CHAPTER 64 Tailored Resections for Epilepsy
Although the first operations performed for the treatment of medically intractable epilepsy were obviously directed by the specific findings in individual patients1,2 and by the large formative experience of Penfield and Jasper in using electrocorticography (ECoG) to guide temporal resection,3 the majority of surgical interventions that have been performed since have been fairly standardized procedures. The recognition of certain epilepsy syndromes and their associated pathologies has enabled widespread application of such procedures as anterior temporal lobe resection, selective amygdalohippocampectomy, and hemispherectomy with remarkable success.4 There are certain settings, however, in which the surgical procedure may be improved in terms of seizure outcome or safety, or both, through tailoring of the surgical procedure to the specific patient. Indeed, in many instances such an approach is the only one possible.
The Basis for Tailored Resection
Temporal Lobe Resection
The role of tailored resection is least agreed on for epilepsy involving the temporal lobe. There are standardized approaches to temporal lobe epilepsy surgery that vary slightly according to side with respect to language dominance and inclusion of mesial structures, and reasonably good seizure outcomes overall have long been reported with these standardized approaches. The 1991 survey of epilepsy surgery centers compiled by Engel for the Second Palm Desert International Conference on the Surgical Treatment of the Epilepsies, held in Indian Wells, California, in February 1992, found seizure-free outcomes in 67.9% of patients undergoing anterior temporal resection.4 Recognition of variability among patients with respect to both the epileptogenic zone and language cortex, however, has led a number of surgical epilepsy teams to advocate tailoring the resection.
Distinguishing between mesial temporal sclerosis and temporal neocortical epilepsy represents one of the first rationales for implementation of this strategy. It was the ability to diagnose seizure onset localized to the hippocampus or amygdala that made selective amygdalohippocampectomy a viable treatment in the first place. Intracranial recording, usually with depth electrodes, made possible the successful selective procedures reported from Zurich5,6; alternatively, neuroimaging showing localized lesions limited to medial structures similarly sufficed. Conversely, neurophysiologic or radiographic data indicating a pathologic process confined to neocortical tissue justified a surgical procedure that spared the amygdala and hippocampus. These strategies are widely implemented today with the use of advanced magnetic resonance imaging (MRI) data or invasive monitoring, or both. Surgical planning and decision making in these instances generally occur outside the operating room, before the actual resective procedure.
Intraoperative “tailoring” of the resection procedure with the assistance of ECoG and functional mapping data obtained at the time of surgery is widely performed today. Intraoperative recordings, with rare exception, necessarily rely on interictal epileptiform discharges, or spikes, rather than ictal onset, which can be diagnosed only with extraoperative studies. The relationship of such interictal spikes to the epileptogenic zone or the area whose resection will result in a seizure-free outcome is not as clear as that for ictal-onset data. Animal models using either penicillin or alumina foci have demonstrated tight correlations between spikes and the epileptogenic zone.7,8 However, human clinical investigations have shown varying degrees of correlation. Using preresection and postresection intraoperative ECoG in a series of 29 patients undergoing standard temporal resection for mesial temporal sclerosis, Schwartz and colleagues investigated the predictive value of corticography for seizure outcome and found no correlation.9 Sugano and associates, in contrast, reported an analysis of 35 temporal lobe epilepsy patients who had undergone either lesionectomy or resection of a lesion plus tissue with residual spike activity (most often the hippocampus) and noted 3-year seizure-free rates of 76.9% and 90.9%, respectively.10 This relationship plus the enhanced ability of ECoG recording to accurately define an epileptogenic zone whose resection will lead to cessation of seizures is one of the two major rationales for tailoring resections.
The other rationale for individualization of temporal lobe seizure surgery relates to the known variability in the spatial representation of normal temporal lobe functions, particularly those related to language. Conventional teaching for untailored temporal lobe resection surgery advocates removing no more than the most anterior 4.5 cm of the middle temporal gyrus in the language-dominant hemisphere and preferably sparing the superior temporal gyrus entirely. With extensive experience in mapping language during epilepsy resections, however, Ojemann and coworkers have clearly documented the high variability of cortical language representation, with some critical language sites observed within anterior temporal lobe regions that would be removed during a standardized resection procedure.11–13 On this basis, cortical mapping has been strongly advocated.14 Those who argue against this position would note that others have reported the absence of new language deficits after standard resection.15
Extratemporal Neocortical Resection
Frontal lobe epilepsy resection requires preservation of primary motor cortex and, on the language-dominant side, speech cortex. Although variability in the primary motor areas has been noted, it is considerably less variable than the critical language sites. Under image guidance, planned surgical approaches well anterior to the precentral gyrus may be performed in accordance with the structural anatomy; incorporation of tractography or functional MRI (fMRI) data provides only further reassurance. Resections that are planned closer to eloquent brain regions, however, are facilitated by intraoperative mapping and monitoring. Language preservation with frontal resection requires sparing of Broca’s area in the posterior inferior frontal gyrus, but recent intraoperative studies have documented more extensive and variable frontal lobe language representation as well.16,17
Parietal resections must preserve primary sensory cortex and, on the language-dominant side, perisylvian language areas. Optic radiations, generally deep to the epileptogenic cortex, are at risk with larger resections but are not generally mapped intraoperatively. When operating within the occipital lobe, the primary visual cortex must be preserved. Although the accumulated surgical experience in posterior brain regions is much more limited than that in the temporal and frontal lobes, surgical interventions in these posterior regions are being carried out with increasing frequency and encouraging results.18–23
Multilobar Resection
Multilobar resection for the treatment of medically intractable epilepsy has understandably been used far less frequently than well-recognized interventions such as anterior temporal lobe resection or single-lobe cortical resection. The extent of surgery, its potential morbidity, associated functional consequences, and not least, the lower seizure control efficacy rate underlie the smaller surgical numbers, and the published experience with multilobar surgery is limited. Engel’s 1991 survey described comparative seizure control outcomes, with multilobar resection achieving seizure-free outcomes in 45.2% of patients and improvement in an additional 35.5%; anterior temporal lobe resection and lesionectomy, in contrast, achieved seizure-free outcomes in 67.9% and 66.6% of patients, respectively.4 Patients undergoing these different procedures, however, are distinctly different patient populations, and it would be a misinterpretation of that previous experience to deny multilobar epilepsy patients consideration of possible surgical intervention. Since the time of Engel’s survey, developments in both evaluation—neuroimaging as well as intracranial investigation—and surgical technique have improved the risk-benefit ratio for these patients.24–27
Methodology and Technique
Preoperative Evaluation
Surgical evaluation of an epilepsy patient today requires the multidisciplinary team approach of a dedicated epilepsy service. In addition to a general and epilepsy-focused history and physical examination, routine evaluation will include scalp electroencephalography (EEG) and epilepsy-protocol MRI; in those in whom surgery appears to be a reasonable preliminary consideration, further neuroimaging with positron emission tomography or single-photon emission computed tomography (SPECT), or both, inpatient video-EEG monitoring, ictal SPECT, and neuropsychological testing generally follows. Not all patients require all of these studies. In patients with MRI-negative epilepsy, subtraction SPECT (ictal minus the coregistered baseline) has often proved invaluable in directing subsequent intracranial investigative studies.28,29 Review and consideration of all this information by a multidisciplinary epilepsy team in a regular working conference subsequently ensue. At this point, patients without surgically treatable epilepsy, those who require additional medical management, and those with straightforward conditions such as medial temporal lobe epilepsy or structural lesions confined to a single lobe will have been identified. More challenging patients, such as those with discordant data, apparent multifocal or bilateral disease, MRI-negative epilepsy, or a more extensive pathophysiologic substrate, require further evaluation.
Intraoperative Mapping and Electrocorticography
When used, intraoperative ECoG may be performed with either awake or general anesthesia; in either instance, attention to anesthetic considerations is critically important. Wide exposure of the suspected cortical region is essential. After visual inspection of the cortical surface, electrodes of a variety of types may be used. A combination of grids and strips can be used to obtain the desired number of contacts, regularity of spacing, and access to less exposed surfaces such as the inferior temporal or orbitofrontal cortex. Large 4 × 8 or 8 × 8 subdural grids with 1-cm spacing of contacts may be placed easily over the convexity (Fig. 64-1); smaller subdural grids and strips (most typically 1 × 8) may supplement the larger grids. In lesional cases, image guidance may be helpful in directing manual placement of these electrode arrays. Intraoperatively placed depth electrodes may be used, particularly electrodes placed into the medial temporal lobe structures, but this has become less common. Once placed, ample recording is performed, and in collaboration with electrocorticographers in the operating room, the epileptogenic zone that would ideally be resected is defined. After the initial recording, mapping (see the next paragraph), and subsequent resection, further ECoG is often performed, although the significance of postresection spikes and the appropriate surgical response are debated. Advocates of this technique cite reports of better outcomes associated with absence of residual epileptiform activity,30–32 although resection in pursuit of residual spike activity is controversial and not universally advised.9
Intraoperative mapping, most commonly for language, motor, or sensory function (or any combination of these functions), typically follows the initial ECoG. For the primary sensorimotor cortex, mapping has a long and successful history. Integration of preoperative MRI or ideally fMRI data through the use of image guidance methods greatly facilitates this activity. Placement of a subdural strip perpendicular to the presumed central sulcus is a method that can be used to obtain somatosensory evoked potentials and assist in localization of the precentral and postcentral gyri. Direct motor mapping may be performed with either a handheld stimulator or a 1 × 4 subdural strip, with appropriate electromyographic recording increasing the sensitivity. Once the motor cortex has been identified, an extremely useful practice involves placing a subdural strip electrode over that area, delivering repeated electrical stimuli, and monitoring motor evoked responses to examine the integrity of the corticospinal tract during the resection.33–35
Language mapping requires an awake craniotomy, and with an experienced team, this approach can be used routinely in an efficient and safe manner. Numerous descriptions of awake craniotomy techniques have been published.13,16 A handheld bipolar stimulator consisting of 1-mm electrodes with a separation of 5 mm is used to apply a 5-second, 60-Hz, biphasic square-wave constant-current or constant-voltage stimulus at sequential sites across the exposed cortex of interest, beginning with low-stimulation parameters and gradually increasing the stimulation intensity until either language is disrupted or the maximal subthreshold for afterdischarges is reached (Fig. 64-2