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Mapping and monitoring for brainstem lesions
Intraoperative Monitoring of Neural Function Handbook of Clinical Neurophysiology, Vol. 8 M.R. Nuwer (Ed.) # 2008 Elsevier B.V. All rights reserved
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CHAPTER 37
Mapping and monitoring for brainstem lesions Georg Neuloh*, Christian Strauss and Johannes Schramm Neurochirurgische Universita¨tsklinik, D-53105 Bonn, Germany
37.1. Brainstem mapping
37.1.2. Stimulation technique
37.1.1. Introduction
Various stimulation techniques can be used (Strauss et al., 1993; Eisner et al., 1995; Morota et al., 1995; Chang et al., 1999). Constant voltage, constant current, bipolar or monopolar techniques have all been successfully employed. Constant current bipolar stimulation with rectangular monophasic impulses (a stimulus duration of 100–400 ms, a stimulus frequency not exceeding 10 Hz and intensities up to 2–5 mA) has proved reliable and safe and has been used by our group since 1996 (Strauss et al., 1999). Following surgical exposure of the rhomboid fossa, a hand-held stimulation probe is moved on the surface of the rhomboid fossa under constant electrical stimulation using rather high stimulation intensities (2 mA). The stimulation tip should have a rather planar area in order to avoid injury to the ependyma and underlying tissue (Fig. 3) (Strauss et al., 1993). The short distance, for example of 0.25 mm, from the ependyma to the ascending fibers of the facial nerve within the facial colliculus has to be considered (Strauss and Fahlbusch, 1997; Strauss et al., 1997). Supramaximal stimulation considerably shortens the period of mapping and easily identifies structures of the facial colliculus within several seconds, but by nature is not specific. With the area of interest identified, stimulation intensity is then turned down to threshold levels, which in a normal anatomical situation usually measures around 0.05 mA, when the colliculus is the target. With the threshold technique, the area of the shortest distance between facial nerve fibers and the ependyma can be selectively identified (Strauss et al., 1999). Usually the area of shortest distance can be identified paramedian to the median sulcus, where the ascending fibers of the facial nerve come closest to the surface (0.25 mm) (Strauss et al., 1997). With marginal variation of the stimulation intensity, a road map of the facial nerve fibers can be drawn (Fig. 1). With the same technique, other motor nerve nuclei (V, VI, IX/X, and XII) can
Surgical treatment of brainstem lesions is limited by dense concentration of functionally important neural pathways, nuclei, and fibers in pons variolii and medulla oblongata and the lack of reliable visible anatomical landmarks (Lang et al., 1991). Since most brainstem lesions are approached via the IVth ventricle, the presence of functionally intact brain tissue between ependyma and lesion poses already a potential risk due to the surgical corridor itself. In pontine lesions, facial and abducens nerve deficits as well as conjugated gaze palsies can affect the quality of life. Deficits of lower cranial nerve nuclei (nucleus n.hypoglossii, nucleus ambiguus, nucleus dorsalis n.vagi as the parasympathetic motor nucleus of the vagal nerve) are severe life-threatening complications following surgery of medullary lesions. Careful anatomical studies have defined safe entry zones into the brainstem above and below the facial colliculus measuring several millimeters (Fig. 1) (Kyoshima et al., 1993; Bogucki et al., 1997a,b, 2000; Strauss et al., 1997). The effect of space occupying intrinsic lesions on the superficial anatomy of the rhomboid fossa, however, limits the value of these morphometric investigations (Strauss et al., 1993, 1997). Direct electrical stimulation during surgery has emerged as a reliable and safe technique for identification of superficially located nuclei and fibers in order to define safe entry zones into pons and medulla (Figs. 1–3) (Strauss et al., 1993, 1999; Eisner et al., 1995; Morota et al., 1995, 1996; Chang et al., 1999; Morota and Deletis, 2006).
* Correspondence to: Georg Neuloh, M.D., Neurochirurgische Universita¨tsklinik, D-53105 Bonn, Germany. Tel.: þ49-228-287-6521; fax: þ49-228-287-4758. E-mail: [email protected] (G. Neuloh).
IV 14 mm VI VII
9 mm
X
XII
Fig. 1. Anatomical schematic drawing of superficially located motor nuclei and fibers of the floor of the rhomboid fossa (left side) with corresponding operative site (right side). The nuclei and fibers were mapped using electrical stimulation and indicated by black silk sutures.
Fig. 2. Selective stimulation of the VIth nerve nucleus. Multiple EMG traces of various target muscles demonstrate selective stimulation effect.
Fig. 3. Supracollicular approach to a recurrent symptomatic pontine cavernous hemangioma. The patient had been operated upon for this lesion several years ago using an approach above the right facial colliculus. Following localization with the hand-held stimulator (upper left), the hematoma was released (upper right) and the vascular malformation subsequently removed (lower left and right).
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be localized. Stimulation intensity has to be adjusted accordingly, since these nuclei are located further away from the ependyma surface. For identification of the nucleus of the hypoglossal nerve, stimulation intensity of 1 mA and more have to be employed. It has also to be taken into consideration that higher stimulation intensities are less specific and may result in diffuse stimulation effects. We have never employed stimulation intensities above 5 mA, except for one patient who was operated upon for a primary hematoma of the pons. In this patient, we used up to 10 mA stimulation intensity. Stimulation intensities may vary according to the underlying disease. In tumors infiltrating the floor of the fourth ventricle, higher intensities may be required when stimulation is applied through the tumor tissue, in order to guide the extent of removal, for example, in primitive neuroectodermal tumor (PNET) and ependymomas. 37.1.3. Recording technique Recording electrodes are placed into the target muscles. We use a pseudobipolar recording setup with two electrodes for each muscle. These electrodes are placed 5–10 mm apart and are secured by tapes in order to avoid dislocation (Strauss et al., 1999; Romstock et al., 2000). For the lateral rectus muscle, we use insulated electrodes to avoid unintended recordings from the orbicularis oris muscle. For lower cranial nerve monitoring, electrodes are placed into the soft palate and into the pharyngeal wall. For vocal cord monitoring, we have directly placed electrodes into the vocalis muscle under laryngoscopic control, but lately have exclusively relied on endotracheal tube electrodes. For hypoglossal nucleus localization, we apply two electrodes into the tip of the tongue. For practicability, it is sufficient to use one pair of electrodes for hypoglossal nuclei, since the nuclei of both sides are located extremely close together (0.6 mm). The distance of the upper pole of the hypoglossal nerve nuclei from the ependyma measures 0.55 mm. This results in a stimulation threshold of 1–2 mA. This stimulus intensity evokes responses from both nuclei. Other than that we record activity separately from both sides. For the trigeminal motor nucleus, we apply electrodes into the masseter muscle. With a standard two-channel recording setup and referential recordings, motor responses from the orbicularis oris muscle may prove difficult to differentiate. We therefore routinely record facial nerve activity from all three branches of the facial nerve.
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Multichannel recordings are required for most brainstem lesions in order to simultaneously record activity from all possible target muscles. This ensures selectivity of responses and proved time saving (Fig. 2). We therefore do not advocate the standard twochannel recording procedure techniques as for example in acoustic neuroma surgery, although in selected cases reduction to two channels may be sufficient (Fig. 3). 37.1.4. Anesthesia The anesthetic regimen is based on total intravenous anesthesia (TIVA). Following induction with midazolam, nitrous oxide and a short-acting muscle relaxant (atracurium besilate) anesthesia was maintained with propofol (6–12 mg/kg/h) and alfentanil (60 mg/kg/h). Muscle relaxing agents were not given until the very end of the surgical procedure (Strauss et al., 1999; Romstock et al., 2000). With respect to cost management, volatile anesthetic regimens have also proved to have no negative influence on the reliability of stimulation (Ruskin et al., 1994; Morota et al., 1995). 37.1.5. Safety aspects Cardiovascular side effects of electrical stimulation are of particular concern, since the parasympathetic motor nucleus dorsalis n.vagi is located directly lateral to the trigonum hypoglossi. With the stimulation parameters outlined above, a short run of asymptomatic ventricular extrasystoles was observed in a single patient of a series of more than 100 cases immediately following stimulation. Other than that measurable effects regarding cardiac arrhythmia or blood pressure were never observed since introduction of this method in 1991. Possible brain damage with respect to electrical stimulation is mainly caused by an imbalance of the blood–brain barrier. Damage of the barrier is dependent on the applied charge density (Coulomb (mC)/cm2 phase) under the stimulation electrode (Agnew and McCreery, 1987; Gordon et al., 1990). From histology of epileptogenic tissue, which was chronically stimulated prior to resection, it is known that up to a charge density of 57 mC/cm2 phase no histological changes occur (Agnew and McCreery, 1987; Gordon et al., 1990). For constant voltage stimulation, the electrode surface of 0.0043 cm2 produces a charge density of 0.59 mC/cm2 phase (M ller and Jannetta, 1984). Constant current stimulation produces
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charge densities up to 0.0014 mC/cm2 phase. For cortical stimulation in surgery of centrally located tumors and in epilepsy surgery, charge densities up to several 100 mC/pulse/cm2 are considered safe (Cedzich et al., 1998). Limitation of electrical stimulation to 1 V (constant voltage technique) and 2 mA (constant current technique) has no noticeable adverse side effects regarding the blood–brain barrier (Strauss et al., 1999). The limitation of the stimulus frequency to 10 Hz is based on animal experiments in which changes of cerebral blood flow, blood pressure, and intracranial pressure were provoked by using stereotactically implanted electrodes into the dorsal and rostral areas of the formatio reticularis. Maximal effects were seen with 40–50 Hz, although when using high stimulus intensities (50 mA) effects were observed with as low as 2 Hz with limitation exclusively to the time period of stimulation (Iadecola et al., 1983). 37.1.6. Site of stimulation Precise location of the stimulation site is a prerequisite for the clinical use of this technique. Since peripheral electromyographic (EMG) responses are obtained with stimulation intensities as low as 0.1 mA and a stimulation duration of 100 ms, the peripheral motor neuron seems most likely the site of stimulation. These parameters are similar to those for identification of the facial nerve during cerebellopontine angle surgery (M ller and Jannetta, 1984; Romstock et al., 2000). These parameters are inadequate for stimulation of the first motor neuron (Cedzich et al., 1998). For direct cortical stimulation of the pyramidal tract, the stimulation intensity usually varies between 2 and 25 mA with frequencies above 40–50 up to 500 Hz using a stimulation duration between 100 and 400 ms (Cedzich et al., 1998). A further peripheral stimulation toward the direction of root exit zones is unlikely, since stimulation would include other peripheral motor neurons of the areas of the cranial nerves. This was excluded by simultaneous bilateral multichannel EMG recordings demonstrating selective responses on the side and site of stimulation (Fig. 2). The selectivity of responses also excludes diffuse brainstem stimulation. The site can be directly calculated with the equation (I ¼ K d2), using the actual motor threshold for the facial nerve fibers and the fibers of the nucleus n.hypoglossii (Strauss et al., 1997, 1999) and the anatomically measured distances between the fibers and
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the ependyma surface (Strauss and Fahlbusch, 1997; Strauss et al., 1997). The clinical observation by Morota et al. using high dosage of volatile anesthetic without negative effect on the stimulation results also point to the peripheral motor neurons as the site of stimulation, since volatile anesthetics have a negative effect on the excitability of the first motor neuron, where as its influence regarding the excitability of the peripheral motor neuron can be neglected (Ruskin et al., 1994; Morota et al., 1995; Cedzich et al., 1998). Most likely, the axonal cone with an electric threshold 10 times lower than the axon’s threshold represents the presumed site of stimulation (Strauss et al., 1999). 37.1.7. Clinical value and review of literature Since the technique of intraoperative localization has rapidly evolved as a mandatory adjunct for brainstem surgery, a prospective study on its clinical value has never been published. Apart from brainstem cavernous hemangiomas (Fig. 3), for which the technique was originally designed (Fahlbusch et al., 1991; Houtteville, 1995; Samii et al., 2001; Sandalcioglu et al., 2002), brainstem tumors such as gliomas and ependymomas are of particular interest (Fig. 4), since the extent of surgical removal has been identified as the major prognostic factor (Pollack et al., 1993; Van Veelen-Vincent et al., 2002). Based on our experience, we have evaluated all surgically treated brainstem tumors between 1991 and 1999, which had been operated upon using this technique and compared their outcome with a matched (histology, location) series of patients undergoing surgery without mapping. Functional outcome of electrically localized motor nuclei and fibers (cranial nerves V, VI, VII, IX/X, and XII) were investigated before, immediately after surgery and on follow up after one year (Fig. 5). The study population consisted of 29 patients in each group (7 PNET, 12 medial ependymomas, 10 gliomas of various growth patterns) with an average age of 23.5 years in the “mapping” group versus 29 years in the nonmonitored group, tumor size averaged at 3.5 cm each, and 18 patients in both groups underwent postoperative radiotherapy. Six patients of the “mapping” group received chemotherapy, as compared to 7 “non-mapped” patients. Before surgery, the absolute number of cranial nerve deficits was comparable. After surgery, both groups deteriorated with respect to their cranial nerve deficits, which was to be expected, but after one year
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Fig. 4. Large pilocytic astrocytoma on axial and sagittal T1-weighted MRI images with contrast enhancement, before (upper) and after surgical removal (lower). The surgical corridor is clearly visible (lower left). Postoperative persistent morbidity was limited to a motor weakness of the trigeminal nerve, corresponding to the surgical corridor at the lateral edge of the rhomboid fossa.
mapped patients showed significantly better functional results (w2 test: p ¼ 0.003). In those patients undergoing surgery without the application of intraoperative mapping, postoperative cranial nerve deficits remained fixed and did not recover over the observation period
(Fig. 5). Dorsally exophytic brainstem gliomas and focal endophytic gliomas as well as low grade ependymomas seem to benefit from careful intraoperative mapping (Fig. 4). These results, although based on a study design implying a low evidence level, underline
Fig. 5. Total number and course of cranial nerve deficits (V, VI, VII, IX/X, and XII) as evaluated in a retrospective analysis of 58 patients with brainstem tumors (glioma, ependymoma, PNET) undergoing surgery with and without brainstem mapping.
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the neurosurgical impact of this technique. Direct electrical brainstem stimulation for mapping of the floor of the IVth ventricle is the neurophysiologic method with the fastest and widest acceptance in neurosurgery. Two years following its first description in 1993 (Strauss et al., 1993), this technique has been stated as mandatory for surgical management of brainstem lesions (Bricolo and Turazzi, 1995). Based on published experiences of several groups, the technique has gained wide acceptance, because it is easy to apply, safe, and provides reliable information on the location of motor brainstem fibers and nuclei (Strauss et al., 1993; Eisner et al., 1995; Morota et al., 1995, 1996; Chang et al., 1999; Strauss et al., 1999; Morota and Deletis, 2006). It must be concluded that identification of superficially located motor nuclei prior to microsurgical removal of brainstem lesions does not exclude functional morbidity of identified structures following surgery (Morota et al., 1996). The technique of threshold stimulation is a method for localization, but not for intraoperative monitoring. Continuous multichannel EMG recordings and analysis of these data have yet failed to identify pathological EMG activity, indicating damage to monitored structures. The presence of prolonged EMG activity (bursts and spikes) has been associated with postoperative morbidity (Grabb et al., 1997); however, in our own data, we have not been able to reliably associate presence of spikes and bursts with cranial motor nerve deficits after surgery. A specific EMG pattern, comparable to the “A-train” indicating pending damage to brainstem nuclei has so far not been identified (Romstock et al., 2000). At present, any prolonged EMG activity has to be considered potentially harmful. Future research should be directed toward detailed software-based analysis of intraoperative EMG in order to reliably apply this technique for continuous monitoring during removal of brainstem lesions. 37.2. Brainstem motor-tract monitoring 37.2.1. Introduction Continuous monitoring of sensory evoked responses [somatosensory evoked potential (SEP) and BAEP, rarely trigeminal sensory responses (Soustiel et al., 1993)] during brainstem surgery was described early (Albright and Sclabassi, 1985) and is still a commonly applied technique for brainstem monitoring, although reports on clinical applications remain anecdotal (Gentili et al., 1985; Kohno et al., 1993; Wagner
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et al., 1994; Pechstein et al., 1997; Cedzich et al., 1999; Anderson et al., 2003). However, the tegmental somatosensory and auditory pathways do not cover an area of the brainstem large enough (Fahlbusch and Strauss, 1991) to represent its general functional state with a high sensitivity, although combined SEP and BAEP monitoring has an increased sensitivity for, for example, brainstem ischemia as compared with either method alone (Manninen et al., 1994). Specifically, the functional integrity of the corticospinal fibers cannot be validly monitored by sensory evoked potentials. It must be remembered that the pyramidal tract courses through the ventral cerebral peduncles, the fibrae longitudinales of the pars ventralis pontis, and the likewise ventrally located decussatio pyramidorum of the medulla oblongata, clearly separated from the bulbothalamic and spinothalamic fibers of the lemniscus medialis and from the auditory pathways and nuclei of the lateral lemniscus and the corpus trapezoideum, also with a partially differing (ventromedial vs. lateral perforators) blood supply, particularly at the pontine level. The same is true for the corticonuclear fibers of the mesencephalic and upper rhombencephalic pyramidal tract. Reliable monitoring of the motor pathway’s functional integrity under general anesthesia is a more recent development (Deletis, 1993; Taniguchi et al., 1993; Pechstein et al., 1996; Deletis and Kothbauer, 1998), and has been extensively explored in the neurosurgical context for supratentorial brain and spinal cord surgery (see Chapters 15–18 and 21 in this volume). The application of motor evoked potential techniques for brainstem monitoring has been discussed more sporadically (Cedzich et al., 1999; Neuloh and Schramm, 2004b; Sala et al., 2004; Akagami et al., 2005; Dong et al., 2005; Glasker et al., 2006). Here, we will briefly summarize methodological and clinical features of the technique which are important for brainstem monitoring. Whereas brainstem monitoring is of obvious importance in child neurosurgery, there are no truly childspecific aspects of brainstem motor monitoring except for the more difficult elicitation of motor responses in young children which require the most careful selection of optimum stimulation and recording parameters in order to obtain reliable motor responses. 37.2.2. Motor evoked potential stimulation Transcranial motor evoked potential pulse-train stimulation (Pechstein et al., 1996; Neuloh and Schramm, 2004b), in general as applicable for posterior fossa
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approaches, is described in detail elsewhere in this volume and cannot be fully discussed here. The electrode montage is at sites about 1–2 cm anterior to the C1-C2 or C3-C4 positions of the International 10– 20 system. A C3/4-Cz þ 2 cm electrode montage has proven optimal for specific corticobulbar tract monitoring (see below). More lateral positions provide a more efficient stimulation of the corticospinal and particularly of the corticobulbar tracts, but the movement artifact typically associated with transcranial electrical stimulation may be more pronounced. Constant current stimulation is preferred for a better control of current distribution and a lesser twitching artifact. Since upper extremity muscle motor evoked potentials (MEPs) are typically recorded for brainstem monitoring, current intensities of 100 mA or less are sufficient to obtain the desired just-above threshold motor responses. Supramaximal stimulation is discouraged to avoid caudal bypassing of the target pathways in particular with mesencephalic procedures. If surgery is performed in a sitting or semi-sitting position, subdural air collection after durotomy may dramatically increase the electrical impedance (Kombos et al., 2000). More lateral electrode positions are preferred over a very strong stimulation intensity to overcome the high apparent motor threshold for the above reasons. Too lateral electrode positions caudally to the target structures may in theory occur in midbrain surgery, but the typical approaches these procedures are usually not performed in a sitting position. Successful MEP monitoring may be impossible in up to 10% of cases mainly due to the problem of subdural air collection. The frequency of MEP stimulation depends on the monitoring program implemented in a given setting. Alternating only with SEPs, a stimulation rate of about 2 per minute can be achieved, in critical situations MEP alone may be performed at a higher rate. If BAEPs are recorded as well, MEPs may be obtained only every few minutes (Dong et al., 2005), although every attempt must be made to increase the update speed since real-time monitoring as required for useful surgery monitoring cannot be realized at such a low stimulation rate. 37.2.2.1. Corticospinal tract mapping With lesions displacing the corticospinal tract or distorting the local peduncular or pontine topography, direct stimulation of the motor fibers via a hand-held probe can be used, employing the multipulse MEP technique to map the motor tract (Cedzich et al.,
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1998; Sala et al., 2004; Quinones-Hinojosa et al., 2005) for identification of safe entry zones for the surgical approach. As opposed to cortex stimulation, “cathodal” stimulation may be most effective (Cedzich et al., 1998). It must be noted that this mapping procedure differs fundamentally from, and cannot replace continuous motor monitoring which is rather intended to pick up impending motor damage at unexpected instances. There are no aspects of anesthesia and safety with MEP stimulation which are truly specific to brainstem monitoring; therefore, we refer the reader to the respective chapters in this volume. 37.2.3. MEP recording and interpretation In our experience, recording of MEPs from distal upper limb muscles is adequate for brainstem corticospinal tract monitoring. We prefer subcutaneous needle electrodes placed in a muscle-tendon fashion in order to pick up compound muscle responses (Neuloh and Schramm, 2004b). As it is well known from MEP monitoring for pericentral tumors, motor responses can be usefully recorded after direct cortical stimulation from facial muscles (Fig. 6, Neuloh and Schramm, 2002, 2004b; Neuloh et al., 2004) to avoid lesions of the corticonuclear projections with lateral resection. Similarly, continuous corticobulbar tract monitoring can be achieved during brainstem surgery with transcranial stimulation and recording
Fig. 6. Facial muscle response to transcranial pulse-train stimulation of the corticonuclear tract in comparison with arm and leg muscle responses. Note the large stimulus artifact and the clearly discernible latency around 15 ms which excludes peripheral cranial nerve stimulation.
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trade-off) in (Dong et al., 2005). Since corticonuclear MEP responses do not seem to represent all of the target fibers, mild paresis despite preserved responses as well as partially preserved function despite irreversible loss may occur (Dong et al., 2005). In spinal cord monitoring (see Chapter 16 in this volume), D-wave monitoring via epidural electrodes provides a semi-quantitative amplitude criterion for assessment of corticospinal tract function, whereas only the presence or absence of muscular motor responses is useful parameter of motor function due to the propriospinal supportive motor system (Kothbauer et al., 1997; Deletis, 2002; Sala et al., 2004). Although a typical median suboccipital craniotomy would allow for placement of cervical epidural electrodes, brainstem surgery does not necessarily require this additional recording technique due to the above semi-quantitative relation between muscular MEP responses and motor function comparable to supratentorial surgery (Neuloh and Schramm, 2004b; Neuloh et al., 2004; Akagami et al., 2005; Dong et al., 2005).
from facial and lower cranial nerve target muscles (Sala et al., 2004; Akagami et al., 2005; Dong et al., 2005), possibly providing a solution for the uncertainties associated with continuous cranial nerve EMG monitoring for brainstem surgery as discussed above in part I of this chapter. Direct peripheral cranial nerve excitation can easily occur with the transcranial stimulation technique and would lead to false-negative monitoring results with brainstem surgery. Therefore, a low suprathreshold stimulation intensity is mandatory for this corticobulbar monitoring technique. A single pulse stimulation at the intended current intensity for corticobulbar tract excitation can exclude peripheral nerve stimulation if it does not evoke a motor response, which would require transsynaptic multipulse train stimulation of the bulbar motoneuron as opposed to the peripheral nerve. However, if a clearly discernible typical MEP onset latency around 12–16 ms can be measured, the corticobulbar pathway must be involved and direct peripheral cranial nerve excitation which yields motor responses after 5–7 ms is very unlikely (Dong et al., 2005). The MEP amplitudes which are achieved with transcranial stimulation are less stable than after direct cortical stimulation. Therefore, the typical 50% amplitude criterion for significant MEP decrement which has proven valid in our experience (Fig. 7, Neuloh and Schramm, 2002, 2004a,b; Neuloh et al., 2004) and seems to apply also for brainstem monitoring (Akagami et al., 2005) is not always applicable. In particular for corticobulbar tract monitoring, where lower amplitudes and a lower signal-tonoise ratio is achieved, a somewhat tighter criterion must be chosen, for example, the 35% criterion which proved most valid (best sensitivity-specificity Intraoperative MEP Findings
37.2.4. Clinical applications 37.2.4.1. Indications for brainstem motor monitoring It is obvious from the above anatomical considerations that corticospinal/corticonuclear monitoring is mandatory with lesions within or in close adjacency to the ventral or ventrolateral aspect of the brainstem. This is true for both intra- and extraaxial lesions, including resectable gliomas, ependymomas, large petroclival and foramen-magnum meningiomas, epidermoids, cavernomas, arteriovenous vascular malformations, and very large vertebral or basilar artery aneurysms (Figs. 8 and 9). The ventral approach
Permanent new deficit
Motor Outcome Transient new deficit
No new deficit
Irreversible Loss
always
Irreversible Deterioration
frequent
frequent
rare
Reversible Loss
rare*
frequent
frequent
Reversible Deterioration
rare*
frequent
frequent
Unaltered
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never**
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*not yet observed in brainstem surgery **exception: mild facial paresis
Fig. 7. Qualitative correlation of intraoperative MEP findings and motor outcome as typically observed during supratentorial brain surgery and apparently applicable also for brainstem procedures. Modified with permission from Neuloh and Schramm (2004b).
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Opening Dura CSF Outflow Dissecting ependymoma
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Fig. 8. During surgery for an ependymoma of the cervicomedullary junction, resection was halted with MEP deterioration. MEPs recovered partially, and there was no new motor deficit postoperatively. Follow-up imaging confirmed the intraoperative impression that complete tumor resection had been achieved at the point of MEP deterioration. Modified with permission from Neuloh and Schramm (2004b).
determines the risk for brainstem motor function as much as a possible resection in adjacency to the motor fibers. One major concern, for example, with foramen magnum meningiomas is a possible affection of the vascular supply of the motor tract which has very little collateralization in this area. In our view, a targeted indication for any monitoring technique is desirable for reliable results rather than the accumulation of all available methods in all posterior fossa cases. We do not perform routine MEP/SEP monitoring in, for example, typical cerebellopontine angle tumor surgery, even with large vestibular schwannomas, where BAEP and cranial nerve mapping/monitoring provides adequate monitoring. Likewise, surgery via a rhomboid fossa approach for tegmental intrinsic tumors or cavernomas will require MEP monitoring only if these lesions extend deep into the brainstem. However, extended corticonuclear MEP monitoring (Dong et al., 2005) is a possible future routine application with such lesions, and preserved SEPs may indirectly indicate preserved functional integrity of the tegmentum.
37.2.4.2. Impact on surgery In our experience, ischemia arises with inadequate retraction, electrocoagulation, or manipulation of vessels during dissection, and is a major cause for new motor deficit in brainstem surgery. Venous congestion can cause delayed deficit and must be carefully avoided as well (Strauss et al., 2000). Therefore, if MEPs deteriorate, dissection is temporarily halted, retractors are released and possibly readjusted, the situs is checked and irrigation is applied as well as papaverine to possibly spastic vessels. With early intervention, MEP deterioration proves reversible in most cases and no permanent new deficit must be expected. If MEPs deteriorate during resection of a brainstem tumor, the above measures should be considered to reverse the MEP change, before opting for definite cessation of tumor resection close to the motor pathways if MEP deterioration proves irreversible or reoccurs after some initial recovery. In turn, very much like in supratentorial surgery, stable recordings allow safe maximization of resection
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Thenar MEPs
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dissecting vertebral artery loop
temporary clip on brainstem perforator
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Fig. 9. In a patient with chronic left hyperpathia and mild spasticity, a large vertebral artery loop compressing the medulla oblongata was dissected from the brainstem and cushioned with a Teflon felt implant under SEP and MEP monitoring. MEPs showed some mild instability throughout the dissection procedure but did not deteriorate further during temporary clipping of a brainstem perforator, allowing for safe completion of this critical step of the procedure. The outcome was uneventful. Reprinted from Neuloh and Schramm (2004b) with permission from Springer, Wien, New York.
without the fear of impending new deficit (Neuloh and Schramm, 2004b; Neuloh et al., 2004). The data available so far do not allow a definite answer to the question whether motor monitoring improves the outcome of brainstem surgery. The multitude of factors involved including the impact of other monitoring and mapping techniques typically applied at the same time would require a very large number of cases in a possible prospectively controlled study, although this might be the way to go in the future. For the time being, it appears prudent enough to conclude from recent retrospectively controlled data for spinal cord surgery (Sala et al., 2006) that MEP monitoring can significantly improve the functional and surgical outcome also in brainstem surgery.
References Agnew, WF and McCreery, DB (1987) Considerations for safety in the use of extracranial stimulation for motor evoked potentials. Neurosurgery, 20(1): 143–147. Akagami, R, Dong, CC and Westerberg, BD (2005) Localized transcranial electrical motor evoked potentials for monitoring cranial nerves in cranial base surgery. Neurosurgery, 57(Suppl. 1): 78–85; discussion 78–85. Albright, AL and Sclabassi, RJ (1985) Use of the Cavitron ultrasonic surgical aspirator and evoked potentials for the treatment of thalamic and brainstem tumors in children. Neurosurgery, 17(4): 564–568. Anderson, RC, Dowling, KC, Feldstein, NA and Emerson, RG (2003) Chiari I malformation: potential role for intraoperative electrophysiologic monitoring. J. Clin. Neurophysiol., 20(1): 65–72.
532 Bogucki, J, Gielecki, J and Czernicki, Z (1997a) The anatomical aspects of a surgical approach through the floor of the fourth ventricle. Acta Neurochir. (Wien), 139(11): 1014–1019. Bogucki, J, Gielecki, J and Czernicki, Z (1997b) Digitalimage analysis of the rhomboid fossa surface. Folia Morphol. (Warsz), 56(3): 129–135. Bogucki, J, Czernicki, Z and Gielecki, J (2000) Cytoarchitectonic basis for safe entry into the brainstem. Acta Neurochir. (Wien), 142(4): 383–387. Bricolo, A and Turazzi, S (1995) Surgery for gliomas and other mass lesions of the brainstem. Adv. Tech. Stand. Neurosurg., 22: 261–341. Cedzich, C, Pechstein, U, Schramm, J and Scha¨fer, S (1998) Electrophysiological considerations regarding electrical stimulation of motor cortex and brainstem in humans. Neurosurgery, 42(3): 527–532. Cedzich, C, Pechstein, U, Zentner, J and Van Roost, D (1999) Minimally invasive stereotactically-guided extirpation of brainstem cavernoma with the aid of electrophysiological methods. Minim. Invasive Neurosurg., 42(1): 41–43. Chang, SD, Lopez, JR and Steinberg, GK (1999) Intraoperative electrical stimulation for identification of cranial nerve nuclei. Muscle Nerve, 22(11): 1538–1543. Deletis, V (1993) Intraoperative monitoring of the functional integrity of the motor pathways. Adv. Neurol., 63: 201–214. Deletis, V (2002) Intraoperative neurophysiology and methodologies used to monitor the functional integrity of the motor system. In: V Deletis and J Shils (Eds.), Neurophysiology in Neurosurgery.Academic Press, London, pp. 25–51. Deletis, V and Kothbauer, K (1998) Intraoperative neurophysiology of the corticospinal tract. In: E Sta˚lberg, HS Sharma and Y Olsson (Eds.), Spinal Cord Monitoring. Springer, Wien, New York, pp. 421–444. Dong, CC, MacDonald, DB, Akagami, R, Westerberg, B, Alkhani, A, Kanaan, I and Hassounah, M (2005) Intraoperative facial motor evoked potential monitoring with transcranial electrical stimulation during skull base surgery. Clin. Neurophysiol., 116(3): 588–596. Eisner, W, Schmid, UD, Reulen, HJ, Oeckler, R, OlteanuNerbe, V, Gall, C and Kothbauer, K (1995) The mapping and continuous monitoring of the intrinsic motor nuclei during brainstem surgery. Neurosurgery, 37(2): 255–265. Fahlbusch, R and Strauss, C (1991) Surgical significance of cavernous hemangioma of the brainstem. Zentralbl. Neurochir., 52(1): 25–32. Fahlbusch, R, Strauss, C and Huk, W (1991) Pontine-mesencephalic cavernomas: indications for surgery and operative results. Acta Neurochir. Suppl. (Wien), 53: 37–41.
G. NEULOH ET AL. Gentili, F, Lougheed, WM, Yamashiro, K and Corrado, C (1985) Monitoring of sensory evoked potentials during surgery of skull base tumours. Can. J. Neurol. Sci., 12 (4): 336–340. Glasker, S, Pechstein, U, Vougioukas, VI and Van Velthoven, V (2006) Monitoring motor function during resection of tumours in the lower brainstem and fourth ventricle. Childs Nerv. Syst., 22(10): 1288–1295. Gordon, B, Lesser, RP, Rance, NE, Hart, J, Jr., Webber, R, Uematsu, S and Fisher, RS (1990) Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr. Clin. Neurophysiol., 75(5): 371–377. Grabb, PA, Albright, AL, Sclabassi, RJ and Pollack, IF (1997) Continuous intraoperative electromyographic monitoring of cranial nerves during resection of fourth ventricular tumors in children. J. Neurosurg., 86(1): 1–4. Houtteville, JP (1995) The surgery of cavernomas both supra-tentorial and infra-tentorial. Adv. Tech. Stand. Neurosurg., 22: 185–259. Iadecola, C, Nakai, M, Arbit, E and Reis, DJ (1983) Global cerebral vasodilatation elicited by focal electrical stimulation within the dorsal medullary reticular formation in anesthetized rat. J. Cereb. Blood Flow Metab., 3(3): 270–279. Kohno, K, Matsui, S, Nishizaki, A, Takeda, S, Sadamoto, K and Sakaki, S (1993) Successful total removal of intramedullary hemangioblastoma from the medulla oblongata. Surg. Neurol., 39(1): 25–30. Kombos, T, Suess, O, Pietila, T and Brock, M (2000) Subdural air limits the elicitation of compound muscle action potentials by high-frequency transcranial electrical stimulation. Br. J. Neurosurg., 14(3): 240–243. Kothbauer, K, Deletis, V and Epstein, FJ (1997) Intraoperative spinal cord monitoring for intramedullary surgery: an essential adjunct. Pediatr. Neurosurg., 26(5): 247–254. Kyoshima, K, Kobayashi, S, Gibo, H and Kuroyanagi, T (1993) A study of safe entry zones via the floor of the fourth ventricle for brainstem lesions. Report of three cases. J. Neurosurg., 78(6): 987–993. Lang, J, Jr., Ohmachi, N and Lang, J, Sr. (1991) Anatomical landmarks of the rhomboid fossa (floor of the 4th ventricle), its length and its width. Acta Neurochir. (Wien), 113(1–2): 84–90. Manninen, PH, Patterson, S, Lam, AM, Gelb, AW and Nantau, WE (1994) Evoked potential monitoring during posterior fossa aneurysm surgery: a comparison of two modalities. Can. J. Anaesth., 41(2): 92–97. M ller, AR and Jannetta, PJ (1984) Preservation of facial function during removal of acoustic neuromas. Use of monopolar constant-voltage stimulation and EMG. J. Neurosurg., 61(4): 757–760.
CEREBRAL NEUROSURGERY Morota, N and Deletis, V (2006) The importance of brainstem mapping in brainstem surgical anatomy before the fourth ventricle and implication for intraoperative neurophysiological mapping. Acta Neurochir. (Wien), 148(5): 499–509. Morota, N, Deletis, V, Epstein, FJ, Kofler, M, Abbott, R, Lee, M and Ruskin, K (1995) Brainstem mapping: neurophysiological localization of motor nuclei on the floor of the fourth ventricle. Neurosurgery, 37(5): 922–929; discussion 929–930. Morota, N, Deletis, V, Lee, M and Epstein, FJ (1996) Functional anatomic relationship between brainstem tumors and cranial motor nuclei. Neurosurgery, 39(4): 787–793; discussion 793–794. Neuloh, G and Schramm, J (2002) Intraoperative neurophysiological mapping and monitoring for supratentorial procedures. In: V Deletis and JL Shils (Eds.), Neurophysiology in Neurosurgery. Academic Press/Elsevier Science, Amsterdam, pp. 339–401. Neuloh, G and Schramm, J (2004a) Monitoring of motor evoked potentials compared with somatosensory evoked potentials and microvascular Doppler ultrasonography in cerebral aneurysm surgery. J. Neurosurg., 100(3): 389–399. Neuloh, G and Schramm, J (2004b) Motor evoked potential monitoring for the surgery of brain tumours and vascular malformations. Adv. Tech. Stand. Neurosurg., 29(5): 171–228. Neuloh, G, Pechstein, U, Cedzich, C and Schramm, J (2004) Motor evoked potential monitoring with supratentorial surgery. Neurosurgery, 54(5): 1061–1070; discussion 1070–1072. Pechstein, U, Cedzich, C, Nadstawek, J and Schramm, J (1996) Transcranial high-frequency repetitive electrical stimulation for recording myogenic motor evoked potentials with the patient under general anesthesia. Neurosurgery, 39(2): 335–343; discussion 343–344. Pechstein, U, Zentner, J, Van Roost, D and Schramm, J (1997) Surgical management of brainstem cavernomas. Neurosurg. Rev., 20(2): 87–93. Pollack, IF, Hoffman, HJ, Humphreys, RP and Becker, L (1993) The long-term outcome after surgical treatment of dorsally exophytic brainstem gliomas. J. Neurosurg., 78(6): 859–863. Quinones-Hinojosa, A, Lyon, R, Du, R and Lawton, MT (2005) Intraoperative motor mapping of the cerebral peduncle during resection of a midbrain cavernous malformation: technical case report. Neurosurgery, 56(Suppl. 2): E439; discussion E439. Romstock, J, Strauss, C and Fahlbusch, R (2000) Continuous electromyography monitoring of motor cranial nerves during cerebellopontine angle surgery. J. Neurosurg., 93(4): 586–593. Ruskin, KJ, Deletis, V and Morota, N (1994) Anesthesia and intraoperative monitoring. J. Neurosurg., 80(5): 946–947.
533 Sala, F, Lanteri, P and Bricolo, A (2004) Motor evoked potential monitoring for spinal cord and brainstem surgery. Adv. Tech. Stand. Neurosurg., 29: 133–169. Sala, F, Palandri, G, Basso, E, Lanteri, P, Deletis, V, Faccioli, F and Bricolo, A (2006) Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery, 58(6): 1129–1143; discussion 1129– 1143. Samii, M, Eghbal, R, Carvalho, GA and Matthies, C (2001) Surgical management of brainstem cavernomas. J. Neurosurg., 95(5): 825–832. Sandalcioglu, IE, Wiedemayer, H, Secer, S, Asgari, S and Stolke, D (2002) Surgical removal of brainstem cavernous malformations: surgical indications, technical considerations, and results. J. Neurol. Neurosurg. Psychiatry, 72 (3): 351–355. Soustiel, JF, Hafner, H, Chistyakov, AV, Guilburd, JN, Zaaroor, M, Yussim, E and Feinsod, M (1993) Monitoring of brainstem trigeminal evoked potentials. Clinical applications in posterior fossa surgery. Electroencephalogr. Clin. Neurophysiol., 88(4): 255–260. Strauss, C and Fahlbusch, R (1997) Anatomical aspects for surgery within the floor of the IVth ventricle. Zentralbl. Neurochir., 58(1): 7–12. Strauss, C, Romstock, J, Nimsky, C and Fahlbusch, R (1993) Intraoperative identification of motor areas of the rhomboid fossa using direct stimulation. J. Neurosurg., 79(3): 393–399. Strauss, C, Lutjen-Drecoll, E and Fahlbusch, R (1997) Pericollicular surgical approaches to the rhomboid fossa. Part I. Anatomical basis. J. Neurosurg., 87(6): 893–899. Strauss, C, Romstock, J and Fahlbusch, R (1999) Pericollicular approaches to the rhomboid fossa. Part II. Neurophysiological basis. J. Neurosurg., 91(5): 768–775. Strauss, C, Naraghi, R, Bischoff, B, Huk, WJ and Romstock, J (2000) Contralateral hearing loss as an effect of venous congestion at the ipsilateral inferior colliculus after microvascular decompression: report of a case. J. Neurol. Neurosurg. Psychiatry, 69(5): 679–682. Taniguchi, M, Cedzich, C and Schramm, J (1993) Modification of cortical stimulation for motor evoked potentials under general anesthesia: technical description. Neurosurgery, 32(2): 219–226. Van Veelen-Vincent, ML, Pierre-Kahn, A, Kalifa, C, Sainte-Rose, C, Zerah, M, Thorne, J and Renier, D (2002) Ependymoma in childhood: prognostic factors, extent of surgery, and adjuvant therapy. J. Neurosurg., 97(4): 827–835. Wagner, W, Peghini-Halbig, L, Maurer, JC and Perneczky, A (1994) Intraoperative SEP monitoring in neurosurgery around the brainstem and cervical spinal cord: differential recording of subcortical components. J. Neurosurg., 81(2): 213–220.
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CHAPTER 37
Mapping and monitoring for brainstem lesions Georg Neuloh*, Christian Strauss and Johannes Schramm Neurochirurgische Universita¨tsklinik, D-53105 Bonn, Germany
37.1. Brainstem mapping
37.1.2. Stimulation technique
37.1.1. Introduction
Various stimulation techniques can be used (Strauss et al., 1993; Eisner et al., 1995; Morota et al., 1995; Chang et al., 1999). Constant voltage, constant current, bipolar or monopolar techniques have all been successfully employed. Constant current bipolar stimulation with rectangular monophasic impulses (a stimulus duration of 100–400 ms, a stimulus frequency not exceeding 10 Hz and intensities up to 2–5 mA) has proved reliable and safe and has been used by our group since 1996 (Strauss et al., 1999). Following surgical exposure of the rhomboid fossa, a hand-held stimulation probe is moved on the surface of the rhomboid fossa under constant electrical stimulation using rather high stimulation intensities (2 mA). The stimulation tip should have a rather planar area in order to avoid injury to the ependyma and underlying tissue (Fig. 3) (Strauss et al., 1993). The short distance, for example of 0.25 mm, from the ependyma to the ascending fibers of the facial nerve within the facial colliculus has to be considered (Strauss and Fahlbusch, 1997; Strauss et al., 1997). Supramaximal stimulation considerably shortens the period of mapping and easily identifies structures of the facial colliculus within several seconds, but by nature is not specific. With the area of interest identified, stimulation intensity is then turned down to threshold levels, which in a normal anatomical situation usually measures around 0.05 mA, when the colliculus is the target. With the threshold technique, the area of the shortest distance between facial nerve fibers and the ependyma can be selectively identified (Strauss et al., 1999). Usually the area of shortest distance can be identified paramedian to the median sulcus, where the ascending fibers of the facial nerve come closest to the surface (0.25 mm) (Strauss et al., 1997). With marginal variation of the stimulation intensity, a road map of the facial nerve fibers can be drawn (Fig. 1). With the same technique, other motor nerve nuclei (V, VI, IX/X, and XII) can
Surgical treatment of brainstem lesions is limited by dense concentration of functionally important neural pathways, nuclei, and fibers in pons variolii and medulla oblongata and the lack of reliable visible anatomical landmarks (Lang et al., 1991). Since most brainstem lesions are approached via the IVth ventricle, the presence of functionally intact brain tissue between ependyma and lesion poses already a potential risk due to the surgical corridor itself. In pontine lesions, facial and abducens nerve deficits as well as conjugated gaze palsies can affect the quality of life. Deficits of lower cranial nerve nuclei (nucleus n.hypoglossii, nucleus ambiguus, nucleus dorsalis n.vagi as the parasympathetic motor nucleus of the vagal nerve) are severe life-threatening complications following surgery of medullary lesions. Careful anatomical studies have defined safe entry zones into the brainstem above and below the facial colliculus measuring several millimeters (Fig. 1) (Kyoshima et al., 1993; Bogucki et al., 1997a,b, 2000; Strauss et al., 1997). The effect of space occupying intrinsic lesions on the superficial anatomy of the rhomboid fossa, however, limits the value of these morphometric investigations (Strauss et al., 1993, 1997). Direct electrical stimulation during surgery has emerged as a reliable and safe technique for identification of superficially located nuclei and fibers in order to define safe entry zones into pons and medulla (Figs. 1–3) (Strauss et al., 1993, 1999; Eisner et al., 1995; Morota et al., 1995, 1996; Chang et al., 1999; Morota and Deletis, 2006).
* Correspondence to: Georg Neuloh, M.D., Neurochirurgische Universita¨tsklinik, D-53105 Bonn, Germany. Tel.: þ49-228-287-6521; fax: þ49-228-287-4758. E-mail: [email protected] (G. Neuloh).
IV 14 mm VI VII
9 mm
X
XII
Fig. 1. Anatomical schematic drawing of superficially located motor nuclei and fibers of the floor of the rhomboid fossa (left side) with corresponding operative site (right side). The nuclei and fibers were mapped using electrical stimulation and indicated by black silk sutures.
Fig. 2. Selective stimulation of the VIth nerve nucleus. Multiple EMG traces of various target muscles demonstrate selective stimulation effect.
Fig. 3. Supracollicular approach to a recurrent symptomatic pontine cavernous hemangioma. The patient had been operated upon for this lesion several years ago using an approach above the right facial colliculus. Following localization with the hand-held stimulator (upper left), the hematoma was released (upper right) and the vascular malformation subsequently removed (lower left and right).
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be localized. Stimulation intensity has to be adjusted accordingly, since these nuclei are located further away from the ependyma surface. For identification of the nucleus of the hypoglossal nerve, stimulation intensity of 1 mA and more have to be employed. It has also to be taken into consideration that higher stimulation intensities are less specific and may result in diffuse stimulation effects. We have never employed stimulation intensities above 5 mA, except for one patient who was operated upon for a primary hematoma of the pons. In this patient, we used up to 10 mA stimulation intensity. Stimulation intensities may vary according to the underlying disease. In tumors infiltrating the floor of the fourth ventricle, higher intensities may be required when stimulation is applied through the tumor tissue, in order to guide the extent of removal, for example, in primitive neuroectodermal tumor (PNET) and ependymomas. 37.1.3. Recording technique Recording electrodes are placed into the target muscles. We use a pseudobipolar recording setup with two electrodes for each muscle. These electrodes are placed 5–10 mm apart and are secured by tapes in order to avoid dislocation (Strauss et al., 1999; Romstock et al., 2000). For the lateral rectus muscle, we use insulated electrodes to avoid unintended recordings from the orbicularis oris muscle. For lower cranial nerve monitoring, electrodes are placed into the soft palate and into the pharyngeal wall. For vocal cord monitoring, we have directly placed electrodes into the vocalis muscle under laryngoscopic control, but lately have exclusively relied on endotracheal tube electrodes. For hypoglossal nucleus localization, we apply two electrodes into the tip of the tongue. For practicability, it is sufficient to use one pair of electrodes for hypoglossal nuclei, since the nuclei of both sides are located extremely close together (0.6 mm). The distance of the upper pole of the hypoglossal nerve nuclei from the ependyma measures 0.55 mm. This results in a stimulation threshold of 1–2 mA. This stimulus intensity evokes responses from both nuclei. Other than that we record activity separately from both sides. For the trigeminal motor nucleus, we apply electrodes into the masseter muscle. With a standard two-channel recording setup and referential recordings, motor responses from the orbicularis oris muscle may prove difficult to differentiate. We therefore routinely record facial nerve activity from all three branches of the facial nerve.
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Multichannel recordings are required for most brainstem lesions in order to simultaneously record activity from all possible target muscles. This ensures selectivity of responses and proved time saving (Fig. 2). We therefore do not advocate the standard twochannel recording procedure techniques as for example in acoustic neuroma surgery, although in selected cases reduction to two channels may be sufficient (Fig. 3). 37.1.4. Anesthesia The anesthetic regimen is based on total intravenous anesthesia (TIVA). Following induction with midazolam, nitrous oxide and a short-acting muscle relaxant (atracurium besilate) anesthesia was maintained with propofol (6–12 mg/kg/h) and alfentanil (60 mg/kg/h). Muscle relaxing agents were not given until the very end of the surgical procedure (Strauss et al., 1999; Romstock et al., 2000). With respect to cost management, volatile anesthetic regimens have also proved to have no negative influence on the reliability of stimulation (Ruskin et al., 1994; Morota et al., 1995). 37.1.5. Safety aspects Cardiovascular side effects of electrical stimulation are of particular concern, since the parasympathetic motor nucleus dorsalis n.vagi is located directly lateral to the trigonum hypoglossi. With the stimulation parameters outlined above, a short run of asymptomatic ventricular extrasystoles was observed in a single patient of a series of more than 100 cases immediately following stimulation. Other than that measurable effects regarding cardiac arrhythmia or blood pressure were never observed since introduction of this method in 1991. Possible brain damage with respect to electrical stimulation is mainly caused by an imbalance of the blood–brain barrier. Damage of the barrier is dependent on the applied charge density (Coulomb (mC)/cm2 phase) under the stimulation electrode (Agnew and McCreery, 1987; Gordon et al., 1990). From histology of epileptogenic tissue, which was chronically stimulated prior to resection, it is known that up to a charge density of 57 mC/cm2 phase no histological changes occur (Agnew and McCreery, 1987; Gordon et al., 1990). For constant voltage stimulation, the electrode surface of 0.0043 cm2 produces a charge density of 0.59 mC/cm2 phase (M ller and Jannetta, 1984). Constant current stimulation produces
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charge densities up to 0.0014 mC/cm2 phase. For cortical stimulation in surgery of centrally located tumors and in epilepsy surgery, charge densities up to several 100 mC/pulse/cm2 are considered safe (Cedzich et al., 1998). Limitation of electrical stimulation to 1 V (constant voltage technique) and 2 mA (constant current technique) has no noticeable adverse side effects regarding the blood–brain barrier (Strauss et al., 1999). The limitation of the stimulus frequency to 10 Hz is based on animal experiments in which changes of cerebral blood flow, blood pressure, and intracranial pressure were provoked by using stereotactically implanted electrodes into the dorsal and rostral areas of the formatio reticularis. Maximal effects were seen with 40–50 Hz, although when using high stimulus intensities (50 mA) effects were observed with as low as 2 Hz with limitation exclusively to the time period of stimulation (Iadecola et al., 1983). 37.1.6. Site of stimulation Precise location of the stimulation site is a prerequisite for the clinical use of this technique. Since peripheral electromyographic (EMG) responses are obtained with stimulation intensities as low as 0.1 mA and a stimulation duration of 100 ms, the peripheral motor neuron seems most likely the site of stimulation. These parameters are similar to those for identification of the facial nerve during cerebellopontine angle surgery (M ller and Jannetta, 1984; Romstock et al., 2000). These parameters are inadequate for stimulation of the first motor neuron (Cedzich et al., 1998). For direct cortical stimulation of the pyramidal tract, the stimulation intensity usually varies between 2 and 25 mA with frequencies above 40–50 up to 500 Hz using a stimulation duration between 100 and 400 ms (Cedzich et al., 1998). A further peripheral stimulation toward the direction of root exit zones is unlikely, since stimulation would include other peripheral motor neurons of the areas of the cranial nerves. This was excluded by simultaneous bilateral multichannel EMG recordings demonstrating selective responses on the side and site of stimulation (Fig. 2). The selectivity of responses also excludes diffuse brainstem stimulation. The site can be directly calculated with the equation (I ¼ K d2), using the actual motor threshold for the facial nerve fibers and the fibers of the nucleus n.hypoglossii (Strauss et al., 1997, 1999) and the anatomically measured distances between the fibers and
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the ependyma surface (Strauss and Fahlbusch, 1997; Strauss et al., 1997). The clinical observation by Morota et al. using high dosage of volatile anesthetic without negative effect on the stimulation results also point to the peripheral motor neurons as the site of stimulation, since volatile anesthetics have a negative effect on the excitability of the first motor neuron, where as its influence regarding the excitability of the peripheral motor neuron can be neglected (Ruskin et al., 1994; Morota et al., 1995; Cedzich et al., 1998). Most likely, the axonal cone with an electric threshold 10 times lower than the axon’s threshold represents the presumed site of stimulation (Strauss et al., 1999). 37.1.7. Clinical value and review of literature Since the technique of intraoperative localization has rapidly evolved as a mandatory adjunct for brainstem surgery, a prospective study on its clinical value has never been published. Apart from brainstem cavernous hemangiomas (Fig. 3), for which the technique was originally designed (Fahlbusch et al., 1991; Houtteville, 1995; Samii et al., 2001; Sandalcioglu et al., 2002), brainstem tumors such as gliomas and ependymomas are of particular interest (Fig. 4), since the extent of surgical removal has been identified as the major prognostic factor (Pollack et al., 1993; Van Veelen-Vincent et al., 2002). Based on our experience, we have evaluated all surgically treated brainstem tumors between 1991 and 1999, which had been operated upon using this technique and compared their outcome with a matched (histology, location) series of patients undergoing surgery without mapping. Functional outcome of electrically localized motor nuclei and fibers (cranial nerves V, VI, VII, IX/X, and XII) were investigated before, immediately after surgery and on follow up after one year (Fig. 5). The study population consisted of 29 patients in each group (7 PNET, 12 medial ependymomas, 10 gliomas of various growth patterns) with an average age of 23.5 years in the “mapping” group versus 29 years in the nonmonitored group, tumor size averaged at 3.5 cm each, and 18 patients in both groups underwent postoperative radiotherapy. Six patients of the “mapping” group received chemotherapy, as compared to 7 “non-mapped” patients. Before surgery, the absolute number of cranial nerve deficits was comparable. After surgery, both groups deteriorated with respect to their cranial nerve deficits, which was to be expected, but after one year
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Fig. 4. Large pilocytic astrocytoma on axial and sagittal T1-weighted MRI images with contrast enhancement, before (upper) and after surgical removal (lower). The surgical corridor is clearly visible (lower left). Postoperative persistent morbidity was limited to a motor weakness of the trigeminal nerve, corresponding to the surgical corridor at the lateral edge of the rhomboid fossa.
mapped patients showed significantly better functional results (w2 test: p ¼ 0.003). In those patients undergoing surgery without the application of intraoperative mapping, postoperative cranial nerve deficits remained fixed and did not recover over the observation period
(Fig. 5). Dorsally exophytic brainstem gliomas and focal endophytic gliomas as well as low grade ependymomas seem to benefit from careful intraoperative mapping (Fig. 4). These results, although based on a study design implying a low evidence level, underline
Fig. 5. Total number and course of cranial nerve deficits (V, VI, VII, IX/X, and XII) as evaluated in a retrospective analysis of 58 patients with brainstem tumors (glioma, ependymoma, PNET) undergoing surgery with and without brainstem mapping.
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the neurosurgical impact of this technique. Direct electrical brainstem stimulation for mapping of the floor of the IVth ventricle is the neurophysiologic method with the fastest and widest acceptance in neurosurgery. Two years following its first description in 1993 (Strauss et al., 1993), this technique has been stated as mandatory for surgical management of brainstem lesions (Bricolo and Turazzi, 1995). Based on published experiences of several groups, the technique has gained wide acceptance, because it is easy to apply, safe, and provides reliable information on the location of motor brainstem fibers and nuclei (Strauss et al., 1993; Eisner et al., 1995; Morota et al., 1995, 1996; Chang et al., 1999; Strauss et al., 1999; Morota and Deletis, 2006). It must be concluded that identification of superficially located motor nuclei prior to microsurgical removal of brainstem lesions does not exclude functional morbidity of identified structures following surgery (Morota et al., 1996). The technique of threshold stimulation is a method for localization, but not for intraoperative monitoring. Continuous multichannel EMG recordings and analysis of these data have yet failed to identify pathological EMG activity, indicating damage to monitored structures. The presence of prolonged EMG activity (bursts and spikes) has been associated with postoperative morbidity (Grabb et al., 1997); however, in our own data, we have not been able to reliably associate presence of spikes and bursts with cranial motor nerve deficits after surgery. A specific EMG pattern, comparable to the “A-train” indicating pending damage to brainstem nuclei has so far not been identified (Romstock et al., 2000). At present, any prolonged EMG activity has to be considered potentially harmful. Future research should be directed toward detailed software-based analysis of intraoperative EMG in order to reliably apply this technique for continuous monitoring during removal of brainstem lesions. 37.2. Brainstem motor-tract monitoring 37.2.1. Introduction Continuous monitoring of sensory evoked responses [somatosensory evoked potential (SEP) and BAEP, rarely trigeminal sensory responses (Soustiel et al., 1993)] during brainstem surgery was described early (Albright and Sclabassi, 1985) and is still a commonly applied technique for brainstem monitoring, although reports on clinical applications remain anecdotal (Gentili et al., 1985; Kohno et al., 1993; Wagner
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et al., 1994; Pechstein et al., 1997; Cedzich et al., 1999; Anderson et al., 2003). However, the tegmental somatosensory and auditory pathways do not cover an area of the brainstem large enough (Fahlbusch and Strauss, 1991) to represent its general functional state with a high sensitivity, although combined SEP and BAEP monitoring has an increased sensitivity for, for example, brainstem ischemia as compared with either method alone (Manninen et al., 1994). Specifically, the functional integrity of the corticospinal fibers cannot be validly monitored by sensory evoked potentials. It must be remembered that the pyramidal tract courses through the ventral cerebral peduncles, the fibrae longitudinales of the pars ventralis pontis, and the likewise ventrally located decussatio pyramidorum of the medulla oblongata, clearly separated from the bulbothalamic and spinothalamic fibers of the lemniscus medialis and from the auditory pathways and nuclei of the lateral lemniscus and the corpus trapezoideum, also with a partially differing (ventromedial vs. lateral perforators) blood supply, particularly at the pontine level. The same is true for the corticonuclear fibers of the mesencephalic and upper rhombencephalic pyramidal tract. Reliable monitoring of the motor pathway’s functional integrity under general anesthesia is a more recent development (Deletis, 1993; Taniguchi et al., 1993; Pechstein et al., 1996; Deletis and Kothbauer, 1998), and has been extensively explored in the neurosurgical context for supratentorial brain and spinal cord surgery (see Chapters 15–18 and 21 in this volume). The application of motor evoked potential techniques for brainstem monitoring has been discussed more sporadically (Cedzich et al., 1999; Neuloh and Schramm, 2004b; Sala et al., 2004; Akagami et al., 2005; Dong et al., 2005; Glasker et al., 2006). Here, we will briefly summarize methodological and clinical features of the technique which are important for brainstem monitoring. Whereas brainstem monitoring is of obvious importance in child neurosurgery, there are no truly childspecific aspects of brainstem motor monitoring except for the more difficult elicitation of motor responses in young children which require the most careful selection of optimum stimulation and recording parameters in order to obtain reliable motor responses. 37.2.2. Motor evoked potential stimulation Transcranial motor evoked potential pulse-train stimulation (Pechstein et al., 1996; Neuloh and Schramm, 2004b), in general as applicable for posterior fossa
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approaches, is described in detail elsewhere in this volume and cannot be fully discussed here. The electrode montage is at sites about 1–2 cm anterior to the C1-C2 or C3-C4 positions of the International 10– 20 system. A C3/4-Cz þ 2 cm electrode montage has proven optimal for specific corticobulbar tract monitoring (see below). More lateral positions provide a more efficient stimulation of the corticospinal and particularly of the corticobulbar tracts, but the movement artifact typically associated with transcranial electrical stimulation may be more pronounced. Constant current stimulation is preferred for a better control of current distribution and a lesser twitching artifact. Since upper extremity muscle motor evoked potentials (MEPs) are typically recorded for brainstem monitoring, current intensities of 100 mA or less are sufficient to obtain the desired just-above threshold motor responses. Supramaximal stimulation is discouraged to avoid caudal bypassing of the target pathways in particular with mesencephalic procedures. If surgery is performed in a sitting or semi-sitting position, subdural air collection after durotomy may dramatically increase the electrical impedance (Kombos et al., 2000). More lateral electrode positions are preferred over a very strong stimulation intensity to overcome the high apparent motor threshold for the above reasons. Too lateral electrode positions caudally to the target structures may in theory occur in midbrain surgery, but the typical approaches these procedures are usually not performed in a sitting position. Successful MEP monitoring may be impossible in up to 10% of cases mainly due to the problem of subdural air collection. The frequency of MEP stimulation depends on the monitoring program implemented in a given setting. Alternating only with SEPs, a stimulation rate of about 2 per minute can be achieved, in critical situations MEP alone may be performed at a higher rate. If BAEPs are recorded as well, MEPs may be obtained only every few minutes (Dong et al., 2005), although every attempt must be made to increase the update speed since real-time monitoring as required for useful surgery monitoring cannot be realized at such a low stimulation rate. 37.2.2.1. Corticospinal tract mapping With lesions displacing the corticospinal tract or distorting the local peduncular or pontine topography, direct stimulation of the motor fibers via a hand-held probe can be used, employing the multipulse MEP technique to map the motor tract (Cedzich et al.,
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1998; Sala et al., 2004; Quinones-Hinojosa et al., 2005) for identification of safe entry zones for the surgical approach. As opposed to cortex stimulation, “cathodal” stimulation may be most effective (Cedzich et al., 1998). It must be noted that this mapping procedure differs fundamentally from, and cannot replace continuous motor monitoring which is rather intended to pick up impending motor damage at unexpected instances. There are no aspects of anesthesia and safety with MEP stimulation which are truly specific to brainstem monitoring; therefore, we refer the reader to the respective chapters in this volume. 37.2.3. MEP recording and interpretation In our experience, recording of MEPs from distal upper limb muscles is adequate for brainstem corticospinal tract monitoring. We prefer subcutaneous needle electrodes placed in a muscle-tendon fashion in order to pick up compound muscle responses (Neuloh and Schramm, 2004b). As it is well known from MEP monitoring for pericentral tumors, motor responses can be usefully recorded after direct cortical stimulation from facial muscles (Fig. 6, Neuloh and Schramm, 2002, 2004b; Neuloh et al., 2004) to avoid lesions of the corticonuclear projections with lateral resection. Similarly, continuous corticobulbar tract monitoring can be achieved during brainstem surgery with transcranial stimulation and recording
Fig. 6. Facial muscle response to transcranial pulse-train stimulation of the corticonuclear tract in comparison with arm and leg muscle responses. Note the large stimulus artifact and the clearly discernible latency around 15 ms which excludes peripheral cranial nerve stimulation.
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trade-off) in (Dong et al., 2005). Since corticonuclear MEP responses do not seem to represent all of the target fibers, mild paresis despite preserved responses as well as partially preserved function despite irreversible loss may occur (Dong et al., 2005). In spinal cord monitoring (see Chapter 16 in this volume), D-wave monitoring via epidural electrodes provides a semi-quantitative amplitude criterion for assessment of corticospinal tract function, whereas only the presence or absence of muscular motor responses is useful parameter of motor function due to the propriospinal supportive motor system (Kothbauer et al., 1997; Deletis, 2002; Sala et al., 2004). Although a typical median suboccipital craniotomy would allow for placement of cervical epidural electrodes, brainstem surgery does not necessarily require this additional recording technique due to the above semi-quantitative relation between muscular MEP responses and motor function comparable to supratentorial surgery (Neuloh and Schramm, 2004b; Neuloh et al., 2004; Akagami et al., 2005; Dong et al., 2005).
from facial and lower cranial nerve target muscles (Sala et al., 2004; Akagami et al., 2005; Dong et al., 2005), possibly providing a solution for the uncertainties associated with continuous cranial nerve EMG monitoring for brainstem surgery as discussed above in part I of this chapter. Direct peripheral cranial nerve excitation can easily occur with the transcranial stimulation technique and would lead to false-negative monitoring results with brainstem surgery. Therefore, a low suprathreshold stimulation intensity is mandatory for this corticobulbar monitoring technique. A single pulse stimulation at the intended current intensity for corticobulbar tract excitation can exclude peripheral nerve stimulation if it does not evoke a motor response, which would require transsynaptic multipulse train stimulation of the bulbar motoneuron as opposed to the peripheral nerve. However, if a clearly discernible typical MEP onset latency around 12–16 ms can be measured, the corticobulbar pathway must be involved and direct peripheral cranial nerve excitation which yields motor responses after 5–7 ms is very unlikely (Dong et al., 2005). The MEP amplitudes which are achieved with transcranial stimulation are less stable than after direct cortical stimulation. Therefore, the typical 50% amplitude criterion for significant MEP decrement which has proven valid in our experience (Fig. 7, Neuloh and Schramm, 2002, 2004a,b; Neuloh et al., 2004) and seems to apply also for brainstem monitoring (Akagami et al., 2005) is not always applicable. In particular for corticobulbar tract monitoring, where lower amplitudes and a lower signal-tonoise ratio is achieved, a somewhat tighter criterion must be chosen, for example, the 35% criterion which proved most valid (best sensitivity-specificity Intraoperative MEP Findings
37.2.4. Clinical applications 37.2.4.1. Indications for brainstem motor monitoring It is obvious from the above anatomical considerations that corticospinal/corticonuclear monitoring is mandatory with lesions within or in close adjacency to the ventral or ventrolateral aspect of the brainstem. This is true for both intra- and extraaxial lesions, including resectable gliomas, ependymomas, large petroclival and foramen-magnum meningiomas, epidermoids, cavernomas, arteriovenous vascular malformations, and very large vertebral or basilar artery aneurysms (Figs. 8 and 9). The ventral approach
Permanent new deficit
Motor Outcome Transient new deficit
No new deficit
Irreversible Loss
always
Irreversible Deterioration
frequent
frequent
rare
Reversible Loss
rare*
frequent
frequent
Reversible Deterioration
rare*
frequent
frequent
Unaltered
never
never**
always
*not yet observed in brainstem surgery **exception: mild facial paresis
Fig. 7. Qualitative correlation of intraoperative MEP findings and motor outcome as typically observed during supratentorial brain surgery and apparently applicable also for brainstem procedures. Modified with permission from Neuloh and Schramm (2004b).
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G. NEULOH ET AL. Thenar MEPs Right
Left
5 mV
OP Start
20 ms
Opening Dura CSF Outflow Dissecting ependymoma
Preoperative MRI
Warning
500 µV
End resection
OP End
Postoperative MRI
20 ms
Fig. 8. During surgery for an ependymoma of the cervicomedullary junction, resection was halted with MEP deterioration. MEPs recovered partially, and there was no new motor deficit postoperatively. Follow-up imaging confirmed the intraoperative impression that complete tumor resection had been achieved at the point of MEP deterioration. Modified with permission from Neuloh and Schramm (2004b).
determines the risk for brainstem motor function as much as a possible resection in adjacency to the motor fibers. One major concern, for example, with foramen magnum meningiomas is a possible affection of the vascular supply of the motor tract which has very little collateralization in this area. In our view, a targeted indication for any monitoring technique is desirable for reliable results rather than the accumulation of all available methods in all posterior fossa cases. We do not perform routine MEP/SEP monitoring in, for example, typical cerebellopontine angle tumor surgery, even with large vestibular schwannomas, where BAEP and cranial nerve mapping/monitoring provides adequate monitoring. Likewise, surgery via a rhomboid fossa approach for tegmental intrinsic tumors or cavernomas will require MEP monitoring only if these lesions extend deep into the brainstem. However, extended corticonuclear MEP monitoring (Dong et al., 2005) is a possible future routine application with such lesions, and preserved SEPs may indirectly indicate preserved functional integrity of the tegmentum.
37.2.4.2. Impact on surgery In our experience, ischemia arises with inadequate retraction, electrocoagulation, or manipulation of vessels during dissection, and is a major cause for new motor deficit in brainstem surgery. Venous congestion can cause delayed deficit and must be carefully avoided as well (Strauss et al., 2000). Therefore, if MEPs deteriorate, dissection is temporarily halted, retractors are released and possibly readjusted, the situs is checked and irrigation is applied as well as papaverine to possibly spastic vessels. With early intervention, MEP deterioration proves reversible in most cases and no permanent new deficit must be expected. If MEPs deteriorate during resection of a brainstem tumor, the above measures should be considered to reverse the MEP change, before opting for definite cessation of tumor resection close to the motor pathways if MEP deterioration proves irreversible or reoccurs after some initial recovery. In turn, very much like in supratentorial surgery, stable recordings allow safe maximization of resection
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Thenar MEPs
Median nerve SEPs
OP start
dissecting vertebral artery loop
temporary clip on brainstem perforator
Preoperative MRI
angiolysis
1 µV
2 mV
closing
10 ms
Preoperative DSA OP end 10 ms
Fig. 9. In a patient with chronic left hyperpathia and mild spasticity, a large vertebral artery loop compressing the medulla oblongata was dissected from the brainstem and cushioned with a Teflon felt implant under SEP and MEP monitoring. MEPs showed some mild instability throughout the dissection procedure but did not deteriorate further during temporary clipping of a brainstem perforator, allowing for safe completion of this critical step of the procedure. The outcome was uneventful. Reprinted from Neuloh and Schramm (2004b) with permission from Springer, Wien, New York.
without the fear of impending new deficit (Neuloh and Schramm, 2004b; Neuloh et al., 2004). The data available so far do not allow a definite answer to the question whether motor monitoring improves the outcome of brainstem surgery. The multitude of factors involved including the impact of other monitoring and mapping techniques typically applied at the same time would require a very large number of cases in a possible prospectively controlled study, although this might be the way to go in the future. For the time being, it appears prudent enough to conclude from recent retrospectively controlled data for spinal cord surgery (Sala et al., 2006) that MEP monitoring can significantly improve the functional and surgical outcome also in brainstem surgery.
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