intraoperataive monitoring in pediatric neurosurgery

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Received: 10 March 2002Revised: 8 April 2002Published online: 13 June 2002

© Springer-Verlag 2002

Abstract Introduction: This reviewis primarily based on peer-reviewedscientific publications and on the au-

thors’ experience in the field of in-traoperative neurophysiology. Thepurpose is a critical analysis of therole of intraoperative neurophysio-logical monitoring (INM) duringvarious neurosurgical procedures,emphasizing the aspects that mainlyconcern the pediatric population.Original papers related to the field of intraoperative neurophysiology werecollected using medline. INM con-sists in monitoring (continuous “on-line” assessment of the functional in-

tegrity of neural pathways) and map-ping (functional identification andpreservation of anatomically ambig-uous nervous tissue) techniques. Weattempted to delineate indications forintraoperative neurophysiologicaltechniques according to their feasi-bility and reliability (specificity andsensitivity). Discussion and conclu-sions: In compiling this review, con-troversies about indications, method-ologies and the usefulness of someINM techniques have surfaced.

These discrepancies are often due tolack of familiarity with new tech-niques in groups from around theglobe. Accordingly, internationallyaccepted guidelines for INM are stillfar from being established. Never-theless, the studies reviewed providesufficient evidence to enable us tomake the following recommenda-tions. (1) INM is mandatory when-

ever neurological complications areexpected on the basis of a knownpathophysiological mechanism. INM

becomes optional when its role islimited to predicting postoperativeoutcome or it is used for purely re-search purposes. (2) INM should al-ways be performed when any of thefollowing are involved: supratentori-al lesions in the central region andlanguage-related cortex; brain stemtumors; intramedullary spinal cordtumors; conus-cauda equina tumors;rhizotomy for relief of spasticity;spina bifida with tethered cord.(3) Monitoring of motor evoked po-

tentials (MEPs) is now a feasibleand reliable technique that can beused under general anesthesia. MEPmonitoring is the most appropriatetechnique to assess the functional in-tegrity of descending motor path-ways in the brain, the brain stemand, especially, the spinal cord.(4) Somatosensory evoked potential(SEP) monitoring is of value in as-sessment of the functional integrityof sensory pathways leading fromthe peripheral nerve, through the

dorsal column and to the sensorycortex. SEPs cannot provide reliableinformation on the functional integ-rity of the motor system (for whichMEPs should be used). (5) Monitor-ing of brain stem auditory evokedpotentials remains a standard tech-nique during surgery in the brainstem, the cerebellopontine angle,and the posterior fossa. (6) Mapping

Child’s Nerv Syst (2002) 18:264–287DOI 10.1007/s00381-002-0582-3 I N V I T E D PA P E R

Francesco SalaMatevž J. KržanVedran Deletis

Intraoperative neurophysiological monitoring

in pediatric neurosurgery: why, when, how?

F. Sala (✉)Section of Neurosurgery,Department of Neurological Sciencesand Vision, University Hospital,Piazzale Stefani 1, 37121 Verona, Italye-mail: [email protected]

Fax: +39-045-916790M.J. KržanDepartment of Neurology,Pediatric Hospital,University Medical Center, Zaloška 7,Ljubljana, Slovenia

V. DeletisDivision of Intraoperative Neurophysiology,Institute for Neurology and Neurosurgery,Beth Israel Medical Center,Singer Division, New York, NY, USA



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techniques (such as the phase rever-sal and the direct cortical/subcorticalstimulation techniques) are invalu-able and strongly recommended forbrain surgery in eloquent cortex oralong subcortical motor pathways.(7) Mapping of the motor nuclei of

the VIIth, IXth–Xth and XIIth crani-al nerves on the floor of the fourthventricle is of great value in identifi-cation of “safe entry zones” into the

brain stem. Techniques for mappingcranial nerves in the cerebellopon-tine angle and cauda equina havealso been standardized. Other tech-niques, although safe and feasible,still lack a strong validation in termsof prognostic value and correlation

with the postoperative neurologicaloutcome. These techniques includemonitoring of the bulbocavernosusreflex, monitoring of the corticobul-

bar tracts, and mapping of the dorsalcolumns. These techniques, howev-er, are expected to open up new per-spectives in the near future.

Keywords Intraoperativeneurophysiological monitoring ·

Motor evoked potentials ·Somatosensory evoked potentials ·Brain mapping · Spinal cordmonitoring · Pediatric neurosurgery

Introduction

Deemed the “decade of the brain” in America, the 1990ssaw the emergence of several concepts in the neurosci-ences and the establishment of new and sophisticatedtools (e.g., neuronavigation, functional neuroimaging,and robotics), in neurosurgery [87]. For intraoperative

neurophysiological monitoring (INM), the advent of newelectrophysiological stimulation techniques and the de-velopment of more refined anesthesiological strategieshave improved and optimized recording of reliable neu-rophysiological signals in the surgical setting. The fre-quency of publication of papers devoted to intraoperativeneurophysiological techniques or their use in associationwith functional studies (e.g., functional magnetic reso-nance imaging (fMRI), positron emission tomography(PET), magnetoencephalography) has increased dramati-cally over the past few years [17, 51, 54, 64, 89, 102,133, 134, 150]. This increased interest in intraoperativeneurophysiology most likely reflects the demand for safe

and low-risk surgery from the patient, his/her family, andthe surgical team.

INM consists of two main categories of techniques:monitoring and mapping techniques [31]. The term“monitoring” refers to the continuous assessment of thefunctional integrity of neural pathways. The principalgoal of monitoring is expeditious identification of thesource of surgically induced neurophysiological changesto allow prompt correction of the cause before neurologi-cal impairment occurs.

Mapping techniques are those that allow the function-al identification and preservation of anatomically ambig-uous nervous tissue. Neurophysiological mapping is

used to identify a sacral root within a lipoma during un-tethering of the spinal cord, displaced motor cranialnerve nuclei during surgery for brain stem tumors, oreloquent cortex invaded or displaced by a glioma.

Children are as much at risk of neurological deteriora-tion during various neurosurgical procedures as adults,and benefit as much from INM [62]. Some neurophysio-logical techniques commonly used in adults, however,may need technical adjustments to adapt then for use inchildren with their immature nervous systems. Because

of the recent advent and widespread use of neurophysio-logical techniques by several groups with different INMexperiences, controversies about indications for and theusefulness and methodologies of INM have surfaced.The purpose of this paper is a critical review of the roleof INM in various neurosurgical procedures, with theemphasis on aspects concerning mainly the pediatric

population.

Materials and methods

This review is based primarily on peer-reviewed scientific publi-cations and on the authors’ experience in the field of intraopera-tive neurophysiology. Original papers related to the field of intra-operative neurophysiology were collected using Medline. With afew exceptions related to some landmark papers in the field of in-traoperative neurophysiology, we limited the review to the lasttwo decades, in light of the relatively recent advent of intraopera-tive neurophysiological techniques.

In the search from 1982 to the present, general keywords suchas intraoperative neurophysiological monitoring, neurophysiologi-

cal mapping, somato-sensory evoked potentials (SEPs), and motorevoked potentials (MEPs) were initially used. These terms weresubsequently combined with more detailed keywords according tovarious surgical procedures (i.e., brain mapping, phase reversal,bulbocavernosus reflex, cauda equina mapping, brain stem map-ping, and spinal cord motor evoked potentials). Finally, to focuson those papers that deal primarily with the pediatric population,an age criterion was introduced. Some articles that were not in-cluded in the databases but were cited in these articles were alsoincluded in the review.

We attempted to delineate indications for intraoperative neuro-physiological techniques according to their feasibility, reliability(specificity and sensitivity), and level of evidence. Unfortunately,a subdivision of articles according to the classification of evidence –as used by the Brain Trauma Foundation and the American Asso-ciation of Neurological Surgeons [25] – into class I (prospective

randomized control trials), class II (prospective reviews or retro-spective analyses based on clearly reliable data) and class IIIstudies (retrospective clinical series, case reports, expert opinions)is only very weekly applicable in the literature on intraoperativeneurophysiological monitoring. This is because controlled trialsare unlikely to have been conducted, because neurosurgeons whosystematically rely on neurophysiological techniques during sur-gery would be reluctant, from both an ethical and a medico-legalperspective, to withhold intraoperative neurophysiological assis-tance from a designated control group. Consequently, the systemof labeling specific techniques as “standard”, “guideline” or“option” can be less effectively applied to INM.



From a pediatric perspective, it is noteworthy thatchildren below the age of 9–10 years often retain SEPsregardless of the magnitude or width of the myelotomy[79]. It may be speculated that in young children intra-medullary spinal cord tumors start to develop during ges-tation, so that dorsal columns are displaced more lateral-ly; direct recordings of SEPs on the dorsal surface of the

cord with a mini-electrode array might confirm this as-sumption some time in the future [81].

Although SEPs were the only intraoperative monitor-ing tool available a decade ago, today these should beused only in association with MEPs or be limited to cen-ters in which MEP techniques are not available. In fact,although MEPs monitoring cannot yet be considered astandard of care, since the technique is not available inmost neurosurgical centers, MEPs have proved to be re-liable and are likely to become indispensable during spi-nal cord surgery.

The past 15 years have been characterized by a con-tinuous evolution in MEP monitoring. In 1986 Tamaki et

al. [163] introduced the “spinal cord to spinal cord tech-nique,” which means nonselective stimulation of thespinal cord with nonselective recordings from the distantsegments of the spinal cord. Unfortunately, this methoddid not provide specific information on the dorsalcolumns or corticospinal tracts (CTs), and only an over-all evaluation of the preservation of long tracts withinthe cord was possible. Spinal cord to peripheral nerve[119] or spinal cord to muscle [94] techniques have alsobeen introduced. However, α-motoneurons are activatednot only by the CTs but also by any descending tractwithin the cord and/or antidromically by segmentalbranches of the dorsal columns that mediate the H-reflex

[30]. Therefore, selective recordings from the peripheralnerves or muscles generated by electrical stimulation of the spinal cord most likely do not arise purely from theCT [32, 101, 167].

The introduction of transcranial electrical stimulationof the motor cortex [100] was followed by the advent of two different recording techniques. The transcranialsingle stimulus technique allows the recording of theD-wave by an epidural catheter electrode placed epi-or subdurally adjacent to the spinal cord (Fig. 1). Thiswaveform is a highly reliable parameter for monitoringthe functional integrity of the CTs intraoperatively, be-cause it represents a population of fast-conducting fibers

of the CT [26, 71, 124] and it is robust under generalanesthesia [30]. The clinical relevance of this epiduralMEP monitoring lies in the correlation between evokedpotentials and motor outcome [34, 35, 79, 80, 105]. Inour earlier experience, monitorability of epidural MEPs(eMEPs) in adults [105] was a better indicator of func-tional outcome than the patient’s preoperative motor sta-tus. Furthermore, deterioration of eMEPs is mostly in-cremental, giving the surgeon the opportunity to alter thesurgical procedure whenever warning changes occur and

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Spinal cord surgery

In a recent survey on pediatric intramedullary spinalcord tumors, Nadkarni and Rekate [106] reviewed 20 ar-ticles reporting the use of INM during the surgical re-moval of spinal cord tumors. What emerged was a lack of agreement on the role of INM during these proce-

dures. Some authors claim that SEP monitoring duringsurgery for spinal cord tumors accounted for false-posi-tive but not for false-negative results, suggesting thatpostoperative motor deficits were predicted by intraoper-ative changes in SEPs [73]. McCormick et al. [98, 99]found the INM of SEPs to be of only limited value,while for Steinbok et al. [159] intraoperative decisionmaking was not influenced by INM data.

SEPs are still widely used during INM for spine sur-gery, especially scoliosis surgery. In these procedures,derangements of the spinal cord functional integrity,based on distraction maneuvers, are expected to be re-flected in dorsal column injury [112]. During spinal cord

surgery, when preservation of proprioception is of para-mount importance for a patient’s professional or educa-tional goals (e.g., for a musician or an athlete), SEPmonitoring is still of critical value in the decision-making process during spinal cord surgery.

However, the inadequacy of SEPs for reliable moni-toring of the functional integrity of motor pathways inthe spinal cord has already been documented in a num-ber of reports [55, 92, 95, 101, 179]. Unfortunately,over the years, there has been a misleading use of theterm “false-negative” to describe the onset of postoper-ative paraplegia in spite of preserved SEPs. Such anevent should not be described as a “false-negative” re-

sult, since SEPs are not aimed at testing the corticospi-nal pathways. Most likely, using MEPs instead of or incombination with SEPs would have transformed thosefalse-negative into “true-positive” results. A typical ex-ample is the occurrence of an anterior spinal artery syn-drome with the patient reporting postoperative paraple-gia in spite of preserved SEPs [101, 179]. Surgery forintramedullary spinal cord tumors could also exposethe patient to the possibility of separate sensory andmotor pathway impairment [79], and this issue has re-cently been raised in connection with medical malprac-tice trials [3]. Besides lacking specificity for motorpathway monitoring, SEPs rely on an averaging tech-

nique, which requires at least 10–40 s for updating (oreven more in the case of poor-quality SEPs). This delaymay impair the efficacy of INM, since the surgeonmight be warned when insufficient time is left to re-verse the effects of a surgical maneuver. Finally, be-cause of the frequent displacement of dorsal columnssecondary to intramedullary tumors, SEPs are frequent-ly lost during the initial myelotomy and become uselessfor the purposes of INM during the remainder of theprocedure [33, 79].



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before these become irreversible [34, 80]. Finally, in themajority of patients the single-stimulus technique doesnot produce muscle twitches in limb muscles.

Unfortunately, in about one third of patients with spi-nal cord tumors, eMEPs cannot be successfully moni-tored [80]. There are several reasons for this. First, if thetumor is located in the conus/cauda region there are noCT fibers to record eMEPs from an electrode caudal tothe lesion. Secondly, dural adhesions can prevent place-

ment of the electrode at the rostral levels of the cord.Thirdly, extensive tumors, previous surgery and/or radia-tion to the cord may have impaired the conduction prop-erties of the corticospinal axons to the point that theirconduction velocities vary widely and traveling wavesare dispersed and therefore not recordable. We have de-scribed this phenomenon as a “desynchronization’’ of the eMEPs [34]. Again, some distinctions are needed forthe pediatric population, since factors that predict eMEPmonitorability in adults are less applicable to children

[105]. This is most probably because immature neuralstructures are more vulnerable to tumor compression andneoplasms tend to extend to multiple levels (holocordtumors) compared with adults [48, 49].

The single-stimulus technique, however, is not com-pletely appropriate for eliciting MEPs from limb muscles(mMEPs) under general anesthesia. This drawback canbe overcome by using a short train of stimuli (multipulsetechnique) for transcranial stimulation of motor cortex

(Fig. 1) [70, 126, 164]. The advantage of mMEPs is thatthe motor system from the cortex down to the neuromus-cular junction is monitored. This allows for monitoringof the lower motor neuron as well, and the ability to as-sess which extremity is going to be affected. SincemMEPs are more easily blocked by anesthesia and mus-cle relaxant than eMEPs, wide variation in mMEPs am-plitude and latency can be observed [70, 174]. Thus, be-cause of this variability, the correlation between intraop-erative changes in mMEPs’ amplitude and/or latency andthe motor outcome is not linear. Based also on reportswhere the only consistent finding was a correlation be-tween intraoperative mMEP loss and postoperative mo-

tor deterioration [70, 177], we prefer to use yes/no crite-ria for mMEPs, at least in spinal cord surgery [80]. Thecombined use of the single-pulse and multipulse tech-niques utilizes beneficial features of both, while com-pensating for their disadvantages, and allows predictionsof short- and long-term neurological outcome (Table 1)[34, 35]. Whenever D-waves are preserved up to 50% of baseline values and muscle MEPs are preserved at theend of surgery, we expect no additional motor deficitspostoperatively. If mMEP are lost intraoperatively but

Fig. 1 Motor evoked potentials for spinal cord surgery. Left Sche-matic illustration of electrode positions for transcranial electricalstimulation of the motor cortex according to the International10–20 EEG system. The site labeled ‘‘6 cm’’ is 6 cm anterior toCZ. Top right Schematic diagram of the position of the epiduralcatheter eletrode placed caudal to the lesion to monitor the incom-ing signal (eMEPs=D-wave) passing through the site of surgery.A single stimulus of 0.5 ms duration is used. Bottom right Record-ing of mMEPs from the thenar and tibialis anterior muscles aftereliciting them with a short train of electrical stimuli (multipulsetechnique) 4 ms apart. Modified from K. Kothbauer, V. Deletis,

F.J. Epstein (2000) Intraoperative neurophysiological monitoring.In: Crockard A, Hayward R, Hoff JT (eds) Neurosurgery: the sci-entific basis of clinical practice, 3rd edn, p 1042



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D-wave is decreased by less than 50%, the patient willsuffer a so-called “transient paraplegia” but will ulti-mately recover [33, 34, 35]. This phenomenon is proba-bly due to the fact that the supportive system of the spi-nal cord (meaning noncorticospinal descending tractsand the propriospinal system) is predominantly affectedby surgery while fast-conducting corticospinal fibers aremostly preserved, warranting generation of voluntarymotor control. This is consistent with experimentalstudies in cats, where as little as 10% of corticospinal fi-bers were sufficient to support locomotion [22]. So far, a

50% decrease in the eMEP (D-wave) amplitude is con-sidered significant and is used as a point to stop surgicaldissection. Applying these criteria, the combination of eMEP and mMEP monitoring showed a sensitivity of 100% and a specificity of 91% in a series of 100 consec-utive procedures for intramedullary spinal cord tumors[80].

INM during spinal cord surgery is the only tool avail-able for continuous evaluation of the functional integrityof CTs. However, to propose such monitoring as a “stan-dard of care” would require validation of its advantagesthrough a randomized prospective control study compar-ing monitored versus unmonitored surgical operations.

Such a trial is unlikely to be feasible owing to differentlevels of surgical and INM experience at different cen-ters. On the other hand, attempting such a study in a sin-gle institution where INM is routinely performed wouldbe ethically questionable. In a retrospective study [8] ona small population of patients with spinal cord ependy-momas operated on over a 37-year period, the neurologi-cal outcome in patients operated on with the aid of thesurgical microscope and INM was compared with that inpatients operated on before these tool were available.The authors conclude that the microscope and INM areindispensable for improving outcome, but the kind of monitoring (SEPs or MEPs) used is not specified and

there are no data providing statistical support for theadvantages of INM versus those of microsurgery.The role of spinal cord monitoring in scoliosis sur-

gery, being mainly of orthopedic interest, will not be dis-cussed in this paper. However, we should mention a re-cent report on the efficacy of INM for pediatric patientswith spinal cord pathology undergoing spinal deformitysurgery [172]. In these children there were no true-posi-tive or false-negative findings with the use of SEP and/orneurogenic MEP monitoring. However, the false-positive

rate was much higher in this group (27.1%) than in thecontrol group of children with idiopathic scoliosis(1.4%). The lack of true-positive results suggests thatINM was as sensitive to neurological deficits in idio-pathic scoliosis patients as to those in patients with spi-nal cord disease.

Brain surgery

There is increasing evidence to indicate that efforts to

achieve “radical” surgical removal, in both low-gradeand high-grade supratentorial gliomas, are rewarding interms of survival and quality of life. This has been re-ported not only in adults [7, 19, 111, 147] but also inchildren [4, 13, 59, 63, 155, 175]. Dealing with surgeryfor supratentorial tumors, however, raises the issue of eloquent brain areas that must be respected. Posteriorfrontal and anterior parietal lobes, as well as the domi-nant temporal lobe, are all suitable for intraoperativemonitoring and/or mapping in order to localize theRolandic cortex, the descending motor pathways, and thecortical sites responsible for naming and reading.

Neurophysiological mapping techniques are used to

identify cortical anatomical landmarks such us the cen-tral sulcus [27, 173], the primary sensory and motorareas [12, 45, 74, 76, 146], and the frontal and temporalareas related to language [61, 64, 115, 116, 146]. Map-ping techniques have also been introduced to follow mo-tor tracts deep in the brain throughout the internal cap-sule during surgery for deep-seated gliomas, insular tu-mors, and lesions involving the cerebral peduncle [11,39, 41, 42, 44, 85]. Functional regions of the human me-sial cortex have recently been highlighted by intraopera-tive neurophysiological techniques [5]. Finally, by dis-closing a functional cortex in a brain invaded by tumor,neurophysiological brain mapping has questioned the

dogmatic assumption that abnormal tissue cannot retainfunction and can therefore be safely removed [117, 148,152].

It has to be emphasized that, in spite of the high levelof interest in mapping techniques, monitoring techniqueshave received less attention. The identification of func-tionally relevant structures (e.g., the motor cortex, theCT within the internal capsule, and the cerebral pedun-cle) seems to be privileged compared with the continu-ous real-time assessment of their functional integrity.

Table 1 Correlations betweenintraoperative eMEP (D-wave)and mMEP with postoperativemotor outcome. Reprinted from[33]

D-wave Muscle MEPa Motor outcome

Unchanged or 30–50% decrease Preserved UnchangedUnchanged or 30–50% decrease Lost uni- or bilaterally Transient motor deficit>50% decrease Lost bilaterally Long term motor deficit

a In the tibialis anterior muscle(s)



Mapping of the motor cortex and monitoringof corticospinal tracts

The functional integrity of motor pathways can be as-sessed from the primary motor cortex, subcortically tothe corona radiata and the internal capsule and then cau-dally to the cerebral peduncle and the spinal cord. This

assessment can be performed intraoperatively by usingdifferent mapping and monitoring methods.

Berger and Ojemann use a constant-current stimulatorgenerating biphasic square wave pulses with a 60 Hzstimulating rate and 1-ms single-phase duration for map-ping purposes [15]. A bipolar electrode with 5-mm spac-ing between the contact points is used to directly stimu-late the cortex for 2–3 s. If a craniotomy is performedunder general anesthesia, a starting current of 4 mA in-tensity is used, and increased in 2 mA increments up tothe point where movements from the face or limbs areelicited [12, 14, 15]. Movements can either be docu-mented by an observer or recorded by multichannel elec-

tromyography; the latter has been found to be the moresensitive method [176]. If no movements are elicited byusing stimulation as high as 16 mA, that stimulation siteis considered not functional and the corresponding cor-tex can be violated [12]. Since negative stimulation map-ping does not always ensure safety, it is advisable to per-form a generous craniotomy, which allows a wide expo-sure of the cortex and therefore increases the chances of obtaining a positive mapping result. Furthermore, techni-cal or anesthesiological drawbacks such as muscular pa-ralysis and hypotension may account for the lack of re-sponse and should be ruled out.

If a craniotomy is performed in an awake patient, the

threshold is usually lower and movements can be elicitedwith current as low as 2–4 mA [12].

Current intensities similar to, or even lower than,those used for cortical stimulation can be used to mapmotor pathways at the subcortical level. Subcorticalstimulation is indicated not only in attempts to removean infiltrating tumor and the adjacent white matter in themotor areas, but also when tumors occupying the insula,subinsular, or thalamic areas are involved [11, 41, 42,44]. Spreading of the current using the 60-Hz stimulationtechnique is limited to 2–3 mm as detected by opticalimaging in monkeys [60]. Therefore it is feasible to re-move tumors very close to motor and sensory pathways

as long as stimulation is repeated whenever a 2- to 3-mmsection of tumoral tissue is removed. Conversely, removalshould be stopped when movements – and/or paresthesiain the awake patient – are evoked [12].

The aforementioned technique has proved very usefulin maximizing resection while preserving function inadults with brain tumors [15, 43, 45, 76], as well as inchildren [13, 16, 18, 156]. The bipolar 60-Hz stimulationtechnique, which is a modification of the original Pen-field technique, is widely used in the neurosurgical com-

munity. While its feasibility and reliability have beenlargely documented [12, 15, 43, 113, 146], there arenonetheless some drawbacks and limitations that shouldbe taken into consideration.

One concern is the fact that this technique is epilepto-genic. According to Sartorius et al. [145, 146] the inci-dence of intraoperative simple partial seizures during

brain mapping ranges from 5% to 20%, despite therapeu-tic levels of anticonvulsivants and regardless of whetherthere is a preoperative history of intractable epilepsy. Re-cently, the use of direct irrigation of the cortex with coldRinger’s solution has proved effective in stopping sei-zures [145]. It should be noted that the administration of short-acting barbiturates must be avoided, since theymay transiently decrease the excitability of the motorcortex, thereby preventing the use of mapping tech-niques.

Another concern about this technique is whether it issuitable for application in the pediatric population. Inchildren less than 5 years old, direct stimulation of the

motor cortex for mapping purposes may not yield local-izing information because of the relative inexcitability of the motor cortex [56, 65]. For this young population, thephase-reversal technique has been advocated as the bet-ter technique to identify the central sulcus [11].

Third, since this is a mapping and not a monitoringtechnique, no matter how often cortical or subcorticalstimulation is repeated, the functional integrity of themotor pathways cannot be assessed continuously. Be-sides the risk of direct mechanical injury, this wouldleave the patient exposed to the risk of undetected injuryto the motor pathways due to vascular derangements. Forexample, pressure from misplaced retractors or distrac-

tion/lesion to perforating arteries could lead to progres-sive ischemia of the CTs at the level of the corona radi-ata or internal capsule. Vascular mechanisms of injurymay have a gradual onset and take longer than direct me-chanical injury to become evident. Therefore, they canbe better disclosed by using monitoring more than map-ping techniques [28, 76, 77, 108].

Based on these concerns, we prefer a transcranial ordirect cortical multipulse electrical stimulation (Fig. 2).This multipulse stimulation technique allows for a com-bination of monitoring and mapping techniques (Fig. 2)and different stimulation parameters, which have lowrisk of inducing seizures [27, 108, 164]. This technique

differs from Penfield’s technique [127] (which calls forcontinuous stimulation over a period of a few secondswith a frequency of stimulation of 50–60 Hz) in that itrequires only five to seven stimuli placed 4 ms apart,with a repetition rate of up to 2 Hz. The multipulse tech-nique is suitable for continuous monitoring since it doesnot induce strong muscle twitches, which can interferewith the surgical procedure.

Muscle MEPs after transcranial or direct cortical multi-pulse electrical stimulation are recorded by placing needle

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electrodes in the contralateral limb muscles. Muscle MEPsallow us to assess the functional integrity of the whole CTand in our experience have proven feasible for use inyoung children (Fig. 3) [79]. However, some precautions

should be taken in children that are not needed in adults.First, in infants and children under 12–18 months inwhom fontanels are not yet closed, it is preferable to usecup instead of needle or screw-like electrodes in order toavoid penetrating injury. Second, in children who haveventriculoperitoneal shunts, care should be taken not todamage the subcutaneous shunt or valve with the elec-trodes; these could be moved 2 or 3 cm away from theiroriginal position – according to the EEG 10–20 system –if this interferes with the shunt system.

Fig. 2a–d Motor evoked potentials for brain surgery. a An electri-cal stimulation, with a multipulse technique using a short train of five or more stimuli and interstimulus interval of 4 ms, is used.b For monitoring purposes, stimulation is applied either transcra-nially (left ) or, once the dura is open, directly from a strip elec-trode placed on the exposed cortex (right ). For direct cortical stim-ulation, stimulus intensities lower than 20 mA are used. c Formapping purposes, cortical stimulation is obtained using a hand-held monopolar probe, with the same stimulation parameters asused for direct cortical stimulation from the strip electrode. d Re-cording of mMEPs from the controlateral thenar and tibialis ante-rior muscles. Modified from K. Kothbauer, V. Deletis, F.J. Epstein(2000) Intraoperative neurophysiological monitoring. In: CrockardA, Hayward R, Hoff JT (eds) Neurosurgery: the scientific basis of clinical practice, 3rd edn, p 1042

Fig. 3 Motor evoked potentials monitoring in young children. Us-ing the transcranial electrical stimulation with a short train of five

stimuli (ST ) and stimulus intensity of 70 mA we were able torecord and monitor mMEPs in an 11-month-old child operated onfor a right thalamic tumor. Recordings from the right and left ab-ductor pollicis ( RA and LA) and right and left extensor digitorumlongus ( RE and LE ) before (opening) and after (closing) tumor re-moval. For stimulation, the C3/C4 montage was used. The patientwoke up with no additional motor deficits compared with the pre-operative status



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Muscle MEPs elicited by multipulse transcranial elec-trical stimulation have the advantage that they can beelicited and monitored throughout the procedure evenwhen the motor cortex is not exposed or the placementof a strip electrode directly on the cortex is not feasible.However, electrode placement sometimes interferes withcutaneous flaps, so that stimulating electrodes have to be

placed far from their original position overlapping themotor areas. In this setting, currents required to elicitmMEPs might be too high. With stronger electrical stim-ulation, the current penetrates the brain more deeply,stimulating the CTs at different depths from the motorcortex [140]. If the current is very high, depolarization of the CTs may occur at the level of the brain stem/foramenmagnum. In this setting, an injury to the motor pathwaysabove the brain stem might remain undetected and therecould be false-negative results [140].

When feasible, direct stimulation of the motor cortexis therefore the method of choice, since it requires muchlower current intensities than transcranial electrical stim-

ulation and limits the occurrence of muscle twitcheswhich may interfere with microneurosurgery.To localize the central sulcus and therefore the adja-

cent primary motor and sensory areas, the phase-reversaltechnique is used. This technique is based on the princi-ple that a somatosensory evoked potential elicited bymedian nerve stimulation at the wrist can be recordedfrom the primary sensory cortex [56], and its mirror-image waveform can be recorded if the electrode isplaced on the opposite side of the central sulcus, on the

motor cortex (Fig. 4) [27, 173]. If necessary, the proce-

dure could be repeated to delineate the motor strip,whose identification could be challenging when normalcortical anatomy has been modified by an intra-axial le-sion or by previous surgery. The success rate of thephase-reversal technique ranges between 91% [27, 74]and 97% [76]. According to Kombos et al. [76], thecombination of phase reversal and monopolar multipulsecortical stimulation allowed intraoperative localizationof the sensorimotor cortex in 100% of the cases. We alsoprefer to combine phase reversal and direct mapping, aswell as preoperative fMRI data, in order to achieve themost reliable identification of neuroanatomical land-marks around the central region.

We also consider the phase-reversal technique usefulin older children, where maturation of motor pathwayshas been completed, since the phase-reversed potential isquickly obtained and easy to record, and provides reli-able information about identification of the central sul-cus, anticipating the information obtainable with the di-rect mapping of the motor cortex.

For phase reversal a strip with eight silver plate elec-trodes placed 1 cm apart can be used. Once the motorstrip has been identified by the phase-reversal technique,the same electrodes are used as an anode to stimulate themotor cortex directly, while cathode is at Fz. The beststimulation point on the motor cortex for eliciting

mMEPs (i.e., that with the lower threshold to elicitmMEPs from contralateral limbs or face), usually corre-sponds to the electrode from which the largest amplitudeof the mirror image SEPs was obtained (Fig. 4). Thiscorrelation was as high as 93% in Bonn’s group [27].Leaving the strip electrode in a position where it doesnot interfere with the surgeon’s maneuvers allows for acontinuous monitoring of the motor pathways. FormMEP monitoring by direct cortical stimulation we nev-er use stimulating intensities higher than 20 mA. Typi-

Fig. 4 Phase-reversal technique. Central sulcus mapping by the

SEP phase reversal method. A mirror image of the sensoryN20/P30 dipole is recorded from electrodes 7 and 8. Inversion of the polarity occurs between electrodes 6 and 7, thus identifyingthe central sulcus. Electrode 7, the first pre-central electrode, isthen selected for continuous mMEPs monitoring. Reprinted from[33]



cally, we use 5–7 pulses with repetition rate of one persecond (1 Hz), which sometimes requires slightly highercurrent intensities than those required by the bipolar60 Hz technique but significantly reduces the chargeapplied to the brain [136].

Besides continuous monitoring through direct corticalstimulation, brain mapping can be performed with a

monopolar electrode using the same stimulation parame-ters as used for monitoring. Although threshold intensi-ties up to 20 mA are usually accepted for mapping themotor cortex through monopolar stimulation [76, 77,108], it should be noted that lower threshold intensitiesare of more value in localization. In our experience –using a multipulse technique with a short train of fivestimuli, interstimulus interval (ISI) of 4 ms, and a repeti-tion rate of 1–2 Hz – a threshold lower than 5–10 mA foreliciting mMEPs usually indicates proximity to the mo-tor cortex. When muscle responses are elicited throughhigher stimulation intensities, activation of the CTs is of less localizing value, because of the possibility that the

current will spread to adjacent areas. At subcorticallevels, the intensities used to elicit mMEP from the con-trolateral limbs can be as low as 2–3 mA when the stim-ulating probe is on the cerebral peduncle [39] or the in-ternal capsule. When the threshold for obtaining a motorresponse secondary to brain mapping is selected, itshould also be considered that body temperature, bloodpressure and anesthesia can all influence cortical excit-ability [46, 153].

Kombos et al. [75] compared multipulse monopolarand single-pulse bipolar stimulation of the motor cortexin 35 patients during surgery in and around the centralregion. Bipolar stimulation was the most sensitive for

mapping motor areas in the premotor frontal cortex,while monopolar stimulation turned out to be the methodof choice for surgery on the primary motor cortex. Themain advantage of multipulse stimulation is the possibil-ity of recording the motor response continuously (allow-ing monitoring), opposed to the 60-Hz technique, whichcan be used only as a mapping technique because of itsepileptogenicity [28, 77, 108]. Furthermore, the multi-pulse technique can be used transcranially, while the60-Hz technique cannot [108].

One of the advantages of performing neurophysiolog-ical monitoring in addition to mapping becomes evidentwhen subcortical pathways cannot be found by mapping.

In order to verify the preservation of CTs in this situa-tion, there is no need for periodic remapping of the cor-tex at known functional sites [10], because the functionalintegrity of motor pathways is warranted by preservationof mMEPs after continuous multipulse transcranial elec-trical stimulation. Moreover, relying on the elicitabilityof mMEPs after subcortical mapping may be misleading,since the stimulation activates axons distally to the stim-ulation point, but the possibility of damage to the path-ways proximal to that point cannot be ruled out.

While we are not aware of published data on MEPmonitoring during brain surgery exclusively in pediatricseries, our personal experience with extending theabove-mentioned technique for use with children hasbeen satisfactory. In particular, we have successfully per-formed neurophysiological monitoring and mapping inchildren less than 1 year of age by using the multipulse

stimulation technique to elicit mMEPs (Fig. 3). Howeverif, preoperatively, patients have a severe motor deficitwith no antigravity movements, elicitation of MEPs andattempts to perform neurophysiological monitoring willmost probably be unsuccessful.

The parameters for cortical stimulation need to be ad- justed in young children and infants because of the im-maturity of their cortex [136]. Data from the ClevelandClinic and Miami’s Children Hospital suggest that stimu-lation parameters used for cortical mapping in adultsmay be inadequate for cortical stimulation in young chil-dren. The highest thresholds are observed in childrenless than 1 year of age [40, 135]. The Cleveland group

reported the absence of motor responses in children lessthan 3.8 years of age despite electrode placement direct-ly over the Rolandic motor areas [107]. Moreover, func-tional motor responses in children might occur onlywhen intensities above the afterdischarge threshold areused, which is not the case in adults [6]. Increasing boththe stimulus intensity and the pulse duration has proveduseful in reaching a compromise between the need forhigher stimulation intensities and safety issues [69].

To some extent, we have overcome this unsatisfactoryrate of successful mapping in children using a multipulsedirect cortical stimulation paradigm. Regarding transcra-nial electrical stimulation, experience with our stimula-

tion paradigm (500 µs square wave impulses in train of five to seven stimuli, a 4-ms interstimulus interval, andconstant current intensities up to 160 mA) has allowedus to elicit muscle MEPs in over 80% of children withintramedullary spinal cord tumors [79], and we are ob-serving a similar monitorability rate in brain tumor pa-tients.

Some considerations peculiar to surgery for lesions inand around the supplementary motor area must be ad-dressed. During the first few days after surgery, a SMAsyndrome can be sufficiently severe to resemble the clin-ical picture of hemiplegia [86]. However, as observed byPenfield and Welsh 50 years ago [128], unilateral exci-

sion of the SMA produces only transitory motor deficitsand the patient will ultimately recover. Typically, withina few days or weeks, motor function in the arms and thenin the legs will recover, with long-lasting deficits limitedto some impairment in fast alternating movements in thehands [9, 21, 86, 139, 178]. If the SMA in the dominanthemisphere is removed, akinesia can be associated withmuteness, which will also regain completely within afew weeks following surgery [9, 86, 139, 178]. In thissetting, the ability to predict outcome has a positive ef-

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fect on the management of these patients. If the motorcortex and motor pathways are stimulated giving posi-tive results at the end of tumor resection, functional re-covery is the rule and a good motor outcome can beprospected to the patient and his/her family [139, 178]. If necessary, preservation of the CTs can be confirmedpostoperatively by multipulse, rather than single-pulse,

magnetic stimulation [144].

Mapping of language areas of the motor cortex

Whenever a tumor involves brain cortex related to lan-guage, mapping by electrical stimulation is necessary torecognize and preserve these eloquent areas. In the past20 years the classic models of language localization havebeen challenged by brain mapping of language areas us-ing electrical stimulations. By mapping cortical languagesites in 117 patients, Ojemann et al. [115] demonstratedthat language sites in individual patients may be smaller

than what has been described in the traditional Broca-Wernicke model. In most individuals, essential corticalareas for language seems confined to a 2-cm2, or evensmaller, area [113, 114, 115]. However, significant vari-ability between patients would suggest that languagefunction could not be reliably localized solely on the ba-sis of anatomic criteria [115, 116].

Functional MRI [53, 66, 141], magnetoencephalography[122, 151], and PET [64] studies have recently implement-ed preoperative assessment of language localization sites.Compared with intraoperative direct cortical mapping, pre-operative assessment is less dependent on patient coopera-tion and also allows for testing of young patients who might

be too immature and uncooperative to undergo craniotomywhile awake [64]. Unfortunately, the spatial resolution andspecificity of activation with these methods are of insuffi-cient accuracy to be used in making critical surgical deci-sions [64, 66]. To date, functional imaging studies representa useful research tool as much as a useful guide for preoper-ative surgical planning [20, 96, 122, 151]. Functional imag-ing sources, however, cannot yet replace direct corticalstimulation, which remains the best approach for localizingareas related to language in brain surgery.

Berger and Ojemann [11, 14, 115] have developed aclassic stimulation paradigm for language mapping.There are a few fundamental steps in this method, which

should be respected to ensure safe, reliable mapping. Thefirst step is to establish an adequate stimulating currentwhich does not induce seizure activity. If stimulationevokes afterdischarges, which indicate the local convul-sive threshold, current should be reduced by 1 or 2 mA.Second, since the majority of aphasias involve a namingdeficit, stimulation evoked anomia (or dysnomia) is con-sidered significant for a language site. It is therefore crit-ical to select a battery of objects to be named in whichthe basic, preoperative naming error is less than 25%. If

basic naming error is higher than 25%, intraoperativemapping is likely to be unsuccessful. Usually, the samecurrent as has been used to stimulate the motor cortexrepresentation of face should be applied to localizeBroca’s area [12]. In order to confirm localization of Broca’s area it is then mandatory to check movements of the mouth or pharynx to rule out the possibility of a

speech arrest secondary to motor movements more thanto specific stimulation of Broca’s site. Electrocortico-gram (ECoG) should also be continuously monitored todetect subclinical epileptiform activity, which may be asource of naming errors. It is of paramount importance toachieve a positive mapping result, since a negative map-ping might not provide enough confidence to make pro-ceeding with resection an option. A wide exposure of thecerebral cortex increases the possibility of obtaining pos-itive mapping results and, on average, 20 or more corti-cal sites need to be mapped to achieve a positive re-sponse [14]. Every site is tested three separate times, andtwo errors out of three are significant for a language site,

which should be preserved with a margin of at least10 mm [61]. A resection margin of this width from thenearest language site resulted in significantly fewer per-manent language deficits in a series of 40 patients whounderwent awake craniotomy for a glioma in the tempo-ral lobe of the dominant hemisphere [61].

From the technical perspective, it should be stressedthat in contrast to mapping of the sensorimotor cortex,intraoperative mapping for language requires a very co-operative patient and can be performed only duringawake craniotomy. This technique would therefore be of limited value in young children and might be replaced byextraoperative chronic subdural stimulation for language

mapping [16, 136].

Surgery of the peripheral nervous system

In spite of constant improvements in morphological tech-niques, it can be difficult to distinguish nervous structuresand nervous tissue from other tissues during surgical pro-cedures involving the peripheral nervous system. Further-more, regardless of its identification during surgery, ner-vous tissue can be damaged through the use of coagula-tion, traction or compression. This is often reversible if detected early and the cause is eliminated. Mapping tech-

niques should therefore be combined with monitoringtechniques, and since many mapping methods are similarto recording and/or stimulating protocols used in monitor-ing procedures this is often relatively easy to accomplish.

Cauda equina surgery

A relatively high percentage of pediatric neurosurgicalpathology is located in the conus cauda region. In the

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past decade, intraoperative neurophysiological monitor-ing has expanded its applications in this area and, todate, complex and multimodality monitoring and map-ping of the lumbosacral system is available (Fig. 5)[169].

One of the applications of intraoperative neurophysio-logical monitoring is surgery for the tethered spinal cord,where the surgeon cuts the filum terminale or removesthe tethering tissue that envelops the conus and/or thecauda equina nerve roots. In a large series of patients op-erated on for tethered cords, permanent neurologicalcomplications were described in up to 4.5% [29, 121,

131]. This rate increased up to 10.9% when transientcomplications were considered [131]. During surgery of any spinal lesion involving nerve roots, a distinction be-tween functional nervous tissue and fibrous bands ismandatory to avoid postoperative sensorimotor deficitsand/or sphincter and sexual dysfunction. Due to tether-ing, the lumbosacral nerve roots leave the spinal cord ina different direction than in a healthy cord. Furthermore,the cord may be skewed and sometimes a nerve root maypass through a lipoma. Nerve fibers may also be in-

volved in the thickened filum terminale that is cut duringuntethering. Direct stimulation of these structures in thesurgical field, or direct recording from them after periph-eral nerve stimulation, has proved helpful. Using map-ping techniques, functional neural structures of the lum-bosacral region can be correctly identified and thus pos-sibly preserved [78, 88, 120, 129, 130, 131].

Besides the already established mapping of fibers of the dorsal penile/clitoral nerves which enter the spinalcord through the dorsal sacral roots [37], the mappingpossibilities of the sacral nervous system have been ex-panded to include mapping of pudendal afferents from

the anal area [68, 120]. We use a specially designed analplug electrode for this purpose [38, 82].To identify motor nerve roots, direct stimulation is

used and bilateral recording from segmental targetmuscles reveals compound muscle action potentials(CMAPs) in muscles supplied by the stimulated nerveroot of the same side [78, 88]. Recording from segmen-tal target muscles for all relevant myotomes simulta-neously insures that all pertinent motor roots are moni-tored. For recordings from the external anal sphincter

Fig. 5 Intraoperative neuro-physiology of the sacralsystem. Schematic diagram of neurophysiological events usedto monitor and map the sacralnervous system. To the left are“afferent” events after stimula-tion of the dorsal penile/clitoralnerves and recording over thespinal cord. Top PudendalSEPs, traveling waves. MiddlePudendal dorsal root action po-tentials ( DRAP). Bottom Pu-dendal SEPs, stationary wavesrecorded over the conus. To theright are “efferent” events. TopAnal M-wave recorded fromthe anal sphincter after stimula-tion of S1–S3 ventral roots. Middle Anal mMEPs recordedfrom the anal sphincter aftertranscranial electrical stimula-tion of the motor cortex. BottomBulbocavernosus reflex ( BCR)obtained from the anal sphinc-

ter muscle after electrical stim-ulation of the dorsal penile/ clitoral nerve. Reprinted from[33]



muscle, care must be taken to place the wire or needleelectrodes just a few millimeters beneath the skin, sincethe muscle is very thin [137]. Whenever recordings aretaken from muscles, the absence of muscle relaxationhas to be confirmed before mapping or monitoring isperformed. This can easily be done with the train-of-four technique, which should be included in every mon-

itoring protocol.In addition, during untethering procedures or tumor

removal, ongoing inadvertent and still reversible dam-age to the conus or certain nerve roots can be detectedby monitoring. SEPs after stimulation of peripheralnerves, recorded both from the spinal cord with an epi-dural electrode and/or from the scalp, can be used forcontinuous monitoring of the peripheral sensory path-ways. The tibial nerve at the ankle or knee is routinelystimulated for monitoring L5 and S1 root or plexus in-tegrity. Their significant deterioration or loss may be in-dicative of damage to these nerves or correspondingposterior roots. Unfortunately, it is difficult to record

spinal and cortical responses to stimulation of the pu-dendal nerve (S1 to S4 roots), except when the record-ing electrode is placed close to the root entry zone of theroots of S2 to S4.

Besides the long averaging times and response fluc-tuations, the main disadvantage of the use of SEPs forsingle root monitoring is the overlap by adjacent rootsthat can mask a lesion of a single root. DermatomalSEPs have been advocated to get round the last disad-vantage [166]. Since the stimulation is limited to thedermatomal distribution, the response is thought to se-lectively reflect the integrity of one sensory root. Al-though this method has been reported to be useful [166]

it has not been accepted for routine monitoring becauseof low-amplitude responses and resulting difficultieswith interpretation.

The muscles innervated by the lumbosacral segmentsselected for mapping purposes can also be used to moni-tor MEPs elicited by transcranial electrical stimulation,as previously described in this article. This provides im-mediate information about the functional integrity of upper and lower motoneurons. Preservation of muscleMEPs in this setting will ensure preserved motor controlafter surgery. Conceptually, a loss of muscle MEPs incauda/conus surgery indicates a complete lower motorneuron lesion and a postoperative motor deficit, presum-

ably with little tendency to recovery. However, the abili-ty of mMEPs to detect lesions of a single motor root hasbeen questioned and, consequently, this technique is notyet as well established as MEP monitoring during spinalcord surgery [35, 80].

The bulbocavernosus reflex (BCR) is used to assessthe functional integrity of motor and sensory sacralnerve roots as well as the S2 to S4 spinal cord segments[36, 170]. The afferent path is composed of sensory fi-bers of the pudendal nerves, while the efferent part rep-

resents motor fibers to pelvic floor muscles as bulbocav-ernosus or external anal sphincter muscles. Since theBCR is an oligosynaptic reflex it is very susceptible togeneral anesthesia, particularly when volatile anestheticsare used. The BCR is abolished by muscle blockingagents. Therefore, the same anesthesia regimen as out-lined for mMEP monitoring should be used for BCR re-

cordings. Equally, temporal summation is necessary toelicit the BCR under these conditions. This is achievedby using more stimuli, and a short train of stimuli seemsto be optimal [36, 137]. Monitoring the BCR allows fortesting of the functional integrity of three anatomicalstructures (sensory and motor fibers, spinal gray matter).This can be an advantage, but also a drawback, since theBCR can be extremely sensitive and may disappear dueto manipulation of any of the three structures without aclear clinical correlate [33]. A definite advantage is thatthe BCR can be recorded in newborns as old as 24 days[33].

It has been shown that another possibility for continu-

ous monitoring of the functional integrity of S1 and S2spinal levels and sensory motor fibers [90] is the record-ing of the H-reflex from the gastrocnemius muscle aftertibial nerve stimulation at the knee. Intraoperative moni-toring of other spinal reflexes as suggested by Leppanen[91] has not been accepted into routine intraoperativeuse.

Because of the lack of published statistical data col-lected in large groups of patients, reliability and specific-ity of monitoring for conus and cauda equina surgery re-main unclear, or at best anecdotal. In a group of 58 pa-tients who presented with tethered cord syndrome wewere able to record tibial nerve SEPs in 47 (81%), leg

mMEPs in 45 (77.5%) and the BCR in 37 (63.7%) [143].Our experience is in concordance with data of Rodi etal., who suggest that the BCR is more difficult to recordin females owing to technical problems [137]. In ourgroup of patients, one had moderate urinary and anal in-continence before surgery and BCR was not present atbaseline. Postoperatively, this patient presented wors-ened urinary and anal incontinence despite appearance of the BCR at the end of tether release. In another patient aneurogenic bladder developed postoperatively, despiteunchanged intraoperative BCR. The correlation betweensphincter control and BCR is even more complex sincethe BCR cannot detect injury to the suprasegmental path-

ways controlling sphincter activity. This could explainthe discrepancy between clinical and neurophysiologicaldata. To date, the correlation of BCR changes with post-operative sphincter control remain unclear and requireslarger studies for clarification [142, 143]. The limitedprognostic value of BCR becomes obvious in infantswho do not retain sphincter control postoperatively. Newinsights on the role of the intraoperative BCR may comefrom correlations with pre- and postoperative urodynamicevaluation.

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Spinal procedures

The incidence of neurological complications associatedwith the placement of pedicle screws has been reportedto be as high as 11% [97]. A useful technique to pre-vent injury to the spinal roots is pedicle screw stimula-tion. This is a modification of the motor root mapping

technique described earlier. Here, motor roots are indi-rectly stimulated through the screw placed in the verte-bral pedicles. If a low current, applied through the pedi-cle screw, elicits CMAP in appropriate myotomes, thissuggests a cracked pedicle or direct contact of thescrew with the root [165, 168]. The cut-off thresholdsuggesting those possibilities is 10 mA according to theliterature [168]. In our experience it is lower, and weusually consider 7–8 mA as a warning threshold. Tolimit pitfalls in threshold measurement, currents notpassing exclusively through the screw should be avoid-ed. This can be done by proper insulation of instru-ments used to apply current and by keeping the surgical

field dry [168]. In patients with neuropathy the thresh-olds can be much higher, even with direct stimulation[168].

Neurosurgery for spasticity

In children with severe, incapacitating spasticity, whichis often a result of cerebral palsy, selective dorsal rhizo-tomy is performed to improve their quality of life andmotor performance [1, 154]. The assumption is that re-flex hyperactivity at the spinal level is due in these chil-dren to a release from supraspinal control, which in-

creases the tonus of leg and foot musculature [1, 154].Reflex activity is not only increased, but also spreads tomuscles beyond the corresponding myotome. Even con-tralateral muscles may be activated by stimulation of aninvolved sensory root. This procedure can be performedwithout significant sensory loss because of overlappinginnervation of the dermatomes by fibers from differentsensory roots. In these cases, mapping is used not be-cause anatomy is distorted but because it is impossible todetermine by inspection which root is involved in in-creased reflex activity [2, 52, 109, 110]. Furthermore, itis morphologically not possible to determine which sac-ral roots carry a significant amount of pudendal afferent

fibers and tremendous individual variability exists in thedistribution of the sensory pudendal fibers entering thespinal cord through dorsal sacral roots [37, 67]. There-fore, functional intraoperative testing is necessary toidentify these roots.

Inclusion of the S2 root has been shown to be benefi-cial in these patients, because it relieves the correspond-ing plantar spasticity produced by involvement of the S2posterior root in plantar reflex arches [84]. Unfortunate-ly, in a significant number of individuals the S2 roots

carry afferent fibers from the pudendal nerves, so that le-sioning them can result in additional sphincter and sexu-al dysfunction. In order to relieve spasticity in the plan-tar flexor muscles that are mainly innervated by S2, andat the same time avoid urogenital side effects, pudendalafferent mapping was introduced. This has reduced theincidence of urinary complications from 24% to 0% [37,

67].Steinbok and Kestle [158] and Staudt et al. [157] have

recently emphasized variation in the neurophysiologictechniques used in different centers during these proce-dures. A description of the technique we currently usenow follows [1].

Following surgical exposure of the lumbosacral rootsthe surgeon records the electrical activity of sacral rootswith a sterile hook electrode after electrical stimulationof the dorsal penile/clitoral nerves. Bilateral testing of S1, S2 and S3 roots determines the “map” of the contri-butions of pudendal afferent fibers in these sacral dorsalroots. Only S2 roots without pudendal afferents can be

cut. When it is essential to cut S2 roots (because theyare known to contribute significantly to the generationof spasticity) separation of the rootlets has to be per-formed and each rootlet is separately tested in the sameway.

A large group of patients who underwent this proce-dure showed that the use of this method can prevent per-manent urinary complications [67]. Patients in whom S2roots are cut show a postoperative decrease in the extentof residual plantar spasticity [84]. It is of interest thatmapping of pudendal afferents in 114 patients who un-derwent selective dorsal rhizotomy frequently showedasymmetric entry of pudendal afferents into the spinal

cord. Extreme asymmetry of pudendal afferents wasfound in 7.6% of these patients. Their afferents from theright and left pudendal nerves entered the spinal cord viaa single S2 root [67].

Although some controversy still exists [118], puden-dal anal afferents should also be identified to spare thoseroots involved in bowel function [123, 125].

Once the pudendal mapping has been done, selectivedorsal rhizotomy can start. After direct stimulation of asensory nerve root, CMAPs from appropriate musclescan be recorded; these are generated in a similar way tothe H-reflex, but instead of the peripheral nerve, the dor-sal roots are stimulated. This technique allows for the

identification of which roots from L2 to S2 are involvedin increased reflex activity and contributing to spasticityin the lower limb muscles. A set-up for reflex measure-ments is used with multichannel recordings from seg-mental target muscles with needle or surface electrodes.This allows visual display of a spreading response on themonitor. Muscle responses can also be detected manuallyby an experienced physical therapist palpating for tonicmuscle contraction during stimulation. Apparently thereis little difference in sensitivity for contractions between

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the manual detection and the electromyographic record-ing [1]. Stimulation is performed through modified sur-gical dissectors with proximal insulation and a bare tip(single stimuli of 200 µs duration, 0.5–3 mA). First, themotor threshold is determined with a single stimulus par-adigm of one stimulus every second (1 Hz). Then theroots are stimulated at these thresholds with a 50-Hz

train for 1 s. Those posterior roots that produce a spread-ing response, i.e. those that elicit tonic muscle contrac-tion beyond their corresponding myotome, are cut. If twoadjacent roots have to be cut at least 50% of a third, adjacent to one of these, must be preserved. This impliesmicrosurgical splitting of posterior roots into rootlets todetermine the spreading contribution of each rootlet [1,154]. Stimulus intensity should also be carefully adjust-ed to distinguish the reflex or non-reflex nature of a dor-sal root-evoked response [93].

In the opinion of many neurosurgeons, mapping ismandatory for this type of surgery although there are dis-crepancies between theory and intraoperative observa-

tions [1, 109, 110, 118, 123, 157, 171]. Unequivocal evi-dence that children treated using the above theoreticalapproach have better functional outcome than thosetreated using only clinical judgment is still lacking [1,160, 171].

Brain stem surgery

The brain stem is a part of the nervous system where ahigh concentration of different nerve structures is found ina small space. Therefore, even small incision injuries tothe brain stem can result in severe neurological complica-tions. Lesioning these areas can be life threatening (e.g.,

damage to cardiovascular or respiratory centers) or havedebilitating consequences (e.g., coma, loss of spontaneousbreathing, hemiplegia, dysphagia, dysarthria) [132].

Brain stem tumors occur quite frequently in the pedi-atric population [24, 149]. Therefore, pediatric neurosur-geons dealing with these pathologies should be aware of the neurophysiological methods available to pre-vent/document neurological injury to the brain stem. Ac-cording to Fahlbusch and Strauss [50], classic intraoper-

Fig. 6 Mapping of the brain stem cranial nerve motor nuclei. Left:Schematic drawing of the exposed floor of the fourth ventricle,with the surgeon’s hand-held stimulator in view. Middle: Sites of insertion of wire hook electrodes for recording the muscle re-sponses. Right: Compound muscle action potentials recorded fromthe orbicularis oculi and oris muscles after stimulation of the up-per and lower facial nuclei (upper two panels) and compound ac-tion potentials recorded from the pharyngeal wall and tongue mus-cles after stimulation of the motor nuclei of IXth/Xth and XIIthcranial nerves (lower two panels). Inset: Photograph from operat-ing microscope showing stimulating probe on the floor of thefourth ventricle. (Reprinted from [39])



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ative neurophysiological methods (e.g., SEPs and brainstem auditory evoked potentials) can evaluate only 20%of the brain stem. Furthermore, data obtained with thesemethods cannot be obtained in real time, having a delayof a minute or so. Thus, we will briefly describe recentlydeveloped methods for mapping and monitoring thebrain stem’s functional integrity. Some of these methodsare still evolving and require extensive evaluation inlarger numbers of patients. Nevertheless, mapping tech-niques (to identify the functional anatomy of the brain

stem) combined with monitoring techniques (to assessthe functional integrity of long tracts and cranial nervenuclei within the brain stem) provide exhaustive intraop-erative neurophysiological assistance to the surgeon.

Mapping techniques: neurophysiological localizationof the motor cranial nerve nuclei on the floorof the fourth ventricle

A number of relatively safe “entry zones” have been pro-posed for the brain stem [23, 83]. These surgical routesallow lesions to be approached from the upper brainstem caudally to the cervicomedullary junction. Unfortu-nately, classic anatomical landmarks – such as the facialcolliculus or the striae medullares – are often displacedby the tumor or are hardly identifiable, even in patientsin whom the anatomy has not been distorted [39].

The initial incision through the floor of the fourth ventri-cle can injure motor nuclei of the cranial nerves (VII, IX, X,XII). The same is true for the motor nuclei of cranial nervesIII, IV and VI of the upper brain stem. A neurophysiologi-cal technique for intraoperative identification of these nu-clei has recently been developed [72, 103, 161, 162]. Thistechnique is based on intraoperative electrical stimulation of the motor nuclei of the cranial nerves using a hand-heldstimulator. Stimulation elicits CMAPs in the musculatureinnervated by the cranial motor nerves (Fig. 6).

Fig. 7 Typical patterns of cranial nerve motor nuclei displacementby brain stem tumors in different locations. Above: Upper (left )and lower (right ) pontine tumors: pontine tumors typically grow topush the facial nuclei around the edge of the tumor, suggestingthat precise localization of the facial nuclei before tumor resectionis necessary to avoid damaging them during surgery. Below left:

Medullary tumors: medullary tumors typically grow more exo-phytically and compress the lower cranial nerve motor nuclei ven-trally; these nuclei may be located on the ventral edge of the tu-mor cavity. Because of the interposed tumor, in these cases map-ping before tumor resection usually does not allow identificationof motor nuclei of the IXth/Xth and XIIth cranial nerves. Respons-es, however, could be obtained close to the end of the tumor resec-tion, when most of the tumoral tissue between the stimulatingprobe and the motor nuclei has been removed. At this point, repeatmapping is recommended because the risk of damaging motor nu-clei is significantly higher than at the beginning of tumor debul-king. Right: Cervicomedullary junction spinal cord tumors; thesetumors simply push the lower cranial nerve motor nuclei rostrallywhen extending into the fourth ventricle. Reprinted from [104]



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This method means that neurophysiological “visual-ization” of the anatomical position of those nuclei isachieved. Thus, in order to prevent injury to the previ-ously mentioned structures, which are often displacedfrom their original anatomical positions by the tumor, theinitial incision into the brain stem can be safely placed.Furthermore, Morota et al. [104] used this method to re-

veal a repeatable displacement pattern of the motor nu-clei of the cranial nerves corresponding to the growthpattern of brain stem tumors (Fig. 7).

Monitoring techniques

Continuous monitoring of the functional integrity of cra-nial motor nuclei and nerves is still unsatisfactory. Theavailable techniques are based on the recording of theongoing electromyographic (EMG) activity in the mus-cles innervated by cranial nerves [47, 57, 138]. However,the correlation between intraoperative EMG activity and

postoperative outcome is still a matter of debate. Grabbet al. [57] did not reach conclusive results that wouldhave proved that EMG of the VIth and VIIth cranialnerves enhanced operative safety or facilitated aggres-sive removal during surgery for fourth ventricle tumors.Conversely, Romstock et al. [138] have recently pro-posed warning criteria based on detailed analyses of EMG waveforms during cerebellopontine angle surgery.

The possibility of monitoring corticobulbar pathwaysby recording MEPs from the facial, laryngeal and tonguemuscles after transcranial stimulation is currently underinvestigation and may prove to be a useful monitoringtool in the near future.

In the case of lesions close to the cerebral peduncle orthe ventral part of the medulla, injury to the CTs be-comes a major concern to the surgeon. Similarly to whatdescribed for spinal cord surgery, mMEP and eMEP canbe elicited transcranially and monitored throughout theprocedure. Using a similar approach, the CT, lying onthe base of the cerebral pedunculi, could be identified bydirect electrical stimulation during recording from thespinal cord in the form of a D wave (Fig. 8) [39]. Thismethod seems very promising and could prevent lesion-ing of the highly concentrated fibers of the CT duringthe initial incision to the cerebral pedunculi.

Owing to the complexity of the brain stem’s function-

al anatomy, the choice of the most appropriate battery of neurophysiological tests should be used for each singlepatient. However, a prompt evaluation of the functionalintegrity of brain stem’s structures is warranted only bythe combined use of multiple monitoring techniques. So,while monitoring only BAEPs, only SEPs or only corti-cospinal/corticobulbar MEPs can be misleading, the ra-tional integration of data from all these modalities willprovide the most reliable assessment of brain stem integ-rity (see Table 2).

Unsolved problems, from a neurophysiological per-spective, remain eye movement coordination deficits andpostoperative swallowing deficits. Monitoring and map-ping of the internuclear fascicles have not yet been es-tablished. Similarly, neurophysiological tests for intraop-erative monitoring of the afferent branch of the swallow-ing reflex are still lacking. Besides descending control tothe motor nuclei of the glossopharyngeal and vagal

nerves, preservation of the afferent arch of this reflex asmuch as of the interneurons involved in the coordinatedact of swallowing is necessary to warrant function.

Anesthesia and INM

The complex relationship between anesthetic agents andintraoperative recordings of evoked potentials deserves adiscussion that is beyond the scope of this review. We

Fig. 8 Mapping of the corticospinal tract. Mapping of the cortico-spinal tract (CT ) on the cerebral peduncle during surgery for re-moval of a left cerebral peduncle tumor in a 27-year-old woman isshown schematically. The cerebral peduncle is being mapped by ahand-held monopolar probe (upper right ). As the probe neared theCT, responses were recorded from an epidural catheter (upper

left ). Responses were consistently repeatable. Stimulation intensi-ty was 2 mA, stimulating rate was 4 Hz, and four responses wereaveraged. Reprinted from [39]



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therefore refer the reader to the pertinent literature for adetailed analysis of the anesthesiological management of patients who undergo INM during neurosurgical proce-dures. In our experience, continuous infusion of propofoland fentanyl – with no boluses –, avoiding halogenatedagents and muscle relaxants after intubation, has provedfeasible and suitable for most of the procedures.

Conclusions

The concept of identifying physiological/pathophysiolog-ical aspects in the operating room by linking functionalinformation to advanced imaging is one path of progressneurosurgery and neuroscience are taking. As we usethese techniques and slowly understand how they work,we are learning how little we understand about them sofar. We are just scratching the surface of a large body of knowledge that we will eventually learn to use better inorder to refine neurosurgical treatment even further.

There follows a brief set of primers as to the “why,when, and how” of monitoring during pediatric neuro-

surgery.

Why?

Intraoperative neurophysiological monitoring has severalpurposes. (1) To enable the surgeon to change his strate-gy in order to prevent neurological complications. (2) Toconfirm that the strategy adopted by the surgeon is ap-propriate and encourage more aggressive surgery in

the case of lesions amenable to total removal and cure.(3) To predict neurological outcome and therefore im-prove the postoperative management of children andtheir families. (4) To provide information useful for ret-rospective analysis and possible adjustment of surgicalstrategies. (5) To provide documentation for medicolegalpurposes. (6) Last but not least, INM allows investiga-tion of the pathophysiology of neurosurgical diseases af-fecting the developing nervous system and can therefore

be used as an educational tool for young neurosurgeons.

When?

Indications for intraoperative monitoring vary in the dif-ferent centers around the world. While priorities should bedefined according to scientific, economic and medico-legal issues at each single institution, INM is mandatorywhenever the expected neurological complication is deter-mined by a known pathophysiological mechanismthat can only be prevented by INM. INM becomes option-al when its role is limited to predicting postoperative out-come [58] or it is being used purely for research purposes.

Below we summarize methods of INM and their indi-cations with reference to pediatric neurosurgical proce-dures, as presented in Table 2.

Brain surgery in the central region and alongsubcortical motor pathways

For surgery in and around the central region, or along thesubcortical motor pathways, cortical and subcortical

Table 2 When and how to monitor in pediatric neurosurgery( BAEP brainstem auditory evoked potentials; BCR bulbocaverno-sus reflex; DRAP dorsal root action potential; EMG electromyog-

raphy; eMEPs epidural motor evoked potentials; mMEPs musclemotor evoked potentials; SEPs somatosensory evoked potentials;CT corticospinal tract)

Procedures Mapping techniques Monitoring techniques

Brain surgery in the central region and Phase reversal Cortical SEPsalong subcortical motor pathways Direct cortical and subcortical mapping (with the mMEPs after multipulse electrical

‘‘60 Hz” or the multipulse technique) transcranial or cortical stimulation

Brain surgery in speech areas Direct cortical mappinga None

Posterior fossa and brainstem surgery Direct mapping of motor nuclei of the cranial BAEPnerves in the floor of the fourth ventricleDirect mapping of the CT within the cerebral Cortical SEPspeduncle mMEPs or eMEPs

Continuous EMG recording of muscleinnervated by motor cranial nerves

Spinal cord surgery Dorsal column mapping Cortical SEPs or epidural (spinal) SEPsmMEPs and eMEPs

Conus-cauda surgery Pudendal DRAP mapping Cortical SEPsMotor roots mapping Pudendal (spinal) SEPs

mMEPs (anal mMEPs included)BCR

Rhizotomy for relief of spasticity Pudendal DRAP mapping None

Motor roots mappinga Only the 60 Hz technique in the awake patient can be used intraoperatively



mapping techniques should be considered standard.These techniques allow for the intraoperative functional –rather than anatomical – identification of eloquent corti-cal areas and subcortical localization of the CT. Patternsof cortical plasticity or reorganization induced by the tu-mor may be disclosed. The phase-reversal techniqueidentifies the border between primary motor and sensory

areas. This information should then be confirmed by di-rect stimulation of the motor cortex.

To map and monitor the functional integrity of themotor cortex and the CT, the multi-pulse technique, al-though less commonly used, offers the advantage of con-tinuous intraoperative monitoring of MEPs. The particu-lar advantage of this technique is that it can be used fortranscranial stimulation. Although still considered op-tional, we strongly suggest neurophysiological monitor-ing as an invaluable adjunct to mapping during brain sur-gery. Finally, cortical SEPs can be used to monitor thefunctional integrity of dorsal sensory pathways.

Brain surgery in speech areas

Intraoperative mapping of cortical areas related to lan-guage is feasible only after craniotomy in awake pa-tients. Thus, this can limit its application in young chil-dren. Mapping of the language areas should be conduct-ed exclusively with the 60 Hz stimulation technique.

Posterior fossa and brain stem surgery

Particularly for brain stem surgery, the more techniques

can be reasonably integrated, the more likely it is that suc-cessful monitoring can be conducted. SEP, mMEP and/oreMEP, and BAEP monitoring should always be used.These techniques provide both specific information abouta particular system (motor, sensory or auditory), and lessspecific information about the “well-being” of the brainstem. Additional techniques should be tailored on the ba-sis of the tumor level and extension. For example, at themidbrain level, mapping of the cerebral peduncle may beadded to the battery of neurophysiological tests.

At the level of the pons and upper medulla, mappingof the motor nuclei of the cranial nerves on the floor of the fourth ventricle will assist the surgeon in choosing

the less dangerous entry zones into the brain stem. Theperipheral portion of the facial cranial nerve can also beidentified in the cerebellopontine angle by direct stimu-lation. Continuous EMG recording from the facial mus-cles (orbicularis oculi, orbicularis oris) provides feed-back on the spontaneous and manipulation-induced ac-tivity of the facial cranial nerve. Unfortunately, the neu-roprotective role of this latter monitoring technique isstill controversial, as is its correlation with the postoper-ative clinical functioning of the facial nerve.

During surgery at the cervicomedullary junction,mapping of the fourth ventricle allows for the identifica-tion of the motor nuclei of cranial nerves IX, X, and XII.Continuous monitoring of the integrity of the lower mo-tor cranial nerves (X and XII) should be added. This canbe performed by EMG recording directly from the pha-ryngeal and tongue muscles, but the same limitations as

discussed for the facial nerve apply.The standardization of techniques currently consid-

ered “experimental” (such as monitoring of corticobulbarpathways) will hopefully augment brain stem monitoringin the near future.

Spinal cord surgery

In the spine and, above all, during spinal cord surgery,both SEPs and mMEPs/eMEPs should be used. To favorSEPs over MEPs is not justified from a scientific back-ground. Although MEPs are still not available in many

intraoperative neurophysiological departments, their useshould be encouraged since MEPs represent the most ap-propriate and reliable tool to assess the functional integ-rity of descending motor tracts. Dorsal column mappingis an “experimental” technique that will hopefully assistin the future during myelotomies for excision of intra-medullary spinal cord tumor.

Conus-cauda equina surgery

Mapping techniques should be used during conus-caudaequina surgery to identify the filum terminale and the

motor and sensory lumbosacral roots. This informationcan be invaluable during rhizotomy for the relief of spas-ticity, during untethering of the spinal cord, or during theremoval of conus-cauda equina tumors. Besides map-ping, continuous monitoring of mMEPs from lower ex-tremity muscles and the anal sphincters (together withcortical SEPs) provide on-line feedback about the func-tional integrity of these structures during their manipula-tions. BCR monitoring can be added to assess the integ-rity of pudendal afferent and efferent pathways as well asof the sacral segments of the spinal cord from S2 to S4.However, the prognostic value of this monitoring modal-ity, with respect to genitourinary function, continues to

be debated.

How?

The role of the neurophysiologist is: first, to extract neu-rophysiological data; second, to analyze these data im-mediately in order to recognize neurophysiological pat-terns promptly; third, to integrate these patterns criticallywith intraoperative clinical features to avoid false-posi-

281



282

tive or false-negative results; fourth, to warn the neuro-surgeon in time, before irreversible injury to the nervoustissue has occurred. A multimodality INM combining in-formation from SEPs, MEPs and other monitoring andmapping modalities increases the sensitivity of INM.Nevertheless, INM should be kept as simple as possible.

Close collaboration with both the surgeon and the an-

esthesiologist, making sure that everybody understands

everybody else’s job, is one of the key factors in success-ful monitoring.

Finally, INM should be performed only by skilledneurophysiologists or neuroscientists (neurologists, neu-rosurgeons, neuroanesthesiologists) who have been spe-cifically trained in intraoperative monitoring. We shouldkeep in mind the adage that no monitoring is better than

bad monitoring.

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