Intraoperative neurophysiologicalmonitoring during cervical spine surgery

INTRAOPERATIVE NEUROPHYSIOLOGICAL MONITORING DURING CERVICAL SPINE SURGERY DANIEL M. SCHWARTZ, PhD

Intraoperative neurophysiological monitoring (IONM) of spinal cord function has become commonplace during surgical correction for scoliosis. Less common, albeit no less important, is its use during cervical spine surgery. This report reviews the application of three IONM techniques during cervical spine surgery; namely, somatosensory evoked potentials (SSEP), dermatomal evoked potentials (DEP), and triggered electromyography (trEMG). Each section presents a brief discussion of technical and anesthetic considerations followed by a series of augmentive exemplary case studies to provide better understanding of how best to use IONM during anterior and posterior cervical spine surgery. Particular attention is given to identifying surgical maneuvers that pose particular risk either to the spinal cord or nerve roots as well as how IONM can reduce the incidence of postoperative neurological deficit when performed and interpreted properly. The initial section on SSEPs provides both a technical and surgical overview with particular emphasis on monitoring the "high-risk" patient with cervical spondylitic myelopathy or one with an unstable cervical spine. Those using DEPs and trEMGs represent recent advanced concepts and applications for monitoring cervical nerve root function during decompression (DEP) and placement of posterior lateral mass screws (trEMG), respectively. KEY WORDS: cervical radiculopathy, cervical spondylotic myelopathy, dermatomal evoked potentials, intraoperative neurophysiological monitoring, motor evoked potentials, somatosensory evoked potentials, spinal cord monitoring, spinal nerve root monitoring, triggered electromyography

Intraoperative neurophysiology represents the application of electrophysiological recording techniques to document changes in the functional status of the central a n d / o r peripheral nervous systems of patients during surgeries that may place them at risk for iatrogenic injury. Intraoperative neurophysiological monitoring (IONM) permits detection of alterations in neural function early enough to enable the surgeon to initiate corrective measures, thus preventing permanent injury that might otherwise result in postoperative neurological deficit. Although IONM has gained wide clinical acceptance for assessing global spinal cord function during posterior spinal fusion with rigid instrumentation for scoliosis correction, it has not received similar routine application during cervical spine surgery. Yet, there is clear indication for using various forms of IONM in these cases given the potential for injury either to the spinal cord or nerve roots. 1-6IONM can also be used to show successful surgical decompression of the cervical spinal cord a n d / o r nerve roots manifested as improved neurophysiological transmission. Historically, detection of spinal cord injury during corrective spine surgery required a wake-up test 7 immediately following some form of surgical maneuver such as, distraction/derotation of a spinal implant or placement of the From the Division of Neurophysiology, Department of Neurosurgery,

Medical College of Pennsylvania-Hahnemann University, Philadelphia, PA.

Address reprint requests to Daniel M. Schwartz, PhD, Department of Neurosurgery, Mail Stop 455, MCP-HU, Broad and Vine, Philadelphia, PA 19102-1192. Copyright © 1996 by W.B. Saunders Company 1048-6666/96/0601-0003505.00/0 6

patient with an unstable spine from the supine to prone positions. Alternatively, assessment of neurological status during cervical spine surgery usually is delayed until completion of surgery and emergence from anesthesia. The obvious shortcomings to the time-honored wake-up test are as follows: (1) it requires a receptive language level high enough to follow simple commands, (2) it presumes at least near normal hearing, (3) it requires understanding of basic English (if performed in an English speaking country), (4) it requires preanesthesia rehearsal, (5) it necessitates informing the anesthesiologist of the need to reverse anesthesia to insure smooth awakening, and (6) it can take up to 15 or more minutes to complete. The last two factors are salient to the assessment of motor function within a critical time period for injury reversal because it is entirely possible that by the time the patient's level of consciousness is raised enough to assess motor function, the anatomical damage could be irreversible. Of particular significance is that the underlying principle of the wake-up test assumes that anatomical injury occurs one time only during surgery; that is, it is time-locked to a specific surgical maneuver such as distraction/derotation of corrective instrumentation. Thus, for example, spinal cord compression secondary to patient positioning, spinal cord contusion after passing a sublaminar wire at C2 or concussion due to a deeply impacted interbody fusion would go entirely unrecognized either until performing a wake-up test or completion of surgery and emergence from anesthesia. This potentially long interval between the time of insult to that of detection not only precludes determining which surgical manipulation was responsible for the adverse result, but it also delays appropriate and timely Operative Techniquesin Orthopaedics,Vol 6, No 1 (January), 1996: pp 6-12

intervention. Finally, even the gold standard wake-up test is subject to false-negative findings. 8 When performed and interpreted on-line by a highly trained and experienced clinical neurophysiologist, IONM can circumvent the need for a wake-up test because it facilitates the continuous assessment of spinal cord or nerve root function from the time of anesthesia induction to emergence. Significant changes in neurophysiological signals serve as precursors to actual anatomical injury and thus promote early warning and intervention, thereby avoiding neurological deficit.

TECHNIQUES Among the myriad neurophysiological monitoring techniques available, three play a salient role for assessing spinal cord and nerve root function during cervical spine surgery; namel)~ mixed nerve somatosensory evoked potentials (SSEP), dermatomal evoked potentials (DEP), and triggered electromyography (trEMG). A fourth, motor evoked potentials (MEP), remains investigational and although important, clinical experience with current methods of stimulation, recording and response interpretation is limited, particularly during cervical spine surgery.

Spinal Cord Monitoring The purpose of monitoring spinal cord function during spine surgery is to identify potentially reversible intraoperative complications promptly. Spinal cord monitoring is warranted, therefore, whenever there is risk of impending neurological injury. As a general rule spinal cord monitoring should be considered during cervical spine surgery whenever the cost of the complication (medico-legal, extended length of hospital stay, rehabilitation, altered quality of life, and so on) outweighs the cost of monitoring. Both human and laboratory animal studies have supported the efficacy of SSEP monitoring for identifying spinal cord injury intraoperatively.9-15 SSEPs reflect the white and gray matter structures of the large-fiber afferent sensory system. When activated by electrical stimulation applied to a peripheral nerve (eg, posterior tibial, peroneal, ulnar, and median), an afferent volley enters the spinal cord via the spinal nerve roots where afferent axons divide into branches that ascend the dorsal (posterior) columnmedial lemrdscal pathways of the spinal cord and brainstem, respectively. With the aid of digital signal averaging instrumentation, electrodes placed about the spine and head can record small (microvolt) volume-conducted potentials generated at the spinal, brainstem, thalamic, and cortical levels. Appropriate selection of peripheral nerve stimulating sites is based on an understanding of spinal anatomy and the specific surgical procedure to be monitored. The most popular sites of stimulation are the posterior tibial and median nerves with the peroneal and ulnar nerves serving as alternate sites for lower and upper extremity stimulation, respectively. In many centers, it is common to monitor cervical spine surgery with median nerve SSEPs based on the theoretical assumption that it enters the spinal cord at approximately the C7-T1 root levels. Although it is true that the medial root of the nerve carries fibers primarily from C7-T1, the fact is that the median nerve arises from MONITORING IN CERVICAL SPINE SURGERY

the heads of both the lateral and medial cords of the nerve. Nerve fibers actually enter the spinal cord at multiple root levels C5-T1, inclusive. 16 Consequently, it is entirely possible for one to record an uncompromised median nerve SSEP despite surgical insult to the distal end of the cervical spinal cord. Whenever there is question of spinal cord integrity we consider the preferred site of stimulation to be the posterior tibial nerves (ie, lower extremities) where the afferent volley ascends the entire neuraxis. If recording a reliably stable lower extremity SSEP is not possible, as might be the case in patients with severe myelopathy, spinal cord tumor, peripheral neuropathy, paraplegia, iatrogenic nerve palsy, and so on, then stimulation of the ulnar nerve is preferred over the median nerve owing to the fact that its root entry is restricted to C7-T1, inclusive. Two desired responses for monitoring spinal cord function reliably during cervical spine surgery are a subcortical and cortical potential. The subcortical response reflects electrical activity of the dorsal column and dorsal horn of the rostral cervical cord, and the dorsal column nuclei of the brain stern as exemplified in Fig 1. The cortical potential reveals synchronous postsynaptic electrical activity generated by neurons of the primary somatosensory cortex.in response to the ascending thalamocortical volley (Fig 2) for posterior tibial and ulnar nerve stimulation, respectively. In pure form, the cervical/brain stem response is bimodal in structure with the earliest peak emanating from the rostral cervical spine. The succeeding brain stem potential arises from the cervicomedullary junction in the caudal brain stem (ie, dorsal column nuclei). This response is more robust with a steep positive slope. The advantage of the brain stem potential is its insensitivity to most anesthetic agents. For surgeries based on an anterior approach to the cervical spine, the cervical/brain stem response is best recorded from a surface electrode affixed over the spinous process of C2. Since this site is within the operative field during a posterior approach, the response can be recorded easily outside the operative field from a nasopharyngeal electrode inserted to approximately the anterior side of C3. Proper nasopharyngeal electrode placement is readily

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Fig 2. Examples of the cortical somatosensory evoked potential to (A) posterior tibial and (B) median nerve stimulation. The respective electrode montage was Cz'-Fpz (posterior tibial nerve) and C3-Fpz (ulnar nerve). Response negativity is up. Note the difference in recording epoch; that is, 100 milliseconds for lower and 50 milliseconds for upper extremity stimulation.

verifiable on initial x-ray. A more near-field response can be recorded from sterile electrodes either placed within an interspinous ligament or from a sterile catheter-type electrode inserted within the epidural space at a cervical level proximal to the surgical site. The cortical potential is recorded extraoperatively from the scalp over the centro-parietal (lower extremity stimulation) or lateral parietal (upper extremity stimulation) cortices. In contrast to its subcortical counterpart, the cortical response is much larger in amplitude; however, despite its large amplitude, the cortical potential is exquisitely sensitive to all inhalational anesthetics, including nitrous oxide. This causes response amplitude to be highly variable, thus increasing the opportunity for interpretation error. Such anesthesia-related variables can be overcome with the use of intravenous drugs such as propofol, midazolam, and fentanyl that when combined in appropriate doses provide adequate anesthesia, amnesia, and analgesia without electrophysiological response consequence. Although injury to the spinal cord a n d / o r nerve roots during anterior approaches to the cervical spine are fortunately uncommon, they remain the single most feared complication. In such cases, monitoring posterior tibial nerve somatosensory-evoked potentials can identify spinal cord insult before irreversible anatomical injury as illustrated in Fig 3. Shown here is a series of cortical potentials depicting the effect of significant spinal cord compression from a deeply impacted interbody fusion at C4/5. Immediately following final impact of the iliac crest graft there was an 83% loss of the pregraft response amplitude. At surgical notification the graft was removed resulting in an immediate amplitude improvement. This negative-positive electrophysiological response serves as verification that the neurophysiological changes were indeed time-locked to impaction of the bone graft and that immediate intervention (eg, removal) reversed what may have resulted in untoward neurological deficit. Although response amplitude remained some 65% decreased at graft removal, the immediacy of the return was sufficient evidence to allay any concern for permanent neurological sequelae. Patients with cervical spondylotic myelopathy (CSM) or those with cervical spine instability are particularly at risk 8

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for spinal cord compression injury as a result of hyperextension of the neck during intubation a n d / o r placement in the prone or sitting positions. It is our practice to monitor the intubation with SSEPs in an effort to identify spinal cord compression injury in the anesthetized patient versus the awake patient as depicted in Fig 4. Note that contralateral cortical SSEPs to left and right ulnar nerve stimulation are completely lost bilaterally (arrows) on hyperextension of the neck to facilitate intubation. Following anesthesia alert the neck is flexed and returned to its neutral position at which time there was immediate return of the responses. Reintubation with limited neck extension was then accomplished without event. This application of IONM is used in lieu of fiber-optic intubation with the patient awake which can be unpleasant and trying both for the patient and for the anesthesiologist. Spinal cord compression is also a potential complication of patient positioning as exemplified in Fig 5. Here again, it is our practice to monitor SSEPs before and after positioning. The sequence of neurophysiological events shown in Figure 5 is illustrative of the effect of positioning on the spinal cord in patients with CSM. The preposition posterior tibiat nerve cortical SSEPs are characterized by large amplitude responses, bilaterally. Upon turning the patient prone, response amplitude was decreased by 80%. The patient's head and neck were subsequently repositioned LEFT

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under continuous monitoring conditions until amplitude began to approach or equal baseline value. As was discussed previously for monitoring intubation, the effect of placing the patient prone on spinal cord electrical transmission was clearly observed in the SSEP data as was the influence of intervention, in this case, repositioning the patient's head and neck. SSEP monitoring during pediatric cervical spine surgery is also highly beneficial for identifying direct contusion to the spinal cord such as when passing sublaminar wires for atlanto-axial arthrodesis (eg, Brooks technique) 17 as exemplified in Fig 6. Observe the acute loss of the cervical/brain stem response following passing a sublaminar wire at C2. Removal of the wire led to almost immediate recovery with continued amplitude improvement over the next 7 minutes. Inadequate spinal cord perfusion as depicted in Fig 7 can also be identified by significant alteration of the SSEP

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MONITORING IN CERVICAL SPINE SURGERY

amplitudes. The ulnar nerve cortical SSEP of this patient with severe CSM show impending spinal cord ischemia during surgical decompression whenever the patient's mean arterial blood pressure (MAP) decreased below 80. In such cases it is critical that the attending neurophysiologist communicate with the anesthesiologist to insure adequate spinal cord blood flow throughout the surgical course. If a 30% to 50% amplitude decrease is noted, MAP should be increased to ->90. Monitoring Cervical N e r v e R o o t s

Despite its value for assessing global spinal cord function, mixed peripheral nerve SSEPs have been unsuccessful for monitoring the effects of nerve root decompression or for identifying instantaneous sharp instrument (eg, bone screw) insult to a nerve root. Recall that a mixed nerve enters the spinal cord at multiple levels and is thus incapable of providing root specific electrophysiological information during decompression. Two electrophysiological techniques that help overcome these limitations are DEPs and trEMGs. Dermatomal evoked potentials. The functional integrity of

an individual nerve root can be assessed by stimulating a dermatomal-field and recording an afferent evoked potential over the scalp similar to that described for mixed nerve SSEPs. In radiculopathic patients undergoing surgical decompression of cervical nerve roots, DEPs are characteristically reduced in amplitude a n d / o r prolonged in latency, or are entirely absent at baseline owing to the nerve root compression. In contrast to monitoring spinal cord function which focuses on identifying degradation of the SSEP in response to spinal cord insult, the intent of monitoring DEPs is to show the adequacy of surgical decompression at each root level as exhibited by improved response amplitude a n d / o r latency relative to the abnormal baseline. The dramatic illustration of how DEPs can be useful during anterior cervical decompression is shown in Fig 8. Here the preincision baseline C6 DEP is entirely absent consistent with the patient's histor~ physical, and radiological evidence of C6 nerve root compression. Continuous monitoring of the nerve root evoked potential during discectomy, osteophytectomy, and so on can be used as a guide as to when the root has been adequately decompressed. Note that following decompression the response not only emerged from the absent baseline, but 9

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that they are not particularly sensitive for instantaneous recognition of sharp root injury as occurs with placement of bone screws. TMAs with the lumbosacral spine, the use of metal plates and bone screws for internal fixation of the unstable cervical vertebrae is becoming increasingly popular. Although posterior lateral mass plating reduces the heightened risk of spinal cord injury known to occur with

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sublaminar wiring, improper positioning of the lateral mass screws or cervical pedicle screws can still compromise important neural elements such as the spinal cord, vertebral arteries or spinal nerve roots. 19 An improper screw trajectory a n d / o r length can in fact violate the nerve root as a result of anatomic and morphological variability among patients. 2° This is particularly true for screws placed at C7 where changes in vertebral morphology poses an increased threat of sharp trauma to the C8 nerve root. 2° One simple and reliable electrophysiological technique that has proven to be exquisitely sensitive for identifying cortical perforation during pedicle screw placement in the lumbosacral spine is trEMG. 21 Our positive experience over the past 4 years with approximately 300 patients undergoing posterior lumbar fusion with internal fixation supports the findings of Clancie et al. 22 This success led us to apply the same trEMG neuromonitoring principles for identifying cortical breach from placement of posterior cervical pedicle screws. For the test procedure, self-adhesive, disposable surface electrodes are affixed over muscle innervated by the nerve root of interest. A sterile monopolar probe insulated down to the bare tip (flush tip) serves as the stimulating cathode. An electroencephalogram needle electrode inserted in nearby adjacent muscle is the anode. Both are connected to the negative and positive poles, respectively of the electrical triggering device of the same neurophysiological instrumentation used for SSEP and DEP monitoring. Following screw placement, the uninsulated tip of the monopolar probe is touched to the screw head and the electrical current output is increased to 12 mA. Too high a stimulus level will cause current to flow even through an intact bony wall resulting in a false-positive response, whereas one too low will be insufficient to excite the nerve root thus effecting a false-negative response. Essential to the success of trEMG is that anesthesia must have the patient completely unparalyzed because all depolarizing and nondepolarizing paralytic agents block the neuromuscular junction, thus precluding muscle contraction. If there is a cortical perforation, the normally high impedance of the intact bony wall will be lowered and the flow of electrical current from the cathode to the anode will take the path of least resistance, namely, through the breach to the root. Subsequently the root will "fire" and the peripherally innervated muscle will contract. This will be recorded as a compound muscle,action potential (CMAP) as shown in the top tracing of Fig 10. This patient presented with tingling and pain sensation in the fourth and fifth fingers several weeks following posterior plating. Upon re-exploration, trEMG was used to identify possible cortical penetration. A CMAP was recorded with screw stimulation verifying the breach and indicating irritation of the C8 nerve root. The screw was replaced with a new one directed in the original hole; however, stimulation again resulted in a recordable CMAP of somewhat smaller amplitude. Subsequently, a new hole was made whereby screw stimulation did not imply presence of a cortical breach as depicted in the last tracing of Fig 10; however, trEMG is invalid with bicortical purchase for lateral mass screws since it insures nerve root excitation when the screw is stimulated.

DANIEL M. SCHWARTZ

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The application of neurophysiological monitoring techniques to assess the functional status of the spinal cord and spinal nerve roots is no longer considered experimental. A substantial body of research has shown that IONM can help reduce the prevalence of postoperative morbidity in patients undergoing operations on the spine. In fact, The Scoliosis Research Society (Rosemont, IL) put forth a position paper which concluded that " . . . the use of intraoperative spinal cord neurophysiological monitoring during operative procedures including instrumentation is not considered investigational. The Scoliosis Research Society considers neurophysiological monitoring a viable alternative to the wake-up test. ,,23In their landmark review of 100 patients, Epstein et a115 found that intraoperative neurophysiological monitoring reduced the prevalence of quadriplegia associated with cervical spine surgery from a previous 3.7% to 0%. If the relatively low cost ($600 to $1,500) for IONM during cervical spine surgery is weighed against the burdensome high cost of potential untoward neurological deficit, the merit of having an on-line means of injury prevention becomes evident. Quite simply, IONM makes spine surgery safer. Given current emphasis on managed health care, preventive medicine, and risk management, it would appear advantageous for the surgeon, patient, hospital administration, and insurance carrier alike to have IONM be a routine reimbursable service.

BRACHIAL PLEXUS MONITORING Among the constellation of complications that can result from posterior spine surgery is brachial plexopathy. Recording cervical/brain stem SSEPs to ulnar nerve stimulation is remarkably effective toward identifying stretch/compression injury in the prone patient positioned with outstretched arms. If at any time during the procedure a ->25% response amplitude decrease is observed, anesthesia should be alerted and the patient's arms repositioned as observed in Fig 11, where the right arm response amplitude is shown to decrease significantly relative to the left during cervical laminectomy. Repositioning of the right arm resulted in amplitude improvement within approximately 2 minutes. We now recommend that ulnar nerve SSEPs be monitored

MONITORING IN CERVICAL SPINE SURGERY

ACKNOWLEDGMENT I am deeply indebted to Drs Said Alemo, Arnold Berman, Todd Albert, Perry Black, Steven Bosacco, Leonard Bruno, John Dormans, Denis Drummond, Ann Christine Duhaime, Robert Dunn, Malcolm Ecker, Craig Israelite, Gary Magram, Tom McCormack, Somnath Nair, Gene Salkind, David Sedor, Leslie Sutton, Ronald Wisneski, and Eric Wolfson who consider neurophysiological monitoring to be an integral part of spine surgery in general and cervical spine surgery in particular, and who continue to support new developments in the field. I also wish to thank my colleagues and associates Robert Pratt, MS, Jamie A. Schwartz, MS, Anthony K. Sestokas, PhD, Joy Wier-

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zbowski, BA, and Larry Wierzbowski, MS, whose standard of excellence in intraoperative neuromonitoring is truly incomparable. Finally, a special thanks to our office manager Joy, who somehow manages to keep a very busy neurophysiological monitoring practice straight on course.

REFERENCES 1. Bohlman H: Cervical spondylosis with moderate to severe myelopathy. Spine 2:151-162, 1977 2. Kraus FR, Stauffer ES: Spinal cord injury as a complication of elective anterior cervical fusion. Clin Orthop 112:130-141, 1975 3. Flyrm TB: Myelopathy following anterior cervical discectomy and fusion: A case report and discussion of recent literature. Neurosurgery 4:550, 1979 4. Flynn TB: Neurologic complications of anterior fusion. Spine 7:536539, 1982 5. Whitecloud T: Complications of anterior cervical fusion, in instructional course lectures, vo127. St Louis, MO, Mosby-Year Book, 1978 6. Cottrell JE, Hassan NF, Hartung J, et al: Hyperflexion and quadriplegia in the seated position. Anesth Rev XII:34 (abstr) 7. Vauzelle C, Stagnara P, Jouvinroux P: Functional monitoring of spinal cord activity during spinal surgery. Clin Orthop 93:173, 1973 8. Diaz J, Lockhart CH: Postoperative quadriplegia after spinal fusion for scoliosis with intraoperative awakening. Anesth Analg 66:10391042, 1987 9. Nash CL Jr, Lorig RA, Schatzinger LA, et al: Spinal cord monitoring during operative treatment of the spine. Clin Orthop 126:100-105, 1977 10. Dorfman LJ, Perkash I, Bosley TM, et al: Use of cerebral evoked potentials to evaluate spinal somatosensory function in patients with traumatic and surgical myelopathies. J Neurosurg 52:654-660,1980 11. Tamaki T, Tsuji H, Inoue S, et al: The prevention of iatrogenic spinal

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cord injury utilizing the evoked spinal cord potential. Int Orthop 4:313-317,1981 Machida M, Weinstein S, Yamada T: Spinal cord monitoring: electrophysiological measures of sensory and motor function during spinal surgery. Spine 10:407-413, 1985 Veilleux M, Daube JR, Cucchiara RF: Monitoring of cortical evoked potentials during surgical procedures on the cervical spine. Mayo Clin Proc 62:256-264, 1987 Owen JH, Bridwell KH, Shimon SM, et al: Sensitivity and specificity of somatosensory and neurogenic motor evoked potentials in animals and humans. Spine 12:1111-1118,1988 Epstein NE, Danto JD, Nardi D: Evaluation of intraoperative somatosensory evoked potentials monitoring during 100 cervical operations. Spine 18:737-747, 1993 Haymaker W, Woodhall B: Peripheral Nerve Injuries: Principals of Diagnosis. Philadelphia, PA, Saunders, 1945 Brooks A, Jenkins E: Atlanto-axial arthrodesis by the wedge compression method. J Bone Joint Surg Am 60A:279-284, 1978 Toleikis JR, Carlvin AO, Shapiro DE, et al: The use of dermatomal evoked responses to monitor surgical procedures involving intrapedicular fixation of the lumbosacral spine. ASNM Newsletter 10, 1991 Heller JG, Carlson GD, Abitbol JJ, et al: Anatomic comparison of the Roy-Camille and Magerl techniques for screw placement in the lower cervical spine. Spine 16:552-557, 1991 An HS, Gordin R, Renner K: Anatomic considerations for plate-screw fixation of the cervical spine. Spine 16:552-557,1991 Calancie B, Lebwohl N, Madsen P, et al: Intraoperative evoked EMG monitoring in the animal model: A new technique for evaluating pedicle screw placement. Spine 17:1229-1235, 1992 Calancie B, Madsen P, Lebwohl N: Stimulus-evoked EMG monitoring during transpedicular lumbosacral spine instrumentation. Spine 19: 2780-2786, 1994 Dawson EG, Sherman JE, Kanim LE, et al: Spinal cord monitoring: Results of the Scoliosis Research Society and the European Spinal Deformity Society survey. Spine 16:$361-$364, 1991 (suppl 8)

DANIEL M. SCHWARTZ