Moderate Hypothermia for Intradural Spinal Tumor Resection: A Cohort Comparison and Feasibility Study

Abstract

To evaluate the safety and feasibility of modest hypothermia as a potential strategy for intraoperative neuroprotection during the removal of intradural spinal tumors. A retrospective review was performed for two groups of patients of a single surgeon who underwent intradural extrameduallary and intramedullary spinal tumor resection of tumors located between cervical level 1 and lumbar 2 over a 10-year period between 2001 and 2010. One cohort received intraoperative moderate hypothermia (33°C) via intravascular catheter cooling during tumor surgery and the second cohort, a historical control group of the same surgeon, underwent surgery at normothermia (≥36°C). The main outcome measured was safety as determined by surgical, medical, and neurological complications. The hypothermia (n=38) and nonhypothermia (n=34) groups were homogenous for patient demographics and baseline comorbidities. There were no differences between the groups regarding tumor level (p=0.51), tumor pathology, or intramedullary versus intradural extramedullary location (p=0.11). The hypothermia group had a lower mean body temperature (33.7°C±0.72 vs. 36.6°C±0.7, p≤0.001) longer postoperative hospital stays (10.8±14.0 vs. 7.3±4.72, p<0.001), but there were no significant differences in operative and perioperative variables such as, total anesthetic time (8.2±2.4 vs. 7.8±2.7 hours, p=0.45), total surgical time (5.9±2.1 vs. 5.7±2.5 hours, p=0.58), or estimated blood loss (483±420 vs. 420±314 mL, p=0.65). There were no statistically significant differences between the two groups with respect to the rate of surgical (3 vs. 2, p=1.0), medical (4 vs. 3, p=1.0), neurological (3 vs. 4, p=0.7), or overall complications (10 vs. 9, p=1.0). In this study, moderate hypothermia via intravascular cooling catheters was successfully performed during 38 intradural spinal tumor surgeries. Compared to the historical control group, the hypothermia patients had longer hospital stays, but did not have higher complication rates. Intraoperative moderate hypothermia during spinal tumor resection is feasible and appeared safe in this limited cohort; however, further studies with larger cohorts will be needed to determine whether peri-operative hypothermia is an effective neuroprotectant strategy in spinal tumor surgery.

Introduction

Modern technological advances have transformed the diagnosis and treatment of intradural spinal tumors. Since the first argument for the feasibility of intramedullary spinal cord tumor resection by Elsberg and Beer in 1911 (Elsberg et al., 1911), technological developments in preoperative imaging, anesthetic techniques, operative magnification, hemostasis, ultrasonic tissue disruption, and electrophysiological monitoring have led to improved safety and better outcomes in spinal tumor surgery (Brotchi et al., 1991; Sala et al., 2006; Sala et al., 2007). Thus, the historical method of treating these lesions through biopsy, duraplasty, and palliative radiation has been supplanted by more aggressive attempts at maximal tumor resection (Wood et al., 1954; Xu et al., 1996; Sandalcioglu et al., 2005; Aghakhani et al., 2008).

Hypothermia has been investigated as a neuroprotectant in both animal models and in humans for decades. In animal models, hypothermia has been found to slow propagation of neural injury and cell death in the viable but damaged tissue by decreasing the metabolic requirements of injured tissue and limiting secondary cell injury (Chatzipanteli et al., 2000; Inamasu et al., 2003). Randomized human clinical studies using hypothermia for various types of neurological insults have been conducted, and human trials in spinal cord injury (SCI) are ongoing (ClinicalTrials.gov Identifier: NCT01739010) (Polderman, 2008; Levi et al., 2009). The surgical removal of intradural spinal tumors with spinal cord compression and intramedullary spinal cord tumors carries significant risk of neural injury and postoperative neurological deficit (Roux et al., 1996; el-Mahdy et al., 1999; Sandalcioglu et al., 2005). Yet, no previous studies have investigated moderate hypothermia as a neuroprotection strategy during spinal tumor resection.

In 2005, based on the potential advantages and the previously established safety profile of induced modest hypothermia, a protocol was developed and instituted by the senior author to cool spinal tumor patients to 33°C during intradural or intramedullary tumor resections. From 2005 to 2010, 38 patients meeting study inclusion criteria underwent intraspinal tumor resection with moderate hypothermia protocol. This unique group of spinal tumor patients was analyzed to gauge moderate hypothermia's impact on perioperative complications. It should be noted that due to the retrospective nature of the study and the small heterogeneous population reviewed with regard to tumor level, location, and pathology, a generalizable conclusion regarding efficacy of hypothermia in blunting neurological injury during spinal tumor resection cannot be reliably made from this data; however, it does provide feasibility and baseline safety information. To our knowledge, this represents the first investigation of moderate hypothermia during spinal tumor surgery.

Methods

Institutional Review Board approval was obtained (IRB approval number 20070850) and retrospective data were collected consecutively between years 2001–2010 from patient records in the University of Miami Miller School of Medicine Department of Neurosurgery database. Inclusion criteria for the study were patients of the author B.A.G. who underwent elective intradural and intramedullary spinal cord tumor resections between 2001–2010. Exclusion criteria included any tumor centered below L2 (no spinal cord involvement) and intradural -extramedullary tumors without radiographic evidence of spinal cord compression. Patients were separated into two cohorts: those who received intraoperative moderate hypothermia treatment (2005–2010) and those who did not (2001–2005). Additionally, these cohorts were subdivided into intradural extramedullary and intramedullary lesions. Intravascular moderate hypothermia was only performed in patients deemed to be at risk of neurological injury during surgery; for example, patients with intramedullary spinal cord tumors and intradural extramedullary tumors with radiographic evidence of spinal cord compression or redo surgery. All patients meeting study eligibility criteria undergoing surgery during the study period are included in the analysis. All surgeries were performed with intraoperative neurophysiologic monitoring including, somatosensory evoked potentials (SSEPs) and motor evoked potentials (MEPs).

The protocol used for performing moderate hypothermia during spinal cord surgery in this series is as follows. Hypothermia patients were consented for intraoperative intravascular hypothermia. All patients received uniform prophylactic antibiotics and steroids. After tracheal intubation and during the anesthesiologists' placement of an arterial line and intravenous lines, a transfemoral venous catheter containing the heat exchange thermocouple was placed in the right femoral vein by the neurosurgical team. During patient positioning and surgical exposure, the Alsius® Coolguard system (Irvine, CA) cooled the patient to a core body temperature of 33°C over a mean of 30 minutes and this temperature was strictly maintained throughout the case. The time taken to place the femoral catheter is included in the total anesthesia time (AT) but not in the surgical time (ST). The Coolguard system lowers and maintains body temperature to within 0.2°C of 33°C by pumping internally cooled saline through balloons in a transfemoral catheter, thereby chilling the traversing venous blood. After the procedure, patients were extubated and monitored in a specialized Neurological Intensive Care Unit. The Coolguard system was programmed to slowly rewarm the patients from 33°C to 37.0°C at a rate of 1.0°C per 8 hours. Patients were monitored in the ICU throughout the 32 hours rewarming process. The After reaching 37.0°C, the coolguard catheter was removed and the patient transitioned to floor care. All patients in the hypothermia group received low molecular weight heparin (Dalteparin 5000 U daily) beginning the morning after surgery. Shivering was managed with superficial blankets and Meperidine injections as needed. Due to the immediate postoperative rewarming protocol, patient shivering was not common beyond the first 4–6 hours after surgery.

Demographic variables collected for each cohort included age, sex, preoperative age-Adjusted Charlson Comorbidity Index (ACCI) score, tumor pathology, and tumor level. Patients' ACCI scores were calculated from documented past medical histories and divided into three groups ≤2, 3–5, and ≥6. Outcome variables collected and analyzed included ST, AT, estimated blood loss (EBL), patient temperature at end of anesthesia, length of hospital stay (LOHS), use of postoperative cerebrospinal fluid (CSF) diversion, and complications.

Complications were divided into three categories: surgical, medical, and neurological. Medical and surgical complications are defined as occurring from surgery start to discharge from neurosurgerical care, but delayed surgical complications (such as CSF leak or wound infection) were also included. A neurological deficit was considered a complication if a negative deviation from preoperative physical examination was present at the 4–6 week follow-up clinic visit. If not late follow-up data were available, neurological deficit was considered a complication if it was present at discharge. In addition, the patient's degree of neurological deficit was pre- and postoperatively assessed with the American Spinal Injury Association impairment scale and functional deficit with the modified McCormick grading scale: I=normal ambulation; II=mild motor sensory deficit, independent without external aid; III=independent with external aid; IV=care required; and V=wheelchair required (McCormick and Stein, 1990).

All data were analyzed using GraphPad Prism. Continuous variables were compared between each cohort using the student's t-test. Categorical variables were compared using Fisher's exact test (one variable) or Chi-squared analysis (multiple variables). Alpha value of 0.05 or less was considered statistically significant.

Results

The patient demographics were similar between the 38 hypothermia and 34 nonhypothermia patients. Average age was 59±15 years (mean±SD) for the hypothermia cohort and 55±16 years for the nonhypothermia cohort. There was no significant difference between the two cohorts in regards to mean age, sex, and preoperative ACCI (Table 1).

Table 1.

Characteristics and Outcomes

Patient demographics	Hypothermia	No hypothermia	p-Value
Patients (n)	38	34
Age (mean±SD, years)	59±15	55±16	0.30
Sex
Male	39% (15)	35% (12)
Female	61% (23)	65% (22)
Preop ACCI score (n)			0.21
≤2	47.4% (18)	52.9% (18)
3–5	50.0% (19)	35.3% (12)
≥6	2.6% (1)	11.8% (4)
Tumor level			0.51
Cervical	35%	39%
Thoracic	54%	44%
Lumbar	11%	17%
Tumor pathology^a
Meningioma	33.3% (13)	32.4% (11)	1.0
Ependymoma	23.1% (9)	8.8% (3)	0.12
Schwannoma	18.0% (7)	29.4% (10)	0.41
Cavernous angioma	5.1% (2)	8.8% (3)	0.66
Astrocytoma	5.1% (2)	0%	0.50
Neurofibroma	5.1% (2)	8.8% (3)	0.66
Metastatic	2.6% (1)	0%	1.0
Other	7.7% (3)	11.8% (4)	0.70
Tumor location			0.11
Intradural extramedullary	63.3% (24)	82.4% (28)
Intramedullary	36.8% (14)	17.6% (6)
CSF diversion			<0.0001
Yes	100% (38)	52.9% (18)
No	0%	47.1% (16)

Procedure	Hypothermia (mean±SD)	No hypothermia (mean±SD)	p-Value
ST (hours)	5.9±2.1	5.7±2.5	0.58
AT (hours)	8.2±2.4	7.8±2.7	0.45
LOHS (days)	10.8±14.0	7.3±4.7	0.002 ^b
EBL (cc)	483±420	420±314	0.65
Patient temp. at end of anesthesia (°C)	33.7±0.7	36.6±0.7	<0.001

	Hypothermia ^c		No hypothermia ^d
Complications	Intramedullary (n=14)	Extramedullary (n=24)	Intramedullary (n=6)	Extramedullary (n=28)	p-Value
Surgical	2	1	0	2	1.0
Medical	2	2	0	3	1.0
Neurological	2	1	1	3	0.700
Total complications	6	4	1	8	1.0

Late neurological outcomes	Hypothermia	No hypothermia	p-Value
Follow-up time (mean±SD)	10.8±11.3 months	14.9±19.2 months	0.59
McCormick grade			0.65
Declined	5.7%	11.1%
Improved	45.7%	44.4%

Bold indicates that a value reached statistical significance.

One patient from the hypothermia cohort had a neurofibroma and schwannoma.

Statistically significant difference, α≤0.05 level of significance.

Three hypothermia patients had multiple complications.

Two nonhypothermia patients had multiple complications.

ACCI, Adjusted Charlson Comorbidity Index; AT, anesthetic time; CSF, cerebrospinal fluid; EBL, estimated blood loss; LOHS, length of hospital stay; ST, surgical time.

The two cohorts are balanced with respect to tumor level within the spinal axis. Although there was a higher percentage of intramedullary tumors in the hypothermia group this difference did not reach statistical significance (Table 1).

The hypothermia group had a lower mean body temperature, but there was no significant difference between the two cohorts with respect to total anesthetic, ST, or EBL (Table 1). However, the mean LOHS was significantly longer in the hypothermia cohort 10.8 days compared with the nonhypothermia cohort 7.3 days (p=0.002). Postoperative CSF diversion was employed as a preventative measure against CSF leak significantly more often in the hypothermia cohort compared with the nonhypothermia group (p<000.1) (Table 1). Combining the two cohorts, the patients receiving postoperative CSF diversion treatment had a mean LOHS of 2.6 days longer than those without.

There was no statistically significant difference in the frequency of surgical complications (3 vs. 2, p=1.0), medical complications (4 vs. 3, p=1.0), neurological complications (3 vs. 4, p=0.7), or total complications between the two cohorts (10 vs. 9, p=1.0). A descriptive comparison of the seven patients who experienced a persistent postoperative neurological change is provided in Table 2. Of note, SSEPs and MEPs were monitored in all cases. The intraoperative neuromonitoring records of patients in both cohorts were examined for any hypothermia-related changes. When body temperature reached 34°C, SSEP latency was observed to increase and the amplitude decrease by 2–3 milliseconds, but there was no change in MEPs signal transmission. The change in SSEP latency and amplitude was not clinically significant in any of the hypothermia cases.

Table 2.

Comparison of Neurological Complications

	Age (years)	Tumor level	Pathology	ST ^a (h)	AT ^a (h)	Complication description
Hypothermia cohort
1	47	C1–4	Oligodendroglioma	7.23	9.83	Mild hemiparesis (LUE 4−/5 and LLE 5−/5)
2	40	T1–7	Subependymoma	5.40	7.35	Left leg weakness and decreased proprioception (LLE 4/5)
3	77	T8–11	Meningioma	5.37	7.47	Incomplete paraplegia after third recurrent tumor removal (4−/5 preop to 2/5 postop strength)
Nonhypothermia cohort
1	43	C1–C2	Meningioma	8.55	10.5	Unilateral arm weakness (LUE 4+/5)
2	19	C1–C3	Meningioma	5.95	8.10	Unilateral arm weakness (5−/5)
3	62	C7–T1	Schwannoma	4.60	6.33	C7–8 distribution numbness
4	80	T12–L2	Hemangioblastoma	4.25	6.12	Leg weakness after recurrent tumor removal (4+/5 preop to 3/5 bilaterally)

LLE, left lower extremity; LUE, left upper extremity.

Overall, there was 10.8±11.3 month mean follow-up in the hypothermia group (n=35) and 14.9±19.2 in the nonhypothermia cohort (n=27). The number of patients who changed McCormick grades postoperatively was similar between the two groups (p=0.65). The hypothermia group experienced postoperative McCormick Grade improvement in 45.7% and worsening in 5.7% while in the nonhypothermia group, 44.4% of patients experienced an improvement in a McCormick Grade and 11.1% a worsening grade (Tables 1 and 3). Follow-up data were incomplete for three patients in the hypothermia group (7.9%), and eight patients in the nonhypothermia group (23.5%). The patients in the hypothermia group with documented neurological complications had follow-ups of 1.25, 22, and 5 months and 1 of the nonhypothermia patients with a neurological complication had late follow-up data.

Table 3.

Late Neurological Outcomes

Hypothermia cohort							Nonhypothermia cohort
Follow-up (mean±SD): 10.8±11.3 months							Follow-up (mean±SD): 14.9±19.2 months
		McCormick grade (n=35): Postop							McCormick grade (n=27): Postop
		1	2	3	4				1	2	3	4
Preop	1	0	0	0	0	Worsening	Preop	1	0	1	0	0	Worsening
	2	15	11	1	0	5.71%		2	10	10	2	0	11.11%
	3	0	0	4	1	Improvement		3	0	2	1	0	Improvement
	4	0	1	0	2	45.71%		4	0	0	0	1	44.44%

Bold indicates that a value reached statistical significance.

Nonhypothermia worsening versus hypothermia worsening: p=0.645.

Discussion

Hypothermia has been studied as a potential neuroprotective agent since the middle of the 20th century when Fay published a report on the effects of cooling in traumatic brain injury (TBI) patients T (Fay, 1943). However, its use never became widespread due to inefficient delivery methods and the inability to manage hypothermia's side effects in the preintensive care unit era (Williams and Spencer, 1958; Polderman, 2008). During the 1970s, local hypothermia, iced water on spinal dura during surgery, was studied as a neuroprotective strategy in SCI (Bricolo et al., 1976). Despite early optimism, experimental animal studies of local hypothermia in SCI yielded mixed results, and clinical studies of local hypothermia during laminectomy for trauma were small, nonrandomized, and poorly designed (Demian et al., 1971; Selker, 1971; Bricolo et al., 1976; Martinez-Arizala and Green et al., 1992; Kwon et al., 2008). Eventually, enthusiasm for local cooling after SCI waned.

In the 1980s and early 1990s, experimental laboratory work reinvigorated interest in hypothermia as a neuroprotective agent and began to uncover mechanisms that might portend a protective effect to nervous tissue (Busto et al., 1987; Colbourne and Corbett, 1994, 1995; Auer, 2001). Hypothermia is thought to affect many elements of the neural tissue secondary injury cascade including, reducing cellular metabolic activity (Rosomoff and Holaday, 1954; Erecinska et al., 2003), decreasing inflammatory response (Whalen et al., 1997; Chatzipanteli et al., 2000), attenuation of oxygen free radical and glutamate production (Marsala et al., 1994; Globus et al., 1995), preventing apoptosis (Ohmura et al., 2005), and other mechanisms (Colbourne and Corbett, 1994; Xu et al., 1996; Kane et al., 1999; Auer, 2001; Berger et al., 2007). Conversely, hyperthermia has been shown to worsen neural injury, thus at a minimum, it is important to prevent fever in the setting of neural injury (Dietrich et al., 1996; Yu et al., 2001).

As a result of animal and clinical hypothermia studies, generally accepted parameters for achieving safe therapeutic hypothermia have emerged including, early institution of hypothermia within 8 hours of a neurological event, target temperature of 33–34°C, cooling duration of 36–48 hours, and a controlled rewarming rate of 0.1°C per hour (Berger et al., 2007; Ohta et al., 2007; Peterson et al., 2008). Over the past decade, numerous studies have looked for a neural protective effect with moderate hypothermia in a variety of clinical settings (Cambria et al., 2000; Clifton et al., 2001; Krieger et al., 2001; Hypothermia after Cardiac Arrest Study Group, 2002; Gluckman et al., 2005; Todd et al., 2005), and thus far, level I evidence has been established for the use of moderate hypothermia for neuroprotection after cardiac arrest and perinatal asphyxia (Hypothermia after Cardiac Arrest Study Group, 2002; Gluckman et al., 2005; Polderman, 2008). Other nonrandomized studies and meta-analyses have shown trends toward benefit from hypothermia in TBI, ischemic stroke, and spinal cord protection during complex abdominal aortic aneurysm repair (McIntyre et al., 2003; Bratton et al., 2007; Polderman, 2008). A phase one safety trial of systemic hypothermia in traumatic SCI has been completed by Levi et al. demonstrating the safety of hypothermia in acute SCI patients (Levi et al., 2009).

Clinical studies of hypothermia in the management of neurological injury are becoming increasingly common; yet, to our knowledge, none have evaluated moderate hypothermia in the removal of spinal tumors. The current study focuses on the surgical and postoperative course of two largely homogenous groups of intradural extramedullary tumors resulting in spinal cord compression and intramedullary tumors resected by a single surgeon at a single institution from 2001–2010. The two groups were similar for demographic and other variables that might influence outcomes (Table 1). Modern hypothermia trials have occasionally noted a trend toward more medical complications with hypothermia. These complications have included bradycardia, arrhythmia, pneumonia, sepsis, deep venous thrombosis (DVT), and coagulopathy (Clifton et al., 2001; Hypothermia after Cardiac Arrest Study Group, 2002; Todd et al., 2005; Kwon et al., 2008). However, only one large randomized controlled trial has reported a statistically significant increased complication rate: a 2% higher rate of bacteremia (p<0.05) in patients undergoing treatment of intracranial aneurysms with induced hypothermia (Todd et al., 2005). Notable medical complications among our 38 hypothermia patients included, 1 DVT, 1 respiratory failure/1 infection, and 1 CSF infection. There were four medical complications in the hypothermia group (10.5%) and three medical complications in the nonhypothermia group (8.8%), which was not significantly different. The lack of medical complications in the hypothermia group is likely attributable to the moderate target temperature of 33.0°C and the brief duration of cooling in our protocol. Although not a direct medical complication, there was a longer LOHS in the hypothermia group of 11.1 days compared with 7.5 days in the nonhypothermia cohort (p<0.001). A significant contributor to the increased LOHS in the hypothermia cohort was the increased use of CSF diversion for CSF leak prevention. The hypothermia group received CSF diversion in 100% of the cases (2005–20010) compared with 52.9% in the nonhypothermia group (2000–2005) (p≤0.0001) (Table 1). Patient who had CSF diversion after surgery had a mean 2.6 day increased hospital stay. The increased use of spinal CSF diversion beginning in 2005 was an effort by the senior author to prevent postoperative CSF leaks and pseudomeningoceles and not related to the hypothermia ptotocol. Postoperative CSF diversion was performed in all of his intradural surgeries where a CSF drain could be placed safely. It is unclear from this data whether the hypothermia protocol or increased CSF diversion rates or both were responsible for the increased LOS in the hypothermia group.

When the surgical data and complications for the 2 cohorts were reviewed, there was no significant difference in surgical complications, EBL, ST, or AT. Some studies have suggested that hypothermia inhibits the coagulation cascade and induces temperature-dependent platelet dysfunction (Valeri et al., 1987; Rohrer and Natale et al., 1992). Interestingly, bleeding complications were higher in the hypothermia group of the HACA trial compared with control but this did not reach statistical significance (Hypothermia after Cardiac Arrest Study Group, 2002). Otherwise, abnormal bleeding has not been seen in modern hypothermia surgical trials (Kwon et al., 2008; Polderman, 2008). In the current study, moderate hypothermia did not increase EBL.

It has been established that the rates of neurological worsening among patients undergoing resection of intraspinal tumors are dependent on the pathology, timing of diagnosis, preoperative neurological status, and location of the tumor (Helseth and Mork et al., 1989; Roux et al., 1996; Innocenzi et al., 1997; el-Mahdy et al., 1999; Kane et al., 1999; Sandalcioglu et al., 2005; Aghakhani et al., 2008; Nakamura et al., 2008). In this study, the rate of neurological worsening was 7.9% (n=3) in the hypothermia group and 11.7% (n=4) in the nonhypothermia group (p=0.7)). The rates of postoperative neurological impairment in our series are consistent with results published in other retrospective surgical series (Solero et al., 1989; McCormick et al., 1990; Roux et al., 1996; Xu et al., 1996; el-Mahdy et al., 1999; Kane et al., 1999; Sandalcioglu et al., 2005; Aghakhani et al., 2008; Safavi-Abbasi et al., 2008). Furthermore, the neurological changes experienced seemed appropriate given the location and pathology of the tumors removed (Tables 1 and 2). Follow-up neurological outcomes of the patients in each group were scored on the McCormick Scale and were similar between the groups (Table 3).

This study is designed to evaluate safety and feasibility of implementing moderate hypothermia as a neuroprotectant strategy during the resection of intramedullary and intradural extramedullary spinal tumors and we conclude that this strategy is both safe and feasible. With regard to efficacy, there was no difference in the rate of neurological complications or change in McCormick Grade between the groups. This could be interpreted to indicate that hypothermia is not an effective neuroprotectant strategy in this setting; however, the subgroup of patients who would most likely benefit from a peri-operative neuroprotectant are those who experience an intraoperative neurological insult and subsequent neurological decline after surgery. Yet, only three patients in the hypothermia cohort and four patients in the nonhypothermia cohort experienced a neurological decline after surgery, and thus, this study is underpowered to detect a neuroprotective effect from moderate hypothermia in this setting. Future studies and ideally randomized, prospective studies in patients at high risk for postoperative neurological deterioration (i.e., intramedullary tumors) are needed to better examine the efficacy of hypothermia as a neuroprotectant strategy during removal of intradural spinal tumors.

Conclusion

The surgical resection of intraspinal tumors carries a risk of neurological injury. We report and compare outcomes of intraspinal tumor resections before and after the implementation of an intraoperative moderate hypothermia protocol. There was no difference in the rate of surgical, medical, or neurological complications between the two groups. There was an increased LOHS in the hypothermia group, in part related to an increased rate of CSF diversion. This study demonstrates the feasibility of brief moderate hypothermia as an adjuvant therapy during the removal of intraspinal tumors, but further investigation is needed to assess its efficacy.

Footnotes

Acknowledgments

The authors would like to thank Dr. Bruno Gallo for his assistance in reviewing and interpreting neuromonitoring records.

Author Disclosure Statement

The authors received no financial support in conjunction with the generation of this submission. Dr. Wang is a consultant for DePuy Spine and Aesculap Spine and Dr. Levi receives teaching honorariums from DePuy, Medtronic, and the American Association of Neurological Surgeons. The remaining authors have no disclosures.

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