Neurological complications after spinal surgery are uncommon yet unfortunate events associated with increased rates of morbidity, mortality, and increased health care costs. The rate of neurological complications was reported to be 1.0% in overall spinal surgery based on 108,419 cases from the Scoliosis Research Society database.1 However, in high-risk spinal surgeries such as for spinal deformity, spinal cord tumors, or ossification of the posterior longitudinal ligament (OPLL), neurological complications are some of the most frequent perioperative complications, with a rate of 13% to 31%.2–5
Intraoperative spinal neuromonitoring (IONM) can reduce neurological deterioration and provide increased accuracy in the detection of spinal cord injury.6,7 Transcranial electrical stimulation motor-evoked potentials (Tc[E]-MEPs) are widely used for intraoperative spinal cord monitoring and have become the criterion standard due to their high sensitivity and to the importance of motor function.8–10 Recently, the efficacy of multimodal IONM methods such as Tc(E)-MEPs coupled with somatosensory-evoked potential (SEP),11 cord-evoked potential after stimulation to the brain (D-wave),12–15 free running wave (continuous electromyography (EMG)),16,17 or triggered EMG (stimulated EMG)18,19 compared to single modal IONM was demonstrated. Although the alarm points for each type of IONM differ depending on the institution and surgeon, all monitoring alerts may indicate neural damage, including direct and indirect spinal injury. Thus, the purpose of IONM is to “prevent” the irreversible neural damage by facilitating proper intervention after the IONM alert rather than “predict” neurological complications. Understanding the timing of alarm points and adequate intervention is essential to “prevent” neurological complications for all members of the surgical team—surgeons, nurses, surgical technicians, anesthesiologists, and electrophysiologists.
The aim of this study is to analyze the incidence and timing of neurological deterioration and monitoring alerts, and to clarify which interventions are effective at preventing neural damage following IONM alerts in high-risk spinal surgeries.
MATERIALS AND METHODS
We performed a prospective multicenter analysis in 16 spinal centers using IONM with Tc(E)-MEPs for 2867 patients undergoing high-risk spinal surgery including for deformities, spinal cord tumors, and OPLL between April 2010 and March 2016. The study protocol was approved by the Institutional Review Board at all centers. Spinal cord tumor was divided into intramedullary or extramedullary, and OPLL was divided into cervical or thoracic OPLL. Spinal deformity was defined as the presence of at least one of the following indicators: degenerative, idiopathic, congenital, symptomatic, or neuromuscular scoliosis with spinal curvature greater than 20° in the coronal plane, C7 sagittal vertical axis greater than 50 mm, pelvic tilt greater than 25°, and/or thoracic kyphosis greater than 60°. There were 1009 spinal deformity cases (35.2%), 622 cervical OPLL cases (21.7%), 249 thoracic OPLL cases (8.7%), 771 extramedullary spinal cord tumor (EMSCT) (26.9%) cases, and 216 intramedullary spinal cord tumor (IMSCT) (7.5%) cases. The surgical techniques used for deformity cases were posterior corrective fusion with/without anterior release and fusion, those used for cervical OPLL were posterior laminectomy/laminoplasty or anterior cervical discectomy/corpectomy and fusion, and those used for thoracic OPLL were posterior decompression and fusion. Some tumor resection was performed with lesion-related nerve root sacrificing.
Tc(E)-MEPs were monitored under uniform monitoring conditions at 16 hospitals belonging to the Spinal Cord Monitoring Working Group of the Japanese Society for Spine Surgery and Related Research. The working group consisted of spinal surgeons who were IONM specialists and participated in round table meetings twice a year to discuss neurologically deteriorated and rescued cases. Exclusion criteria for IONM were the lack of informed consent or history of epilepsy.
Total intravenous anesthesia was administered during intraoperative spinal cord monitoring. Systolic blood pressure was controlled at >90 mmHg. The drugs administered were propofol (3–4 μg/mL), fentanyl (2 μg/kg), and vecuronium (0.12–0.16 mg/kg). Anesthesia was maintained using propofol (100–150 μg/kg/min with target-controlled infusion technique), remifentanil (1 μg/kg/h), and vecuronium (0–0.04 mg/kg/h). The transcranial stimulus conditions comprised 5 to 10 train stimuli, stimulus interval of 2 ms, stimulus of 100 to 200 A, stimulus duration of 500 μs, filter of 50 to 1000 Hz, recording time of 100 ms, and total of fewer than 20 stimuli. Corkscrew type stimulating electrodes (Nihon Kohden Inc., Tokyo, Japan) were bilaterally and symmetrically inserted 5 cm lateral and 2 cm anterior to Cz (international 10–20 system of electrode placement).
The Tc(E)-MEPs were recorded from the peripheral limbs via needle or surface electrodes and from the anus via plug-type electrodes. The evoked muscles, depending on the site of surgery, were selected from some or all of the deltoid, biceps, triceps, abductor pollicis brevis, quadriceps femoris, hamstrings, tibialis anterior, gastrocnemius, abductor hallucis, and sphincter muscles. We measured the amplitudes of the Tc(E)-MEPs using baseline-to-first negative peak voltages. The amplitudes before the invasive procedures were regarded as the control values. In this study, the authors set a 70% decrease in amplitude as the alarm threshold for Tc(E)-MEPs in all cases, based on a previously reported prospective multicenter study.19–22 In this study, a true positive (TP) case was defined as a Tc(E)-MEPs alert with a persistent decrease in the number of potentials at the end of the operation, followed by the observation of a new neurological motor deficit after the operation. A false positive (FP) case was defined as an alert with a persistent decrease in the number of potentials at the end of the operation and the absence of any new postoperative deficit. A true negative (TN) case was defined as the absence of any Tc(E)-MEPs alerts during surgery and no new postoperative deficits. A false negative (FN) case was defined as the absence of an alert in a patient with a new postoperative motor deficit. A Tc(E)-MEPs alert that normalized after corrective measures in a patient who emerged without new motor deficits was defined as a rescue case. For statistical analysis, rescue cases (patients who experienced a decrease in Tc[E]-MEPs amplitude during surgery, which recovered by the end of the surgery following intervention) were excluded from accuracy analysis because we could not be certain that the temporal decrease in amplitude indicated real motor deficits without a wake-up test. Variability in the Tc(E)-MEPs and the pre- and postoperative motor deficits were analyzed prospectively. Subjects that exhibited a reduction in Muscle Manual Testing with a Muscle Manual Testing value of ≥1 on the day after the surgery were classified as the group with postoperative paralysis. Neurological examination was performed immediately, at 1 day, and at 1 to 6 months after surgery.
Among the 2867 continuous patients, Tc(E)-MEPs yielded 126 TP cases, 2362 TN cases, 234 FP cases, and 9 FN cases in this study (Figure 1). One hundred thirty-six patients were classified as rescue cases because they had no neurological deficits, although their Tc(E)-MEPs amplitudes decreased during surgery and recovered after intentional intervention. These 136 cases were excluded from the accuracy analysis. The sensitivity of the Tc(E)-MEPs was 93.3%, the specificity was 91.0%, the positive predictive value was 35.0%, the negative predictive value was 99.6%, the FP rate was 8.6%, and the FN rate was 0.3%.
The 126 TP cases consisted of 22 patients with deformity, 7 patients with cervical OPLL, 30 patients with thoracic OPLL, 28 patients with EMSCT, and 39 patients with IMSCT. There was no relation between the duration of postoperative paresis and the amount of reduction of amplitude of the Tc(E)-MEPs. On the contrary, the 136 rescue cases consisted of 35 patients with deformity, 32 patients with cervical OPLL, 20 patients with thoracic OPLL, 31 patients with EMSCT, and 18 patients with IMSCT. Therefore, 52% (136/126 + 136) of patients with potential neural damage were rescued with Tc(E)-MEPs. The motor deficit (TP) rate according to the pathology was 2.2% for deformity surgery, 1.1% for cervical OPLL, 12.0% for thoracic OPLL, 3.6% for EMSCT, and 18.1% for IMSCT. Furthermore, the potential neurological deficit rate (TP + rescue) was 5.6% for deformity surgery, 6.3% for cervical OPLL, 20.1% for thoracic OPLL, 7.7% for EMSCT, and 26.4% for IMSCT (Figure 2). The nine FN cases consisted of seven IMSCT, one EMSCT, and one thoracic OPLL cases.
Mean operative time in FP cases was longer than that in TN cases (P < 0.001, 365 vs. 260 min, 817 cases in the first author's institution).
Timing of Transcranial Electrical Motor-Evoked Potentials Alert for Each Pathology
The timing of the alarm for each pathology is listed in Table 1. During deformity surgery, alerts occurred at de-rotation in 21 (36.8%) cases, pedicle screw insertion in seven (12.3%) cases, spinal shortening/three-column osteotomy (3CO) in six (10.5%) cases, and were unrelated to surgery in six (10.5%) cases. For cervical OPLL, alerts occurred at lamina opening for laminoplasty in 24 (61.5%) cases, corpectomy in 6 (15.4%) cases, and were unrelated to surgery in 7 (17.9%) cases. For thoracic OPLL, alerts occurred during decompression in 27 (54.0%) cases, dekyphosis in 5 (10.0%) cases, exposure in 4 (8.0%) cases, rodding in 4 (8.0%) cases, and were unrelated to surgery in 4 (8.0%) cases. For EMSCT and IMSCT, alerts occurred at tumor resection in 31 (52.5%) and 51 (89.5%) cases, root sacrifice in 6 (10.2%) and 2 (5.3%) cases, and were unrelated to surgery in 18 (30.5%) and 3 (5.3%) cases, respectively.
Interventions After Transcranial Electrical Motor-Evoked Potentials Alert and Outcomes
After the monitoring alert, adequate interventions were implemented by the surgeons, anesthesiologists, and electrophysiologists according to the individual situation (Table 2). Adjustment of blood pressure, heart rate, body temperature, and depth of anesthesia was performed by the anesthesiologist after an impedance check by the electrophysiologist. During deformity surgery, most of the interventions by the surgeon consisted of revised procedures such as correction release, pedicle screw replacement, or additional foraminotomy/laminectomy for iatrogenic foraminal stenosis. These interventions were highly effective, and 50% to 77.8% of cases with alerts were rescued (e.g., case 1, Figure 3A,B). However, interventions after 3CO with root sacrifice were ineffective in all three cases. In cervical OPLL, most of the alerts (61.5%) occurred during lamina opening for laminoplasty. Among these patients, 73.3% were rescued by suspension surgery, irrigation, or additional decompression/foraminotomy after the monitoring alarm. However, suspension surgery and waiting in corpectomy cases were mostly ineffective. In thoracic OPLL, most alerts (54.0%) occurred during posterior decompression for OPLL. For these patients, suspension surgery and steroid injection after the monitoring alarm were also ineffective. However, posture change, bilateral rodding, or additional dekyphosis after the monitoring alarm were effective (e.g., case 2, Figure 4A,B). In EMSCT and IMSCT, steroid injection after tumor resection and root sacrifice were ineffective (e.g., case 3, Figure 5); however, rescue was achieved after hematoma removal or additional duraplasty.
Rescue Cases After Transcranial Electrical Motor-Evoked Potentials Alarm
In this study, we determined the rescue rate, defined as the ratio of rescued patients with potential neurological deficits, as follows: the number of rescued patients/(the number of rescued patients + TP). The rescue rates for each pathology was 61.4% for deformity surgery, 82.1% for cervical OPLL, 40.0% for thoracic OPLL, 52.5% for EMSCT, and 31.5% for IMSCT (Figure 6). The rescue rates for deformity surgery and cervical OPLL were relatively high, whereas those for thoracic OPLL and IMSCT were less than 50%.
Among various types of spinal surgery, deformity correction, intramedullary tumor resection, and OPLL decompression have high neurological deficit rates due to long operative times, complicated procedures, and pathologically critical situations.2–5 Tc(E)-MEPs during these high-risk spinal surgeries are indispensable for predicting neurological deterioration and have been proven to have high sensitivity and specificity.6,7 However, there were few reports concerning effective interventions according to the pathology, timing of Tc(E)-MEPs alerts, and interventions to “prevent” irreversible neural damage. Normally, in the event of Tc(E)-MEPs alerts, routine interventions are performed by anesthesiologists and surgeons. The anesthesiologist controls the patient's blood pressure and heart rate while the surgeon attempts to protect the spinal cord through suspension of the surgery or administration of steroids/antihydropic agents. In the present study, we found that for each pathology, the alarm, which is an indication of neurological injury, was more likely to occur in specific situations according to the disease and surgical procedure. Furthermore, proper intervention depending on the pathology and situation can rescue neural damage and prevent neurological complications. In deformity surgery, the alert occurred during deformity correction, especially during derotation, compression/distraction, or translation. Releasing the correction was effective in preventing neurological deterioration, similar to what was described in a previous report.24 Furthermore, foraminotomy or pediclectomy is recommended in cases of root compression or tethering after the derotation maneuver. These interventions increased the rescue rate to more than 60%. On the contrary, multiple root sacrifice (three Caries spine cases in this series) and spinal shortening in 3CO had a high rate of both IONM alerts and neurological deficit.24 Therefore, surgeons should refrain from multiple root sacrifice or adjust the spinal shortening length before implementing Tc(E)-MEPs alerts. In cervical OPLL, most alarms occurred during lamina opening for laminoplasty and were rescued by additional laminectomy or foraminotomy, although corpectomy for cervical OPLL is a high risk factor for neurological deficit. In thoracic OPLL, the total rescue rate remained at only 40%. In addition, decompression for the stricture of OPLL was particularly risky and ineffective. In this situation, suspension of the surgery and administration of steroids were ineffective, and the rescue rate was merely 29.6%. The thoracic spinal cord has a low blood supply from the radiculomedullary artery and is located in an ischemic area. In severe thoracic OPLL cases, thoracic spinal cord ischemia and ischemia-reperfusion injury upon decompression may aggravate irreversible cord damage. Thus, interventions after the monitoring alarm may not be meaningful for protecting the spinal cord. Therefore, interventions (e.g., steroid or prostaglandin E1 injection, stable blood pressure) before a monitoring alert may be essential to avoid aggravated cord damage from spinal cord edema or ischemia. Alerts also occurred at posture change, dekyphosis, and rodding as well as exposure and pedicle screw (PS) insertion. These maneuvers may change the spinal alignment before and during surgery.25 Even in the thoracic spine, there is limited range of motion in the sagittal plane.27 The sagittal alignment of patients with thoracic OPLL may also change at posture change or during surgical maneuvers. In these situations, adequate interventions were effective with realignment or posterior shifting of the spinal cord. In EMSCT, the majority of the Tc(E)-MEPs alert cases (52.5%) were rescued and motor paresis was temporary. On the contrary, IMSCT cases were not rescued using most of the interventions, and the rescue rate was only 31.5%. In IMSCT, the spinal cord is already aggravated by the tumor, and incisions in the spinal cord have a higher risk of causing neurological deficits. By peeling off the tumor from the spinal cord, the small blood vessels entering the spinal cord and tumors are blocked from the segmental artery and the anastomotic branch to reduce the blood flow. The efficacy of Tc(E)-MEPs for IMSCT is controversial.26 Most studies indicated the high sensitivity of muscle MEPs for detecting postoperative motor deficits of the corticospinal tract.27–29 However, Tc(E)-MEPs cannot detect segmental spinal cord injury when the muscles recorded are different from the innervated muscles arising from the spinal anterior horn cell exposed to the risk of injury due to the localization of the spinal cord tumor and the removal operation. Raynor et al23 reported 45 (0.36%) FNs in 12,375 patients without spinal cord tumors who underwent various spinal surgeries and multimodality IONM, and no FNs were observed with Tc(E)-MEPs monitoring. The authors noted that 82.2% (37/45) of the FN results involved nerve root monitoring other than Tc(E)-MEPs. In this study, we had seven FN cases for IMSCT. Most of our FN cases were suspected segmental spinal cord injury, not spinal tract injury, because motor deficits were observed in a limited number of muscles and were mostly transient and all paralysis recovered within 3 months after surgery. Macdonald et al7 described a similar situation of two FN IMSCT cases resulting from suspected segmental spinal cord injury. On the contrary, we had only one FN involving nerve root injury. We used a multichannel monitoring device with a minimum of 8 and a maximum of 32 channels in all 16 hospitals that participated in this prospective study. As a result, we could detect most root injuries, which in turn led to few FN cases.
The most important finding in the present study is that knowing the timing of the alarm is useful to distinguish TN and TP from FP for Tc(E)-MEPs. An alarm immediately after a specific surgical procedure strongly indicates TP for deformity surgery or spinal cord tumor cases, although an alarm unrelated to the surgical procedure (e.g., posture change, exposure) could be TP in OPLL cases. Most of alarm arise associated with surgical maneuver mainly correction or instrumentation. However, some spinal surgeons still use the classic wake-up test to make sure whether the alarm is TP or FP. The indication for wake-up test may be limited in the cases of unrecovered MEP after intervention, such as release or remove implants against preceded radical surgical maneuver. Another indication for wake-up test may be unstable control MEP or uncertain FP cases. The causes of FP are controversial; however, most of FP may appear gradually with the progress of surgery, seen as anesthetic fade7 including high propofol dose, low blood pressure, low body temperature, or compression of inguinal artery because of prone position. Therefore, it is important to have a method to detect FP from various IONM alarms.
Moreover, we found that the individual timing is related to the surgical procedure for different pathologies. This information is valuable as it enables the spinal surgeon to act immediately to mitigate potential neural damage. It is noteworthy that our study included 136 cases in which the Tc(E)-MEPs recovered after adequate intervention for spinal cord injury without postoperative motor deterioration. These rescue cases demonstrate the advantages of IONM for preventing neurological complications for the surgical team and for patients.
The current study has several limitations. First, the alarm threshold was set as 70% amplitude reduction in this prospective study. This led to a relatively large number of FP and nine FN cases, the former due to the high sensitivity of Tc(E)-MEPs. Furthermore, FPs may have occurred due to a long operative time and to large amounts of propofol/opioid usage because our series was limited to high-risk pathologies, which required complicated surgical procedures and long operative times. The FN cases appeared to be due to selective spinal cord injury of resection IMSCT (as mentioned above, seven of nine FN cases were IMSCT). Selective spinal cord injury may be more difficult to detect compared to whole spinal cord injury, and there are differences in alarm thresholds between segmental spinal cord injury and spinal tract injury.30 Adjustment of the alarm criteria according to the disease or pathology (e.g., IMSCT/thoracic OPLL may require <70% amplitude) may be a viable solution. Second, this study did not include operative details including severity of the disease, spinal level, operative time, and estimated blood loss. Tc(E)-MEPs may be influenced by the anesthetic time and blood loss or pressure, and the anesthetic fade is particularly important.11 The operative times for deformity, thoracic OPLL and IMSCT were longer than those for cervical OPLL and EMSCT. Therefore, FP with a long procedure might confuse the surgeon, preventing timely intervention. Finally, we did not investigate the results of other monitoring modalities including SEP and D-wave. D-wave registration was the most useful intraoperative tool, especially when MEP and SEP responses were absent or poorly recordable. We agree that multimodal intraoperative monitoring should be encouraged during high risk spinal surgery. In this study, we had to limit the Tc(E)-MEPs analysis to unify indications and the methodology for monitoring the prospective multicenter study. Further investigation into multimodal monitoring is necessary to determine methods for preventing neurological complications.
Our prospective multicenter study results revealed the procedure-specific nature of IONM alarms in high-risk spinal surgery, and indicated that 52% of the patients were rescued from possible neural damage with Tc(E)-MEPs. Although the rescue ratios for thoracic OPLL and IMSCT were relatively low, appropriate intervention immediately after the IONM alert may prevent neurological deterioration even in high-risk spinal pathologies.Key PointsThe alerts revealed potential neural damage in 9.5% of patients and intervention after the alert led to the prevention of damage in 52% of patients, defined as the recovery of Tc-MEP amplitude.The timing of the Tc-MEP alerts varied according to the procedure and pathology.Adequate intervention immediately after an IONM alert can prevent neural damage even in high risk spinal surgeries.
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Keywords:Copyright © 2018 Wolters Kluwer Health, Inc. All rights reserved.
complication; intraoperative neuromonitoring; neurological deficit; ossification of posterior longitudinal ligament; spinal cord tumor; spinal deformity