Convergence of Stereotactic Surgery and Epilepsy

Because successful resective epilepsy surgery relies on accurate preoperative localization of the epileptogenic zone (EZ), presurgical evaluation is necessary to obtain the widest and most accurate spectrum of information from clinical, anatomic, and neurophysiological aspects, with the ultimate goal of performing an individualized resection for each patient.1-3 Noninvasive studies are successful in identifying and anatomically delineating the EZ in approximately 70% of the patients who are operated on at the Cleveland Clinic Epilepsy Center (unpublished data). Consequently, a formulation of a clear anatomo-electro-clinical (AEC) hypothesis may not be possible in the remaining 30% of patients, or an AEC hypothesis is partially generated but the exact location of the epileptogenic area within a specific neuronal network, its extent, or its overlap with functional (eloquent) cortex remains unclear. In these clinical scenarios, when the noninvasive data are insufficient to define the EZ, extraoperative invasive monitoring may be indicated. The stereoelectroencephalography (SEEG) is one of the extraoperative invasive methods that can be applied in patients with medically refractory focal epilepsy to anatomically define the EZ and the possible related functional cortical areas. SEEG: HISTORICAL PERSPECTIVE AND PRINCIPLES Human cerebral stereotaxis was conceptualized and initiated in 1947 by Spiegel and Wycis,4 and its use in recording from deep brain structures has been reported since 1950. Since then, stereotactic placement of intracerebral electrodes has gained progressive popularity and was reported for the first time in the evaluation of temporal lobe epilepsy in the early 1960s by Crandall and colleagues.5,6 Meanwhile, in the neurosurgical unit of the Saint Anne Hospital in Paris, stereotactic investigations of epileptic patients with intracerebral electrodes were inspired by a new, innovative concept: Epileptic seizures were regarded as a dynamic process, with a spatial-temporal, often multidirectional organization best defined as a 3-dimensional arrangement. This method was originally called SEEG.7,8 The SEEG method was originally developed by Jean Talairach and Jean Bancaud during the 1950s and has been used mostly in France and Italy as the method of choice for invasive mapping in refractory focal epilepsy.9-19 In France, after the development of the stereotactic techniques and frames, which were applied initially for abnormal movement disorder surgery, Jean Talairach focused most of his attention to the field of epilepsy, along with Jean Bancaud, who joined him in 1952. The new methodology created by both physicians led them to depart very quickly from an approach limited to the mapping of the superficial cortical areas, as did Wilder Penfield and colleagues at Montreal Neurological Institute. Posteriorly, the development of specific surgical tools, adapted to a new stereotactic frame designed by Talairach and colleagues, directed the Saint Anne investigators to propose the functional exploration of the brain by depth electrodes, allowing the study of both superficial and deep cortical areas. The debut of SEEG was on May 3, 1957, with the first implantation of intracerebral electrodes for epilepsy in Saint Anne Hospital. By departing from the current methods of invasive monitoring, such implantations have allowed the exploration of the activity of different brain structures and recording of the patient’s spontaneous seizures, something that Penfield’s method of investigation failed to achieve. The principle of SEEG methodology remains similar to the principles originally described by Bancaud and Talairach, which are based on AEC correlations with the main aim of conceptualizing the 3-dimensional spatial-temporal organization of the epileptic discharge within the brain.9,10,14-18,20-26 The implantation strategy is individualized, with electrode placement based on a preimplantation hypothesis that takes into consideration the primary organization of the epileptiform activity and the hypothetical functional epileptic network that may be involved in the propagation of seizures. For these reasons, the preimplantation AEC hypothesis is the single most important element in the process of planning the placement of SEEG electrodes. If the preimplantation hypothesis is incorrect, the placement of the depth electrodes will be inadequate, and the interpretation of the SEEG recordings likely will be misleading. SELECTING THE APPROPRIATE METHOD FOR INVASIVE MONITORING There is no clear consensus on the best selection criteria for each method. Some epilepsy centers have applied both technical procedures in a systematic matter, but none of them have conducted definitive comparative studies. The “pro-SEEG groups” consider that this method can answer any question an invasive method can provide. On the contrary, the “prosubdural groups” who are not familiar with depth electrode explorations tend to limit its indications strictly to the exploration of deep structures, for example, to distinguish unilateral or bilateral lobe epilepsy, and possibly to study epilepsy related to nodular heterotopia. However, differences between SEEG and subdural grids and strips are more extensive and complex than just the dichotomy between deep and superficial mapping.27 The philosophy, definitions, and concepts of the 2 types of explorations are quite different and at times divergent. Subdural explorations were initially oriented toward the invasive study of lesional epilepsy, whereas SEEG takes little into account the lesion itself.15,18,23,26-44 We may speculate that SEEG is more suitable to explore patients with nonlesional magnetic resonance images (MRIs) for whom, in some cases, it is not at all clear that surgery should be performed.27 In addition, SEEG allows exploration of remote and multilobar areas without the need for craniotomies and the need for immediate surgery, allowing a prolonged reflection time for the patient and consequently a more complete informed consent process. Conversely, extraoperative mapping with the subdural method (including grids, strips, and the possible combination with depth electrodes) has the advantage of allowing an optimal anatomic and contiguous coverage and sampling of the adjacent cortex, leading to accurate superficial functional mapping exploration.45 This is especially the case when there is a need to determine the extension of the EZ associated with a superficial lesion and its anatomic relation to a close functional area. This is not quite true if the lesion includes a deep-seated component in which functional mapping cannot be obtained from subdural mapping. From a surgical perspective, subdural implantations are open procedures, with better management of occasional intracranial hemorrhagic complications. The main disadvantages of the subdural method are related to the inability to record and map deep structures such as the insula cortex, posterior orbitofrontal cortex, cingulate gyrus, and depths of sulci and consequently its inability to analyze the 3-dimensional aspects of the epileptic network.43 In these scenarios, the SEEG methodology may be considered a more adequate and safer option. SEEG has the advantages of allowing extensive and precise deep brain recordings and stimulations with minimal associated morbidity. Consequently, on the basis of the potential advantages and disadvantages from each method, one can consider possible specific indications to choose SEEG over other methods of invasive monitoring: The possibility of a deep-seated or difficult-to-cover location of the EZ in areas such as the mesial structures of the temporal lobe, opercular areas, cingulate gyrus, interhemispheric regions, posterior orbitofrontal areas, insula, and depths of sulci. A failure of a previous subdural invasive study to clearly outline the exact location of the seizure-onset zone. The failure to identify the EZ in these patients may be due to multiple reasons, including the lack of adequate sampling from a deep focus or a clinically silent focus upstream from the EZ. The need for extensive bihemispheric explorations (in particular, in focal epilepsies arising from the interhemispheric or deep insular regions). Presurgical evaluation suggestive of a functional network involvement (eg, limbic system) in the setting of a normal MRI. It is important to emphasize that the possible specific indications for SEEG highlighted above are a work in progress and that clinical validation with long-term seizure outcome is necessary. PLANNING THE SEEG IMPLANTATION As indicated above, the development of an SEEG implantation plan requires the clear formulation of a specific AEC hypothesis to be tested. This hypothesis is typically generated during the multidisciplinary patient management conference based on the results of various noninvasive tests. At our center, a final tailored implantation strategy is generated during a separate presurgical implantation meeting. Depth electrodes should sample the anatomic lesion (if identified), the more likely structure(s) of ictal onset, the clinically active regions, and the possible electric pathway(s) of seizure-onset propagation (functional networks). The EZ may correspond to the first clinical sign or may reflect a spread area from a “clinically silent” ictal onset zone within a functional network. For these reasons, a 3-dimensional conceptualization of the network nodes upstream and downstream from the hypothesized epileptic network is an essential component of the presurgical implantation strategy. Initially, through analysis of the available noninvasive data and the temporal evolution of the epileptic clinical manifestations, a hypothesis of the anatomic location of the EZ is formulated. The implantation plan is created in collaboration with experienced epileptologists, neurosurgeons, and neuroradiologists who together formulate an adequate hypothesis of the location of the EZ. Adequate knowledge of the possible functional networks involved in the primary organization of the epileptic activity is mandatory to formulate an adequate hypothesis. In addition, the treating physicians will have to take into account the 3-dimensional aspects of depth electrode recordings, which, despite a limited coverage of the cortical surface compared with subdural grids and strips, enable an accurate sampling of the structures along the trajectory from the entry site to the final impact point. Thus, the trajectory, not just the target or entry point areas, is important. Consequently, the investigation may include lateral and mesial surfaces of the different lobes, deep-seated cortices such as the depths of sulci, insula, posterior, areas in the interhemispheric cortical surface, etc. The implantation should also consider the different cortical cytoarchitectonic areas involved in the seizure organization patterns and their likely connectivity to other cortical and subcortical areas. It is important to emphasize that the implantation strategy focus is to map not lobes or lobules but epileptic networks, which, in general, involve multiple lobes. Furthermore, exploration strategy should also take into consideration a possible alternative hypothesis of localization (the secondary hypothesis).23,27,46 TECHNIQUE OF IMPLANTATION Once the SEEG planning is finalized, the desired targets are reached with the use of commercially available depth electrodes in various lengths and numbers of contacts, depending on the specific brain regions to be explored. The depth electrodes are implanted with the use of conventional stereotactic technique or with the assistance of stereotactic robotic devices through 2.5-mm-diameter drill holes. In both techniques, depth electrodes are inserted through 2.5-mm-diameter drill holes with orthogonal or oblique orientation, allowing intracranial recording from lateral, intermediate, or deep cortical and subcortical structures in a 3-dimensional arrangement, thus accounting for the dynamic, multidirectional, spatiotemporal organization of the epileptic pathways. Initially, frame-based implantations were performed in our center. More recently, however, robotic-assisted devices have been applied. Similar to the conventional approach, volumetric preoperative MRIs are obtained, and DICOM (Digital Imaging and Communications in Medicine) format images are digitally transferred to the native planning software of the robot. Individual trajectories are planned within the 3-dimensional imaging reconstruction according to predetermined target locations and intended trajectories. Briefly, on the day of surgery, patients are placed under general anesthesia. The patient’s head is placed in a 3-point fixed head holder. The robot is then positioned so that the working distance (distance between the base of the robotic arm and the midpoint of the cranium) is approximately 70 cm. The robot is locked into position, and the head holder device is secured to the robot. No additional position adjustments are made to the operating table during the implantation procedure. After the patient is positioned and secured to the robot, image registrations are performed. Semiautomatic laser-based facial recognition is used to register the preoperative volumetric MRI with the patient. The laser is first calibrated with a set-distance calibration tool. Preset anatomic facial landmarks are then manually selected with the laser. The areas defined by the manually entered anatomic landmarks subsequently undergo automatic registration using laser-based facial surface scanning. Accuracy of the registration process is then confirmed by correlating additional independently chosen surface landmarks with the registered MRI. After successful registration, the accessibility of the planned trajectories is automatically verified by the robot software. The patient is then prepped and draped in a standard sterile fashion. The robotic working arm is also draped with a sterile plastic cover. A drilling platform with a 2.5-mm-diameter working cannula is secured to the robotic arm. The desired trajectories are selected on the touch screen interface. After trajectory confirmation, the arm movement is initiated through the use of a foot pedal. The robotic arm automatically locks the drilling platform into a stable position once it reaches the calculated position for the selected trajectory. A 2-mm-diameter handheld drill (Stryker) is introduced through the platform and used to create a pinhole. The dura is then opened with an insulated dural perforator using monopolar cautery at low settings. A guiding bolt (Ad-Tech, Racine, Wisconsin) is screwed firmly into each pinhole. The distance from drilling platform to the retaining bolt is measured, and this value is subtracted from the standardized 150-mm platform to target distance. The resulting difference is recorded for later use as the final length of the electrode to be implanted. This process is repeated for each trajectory. All pinholes and retaining bolts are placed before electrode insertion is started. A small stylet (2 mm in diameter) is then set to the previously recorded electrode distance and passed gently into the parenchyma, guided by the implantation bolt, followed immediately by the insertion of the premeasured electrode (Figure).47FIGURE: Robotic stereoelectroencephalography (SEEG) technique. A, operating room setup during left-sided SEEG robotic implantation, with the surgeon and scrub nurse positioned on each side of the patient and the robot device placed in the middle at the vertex. B, intraoperative aspect of left-sided frontal-temporal SEEG implantation with the guiding bolts in their final positions. C, left-sided frontal-temporal SEEG implantation after implantation of the depth electrodes. Final aspect.MORBIDITY AND SEIZURE OUTCOME Our center recently reported 200 patients undergoing 2663 SEEG electrode implantations for the purposes of invasive intracranial EEG monitoring in accordance with a tailored preimplantation hypothesis to investigate and anatomically characterize the extension of the EZ. The studied group was challenging because of the paucity of noninvasive data and the possibility of a more diffuse pathology suggested by a previous failure of an invasive monitoring exploration: Nearly one-third of the studied patients (58 patients, 29.0%) had undergone prior surgical intervention for medically refractory epilepsy resulting in postoperative recurrent seizures. Despite the challenging and discouraging clinical scenario, the SEEG method was able to confirm the EZ in 154 patients (77.0%). Of these, 134 patients (87.0%) underwent subsequent craniotomy for SEEG-guided resection. Within this cohort, 90 patients had a minimum postoperative follow-up of at least 12 months; of these 90 patients, 61 (67.8%) remained seizure free (ie, Engel I outcome). The most common pathological diagnosis in this group was focal cortical dysplasia type I (55 patients, 61.1%). Complications were minimal. They included wound infections (0.08%), hemorrhagic complications (0.08%), and a transient neurological deficit (0.04%) in a total of 5 patients. The total morbidity rate was 2.5%.26 Results in terms of seizure outcome and complications are compatible with already published results from other groups. These results parallel those of previous studies in the recent literature. Munari et al48 reported their experience with SEEG in 70 patients undergoing a collective total of 712 electrode implantations. Within this cohort, an individualized and tailored surgical resection was performed in 60 patients (85.7%). In their series, specifically relating to SEEG, the authors identified 1 permanent complication resulting from the procedure: the formation of an asymptomatic intracerebral hematoma after the removal of an SEEG electrode (accounting for a morbidity rate of 1.4%, or 0.1% per electrode). More recently, Sindou et al49 presented a series of 100 patients collectively undergoing 1118 SEEG electrode implantations for invasive EEG monitoring. In that series, SEEG was deemed helpful in 84 patients (84%) by either annulling or confirming (and additionally, in the latter case, guiding) surgical resection of the EZ. Moreover, SEEG confirmed the indication for resection in 14 cases (14%) that were previously disputed on the basis of the noninvasive workup. These authors reported 5 complications (5% of cases), including 2 electrode site infections (0.2% per electrode), 2 intracranial electrode fractures (0.2% per electrode), and 1 intracerebral hematoma resulting in death (accounting for a mortality rate of 1% in the study). In a large series, Cossu et al50 reported a morbidity rate of 5.6%, with severe permanent deficits from intracerebral hemorrhage in 1%. In another study, Tanriverdi et al51 summarized their experience with a subgroup of 491 refractory epilepsy patients collectively undergoing 2490 intracerebral SEEG electrode implantations and 2943 depth electrode implantations. From their experience, those authors identified 4 patients (0.8%) with an intracranial hematoma at the electrode site (0.07% per electrode) and 9 patients (1.8%) with an infection arising from electrode placement (0.2% per electrode); moreover, they reported no mortalities ensuing directly from SEEG electrode placement. Finally, Cardinale et al52 most recently presented their experience with 6496 electrodes stereotactically implanted in 482 epilepsy patients with refractory epilepsy. These authors identified 2 patients (0.4%, or 0.03% per electrode) with permanent neurological deficits in their series, 14 patients (2.9%, or 0.2% per electrode) with hemorrhagic complication, 2 patients (0.4%, or 0.03% per electrode) with infection, and 1 mortality (0.2%) resulting from massive brain edema and concomitant hyponatremia after electrode implantation.53 In terms of morbidity, subdural grid electrode implantation has historically been to have low permanent morbidity compared with depth electrodes because there is no it is to morbidity between subdural grids and SEEG because of the in patient different and of implanted electrodes, the clinical experience different in and that the SEEG method at least a similar of compared with subdural grids or The SEEG technique was developed 60 in its and over the The main advantage of the SEEG method is the possibility of the epileptic neuronal network in its dynamic and with better time and correlations with the clinical The main clinical for the remains the of specific selection criteria for the different methods of invasive monitoring, with the ultimate goal of and the results obtained from different methods of invasive monitoring. The has no or in any of the or devices described in this

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