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Intraoperative neurophysiologic monitoring: its impacton the practice of a pediatric neurosurgeon

Rick Abbott

Received: 18 August 2009 /Published online: 24 November 2009# Springer-Verlag 2009

AbstractIntroduction From its introduction in the early 1970s,intraoperative neurophysiological monitoring has evolvedinto an extremely useful and reliable adjunct for operatingon the central and peripheral nervous system.Objective This manuscript reviews the author’s experiencewith its evolution in his practice and how it impacts it today.

Keywords Intraoperative monitoring . Intraoperativemapping . Intraoperative physiologic monitoring .

Intraoperative neurophysiologic monitoring .

Spinal cord tumor . Brainstem tumor

Introduction

I entered neurosurgical training in 1980, a time when surgicaltechnology was under rapid evolution. Our field was in theprocess of accepting the surgical microscope and understand-ing how best to use computerized axial tomographic imaging.The thrust for this was improved patient safety, and we saw adramatic improvement in our patients’ outcomes. In 1985, Ifirst saw machinery for recording evoked action potentialswithin the nervous system brought into our operating room inHouston. I was intrigued by the promise of being able toobserve neurologic function while operating on the nervous

system. Intuitively, it made sense. From there, I have had thefortune of witnessing the evolution of monitoring of thenervous system during surgery to a point where today weroutinely employ this technology to keep our patients safeduring their surgery. What follows is a description of myexperience with intraoperative neurophysiologic monitoring(ION) and how it has impacted my patients and practice.

My introduction

As mentioned above, it was in 1985 that I first witnessedan attempt to using ION during a surgery. The case wasthe simple, straight-forward decompression of a cervicalstenosis. A neurologist who performed outpatientsomato-sensory evoked potential (SSEP) testing wasinvited into our surgery to see what he could accomplish.He brought with him the Nicolet Pathfinder and pro-ceeded to attach stimulating and recording electrodes.Then, what followed was 30 min of attempts to recordmeaningful potentials. He totally failed and could notexplain why. He left with his equipment to return to hisoffice where patients waited for their outpatient tests. Iwitnessed no further such attempts, presumably becausemore compelling areas of research where drawing theattention of my attending surgeon and the neurologist.

The following year, I traveled to New York to completemy training as a pediatric neurosurgeon with Fred Epstein. Ihad been impressed with the concept that, by watchingnerve potentials triggered during surgery, one could gain anappreciation of how well the nervous system was toleratingthe surgery. Fred too was intrigued by the prospect and had,in fact, been working with a research neurophysiologist tointroduce reliable ION. Their efforts had focused onsomatosensory evoked potentials. The results, however,

R. AbbottClinical Neurosurgery, Albert Einstein College of Medicine,Bronx, NY, USA

R. Abbott (*)Department Neurosurgery, Montefiore Medical Center,111 E 210th St,Bronx, NY 10467, USAe-mail: rabbott@montefiore.org

Childs Nerv Syst (2010) 26:237–240DOI 10.1007/s00381-009-1021-5

were inconsistent, and in reality, much of the time spent bythe physiologist was troubleshooting an inability to recordmeaningful data. In 1987, Dr. Vedran Deletis was recruitedto join our surgical team. Dr. Deletis, a M.D./Ph.D. trainedin neurology and neurophysiology, was, and still is,dedicated to evolving ION to its acceptance as anindispensible tool in the neurosurgical operating room. Hemethodically set to work, first cleaning up the electromag-netic environment of our operating rooms, building reliablerecording, and stimulating electrodes and developingdependable hardware and software to recorded electricalpotentials of interest. Soon, he was able to record firstSSEP and then motor evoked potentials of the upper motorneurons (D wave). I began to feel justified in my hopes thatpatient safety could be enhanced using such informationduring their surgery.

Monitoring and mapping

As we utilized ION more and more, an important insight wasgained. Mapping, or the identification of neural structures byelectrical stimulation, differed from monitoring or theongoing activation of neural pathways and the observationof these evoked potentials during a surgery. The surgeonneeded to stop operating to stimulate structures in order toidentify or “map” them. Once surgery resumed, theinformation used to map location became increasinglyhistoric and inaccurate. Monitoring, on the other hand, tookplace in the back ground as the surgeon operated andrequired no action on the part of the surgeon once thestimulating and recording electrodes had been placed.Changes in the recorded potentials being monitored couldbe used as warning signs for impending injury to the circuitsthrough which the potentials were passing. Both techniqueshad values, but one could not be used to replace the other.

There is a long history of the use of mapping to establishthe location of critical structures of the nervous system thatdates back to the work of scientists in the eighteenthcentury [4]. The study of electricity was quite popular at thetime, and many reported on its use in experimentallystimulating muscles and peripheral nerves to trigger musclemovement in animals. Galvani reported on the electricalstimulation of the spinal cord and brain of frogs to triggermovement in their legs [4]. Throughout the nineteenthcentury, reports of experimental stimulation of the brains ofexperimental animals and human corpses were published asargument raged on the location of motor function. Thethrust of these experiments was to support the argumentthat motor function lay within the cortex and not in deeperstructures of the brain [3, 4]. Bartholow was the first toreport on the electrical stimulation of the cortex of an alivepatient, an event that was not without controversy [1, 19].

After his patient first seized multiple times and then diedseveral days later, Bartholow was questioned about theappropriateness of such experimentation. He responded thatto repeat such a procedure would be “…in the highestdegree criminal” given the resulting postoperative courseculminating in death [2]. Others were not deterred. Keen[12] reported stimulating the cortex of a patient during acraniotomy. Dana, in 1893, reported stimulating the cortex ofa patient bothered by chorea [4, 5]. Needle electrodes wereinserted via a burr hole into the patient’s cortex, and whencurrent was applied, the patient experienced a brief convul-sive movement and sensory changes in the contralaterallimbs. Kraus followed by Foerster reported on the frequentuse of electrical stimulation of the brain to map out areas ofcritical function during epilepsy surgery [4, 9]. Penfieldtraveled to Breslau to observe Foerster’s technique forepilepsy surgery and then brought it back to Montreal wherehe developed his now famous homunculus [3, 20]. His workresulted in the routine use of cortical stimulation at centersengaged in the surgical management of epilepsy and pavedthe wave for its wider use in neurosurgery by the late 1980s.

The history of monitoring is not as long. Initial effortsfocused on establishing the ability to monitor SSEPs duringsurgery [8]. This was a natural path given that SSEPs werebeing routinely performed on outpatients in the 1980s.Consequently, most centers had physicians who werefamiliar with the technique and had the equipment toperform the procedure. The inherent problems with theperforming SSEPs soon became obvious, as its applicationwas broadened to monitor motor function during intra-medullary spinal cord surgery. Reports began to appear of“false negative” results, with patients awakening from theirsurgeries paralyzed [14]. In addition, the use of SSEPsproved unpracticable when used on patients with preoper-ative sensory lesions or when a myelotomy through thedorsal spinal cord was required [7]. Attempts at monitoringthe motor system used direct, nonfocal stimulation of thespinal cord with monitoring of the evoked potentials eitherwithin the spinal cord or peripheral nerve/muscle thenfollowed [15, 18, 22, 24]. These techniques provedproblematic, however, owing to the diffuse nature of thestimulation resulting in the activation of multiple sensoryand motor pathways [7]. Monitoring in such a setting couldgive one the false impression that the corticospinal tract(CST) was being preserved when, in fact, the potentialsbeing monitored were the summation of action potentialstraveling via pathways other than the CST tract. In 1980,Merton and Morton [16] reported on the successful trans-cranial stimulation of the motor cortex with activation ofdescending potentials within the CST tract. This was doneon awake individuals. Several hurdles lay in the way for theroutine use of transcranial stimulation of the motor path-ways in anesthetized patients. Cortical stimulation results in

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the generation of both the D wave (direct wave) and the Iwaves (internuncial pathways potentials) within the CST.The D wave results from the activation of the upper motorneuron’s axon and passes through no synapse to reach theCST within the spinal cord. Consequently, it is relativelyimmune to the effects of anesthesia [21]. The I waves, onthe other hand, are a series of waves that follow the D waveand are thought to require synaptic activation of the uppermotor neurons by corticocortical fibers from lamina V aswell as fibers from the premotor and precentral cortex.Since anesthesia targets synapses, the I waves can bedifficult to record in an anesthetized patient, and thesepotentials are very vulnerable to increasingly deep anesthesia.Initial attempts at the generation of upper motor neuronpotentials used single pulse stimuli. The action potentialgenerated in this manner requires both a D and I wave to bringthe neuron to its threshold for generating such a potential. In1993, an observation was made that a short train of stimulidelivered to the motor cortex could generate a D wave and anupper motor neuron action potential even without thegeneration of I waves [10]. As the routine use of monitoringof the D wave grew, so did our appreciation of factors thataffected the monitoring. We learned that the stimulusintensity affected what was activated. Low-intensity stimulipassed out only from the anode activating only motor cortex/subcortex within the immediate neighborhood of theelectrode. As stimulus intensity was increased, deeperstructures such as the internal capsule were activated, whilestrong stimuli would activate structures as deep as thebrainstem at the foramen magnum [7]. Additionally, as theintensity of stimulus increases, the cathode begins tostimulate tissue directly under it. Consequently, when thestimulating electrodes are placed with the anode on one sideof the head and the cathode on the other, a low-intensitystimulation will result in the generation of a D wave in theCST contralateral to the stimulating anode, while strongerstimuli will result in bilateral D wave propagation in the CSTof the spinal cord. We learned that cooling of the spinal cordeither by its exposure to the surgical environment or byirrigation could lead to an increased latency in the D wave.In 1997, our group reported on being unable to record Dwaves in some of our spinal cord tumor patients [17]. Thiswas the result of a desynchronization of the D waves due tothe tumor’s effect on the CST. This caused a variation in thelatency of the individual D waves so that the amplitude ofthe summation of these potentials was too small to record atany given point in time.

As experience grew, greater success was experienced inrecording evoked muscle potentials (muscle MEPs) inresponse to transcranial stimulation. This was an extremelyimportant addition to our armamentarium for severalreasons. First, up to that point when the epidural space ofthe spinal cord was not surgically exposed, a percutaneous

placement of an epidural spinal electrode was required.While technically feasible, in reality, it was a time-consuming process that discouraged its common use.Secondly, as mentioned above, spinal cord tumors candesynchronize the D waves, making their recordingdifficult and sometimes impossible. We found, however,that desynchromized D waves summate when they reach agiven spinal segment’s ventral horn and can successfullytrigger an α-motor neuron action potential that results inmuscle contraction [17]. As the use of muscle MEPsincreased, it was learned that the smaller muscles seemedbetter candidates for recording these potentials [23]. Thesmall muscles of the hands and feet and the muscles ofthe forearm and anterior tibialis became preferred over thelarger, more proximal muscles.

By the mid-1990s enough experience had been gainedfor Kothbauer to report on criteria that could be usedintraoperatively to predict a patient’s postoperative motorfunction when undergoing intramedullary spinal cordsurgery [13]. He found that a loss of greater than 50% ofthe premyelotomy D wave amplitude resulted in severe,lasting loss of motor function. Loss of the muscle MEPspredicted a loss of motor function in the immediatepostoperative period, but preservation of >50% of thepremyelotomy D wave amplitude in this setting predictedan ultimate return of the patient to their preoperativefunctional status. It was at this point that the promise ofION was met and the seemingly random outcome in ourpatient’s undergoing intramedullary spinal cord surgeryceased for we had a guide post on when to stop a resection.

During the early 1990s, we became interested in themonitoring of the neurological system of the bowel andbladder. This was the result of our patients’ undergoingselective dorsal rhiztoomy experiencing a 25% incidence oftransient postoperative urinary retention that wouldtypically last several weeks. We started by first mappingthe sacral dorsal nerve roots for afferent action potentialsin response to stimulation of the pudendal nerve. Wefound that these potentials were distributed over the S1,S2, and S3 nerve roots in an unsymmetric, randomfashion that varied from patient to patient. We elected notto section those roots carrying these action potentials outof concern over the children’s sexual function latter inlife. What we found was that the incidence of urinaryretention dropped to around 7% and that the period ofretention, when present, was measured in days and notweeks [6, 11]. From this work, we developed the ability torecord the bulbocavernous reflex, pudendal spinal andcortical SSEPs, and anal muscle MEPs evoked by trans-cranial simulation. These became not only valuable toolswhen performing rhizotomies but also for other workwithin and about the conus and cauda equina. It alsoallowed us to appreciate factors that interfered with our

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ability to record these potentials. That knowledge wasthen taken to the brainstem where we developed the abilityto monitor evoked motor and sensory cranial nervepotentials.

Present day

Today, I am blessed in having a broad armamentarium tochoose from when operating on the central and peripheralnervous systems. I am able to map the cortical andsubcortical brain for its motor pathways, the brainstem forits motor nuclei, and nerve roots conducting sensory ormotor action potentials. I can monitor function in the Vth,VIIth, VIIIth, IXth, Xth, XIth, and XIIth cranial nerves, theCST, and sensory pathways for the extremities, bladder, andbowel. I can also monitor reflex circuits involved inbrainstem and bowel and bladder function. If a surgery isto take place near one of these structures, I will monitortheir ability to conduct potentials and frequently will mapout their precise locations using this information indetermining my pathway to the surgical target. If I amworking in the posterior frontal lobe or parietal lobe, thenmapping will be done to locate the Rolandic fissure, andmuscle MEP recordings and SSEPs will be used to monitorthe motor and sensory pathways during the resection.Similarly, the motor and sensory pathways will bemonitored during subcortical resections, temporal loberesections, and brainstem tumor resections. Cranial motornerve nuclei mapping will be used prior to entering thefloor of the fourth ventricle, and I will select cranial nervesand brainstem reflexes to monitor during the resectionbased on the level of the brainstem being worked upon. Forwork in and around the cervical and thoracic spinal cord,motor (D wave and muscle MEPs) and sensory evokedpotentials will be monitored, and when working around theconus, the extremity and bowel/bladder SSEPs and muscleMEPs will be monitored in addition to the bulbocavernousreflex. In the cauda equina and peripheral nerves, we willcommonly map out which nerves are carrying potentialsthat we want to protect and we also can monitor SSEPs andmuscle MEPs.

I have come to view mapping and monitoring asindispensible tools for the majority of my cases within thenervous system. Having seen how their use has impactedmy patient’s outcome over the past two decades, I wouldfind it unacceptable not to have these tools available.

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