intraoperative neurophysiology and methodologies used to...

CHAPTER 2

IntraoperativeNeurophysiologyand MethodologiesUsed to Monitor theFunctional Integrityof the Motor SystemVEDRAN DELETIS

Division of Intraoperative Neurophysiology, Hyman-Newman Institute for Neurologyand Neurosurgery, Beth Israel Medical Center, New York

1 Intraoperative Monitoring of the Motor System:A Brief History1.1 Penfield’s Time1.2 Spinal Cord to Spinal Cord1.3 Spinal Cord to Peripheral Nerve (Muscle)

2 New Methodologies2.1 Single-Pulse Stimulation Technique2.2 Multipulse Stimulation Technique

3 Methodological Aspects of TES During GeneralAnesthesia3.1 Electrode Montage Over the Scalp for Eliciting

MEPs (for Single- and Multipulse StimulationTechniques)

4 Recording of MEPs over the Spinal Cord (Epiduraland Subdural Space) Using Single-PulseStimulation Technique4.1 D Wave Recording Technique Through an

Epidurally or Subdurally Inserted Electrode4.2 Proper Placement of Epidural Electrodes

25Neurophysiology in Neurosurgery: A Modern Intraoperative ApproachCopyright 2002, Elsevier Science (USA). All rights of reproduction in any form reserved.

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4.3 Factors Influencing D and I Wave Recordings 4.4 Neurophysiological Mechanisms Leading to the

Desynchronization of the D Wave5 Recording of MEPs in Limb Muscles Elicited by a

Multipulse Stimulating Technique5.1 Selection of Optimal Muscles in Upper and Lower

Extremities for MEP Recordings5.2 Neurophysiological Mechanisms for Eliciting

MEPs using a Multipulse Stimulation Technique5.3 Surgically Induced Transient Paraplegia

6 ConclusionReferences

ABSTRACT

Beginning with Penfield’s early work and covering the latest developments in thefield, this chapter will present a brief history of intraoperative neurophysiology of themotor system, paying special attention to the use of motor evoked potentials (MEPs)during surgeries that place the motor system at risk of injury. The chapter will assessthe advantages and disadvantages of traditional techniques previously used to mon-itor the corticospinal tract (CT), discuss modern methodologies for eliciting andrecording MEPs (single and/or multipulse, transcranially applied, electrical stimu-lation, with recorded activity from either the spinal cord or from the limb muscles),and assess the neurophysiological background for both sets of techniques. Particu-lar interest will be placed on the intraoperative changes of MEPs, their relationshipto neurological outcome, and their potential neurophysiological explanations. As anexample, the phenomenon of surgically induced transient paraplegia, and thechanges in monitoring parameters accompanying it, will be discussed.

1 INTRAOPERATIVE MONITORINGOF THE MOTOR SYSTEM: A BRIEF HISTORY

1.1 PENFIELD’S TIME

When discussing the use of intraoperative electrical stimulation of the uppermotoneurons in humans, it is essential to mention Wilder Penfield (1891– 1976).His publication with Edwin Boldrey in the journal Brain [1] summarized hiswork on the motor and somatosensory system’s organization of the cerebralcortex in humans, as explored with intraoperative electrical stimulation. Penfield’ssystematic exploration of the brain with intraoperative stimulation laid thefoundation for the field of intraoperative neurophysiology (ION).

After Penfield—except for the work done to intraoperatively localize epilep-tic foci—almost half a century passed without any significant developments in

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Intraoperative Neurophysiology and Methodologies 27

ION exploration of the nervous system. However, a transformation took placeduring the 1950s and the 1960s when clinical neurophysiology branched intothree subfields: electromyography (EMG), electroencephalography (EEG), andevoked potentials. These developments helped to widen the doors of the oper-ating room to the use of these methods intraoperatively.

By the late 1970s, somatosensory evoked potentials (SEPs) became routinelyused to intraoperatively assess the functional integrity of the somatosensorysystem in the spinal cord during surgical correction for scoliosis [2]. The sameSEPs data were also routinely extrapolated to assess the functional integrity ofthe upper motor neuron tracts; however, as data mounted, this approach provedunreliable: (a) it provided false results when SEPs were found to be presentdespite postoperative motor deficits [3, 13] (see Chapter 15, Fig. 15.19, page 386);(b) it provided unreliable (low-quality) or unmonitorable (complete absence) SEPsin patients in whom certain pathologies affected the somatosensory system; and(c) because dorsal myelotomy often destroyed the dorsal column’s integrity inpatients undergoing surgery for intramedullary spinal cord tumors, the abilityto monitor SEPs was immediately nullified [4].

Because of these difficulties, ION was forced to search for more reliable meth-ods to assess the motor system’s functional integrity. Initial attempts to monitormotor tracts in the spinal cord were made in both Japan and the United States.These attempts focused on two neurophysiological techniques: spinal-cord-to-spinal-cord recording, and spinal-cord-to-muscle/peripheral-nerve recording.

1.2 SPINAL CORD TO SPINAL CORD

This technique operates with nonselective electrical stimulation of the spinal cordand with nonselective recordings of elicited potentials from the spinal cord. It isused to record signals from the spinal cord regardless of the direction of prop-agation of the action potentials (either ascending, descending, or ortho/antidromic). The type of action potential recorded depends on the position ofthe stimulating and recording electrodes and the direction of the travelingwaves through the spinal cord with regards to the natural direction of the con-ducting pathways [5].

The evoked potentials recorded from the spinal cord using this technique arethe electrical sum of activity from multiple pathways. Because of the differentconduction properties of the various spinal cord pathways, the recorded poten-tials can show two distinctive wave morphologies. It has been speculated thatone of these waves represents transmission in the dorsal columns (DCs) and theother by the corticospinal tract (CT). Clinical testing on a large number ofpatients with different and relevant pathologies has not been done to confirmthis hypothesis.


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This method can evaluate the integrity of ascending and descending, and prob-ably propriospinal pathways, within the spinal cord. However, specific informationabout the DC or CT cannot be obtained with this method. Critical reports [6]could not confirm the value of the spinal cord to spinal cord technique in moni-toring motor pathways during surgery for intramedullary spinal cord tumors.

1.3 SPINAL CORD TO PERIPHERAL NERVE (MUSCLE)

This technique operates with nonselective stimulation of the spinal cord and selec-tive recordings from the peripheral nerves or muscles. Recordings from the muscle[7, 8] and peripheral nerves [9] presume that after electrical stimulation of thespinal cord, α-motoneurons are activated only by the CT tract. Therefore, com-pound muscle action potentials (CMAPs) in the limb muscles or electrical activ-ity in the peripheral nerves should be generated by CT stimulation. Unfortunately,α-motoneurons can also be activated by any of the multiple descending tractswithin the spinal cord after diffuse electrical stimulation of the spinal cordand/or by antidromically activated dorsal columns and their segmental branchesthat mediate the H reflex [10]. Electrical activity recorded from mixed periph-eral nerves is a combination of α-motoneuron discharges initiated by the CTand other descending tracts. Because the sensory component of mixed periph-eral nerves is a physical continuation of the dorsal columns, part of the electricalactivity recorded from mixed peripheral nerves after stimulation of the spinalcord arises from the antidromically activated dorsal columns that convey trav-eling waves to the peripheral nerves [10]. Collision studies have challenged thewidely accepted presumption that potentials recorded from peripheral nervesin the lower extremities after stimulation of the spinal cord are generated by theCT [11]. Therefore, there is convincing evidence that selective recording ofthe electrical activity from peripheral nerves elicited by electrical stimulation ofthe spinal cord does not arise from the CT [12]. Additional evidence concern-ing the inaccuracy of monitoring the motor pathways through potentialsrecorded from peripheral nerves is provided in a recent paper by Minahan et al.This paper describes two patients with postoperative paraplegia in spite ofpreservation of these potentials [13].

It is fair to say that both of the techniques described can grossly monitor thefunctional integrity of multiple pathways inside the spinal cord without beingspecific for any of them. In other words, these methods can indicate that cer-tain lesions to the spinal cord have occurred, but they lack the ability to pro-vide specific information as to which of the spinal cord pathways has beendamaged. This methodology may be useful in orthopedic surgical proceduresand other surgeries where lesioning of the nervous tissue within the spinal cordis diffuse in nature and where all pathways are usually affected. An exception to



this phenomenon involves vascular lesions of the spinal cord where selective lesion-ing of the anterolateral columns can occur.

Unfortunately, this nonselective evaluation of multiple pathways is not suf-ficient during surgery of the spinal cord, during which the DCs can be inde-pendently damaged from the anterior and lateral columns [4, 14]. Furthermore,these two techniques (for methodological reasons) cannot evaluate the func-tional integrity of the CT from the motor cortex to the upper cervical spinalcord. Therefore, supratentorial, brainstem, foramen magnum, and upper cervi-cal spinal cord surgeries cannot be monitored using these techniques. This isalso the case in procedures involving the clipping of an intracerebral aneurysm,where the perforating branches for the CT tract in the internal capsula can beselectively damaged while leaving the lemniscal pathways intact. This results ina so-called pure motor hemiplegia (i.e., the patient is postoperatively hemi-plegic while the sensory system is intact and SEPs are present) [10, 15, 16]. Sinceit requires the motor cortex to be surgically exposed, Penfield’s technique maynot be used for monitoring motor tracts within the spinal cord.

2 NEW METHODOLOGIES

Based on previous work by Hill et al. [17], Merton and Morton [18] discoveredthat high-voltage current applied over the skull could penetrate to the brain andactivate the motor cortex and the CT. Although they produced discomfort,these methods of transcranial electrical stimulation (TES) became an additionaltool used to diagnose upper motoneuron lesions in awake patients. On the basisof this work, two methodologies for monitoring the CT intraoperatively weredeveloped, the single-pulse stimulation technique and the multipulse stimula-tion technique.

2.1 SINGLE-PULSE STIMULATION TECHNIQUE

A single-pulse stimulating technique involves a single electrical stimulusapplied transcranially or over the exposed motor cortex while the descendingvolley of the CT is recorded over the spinal cord as a direct wave (D wave).

2.2 MULTIPULSE STIMULATION TECHNIQUE

A multipulse stimulating technique involves a short train of five to seven elec-trical stimuli applied transcranially or over the exposed motor cortex whilemuscle motor-evoked potentials (MEPs) from limb muscles in the form of


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CMAPs are recorded (Fig. 2.1) [28]. (This latter technique differs essentially fromthe Penfield technique in that it calls for only five to seven stimuli with a stimulat-ing rate of up to 2 Hz. Penfield’s technique calls for continuous stimulation over aperiod of a few seconds with a frequency of stimulation of 50–60 Hz, and only inthe cases when the motor cortex is surgically exposed. Furthermore, at such fre-quencies and train durations, seizures are easily induced.)

FIGURE 2.1 (A) Schematic illustration of electrode positions for transcranial electrical stimula-tion of the motor cortex according to the International 10–20 EEG system. The site labeled “6 cm”is 6 cm anterior to CZ. (B) Illustration of grid electrode overlying the motor and sensory cortexes.(C) Schematic diagram of the positions of the catheter electrodes (each with three recording cylin-ders) placed cranial to the tumor (control electrode) and caudal to the tumor to monitor thedescending signal after it passes through the site of surgery (left). In the middle are D and I wavesrecorded rostral and caudal to the tumor site. On the right is depicted the placement of an epiduralelectrode through a flavectomy/flavotomy when the spinal cord is not exposed. (D) Recordingof muscle motor evoked potentials from the thenar and tibialis anterior muscles after being elicitedwith multipulse stimuli applied either transcranially or over the exposed motor cortex. Modifiedfrom [31].



3 METHODOLOGICAL ASPECTS OF TESDURING GENERAL ANESTHESIA

3.1 ELECTRODE MONTAGE OVER THE SCALP

FOR ELICITING MEPS (FOR SINGLE AND MULTIPULSE

STIMULATION TECHNIQUES)

The electrode placement on the skull is based on the international 10–20 EEGsystem (Fig. 2.1A). Note that, instead of CZ, the CZ electrode is placed 1 cmbehind the typical CZ point. Some laboratories have used 2 cm in front of C3or C4 (Z. Rodi, personal communication). For transcranial stimulation, corkscrew–like electrodes (Corkscrew electrodes, Nicolet, Madison, WI) are prefer-able because of their secure placement and low impedance (usually 1 KΩ).Alternatively, an EEG needle electrode may be used. We do not recommendthe use of EEG cup electrodes fixed with collodium since they are impracti-cal and their placement is time-consuming. The only exception is for youngchildren in whom the fontanel still exists. Since the CS electrodes couldpenetrate the fontanel during placement, the use of EEG cup electrodes issuggested.

The skull presents a barrier of high impedance to the electrode currentapplied transcranially; therefore, we cannot completely control the spreadof electrical current when it is applied. For this reason, various combina-tions of electrode montages may need to be explored to obtain an optimal res-ponse. The standard montage is C3/C4 for eliciting MEPs in the upper extrem-ities and C1/C2 for eliciting MEPs in the lower extremities. With sufficientintensity of stimulation at C1/C2, MEPs are preferentially elicited in theright limb muscles while stimulation at C2/C1 elicits MEPs in the left limbmuscles.

With stronger electrical stimulation, the current will penetrate the brainmore deeply, stimulating the CT at a different depth from the motor cortex(Fig. 2.2). On the basis of measurements of the D wave latency, it has been pos-tulated that there are three favorable points that are susceptible to depolariza-tion of the CT: cortex/subcortex (weak electrical stimulation), internal capsula(moderate electrical stimulation), and brainstem/foramen magnum (strongelectrical stimulation). Selectivity of stimulation is possible at the level of thecortex (subcortex). Therefore, only the application of relatively weak electricalstimuli to the cortex is selective, and it activates only a small portion of the CTfibers (e.g., activating only one extremity) or only one CT. It is important toremember that during electrical stimulation of the motor cortex, the anode ispreferentially the stimulating electrode. With increasing intensity of the current,the cathode becomes the stimulating electrode as well.


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As an example, stimulation with the C3+/C4− will selectively activate mus-cles of the right arm. When stimulation intensity is increased, the cathode(C4−) becomes the stimulating electrode as well, resulting in the stimulationof the left arm. Finally, when current intensity becomes strong enough to pen-etrate to the internal capsule more caudally, all four extremity muscles can beactivated. For anatomical reasons (deep position of the leg motor area in theinterhemispheric fissure), more intense current is usually needed to obtainMEPs in the lower extremities. It is especially difficult to obtain them sepa-rately without also activating the upper extremities. Our observation has beenthat it can be done in certain patients, especially when using the CZ/6 cm infront montage (see Fig. 2.1).

By their anatomical location, recording electrodes in the limb muscles canindicate which fibers of the CT are activated predominantly (left or right,fibers for upper or lower extremities). If one would like to activate left andright CT simultaneously to obtain D wave recordings, weak electrical stimu-lation should be avoided and a moderate intensity should be used. In Fig. 2.3,it is obvious that weak electrical stimulation activates fibers of the CT for theleft upper extremities only. This can result in activation of only one CT whilenot affecting the other CT. Therefore, the intensity of electrical stimulationfor eliciting a D wave should be determined by simultaneous recordings ofMEPs from limb muscles (indicating which fibers of the CT have been pre-dominantly activated), or only moderate intensities of electrical current foreliciting D waves should be used. The moderate intensity of electrical current

FIGURE 2.2 D and I waves recorded after a single electrical stimulus delivered transcranially (CZanode/6 cm anterior cathode) in 14-year-old patient with idiopathic scoliosis. When the intensityof the stimulus is increased, electrical current activates the CT deeper within the brain and thelatency of the D wave becomes shorter. As current becomes stronger, more I waves are induced(100% corresponds to 750 volts of stimulator output). Modified from [10].



will activate both CTs at the level of the internal capsule. If MEP waves havenot been simultaneously recorded with D waves, the following guidelinesshould be followed: increase the intensity of the stimulation until D waves donot increase in amplitude (Fig. 2.2, the third trace from the top). This is a signthat most of the fast conducting neurons of CT from the left and right CT havebeen activated.

The neurophysiological mechanism for eliciting MEPs by stimulating themotor cortex in patients under the influence of anesthetics is different fromthe mechanism in the awake subject. In the latter, electrical current stimulates thebody of the motor neuron transynaptically over the chain of vertically orientedexcitatory neurons, resulting in I waves (indirect activation of the motoneu-rons). At the same time, electrical current activates axons of the corticalmotoneurons, directly generating D waves [19]. In anesthetized patients, anes-thetics block the synapses of the vertically oriented excitatory chains of neuronsterminating on the cortical motoneuron’s body. Therefore, only the D wave isgenerated after electrical stimulation of the motor cortex [19, 20]. Patients withidiopathic scoliosis are an exception. In this group, abundant I waves can berecorded (Fig. 2.2). We believe that this is one of the neurogenic markers of thedisease present in these patients [21]. Furthermore, it has been shown that afrontally oriented cathode preferentially generates I waves because at this stim-ulating setting corticocortical projections of vertically oriented interneuronsare optimally activated. With the cathode in the lateral position, this is not thecase [22, 23] (Fig. 2.4).

FIGURE 2.3 Transcranial electrical stimulation over the C4 anode/C3 cathode with recordingsof the D wave over the C6–C7 segment (above) and the T7–T8 segment of the spinal cord (below).Stimulus intensity was 35 and 40 mA, respectively. Stronger stimuli elicit the D wave over the tho-racic spinal cord, while a weaker stimulus (35 mA) elicits the D wave only over the cervical spinalcord.


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4 RECORDING OF MEPs OVER THE SPINAL CORD(EPIDURAL AND SUBDURAL SPACES) USINGSINGLE-PULSE STIMULATION TECHNIQUE

4.1 D WAVE RECORDING TECHNIQUE THROUGH AN

EPIDURALLY OR SUBDURALLY INSERTED ELECTRODE

This method is a direct clinical application of Patton and Amassian’s [19] dis-covery in the 1950s that electrically stimulated motor cortex in monkeys gen-erates a series of well-synchronized descending volleys in the pyramidal tract.This knowledge of CT neurophysiology, which was collected in primates, canbe applied to humans in most cases.

We have to be aware that even small methodological aspects of recording Dwaves are of the utmost importance and should be followed in order to achievereliable results.

4.1.1 Choice of Electrode

Practically any type of catheter-type electrode designed for electrical stimulationof the spinal cord epidurally can be used for recording D and I waves. We preferto use the JX-300 (Arrow International, Reading, PA) because of its optimalrecording properties and intercontact recording electrode distance (Fig. 2.5). Thiselectrode has three platinum-iridium recording cylinders 3 mm in length, 1.3 mmin diameter, and 18 mm apart, with recording surfaces of approximately 12.3 mm2.

FIGURE 2.4 Upper thoracic epidural recordings of D and I waves in a 14-year-old female duringsurgery for a low cervical intramedullary tumor. The upper trace was obtained after transcranialelectrical stimulation over C1 (anode) and C2 (cathode) using 140 mA stimulus intensity and astimulus duration of 500 µs. The lower trace was obtained after anodic stimulation at CZ and catho-dal stimulation at 6 cm anterior to CZ, using the same stimulus duration but at 200 mA. Note theappearance of the D and I waves with this electrode arrangement. (An upward deflection is nega-tive.) Reprinted from [23].



This electrode is semi-rigid, a property that facilitates its placement either per-cutaneously or through flavotomy. Furthermore, it consists of a double lumenwith two openings at the tip of the electrode. This allows for the injection ofsaline to flush the recording contact surfaces and reduce impedance. This is animportant methodological detail in the case of bad electrode contact if the elec-trode is placed percutaneously in the epidural space (where it can face a highimpedance). Once the electrode is in place, it is very difficult to reposition it.Thus an injection of saline through the outer lumen is a method of rectifyingthe high-impedance problem (Fig. 2.6). When the electrode is placed afterlaminectomy, problems with impedance and positioning of the electrode areeasier to solve because the surgeons are able to reposition the lead.

Most epidural electrodes are disposable. If one uses a nondisposable type,extreme care should be taken to ensure that the electrode is clean before steril-ization and thus has improved electrical properties. To clean the electrode, werecommend one of the following procedures. You can immerse the electrode tipin saline and pass a 9 V DC current (regardless of polarity) through it until abubble of gas cleans the contact surface for a period of a few minutes, or youcan use an ultrasound cleaner (Branson 1210, Branson Ultrasonics Corpora-tion, Danbury, CT) by submersing the electrode in the cleaner for 5 minutes.

FIGURE 2.5 Semi-rigid catheter electrode for recording MEPs (D wave) from the spinal cord, epi-or subdurally. The electrode has passed through a 14-gauge Touhy needle for percutaneous place-ment epidurally. To the left (enlarged) are two openings marked with asterisks for flushing the threecylindrical recording contacts (1, 2, 3) through the injection site (top, right).


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Both techniques will remove any film or biological material remaining on theelectrode from the contact surfaces and will decrease their impedance. Thismaneuver will diminish the stimulus artifact, which usually appears when con-tact surfaces have high impedance. Because of the short latency of the D wave,a large stimulus artifact in an uncleaned electrode can pose an insurmountableobstacle for D wave recording.

4.2 PROPER PLACEMENT OF EPIDURAL ELECTRODES

Depending on the surgical procedure, there are two methods of electrode place-ment: percutaneously, or after laminectomy/laminotomy or flavotomy/flavectomy.

4.2.1 Percutaneous Placement of Catheter Electrode

This technique is rather popular in Japan [5]. As used there, it is slightly differ-ent from the one we employ, since the neurosurgeon may ask for a subduralplacement of the catheter electrode. We have performed this procedure to mon-itor the CT during brainstem and supratentorial surgeries where there is high riskof potential damage. Today, because of the increasing popularity of MEPs moni-toring during procedures involving the spinal cord and brainstem, the demand(indications) for percutaneous placement of this type of electrode has dimin-ished. When we do use percutaneous placement, a 14-gauge, thin-wall Touhyneedle (T466LNRH, Becton Dickinson and Comp, Franklin Lakes, NJ; Fig. 2.5),is used for introducing the electrode into the epidural space percutaneously. Fol-lowing percutaneous electrode placement, care must be taken not to withdraw theelectrode while the Touhy needle is in place. Otherwise, the sharp edge of the

FIGURE 2.6 Two traces with a D wave recorded epidurally at the lower cervical spinal cord afterpercutaneous placement of the epidural electrode in a patient with a brain tumor. High impedanceresults in a large artifact (lower trace) which has been reduced (upper trace) after injection of salineinto the epidural space (see Fig. 2.5).



needle could shred the wall of the electrode. The optimal position for penetrat-ing the epidural space with the Touhy needle is the upper thoracic (T1–T2)epidural space. With the needle in this region, the catheter electrode can be gentlypushed up to the level of the lower cervical spinal cord. With this electrode place-ment we can monitor the CT for both the upper and lower extremities by record-ing D waves after selective stimulation of the motor cortex. Appropriate electrodeplacement can be confirmed either by x-ray or by recording epidural SEPs fromthe same electrode after stimulation of the median or ulnar nerves.

In two series consisting of 57 patients [24] and 16 patients [25], no compli-cations from the placement of the electrode occurred (e.g., bleeding, infection,or puncture of the spinal cord). This method requires skills that the anesthesi-ologist practiced in the epidural injection of anesthetics would typically have.

4.2.2 Placement of Electrode after Laminectomy/Laminotomyor Flavectomy/Flavotomy

Our center uses this technique regularly for all procedures that require CT mon-itoring when a laminectomy is performed. These procedures include surgery forthe removal of spinal cord tumors and different surgical interventions on thespinal cord. The surgeon places two catheter electrodes in the epi- or subduralspace at the rostral and caudal edge of the laminectomy. The rostral electrode isthe control electrode for nonsurgically induced changes in the D wave, while thecaudal one monitors the surgically induced changes to the CT (see Fig. 2.1).Massive dural adhesions, usually from previous surgery or after spinal cord radi-ation, can prevent the placement of the catheter electrode. Also, placementbelow the T10 bony level cannot record a D wave of sufficient amplitude becauseof lack of sufficient CT fibers. The control (rostral) electrode cannot be placedin cases of high cervical spinal cord pathology because of the lack of space. Theamplitude of the D wave recorded over the cervical spinal cord could be 60 µVor more, while over thoracic segments it may be only 10 µV. With a stimulatingrate of 2 Hz, it takes two to four averaged responses to get a reliable D wave. Thisresults in an update every second. Unfortunately, the maximal stimulating ratefrom commercially available TES stimulators is 1 stimulus per second.

In surgical procedures in which the spine is exposed but a laminectomy is notperformed (e.g., surgical corrections of scoliosis or dorsal approach to spine stabi-lization), the catheter electrode may be inserted through a flavotomy/flavectomy.

4.3 FACTORS INFLUENCING D AND I WAVE RECORDINGS

D waves represent a neurogram of the CT which is not significantly influencedby nonsurgically induced factors. Stimulation of the CT takes place intracraniallydistal to the cortical motoneuron body, while recording is done caudal to the


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surgical site but above the synapses of the CT at the α-motoneuron. Since nosynapses are involved between the stimulating site and the recording site, theD wave is very stable and reliable. Therefore, we consider D wave recordings tobe the “gold standard” for measuring the functional integrity of the CT.

Still, there exists a few nonsurgically induced changes that will affect the Dwave. Being able to correctly recognize them is essential to giving the surgeonappropriate information. If the exposed spinal cord is cooled, either by cold irri-gation with saline or low operating room temperature, the latency of the Dwave will be temporarily prolonged (Fig. 2.7). Sometimes during stimulation,even with a single stimulus, the epidural electrode can pick up the paraspinalmuscle artifact. This would affect the I wave, but not the D wave, parameters(see Fig. 2.8). If this phenomenon occurs, it is more frequent during cervicalthan thoracolumbar catheter placement.

In contrast to those of others [26], our data demonstrate that volatile anes-thetics do not change the parameters of the D wave by influence on the mem-brane properties of the CT. To demonstrate this, we see that as isofluraneconcentration increases (e.g., >2%), the latency of the D wave gets prolongedwhile the amplitude diminishes (see Fig. 2.9). However, this can be easily cor-rected by increasing the intensity of the current. Therefore, we believe that themechanism by which isoflurane influences the parameters of the D wave isvasodilatation of the cortical blood vessels. Because of the vasodilatation, cur-rent between the stimulating electrodes shunts and activates the CT moresuperficially, resulting in longer latencies of the D wave. The smaller amplitudeof the D wave results from fewer fibers of the CT being activated if current flowssuperficially (Fig. 2.10). A prolongation of the latency and a diminished ampli-tude of the D wave occur only if the CT is activated transcranially. In contrast,this phenomenon is not present when the motor cortex is stimulated directly

FIGURE 2.7 D waves recorded over the lower cervical spinal cord in a patient with an upper cer-vical intramedullary spinal cord tumor, after stimulation with CZ anode/6 cm anterior cathode.Temporary cooling of the exposed spinal cord results in delayed latency of the D and I waves. Afterwarming of the spinal cord, the latency of the D and I waves returned to the previous values.Reprinted from [10].



FIGURE 2.8 Epidurally recorded D and I waves over the cervical spinal cord showing a muscleartifact. After administration of the muscle relaxant, the muscle artifact disappears. The muscle arti-fact affects the I wave, but not the D wave, recordings. S = beginning of transcranially applied stim-ulus. Modified from [10].

FIGURE 2.9 Transcranial electrical stimulation (CZ anode/6 cm anterior cathode) and directelectrical stimulation of the exposed motor leg area with recording of the D wave over the lowerthoracic spinal cord in two different patients. Identical concentrations of isoflurane showed aprominent effect on the amplitude and latency of the D wave (50% decrement of amplitude and0.5 ms prolonged latency after end tidal concentration of 2% isoflurane). This effect is only evidentwhen transcranial electrical stimulation is used. A minimal effect of isoflurane on D wave parame-ters was observed when electrical stimulation was applied to the exposed cortex. Reprinted from [10]and [34].


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through a grid electrode with a short distance between the electrodes. All of theabove observations provide evidence that changes in the D wave are due tomechanisms other than influence on the CT axon membranes.

4.4 NEUROPHYSIOLOGICAL MECHANISMS LEADING

TO THE DESYNCHRONIZATION OF THE D WAVE

In certain patients with spinal cord tumors (usually involving a few segments)the D wave is not recordable at the beginning of surgery [27]. At the same time,muscle MEPs are recordable, even in patients that may not necessarily have amajor motor deficit (Fig. 2.11). The temporal summation of the desynchro-nized D waves occurs at the segmental level. The same phenomenon is presentin patients who undergo radiation of the spinal cord. We believe this is a resultof a desynchronization in conduction of the CT axon. In other words, fast fibersof the CT conduct D waves with different speeds over the site of the lesion orirradiation. Therefore, desynchronized D waves cannot be easily demonstratedcaudal to the lesion site with the present methodology. There are differentgrades of desynchronization, which will be seen as low-amplitude and wide-base D waves (Fig. 2.11A). A higher degree of desynchronization is representedby a nonrecordable D wave (Fig. 2.11B).

Patients who do not have a recordable D wave at the beginning of surgeryare challenging for the monitoring team because they represent a high-riskgroup of patients for injury to the CT. With the present methodology, we canonly monitor them by recording MEPs from limb muscles. Because of the

FIGURE 2.10 To the left, current flow is represented schematically before (white line) and after(grey line) administration of isoflurane. Because of the vasodilatatory effects of isoflurane on thecortical blood vessels, the current between the two stimulating electrodes is shunted, flowingthrough the brain more superficially. This results in a prolonged latency and smaller amplitude ofthe D wave when compared to a D wave elicited with the same intensity of current without isoflu-rane (6.0 ms vs. 6.3 ms, respectively; to the right). At the same time, the disappearance of the I wavecan be observed under the influence of isoflurane.



possibility that transient paraplegia may occur, this is not an ideal monitoringtool. When muscle MEPs disappear during surgery in the patients who do nothave a recordable D wave at baseline, it is not possible to distinguish transientfrom permanent motor deficit intraoperatively (see Section 5.3).

5 RECORDING OF MEPs IN LIMB MUSCLESELICITED BY A MULTIPULSESTIMULATING TECHNIQUE

5.1 SELECTION OF OPTIMAL MUSCLES IN UPPER

AND LOWER EXTREMITIES FOR MEP RECORDINGS

The selection of appropriate muscles to record from is an important issue in themonitoring of MEPs. In certain patients who have deep paresis, not choosingthe optimal muscles can result in “nonmonitorable” patients. The small handmuscle (e.g., abductor pollicis brevis, or APB) is one of the optimal muscles to

FIGURE 2.11 (A) Recording of a D wave cranially (upper trace) and caudally (lower trace) to theintramedullary spinal cord tumor. Note the well-synchronized D wave cranially, in contrast to thedesynchronized D wave caudal to the tumor. (B) Very small epidurally recorded MEPs caudal to ahigh cervical intramedullary tumor (due to extreme desynchronization), despite large muscle MEPsrecorded from a small hand muscle elicited after a short train of six stimuli were present (to theright). Modified from [33].


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monitor the CT for the upper extremities. It has been shown that a good alter-native is the long forearm flexors [28], or even the forearm extensors. Thespinal motoneurons for these muscle groups have rich CT innervation and aretherefore suitable for monitoring the functional integrity of the CT. This is notthe case with the proximal muscle of the arm or of the shoulder (biceps, triceps,or deltoid muscles).

For the lower extremities, abductor hallucis brevis (AHB) is the optimalmuscle because of its dominant CT innervation. In animal experiments, it hasbeen shown that after CT stimulation the highest amplitude of the excitatorypostsynaptic potential (EPSP) has been found in the α-motoneuron pools forthe lower extremities in the small and long flexors of the foot [29]. An alterna-tive to this muscle is the tibialis anterior muscle (TA). Our standard electrodemontage for recording MEPs in the upper and lower extremities are the AHBand TA for the lower extremities and the ABP for the upper extremities.

5.2 NEUROPHYSIOLOGICAL MECHANISMS

FOR ELICITING MEPS USING A MULTIPULSE

STIMULATION TECHNIQUE

Understanding the mechanism involved in the generation of MEPs is essentialfor describing their appropriate use, explaining their behavior, understandingtheir value, and knowing their limits during the monitoring of the CT. Gener-ation of MEPs is more complex in nature than the generation of the D and Iwaves. Therefore, their interpretation, especially during anesthesia, is rathercomplex. Generation of MEPs and their propagation to the end organ (muscle)depends on (a) the excitability of the motor cortex and the CT tract, (b) theconductivity of CT axons, (c) the excitability level of α-motoneuron pools,(d) the role played by the supportive system of the spinal cord (helping toincrease the excitability of α-motoneurons), and (e) the integrity of motornerves, the motor endplates and muscles.

5.2.1 Recovery of Amplitude and Latency of the D Wave

There is a frequency limit for the transmission of descending volleys throughthe CT axons to the α-motoneurons. This limit can be easily tested by apply-ing two identical electrical stimuli transcranially with different interstimulus inter-vals (ISIs). This test can show the recovery time of the second D wave response.



Using this paradigm (conditioning and test stimuli), a D wave recovery curvecan be plotted relative to the amplitude and latency of the second D wave (Fig.2.12). In a paper recently published [30], we show that the optimal ISI for com-plete recovery of the second D wave amplitude and latency is around 4 ms,using a moderate stimulus intensity with a duration of 500 µs. Because the α-motoneuron is optimally bombarded when the train of equal stimuli elicits Dwaves of equal amplitudes, the optimal ISI for muscle activation is expected tobe 4 ms. Fig. 2.13 indicates that with an ISI of 4 ms, three stimuli are sufficientto elicit MEPs because of the complete recovery of each consecutive D wave(Fig. 2.13B3). Comparatively, using the identical stimulus intensity but decreas-ing the ISI to 2 ms, five stimuli are needed to elicit MEPs, which are of even smalleramplitude, because of incomplete recovery of the amplitude of each consecu-tive D wave (Fig. 2.13A5). This rule applies only if a single stimulus elicits asingle D wave (see Section 5.2.3).

FIGURE 2.12 Two diagrams showing the relationship between interstimulus interval (ISI), dura-tion of stimuli, and recovery of the amplitude and latency of the conditioning D wave. Two iden-tical stimuli have been applied transcranially with different ISIs. Amplitude and latency of thesecond D wave (D2) were compared to those of the first one (D1). Note that earlier and completerecovery of the amplitude and latency of the second D wave occurs with a stimulus duration of 500 µsand an ISI of around 4 ms. Reprinted from [30].


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5.2.2 Facilitation of I Wave

We have been shown that three stimuli applied transcranially over the motorcortex can elicit more than three descending volleys in lightly anesthetizedpatients [31]. In Fig. 2.13A3, it is clearly visible that three stimuli generate fourdescending volleys (D1, D2, D3, and an additional I wave). Facilitation of pre-viously nonexisting I waves (after a single stimulus, Fig. 2.13A1) is one of theimportant factors underlying the potency of the multipulse stimulating tech-nique for eliciting MEPs in lightly anesthetized patients. Furthermore, it hasbeen shown that because of the lack of synchronicity of I waves, their recordedamplitude is only one third of their actual amplitude [32]. Certainly, if thepatient is deeply anesthetized, the cortical synapses where the I wave was facil-itated are completely blocked, so this phenomenon does not occur.

5.2.3 Total Number of D and I Waves

As stated previously, to allow for the complete recovery of the D wave, the ISIin the multipulse train should be 4 ms. In situations where a single stimulusgenerates more than a single D wave, the optimal ISI should be set long enoughto allow the entire set of D and I waves to recover, and in turn, to allow the next

FIGURE 2.13 Relationship between MEPs recorded epidurally and from muscle. (A) Train of fivestimuli are needed with an ISI of 2 ms in order to elicit muscle MEPs in tibialis anterior muscle (A5).(B) With an ISI of 4 ms, only three stimuli are needed to elicit muscle MEPs in the tibialis anteriormuscle (B3). D = D wave; I = I wave; PM = paraspinal muscle artifact. Reprinted from [31].



set of D and I waves to fully develop. Therefore, the second stimulus can gen-erate the same pattern of D and I waves (Fig. 2.14). Otherwise, the second setof D and I waves could fall into the CT axon refractory period resulting fromthe first set. This is the case in Fig. 2.14, where a single stimulus generates asingle D wave and multiple I waves (A). In this case only two stimuli, 8 ms apart,were necessary to generate the maximum amplitude of muscle MEPs (Fig. 2.14D).If the ISI is shorter (e.g., 4.1 ms in Fig. 2.14B), partial cancellation of the D andI waves elicited by a second stimulus will occur. Consequently, the total numberof D and I waves will be insufficient to bring an α-motoneuron to the firing leveland MEPs will not be generated. This mechanism could be important in thelightly anesthetized patient as well as in patients with idiopathic scoliosis wherea single stimulus generates multiple I waves (see Fig. 2.2).

5.2.4 Generation of Muscle MEPs Depends on Two Systems:The CT and the Supportive System of the Spinal Cord

To reiterate, descending activity from the CT axons alone is not sufficient togenerate muscle MEPs in anesthetized patients. The other system(s) should beactivated as well. Three examples support this statement:

FIGURE 2.14 (A) In this patient, a single stimulus delivered over the exposed motor hand area elic-its a single D wave and multiple I waves. The ISI should be long enough to prevent the second set ofD and I waves, elicited by a second stimulus, from falling into the CT axon refractory period result-ing from the previous waves (as is the case in trace B). When the ISI is 5.9 ms (C) and 8.0 ms (D),this will not occur, resulting in a sufficient numbers of D and I waves to elicit MEPs (trace D). Thestimulus is marked by an arrow and the D wave by an asterisk. Reprinted from [31].


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A. If the multipulse technique (in a non-deeply anesthetized patient) with arepetition rate of 1 or 2 trains per second is performed, each consecutiveresponse recorded from muscle will have an increasing amplitude. In caseswhere the intensity of stimuli is just slightly above the threshold, the first fewtrains will not generate muscle MEPs at all. At the same time, the D wave ampli-tudes remain the same (Fig. 2.15).

B. In the patients with intramedullary spinal cord tumors presented in Fig.2.16, recording of the D waves from the left and right CT generates symmet-rical D waves cranially and caudally to the tumor site. Yet muscle MEPs are sig-nificantly smaller over the right TA muscle where the patient has clinicalweakness. The presumption is that the current required to elicit MEPs frommuscles on one side of the body is activating only one CT. Therefore, the Dwave, recorded from the spinal cord using this same intensity, must predom-inantly belong to one CT.

C. During surgery for intramedullary spinal cord tumors, muscle MEPs cancompletely disappear with no significant changes in the amplitude of the Dwave (see further transient paraplegia, Fig. 2.17).

These three examples provide convincing evidence that the generation of MEPsinvolves more than just the CT system (see Section 5.3.1).

FIGURE 2.15 Recordings of 10 consecutive muscle MEPs from the right abductor hallucis brevismuscle (after delivering 10 trains consisting of five stimuli, pulse width of 100 µs, intensity of288 mA, stimulus rate of 1 Hz) over C3 anode/C4 cathode in a 60-year-old patient undergoing ante-rior cervical spine decompression and stabilization. Note that after the fifth train the amplitude ofthe muscle MEPs increases 10-fold, showing a tendency to further increase its amplitude.



FIGURE 2.16 Simultaneous recording of the D wave from the right and left CT, cranial and caudalto a midthoracic intramedullary spinal cord tumor (upper), showing a symmetrical amplitude of theD wave. At the same time, muscle MEPs showed significantly smaller amplitude over the right TAmuscle when compared to the left, correlating with the patient’s weakness in the right leg. Thisrecording indicates involvement of pathways other than the CT in the generation of the MEPs.

FIGURE 2.17 Muscle MEPs recorded from right and left TA muscle (left) and D wave recordedepidurally over the lower cervical spinal cord (right). During surgery, muscle MEPs completely dis-appeared while the D wave decreased in amplitude (less than 50%), resulting in transient paraple-gia for this patient during surgery for an intramedullary spinal cord tumor. The patient recoveredcompletely within a week. Reprinted from [33].


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5.3 SURGICALLY INDUCED TRANSIENT PARAPLEGIA

During surgery for intramedullary spinal cord tumors in the thoracic region,MEPs in the TA muscles will frequently disappear while the D wave remainsunaffected. All patients demonstrating this finding during surgery wake upparaplegic (or monoplegic if the TA MEPs disappear in one leg). In patientsin whom we have observed this phenomenon, motor strength is typicallyrecovered in a few hours to a few days following surgery. No permanentmotor deficits have been observed [14, 33] (Fig. 2.17). With almost all casesof transient paraplegia, the first changes are seen in the MEPs and not in theparameters of the D wave. This gives the surgeon a warning sign and awindow of time to plan to end the tumor removal. This is a critical point forintraoperative planning of the extent of tumor removal. If changes in theMEPs do not appear, tumor removal can proceed until a gross total resec-tion is accomplished without the patients having permanent motor deficitspostoperatively.

5.3.1 Neurophysiological Basis for Surgically InducedTransient Paraplegia

Taking into account the previous evidence that the generation of muscle MEPsinvolves more than just the CT, activation of the CT and other descendingsystems within the spinal cord is necessary. We speculate that the pro-priospinal (diffuse) system of the spinal cord is activated by CT axons that arelinked via synaptic connections to the propriospinal system within the spinalcord. In the case of surgically induced transient paraplegia, this system istemporarily compromised by selective surgery while the CT is left intact.After the patient wakes up, other descending systems compensate for the lackof propriospinal tonic influence on α-motoneurons. This results in the fastrecovery of these patients. This suggested mechanism is speculative but froma prognostic and pragmatic point of view is critical because it correlatesextremely well with clinical outcome. Comparatively, if the CT tract is dam-aged during surgery (complete loss of D wave or decrement of the amplitudecompared with the baseline of more than 50%), a permanent motor deficit isexpected [27].

Combining the information about the D wave and about the muscle MEPsduring surgery for intramedullary spinal cord tumors makes this surgery safer,changes the intraoperative strategy, and significantly diminishes the occurrenceof postoperative deficits (see Chapter 4).



6 CONCLUSION

Historically, intraoperative neurophysiology has progressed by means of trialand error. Unfortunately, this has resulted in a number of different opinions asto its utility in documenting and preventing surgically induced neurologicalinjury. In spite of this, the methodology for monitoring the functional integrityof the CT has progressed over the last 10 years into a reliable, fast, and relativelysimple tool that is easily utilized intraoperatively. The development of such asolid methodology has given us reliable and specific data that highly correlatewith neurological outcome postoperatively. This correlation and the publishedsurgical outcome data demonstrate the merits of these techniques.

Further developments in intraoperative neurophysiology should be directedtoward developing a methodology for the functional mapping of the nervoustissue in the exposed brain, brainstem, and spinal cord during surgery. Thefirst steps in this direction have given promising results (see mapping of thedorsal columns, Chapter 7), brainstem cranial motor nuclei (see Chapter 14),and mapping of pudendal afferents (see Chapter 9). We have recently reportedthe first trials using a technique for mapping the CT intraoperatively [35], andwe hope that this technique will evolve into a method for identifying the CTduring exposed brain and spinal cord surgery. Included with the accompany-ing CD is a video showing epidurally recorded D waves and muscle MEPsrecorded from limb muscles during surgery for the removal of an intramed-ullary tumor.

A CD-ROM video presentation will depict actual operating room imple-mentations of these methods (choose Chapter 2 from the accompanying CD’smain menu).

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