Evoked Response Monitoring

CHAPTER 6

Evoked Response Monitoring Antoun Koht1, Tod B. Sloan2 1

Northwestern University Feinberg School of Medicine, Chicago, IL, United States; University of Colorado School of Medicine, Aurora, CO, United States

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Contents Introduction Basic Principles General Overview of Monitoring Auditory Brainstem Response Monitoring Other Cranial Nerves Somatosensory Evoked Potentials Motor Evoked Potentials Electromyography Other Specialized EMG Responses Understanding the Equipment Stimulation, Wiring, and Connections Recording, Electrical Contaminations, and Storage Indications and Contraindications Monitoring and Mapping for Brain Tumors Monitoring for Cerebral Vascular Lesions

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Intracranial Vascular Surgery Interventional Vascular Procedures

Brainstem Procedures Monitoring Spinal Corrective Surgery Intramedullary Spinal Tumors Monitoring the Lumbosacral Spine Thoracic Aorta Aneurysm Surgery Contraindication for Monitoring Effect of Anesthetics Effects of Inhalation Agents Effects of Intravenous Agents Effects of Adjunct Medications Readings and Interpretation Advantages and Disadvantages Current Evidence Conclusion Suggested Readings References

Neuromonitoring Techniques ISBN 978-0-12-809915-5 http://dx.doi.org/10.1016/B978-0-12-809915-5.00006-1

© 2018 Elsevier Inc. All rights reserved.

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INTRODUCTION Monitoring of the central nervous system using evoked responses allows assessment of neural tracts that are normally silent during coma or anesthesia. This differs from the electroencephalogram (EEG), which monitors spontaneous activity. They are not a replacement for awake testing such as performed during awake craniotomy or under local anesthesia, but they allow examination during general anesthesia. This chapter will discuss the techniques of the auditory brainstem response (ABR), somatosensory evoked potential (SSEP), motor evoked potential (MEP), electromyography (EMG), and a few related techniques. These have been applied widely in a large number of surgical and neuroradiological procedures and are a standard of care in selected procedures.1e9 The implications for anesthesia management will be mentioned as the anesthesiologist plays a key role in facilitating the monitoring.

BASIC PRINCIPLES General Overview of Monitoring Using these techniques, a stimulus is applied to the neural tract, and a response is “evoked” that indicates the tract is functioning. This allows probing tissue to locate or “map” the tract, and it allows repeated testing of a tract during procedures to identify conditions of impending neural injury (“monitoring”). This allows improved decision-making during procedures and facilitates improved outcome. It also allows an assessment of the physiological environment of the neural tissue (e.g., perfusion pressure) to facilitate improved outcome. In general, evoked responses are measured along the neural tract after the stimulus is applied. The response consists of series of peaks, each of which is produced by the neural tissue in the tract. For mapping, the presence of the response indicates that the tract has been located in the vicinity of the stimulator. For monitoring, repeated measurements are taken to watch for significant peak changes. Changes are usually noted from peak measurements such as the time from stimulation to the peak (referred to as “latency”) and the “amplitude” of the peak as measured to an adjacent peak of opposite polarity. Frequently, several monitoring techniques are utilized during procedures recognizing risk in multiple areas (“multimodality monitoring”).

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Auditory Brainstem Response The ABR is produced when the cochlea is stimulated using sound delivered into the external ear canal.2,10e12 It has also been referred to as the brainstem auditory evoked response (BAER) and the brainstem auditory evoked potential. Traditionally, broad-spectrum “clicks” are used with white noise (like a television tuned to an empty channel) delivered to the opposite ear to prevent the other cochlea from being activated by sound vibrations transmitted through the skull. The response of the eighth cranial nerve can be measured using electrodes placed during surgery on the nerve or near the cochlear nucleus; however, it is usually monitored using electrodes at the external ear and top of head. The response consists of a series of five peaks produced within the 10 ms following stimulation. The latency of peaks I, III, and V and the amplitude of peak V are usually monitored. Wave I is produced by the extracranial portion of CN VIII, wave III by acoustic relay nuclei and tracts deep in the midline of the lower pons, and wave V by the lateral lemniscus and inferior colliculus contralateral to the side of stimulation (Fig. 6.1).11

Figure 6.1 Normal auditory brainstem response tracing and corresponding region of brainstem generating the response peaks (labelled by Roman numerals by convention). I, organ of Corti and extracranial cranial nerve VIII; II, cochlear nucleus; III, superior olivary complex; IV, lateral lemniscus; V, inferior colliculus; VI, medial geniculate body; VII, auditory radiation. (From Aravabhumi S, Izzo KL, Bakst BL, et al. Brainstem auditory evoked potentials: intraoperative monitoring technique in surgery of posterior fossa tumors. Arch Phys Med Rehabil 1987;68:142.)

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The response of the auditory cortex is referred to as the midlatency auditory evoked potential (MLAEP). Experience has shown that increases in latency of 10% or more of peaks (or between peaks, interwave latency), decrease in peak amplitude of more than 50%, or loss of peaks is associated with significant dysfunction in the pathway, which correlate with changes in useful hearing.13 Hence the ABR is used to reduce the risk of hearing loss in surgery in the cerebellopontine angle of the brainstem. It has also been used as a general monitor of brainstem viability during surgery on the midbrain and pons. The MLAEP has been used as a measure of anesthetic effect but is rarely used for procedural monitoring.

Monitoring Other Cranial Nerves The ABR is the only evoked sensory response testing routinely utilizing a sensory cranial nerve. Methods for testing the olfactory nerve (CN 1) have not been adequately developed for monitoring. Methods for monitoring the evoked response of the optic nerve (CN 2) (visual evoked potentials) have been developed using flash stimulation to closed eyes; however, routine use has not found utility similar to ABR. Finally, methods for evoked response testing of the trigeminal nerve (CN 5) have been developed and are occasionally used.

Somatosensory Evoked Potentials The somatosensory evoked potential (SSEP) is one of the most commonly monitored evoked responses.6,14 The response is produced by applying an electrical stimulus to a peripheral nerve (much like that used for assessing train of four for neuromuscular blockade). The nerves (and their component nerve roots) usually utilized for monitoring are major motor and sensory nerves to the hands and feet (median n. (C6-T1), ulnar n. (C8-T1), and posterior tibial n. (L4-S2)). Stimulation activates large-diameter, fast-conducting Ia muscle afferent fibers producing a muscle movement and group II cutaneous nerve sensory fibers that produce cephalad traveling SSEP signals. The major sensory response travels through the component roots of the nerves in the brachial and lumbar plexus15 (Fig. 6.2). Entering the spinal cord via the dorsal root, the response ascends the spinal cord via the dorsal columns in the pathway of joint proprioception and vibration. A first synapse occurs near the nucleus cuneatus and nucleus gracilis, and it ascends

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Figure 6.2 The SSEP response is produced by stimulation of the peripheral nerve (arrow). The response in the nerve can be recorded (shown is a response recorded at the popliteal fossa from posterior tibial nerve stimulation). The response ascends through the dorsal spinal columns and can be recorded epidurally over the cervical spine and over the sensory cortex. (From Jameson LC, Sloan TB. Monitoring of the brain and spinal cord. Anesthesiol Clin 2006;24:777.)

the brainstem in the medial lemniscus after crossing the midline. After a second synapse in the ventroposterolateral nucleus of the thalamus, it travels to the primary somatosensory cortex contralateral to the side of stimulation. For mapping purposes, stimulation of the posterior surface of the spinal cord can be used to locate the midline, and recording on the surface of the brain can be used to locate the gyrus between the sensory and motor cortex. For procedure monitoring, the response can be monitored along the peripheral nerve (verifying stimulation similar to seeing the motor response), over the brachial plexus (Erb point), epidurally near the spinal cord, and, most commonly, over the cervical spine (referred to as the subcortical response) and over the sensory cortex.15 Monitoring has been used for surgery on peripheral nerves and plexus, monitoring for unfavorable positioning of the arm (brachial plexus), spine procedures, general brainstem viability, and procedures placing the subcortical and cortical pathways at risk. Experience indicates that more than 50% decrease in amplitude of response peaks or increase in latency of 10% or more are associated with concerns of unfavorable neural environment.

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Motor Evoked Potentials MEP are the most recent addition to the techniques used for monitoring. Of the various methods that have been used to stimulate the motor pathways, electrical stimulation of the motor cortex has emerged as the most commonly used technique that unquestionably allows motor tract assessment.4,15e17 The pyramidal cells of the motor cortex can be stimulated directly through a craniotomy (direct cortical stimulation); however the most commonly employed technique utilizes multipulse electrical stimuli applied via scalp electrodes (transcranial motor evoked potentials, TcMEP). Enhanced stimulation techniques have also been developed using a priming stimulus prior to the main stimulus to assist in young children, adults with neural pathology, and with partial neuromuscular blockade.18 Transcranial stimulation utilizing a brief magnetic stimulation has largely been abandoned due to depression by anesthesia. This technique activates 4%e5% of the fast-conducting fibers of the cortico-spinal tract (CST), which descends the brain, brainstem (crossing in the brainstem), and spinal cord until it synapses on anterior horn cells15 (Fig. 6.3). The descending response in the spinal cord consists of a D wave from the direct stimulation of the motor cortex and is considered an approximation of the volume of motor pathway activated. Its amplitude varies less than 10%. I waves accompany the D wave and represent the contribution of the response from transsynaptic activation of internuncial pathways in the motor cortex. I waves are sensitive to anesthesia. Temporal summation of the D wave and I waves activates the anterior horn cells to produce a response in motor fibers of lower motor neurons. This response travels to the neuromuscular junction and produces a compound muscle action potential (CMAP) in about 4%e5% of muscle fibers.19 Not all of the descending spinal fibers directly innervate anterior horn cells; many have intervening synapses. In addition, several other motor pathways are either activated or influence the sensitivity of the anterior horn cell to activation. These additional synapses and other pathways give rise to wide variability of the CMAP produced under anesthesia. Of note, individual muscles are often innervated by muscle fibers from more than one nerve root. MEP stimulation techniques can be utilized for mapping of the location of the motor cortex, and for the location of the CST in the subcortical tissue, brainstem, and spinal cord. The MEP response can be monitored utilizing an epidural electrode (monitoring the D wave) or using electrodes placed in peripheral muscles (monitoring the CMAP). The most commonly

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Figure 6.3 Motor evoked potentials are produced by stimulation of the motor cortex (arrow). The response can be recorded epidurally over the spinal column as a D wave followed by a series of I waves. The pathway synapses in the anterior horn of the spinal cord, and the response travels to the muscle via the neuromuscular junction (NMJ). The response is typically recorded near the muscle as a compound muscle action potential (CMAP). (From Jameson LC, Sloan TB. Monitoring of the brain and spinal cord. Anesthesiol Clin 2006;24:777.)

monitored muscles include those of the distal upper (e.g., abductor or flexor pollicis brevis) and lower extremity (e.g., abductor hallucis brevis and tibialis anterior), although muscles related to specific spinal cord regions can be used. Since the MEP has good correlation with motor outcome, it has been used to monitor motor cortex and general brainstem viability and procedures on the spine and spinal cord. It is frequently monitored along with SSEP, where it is thought to be more sensitive than the SSEP to ischemia in areas of the cortex, brainstem, and spinal cord.15,20 Because of the stability of the D wave, a 50% reduction in amplitude has been used as criteria for concern. However, the wide variability of the CMAP response has created controversy about warning criteria. Suggestions have included changes in the configuration of the multipeaked CMAP response (indicating changes in the motor units responding), the need for increased cortical stimulation voltage (50e100 V) or current, and very

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substantial declines in the CMAP amplitude (i.e., >70%). One of the most commonly utilized MEP criteria is simply the loss of a CMAP response.

Electromyography Electromyography (EMG) is the recording of activity using needle pairs placed in muscles.5,21,22 This differs from MEP in that the muscle responses are spontaneous or evoked by stimulation of cranial or peripheral nerves rather than central motor stimulation of the cerebral cortex. Two basic types of recording are used. Electrical stimulation of nerves leading to a muscle response is referred to as triggered EMG and is used to map the location or assess the continuity of nerve structures. The second type of recording is referred to as spontaneous or “free-run” EMG. In this case, muscle activity is seen in a usually silent background caused by other forms of stimulation such as mechanical or thermal irritations. Some of these stimuli are usually innocuous (e.g., inadvertent mechanical irritation); however, some are potentially injurious and signal the need to reassess the procedure (e.g., nerve stretching). In addition to seeing the response on the recording device, the response may be played on a loudspeaker. The nerves innervating the muscles involved in EMG recording include cranial and peripheral nerves. For cranial nerves, any nerve with a motor component can potentially be monitored using the muscles innervated by the nerve (Table 6.1). Mapping techniques have been developed to locate cranial nerve nuclei and the cranial nerve as it traverses the brainstem to the muscles recorded. Mapping of cranial nerve nuclei on the brainstem surface allows surgeons to approach deeper structures through designated safe entry zones.23

Table 6.1 Cranial nerve EMG monitoring Cranial Nerve Muscles used for monitoring and mapping

III IV V VI VII IX X XI XII

Oculomotor Trochlear Trigeminal Abducens Facial Glossopharyngeal Vagus Spinal accessory Hypoglossal

Superior, medial, inferior rectus Superior oblique Masseter Lateral rectus Orbicularis oculi, oris, mentalis Stylopharyngeus muscle (posterior soft palate) Vocal folds Trapezius, sternocleidomastoid Tongue

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Monitoring usually involves repeated intermittent stimulation in the operative field. Techniques which are not dependent on the surgeon providing the stimulation have been developed that are similar to MEP where transcranial stimuli evoke the muscle activity, thereby allowing monitoring independent of surgical stimulation (corticobulbar techniques).24,25 Such techniques have been described for facial nerve and vagus/recurrent laryngeal nerve monitoring. This latter technique also allows assessment of the cranial nerve function proximal to the surgical site. For peripheral nerves a large number of muscles can be used depending on the specific nerve root desired (Table 6.2). For these nerves, mapping can be utilized in injured peripheral nerves (neuroma in continuity) or to assess locations of injury in brachial plexus lesions. Mapping is also used to identify component rootlets of nerve roots to be sacrificed in dorsal rhizotomy for spasticity.26 Mapping is also used in surgery on the cauda equina (e.g., release of tethered cord) to identify functional nerve tissue to be preserved and nonfunctional tissue for sacrifice. Finally, as discussed subsequently, pedicle screw testing is a form of mapping the proximity of screws to nerve roots. Monitoring of peripheral nerves using EMG is frequently done to identify the injurious stimuli mentioned earlier during procedures where nerve roots, the cauda equina, or peripheral nerves are at risk. Of note, when a particular nerve root is at risk, monitoring using intermittent triggered EMG of that root is more frequently utilized than free-run EMG since muscles used with MEP are usually innervated by more than one nerve root. Table 6.2 Peripheral nerve roots and muscles commonly monitored Spinal cord nerve(s) Muscle(s)

Cervical

Thoracic

Lumbar Lumbosacral Sacral

C2-4 C5-6 C6-7 C8-T 1 T2-6 T5-T12 L2 L2-4 L4-S1 L5-S1 S1-2 S2-4

Trapezoids, sternocleidomastoid Biceps, deltoid Flexor carpi radialis Adductor pollicis brevis, abductor digitiminimi Specific intercostals Specific areas of rectus abdominis Adductor longus Vastus medialis Tibialis anterior Peroneus longus Gastrocnemius Anal sphincter

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Several forms of evoked response can be seen in EMG. Triggered responses are usually brief CMAP responses linked in time to the stimulus as mentioned before. Free-run EMG has two basic forms of response27,28 (Fig. 6.4). High-frequency CMAP bursts can identify blunt mechanical trauma or irritation to motor nerves. Causes of irritation include mechanical stimulation (e.g., nearby dissection; ultrasonic aspiration or drilling), nerve retraction, thermal irritation (e.g., heating from irrigation, lasers, drilling, or electrocautery), and chemical or metabolic insults. More continuous EMG activity is referred to as “trains”or “neurotonic discharges,” and may be associated with impending nerve injury (nerve compression, traction, or ischemia of the nerve). When played on a

Figure 6.4 Examples of continuously recorded muscle potentials during posterior fossa surgery. Responses are recorded from the orbicularis oculi, orbicularis oris, and mentalis muscles. Top, Multiple short responses (neurotonic bursts) in the mentalis muscle from dissection near the fifth cranial nerve. Bottom, Prolonged neurotonic discharges in the other muscles after irrigation with cool fluids. (From Cheek JC. Posterior fossa intraoperative monitoring. J Clin Neurophysiol 1993;10:412.)

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loudspeaker, they have musical qualities like the sound of an outboard motor boat engine, swarming bees, popping corn (“popcorn”), or an aircraft engine (“bomber”) potentials. These neurotonic discharge trains raise concern for nerve injury as does very high amplitude bust responses. Unfortunately, nerve injury can occur without EMG activity such as when the nerve is severed.

Other Specialized EMG Responses A specialized type of triggered EMG response is reflex testing.5 In this case the stimulus is applied to a peripheral sensory nerve that sends a volley of activity to the spinal cord via the dorsal root. It triggers reflex pathways in the spinal cord that activates motor fibers in the ventral root and peripheral nerve resulting in a CMAP. Three CMAP responses can be seen. The first “M” response is from direct activation of motor fibers in the stimulated nerve (like used for train of four assessment). The second “Hoffmann” (H) response is the reflex response.29 The last is an “F” response that is produced by the reflection of the incoming sensory volley at the spinal cord that sends a motor response back to the muscle via the stimulated nerve. Of note, the H reflex pathway in the spinal cord is dependent on normal cephalad spinal cord function. As such, a spinal cord injury will depress the H reflex activity caudal to the injury, even when the reflex occurs in uninjured spinal cord. As such the H reflex has been used in spinal surgery as a measure of spinal integrity cephalad to the region of reflex.30,31 Another commonly utilized reflex is the bulbocavernosus reflex.32 This reflex results from stimulation of the pudendal nerve at the genitalia, reflex activity in the S2eS4 spinal cord segments, and efferent activity also via the pudendal nerve resulting in a CMAP in the external anal sphincter. This has found utility for testing during cauda equina surgery to preserve neural innervation of the bowel and bladder, which travel in the pudendal nerve.

UNDERSTANDING THE EQUIPMENT Equipment for conducting evoked response mapping and monitoring largely emerged in the 1960s and 1970s when digital computers became widely available. As such, the current equipment usually consists of a digital computer connected to a set of stimulating devices, a set of recording amplifiers, a display, and a storage device. The technology is sufficiently complex that a dedicated professional is needed to conduct the technological component of the mapping and monitoring. In addition, the

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equipment usually has the capability of HIPPA-compliant real-time data transfer to a remote computer for shadow observation and consultation by another monitoring professional. Since the equipment is electrically connected to the patient, methods to prevent electrical risk to the patient are employed, and the equipment is routinely checked for leakage current similar to other equipment in the procedure room.

Stimulation, Wiring, and Connections As before, each type of evoked response testing requires specialized stimulation devices. The specifics of each stimulator device applied to the patient and the electrical characteristics of the stimulation are designed for the specific response being tested.

Recording, Electrical Contaminations, and Storage The response is recorded from electrodes attached to the patient and amplified prior to being processed by the digital computer. Since the responses are very small compared to other physiological signals (e.g., the electrocardiogram and EEG), a preamplifier is usually placed near the patient, and other efforts are made to reduce the interference of other signals. The processing of the signal usually involves filters to remove frequencies of electrical activity not characteristic for the response being measured and conversion to digital data for processing and storage. The conversion to digital information is particularly important for signal averaging required for the ABR and SSEP. For these responses, their very small size requires that many signals be averaged by adding the responses time locked to the stimulus. The need for this signal averaging is why the routine application of SSEP testing awaited the availability of digital computers. For responses, such as muscle CMAP, which are very large compared to the background noise, signal processing is not required, and the response can be displayed similar to the EEG.

INDICATIONS AND CONTRAINDICATIONS Monitoring and Mapping for Brain Tumors Mapping and monitoring have found utility in removing brain tumors and cavernous angiomas near the motor cortex, motor tracts, and insula.33e36 Mapping with the SSEP and MEP has been used to locate the sensory and motor cortex, so undesired motor injury is avoided when the presence of a tumor distorts the usual surface anatomy.37 Direct cortical stimulation has

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been used to map the edge of the tumor as it interfaces with the motor cortex.38,39 Similarly, monitoring, especially using the MEP, has been used to warn of encroachment on motor tracts during resection.39,40 Mapping and monitoring has been shown to improve outcome and allow more extensive tumor resection in both children and adults for all supratentorial tumors.41,42

Monitoring for Cerebral Vascular Lesions Intracranial Vascular Surgery Since monitoring is sensitive to ischemia, monitoring can signal unfavorable reductions in blood flow during vascular surgery. For example, during carotid endarterectomy (CEA) the SSEP can be used complementary to the EEG since the SSEP will be sensitive to ischemia in the subcortical pathways not monitored by the EEG.43 The SSEP and MEP have also found utility during surgery of intracranial aneurysms and arteriovenous malformations (AVM) where outcome has correlated with monitoring changes.44e47 With aneurysms, changes have been seen with inadvertent vessel occlusion, temporary clipping, vasospasm, retractor pressure, suboptimal clip application, and relative hypotension. The SSEP has found substantial utility to assess ischemia downstream from intracranial aneurysm surgery and improve outcome.48 A growing appreciation of the value of MEP has been gained by the realization that perforating arteries (especially with middle and anterior cerebral artery aneurysms) can be inadvertently occluded by clips, which do not produce SSEP change, but rather produce ischemia in the motor tracts that are detected by the MEP.46,49,50 Of note the stimulation intensity of the MEP is critical in this monitoring to insure the motor tracts are only stimulated cephalad to the area of potential ischemia. In addition to complementing the SSEP by monitoring different tissue, the MEP appears to be more sensitive to ischemia than the SSEP, suggesting their use should be considered in all intracranial vascular surgery.8 Interventional Vascular Procedures Evoked response monitoring has found utility in interventional procedures for the detection of ischemia. As with the intracranial procedures, SSEP has been widely utilized. MEP is similarly valuable; however, its use has been somewhat reduced due to concerns about movement interfering with radiographic imaging (masking). As with intracranial procedures, MEP can be used with attention to detail to reduce movement.51

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Differing from intracranial procedures, monitoring during interventional procedures may also detect ischemia due to the intravascular nature of the procedure. Hence, they include placement of vascular stents (e.g., carotid, cerebral arteries, thoracic aorta), aneurysm coiling, embolization of AVMs (intracranial and spinal cord), and balloon angioplasty (e.g., post subarachnoid hemorrhage vasospasm). With AVMs, monitoring has found utility for assessment of the impact of arterial flow prior to permanent occlusion.52 Also, occlusion can be used to assess feeding arteries of AVMs.8,9,53 Alternatively, for AVMs, provocative testing using synaptic blockade with a barbiturate (e.g., sodium amytal) or white matter conduction blockade using lidocaine can be done to assess if the artery is critical to the monitored pathway. Similarly, an assessment can be made of blood vessels planned to be embolized to reduce the vascularity of tumors prior to resection.

Brainstem Procedures For procedures in the brainstem, EMG mapping and monitoring of cranial nerves are frequently used. The cranial nerves are susceptible to damage due to their small size, limited epineurium, and that they may be intertwined or obscured by the pathology to be resected. Mapping techniques are of assistance in defining the safe entry zone for approaching deeper tumors.23 One of the most frequently monitored cranial nerves is the facial nerve.8,28,54,55 Its monitoring has allowed significant improvement in outcome, so an NIH consensus panel recommended it be used with vestibular schwannoma (acoustic neuroma).56 It is thought that monitoring assists to maintain the structural integrity of the facial nerve, which increases the chance of functional recovery. Monitoring of other cranial nerves has been used in surgery on the base of the skull, cavernous sinus, and posterior fossa with the specific nerves monitored based on the risks and brainstem region of the procedure. One unique monitoring technique is called the lateral spread response and is used during microvascular decompression.57 This technique involves stimulation of one branch of the facial nerve and monitoring for a response in other branches of the nerve, which is normally not seen except with pathology. In patients with hemifacial spasm, this anomalous response will be seen, which disappears after successful decompression. ABR has been utilized to attempt a preservation of hearing with tumors where the cochlear nerve is involved.2 In general, if waves I and V are

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preserved during surgery, hearing is usually preserved. ABR has also been utilized as a monitor to assess the general viability of the brainstem when mechanical or vascular compromise may occur. The ABR is more sensitive than heart rate or blood pressure for detecting brainstem injury.58 In general, the use of multiple modalities is usually used with brainstem surgery and has allowed procedures that previously had been considered unresectable.59 The SSEP and MEP have also been used like the ABR to assess general brainstem viability.8,60 It is thought that the combination of ABR with SSEP assesses about 20% of the brainstem. The MEP is thought to be particularly important with surgery close to the cerebral peduncles or in the ventral medulla, and mapping to locate the CST has been described in this region.60 In addition to the NIH consensus panel noted for facial nerve monitoring, several other studies have shown a correlation of monitoring with outcome in brainstem surgery. For example, the amount of abnormal EMG activity correlates with outcome after tumor surgery.61

Monitoring Spinal Corrective Surgery One of the early applications of evoked response monitoring was the use of SSEP during Harrington rod correction of scoliosis. In these early cases, distraction by the rod produced a mechanical stress on the spinal cord that affected the posterior column function (SSEP pathway) and anterior spinal cord (motor pathways). As such, SSEP monitoring changes reflected motor outcome. An assessment by the Scoliosis Research Society and European Spinal Deformities Society demonstrated a reduction in the rate of paralysis to 0.55% from 0.7% to 4%.62 A position statement made monitoring a standard of care.63 Of note, since the SSEP and MEP are conducted in different anatomic and vascular regions of the spinal cord, paralysis was not completely eliminated, leading to interest in monitoring the motor tracts.64 Since that over time, spinal column surgeries and instrumentation have become more complex with multiple potential injurious components (e.g., distraction or compression of the spinal cord from correction by instrumentation such as hooks, wires, and pedicle screws, direct spinal cord trauma, epidural hematoma, and derotation, and ischemia from tension on blood vessels, relative hypotension, anemia, and ligation of anterior segmental vessels). Since many of these factors could differentially effect the motor tracts, the addition of MEP to the SSEP has become routine. Further, these multitude of potential insults have stressed the value of continuous

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monitoring assessment making the once used wake-up test less valuable because the latter is a one-time assessment. Since many of these factors are reversible (such as ischemia), the ability to detect neural compromise and correct it has led to excellent correlation with and improved outcome.65e67 The success with scoliosis has also led to interest in monitoring with a large variety of spinal column surgeries and a wide variety of pathologies. The combination of SSEP, EMG, and MEP has been shown to be extremely effective in detecting spinal compromise and improving outcome. A recent evidence-based review by the American Academy of Neurology and American Clinical Neurophysiology Society found sufficient evidence to publish a guideline supportive of multimodality monitoring in spinal surgery.68,69 An important addition to SSEP and MEP has been EMG because of the risk to nerve roots from instrumentation such as pedicle screws (injury in 15%e25% of cases).5,70 The EMG is important because it allows assessment of nerve roots not included in the SSEP or MEP and can allow assessment of an individual nerve root where the SSEP and MEP cannot.5 For pedicle screws, medial misalignment can breach the pedicle wall and place the screw threads adjacent to the nerve roots causing injury and/or postoperative pain. This latter situation has been detected by stimulating the pilot hole or screw and determining the proximity of the screw to the nerve roots by measuring the current necessary to trigger a CMAP response in the muscle innervated by nerve root (threshold). If this current is low, then misalignment has likely occurred, and realignment should be considered.70,71 Numerous studies show good utility for detecting misalignment, notably in screws placed in the lumbar spine.72e75 Challenges with this technique include poor bone densityelowering thresholds and increases in threshold due to newer screws, which are poor electrical conductors, chronically compressed nerve roots, or pathology in the nerve roots. Another challenge with threshold testing is assessing screw placement in the thoracic spine where fewer muscles are available for recording. Since the spinal cord is close to the pedicle, an alternative approach has been to assess the threshold to stimulation of the CST using CMAP responses in lower extremity muscles.76 During cervical spine surgery, MEP monitoring is desirable because it is believed to improve outcome by differentiating cervical cord myelopathy from peripheral neuropathy.77 EMG is also used to detect problems with lateral mass screw placement and the common occurrence of C5 radiculopathy likely due to its shorter length and obtuse angle of exit from the

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spine.78 Spontaneous EMG is also used during anterior cervical spinal surgery to assess the vagal and recurrent laryngeal nerves that are at risk due to the retractor used to expose the spine. This is typically recorded continuously using electrodes on the surface of the endotracheal tube, which are placed to oppose the vocal cords and record EMG from the vocalis muscle. This technique is similar to that used with neck dissections and thyroid and parathyroid removal, except these other procedures typically use a handheld stimulator to map the location of the nerve and periodically verify its integrity.79

Intramedullary Spinal Tumors Intramedullary spinal cord tumors are usually benign tumors within the spinal cord that produce damage as they grow. In particular, there are substantial risks to the motor tracts as the surgeon attempts to resect the tumor. Prior to evoked response monitoring the risks of motor injury were substantial and limited the resection. The SSEP is used to map the midline since the left and right dorsal column responses straddle the midline.80 This minimizes the damage on entering the spinal cord but frequently causes a loss of the SSEP precluding its use for further monitoring. The CST can be mapped within the spinal cord using a collision technique where stimulation in the spinal cord blocks the CMAP response from transcranial stimulation.80,81 Monitoring during tumor resection usually focuses on the MEP D wave recorded from epidural electrodes and CMAP responses from muscles innervated by nerve roots caudal to the surgical site to warn when the resection is encroaching into the motor tracts. Since the D wave is a semiquantitative measure of stimulated CST fibers, a loss of 50% amplitude of the D wave has been found to be an adequate warning that further resection will risk loss of motor function.60,82 If the CMAP response is lost, then temporary loss of motor function occurs, but function returns longterm if the D wave changes less than 50%. Studies show an excellent correlation of monitoring with and improvement in motor outcome.83

Monitoring the Lumbosacral Spine For spine surgery below the end of the spinal cord (usually about L1), surgery places the cauda equina and nerve roots at risk. As such, monitoring using the EMG has been useful. Because of the multiroot nature of the SSEP and MEP mentioned earlier, they are less specific for risk assessment

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of individual nerve roots. Nevertheless, studies have demonstrated their utility in improving outcome.65,84 EMG is also considered useful to assess peripheral nerves that may be injured due to limited vision with minimally invasive techniques or injured by techniques that traverse the lumbar plexus during the extreme lateral approach to the spine. For procedures involving the cauda equina (e.g., tethered cord or tumors of the cauda equina) mapping and monitoring shifts to identifying and retaining functional tissue (especially the innervation of the lower extremity, bowel, bladder, and sexual function). For this, EMG is utilized, including monitoring the anal musculature and the bulbocavernosus reflex.85 Bladder pressure manometry has also been used to assess detrusor muscle stimulation.86 These techniques have shown an improvement in outcome.82,85,87

Thoracic Aorta Aneurysm Surgery Monitoring has also been utilized during the repair of thoracic aortic aneurysms where the risks of paralysis are extremely high due to the risks to the blood supply of the spinal cord.88 The SSEP and MEP can be used for monitoring to detect ischemia in the white or grey matter tracts of the spinal cord. Both MEP and SSEP can be used during an occlusion test to evaluate the importance of intercostal and other perforators. The MEP is more sensitive due to the greater sensitivity of the grey matter, and it has a better correlation with motor outcome.

Contraindication for Monitoring In general, there are very few contraindications for these monitoring techniques, but complications do occur. In essence, the evaluation of risk and benefit needs to be applied with each patient to weigh the risks of the technique versus the potential benefit for surgical decision-making and patient outcome. As mentioned earlier, all of these techniques utilize electrical connections to the patient, but properly maintained equipment is associated with a rare risk of electrical burn. Also, many of these techniques use needle electrodes for stimulation or recording; the risks of needle injury may be more to providers than the patient. The technique with the most likely complication is the MEP. A variety of potential complications have been described (e.g., electrical injury from stimulation); however, in practice the actual incidence is small, dominated by bite injuries to the tongue (prevented by the use of soft bite blocks

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between the molars).4,50,89 Contraindications usually mentioned often include electrical wires or devices implanted in the brain or defects in the skull that might change the usual flow of stimulation current. Others such as the presence of a seizure disorder do not appear to be a contraindication. This is an area that is still evolving with many possible contraindications being found not to be a reason to withhold monitoring when it is beneficial. Finally, some raise concern for patient movement; however, proper choice of stimulation parameters, anesthesia, and timing with the procedure will minimize unacceptable movement.51

EFFECT OF ANESTHETICS Anesthetic management is critical to the effectiveness of evoked response monitoring.90e92 The impact of anesthetic agents varies with the monitoring modality utilized. In general, the effect depends on the sensitivity of the modality to inhalational agents and to neuromuscular blocking drugs. Since anesthetic effects are primarily at synapses, they usually produce amplitude decreases rather than latency prolongations. The major effects are usually noted in the SSEP and MEP (Table 6.3). The ABR is relatively insensitive to both of these types of agents, and monitoring can usually be done with any anesthetic choice. The sole exception is the rare possibility of reduced stimulation when nitrous oxide increases middle ear tension with a blocked Eustachian tube. EMG is an example of a technique that is effected by neuromuscular block (NMB) but relatively insensitive to inhalational agents. For triggered EMG, numerous studies show that monitoring can be done with partial blockade.18 However, the situation is unclear when the responses are small or pathology is present since NMB will inevitably reduce the response amplitude and may obscure small or abnormal responses. The situation is also unclear for free-run EMG. As such, it is usually recommended to avoid NMB during periods where EMG monitoring is utilized. It is also known that substantial blockade falsely elevates pedicle screw thresholds.18 The SSEP and MEP are both sensitive to inhalational agents. The SSEP can usually be recorded in the presence of 0.5e1.0 minimal alveolar concentration (MAC) of inhalational agents.93 MEP is more sensitive, often being recorded with 0.5 MAC inhalational agents. The considerations for NMB for EMG also apply to MEP.18

Decrease

Decrease

Sevoflurane Desflurane NO2

Decrease Decrease Decrease

Decrease Decrease Decrease

Propofol

Decrease

Decrease

Opioids

Minimal

Minimal

Etomidate

Benzodiazepines

Increase at low doses e decrease at higher doses Minimal, increase at low doses Minimal at low doses

Dexmedetomidine

Minimal

Lidocaine

Minimal

Increase at low doses e decrease at higher doses Minimal, increase at low doses Minimal at low doses, prolonged decrease at higher doses Minimal e decrease at higher doses Minimal

Ketamine

Comments

SSEP usually recorded at <1 MAC, MEP < 1/2 MAC Similar to isoflurane Similar to isoflurane Similar to isoflurane, synergistic when combined with halogenated agents SSEP and MEP usually recorded at anesthetic doses but MEP may be lost at high doses SSEP and MEP usually recorded even at high doses Enhancement of SSEP and MEP seen at low doses, depression at very high doses Enhancement SSEP and MEP seen at low doses SSEP and MEP usually recorded with small doses for amnesia SSEP and MEP usually recorded at low doses but MEP lost at higher doses Can be used as intravenous supplement in SSEP and MEP

a Anesthetic effects may be significantly greater in young children (immature pathways) and adults with significant neural dysfunction. Latency increases generally occur as amplitude is decreased. Adapted from Shils JL, Sloan TB. Intraoperative neuromonitoring. Int Anesthesiol Clin 2015;53(1):53e73.

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Isoflurane

166

Table 6.3 Effects of common agents on the cortical SSEPs and muscle MEPsa Agent SSEP amplitude MEP amplitude

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Effects of Inhalation Agents Inhalational agents have the most profound effects on evoked responses.90,92 The agents typically used include desflurane (DES), sevoflurane (SEVO), and nitrous oxide. Nitrous oxide is usually not recommended since it is more depressant on MEP at MAC equivalent doses, provides less beneficial effects on amnesia and unconsciousness, and may need to be turned off in an emergency producing a paradoxical increase in response amplitude obscuring a worrisome decrease in amplitude. The halogenated agents (DES and SEVO) have profound effects on cortical responses (e.g., SSEP) due to cortical depression and blocking of sensory transmission through the thalamus.90 They have very profound impact on MEP CMAP responses due to depression of the motor pathways in the spinal cord.90 Fortunately, these agents have minimal effects on the subcortical SSEP responses and the D wave. It is important to note the ability to record responses with inhalational agents depends on robust responses in adult patients with minimal pathology.93,94 Hence, since pathology may be present, it is suggested to use agents with low solubility (desflurane or sevoflurane) in case the agent needs to be eliminated to allow recording. In young children and in adults with substantial neural pathology, it is usually recommended that the inhalational agents be avoided and a total intravenous-based anesthetic technique (TIVA) be utilized.90

Effects of Intravenous Agents The intravenous agents have less profound impact on the responses. Opioids produce minimal effects when delivered by infusion and therefore are an important component of anesthesia during monitoring evoked responses. Since a complete anesthetic requires unconsciousness and amnesia, a sedative agent must be combined with the primarily antinociceptive action of the opioids. Propofol is currently the most commonly utilized agent. Propofol does produce SSEP and MEP depression at bolus doses (e.g., induction) and when utilized at high doses.95 Usually an infusion can be utilized with opioids to provide adequate anesthesia. The primary exception is opioid-tolerant patients where high doses of propofol are needed, which depresses responses. In these cases, ketamine or lidocaine are often utilized (see later). Dexmedetomidine has been utilized as an alternative to propofol.90 It appears to be compatible with SSEP, but it can be depressant of the MEP.

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Since it does not provide amnesia, the addition of other agents will also augment the depression of MEP.96 Other agents that have been used as alternatives to propofol include etomidate97 and methohexital,98 but these are uncommonly utilized. Etomidate is particularly interesting because it can increase the amplitude of the cortical SSEP and MEP, but it is associated with morbidity possibly associated with adrenal depression.

Effects of Adjunct Medications In general, the anesthetic technique is initially chosen based on the patient comorbidities, the degree of patient neural dysfunction or pathology, the actual surgery to be performed, and the specific monitoring modalities to be used. For challenging cases, TIVA is usually chosen, but when a propofolopioid TIVA is inadequate for anesthesia, supplementation with ketamine and/or lidocaine has been utilized. Ketamine has been favored in pediatric patients and adults with opioid tolerance.99 Ketamine is desirable because it can enhance the amplitude of the cortical SSEP and MEP while reducing the needed infusion of propofol (and the associated MEP depression) and reducing acute tolerance to opioids. A second agent useful to supplement TIVA is an infusion of lidocaine.100 This has been shown to reduce propofol and opioid doses due to a large number of mechanisms. These include potentiation of agents like propofol, actions like those of ketamine, and other mechanisms.

READINGS AND INTERPRETATION 1. What is a change? Establishing baseline IOM signals utilizing supportive anesthesia and technical settings is essential. The responses are repeatedly monitored to identify changes that may signify possible neural compromise. Confirmed changes should be analyzed for technical, physiological, pharmacological, positional, or surgical origin. Physiological and pharmacological caused EP changes tend to be global and more cortical than subcortical. While surgical, technical and positional causes tend to be localized. Each of these changes has special characteristics that can be used to establish cause and guide management.101 2. Changes in amplitude, latency, and stimulation intensity and the EMG changes are discussed in their prospective sections.

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3. What is the cause of a change? When evoked responses change, this may signal unfavorable conditions to prompt changes in management to improve outcome. In general, the events leading to changes in the responses can be categorized as technical, anesthetic/pharmacologic, physiologic, positioning, and procedural/surgical. Usually the monitoring staff will immediately search for technical issues, and the surgical/procedural staff should pause the procedure to reflect on things they have done and possible reversible components. At the same time the search for other possible issues in coordination with the anesthesiologist should be conducted. Assistance can usually occur if the effect can be isolated to a portion of the monitored tract anatomy (e.g., cerebral cortex, peripheral nerve). In addition, since most monitoring involves multimodality, changes in other evoked responses may also help isolate the region of neuroanatomy involved. a. Technical Technical issues revolve around the response acquisition and may not reflect an adverse neural environment. Although sorting this out rests in the purview of the monitoring professional, the stimulation and recording electrodes may be the problem and in shared space, as can be electrical noise from newly added equipment (e.g., blood warmers). b. Pharmacological As before, anesthetic effects can cause evoked response changes.90 Often these involve changes in the drug delivery, including bolus dosing. Even drugs thought to be relatively innocuous (e.g., opioids) can have detrimental effects when delivered as boluses. Usually a review of the anesthetic management prior to the evoked response change can assist in identifying anesthetic-related issues. The occurrence of anesthetic issues stresses the importance of a steady anesthetic delivery during monitoring (e.g., delivery by infusions where possible).90 c. Positional Position-related effects can lead to unfavorable conditions for the nerve pathway monitored. Some of these may be anticipated given the pathology involved (e.g., unfavorable neck flexion or extension). Others may be related to limbs placed or moved into a position that could potentially injure a nerve.

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d. Physiological Physiological changes often involve inadequate oxygen delivery to the neural tract monitored.92,95 This may be a direct effect (e.g., hypotension, hypoxemia, excessive hyperventilation, hypothermia, pneumocephalus), secondary (e.g., elevated intracranial or cerebrospinal fluid pressure, retraction or pressure of surgical device on neural tissue), or a combination of factors that might not individually be a problem. It is important to recognize that physiological issues may be global (e.g., hypotension) or may be regional (e.g., tourniquet effect of an inflated blood pressure cuff). For ischemia-related changes an elevation in the blood pressure may be helpful; not surprisingly, raising the blood pressure is often done when evoked responses change. e. Surgical Surgical changes usually are localized and tend to follow surgical maneuvers, which can result in ischemia or direct nerve insult. Early reversal of these conditions, such as releasing temporary clip, adjusting permanent clip, or as in the spine removing a rod or adjusting a spinal fusion, may result in recovery of the signals and may prevent postoperative neurological deficits. During these periods, while still checking for a cause, the anesthesiologist can raise the blood pressure to enhance collateral circulation.

ADVANTAGES AND DISADVANTAGES 1. Monitoring when the nervous system is at risk may help to decrease postoperative complications and help the surgeon to navigate through the nervous system. 2. The cost of monitoring is an added expense to the total surgical procedure that can limit its use. Efforts to minimize the cost and optimize the use may help to keep the essential use of these monitors. 3. False sense of security. Monitoring may provide the surgeon with a false sense of security since false positive and false negative can be present. Changes of the signal or the lack of it should always be examined in the clinical setting. 4. Complications from needles (needles in the scalp tend to leave minor bleeding) can be aggravated if the patient is on blood thinners or receives anticoagulant during the case. Blood clots can be seen at the end of the case and need to be cleaned. Possible infection is always there but is rare.

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CURRENT EVIDENCE 1. Level one evidence is limited, and the prospect of getting such evidence in the USA and Europe where monitoring is very common is hard to get at this time due to the inability to do prospective randomized blind studies, which will require a very large number of patients, which is not available in many of these centers. 2. What do we have A recent paper reviewed the current literature for the question “does IOM with SSEP and MEP predict adverse outcome?” They utilized the American Association of Neurology four-tiered classification of evidence looking for paraparesis, paraplegia, and quadriplegia.102 They found only four papers with class I evidence and eight papers with class II evidence to support the use of IOM. 3. Evoked potentials are a surrogate for outcome Recently the SSEP and MEP were evaluated as biomarkers and surrogate endpoints for postoperative neurological deficits for both spine and intracranial surgeries.103 Utilizing the evaluation framework recommended by the Institute of Medicine (Institute of Medicine Committee on Qualification of, Biomarkers Surrogate Endpoints in Chronic Disease, 2011)104 and the guidelines adopted by the GRADE working group,105 they concluded that SSEP and MEP as biomarkers could serve as surrogate endpoints. This supports the association of SSEP and MEP with surgical events and a beneficial impact on postoperative outcomes.103

CONCLUSION Intraoperative electrophysiologic monitoring has become commonplace in many procedures where procedural decision-making and neurological risk can be enhanced by mapping or monitoring using the techniques described. The anesthesiologist plays a key role in providing an anesthetic that is favorable for the techniques, providing a positional and physiological environment conducive to good neural outcome, and by actively participating in determining the optimal management when deteriorations in the monitoring suggest impending neural compromise.

SUGGESTED READINGS Refs. 1e9.

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62. Nuwer MR, Dawson EG, Carlson LG, et al. Somatosensory evoked potential spinal cord monitoring reduces neurologic deficits after scoliosis surgery: results of a large multicenter survey. Electroencephalogr Clin Neurophysiol 1995;96(1):6e11. 63. Anonymous, Scoliosis Research Society. Position statement on somatosensory evoked potential monitoring of neurologic spinal cord function during surgery. September 1992. Park Ridge, Illinois. 64. Pelosi L, Lamb J, Grevitt M, et al. Combined monitoring of motor and somatosensory evoked potentials in orthopaedic spinal surgery. Clin Neurophysiol 2002;113(7):1082e91. 65. Voulgaris S, Karagiorgiadis D, Alexiou GA, et al. Continuous intraoperative electromyographic and transcranial motor evoked potential recordings in spinal stenosis surgery. J Clin Neurosci 2010;17(2):274e6. 66. Pastorelli F, Di Silvestre M, Plasmati R, et al. The prevention of neural complications in the surgical treatment of scoliosis: the role of the neurophysiological intraoperative monitoring. Eur Spine J 2011;20(Suppl. 1):S105e14. 67. Malhotra NR, Shaffrey CI. Intraoperative electrophysiological monitoring in spine surgery. Spine 2010;35(25):2167e79. 68. Ney JP, van der Goes DN, Nuwer M, et al. Evidence-based guideline update: intraoperative spinal monitoring with somatosensory and transcranial electrical motor evoked potentials: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology and the American Clinical Neurophysiology Society. Neurology 2012;79(3):292e4. 69. Nuwer MR, Emerson RG, Galloway G, et al. Evidence-based guideline update: intraoperative spinal monitoring with somatosensory and transcranial electrical motor evoked potentials. J Clin Neurophysiol 2012;29(1):101e8. 70. Isley MR, Zhang XF, Balzer JR, et al. Current trends in pedicle screw stimulation techniques: lumbosacral, thoracic, and cervical levels. Neurodiagn J 2012;52(2):100e75. 71. Toleikis JR. Neurophysiological monitoring during pedicle screw placement. In: Deletis V, Shils JL, editors. Neurophysiology in neurosurgery. New York: Academic Press; 2002. p. 231e64. 72. Djurasovic M, Dimar 2nd JR, Glassman SD, et al. A prospective analysis of intraoperative electromyographic monitoring of posterior cervical screw fixation [see comment] J Spinal Disord Tech 2005;18(6):515e8. 73. Raynor BL, Lenke LG, Kim Y, et al. Can triggered electromyograph thresholds predict safe thoracic pedicle screw placement? [see comment] Spine 2002;27(18):2030e5. 74. Reidy DP, Houlden D, Nolan PC, et al. Evaluation of electromyographic monitoring during insertion of thoracic pedicle screws. J Bone Joint Surg Br 2001;83(7):1009e14. 75. Bose B, Wierzbowski LR, Sestokas AK, et al. Neurophysiologic monitoring of spinal nerve root function during instrumented posterior lumbar spine surgery. Spine 2002;27(13):1444e50. 76. Donohue ML, Murtagh-Schaffer C, Basta J, et al. Pulse-train stimulation for detecting medial malpositioning of thoracic pedicle screws. Spine 2008;33(12):E378e85. 77. Freedman B, Potter B. Managing neurologic complications in cervical spine surgery. Curr Opin Orthop 2005;16:169e77. 78. Yanase M, Matsuyama Y, Mori K, et al. Intraoperative spinal cord monitoring of C5 palsy after cervical laminoplasty. J Spinal Disord Tech 2010;23(3):170e5. 79. Audu P, Artz G, Scheid S. Recurrent laryngeal nerve palsy after anterior cervical spine surgery. Anesthesiology 2006;105:898e901. 80. Deletis V, Bueno De Camargo A. Interventional neurophysiological mapping during spinal cord procedures. Stereotact Funct Neurosurg 2001;77(1e4):25e8. 81. Quinones-Hinojosa A, Gulati M, Lyon R, et al. Spinal cord mapping as an adjunct for resection of intramedullary tumors: surgical technique with case illustrations. Neurosurgery 2002;51(5):1199e206. Discussion 1206e1197.

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