Childs Nerv Syst (2002) 18:264287 DOI 10.

1007/s00381-002-0582-3

I N V I T E D PA P E R

Francesco Sala Matev J. Kran Vedran Deletis

Intraoperative neurophysiological monitoring in pediatric neurosurgery: why, when, how?

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

F. Sala () Section of Neurosurgery, Department of Neurological Sciences and Vision, University Hospital, Piazzale Stefani 1, 37121 Verona, Italy e-mail: francescosala@yahoo.com Fax: +39-045-916790 M.J. Kran Department of Neurology, Pediatric Hospital, University Medical Center, Zaloka 7, Ljubljana, Slovenia V. Deletis Division of Intraoperative Neurophysiology, Institute for Neurology and Neurosurgery, Beth Israel Medical Center, Singer Division, New York, NY, USA

Abstract Introduction: This review is primarily based on peer-reviewed scientific publications and on the authors experience in the field of intraoperative neurophysiology. The purpose is a critical analysis of the role of intraoperative neurophysiological monitoring (INM) during various neurosurgical procedures, emphasizing the aspects that mainly concern the pediatric population. Original papers related to the field of intraoperative neurophysiology were collected using medline. INM consists in monitoring (continuous online assessment of the functional integrity of neural pathways) and mapping (functional identification and preservation of anatomically ambiguous nervous tissue) techniques. We attempted to delineate indications for intraoperative neurophysiological techniques according to their feasibility and reliability (specificity and sensitivity). Discussion and conclusions: In compiling this review, controversies about indications, methodologies and the usefulness of some INM techniques have surfaced. These discrepancies are often due to lack of familiarity with new techniques in groups from around the globe. Accordingly, internationally accepted guidelines for INM are still far from being established. Nevertheless, the studies reviewed provide sufficient evidence to enable us to make the following recommendations. (1) INM is mandatory when-

ever neurological complications are expected on the basis of a known pathophysiological mechanism. INM becomes optional when its role is limited to predicting postoperative outcome or it is used for purely research purposes. (2) INM should always be performed when any of the following are involved: supratentorial lesions in the central region and language-related cortex; brain stem tumors; intramedullary spinal cord tumors; conus-cauda equina tumors; rhizotomy for relief of spasticity; spina bifida with tethered cord. (3) Monitoring of motor evoked potentials (MEPs) is now a feasible and reliable technique that can be used under general anesthesia. MEP monitoring is the most appropriate technique to assess the functional integrity of descending motor pathways in the brain, the brain stem and, especially, the spinal cord. (4) Somatosensory evoked potential (SEP) monitoring is of value in assessment of the functional integrity of sensory pathways leading from the peripheral nerve, through the dorsal column and to the sensory cortex. SEPs cannot provide reliable information on the functional integrity of the motor system (for which MEPs should be used). (5) Monitoring of brain stem auditory evoked potentials remains a standard technique during surgery in the brain stem, the cerebellopontine angle, and the posterior fossa. (6) Mapping

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techniques (such as the phase reversal and the direct cortical/subcortical stimulation techniques) are invaluable and strongly recommended for brain surgery in eloquent cortex or along subcortical motor pathways. (7) Mapping of the motor nuclei of the VIIth, IXthXth and XIIth cranial nerves on the floor of the fourth ventricle is of great value in identification of safe entry zones into the

brain stem. Techniques for mapping cranial nerves in the cerebellopontine angle and cauda equina have also been standardized. Other techniques, although safe and feasible, still lack a strong validation in terms of prognostic value and correlation with the postoperative neurological outcome. These techniques include monitoring of the bulbocavernosus reflex, monitoring of the corticobul-

bar tracts, and mapping of the dorsal columns. These techniques, however, are expected to open up new perspectives in the near future. Keywords Intraoperative neurophysiological monitoring Motor evoked potentials Somatosensory evoked potentials Brain mapping Spinal cord monitoring Pediatric neurosurgery

Introduction
Deemed the decade of the brain in America, the 1990s saw the emergence of several concepts in the neurosciences and the establishment of new and sophisticated tools (e.g., neuronavigation, functional neuroimaging, and robotics), in neurosurgery [87]. For intraoperative neurophysiological monitoring (INM), the advent of new electrophysiological stimulation techniques and the development of more refined anesthesiological strategies have improved and optimized recording of reliable neurophysiological signals in the surgical setting. The frequency of publication of papers devoted to intraoperative neurophysiological techniques or their use in association with functional studies (e.g., functional magnetic resonance imaging (fMRI), positron emission tomography (PET), magnetoencephalography) has increased dramatically over the past few years [17, 51, 54, 64, 89, 102, 133, 134, 150]. This increased interest in intraoperative neurophysiology most likely reflects the demand for safe and low-risk surgery from the patient, his/her family, and the surgical team. INM consists of two main categories of techniques: monitoring and mapping techniques [31]. The term monitoring refers to the continuous assessment of the functional integrity of neural pathways. The principal goal of monitoring is expeditious identification of the source of surgically induced neurophysiological changes to allow prompt correction of the cause before neurological impairment occurs. Mapping techniques are those that allow the functional identification and preservation of anatomically ambiguous nervous tissue. Neurophysiological mapping is used to identify a sacral root within a lipoma during untethering of the spinal cord, displaced motor cranial nerve nuclei during surgery for brain stem tumors, or eloquent cortex invaded or displaced by a glioma. Children are as much at risk of neurological deterioration during various neurosurgical procedures as adults, and benefit as much from INM [62]. Some neurophysiological techniques commonly used in adults, however, may need technical adjustments to adapt then for use in children with their immature nervous systems. Because

of the recent advent and widespread use of neurophysiological techniques by several groups with different INM experiences, controversies about indications for and the usefulness and methodologies of INM have surfaced. The purpose of this paper is a critical review of the role of INM in various neurosurgical procedures, with the emphasis on aspects concerning mainly the pediatric population.

Materials and methods

This review is based primarily on peer-reviewed scientific publications and on the authors experience in the field of intraoperative neurophysiology. Original papers related to the field of intraoperative neurophysiology were collected using Medline. With a few exceptions related to some landmark papers in the field of intraoperative neurophysiology, we limited the review to the last two decades, in light of the relatively recent advent of intraoperative neurophysiological techniques. In the search from 1982 to the present, general keywords such as intraoperative neurophysiological monitoring, neurophysiological mapping, somato-sensory evoked potentials (SEPs), and motor evoked potentials (MEPs) were initially used. These terms were subsequently combined with more detailed keywords according to various surgical procedures (i.e., brain mapping, phase reversal, bulbocavernosus reflex, cauda equina mapping, brain stem mapping, and spinal cord motor evoked potentials). Finally, to focus on those papers that deal primarily with the pediatric population, an age criterion was introduced. Some articles that were not included in the databases but were cited in these articles were also included in the review. We attempted to delineate indications for intraoperative neurophysiological 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 Association of Neurological Surgeons [25] into class I (prospective randomized control trials), class II (prospective reviews or retrospective analyses based on clearly reliable data) and class III studies (retrospective clinical series, case reports, expert opinions) is only very weekly applicable in the literature on intraoperative neurophysiological monitoring. This is because controlled trials are unlikely to have been conducted, because neurosurgeons who systematically rely on neurophysiological techniques during surgery would be reluctant, from both an ethical and a medico-legal perspective, to withhold intraoperative neurophysiological assistance from a designated control group. Consequently, the system of labeling specific techniques as standard, guideline or option can be less effectively applied to INM.

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Spinal cord surgery

In a recent survey on pediatric intramedullary spinal cord tumors, Nadkarni and Rekate [106] reviewed 20 articles reporting the use of INM during the surgical removal of spinal cord tumors. What emerged was a lack of agreement on the role of INM during these procedures. Some authors claim that SEP monitoring during surgery for spinal cord tumors accounted for false-positive but not for false-negative results, suggesting that postoperative motor deficits were predicted by intraoperative 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 decision making was not influenced by INM data. SEPs are still widely used during INM for spine surgery, especially scoliosis surgery. In these procedures, derangements of the spinal cord functional integrity, based on distraction maneuvers, are expected to be reflected in dorsal column injury [112]. During spinal cord surgery, when preservation of proprioception is of paramount importance for a patients professional or educational goals (e.g., for a musician or an athlete), SEP monitoring is still of critical value in the decisionmaking process during spinal cord surgery. However, the inadequacy of SEPs for reliable monitoring of the functional integrity of motor pathways in the spinal cord has already been documented in a number of reports [55, 92, 95, 101, 179]. Unfortunately, over the years, there has been a misleading use of the term false-negative to describe the onset of postoperative paraplegia in spite of preserved SEPs. Such an event should not be described as a false-negative result, since SEPs are not aimed at testing the corticospinal pathways. Most likely, using MEPs instead of or in combination with SEPs would have transformed those false-negative into true-positive results. A typical example is the occurrence of an anterior spinal artery syndrome with the patient reporting postoperative paraplegia in spite of preserved SEPs [101, 179]. Surgery for intramedullary spinal cord tumors could also expose the patient to the possibility of separate sensory and motor pathway impairment [79], and this issue has recently been raised in connection with medical malpractice trials [3]. Besides lacking specificity for motor pathway monitoring, SEPs rely on an averaging technique, which requires at least 1040 s for updating (or even more in the case of poor-quality SEPs). This delay may impair the efficacy of INM, since the surgeon might be warned when insufficient time is left to reverse the effects of a surgical maneuver. Finally, because of the frequent displacement of dorsal columns secondary to intramedullary tumors, SEPs are frequently lost during the initial myelotomy and become useless for the purposes of INM during the remainder of the procedure [33, 79].

From a pediatric perspective, it is noteworthy that children below the age of 910 years often retain SEPs regardless of the magnitude or width of the myelotomy [79]. It may be speculated that in young children intramedullary spinal cord tumors start to develop during gestation, so that dorsal columns are displaced more laterally; direct recordings of SEPs on the dorsal surface of the cord with a mini-electrode array might confirm this assumption some time in the future [81]. Although SEPs were the only intraoperative monitoring tool available a decade ago, today these should be used only in association with MEPs or be limited to centers in which MEP techniques are not available. In fact, although MEPs monitoring cannot yet be considered a standard of care, since the technique is not available in most neurosurgical centers, MEPs have proved to be reliable and are likely to become indispensable during spinal cord surgery. The past 15 years have been characterized by a continuous evolution in MEP monitoring. In 1986 Tamaki et al. [163] introduced the spinal cord to spinal cord technique, which means nonselective stimulation of the spinal cord with nonselective recordings from the distant segments of the spinal cord. Unfortunately, this method did not provide specific information on the dorsal columns or corticospinal tracts (CTs), and only an overall evaluation of the preservation of long tracts within the cord was possible. Spinal cord to peripheral nerve [119] or spinal cord to muscle [94] techniques have also been introduced. However, -motoneurons are activated not only by the CTs but also by any descending tract within the cord and/or antidromically by segmental branches of the dorsal columns that mediate the H-reflex [30]. Therefore, selective recordings from the peripheral nerves or muscles generated by electrical stimulation of the spinal cord most likely do not arise purely from the CT [32, 101, 167]. The introduction of transcranial electrical stimulation of the motor cortex [100] was followed by the advent of two different recording techniques. The transcranial single stimulus technique allows the recording of the D-wave by an epidural catheter electrode placed epior subdurally adjacent to the spinal cord (Fig. 1). This waveform is a highly reliable parameter for monitoring the functional integrity of the CTs intraoperatively, because it represents a population of fast-conducting fibers of the CT [26, 71, 124] and it is robust under general anesthesia [30]. The clinical relevance of this epidural MEP monitoring lies in the correlation between evoked potentials and motor outcome [34, 35, 79, 80, 105]. In our earlier experience, monitorability of epidural MEPs (eMEPs) in adults [105] was a better indicator of functional outcome than the patients preoperative motor status. Furthermore, deterioration of eMEPs is mostly incremental, giving the surgeon the opportunity to alter the surgical procedure whenever warning changes occur and

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Fig. 1 Motor evoked potentials for spinal cord surgery. Left Schematic illustration of electrode positions for transcranial electrical stimulation of the motor cortex according to the International 1020 EEG system. The site labeled 6 cm is 6 cm anterior to CZ. Top right Schematic diagram of the position of the epidural catheter eletrode placed caudal to the lesion to monitor the incoming signal (eMEPs=D-wave) passing through the site of surgery. A single stimulus of 0.5 ms duration is used. Bottom right Recording of mMEPs from the thenar and tibialis anterior muscles after eliciting them with a short train of electrical stimuli (multipulse technique) 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 scientific basis of clinical practice, 3rd edn, p 1042

before these become irreversible [34, 80]. Finally, in the majority of patients the single-stimulus technique does not produce muscle twitches in limb muscles. Unfortunately, in about one third of patients with spinal cord tumors, eMEPs cannot be successfully monitored [80]. There are several reasons for this. First, if the tumor is located in the conus/cauda region there are no CT fibers to record eMEPs from an electrode caudal to the lesion. Secondly, dural adhesions can prevent placement of the electrode at the rostral levels of the cord. Thirdly, extensive tumors, previous surgery and/or radiation to the cord may have impaired the conduction properties of the corticospinal axons to the point that their conduction velocities vary widely and traveling waves are dispersed and therefore not recordable. We have described this phenomenon as a desynchronization of the eMEPs [34]. Again, some distinctions are needed for the pediatric population, since factors that predict eMEP monitorability in adults are less applicable to children

[105]. This is most probably because immature neural structures are more vulnerable to tumor compression and neoplasms tend to extend to multiple levels (holocord tumors) compared with adults [48, 49]. The single-stimulus technique, however, is not completely appropriate for eliciting MEPs from limb muscles (mMEPs) under general anesthesia. This drawback can be overcome by using a short train of stimuli (multipulse technique) for transcranial stimulation of motor cortex (Fig. 1) [70, 126, 164]. The advantage of mMEPs is that the motor system from the cortex down to the neuromuscular junction is monitored. This allows for monitoring of the lower motor neuron as well, and the ability to assess which extremity is going to be affected. Since mMEPs are more easily blocked by anesthesia and muscle relaxant than eMEPs, wide variation in mMEPs amplitude and latency can be observed [70, 174]. Thus, because of this variability, the correlation between intraoperative changes in mMEPs amplitude and/or latency and the motor outcome is not linear. Based also on reports where the only consistent finding was a correlation between intraoperative mMEP loss and postoperative motor deterioration [70, 177], we prefer to use yes/no criteria for mMEPs, at least in spinal cord surgery [80]. The combined use of the single-pulse and multipulse techniques utilizes beneficial features of both, while compensating for their disadvantages, and allows predictions of 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 the end of surgery, we expect no additional motor deficits postoperatively. If mMEP are lost intraoperatively but

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Table 1 Correlations between intraoperative eMEP (D-wave) and mMEP with postoperative motor outcome. Reprinted from [33]

D-wave Unchanged or 3050% decrease Unchanged or 3050% decrease >50% decrease

a In

Muscle MEPa Preserved Lost uni- or bilaterally Lost bilaterally

Motor outcome Unchanged Transient motor deficit Long term motor deficit

the tibialis anterior muscle(s)

D-wave is decreased by less than 50%, the patient will suffer a so-called transient paraplegia but will ultimately recover [33, 34, 35]. This phenomenon is probably due to the fact that the supportive system of the spinal cord (meaning noncorticospinal descending tracts and the propriospinal system) is predominantly affected by surgery while fast-conducting corticospinal fibers are mostly preserved, warranting generation of voluntary motor control. This is consistent with experimental studies in cats, where as little as 10% of corticospinal fibers were sufficient to support locomotion [22]. So far, a 50% decrease in the eMEP (D-wave) amplitude is considered significant and is used as a point to stop surgical dissection. 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 consecutive procedures for intramedullary spinal cord tumors [80]. INM during spinal cord surgery is the only tool available for continuous evaluation of the functional integrity of CTs. However, to propose such monitoring as a standard of care would require validation of its advantages through a randomized prospective control study comparing monitored versus unmonitored surgical operations. Such a trial is unlikely to be feasible owing to different levels of surgical and INM experience at different centers. On the other hand, attempting such a study in a single institution where INM is routinely performed would be ethically questionable. In a retrospective study [8] on a small population of patients with spinal cord ependymomas operated on over a 37-year period, the neurological outcome in patients operated on with the aid of the surgical microscope and INM was compared with that in patients operated on before these tool were available. The authors conclude that the microscope and INM are indispensable for improving outcome, but the kind of monitoring (SEPs or MEPs) used is not specified and there are no data providing statistical support for the advantages of INM versus those of microsurgery. The role of spinal cord monitoring in scoliosis surgery, being mainly of orthopedic interest, will not be discussed in this paper. However, we should mention a recent report on the efficacy of INM for pediatric patients with spinal cord pathology undergoing spinal deformity surgery [172]. In these children there were no true-positive or false-negative findings with the use of SEP and/or neurogenic MEP monitoring. However, the false-positive

rate was much higher in this group (27.1%) than in the control group of children with idiopathic scoliosis (1.4%). The lack of true-positive results suggests that INM was as sensitive to neurological deficits in idiopathic scoliosis patients as to those in patients with spinal cord disease.

Brain surgery
There is increasing evidence to indicate that efforts to achieve radical surgical removal, in both low-grade and high-grade supratentorial gliomas, are rewarding in terms of survival and quality of life. This has been reported not only in adults [7, 19, 111, 147] but also in children [4, 13, 59, 63, 155, 175]. Dealing with surgery for supratentorial tumors, however, raises the issue of eloquent brain areas that must be respected. Posterior frontal and anterior parietal lobes, as well as the dominant temporal lobe, are all suitable for intraoperative monitoring and/or mapping in order to localize the Rolandic cortex, the descending motor pathways, and the cortical sites responsible for naming and reading. Neurophysiological mapping techniques are used to identify cortical anatomical landmarks such us the central sulcus [27, 173], the primary sensory and motor areas [12, 45, 74, 76, 146], and the frontal and temporal areas related to language [61, 64, 115, 116, 146]. Mapping techniques have also been introduced to follow motor tracts deep in the brain throughout the internal capsule during surgery for deep-seated gliomas, insular tumors, and lesions involving the cerebral peduncle [11, 39, 41, 42, 44, 85]. Functional regions of the human mesial cortex have recently been highlighted by intraoperative neurophysiological techniques [5]. Finally, by disclosing a functional cortex in a brain invaded by tumor, neurophysiological brain mapping has questioned the dogmatic assumption that abnormal tissue cannot retain function and can therefore be safely removed [117, 148, 152]. It has to be emphasized that, in spite of the high level of interest in mapping techniques, monitoring techniques have received less attention. The identification of functionally relevant structures (e.g., the motor cortex, the CT within the internal capsule, and the cerebral peduncle) seems to be privileged compared with the continuous real-time assessment of their functional integrity.

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Mapping of the motor cortex and monitoring of corticospinal tracts The functional integrity of motor pathways can be assessed from the primary motor cortex, subcortically to the corona radiata and the internal capsule and then caudally to the cerebral peduncle and the spinal cord. This assessment can be performed intraoperatively by using different mapping and monitoring methods. Berger and Ojemann use a constant-current stimulator generating biphasic square wave pulses with a 60 Hz stimulating rate and 1-ms single-phase duration for mapping purposes [15]. A bipolar electrode with 5-mm spacing between the contact points is used to directly stimulate the cortex for 23 s. If a craniotomy is performed under general anesthesia, a starting current of 4 mA intensity is used, and increased in 2 mA increments up to the point where movements from the face or limbs are elicited [12, 14, 15]. Movements can either be documented by an observer or recorded by multichannel electromyography; the latter has been found to be the more sensitive method [176]. If no movements are elicited by using stimulation as high as 16 mA, that stimulation site is considered not functional and the corresponding cortex can be violated [12]. Since negative stimulation mapping does not always ensure safety, it is advisable to perform a generous craniotomy, which allows a wide exposure of the cortex and therefore increases the chances of obtaining a positive mapping result. Furthermore, technical or anesthesiological drawbacks such as muscular paralysis and hypotension may account for the lack of response and should be ruled out. If a craniotomy is performed in an awake patient, the threshold is usually lower and movements can be elicited with current as low as 24 mA [12]. Current intensities similar to, or even lower than, those used for cortical stimulation can be used to map motor pathways at the subcortical level. Subcortical stimulation is indicated not only in attempts to remove an infiltrating tumor and the adjacent white matter in the motor 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 stimulation technique is limited to 23 mm as detected by optical imaging in monkeys [60]. Therefore it is feasible to remove tumors very close to motor and sensory pathways as long as stimulation is repeated whenever a 2- to 3-mm section of tumoral tissue is removed. Conversely, removal should be stopped when movements and/or paresthesia in the awake patient are evoked [12]. The aforementioned technique has proved very useful in maximizing resection while preserving function in adults with brain tumors [15, 43, 45, 76], as well as in children [13, 16, 18, 156]. The bipolar 60-Hz stimulation technique, which is a modification of the original Penfield technique, is widely used in the neurosurgical com-

munity. While its feasibility and reliability have been largely documented [12, 15, 43, 113, 146], there are nonetheless some drawbacks and limitations that should be taken into consideration. One concern is the fact that this technique is epileptogenic. According to Sartorius et al. [145, 146] the incidence of intraoperative simple partial seizures during brain mapping ranges from 5% to 20%, despite therapeutic levels of anticonvulsivants and regardless of whether there is a preoperative history of intractable epilepsy. Recently, the use of direct irrigation of the cortex with cold Ringers solution has proved effective in stopping seizures [145]. It should be noted that the administration of short-acting barbiturates must be avoided, since they may transiently decrease the excitability of the motor cortex, thereby preventing the use of mapping techniques. Another concern about this technique is whether it is suitable for application in the pediatric population. In children less than 5 years old, direct stimulation of the motor cortex for mapping purposes may not yield localizing information because of the relative inexcitability of the motor cortex [56, 65]. For this young population, the phase-reversal technique has been advocated as the better technique to identify the central sulcus [11]. Third, since this is a mapping and not a monitoring technique, no matter how often cortical or subcortical stimulation is repeated, the functional integrity of the motor pathways cannot be assessed continuously. Besides the risk of direct mechanical injury, this would leave the patient exposed to the risk of undetected injury to the motor pathways due to vascular derangements. For example, pressure from misplaced retractors or distraction/lesion to perforating arteries could lead to progressive ischemia of the CTs at the level of the corona radiata or internal capsule. Vascular mechanisms of injury may have a gradual onset and take longer than direct mechanical injury to become evident. Therefore, they can be better disclosed by using monitoring more than mapping techniques [28, 76, 77, 108]. Based on these concerns, we prefer a transcranial or direct cortical multipulse electrical stimulation (Fig. 2). This multipulse stimulation technique allows for a combination of monitoring and mapping techniques (Fig. 2) and different stimulation parameters, which have low risk of inducing seizures [27, 108, 164]. This technique differs from Penfields technique [127] (which calls for continuous stimulation over a period of a few seconds with a frequency of stimulation of 5060 Hz) in that it requires only five to seven stimuli placed 4 ms apart, with a repetition rate of up to 2 Hz. The multipulse technique is suitable for continuous monitoring since it does not induce strong muscle twitches, which can interfere with the surgical procedure. Muscle MEPs after transcranial or direct cortical multipulse electrical stimulation are recorded by placing needle

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Fig. 2ad Motor evoked potentials for brain surgery. a An electrical 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 transcranially (left) or, once the dura is open, directly from a strip electrode placed on the exposed cortex (right). For direct cortical stimulation, stimulus intensities lower than 20 mA are used. c For mapping purposes, cortical stimulation is obtained using a handheld monopolar probe, with the same stimulation parameters as used for direct cortical stimulation from the strip electrode. d Recording of mMEPs from the controlateral thenar and tibialis anterior muscles. Modified from K. Kothbauer, V. Deletis, F.J. Epstein (2000) Intraoperative neurophysiological monitoring. In: Crockard A, Hayward R, Hoff JT (eds) Neurosurgery: the scientific basis of clinical practice, 3rd edn, p 1042

electrodes in the contralateral limb muscles. Muscle MEPs allow us to assess the functional integrity of the whole CT and in our experience have proven feasible for use in young children (Fig. 3) [79]. However, some precautions should be taken in children that are not needed in adults. First, in infants and children under 1218 months in whom fontanels are not yet closed, it is preferable to use cup instead of needle or screw-like electrodes in order to avoid penetrating injury. Second, in children who have ventriculoperitoneal shunts, care should be taken not to damage the subcutaneous shunt or valve with the electrodes; these could be moved 2 or 3 cm away from their original position according to the EEG 1020 system if this interferes with the shunt system.

Fig. 3 Motor evoked potentials monitoring in young children. Using the transcranial electrical stimulation with a short train of five stimuli (ST) and stimulus intensity of 70 mA we were able to record and monitor mMEPs in an 11-month-old child operated on for a right thalamic tumor. Recordings from the right and left abductor pollicis (RA and LA) and right and left extensor digitorum longus (RE and LE) before (opening) and after (closing) tumor removal. For stimulation, the C3/C4 montage was used. The patient woke up with no additional motor deficits compared with the preoperative status

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Fig. 4 Phase-reversal technique. Central sulcus mapping by the SEP phase reversal method. A mirror image of the sensory N20/P30 dipole is recorded from electrodes 7 and 8. Inversion of the polarity occurs between electrodes 6 and 7, thus identifying the central sulcus. Electrode 7, the first pre-central electrode, is then selected for continuous mMEPs monitoring. Reprinted from [33]

Muscle MEPs elicited by multipulse transcranial electrical stimulation have the advantage that they can be elicited and monitored throughout the procedure even when the motor cortex is not exposed or the placement of a strip electrode directly on the cortex is not feasible. However, electrode placement sometimes interferes with cutaneous flaps, so that stimulating electrodes have to be placed far from their original position overlapping the motor areas. In this setting, currents required to elicit mMEPs might be too high. With stronger electrical stimulation, the current penetrates the brain more deeply, stimulating the CTs at different depths from the motor cortex [140]. If the current is very high, depolarization of the CTs may occur at the level of the brain stem/foramen magnum. In this setting, an injury to the motor pathways above the brain stem might remain undetected and there could be false-negative results [140]. When feasible, direct stimulation of the motor cortex is therefore the method of choice, since it requires much lower current intensities than transcranial electrical stimulation and limits the occurrence of muscle twitches which may interfere with microneurosurgery. To localize the central sulcus and therefore the adjacent primary motor and sensory areas, the phase-reversal technique is used. This technique is based on the principle that a somatosensory evoked potential elicited by median nerve stimulation at the wrist can be recorded from the primary sensory cortex [56], and its mirrorimage waveform can be recorded if the electrode is placed on the opposite side of the central sulcus, on the

motor cortex (Fig. 4) [27, 173]. If necessary, the procedure could be repeated to delineate the motor strip, whose identification could be challenging when normal cortical anatomy has been modified by an intra-axial lesion or by previous surgery. The success rate of the phase-reversal technique ranges between 91% [27, 74] and 97% [76]. According to Kombos et al. [76], the combination of phase reversal and monopolar multipulse cortical stimulation allowed intraoperative localization of the sensorimotor cortex in 100% of the cases. We also prefer to combine phase reversal and direct mapping, as well as preoperative fMRI data, in order to achieve the most reliable identification of neuroanatomical landmarks around the central region. We also consider the phase-reversal technique useful in older children, where maturation of motor pathways has been completed, since the phase-reversed potential is quickly obtained and easy to record, and provides reliable information about identification of the central sulcus, anticipating the information obtainable with the direct mapping of the motor cortex. For phase reversal a strip with eight silver plate electrodes placed 1 cm apart can be used. Once the motor strip has been identified by the phase-reversal technique, the same electrodes are used as an anode to stimulate the motor cortex directly, while cathode is at Fz. The best stimulation point on the motor cortex for eliciting mMEPs (i.e., that with the lower threshold to elicit mMEPs from contralateral limbs or face), usually corresponds to the electrode from which the largest amplitude of the mirror image SEPs was obtained (Fig. 4). This correlation was as high as 93% in Bonns group [27]. Leaving the strip electrode in a position where it does not interfere with the surgeons maneuvers allows for a continuous monitoring of the motor pathways. For mMEP monitoring by direct cortical stimulation we never use stimulating intensities higher than 20 mA. Typi-

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cally, we use 57 pulses with repetition rate of one per second (1 Hz), which sometimes requires slightly higher current intensities than those required by the bipolar 60 Hz technique but significantly reduces the charge applied to the brain [136]. Besides continuous monitoring through direct cortical stimulation, brain mapping can be performed with a monopolar electrode using the same stimulation parameters as used for monitoring. Although threshold intensities up to 20 mA are usually accepted for mapping the motor cortex through monopolar stimulation [76, 77, 108], it should be noted that lower threshold intensities are of more value in localization. In our experience using a multipulse technique with a short train of five stimuli, interstimulus interval (ISI) of 4 ms, and a repetition rate of 12 Hz a threshold lower than 510 mA for eliciting mMEPs usually indicates proximity to the motor cortex. When muscle responses are elicited through higher stimulation intensities, activation of the CTs is of less localizing value, because of the possibility that the current will spread to adjacent areas. At subcortical levels, the intensities used to elicit mMEP from the controlateral limbs can be as low as 23 mA when the stimulating probe is on the cerebral peduncle [39] or the internal capsule. When the threshold for obtaining a motor response secondary to brain mapping is selected, it should also be considered that body temperature, blood pressure and anesthesia can all influence cortical excitability [46, 153]. Kombos et al. [75] compared multipulse monopolar and single-pulse bipolar stimulation of the motor cortex in 35 patients during surgery in and around the central region. Bipolar stimulation was the most sensitive for mapping motor areas in the premotor frontal cortex, while monopolar stimulation turned out to be the method of choice for surgery on the primary motor cortex. The main advantage of multipulse stimulation is the possibility of recording the motor response continuously (allowing monitoring), opposed to the 60-Hz technique, which can be used only as a mapping technique because of its epileptogenicity [28, 77, 108]. Furthermore, the multipulse technique can be used transcranially, while the 60-Hz technique cannot [108]. One of the advantages of performing neurophysiological monitoring in addition to mapping becomes evident when subcortical pathways cannot be found by mapping. In order to verify the preservation of CTs in this situation, there is no need for periodic remapping of the cortex at known functional sites [10], because the functional integrity of motor pathways is warranted by preservation of mMEPs after continuous multipulse transcranial electrical stimulation. Moreover, relying on the elicitability of mMEPs after subcortical mapping may be misleading, since the stimulation activates axons distally to the stimulation point, but the possibility of damage to the pathways proximal to that point cannot be ruled out.

While we are not aware of published data on MEP monitoring during brain surgery exclusively in pediatric series, our personal experience with extending the above-mentioned technique for use with children has been satisfactory. In particular, we have successfully performed neurophysiological monitoring and mapping in children less than 1 year of age by using the multipulse stimulation technique to elicit mMEPs (Fig. 3). However if, preoperatively, patients have a severe motor deficit with no antigravity movements, elicitation of MEPs and attempts to perform neurophysiological monitoring will most probably be unsuccessful. The parameters for cortical stimulation need to be adjusted in young children and infants because of the immaturity of their cortex [136]. Data from the Cleveland Clinic and Miamis Children Hospital suggest that stimulation parameters used for cortical mapping in adults may be inadequate for cortical stimulation in young children. The highest thresholds are observed in children less than 1 year of age [40, 135]. The Cleveland group reported the absence of motor responses in children less than 3.8 years of age despite electrode placement directly over the Rolandic motor areas [107]. Moreover, functional motor responses in children might occur only when intensities above the afterdischarge threshold are used, which is not the case in adults [6]. Increasing both the stimulus intensity and the pulse duration has proved useful in reaching a compromise between the need for higher stimulation intensities and safety issues [69]. To some extent, we have overcome this unsatisfactory rate of successful mapping in children using a multipulse direct cortical stimulation paradigm. Regarding transcranial electrical stimulation, experience with our stimulation paradigm (500 s square wave impulses in train of five to seven stimuli, a 4-ms interstimulus interval, and constant current intensities up to 160 mA) has allowed us to elicit muscle MEPs in over 80% of children with intramedullary spinal cord tumors [79], and we are observing a similar monitorability rate in brain tumor patients. Some considerations peculiar to surgery for lesions in and around the supplementary motor area must be addressed. During the first few days after surgery, a SMA syndrome can be sufficiently severe to resemble the clinical picture of hemiplegia [86]. However, as observed by Penfield and Welsh 50 years ago [128], unilateral excision of the SMA produces only transitory motor deficits and the patient will ultimately recover. Typically, within a few days or weeks, motor function in the arms and then in the legs will recover, with long-lasting deficits limited to some impairment in fast alternating movements in the hands [9, 21, 86, 139, 178]. If the SMA in the dominant hemisphere is removed, akinesia can be associated with muteness, which will also regain completely within a few weeks following surgery [9, 86, 139, 178]. In this setting, the ability to predict outcome has a positive ef-

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fect on the management of these patients. If the motor cortex and motor pathways are stimulated giving positive results at the end of tumor resection, functional recovery is the rule and a good motor outcome can be prospected to the patient and his/her family [139, 178]. If necessary, preservation of the CTs can be confirmed postoperatively 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 language, mapping by electrical stimulation is necessary to recognize and preserve these eloquent areas. In the past 20 years the classic models of language localization have been challenged by brain mapping of language areas using electrical stimulations. By mapping cortical language sites in 117 patients, Ojemann et al. [115] demonstrated that language sites in individual patients may be smaller than what has been described in the traditional BrocaWernicke model. In most individuals, essential cortical areas for language seems confined to a 2-cm2, or even smaller, area [113, 114, 115]. However, significant variability between patients would suggest that language function could not be reliably localized solely on the basis of anatomic criteria [115, 116]. Functional MRI [53, 66, 141], magnetoencephalography [122, 151], and PET [64] studies have recently implemented preoperative assessment of language localization sites. Compared with intraoperative direct cortical mapping, preoperative assessment is less dependent on patient cooperation and also allows for testing of young patients who might be too immature and uncooperative to undergo craniotomy while awake [64]. Unfortunately, the spatial resolution and specificity of activation with these methods are of insufficient accuracy to be used in making critical surgical decisions [64, 66]. To date, functional imaging studies represent a useful research tool as much as a useful guide for preoperative surgical planning [20, 96, 122, 151]. Functional imaging sources, however, cannot yet replace direct cortical stimulation, which remains the best approach for localizing areas related to language in brain surgery. Berger and Ojemann [11, 14, 115] have developed a classic stimulation paradigm for language mapping. There are a few fundamental steps in this method, which should be respected to ensure safe, reliable mapping. The first step is to establish an adequate stimulating current which does not induce seizure activity. If stimulation evokes afterdischarges, which indicate the local convulsive threshold, current should be reduced by 1 or 2 mA. Second, since the majority of aphasias involve a naming deficit, stimulation evoked anomia (or dysnomia) is considered significant for a language site. It is therefore critical to select a battery of objects to be named in which the basic, preoperative naming error is less than 25%. If

basic naming error is higher than 25%, intraoperative mapping is likely to be unsuccessful. Usually, the same current as has been used to stimulate the motor cortex representation of face should be applied to localize Brocas area [12]. In order to confirm localization of Brocas 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 than to specific stimulation of Brocas site. Electrocorticogram (ECoG) should also be continuously monitored to detect subclinical epileptiform activity, which may be a source of naming errors. It is of paramount importance to achieve a positive mapping result, since a negative mapping might not provide enough confidence to make proceeding with resection an option. A wide exposure of the cerebral cortex increases the possibility of obtaining positive mapping results and, on average, 20 or more cortical sites need to be mapped to achieve a positive response [14]. Every site is tested three separate times, and two errors out of three are significant for a language site, which should be preserved with a margin of at least 10 mm [61]. A resection margin of this width from the nearest language site resulted in significantly fewer permanent language deficits in a series of 40 patients who underwent awake craniotomy for a glioma in the temporal lobe of the dominant hemisphere [61]. From the technical perspective, it should be stressed that in contrast to mapping of the sensorimotor cortex, intraoperative mapping for language requires a very cooperative patient and can be performed only during awake craniotomy. This technique would therefore be of limited value in young children and might be replaced by extraoperative chronic subdural stimulation for language mapping [16, 136].

Surgery of the peripheral nervous system

In spite of constant improvements in morphological techniques, it can be difficult to distinguish nervous structures and nervous tissue from other tissues during surgical procedures involving the peripheral nervous system. Furthermore, regardless of its identification during surgery, nervous tissue can be damaged through the use of coagulation, traction or compression. This is often reversible if detected early and the cause is eliminated. Mapping techniques should therefore be combined with monitoring techniques, and since many mapping methods are similar to recording and/or stimulating protocols used in monitoring procedures this is often relatively easy to accomplish. Cauda equina surgery A relatively high percentage of pediatric neurosurgical pathology is located in the conus cauda region. In the

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Fig. 5 Intraoperative neurophysiology of the sacral system. Schematic diagram of neurophysiological events used to monitor and map the sacral nervous system. To the left are afferent events after stimulation of the dorsal penile/clitoral nerves and recording over the spinal cord. Top Pudendal SEPs, traveling waves. Middle Pudendal dorsal root action potentials (DRAP). Bottom Pudendal SEPs, stationary waves recorded over the conus. To the right are efferent events. Top Anal M-wave recorded from the anal sphincter after stimulation of S1S3 ventral roots. Middle Anal mMEPs recorded from the anal sphincter after transcranial electrical stimulation of the motor cortex. Bottom Bulbocavernosus reflex (BCR) obtained from the anal sphincter muscle after electrical stimulation of the dorsal penile/ clitoral nerve. Reprinted from [33]

past decade, intraoperative neurophysiological monitoring has expanded its applications in this area and, to date, complex and multimodality monitoring and mapping of the lumbosacral system is available (Fig. 5) [169]. One of the applications of intraoperative neurophysiological monitoring is surgery for the tethered spinal cord, where the surgeon cuts the filum terminale or removes the tethering tissue that envelops the conus and/or the cauda equina nerve roots. In a large series of patients operated on for tethered cords, permanent neurological complications were described in up to 4.5% [29, 121, 131]. This rate increased up to 10.9% when transient complications were considered [131]. During surgery of any spinal lesion involving nerve roots, a distinction between functional nervous tissue and fibrous bands is mandatory to avoid postoperative sensorimotor deficits and/or sphincter and sexual dysfunction. Due to tethering, the lumbosacral nerve roots leave the spinal cord in a different direction than in a healthy cord. Furthermore, the cord may be skewed and sometimes a nerve root may pass through a lipoma. Nerve fibers may also be in-

volved in the thickened filum terminale that is cut during untethering. Direct stimulation of these structures in the surgical field, or direct recording from them after peripheral nerve stimulation, has proved helpful. Using mapping techniques, functional neural structures of the lumbosacral region can be correctly identified and thus possibly preserved [78, 88, 120, 129, 130, 131]. Besides the already established mapping of fibers of the dorsal penile/clitoral nerves which enter the spinal cord through the dorsal sacral roots [37], the mapping possibilities of the sacral nervous system have been expanded to include mapping of pudendal afferents from the anal area [68, 120]. We use a specially designed anal plug electrode for this purpose [38, 82]. To identify motor nerve roots, direct stimulation is used and bilateral recording from segmental target muscles reveals compound muscle action potentials (CMAPs) in muscles supplied by the stimulated nerve root of the same side [78, 88]. Recording from segmental target muscles for all relevant myotomes simultaneously insures that all pertinent motor roots are monitored. For recordings from the external anal sphincter

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muscle, care must be taken to place the wire or needle electrodes just a few millimeters beneath the skin, since the muscle is very thin [137]. Whenever recordings are taken from muscles, the absence of muscle relaxation has to be confirmed before mapping or monitoring is performed. This can easily be done with the train-offour technique, which should be included in every monitoring protocol. In addition, during untethering procedures or tumor removal, ongoing inadvertent and still reversible damage to the conus or certain nerve roots can be detected by monitoring. SEPs after stimulation of peripheral nerves, recorded both from the spinal cord with an epidural electrode and/or from the scalp, can be used for continuous monitoring of the peripheral sensory pathways. The tibial nerve at the ankle or knee is routinely stimulated for monitoring L5 and S1 root or plexus integrity. Their significant deterioration or loss may be indicative of damage to these nerves or corresponding posterior roots. Unfortunately, it is difficult to record spinal and cortical responses to stimulation of the pudendal nerve (S1 to S4 roots), except when the recording electrode is placed close to the root entry zone of the roots of S2 to S4. Besides the long averaging times and response fluctuations, the main disadvantage of the use of SEPs for single root monitoring is the overlap by adjacent roots that can mask a lesion of a single root. Dermatomal SEPs have been advocated to get round the last disadvantage [166]. Since the stimulation is limited to the dermatomal distribution, the response is thought to selectively reflect the integrity of one sensory root. Although this method has been reported to be useful [166] it has not been accepted for routine monitoring because of low-amplitude responses and resulting difficulties with interpretation. The muscles innervated by the lumbosacral segments selected for mapping purposes can also be used to monitor MEPs elicited by transcranial electrical stimulation, as previously described in this article. This provides immediate information about the functional integrity of upper and lower motoneurons. Preservation of muscle MEPs in this setting will ensure preserved motor control after surgery. Conceptually, a loss of muscle MEPs in cauda/conus surgery indicates a complete lower motor neuron lesion and a postoperative motor deficit, presumably with little tendency to recovery. However, the ability of mMEPs to detect lesions of a single motor root has been questioned and, consequently, this technique is not yet as well established as MEP monitoring during spinal cord surgery [35, 80]. The bulbocavernosus reflex (BCR) is used to assess the functional integrity of motor and sensory sacral nerve roots as well as the S2 to S4 spinal cord segments [36, 170]. The afferent path is composed of sensory fibers of the pudendal nerves, while the efferent part rep-

resents motor fibers to pelvic floor muscles as bulbocavernosus or external anal sphincter muscles. Since the BCR is an oligosynaptic reflex it is very susceptible to general anesthesia, particularly when volatile anesthetics are used. The BCR is abolished by muscle blocking agents. Therefore, the same anesthesia regimen as outlined for mMEP monitoring should be used for BCR recordings. Equally, temporal summation is necessary to elicit the BCR under these conditions. This is achieved by using more stimuli, and a short train of stimuli seems to be optimal [36, 137]. Monitoring the BCR allows for testing of the functional integrity of three anatomical structures (sensory and motor fibers, spinal gray matter). This can be an advantage, but also a drawback, since the BCR can be extremely sensitive and may disappear due to manipulation of any of the three structures without a clear clinical correlate [33]. A definite advantage is that the BCR can be recorded in newborns as old as 24 days [33]. It has been shown that another possibility for continuous monitoring of the functional integrity of S1 and S2 spinal levels and sensory motor fibers [90] is the recording of the H-reflex from the gastrocnemius muscle after tibial nerve stimulation at the knee. Intraoperative monitoring of other spinal reflexes as suggested by Leppanen [91] has not been accepted into routine intraoperative use. Because of the lack of published statistical data collected in large groups of patients, reliability and specificity of monitoring for conus and cauda equina surgery remain unclear, or at best anecdotal. In a group of 58 patients who presented with tethered cord syndrome we were 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 et al., who suggest that the BCR is more difficult to record in females owing to technical problems [137]. In our group of patients, one had moderate urinary and anal incontinence before surgery and BCR was not present at baseline. Postoperatively, this patient presented worsened urinary and anal incontinence despite appearance of the BCR at the end of tether release. In another patient a neurogenic bladder developed postoperatively, despite unchanged intraoperative BCR. The correlation between sphincter control and BCR is even more complex since the BCR cannot detect injury to the suprasegmental pathways controlling sphincter activity. This could explain the discrepancy between clinical and neurophysiological data. To date, the correlation of BCR changes with postoperative sphincter control remain unclear and requires larger studies for clarification [142, 143]. The limited prognostic value of BCR becomes obvious in infants who do not retain sphincter control postoperatively. New insights on the role of the intraoperative BCR may come from correlations with pre- and postoperative urodynamic evaluation.

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Spinal procedures The incidence of neurological complications associated with the placement of pedicle screws has been reported to be as high as 11% [97]. A useful technique to prevent injury to the spinal roots is pedicle screw stimulation. This is a modification of the motor root mapping technique described earlier. Here, motor roots are indirectly stimulated through the screw placed in the vertebral pedicles. If a low current, applied through the pedicle screw, elicits CMAP in appropriate myotomes, this suggests a cracked pedicle or direct contact of the screw with the root [165, 168]. The cut-off threshold suggesting those possibilities is 10 mA according to the literature [168]. In our experience it is lower, and we usually consider 78 mA as a warning threshold. To limit pitfalls in threshold measurement, currents not passing exclusively through the screw should be avoided. This can be done by proper insulation of instruments used to apply current and by keeping the surgical field dry [168]. In patients with neuropathy the thresholds can be much higher, even with direct stimulation [168]. Neurosurgery for spasticity In children with severe, incapacitating spasticity, which is often a result of cerebral palsy, selective dorsal rhizotomy is performed to improve their quality of life and motor performance [1, 154]. The assumption is that reflex hyperactivity at the spinal level is due in these children to a release from supraspinal control, which increases the tonus of leg and foot musculature [1, 154]. Reflex activity is not only increased, but also spreads to muscles beyond the corresponding myotome. Even contralateral muscles may be activated by stimulation of an involved sensory root. This procedure can be performed without significant sensory loss because of overlapping innervation of the dermatomes by fibers from different sensory roots. In these cases, mapping is used not because anatomy is distorted but because it is impossible to determine by inspection which root is involved in increased reflex activity [2, 52, 109, 110]. Furthermore, it is morphologically not possible to determine which sacral roots carry a significant amount of pudendal afferent fibers and tremendous individual variability exists in the distribution of the sensory pudendal fibers entering the spinal cord through dorsal sacral roots [37, 67]. Therefore, functional intraoperative testing is necessary to identify these roots. Inclusion of the S2 root has been shown to be beneficial in these patients, because it relieves the corresponding plantar spasticity produced by involvement of the S2 posterior root in plantar reflex arches [84]. Unfortunately, in a significant number of individuals the S2 roots

carry afferent fibers from the pudendal nerves, so that lesioning them can result in additional sphincter and sexual dysfunction. In order to relieve spasticity in the plantar flexor muscles that are mainly innervated by S2, and at the same time avoid urogenital side effects, pudendal afferent mapping was introduced. This has reduced the incidence of urinary complications from 24% to 0% [37, 67]. Steinbok and Kestle [158] and Staudt et al. [157] have recently emphasized variation in the neurophysiologic techniques used in different centers during these procedures. A description of the technique we currently use now follows [1]. Following surgical exposure of the lumbosacral roots the surgeon records the electrical activity of sacral roots with a sterile hook electrode after electrical stimulation of the dorsal penile/clitoral nerves. Bilateral testing of S1, S2 and S3 roots determines the map of the contributions of pudendal afferent fibers in these sacral dorsal roots. Only S2 roots without pudendal afferents can be cut. When it is essential to cut S2 roots (because they are known to contribute significantly to the generation of spasticity) separation of the rootlets has to be performed and each rootlet is separately tested in the same way. A large group of patients who underwent this procedure showed that the use of this method can prevent permanent urinary complications [67]. Patients in whom S2 roots are cut show a postoperative decrease in the extent of residual plantar spasticity [84]. It is of interest that mapping of pudendal afferents in 114 patients who underwent selective dorsal rhizotomy frequently showed asymmetric entry of pudendal afferents into the spinal cord. Extreme asymmetry of pudendal afferents was found in 7.6% of these patients. Their afferents from the right and left pudendal nerves entered the spinal cord via a single S2 root [67]. Although some controversy still exists [118], pudendal anal afferents should also be identified to spare those roots involved in bowel function [123, 125]. Once the pudendal mapping has been done, selective dorsal rhizotomy can start. After direct stimulation of a sensory nerve root, CMAPs from appropriate muscles can be recorded; these are generated in a similar way to the H-reflex, but instead of the peripheral nerve, the dorsal roots are stimulated. This technique allows for the identification of which roots from L2 to S2 are involved in increased reflex activity and contributing to spasticity in the lower limb muscles. A set-up for reflex measurements is used with multichannel recordings from segmental target muscles with needle or surface electrodes. This allows visual display of a spreading response on the monitor. Muscle responses can also be detected manually by an experienced physical therapist palpating for tonic muscle contraction during stimulation. Apparently there is little difference in sensitivity for contractions between

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the manual detection and the electromyographic recording [1]. Stimulation is performed through modified surgical dissectors with proximal insulation and a bare tip (single stimuli of 200 s duration, 0.53 mA). First, the motor threshold is determined with a single stimulus paradigm of one stimulus every second (1 Hz). Then the roots are stimulated at these thresholds with a 50-Hz train for 1 s. Those posterior roots that produce a spreading response, i.e. those that elicit tonic muscle contraction beyond their corresponding myotome, are cut. If two adjacent roots have to be cut at least 50% of a third, adjacent to one of these, must be preserved. This implies microsurgical splitting of posterior roots into rootlets to determine the spreading contribution of each rootlet [1, 154]. Stimulus intensity should also be carefully adjusted to distinguish the reflex or non-reflex nature of a dorsal root-evoked response [93]. In the opinion of many neurosurgeons, mapping is mandatory for this type of surgery although there are discrepancies between theory and intraoperative observations [1, 109, 110, 118, 123, 157, 171]. Unequivocal evidence that children treated using the above theoretical approach have better functional outcome than those treated using only clinical judgment is still lacking [1, 160, 171].

Brain stem surgery

The brain stem is a part of the nervous system where a high concentration of different nerve structures is found in a small space. Therefore, even small incision injuries to the brain stem can result in severe neurological complications. Lesioning these areas can be life threatening (e.g., damage to cardiovascular or respiratory centers) or have debilitating consequences (e.g., coma, loss of spontaneous breathing, hemiplegia, dysphagia, dysarthria) [132]. Brain stem tumors occur quite frequently in the pediatric population [24, 149]. Therefore, pediatric neurosurgeons dealing with these pathologies should be aware of the neurophysiological methods available to prevent/document neurological injury to the brain stem. According to Fahlbusch and Strauss [50], classic intraoperFig. 6 Mapping of the brain stem cranial nerve motor nuclei. Left: Schematic drawing of the exposed floor of the fourth ventricle, with the surgeons hand-held stimulator in view. Middle: Sites of insertion of wire hook electrodes for recording the muscle responses. Right: Compound muscle action potentials recorded from the orbicularis oculi and oris muscles after stimulation of the upper and lower facial nuclei (upper two panels) and compound action potentials recorded from the pharyngeal wall and tongue muscles after stimulation of the motor nuclei of IXth/Xth and XIIth cranial nerves (lower two panels). Inset: Photograph from operating microscope showing stimulating probe on the floor of the fourth ventricle. (Reprinted from [39])

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Fig. 7 Typical patterns of cranial nerve motor nuclei displacement by brain stem tumors in different locations. Above: Upper (left) and lower (right) pontine tumors: pontine tumors typically grow to push the facial nuclei around the edge of the tumor, suggesting that precise localization of the facial nuclei before tumor resection is necessary to avoid damaging them during surgery. Below left: Medullary tumors: medullary tumors typically grow more exophytically and compress the lower cranial nerve motor nuclei ventrally; these nuclei may be located on the ventral edge of the tumor cavity. Because of the interposed tumor, in these cases mapping before tumor resection usually does not allow identification of motor nuclei of the IXth/Xth and XIIth cranial nerves. Responses, however, could be obtained close to the end of the tumor resection, when most of the tumoral tissue between the stimulating probe and the motor nuclei has been removed. At this point, repeat mapping is recommended because the risk of damaging motor nuclei is significantly higher than at the beginning of tumor debulking. Right: Cervicomedullary junction spinal cord tumors; these tumors simply push the lower cranial nerve motor nuclei rostrally when extending into the fourth ventricle. Reprinted from [104]

stem) combined with monitoring techniques (to assess the functional integrity of long tracts and cranial nerve nuclei within the brain stem) provide exhaustive intraoperative neurophysiological assistance to the surgeon. Mapping techniques: neurophysiological localization of the motor cranial nerve nuclei on the floor of the fourth ventricle A number of relatively safe entry zones have been proposed for the brain stem [23, 83]. These surgical routes allow lesions to be approached from the upper brain stem caudally to the cervicomedullary junction. Unfortunately, classic anatomical landmarks such as the facial colliculus or the striae medullares are often displaced by the tumor or are hardly identifiable, even in patients in whom the anatomy has not been distorted [39]. The initial incision through the floor of the fourth ventricle can injure motor nuclei of the cranial nerves (VII, IX, X, XII). The same is true for the motor nuclei of cranial nerves III, IV and VI of the upper brain stem. A neurophysiological technique for intraoperative identification of these nuclei has recently been developed [72, 103, 161, 162]. This technique is based on intraoperative electrical stimulation of the motor nuclei of the cranial nerves using a hand-held stimulator. Stimulation elicits CMAPs in the musculature innervated by the cranial motor nerves (Fig. 6).

ative neurophysiological methods (e.g., SEPs and brain stem auditory evoked potentials) can evaluate only 20% of the brain stem. Furthermore, data obtained with these methods cannot be obtained in real time, having a delay of a minute or so. Thus, we will briefly describe recently developed methods for mapping and monitoring the brain stems functional integrity. Some of these methods are still evolving and require extensive evaluation in larger numbers of patients. Nevertheless, mapping techniques (to identify the functional anatomy of the brain

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This method means that neurophysiological visualization of the anatomical position of those nuclei is achieved. Thus, in order to prevent injury to the previously mentioned structures, which are often displaced from their original anatomical positions by the tumor, the initial incision into the brain stem can be safely placed. Furthermore, Morota et al. [104] used this method to reveal a repeatable displacement pattern of the motor nuclei of the cranial nerves corresponding to the growth pattern of brain stem tumors (Fig. 7). Monitoring techniques Continuous monitoring of the functional integrity of cranial motor nuclei and nerves is still unsatisfactory. The available techniques are based on the recording of the ongoing electromyographic (EMG) activity in the muscles innervated by cranial nerves [47, 57, 138]. However, the correlation between intraoperative EMG activity and postoperative outcome is still a matter of debate. Grabb et al. [57] did not reach conclusive results that would have proved that EMG of the VIth and VIIth cranial nerves enhanced operative safety or facilitated aggressive removal during surgery for fourth ventricle tumors. Conversely, Romstock et al. [138] have recently proposed warning criteria based on detailed analyses of EMG waveforms during cerebellopontine angle surgery. The possibility of monitoring corticobulbar pathways by recording MEPs from the facial, laryngeal and tongue muscles after transcranial stimulation is currently under investigation and may prove to be a useful monitoring tool in the near future. In the case of lesions close to the cerebral peduncle or the ventral part of the medulla, injury to the CTs becomes a major concern to the surgeon. Similarly to what described for spinal cord surgery, mMEP and eMEP can be elicited transcranially and monitored throughout the procedure. Using a similar approach, the CT, lying on the base of the cerebral pedunculi, could be identified by direct electrical stimulation during recording from the spinal cord in the form of a D wave (Fig. 8) [39]. This method seems very promising and could prevent lesioning of the highly concentrated fibers of the CT during the initial incision to the cerebral pedunculi. Owing to the complexity of the brain stems functional anatomy, the choice of the most appropriate battery of neurophysiological tests should be used for each single patient. However, a prompt evaluation of the functional integrity of brain stems structures is warranted only by the combined use of multiple monitoring techniques. So, while monitoring only BAEPs, only SEPs or only corticospinal/corticobulbar MEPs can be misleading, the rational integration of data from all these modalities will provide the most reliable assessment of brain stem integrity (see Table 2).

Fig. 8 Mapping of the corticospinal tract. Mapping of the corticospinal tract (CT) on the cerebral peduncle during surgery for removal of a left cerebral peduncle tumor in a 27-year-old woman is shown schematically. The cerebral peduncle is being mapped by a hand-held monopolar probe (upper right). As the probe neared the CT, responses were recorded from an epidural catheter (upper left). Responses were consistently repeatable. Stimulation intensity was 2 mA, stimulating rate was 4 Hz, and four responses were averaged. Reprinted from [39]

Unsolved problems, from a neurophysiological perspective, remain eye movement coordination deficits and postoperative swallowing deficits. Monitoring and mapping of the internuclear fascicles have not yet been established. Similarly, neurophysiological tests for intraoperative monitoring of the afferent branch of the swallowing reflex are still lacking. Besides descending control to the motor nuclei of the glossopharyngeal and vagal nerves, preservation of the afferent arch of this reflex as much as of the interneurons involved in the coordinated act of swallowing is necessary to warrant function.

Anesthesia and INM

The complex relationship between anesthetic agents and intraoperative recordings of evoked potentials deserves a discussion that is beyond the scope of this review. We

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Table 2 When and how to monitor in pediatric neurosurgery (BAEP brainstem auditory evoked potentials; BCR bulbocavernosus reflex; DRAP dorsal root action potential; EMG electromyogProcedures Brain surgery in the central region and along subcortical motor pathways Brain surgery in speech areas Posterior fossa and brainstem surgery Mapping techniques

raphy; eMEPs epidural motor evoked potentials; mMEPs muscle motor evoked potentials; SEPs somatosensory evoked potentials; CT corticospinal tract) Monitoring techniques Cortical SEPs mMEPs after multipulse electrical transcranial or cortical stimulation None BAEP Cortical SEPs mMEPs or eMEPs Continuous EMG recording of muscle innervated by motor cranial nerves Cortical SEPs or epidural (spinal) SEPs mMEPs and eMEPs Cortical SEPs Pudendal (spinal) SEPs mMEPs (anal mMEPs included) BCR None

Phase reversal Direct cortical and subcortical mapping (with the 60 Hz or the multipulse technique) Direct cortical mappinga Direct mapping of motor nuclei of the cranial nerves in the floor of the fourth ventricle Direct mapping of the CT within the cerebral peduncle Dorsal column mapping Pudendal DRAP mapping Motor roots mapping Pudendal DRAP mapping Motor roots mapping

Spinal cord surgery Conus-cauda surgery

Rhizotomy for relief of spasticity

a Only

the 60 Hz technique in the awake patient can be used intraoperatively

therefore refer the reader to the pertinent literature for a detailed analysis of the anesthesiological management of patients who undergo INM during neurosurgical procedures. In our experience, continuous infusion of propofol and fentanyl with no boluses , avoiding halogenated agents and muscle relaxants after intubation, has proved feasible and suitable for most of the procedures.

Conclusions
The concept of identifying physiological/pathophysiological aspects in the operating room by linking functional information to advanced imaging is one path of progress neurosurgery and neuroscience are taking. As we use these techniques and slowly understand how they work, we are learning how little we understand about them so far. We are just scratching the surface of a large body of knowledge that we will eventually learn to use better in order to refine neurosurgical treatment even further. There follows a brief set of primers as to the why, when, and how of monitoring during pediatric neurosurgery. Why? Intraoperative neurophysiological monitoring has several purposes. (1) To enable the surgeon to change his strategy in order to prevent neurological complications. (2) To confirm that the strategy adopted by the surgeon is appropriate and encourage more aggressive surgery in

the case of lesions amenable to total removal and cure. (3) To predict neurological outcome and therefore improve the postoperative management of children and their families. (4) To provide information useful for retrospective analysis and possible adjustment of surgical strategies. (5) To provide documentation for medicolegal purposes. (6) Last but not least, INM allows investigation of the pathophysiology of neurosurgical diseases affecting the developing nervous system and can therefore be used as an educational tool for young neurosurgeons. When? Indications for intraoperative monitoring vary in the different centers around the world. While priorities should be defined according to scientific, economic and medicolegal issues at each single institution, INM is mandatory whenever the expected neurological complication is determined by a known pathophysiological mechanism that can only be prevented by INM. INM becomes optional when its role is limited to predicting postoperative outcome [58] or it is being used purely for research purposes. Below we summarize methods of INM and their indications with reference to pediatric neurosurgical procedures, as presented in Table 2. Brain surgery in the central region and along subcortical motor pathways For surgery in and around the central region, or along the subcortical motor pathways, cortical and subcortical

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mapping techniques should be considered standard. These techniques allow for the intraoperative functional rather than anatomical identification of eloquent cortical areas and subcortical localization of the CT. Patterns of cortical plasticity or reorganization induced by the tumor may be disclosed. The phase-reversal technique identifies the border between primary motor and sensory areas. This information should then be confirmed by direct stimulation of the motor cortex. To map and monitor the functional integrity of the motor cortex and the CT, the multi-pulse technique, although less commonly used, offers the advantage of continuous intraoperative monitoring of MEPs. The particular advantage of this technique is that it can be used for transcranial stimulation. Although still considered optional, we strongly suggest neurophysiological monitoring as an invaluable adjunct to mapping during brain surgery. Finally, cortical SEPs can be used to monitor the functional integrity of dorsal sensory pathways. Brain surgery in speech areas Intraoperative mapping of cortical areas related to language is feasible only after craniotomy in awake patients. Thus, this can limit its application in young children. Mapping of the language areas should be conducted 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 successful monitoring can be conducted. SEP, mMEP and/or eMEP, and BAEP monitoring should always be used. These techniques provide both specific information about a particular system (motor, sensory or auditory), and less specific information about the well-being of the brain stem. Additional techniques should be tailored on the basis of the tumor level and extension. For example, at the midbrain level, mapping of the cerebral peduncle may be added to the battery of neurophysiological tests. At the level of the pons and upper medulla, mapping of 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. The peripheral portion of the facial cranial nerve can also be identified in the cerebellopontine angle by direct stimulation. Continuous EMG recording from the facial muscles (orbicularis oculi, orbicularis oris) provides feedback on the spontaneous and manipulation-induced activity of the facial cranial nerve. Unfortunately, the neuroprotective role of this latter monitoring technique is still controversial, as is its correlation with the postoperative clinical functioning of the facial nerve.

During surgery at the cervicomedullary junction, mapping of the fourth ventricle allows for the identification of the motor nuclei of cranial nerves IX, X, and XII. Continuous monitoring of the integrity of the lower motor cranial nerves (X and XII) should be added. This can be performed by EMG recording directly from the pharyngeal and tongue muscles, but the same limitations as discussed for the facial nerve apply. The standardization of techniques currently considered experimental (such as monitoring of corticobulbar pathways) will hopefully augment brain stem monitoring in 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 favor SEPs over MEPs is not justified from a scientific background. Although MEPs are still not available in many intraoperative neurophysiological departments, their use should be encouraged since MEPs represent the most appropriate and reliable tool to assess the functional integrity of descending motor tracts. Dorsal column mapping is an experimental technique that will hopefully assist in the future during myelotomies for excision of intramedullary spinal cord tumor. Conus-cauda equina surgery Mapping techniques should be used during conus-cauda equina surgery to identify the filum terminale and the motor and sensory lumbosacral roots. This information can be invaluable during rhizotomy for the relief of spasticity, during untethering of the spinal cord, or during the removal of conus-cauda equina tumors. Besides mapping, continuous monitoring of mMEPs from lower extremity muscles and the anal sphincters (together with cortical SEPs) provide on-line feedback about the functional integrity of these structures during their manipulations. BCR monitoring can be added to assess the integrity of pudendal afferent and efferent pathways as well as of the sacral segments of the spinal cord from S2 to S4. However, the prognostic value of this monitoring modality, with respect to genitourinary function, continues to be debated. How? The role of the neurophysiologist is: first, to extract neurophysiological data; second, to analyze these data immediately in order to recognize neurophysiological patterns promptly; third, to integrate these patterns critically with intraoperative clinical features to avoid false-posi-

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tive or false-negative results; fourth, to warn the neurosurgeon in time, before irreversible injury to the nervous tissue has occurred. A multimodality INM combining information from SEPs, MEPs and other monitoring and mapping modalities increases the sensitivity of INM. Nevertheless, INM should be kept as simple as possible. Close collaboration with both the surgeon and the anesthesiologist, making sure that everybody understands

everybody elses job, is one of the key factors in successful monitoring. Finally, INM should be performed only by skilled neurophysiologists or neuroscientists (neurologists, neurosurgeons, neuroanesthesiologists) who have been specifically trained in intraoperative monitoring. We should keep in mind the adage that no monitoring is better than bad monitoring.

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