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 14
Somatosensory evoked potentials for intraoperative mapping of the sensorimotor cortex Theodoros Kombos* Department of Neurosurgery, Charite´-Universita¨tsmedizin Berlin, D-12200 Berlin, Germany
14.1. Introduction Modern neurophysiological imaging and monitoring techniques enable precise localization of lesions and correlation of them to anatomical landmarks. These techniques increase safety and efficacy and reduce invasiveness. A more aggressive approach to a brain tumor increases survival and quality of life (Hirakawa et al., 1984; Laws et al., 1984; Ammirati et al., 1987; Ciric et al., 1987). Radicality though, is often limited by the proximity of functionally eloquent areas. MR imaging enables exact localization of lesions in relation to the central sulcus (Berger et al., 1990; Yousry et al., 1996), but the morphology and function do not necessarily correlate. Although functional imaging techniques such as positron emission tomography (PET) or fMRI do allow preoperative localization of eloquent areas, they are only available in a few centers worldwide and cannot be used routinely. Furthermore, image guidance alone is limited by the individual variations in the functional organization of the brain. Thus, intraoperative functional mapping and monitoring have proven to be complementary for localizing functionally relevant areas and allowing maximal tumor resection with minimal morbidity. The method of somatosensory evoked potential phase reversal (SEP-PR) was introduced by Goldring et al. (Goldring, 1978; Goldring and Gregorie, 1984) based on experience gained in epileptic surgery. A number of studies have since described its application in tumor surgery (Lesser et al., 1979; Allen et al., 1981; Allison, 1982, 1987; Desmedt and Che´ron, 1982; Grundy, 1983; Lu¨ders et al., 1983; Amassian and Cracco, 1987; Aiba and Seki, 1988; *
Correspondence to: Theodoros Kombos, Charite´-Universita¨tsmedizin Berlin, Campus Benjamin Franklin, Hindenburgdamm 30, D-12200 Berlin, Germany. E-mail:
[email protected] (T. Kombos).
Allison et al., 1989; Nuwer, 1991; Firsching et al., 1992; Cedzich et al., 1996). SEP-PR does allow intraoperative localization of the central sulcus but yields no functiona information. Following the technique of SEP-PR, its application as well as its limitations will be described. 14.2. Method Phase reversal of somatosensory evoked potentials is performed by stimulating the median or tibial nerve contralateral to the lesion. The median nerve contralateral to the lesion is stimulated at the wrist using surface electrodes placed 1.5 cm apart. For tibial nerve stimulation, the same electrode setup is used, but stimulation electrodes are placed at the inner ankle. A stimulus of 5.7 Hz is applied using a constant voltage electrical stimulator. Current intensity varies between 5 and 65 mA. Starting with 5 mA, the intensity is gradually increased until slight twitches of the thumb (median nerve) or the foot (tibial nerve) are obtained. Control of the proper function of the stimulator is achieved by using a stimulus level above the stimulation threshold. This minimizes technical problems during SEP-PR. Cortical SEPs, and therefore also SEP-PRs, are recorded by a strip electrode (a row of five or six electrodes embedded in silicon) or by a grid electrode (2 5 or 3 5) placed on the cortex (Fig. 1). Recordings are performed by a filter bandpass of 100– 1,500 Hz, but the filter bandpasses in intraoperative monitoring are “individually” set for each operation theater. The time base for median nerve SEP-PR is set at 50 ms and for tibial nerve SEP-PR at 80 ms. Grid or strip electrodes can be used. Using grid electrodes allows SEPs from larger cortical areas to be recorded simultaneously. A larger amplifier with more recording channels would be needed though, and the software setup for the recording would be
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Fig. 1. Grid electrode for recording somatosensory evoked potential phase reversal (SEP-PR). The black line indicates the central sulcus.
more demanding. Strip electrodes, in contrast, need up to eight recording channels, depending on their size. Repositioning of the electrode though, might be necessary in order to record clear SEP-PR. Care must be taken for the placement of the recording electrodes. The following factors must be taken into consideration during electrode placement: the electrodes must (1) cross the central sulcus, (2) cover the hand or leg area of the sensorimotor gyri, (3) make an angle of 15 with the sagittal direction, and (4) not cover the center of the lesion but instead lie adjacent to the visible margins of the tumor mass (Fig. 2). The location of the electrode must be adjusted to obtain maximum peak amplitudes by moving it in a mediolateral and frontolateral direction or by rotating it at angles of 15 .
Fig. 2. Diagram showing the correct positioning of the recording grid. Optimal position must have a 15 angle to the central sulcus.
T. KOMBOS
For median nerve SEP-PRs, the electrode must be placed in a cortical area between 3 and 8 cm from the midline. The largeness of this area is due to the large cortical representation area of the hand. For tibial nerve SEP-PR though, the cortical area is limited to 0–3 cm from the midline. Positioning the strip in the interhemispheric space is not recommended as this is technically very difficult and the correct position cannot be verified. The distance between the recording anode and cathode, especially in the operation theater, determines the quality of the recorded potential: the shorter the distance, the better the potential. The recording of the cortical SEP can be performed in two ways. For the “monopolar” setup, the cathode is placed on the forehead and every contact of the strip or grid is used as a cathode (Fig. 3A). For the “bipolar” setup, neighboring contacts of the strip are used alternatively as anodes or as cathodes (Fig. 3B). For example, using a four-contact strip, the recording setup would be: 1–2þ, 2–3þ, 3–4þ (Fig. 3). The advantage of the “bipolar” setup is, as mentioned before, the better quality of the recorded potentials, but interpretation is more difficult and advanced programming of the amplifier is needed. The time spent on identifying the central fissure after opening the dura did not usually exceed 5 min. 14.3. Discussion Phase reversal of somatosensory evoked potentials is based on the fact that the dipole of the afferent volley changes from the postcentral to the (Nuwer, 1991). A stimulus applied on a peripheral nerve is forwarded through the somatosensory pathway in the contralateral postcentral gyrus. Here, the electrical afferent volley can be recorded as SEP potential. In other words, the electrical stimulus applied on a peripheral nerve generates an electrical dipole on the postcentral gyrus. The polarity of this dipole changes, however, on the adjacent precentral gyrus (Fig. 4). Therefore, a somatosensory potential (N20/P30; N ¼ negative, P ¼ positive) can thus be recorded from the postcentral gyrus, and its mirror image (P0 20/N0 30) can be recorded from the precentral gyrus (Wood et al., 1988) (Fig. 5). For the tibial nerves, the recordings read P40/N45 and N0 40/P0 45 respectively (Fig. 6). The phase-reversal potential is quick and easy to record, and it provides reliable identification of the central sulcus until direct mapping can be done. Many studies have described the application of SEP-PR in tumor surgery in adults (Lesser et al.,
SOMATOSENSORY EVOKED POTENTIALS
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Fig. 3. A: Monopolar recording setup for somatosensory evoked potential phase reversal (SEP-PR). The cathode is placed on the forehead and every contact of the strip or grid is used as a cathode. B: Bipolar setup for SEP-PR. Neighboring contacts of the strip are used alternatively as anodes or as cathodes.
1979; Woolsey et al., 1979; Allen et al., 1981; Allison, 1982, 1987; Desmedt and Che´ron, 1982; Grundy, 1983; Lu¨ders et al., 1983; Amassian and Cracco, 1987; Aiba and Seki, 1988; Wood et al., 1988; Allison et al., 1989; Nuwer, 1991; Firsching et al., 1992; Cedzich et al., 1996). Hence, the technique is not only useful in adults but also in older children, where maturation of motor pathways is complete (Sala et al., 2002). In some cases, the typical phase reversal at 20 ms is questionable or missing, but characteristic late waveform components can be recorded from the electrode lying over the postcentral gyrus (Romsto¨ck et al., 2002). This involves either one single negative wave with a markedly high amplitude at 35 ms or a polyphasic sequence of positive and negative peaks
between 25 and 45 ms (Fig. 7). Waveforms may be more complex if the electrode is lying adjacent to or directly over the central sulcus. As a result, a varying number of small peaks within the major waves are seen, giving the impression of a transitional and less smooth waveform (Romsto¨ck et al., 2002). The most prominent succeeding components for the median nerve are a postcentral negative wave between 30 and 40 ms and a precentral N27 in recordings adjacent to the central sulcus. At more posterior recordings sites, the pattern of the postcentral N35 is not changed except for a gradual reduction in amplitude. In general, there is no systematic effect of the tumor masses on SEP-PR despite the fact that some of the patients had motor or sensory deficits. The
Fig. 4. Schematic explanation of somatosensory evoked potential phase reversal (SEP-PR). The dipole of the afferent volley changes from the postcentral to the precentral gyrus.
Fig. 5. Somatosensory evoked potential phase reversal (SEP-PR) following stimulation of the median nerve.
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Fig. 6. Somatosensory evoked potential phase reversal (SEP-PR) following stimulation of the tibial nerve.
situation is more complicated though with larger tumor sizes, severe preoperative neurological deficits, or lesions invading the precentral and postcentral gyri. Under such circumstances, reduced feasibility and reliability of the SEP-PR technique must be expected. Wood et al. (1988) have suggested that the large positive–negative waveform at 25 and 35 ms may serve
Fig. 7. No somatosensory evoked potential phase reversal (SEP-PR) is recorded; however, a single negative wave with a markedly high amplitude at 35 ms from the electrodes 3–6 is recorded. Electrodes 1 and 2 show no SEP.
T. KOMBOS
as an additional localizing criterion, as it is usually recorded with the highest amplitude from the postcentral gyrus at a location 10 mm medial to the hand area. SEP-PR is associated with a success rate of over 90% for intraoperative localization of the central sulcus (King and Schell, 1987; Wood et al., 1988). In our series (Kombos et al., 2000; Suess et al., 2003), SEP-PR was recorded as 97.14%, which corresponds to the results of other series. The failure rate may be accounted for by various factors: (1) tumor-related shifting of the central sulcus (Cedzich et al., 1996), (2) misplacement of the recording electrodes in relation to the anatomical location of the sensorimotor cortex — also called “off axis placement” (Wood et al., 1988), and (3) the influence of narcotic agents and brain edema (Cedzich et al., 1996). Dural adhesions in particular may have prevented correct placement of the electrodes and thus resulted in “failure-cases.” Babu and Chandy (1997) have reported that the SEPPR could be recorded in all patients with predominant motor disturbance. But in patients with marked sensorimotor deficits, the attempt to record an SEP was futile. In contrast, Sonoo et al. (1991) have reported on two patients with major sensory deficits and localized lesions of the postcentral gyrus in whom the scalp recording of N20–P20 and later waveforms were eliminated, and only a widespread frontal activity was obtained. These examples show that perplexing findings must be expected in patients with tumors. About 10% of the patients will not show the classic N20–P20 inversion, possibly as a result of three causes: (1) the tumor desynchronizes the propagated afferent electrical volleys along the thalamocortical pathway, (2) the mass effect of the lesion distorts the spatiotemporal projection of cortical electrical dipoles to the brain surface, and (3) the recording site may not be appropriate for recording a potential generated in the hand area of the postcentral gyrus. While phase reversal of sensory evoked potentials reliably identifies the central sulcus, it yields no information about motor function. Thus, anatomical identification of the central sulcus alone is not a sufficient safeguard against postoperative motor deficits. Therefore, an additional method must be used to map motor function. References Aiba, T and Seki, Y (1988) Intraoperative identification of the central sulcus: a practical method. Acta Neurochir. (Wien), 42: 22–26.
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