Spinal cord monitoring

Handbook of Clinical Neurology, Vol. 160 (3rd series) Clinical Neurophysiology: Basis and Technical Aspects K.H. Levin and P. Chauvel, Editors https://doi.org/10.1016/B978-0-444-64032-1.00021-7 Copyright © 2019 Elsevier B.V. All rights reserved

Chapter 21

Spinal cord monitoring MARC R. NUWER1,2* AND LARA M. SCHRADER1,2 Department of Neurology, David Geffen School of Medicine at UCLA, Ronald Reagan UCLA Medical Center, Los Angeles, CA, United States

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Department of Clinical Neurophysiology, Ronald Reagan UCLA Medical Center, Los Angeles, CA, United States

Abstract Spinal cord surgery carries the risk of spinal cord or nerve root injury. Neurophysiologic monitoring decreases risk of injury by continuous assessment of spinal cord and nerve root function throughout surgery. Techniques include somatosensory evoked potentials (SEPs), transcranial electrical motor evoked potentials (MEPs), and electromyography (EMG). Baseline neurophysiologic data are obtained prior to incision. Real-time signal changes are identified in time to correct compromised neural function. Such monitoring improves postoperative neurologic functional outcomes. Challenges in neurophysiologic intraoperative monitoring (NIOM) include effects of anesthetics, neuromuscular blockade, hypotension, hypothermia, and preexisting neurological conditions, e.g., neuropathy or myelopathy. Technical factors causing poor quality data must be overcome in the electrically noisy operating room environment. Experienced monitoring teams understand tactics to obtain quality recordings and consider confounding variables before raising alarms when change occurs. Once an alert is raised, surgeons and anesthesiologists respond with a variety of actions, such as raising blood pressure or adjusting retractors. In experienced hands, NIOM significantly reduces postoperative neurological deficits, e.g., 60% reduction in risk of paraplegia and paraparesis. A technologist in the operating room sets up the NIOM procedure. An experienced clinical neurophysiologist supervises the case, either in the operating room or remotely on-line continuously in real time.

INTRODUCTION The spinal cord and nerve roots can be at risk of injury during spine surgery. This risk is decreased through the use of neurophysiologic intraoperative monitoring (NIOM). NIOM is performed during spine surgery to provide continuous real-time assessment of the function and integrity of neural structures. For spine surgery, the most commonly used neurophysiological techniques for NIOM include somatosensory evoked potentials (SEPs), motor evoked potentials (MEPs), and electromyography (EMG). SEPs assess spinal cord dorsal column integrity by stimulating peripheral nerves in upper and lower extremities and recording the scalp potentials evoked

from this stimulation. Intact SEPs suggest intact dorsal column function in the posterior cord. MEPs assess cord function differently. A train of transcranial brain stimulation provokes a muscle response recorded in upper and lower extremities. Intact MEPs suggest intact corticospinal tract function in the lateral cord. EMG can be continuously recorded from muscles supplied by at-risk nerves or nerve roots. Nerve root irritation or injury during surgery can produce EMG discharges. In some cases, stimulation is done to produce an EMG discharge (stimulation-triggered EMG) to correctly identify nerve tissue or to verify proper pedicle screw placement. SEPs are usually tested continuously. If SEP waveforms deteriorate, the neurophysiology team alerts the

*Correspondence to: Marc R Nuwer MD PhD, UCLA Dept Neurology, Reed Bldg, room 1190, 710 Westwood Plaza, Los Angeles, CA 90095, United States. Tel: +1-310-206-3093, Fax: +310-267-1167, E-mail: [email protected]

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surgeon to changes. These changes suggest imminent spinal cord injury, in time for interventions to reverse or halt complications. MEPs are usually tested intermittently, such as at times when the surgeon believes the cord may be at risk. EMG monitoring often is added to SEP and MEP monitoring. A combination of modalities can be monitored simultaneously (Fig. 21.1). The neural structures at risk for injury during each surgery determine which combination of SEP, MEP, and/or EMG to use for NIOM. Furthermore, the individual SEP, MEP, and EMG monitoring techniques can be tailored to optimize monitoring of neural structures most at risk in an individual surgery. The neurophysiology team establishes baseline findings at the beginning of a procedure. The ongoing actively recorded findings are compared to baseline data. Changes from baseline can trigger alerts. The thresholds for alerts typically are predetermined, such as a 50% decrease in SEP cortical peak amplitude. The neurophysiology team informs the surgeon at baseline if data is reliable for monitoring. If baseline data is poor, technical and physiologic reasons should be explored. Physiologic issues related to the patient can cause poorly reliable baseline data. For example, lower extremity SEPs and/or MEPs may be absent in a thoracic myelopathy case. This is an expected finding. However, in such a case it is nonetheless worthwhile to maximize

stimulation parameters, which can sometimes produce reproducible potentials that were initially absent. When the baseline data do not correlate with the clinical picture, technical reasons should be ruled out.

SOMATOSENSORY EVOKED POTENTIALS SEPs typically are obtained through stimulation of the median or ulnar nerve of the upper extremities and the peroneal or posterior tibial nerves in the lower extremities. SEPs are often used in spinal cord monitoring. For SEPs to be useful for monitoring, the potentials need to be reliably present with relatively stable amplitudes and latencies from trial to trial. Optimizing the “signalto-noise” ratio is key to successful SEP monitoring. The “signal” is the evoked potential itself that can be optimized by adjusting the site of stimulation and/or maximizing stimulation or recording parameters. The “noise” is the electrical noise in the operating room that can contaminate the SEP recording. If the noise is at a high enough level relative to the amplitude of the neurophysiologic potential, the potential will not be discernable from noise. Improved signal-to-noise ratio can be achieved by increasing the signal amplitude or decreasing the recorded noise. Techniques for accomplishing this are discussed in the paragraphs that follow.

Fig. 21.1. Multimodality monitoring simultaneously assesses four-limb somatosensory evoked potentials, four-limb motor evoked potentials, the multichannel ongoing electromyogram, and several channels of ongoing electroencephalogram. An Event Window text box documents stages of activity. This typical spinal surgery page allows the monitoring team to overview many modalities. Other available screen pages focus on specific modalities in greater detail. A Chat Window (not shown) also is available for quick communication between the technologist and monitoring physician.

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Stimulation Ulnar nerve or median nerve SEP testing begins with stimulation at the wrist. Stimulus intensity of 20–40 mA is above the motor threshold to produce finger movements. Ulnar nerve SEPs are preferable to median nerve SEPs for cervical cases. This is because the ulnar SEPs give more complete cervical spinal cord coverage. Ulnar monitoring is used in lumbar cases to prevent ulnar palsy due to arm positioning (Schwartz et al., 2006). Posterior tibial nerve stimulation is used for lower extremities in many cases. Stimulation is delivered posterior to the medial malleolus at the ankle at an intensity of 25–50 mA. In patients with peripheral neuropathy, diabetes, or age greater than 65 years, more proximal nerve stimulation is often necessary for obtaining reliable SEPs. In these patients, peroneal nerve SEP monitoring also is set up. The peroneal nerve is stimulated at the fibular head just below the knee. By preparing both nerves, the team can choose which produces optimal potentials. In patients with peripheral neuropathy, diabetes, or age greater than 70 years, the lower extremity SEPs often are absent with stimulation at the ankle. In these patients, it is especially helpful to have the option to stimulate proximally at the knee. Increasing pulse width is another useful strategy for optimizing SEPs in these individuals. Higher stimulation intensities produce signals of higher amplitude. However, higher intensities also produce more movement in unparalyzed patients. Posterior tibial nerve stimulation causes plantar flexion at the ankle, and peroneal nerve stimulation causes foot dorsiflexion. In the absence of neuromuscular blockade, these movements can become disruptive to the surgeon and therefore can limit the stimulus intensity used. Nerves are stimulated at fixed repetition rates of 1.3–5 per second. Since several hundred stimulations are averaged to produce a single SEP, faster stimulation rates have the benefit of producing SEP tracings more quickly and therefore providing the surgeon with feedback more quickly. Unfortunately, faster rates produce SEPs with lower amplitudes (Nuwer and Dawson 1984). Therefore, lower repetition rates are often necessary for obtaining SEPs with high enough amplitude to be reliable for monitoring. The NIOM team adjusts the rate to find the optimal rate vs amplitude trade-off. If baseline SEPs are low amplitude, a typical strategy is to decrease the stimulation rate to improve SEP amplitudes. Repetition rates necessary for reproducible SEPs in older patients are often around 2.5 per second, whereas a rate twice as fast can be used in younger patients. Other strategies helpful for improving the SEP amplitude are to increase the stimulation pulse width and/or intensity. To decrease 60-Hz noise contamination, repetition rates should not be a multiple of 60.

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Typically, 300 stimulation repetitions are averaged to obtain each SEP trial. Two minutes are required to produce a new SEP tracing obtained by averaging 300 repetitions at 2.5 per second. In cases with high background noise and low-amplitude peaks (i.e., a low signal-tonoise ratio), larger sample sizes of up to 500–1000 repetitions can improve signals. A downside to this approach is the longer time interval between trials, resulting in less frequent feedback to the surgeon. Electrocautery and other problems can create noise that prevents recording and further slows the process of acquiring new tracings.

Recordings Primary recording electrodes are placed at the scalp and neck. Scalp electrode locations are based on the modified 10% extension of the 10/20 system (Nuwer et al., 1998). Additional scalp recording channels can help locate the highest amplitude cortical peaks. Flexibility in scalp recording channels is preferable to using the same preset recording montage. Optimal scalp locations for SEP peaks can differ from patient to patient. Searching for optimal sites early in the case can help ensure adequate monitoring channels for an individual patient. An example of monitoring over an hour is illustrated in Fig. 21.2A. An electrode is placed over the fifth cervical spine for recording cervical potentials in thoracolumbar spinal cases. During cervical spine surgery, a substitute site is the mastoid process or ear. Peripheral potentials can be recorded using electrodes placed over the shoulder, lumbar spine, or popliteal fossa. SEPs are recorded using a low-frequency filter set to 30 Hz. The high-frequency filter setting ranges between 500 and 1500 Hz. This can be adjusted to optimize the signal-to-noise ratio. A higher setting records more background noise but produces higher amplitude SEPs, whereas a lower setting attenuates the noise but also attenuates the SEP amplitude. When recording EMG or EEG, the notch filter successfully removes the 50- or 60-Hz line noise commonly encountered in the operating room. However, the notch filter should not be used for recording SEPs. First, the notch filter can attenuate SEPs because SEP waveforms are composed of frequencies in the 50–60 Hz range. Second the notch filter can also produce ringing artifact that can mimic SEP peaks. The ideal method for eliminating excessive electrical environmental noise is to turn off and unplug the equipment responsible.

Interpreting changes The potentials generated by ulnar nerve stimulation include the cortical N20, the subcortical N18, and the

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Fig. 21.2. Typical routine reproducible SEPs and MEPs in waterfall displays. (A) Posterior tibial nerve SEP cortical peaks, 10 ms/div, 0.5 mV/div, tested repeatedly over an hour, demonstrating good reproducibility. Most recent tracings are graphed at the bottom. (B) MEP responses recorded from abductor pollicis brevis (hand), tibialis anterior (leg), and abductor halluces (foot), 10 ms/div, 100–1000 mV/div. A double pulse stimulus artifact is seen at the beginning of each MEP trace, most notably in the leg traces. MEPs were tested periodically over an hour and demonstrated good reproducibility.

cervical N13 peaks. For posterior tibial or peroneal stimulation, the potentials generated include the cortical P37 peak and subcortical P30 peak in a cervical channel. Both latency and amplitude are measured for each peak. The standard criteria for raising an alarm are a 50% drop in amplitude or a 10% increase in latency. The monitoring team must quickly decide whether observed changes are due to technical, anesthetic, or systemic changes, or due to a surgical maneuver. If peripheral peaks are recorded (such as the Erb’s point N9 for upper extremity SEPs or the popliteal fossa N8 for lower extremity SEPs), drop of peripheral peaks simultaneous with drop in subcortical and cortical potentials indicates an issue with stimulation, such as a loose electrode or stimulator malfunction. When SEPs from all four limbs are simultaneously affected, systemic problems or anesthetic affects are more strongly suspected, although when working on the high cervical cord, a surgical cause should also be considered. Systemic issues that can adversely affect SEPs include hypothermia, hypotension, and hypoxia. Fig. 21.3 illustrates the temperature effect on SEPs. Anesthesia effects are considered when changes occur. If no obvious causes are identified, the surgeon and anesthesiologist are alerted. Changes in anesthetics during a case can alter SEPs and confound NIOM interpretation. Inhalation anesthetics attenuate cortical peak amplitudes and increase latencies. Compared to cortical peaks, subcortical N18 and P30 peaks are less affected by inhalation anesthetics.

Fig. 21.3. Temperature effect: SEP ulnar nerve N20 cortical peaks in a waterfall display. SEP tracings are displayed over an hour as the patient is cooled. Time reads upward and notes the tracings at 22 and 45 min after the bottom tracing. Most recent tracings are graphed at the top. Reduced temperature results in longer latency peaks, lower amplitude, and eventually loss of the peak. Hypothermia below 20°C is used for nervous system protection in certain surgeries.

SPINAL CORD MONITORING Boluses of anesthetic agents, such as propofol, may abruptly but transiently affect cortical peak amplitudes. Anesthetic fade is a gradual increase in latency and decrease in amplitude in cortical potentials that is due to the gradual cumulative effect of anesthesia. Fade of SEPs is most noticeable in the initial 40 min following induction. When alerted, the surgeon reviews surgical maneuvers over the past 20 min. Some surgical actions may take 20 min before a significant change in SEPs occurs. Compression or stretching or marginal degrees of ischemia to neural tissue may require a gradual accumulation of physiologic effects before there is a change in function noted in NIOM. Fig. 21.4 illustrates a case with SEP monitoring during cervical spine surgery. The changes alerted the surgeon who intervened to mitigate the impairment. The

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monitoring suggested the localization of impairment. With this information, the surgeon was in a position to best understand the situation and prevent further impairment. Fig. 21.5 illustrates a case in which signals were lost during spinal correction of scoliosis. Both SEP and MEP were lost abruptly. The surgery was altered, blood pressure was raised, and steroids were administered. The patient awoke with a paraparesis that gradually resolved over months. Presumably the changes to the procedure prompted by monitoring saved the patient from a much denser, longer-lasting deficit. Fig. 21.6 illustrates a lumbar spine surgery in which the SEP identified an incipient brachial plexus injury. Prompt intervention corrected the positioning problem, reducing the risk of postoperative plexus injury. SEP showed a return to baseline upon repositioning.

Fig. 21.4. Identification and localization of intraoperative adverse processes: A 68-year-old man underwent cervical posterior fusion with monitoring of bilateral SEPs of the upper and lower extremities. The SEPs disappeared during initial exposure of the C1 lamina. Changes were asymmetric in degree and duration. The type of SEP changes gave localizing information about the nature of the impairment, consistent with injury above the cervicomedullary junction. This illustrates how intraoperative SEP monitoring can provide important information on the functional integrity of brainstem structures even during cervical surgery. In this case, the cause was a vascular event related to a vertebral artery. The surgeon initiated prompt steps to intervene and mitigate the adverse effect. Postoperative imaging demonstrated posterior inferior cerebellar artery (PICA) infarct involving the left lateral medulla. The right nucleus cuneatus region peak was spared (column 3), whereas the left was lost (column 1) due to left vertebral artery impairment, and both cortical peaks (columns 2 and 4) were lost due to further ischemia at the decussation of the lemniscus. From Tran, C.T., Khoo, L.T., Martin, N.A., et al., 2012. Somatosensory-evoked potential asymmetry in medullary ischemia during cervical spine surgery. J Clin Neurophysiol 29, 17–22, with permission.

Fig. 21.5. Impairment identified during spine surgery. An 11-year-old underwent a spinal corrective procedure for severe kyphoscoliosis. Upon decompression, the lower extremity SEPs were lost while upper extremity SEPs were unchanged. MEPs also acutely changed. The surgeon was notified and altered his procedure. The patient awoke with a paraparesis that gradually resolved over months. Presumably the changes to the procedure prompted by monitoring saved the patient from a much denser, more long-lasting deficit. Upper panels are upper extremity tests, two cortical and one cervical channel, 5 ms/div, 0.5mV/div. Lower panels are lower extremity tests, one cortical and one cervical channel, 10 ms/div, 0.3 mV/div; light gray tracings are baselines for comparison.

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through transcranial electrical (tce) stimulation of the motor cortex, although higher levels of stimulation may stimulate its descending white matter tracts.

Stimulation

Fig. 21.6. Ulnar nerve compression identified: A 70-year-old underwent a lumbar spine decompression and fusion surgery. The figure shows successively recorded right ulnar SEPs. Time runs from the top downward. Trial 1 served as a baseline. A significant change occurs between trials 5 and 6. SEP amplitude decreased by >50% and latency increased by >10%. Arm repositioning and removal of shoulder taping resulted in a gradual return to baseline amplitude and latency (run 14). Brachial plexus injury is an occasional adverse outcome of lumbar surgery, which may be avoided by monitoring.

Clinical risk of change A reduction in SEP amplitude does not always predict an adverse neurologic outcome. A 50%–80% SEP amplitude decrease lasting several minutes is associated with only a small to modest risk of postoperative deficit. This is the case especially if the SEP amplitude subsequently returns to baseline. On the other hand, abrupt and complete loss that persists carries a 50%–75% risk of adverse outcome.

MOTOR EVOKED POTENTIALS MEPs monitor corticospinal tract function. This modality is especially important since preserving motor function is a high priority of surgery. MEPs are elicited

Stimulating electrodes are secured on the scalp at locations near the motor cortex of each hemisphere. The scalp sites of electrode placement are named according to the 10% extension of the 10–20 electrode system (Nuwer et al., 1998). The anode electrode is placed 2 cm anterior to C3 or C4, and the cathode electrode is placed at Cz or CPz. Alternate scalp sites may result in optimal responses. A stimulus intensity of 200–400 mA usually is adequate to produce MEPs. Stronger stimulation, up to 600mA, which may correspond to 1000–1200 mV, is sometimes used. The stimulus pulse width is set to 0.05 ms, but can be increased if responses are difficult to obtain. A single tce stimulation pulse typically does not generate an adequate MEP response. Brief multipulse tce stimulation trains are used and are effective in most patients. Commonly, tce stimulation trains consist of 5–7 stimuli separated by a fixed interpulse interval of 1.0–3.0 ms. This multipulse train creates a buildup of excitatory postsynaptic potentials at anterior horn cells in the spine that results in the cell firing an action volley and thus creating recordable tceMEP muscle activity. In some cases, single multipulse trains are unsuccessful at generating MEPs. In such a case, double train stimulation may be effective. An initial priming of a 2- to 3-pulse train is followed by a second 5- to 7-pulse train. An interstimulus interval of about 2 ms is typical. An intertrain interval of about 10 ms results in a facilitated response. A first brief train primes anterior horn cells; the second longer train more effectively discharges the anterior horn cells. Each tce pulse stimulates corticospinal axons in the cerebral hemispheres. Higher intensities stimulate axons in deeper white matter. High stimulation intensities result in reduced MEP latencies by stimulating corticospinal axons at deeper anatomical levels.

Recording Electrodes are placed in arm and leg muscles to record tceMEP responses. Proximal and distal limb muscles are often chosen. Distal muscles of the hands and feet often have more robust MEP responses due to greater cortical representation of those muscles in the motor cortex. It can be helpful to record from several muscles in each limb because good results may appear in one muscle group, whereas only marginally recordable or absent results may appear in other muscles. Recording more muscles increases the likelihood of getting reliable MEPs from each limb. Fig. 21.2B illustrates MEPs recorded

336 M.R. NUWER AND L.M. SCHRADER over an hour; only three channels are illustrated. When arrhythmias are also relative contraindications. Absolute obtaining baseline MEP responses, tce stimulation intencontraindications include intracranial electrodes (e.g., sity is gradually increased until adequate MEPs are deep brain stimulators) and vascular aneurysm clips. One recorded. report suggests that implanted devices are not adversely The tceMEP responses are polyphasic complex comaffected by MEP stimulation (Yellin et al., 2016). With pound muscle action potentials (CMAPs) recorded in appropriate precautions the benefits of MEP monitoring in preventing spinal cord injury outweigh the risks in the each muscle site. MEP amplitude can be measured. As large majority of spinal surgery cases. secondary criterion, the complexity of the response in terms of the number of polyphasic turns in the response is noted. Interpretation Stimulation used to elicit MEPs also creates potentials that can be recorded in the spinal cord itself from elecWithin a single patient undergoing a single surgical case, trodes in the epidural space. These recordings measure MEP potentials generated from a muscle may vary someaxon volleys from the corticospinal tracts. These potenwhat in amplitude and morphology from one trial to the tials are called D-waves. D-waves are recorded using epinext. Therefore, many NIOM teams use an all or none criteria for MEP alerts. Fig. 21.7 illustrates complete loss dural electrodes either bipolar or with a nearby reference. of MEPs upon placement of a pedicle screw at T6. Using Since D-waves’ very small amplitude decreases more caudally, they are more easily recorded at cervical and this criterion of complete loss, a potential that was preupper thoracic levels. D-waves can be recorded under sent at baseline but then disappears is a potential alarm. conditions of complete neuromuscular blockade and While this seems quite straightforward, the monitoring are minimally affected by anesthesia. However, the team routinely first assesses other factors before deciding recording electrodes are easily dislodged, and movement to alert the surgeon. The monitoring team considers the of a recording electrode can create a change in amplitude. muscle baseline MEP response. If the baseline amplitude was low and the MEP lacked complex polyphasic morAlso, the pathway responsible for a reduced signal can be phology, such simple MEP responses may disappear due challenging to lateralize. to anesthesia fade. The monitoring team also considers the responses from other muscles in the same limb. If a Safety limb has several muscles with good, well-defined MEPs, Few adverse events are associated with tceMEP stimulathe loss of MEP from just one muscle may not be of clintion (MacDonald, 2002). Tongue and lip laceration can ical significance. A potential may be small because the occur because the stimulation activates not only the brain stimulation intensity is near the motor threshold for a but also nearby muscles on the skull, resulting in a brisk response. When stimulation intensity is just at the motor jaw closure. To prevent tongue and lip lacerations, a threshold, a response may not be present with each stimmouth guard is placed prior to surgery. Mouth guard placeulation. A sudden loss of all MEPs from several muscles ment is reassessed after turning the patient prone for spine within one limb is cause for an alert. Sudden loss of all surgery. While seizures are rare, many NIOM teams nevMEPs from both lower extremities is a straightforward ertheless monitor EEG during tceMEP as a precaution to reason for an alert, especially in the absence of an anesmonitor for stimulation-induced afterdischarges or seithetic reason for the loss. zures. EEG monitoring should especially be considered Other NIOM teams apply a more graded method to in patients with epilepsy. The spatial distribution of the assess an alert. In other warning criteria described, an electrical field generated by stimulation extends over a 80% amplitude loss is considered sufficient to raise an small region of the head. It does not spread significantly MEP alarm. In another system, the degree of polyphasic to the chest. Therefore, metal in the neck or chest is genturns in the MEP tracing is the focus, and an alert may be erally considered relatively safe. That includes a cardiac raised, for example, if a polyphasic MEP becomes simpacemaker, although in that case anesthesia should monplified to just phases. itor the EKG during MEP stimulation. However, Anesthesia greatly impacts the ability to find MEPs. stimulation-induced cardiac arrhythmia is not likely to MEPs are very sensitive to commonly used inhalation occur. Minor scalp burns are rare. No spinal epidural anesthetics, significantly attenuating or disappearing recording electrode complications are reported for the with use of relatively low levels of halogenated agents D-wave technique. Relative contraindications for MEP or nitrous oxide. Furthermore, neuromuscular blockade monitoring are epilepsy, cortical lesions, convexity skull is ideally avoided, given the need to record stimulationdefects, raised intracranial pressure, cardiac disease, proprovoked EMG responses. The classic rule of thumb is convulsant medications or anesthetics, and cardiac pacethat total intravenous anesthesia (TIVA) is required and makers. Unexplained intraoperative seizures and cardiac neuromuscular blockade must be avoided. Neither of

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Fig. 21.7. Loss of MEPs: A 45-year-old man suffered a thoracic spinal fracture in a bicycle vs auto accident. He was brought to surgery to stabilize his spine with instrumentation. Upon placing a pedicle screw at T6, the MEP from lower extremity sites disappeared. Surgeon was alerted that the screw may have breeched the pedicle medial wall causing spinal cord compression. The screw was removed and repositioned more laterally. The patient later awoke without new motor deficits. Monitoring may have averted an adverse motor outcome. Only the left sided muscles are shown. Right leg muscles showed similar changes. Channels are quadriceps, tibialis anterior and abductor halluces, 10 ms/div, 100–1000 mV/div. Double pulse stimulation artifact is present at the beginning of each trace.

these ideal requirements is absolutely true. In younger patients with robust baseline MEPs and no preexisting neurologic conditions, some inhalation anesthesia can be tolerated, while older patients with preexisting neurologic conditions are less likely to tolerate inhalation anesthetics. A continuous low-dose drip of neuromuscular blockade that allows for a 3 out of 4 train-of-four response can be compatible with MEP monitoring while diminishing bothersome body movement elicited by tce stimulation. While TIVA is compatible with MEP monitoring, it is also not as straightforward as the classical teaching. Propofol is the most commonly used agent for TIVA, but propofol boluses and high-dose continuous infusion can cause MEP amplitude reduction. Therefore, MEP monitoring typically requires a TIVA technique that limits the amount of propofol (or barbiturate) used by employing a second agent such as an opioid (e.g., remifentanil). Opioids have almost no effect on NIOM. D-waves are not affected by neuromuscular junction blockade, since they are direct recordings of the spinal cord. D-waves also are quite stable signals under most anesthetic conditions. Recording electrode movement during surgery can attenuate them. They can be used along with tceMEPs. When neuromuscular blockade is required, they offer a possible method for following motor pathways. Anesthetic fade, as discussed for SEPs, is the gradual cumulative effect of anesthesia reducing evoked potential amplitudes. For MEPs, anesthetic fade becomes more noticeable as the case continues over hours.

Baseline MEPs that are low amplitude and lack polyphasic morphology may be expected to disappear over hours due to anesthetic fade. The clinical decision to raise a tceMEP alert is complex. The decision takes into consideration which muscles changed, how many muscles changed, whether there was a loss of phases within the waveform, the degree of amplitude change (80% loss vs total loss), the qualities of the baseline recordings in those muscles, whether anesthesia fade is occurring, whether inhalation anesthesia has increased, and whether a bolus of centrally active medication was recently given.

ELECTROMYOGRAPHY The EMG can be monitored from limb or trunk muscles during spine surgery. Continuous free-run EMG monitoring can detect neurotonic discharges, or A-trains, which are signs of nerve injury (Daube and Harper, 1989). Free-run EMG can also detect brief bursts and short low-frequency trains of EMG activity that indicate lesser degrees of nerve irritation. Stimulation-triggered EMG is also used to assess placement of pedicle screws. EMG monitoring is conducted in the absence of neuromuscular blockade, or with minimal continuous drip blockade that results in three out of four responses in train-of-four testing.

Recordings Recording is done through needle electrodes inserted into muscles that are innervated by nerve roots or nerves

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that are at risk during surgery. Electrodes are uninsulated over an extended portion of the needle shaft, unlike traditional needle electrodes used in outpatient EMG testing. Real-time EMG is recorded and monitored. Lowfrequency filters are set to 10 Hz, and high-frequency filters are set to 3 kHz to 10kHz. Typically, there is one channel for each muscle recorded. Often 10 or more muscles are monitored with a typical set-up, including roughly five muscles from each limb on the left and right side at the level of surgery. Proximal and distal muscles are selected that represent the regions at risk specific to that surgery. In cervical spine surgery, EMG monitoring is conducted using muscles across the relevant root levels. Commonly chosen muscles include trapezius, deltoid, biceps, triceps, brachioradialis, flexor carpi ulnaris, flexor carpi radialis, abductor pollicis, and abductor digiti minimi. To monitor the upper thoracic region with EMG, electrodes can be carefully inserted into intercostal muscles or placed in paraspinal muscles. For monitoring levels T6 through L1, the rectus abdominal muscles can be monitored using recording electrodes placed at upper, middle, and lower abdominal levels. For lumbosacral surgeries, EMG is recorded in muscles across the relevant root levels. Typical muscles chosen for monitoring often include the iliopsoas, quadriceps, adductor magnus, biceps femoris, tibialis anterior, medial gastrocnemius, extensor digitorum brevis, and flexor hallucis. Needle electrodes in the anal sphincter are added when the conus or cauda equina are at risk during surgery. In cervical surgery, the recurrent laryngeal nerve can be at risk. In this case, vocal cords can be monitored with surface electrodes attached to the sides of the endotracheal tube.

Stimulation When screws are placed into the narrow vertebral pedicles to secure surgical hardware, a misguided screw can create a breach of the medial pedicle wall. When such a breach occurs, the nearby nerve root or spinal cord can be injured. Pedicle screw stimulation testing using stimulation-triggered EMG is performed to assess proper pedicle screw placement. Stimulation can be directed at the hole drilled prior to screw placement by using a probe placed into the hole. Stimulation can also be directly applied to the screw once it is in place. With each stimulation, the EMG recording is triggered to assess whether an EMG response occurs. If the guide hole or screw breaches the medial pedicle wall, low intensity electrical stimulation will activate nearby nerves or the spinal cord and result in a stimulation-triggered EMG response. Fig. 21.8 illustrates a case with a low threshold of EMG response. The lowest stimulation intensity at which an EMG response is elicited with stimulation is

the threshold intensity. At each spinal level, the threshold intensity is determined. A low threshold indicates a likely medial wall breach. In this case, the pedicle screw is removed and redirected. The probability of a breach in the pedicle wall decreases as the threshold intensity increases. The type of screw used can greatly impact the reliability of pedicle screw stimulation data. Screws coated with hydroxyapatite to help bone ingrowth and osseointegration into the screw are not acceptable for reliable stimulation testing, because the hydroxyapatite coating is an electrical insulator. Similarly, titanium screws that have been anodized to produce an electrically insulating titanium oxide coating are not fit for stimulation testing. Both hydroxyapatite and titanium oxide coatings impede electrical conduction from the screw. Polyaxial screw constructs in which a mobile screw head is not firmly connected to the shank can create a gap in conducting material such that electrical conduction cannot bridge the gap. Testing electrical stimulation at the screw head in these circumstances will not necessarily give correct results about a wall breach. Pedicle screw stimulation threshold testing is about 85% accurate in predicting when a medial wall breach occurs. This means there is a roughly 15% false negative rate. While some false negatives may be due to screw deficiencies, there are other potential reasons. If nerves are chronically injured at baseline, it may take a higher stimulation intensity to elicit an EMG response. If the wrong muscles are monitored for the spinal level, no EMG response will be seen to stimulation. Furthermore, at certain levels, such as around L1 or upper thoracic levels, suitable muscles may not be readily available. In cases of the lateral transpsoas approach to the lumbar spine (also known as extreme lateral interbody fusion (XLIF)), stimulation is delivered through a dilator as it is passed through the psoas muscle to the lumbar spine in this minimally invasive procedure. The goal of dilator stimulation is to identify lumbosacral plexus nerves adjacent to the dilator tip to avoid damage to the nerve if the dilator were to be advanced.

Interpretation Free-run EMG is monitored continuously in real time. At baseline, the NIOM team makes note of any ongoing spontaneous irregular background EMG activity. EMG channels typically quiet at baseline. However, spontaneous EMG activity may be present at baseline. This may be due to the underlying pathophysiology that is the cause for the surgery. For example, surgery may be performed for radiculopathy, which is known to cause spontaneous EMG activity from denervation on outpatient EMG testing.

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Fig. 21.8. This 68-year-old had a left L3–L4 lateral transpsoas approach for lumbar stenosis followed by posterior spinal fusion with instrumentation. Electrical stimulation was applied to the right L4 pedicle screw at 8 mA. Local EMG response is seen at the left vastus lateralis, along with secondary movement artifacts at tibialis anterior and medial gastroc muscles, 150 ms/div, 200 mV/div. Stimulus artifact is seen at several channels. This relatively low threshold for EMG response suggested a malpositioned screw. The screw was removed and repositioned.

Irritation or injury to a nerve during surgery can generate activation of motor unit potentials (MUPs) on freerun EMG. A MUP consists of the activation of the muscle fibers innervated by a single axon. Whether a surgical action creates MUPs depends upon the baseline health of the nerve itself and the degree and cause of injury. In general, greater degrees of irritation/injury result in more intense degrees of EMG activity. For example, during nerve root manipulation, a minor brief EMG burst of polyphasic activity might be seen, corresponding to the brief summation of multiple MUPs. An EMG train can last seconds to minutes and consists of repetitive firing of one or more motor units. If the degree of irritation is relatively low, each MUP can be distinguished by its unique morphology and firing rate. With higher levels of irritation/injury, the EMG can fill up with so many MUPs that individual MUP waveforms cannot be distinguished, similar to the classic

“interference pattern” seen during diagnostic EMG testing. When a surgeon causes mechanical compression or stretches a nerve or root, such as when placing a retractor too close to a nerve, a MUP train may be seen. A greater degree of compression or stretching can result in a continuous EMG interference pattern. A classical sign of more acute irritation or injury is a neurotonic discharge, or A-train, which is a dense, high-frequency EMG discharge often lasting 30–45 s (Daube and Harper, 1989). Overall, short bursts and low-frequency MUP trains suggest minor irritation and a low risk of persisting nerve injury. Trains that persist beyond the provoking surgical action are considered significant and suggest some degree of ongoing injury. Pedicle screws are stimulated at constant current up to 20 mA for lumbar lower intensities at more rostral levels. Fig. 21.8 illustrates muscle response recorded during a stimulation test. As discussed earlier, a stimulus intensity

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Fig. 21.9. EMG discharges warn of impending nerve injury: A 37-year-old with a left L4–L5 disc herniation underwent a minimally invasive microdiscectomy. (A) On baseline free-run EMG, spontaneous firing of two different MUAPs was noted in the left TA-MG channel. Each motor unit action potential (MUAP) has a different morphology, with one being triphasic and the other being biphasic. (B) A dense firing of the MUAPs was reported during decompression, a neurotonic discharge. In response to the EMG warning, the surgeon altered his approach near the nerve root. (C) Subsequently, the EMG train slowed down and individual MUAPs can again be appreciated after the source of nerve root irritation was removed. AH: abductor halluces, MG: medial gastrocnemius, Rect Fem: rectus femoris, TA: tibialis anterior, Vas Med: vastus medialis.

threshold is determined for each screw site. At lumbar and lower thoracic spinal levels, a threshold of 10 mA or greater is generally considered adequate for confirming proper screw placement. A threshold of 5 mA or lower is considered a sign of pedicle wall breach. Values for thresholds are lower for higher spinal levels, such as in the cervical spine. Osteoporosis can produce a false positive stimulation threshold because the poorly mineralized bones create lower thresholds for evoking EMG responses. EMG monitoring identifies most but not all intraoperative nerve injuries. If the EMG is not watched consistently, a neurotonic discharge may appear briefly, disappear, and be overlooked by the monitoring technologist and physician. Fig. 21.9 illustrates a case with a neurotonic discharge. Not all nerve injuries will elicit an EMG discharge. For example, a nerve that is cleanly cut may generate no EMG discharges (Crum and Strommen, 2007). A chronically injured nerve may have a higher threshold for the level of irritation needed to generate discharges. Since compressed or chronically injured nerves are those for which surgery most often is undertaken,

EMG monitoring may fail to detect some intraoperative compressive, mechanical, or ischemic nerve injuries. Nevertheless, EMG monitoring is useful because it detects most nerve injuries, even though it does not identify about 15% of them. For lateral transpsoas dilator stimulation, the dilator is stimulated repeatedly as the instrument is advanced in small increments while stimulation-triggered EMG is recorded and monitored real time for muscle responses. Stimulations should not provoke EMG responses except for the local direct response of the psoas muscle itself. To avoid false negatives, the muscles selected for EMG monitoring should be relevant to the level through which the dilator is passed. The team should also be cognizant of the fact that nerves from higher lumbar levels also may be encountered as the dilator passes through the psoas. Monitoring from too few muscles may miss important EMG responses to stimulation. A disadvantage of this technique is that it assesses motor pathways only and does not monitor function of sensory or autonomic nerves. The lower the current intensity needed to trigger an EMG response, the closer the dilator is to a motor nerve.

SPINAL CORD MONITORING Table 21.1 Neurologic outcome prediction rates for SEP monitoring in spinal surgery Total procedures monitored 51,263

(100%)

False-negative (FN) rate: neurologic postoperative deficits despite stable SEPs Definite 34 (0.063%) Equivocal 13 (0.025%) Delayed onset 18 (0.035%) Total: 65 (0.127%) False-positive rate: no neurologic deficits despite SEP changes Definite 504 (0.983%) Equivocal 270 (0.527%) Total: 774 (1.510%) True-positive (TP) rate: neurologic deficits predicted by SEP changes Definite 150 (0.293%) Equivocal 67 (0.131%) Total: 217 (0.423%) Neurologic deficits (FN plus TP) Definite 184 (0.356%) Equivocal 80 (0.156%) Delayed Onset 18 (0.035%) Total: 282 (0.550%) True-negative rate: no neurologic deficit and stable SEPs Total: 50,207 (97.94%) These data are from the multicenter outcome study of SEP spinal cord monitoring by 153 US surgeons (Nuwer et al., 1995). Note the very low rate of definite false negative cases (0.063%). Equivocal cases were transient or minor degrees of impairment. Delayed onset cases awoke from surgery intact but developed impairment within the first day postoperatively.

SPINAL CORD MONITORING SEP and MEP techniques monitor the spinal cord and most often are used together. SEP monitoring is performed continuously, whereas MEPs are tested intermittently as needed. MEP techniques have some disadvantages, such as stimulation-related movement and high sensitivity to inhalation agents and neuromuscular blockade. Therefore, some spinal cord surgery cases are monitored with SEP alone. Alerts without postoperative neurological deficits are considered false positives. However, many of these “false positives” may be true detections of neurologic risk, and the lack of postoperative deficit occurs because the surgeon responds to the alert. Therefore, these could be considered true save events. False alerts and true saves cannot be differentiated methodologically. However, animal literature shows that failure to respond to an SEP alert is associated with high risk of a postoperative deficit, while responding to alerts prevents postoperative deficits (Kojima et al., 1979; Nordwall et al., 1979; Coles

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et al., 1982; Laschinger et al., 1982; Bennett, 1983). Such literature strongly supports the conclusion that NIOM is effective in reducing postoperative deficits. False negatives in NIOM occur when a patient awakens with a new neurologic deficit despite no NIOM alert. False negatives occur very rarely during spinal cord monitoring (Nuwer et al., 1995) (Table 21.1). In clinical practice, SEPs and MEPs detect spinal cord impairment relatively early in the course of complications, so that a surgeon’s response to alerts can avert many deficits. The American Academy of Neurology and American Clinical Neurophysiology Society published an evidence-based assessment of the utility of NIOM in spinal cord monitoring (Nuwer et al., 2012). Their analysis of the literature included class 1 and 2 studies of MEP and SEP alerts (May et al., 1996; Jacobs et al., 2000; Pelosi et al., 2002; Langeloo et al., 2003; Hilibrand et al., 2004; Etz et al., 2006; Lee et al., 2006; Khan et al., 2006; Costa et al., 2007; Sutter et al., 2007; Weinzierl et al., 2007). The joint assessment concluded, upon a methodical review of the published evidence, that NIOM is effective at predicting an increased risk of new postoperative paraparesis, paraplegia, and quadriplegia from spinal surgery. This publication furthermore recommended intervention in response to alerts to attempt to reduce the risk of adverse neurologic outcomes. A large multicenter study (Nuwer et al., 1995) analyzed over 100,000 spinal surgery cases performed by 184 surgeons over 7 years. Of these cases, half were performed with concurrent NIOM. Outcomes were compared between cases with and without monitoring, and outcomes in monitored cases were compared against historical controls for the same cohort. NIOM was associated with a 60% reduction in postoperative paraparesis and paraplegia. False negative cases occurred in less than 0.1% of cases. Sala et al. (2006) used historical controls and assessed postoperative motor exam changes with McCormick grading. The aggregate grade increased by +0.28 in monitored patients, whereas without NIOM it worsened by 0.16 (P < 0.002). Studies have assessed the benefits of SEP and MEP monitoring, but no definitive comparison has been done. SEPs have some advantages. SEPs are monitored continuously, while MEPs are monitored intermittently. MEPs generate movements, so some surgeons use them sparingly. However, clearly preservation of motor function is a priority, which is assessed through MEPs. Since SEPs and MEPs monitor different spinal pathways in anatomically different locations within the cord, both are typically monitored. Use of MEPs and SEPs together is also ideal for detecting cord ischemia since their spinal cord pathways have different blood supplies (anterior spinal artery and posterior spinal arteries,

342 M.R. NUWER AND L.M. SCHRADER respectively). Furthermore, some reports show signifineurophysiologist has extended specialized training in cant MEP changes a few minutes before clinically signifclinical neurophysiology and NIOM. This experienced icant SEP changes are noted. subspecialist brings to the case knowledge about NIOM literature and lore, experience in communicating effectively in the OR setting, skills in technological troubleSTAFFING shooting, and experience with many events as they NIOM requires a knowledgeable, experienced team for may occur during cases. both technical skills and clinical assessments. Staffing The monitoring neurophysiology physician may for NIOM services includes individuals with three levels supervise remotely from a location outside of the OR of skills, knowledge, ability, training, and experience: (Nuwer et al., 2013). Physicians who remotely monitor (A) A technologist applies the electrodes and sets up must have continuous communication with the operating room. The simple remote monitoring method involves and runs the equipment. If the monitoring professional screen displays that show only what the technologist is remote, the technologist establishes internet connectivselects on the operating room equipment screen. ity and assists with communication. A trained, certified Advanced remote monitoring allows the neurophysioloEEG technologist usually performs this role. In the gist to change among various screen displays of the data United States, the recognized national technologist’s cerand to manipulate the data. The advanced method allows tificate is Certified in Neurophysiologic Intraoperative the monitoring physician to monitor at his or her discreMonitoring (CNIM). (B) A professional with significant tion all aspects of the case, rather than being restricted to knowledge, training, and experience in intraoperative what the technologist chooses to display. The advanced monitoring assists the technologist in decision making method is preferred because it allows for a more detailed and problem solving, and trains technologists to perform and thorough assessment of multiple aspects of data and their jobs well. (C) A licensed physician, knowledgeable allows the physician to see a temporal sequence of differin both neurophysiology and medicine, aids in the ent aspects of an evolving clinical situation. establishment of reliable baseline data, monitors the data Alternatives to traditional NIOM include (a) automated continuously, makes determinations about alerts, and monitoring, (b) surgeon-directed monitoring, discusses the meaning of changes. The physician is in (c) technologist-directed monitored, and (d) proctored monthe best position to recommend adjustments in anesthesia itoring. Automated monitoring utilizes a computerized or surgery, wake-up testing, or medical interventions. algorithm to search recorded signals, score peaks for desired The physician integrates NIOM data with the patient’s criteria, and identify if alert criteria are met. In this method, medical history and adds medical quality assurance. Of no person checks the computer’s assessment, and the data the three roles described, one person may serve in more itself may not be readily available for an expert’s review. than one role. For example, some physicians who are sufSurgeon-directed monitoring is not ideal because the ficiently expert in NIOM may serve both the second and surgeon is generally not trained in the technical details, third roles. Other times, a highly skilled nonphysician problem solving, artifact elimination, how to improve PhD neurophysiologist may fill the second role, while recording quality, or the monitoring literature and lore. a physician fills the third role. The surgeon is busy operating and therefore is not able In general, the tasks of interpreting and problem solvto pay on-going attention to the tracings. Technologisting during the neurophysiologic monitoring are not perdirected monitoring without a neurophysiologist supervisor formed by the operating surgeon or anesthesiologist. is also suboptimal, because many technologists are not Rather, this duty is performed by a third physician, a neufamiliar with the literature and lore of the monitoring rophysiologist who is able to devote full attention to field and are not in a position to answer questions about problems that require detailed time and effort. Neurowhy signals changed, and they often monitor in a simple physiologists make various clinical decisions during cookbook fashion. Unsupervised technologists may misNIOM. Of obvious importance is decision making about take real clinical changes for technical problems and may whether developing NIOM changes require an alert to fail to raise timely alerts. the surgeon. This decision involves integration of NIOM Proctoring differs from traditional active monitoring. findings with anesthetic and surgical events. The neuroMonitoring involves ongoing attention to the recorded physiologist also helps ensure optimal usefulness of signals, whereas proctoring dilutes the supervision of monitoring conditions by determining whether the neuthe recorded signals by dividing attention among many rophysiological testing needs to be modified to meet simultaneous cases or leaving the screen unattended the individual patient’s clinical circumstances. Neurowhile providing other patient care. The proctoring phyphysiologists also work to improve quality of recordings sician may supervise 4–10 online simultaneous cases, by eliminating artifacts, optimizing technical set-up, and dividing attention among all cases. The technologist overcoming other technical problems. The physician

SPINAL CORD MONITORING screens for significant events and brings them to the proctoring physician’s attention for advice or intervention. In contrast, the traditional monitoring neurophysiology physician supervises one or a few cases, e.g., one to three simultaneously (American Clinical Neurophysiology Society, 1994). The traditional monitoring model allows for substantial attention to each case’s recorded signals. This monitoring physician actively participates and may identify changes that the technologist missed. Multiple screens are available for each case, and the monitoring physician changes screens as the case progresses. The actively monitoring physician can evaluate in real-time multiple pages of recorded data different from what the technologist is viewing. This brings to bear useful extra attention and decision making to the case. When one case requires individual attention, a physician supervising simultaneous cases remotely must turn over the additional cases to a colleague. Physicians who monitor at their local hospitals typically supervise one case, and one-quarter of the time supervise two or three simultaneous cases (29). Physicians who remotely monitor multiple distant hospitals supervise four or more simultaneous cases one-quarter of the time, and during busier times the caseload could exceed six simultaneous cases. Surgeon-directed monitoring is a form of proctoring, because the surgeon does not pay attention to the recorded signals throughout the case. Many surgeons also are insufficiently trained to distinguish technical problems from clinical changes. An unfortunate example of surgeondirected monitoring claimed a failure of MEP spinal cord monitoring (Modi et al., 2009). The patient awoke paraplegic despite preserved lower extremity MEPs in a thoracic surgery case, a supposed false negative MEP monitoring. Published figures showed that the arms and legs were reversed in the technical set-up, so the case actually was a true positive MEP alert. The case lacked a neurophysiology team to assist the surgeon by reviewing the set-up and data, which quickly would have detected the obvious mixup. Neurophysiology teams are needed in monitoring, to bring to the case the substantial skills, knowledge, ability, training, and experience to set up, recognize, and correctly interpret monitoring tracings.

SUMMARY Intraoperative neurophysiologic monitoring involves real-time recording and interpretation of SEP, MEP, and EMG. SEP provides new data continuously, whereas MEP is run intermittently. Anesthesia choice is constrained by both, more strictly by MEP. EMG is used to check pedicle screw placement for medial wall breach, although occasional breach or nerve impingement is undetected. Monitoring requires a technologist in the

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room and the supervision of a neurophysiology physician who is in-room or remote. Techniques are now known for obtaining quality recordings in a variety of spinal surgical settings. In traditional experienced hands, spinal cord monitoring reduces the risk of paraplegia and paraparesis by 60%.

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MacDonald DB (2002). Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol 19: 416–429. May DM, Jones SJ, Crockard HA (1996). Somatosensory evoked potential monitoring in cervical surgery: identification of pre- and post-operative risk factors associated with neurological deterioration. J Neurosurg 85: 566–573. Modi HN, Suh SW, Yang JH et al. (2009). False-negative transcranial motor evoked potentials during scoliosis surgery causing paralysis. Spine 34: E896–E900. Nordwall A, Axelgaard J, Harada Y et al. (1979). Spinal cord monitoring using evoked potentials recorded from feline vertebral bone. Spine 4: 486–494. Nuwer MR, Dawson EG (1984). Intraoperative evoked potential monitoring of the spinal cord: enhanced stability of cortical recordings. Electroencephalogr Clin Neurophysiol 59: 318–327. Nuwer MR, Dawson EG, Carlson LG et al. (1995). Somatosensory evoked potential spinal cord monitoring reduces neurologic deficits after scoliosis surgery: results of a large multicenter survey. Electroencephalogr Clin Neurophysiol 96: 6–11. Nuwer MR, Comi ERG et al. (1998). I.F.C.N. standards for digital recording of clinical EEG. Electroencephalogr Clin Neurophysiol 106: 259–261. Nuwer MR, Emerson RG, Galloway G et al. (2012). Evidence-based guideline update: intraoperative spinal monitoring with somatosensory and transcranial electrical motor evoked potentials. J Clin Neurophysiol 29: 101–108. Nuwer MR, Cohen BH, Shepard KM (2013). Practice patterns for intraoperative neurophysiologic monitoring. Neurology 80: 1156–1160. Pelosi L, Lamb J, Grevitt M et al. (2002). Combined monitoring of motor and somatosensory evoked potentials

in orthopaedic spinal surgery. Clin Neurophysiol 113: 1082–1091. Sala F, Palandri G, Basso E et al. (2006). Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery 58: 1129–1143. Schwartz DM, Sestokas AK, Hilibrand AS et al. (2006). Neurophysiological identification of position-induced neurologic injury during anterior cervical spine surgery. J Clin Monit Comput 20: 437–444. Sutter M, Eggspuehler A, Grob D et al. (2007). The validity of multimodal intraoperative monitoring (MIOM) in surgery of 109 spine and spinal cord tumors. Eur Spine J 16: S197–S208. Weinzierl MR, Reinacher P, Gilsbach JM et al. (2007). Combined motor and somatosensory evoked potentials for intraoperative monitoring: intra- and postoperative data in a series of 69 operations. Neurosurg Rev 30: 109–116. Yellin JL, Wiggins CR, Franco AJ et al. (2016). Safe transcranial electric stimulation motor evoked potential monitoring during posterior spinal fusion in two patients with cochlear implants. J Clin Monit Comput 30: 503–506.

FURTHER READING Cheng MK, Robertson C, Grossman RG et al. (1984). Neurological outcome correlated with spinal evoked potentials in a spinal cord ischemia model. J Neurosurg 60: 786–795. Cunningham Jr JN, Laschinger JC, Spencer FC (1987). Monitoring of somatosensory evoked potentials during surgical procedures on the thoracoabdominal aorta. IV: clinical observations and results. J Thorac Cardiovasc Surg 94: 275–285.