Compound muscle action potentials were recorded from the belly of these muscles with a pair of uninsulated subcutaneous needle electrodes placed 5 cm apart. The time base was set at 100 msec and the filter band pass was Hz. Any amplitude of MMEP was considered a successful recording. Clinical Assessment Functional status of all patients was recorded using the Nurick grading system. Muscle power in the muscles undergoing monitoring was graded according to the MRC grading system. The motor power of the strongest muscle that was monitored (excluding the external anal sphincter) was used for analysis. Anesthesia Anesthesia was induced with thiopentone (mean dose 228 ± 21 mg, range mg), and maintained with isoflurane (end-tidal 0.8%) in 77 patients (propofol at 6 mg/ kg/hr added in 33 patients), supplemented by O 2 and air in a 1:2 ratio. Analgesia was provided by intravenous fentanyl bolus at a mean of 168 ± 12 μg (range μg). Neuromuscular Block Vecuronium (in 93 patients) or atracurium (in 17 patients) was used to facilitate tracheal intubation and ventilation, and further doses were given by an infusion titrated to induce 2 3 clearly visible twitches on stimulation of a peripheral nerve (posterior tibial nerve at ankle or median nerve at wrist). Vecuronium infusion was used in the range of ± mg/kg/hr and atracurium was used in the range of 0.15 ± 0.06 mg/kg/hr. Statistical Analysis Bivariate analysis was initially performed and then multivariate logistic regression analysis was performed using the enter method. Data were analyzed using SPSS statistical software version Results Factors Predicting Successful Recordings A successful baseline recording of MMEPs was obtained in 75 patients (68.2%). The effect of different factors on the feasibility of obtaining MMEPs is shown in Tables 1 and 2. The preoperative functional status as assessed by the Nurick grade and the motor power of the strongest muscle that was monitored showed significant and strong correlation with the likelihood of obtaining baseline MMEPs (p < 0.001). Eighty-nine percent of patients with Nurick Grades 0 3 had successful recordings, but only 7.1% of patients 749

3 V. Rajshekhar et al. TABLE 1: Influence of different variables on success rate of lower-limb MMEPs Variable Total No. of Patients (%) No. w/ Successful Recordings (%) Nurick grade (74.5) 73 (89) 4 or 5 28 (25.5) 2 (7.1) MRC grade (36.4) 11 (27.5) 4 or 5 70 (63.6) 64 (91.4) duration of symptoms 12 mos 77 (70.0) 57 (74.0) >12 mos 33 (30.0) 18 (54.5) tumor location intramedullary 44 (40.0) 32 (72.7) extramedullary 66 (60.0) 43 (65.2) segmental location cervical & cervicothoracic 45 (40.9) 29 (64.4) thoracic & lumbar 65 (59.1) 46 (70.8) age <20 yrs 13 (11.8) 11 (84.6) 20 yrs 97 (88.2) 64 (66.0) with Nurick grades of 4 or 5 had the same success. Muscle MEPs could not be obtained in any patient in whom muscle power was 2/5 or less, but were obtained from 91.4% of patients with muscle power of 4/5 or more (MMEPs were obtained in some patients with muscle power of 3/5). All the other parameters such as patient age, duration of symptoms, location of the tumor (intramedullary vs intradural extramedullary and cervical, thoracic, or lumbar) did not predict the likelihood of obtaining MMEPs. Because we excluded patients younger than 10 years of age, our results do not truly reflect the influence of age on the feasibility of obtaining MMEPs. However, our results show that in patients over the age of 10 years, there is no significant influence of age on the success of MMEP monitoring. Most Consistent Muscle for MMEPs As expected, the tibialis anterior was the muscle from which MMEPs were most consistently obtained (p = 0.01). Rates of successful recording of MMEPs were lower in the soleus, external anal sphincter, and quadriceps muscles, in that order. Number of Muscles With Successful MMEP Recording Muscle MEPs were obtained from all muscles monitored in only 59% of patients, while in 12% recordings were obtained from only 1 muscle (Table 3). Muscle MEPs were recorded from the tibialis anterior muscle in 68% of patients, while in the other 32% monitoring was based on MMEPs obtained from other muscles (Fig. 1). In 9 of the 18 patients in whom MMEPs were obtained from only 1 muscle, responses were obtained from the tibialis anterior muscle, while in the other 9 patients recordings were obtained from the soleus (5 patients) and the external anal sphincter (4 patients) muscles. Successful MMEP Recording and Early Postoperative Motor Outcome The effect of preoperative Nurick grade, tumor location, and the ability to monitor MMEPs on early postoperative motor outcome was analyzed using multiple regression analysis (Table 4). While the location of the tumor was significantly associated with the motor outcome, with early postoperative motor deterioration noted more frequently in patients with intramedullary tumors, the ability to monitor MMEPs also had a significant association (p = 0.052) with early postoperative motor outcome. Discussion Feasibility of Obtaining Lower-Limb MMEPs There is considerable debate regarding the feasibility and low success rate of obtaining MMEPs, especially in the lower-limb muscles, with sparse data on the factors predicting successful recordings. It is generally accepted that the possibility of obtaining MMEP recordings is higher in the upper limbs than in the lower limbs. Chen et al. 4 reported a success rate of 94.8% for recording upperlimb MMEPs, whereas they could only successfully record baseline lower-limb MMEPs in 66.6% of patients. Their study included patients who had both brain and spinal disorders with the majority of their patients undergoing brain surgery. We were able to successfully record responses in 68.2% of patients with exclusively spinal pathology. Influence of Age Chen et al. 4 reported a success rate of 55% for obtaining baseline lower-limb MMEPs in children younger than 7 years, whereas it was 70.2% in those aged 7 64 years, declining again to 55.6% in those older than 64 years. The TABLE 2: Univariate and multivariate analysis of the effect of variables on MMEP recording success rate Variable Univariate Multivariate OR (95% CI) p Value OR (95% CI) p Value Nurick grade ( ) < ( ) < MRC grade ( ) < ( ) < duration of symptoms 2.37 ( ) ( ) 0.58 tumor location 0.75 ( ) ( ) 0.85 segmental location 1.43 ( ) ( ) J Neurosurg: Spine / Volume 14 / June 2011

4 Intraoperative lower-limb motor evoked potentials TABLE 3: Proportion of muscles from which baseline MMEPs could be recorded* Variable Proportion w/ Responses (%) IDEM IM Total (%) no. of patients 53 (71) 22 (29) 75 (100) muscle recorded tibialis anterior 68/106 (64) 34/44 (77) 102/150 (68) soleus 54/106 (51) 26/44 (59) 80/150 (53) external anal sphincter 58/106 (55) 14/44 (32) 72/150 (48) quadriceps 41/106 (39) 10/44 (23) 51/150 (34) only 1 15/106 (14) 3/44 (7) 18/150 (12) all 55/106 (52) 17/44 (39) 89/150 (59) * IDEM = intradural extramedullary tumors; IM = intramedullary tumors. All MMEPs were recorded bilaterally (left and right sides). lower success rate in children is believed to be due to the immaturity of the pyramidal tract, and it is postulated that full maturity in this respect is reached between 8 and 11 years of age. In our study, we excluded patients younger than 10 years and therefore are unable to corroborate these findings. The success rate again decreases in the older age group due to effects of peripheral neuropathy or age-related disorders such as cervical spondylotic myelopathy or nerve fiber loss. Influence of Motor Power Almost all reports on MMEPs conclude that the preoperative motor power has a major influence on the feasibility of obtaining baseline MMEPs. Calancie et al. 2,3 excluded patients with a motor power of Grade 1/5 or lower. They did not report their success rates for individual muscle grades but noted that MMEPs are unlikely to be obtained from muscles with a power of 2/5 or less. Chen et al. 4 found that patients with preoperative motor weakness had lower MMEP recording success rates compared with those with no weakness. However, they did not further categorize the degree of motor weakness; they only commented that there was no direct correlation between the degree of motor weakness and the success rate in individual patients. Our study confirms that the degree of preoperative motor weakness as determined by MRC grading significantly influenced the ability to monitor MMEPs in individual patients. We could not obtain MMEPs in any patient with a muscle power of Grade 2/5 or less in the lower limbs. Influence of Functional Grade Sala et al. 14 reported on the effect of preoperative Mc- Cormick grade on the success rate of recording MMEPs. The success rate for 40 patients with McCormick Grades I and II was 100%, but was only 60% for the 10 patients with McCormick Grades III and IV. The authors grouped both upper- and lower-limb responses together, and did not mention the success rates for lower-limb MMEPs separately. We preferred to use the Nurick grading system because our main focus in this study was the MMEPs in the lower limbs, and Nurick grades are based on the function of the lower limbs. We found that the preoperative Nurick grade was a strong predictor of the ability to monitor lower-limb MMEPs. Monitoring of lower-limb MMEPs was only possible in 7.1% of patients with poor Nurick grades (4 and 5). Although the recording success rate in these patients is very low, we would still recommend that attempts at monitoring lower-limb MMEPs be made in patients with high Fig. 1. Muscle MEP recordings obtained in a patient with a T11 12 schwannoma. Muscle MEPs were obtained from all muscles except for the tibialis anterior bilaterally and the right soleus. This recording highlights the need to monitor muscles other than the tibialis anterior to optimize the recording of intraoperative baseline MMEPs in the lower limbs. J Neurosurg: Spine / Volume 14 / June

5 V. Rajshekhar et al. TABLE 4: Effect of different variables on early postoperative motor outcome* Variable No. of Patients No. w/ Postop Worsening (%) p Value (95% CI) preop Nurick grade ( ) (11) 4 or (10.7) location ( ) intramedullary (25) extramedullary 66 1 (1.5) successful MMEP recording ( ) yes 75 6 (8) no 35 6 (17.1) * Analyzed using multiple regression analysis. Nurick grades. A poor Nurick grade was an independent predictor of a low success rate in obtaining lower-limb MMEPs, even in the presence of good motor power (MRC Grades 4 and 5) in the lower limbs. Effect of Tumor Location Chen et al. 4 reported a higher success rate for recording lower-limb MMEPs when the lesion was located in the cranial cavity as opposed to lesions in the spine. There is no specific information on the location of the tumor in the spine and feasibility of MMEP monitoring. We did not find any influence of the location of the tumor (cervical, thoracic, or lumbar, as well as intramedullary or intradural extramedullary) on the feasibility of lowerlimb MMEP monitoring. Number of Muscles to Monitor Most authors have reported the use of 1 or 2 lowerlimb muscles for MMEP monitoring of lower limbs. The tibialis anterior muscle alone was monitored by Chen et al. 4 and Kothbauer et al., 7 while Sala et al. 13 used both the tibialis anterior and abductor hallucis muscles. Calancie et al. 3 reported the use of 8 12 muscles in the upper and lower limbs but did not specify the muscles in the lower limbs; from their illustrations it appears that they monitored the tibialis anterior and abductor hallucis muscles. Our findings support the use of the tibialis anterior muscle for monitoring the lower limbs because MMEPs were most consistently obtained from the tibialis anterior muscle. It is the optimal muscle to monitor pyramidal tract function because of its dominant corticospinal tract innervation, and in this respect it is similar to the abductor hallucis. 5 Our data show that using only the tibialis anterior muscle would have resulted in a lower success rate because MMEPs from that muscle were obtained in only 68% of those with successful MMEP monitoring. In the other 32% of patients, MMEPs were obtained from one of the other monitored muscles. Therefore, we recommend the use of 2 or more muscles for lower-limb MMEP monitoring. The importance of including the tibialis anterior among the lower-limb muscles chosen to monitor is that postoperative motor outcome can be predicted with 100% sensitivity and 81% specificity on the basis of intraoperative changes in tibialis anterior MMEPs. 8 Effect of Successful MMEP Monitoring on Postoperative Outcome It has been difficult to document the value of MMEP monitoring on postoperative outcome for a number of reasons. A randomized study is unlikely to be performed because surgeons who are convinced of its utility would consider it unethical to withhold such monitoring. Even if there are surgeons who are unconvinced of its utility and therefore willing to perform such a study, it is unlikely that they would get approval from the institutional review boards. Medicolegal concerns will also be a hurdle in the conduction of a randomized study to test the value of MMEP monitoring. Therefore, authors have resorted to other means to evaluate the effect of MMEP monitoring on postoperative outcome. One method would be to compare the postoperative outcomes in patients with spinal cord tumors in whom MMEPs could be monitored with those in whom it could not be monitored. Morota et al. 11 used such a strategy to show that the ability to monitor MEPs (using epidural electrodes to record the D wave) was correlated with a better postoperative outcome in adults but not in children. Because they did not study the effect of other prognostic variables in a multivariate analysis, it is unclear whether the feasibility of MEP monitoring was an independent predictor of postoperative outcome. Our results obtained in a multivariate analysis that included other prognostic variables demonstrate that the feasibility of MMEP monitoring is associated with better postoperative outcome. The possible explanations for this association could be 1) that the feasibility of MMEP monitoring is an indicator of better preservation of the motor tracts, even in patients with the same functional status, which allows them to better tolerate the operative trauma; and/or 2) MMEP monitoring prevented irreversible intraoperative trauma to the spinal cord and thus ensured a better postoperative outcome. Sala et al. 14 used a historical control model to study the value of MMEP monitoring on postoperative outcome. They compared the outcome of 100 patients with intramedullary tumors who underwent surgery with MMEP and D wave monitoring (50 patients) to those without such monitoring (50 patients). Patients in the latter group, who underwent surgery before MMEP monitoring was available, were matched for functional grade, location 752 J Neurosurg: Spine / Volume 14 / June 2011

6 Intraoperative lower-limb motor evoked potentials of tumor, and extent of resection. Only patients whose MMEPs or SSEPs could be monitored were included in the study, and those in whom baseline SSEPs or MMEPs could not be recorded were excluded from the study. These investigators found that the monitored group had better functional outcome 3 months after surgery compared with the control group, although the outcomes at discharge were similar in the 2 groups. Even at discharge from the hospital, the monitored group tended to have a better functional outcome. Because patients without baseline SSEPs and MMEPs were excluded from the study, it is unclear whether the presence of baseline MMEPs or the ability to react to changes in MMEPs during surgery was the real reason for the better postoperative outcome. Technical Modifications to Improve Success Rate Chen et al. 4 also suggested several modifications to the technique of transcranial electrical stimulation to improve the success rate of obtaining MMEPs. The simplest of these suggested modifications is to place the stimulation electrode at the Cz location. However, they reported that this modification to the stimulation technique did not result in a higher success rate for lower-limb MMEPs. Quiñones-Hinojosa et al. 12 suggested placement of the stimulation electrode at the C1 2 region rather than at the C3 4 region. Of all the suggested modifications, Chen et al. 4 found that switching the polarity of the stimulating electrodes yielded the best results. In 36.4% of their patients (124 of 341 cases) baseline MMEPs in the lower limbs could only be obtained by switching the polarity of the C3 4 stimulation without increasing the intensity of the stimulation. Increasing the intensity of the stimulation current, its duration, and the interval between the stimulations have all been reported as modifications to improve the yield of lower-limb MMEPs. Conclusions Successful MMEP monitoring is unlikely in patients with lower-limb motor power of 0/5 2/5, or those with a poor Nurick grade of 4 or 5. In these patients it might be worth pursuing other modalities of monitoring spinal cord function such as SSEPs if the location of the tumor is appropriate for such monitoring. Our findings could help in preoperatively assessing the feasibility of intraoperative monitoring of MMEPs in the lower limbs of a patient undergoing planned surgery of a spinal cord tumor. Disclosure This study was supported by a research grant from the Indian Council for Medical Research (No. 5/4-5/1/Neuro/2003-NCD-1). Author contributions to the study and manuscript preparation include the following. Conception and design: Babu, Rajshekhar. Acquisition of data: Babu, Velayutham. Analysis and interpretation of data: Rajshekhar. Drafting the article: Rajshekhar, Velayutham. Critically revising the article: Joseph. Reviewed final version of the manuscript and approved it for submission: all authors. Statistical analysis: Velayutham. Administrative/technical/material support: Babu. Study supervision: Babu, Joseph. Acknowledgments The authors are grateful to Dr. Steve Jones, Clinical Neurophysiologist, Queen Square, London, for helping in the development of protocols. The authors also thank Dr. L. Jayaseelan, Department J Neurosurg: Spine / Volume 14 / June 2011 of Biostatistics, for helping with the statistical analysis, and Mr. Benjamin Franklin for technical help in monitoring the patients. References 1. Bartley K, Woodforth IJ, Stephen JP, Burke D: Corticospinal volleys and compound muscle action potentials produced by repetitive transcranial stimulation during spinal surgery. 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Neurosurgery 58: , Taniguchi M, Cedzich C, Schramm J: Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery 32: , 1993 Manuscript submitted April 23, Accepted January 25, Please include this information when citing this paper: published online March 25, 2011; DOI: / SPINE Address correspondence to: Dr. K. Srinivasa Babu, Ph.D., De - partment of Neurological Sciences, Christian Medical College, Vellore , India. srinivas@cmcvellore.ac.in. 753