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INTRODUCTION
Stereoelectroencephalography (SEEG) derives its name from the combination of “stereo-” and “electroencephalography (EEG)”, which reflects its basis in the concept of three-dimensional (3D) stereographic EEG monitoring. Historically, pioneering neurosurgeon J. Talairach introduced SEEG for long-term invasive epilepsy monitoring [35]. Building on his prior experience with stereotactic techniques originally used for anatomical localization of intracranial structures via pneumocephalogram, he developed a method for 3D analysis of intracranial EEG recordings in collaboration with epileptologist J. Bancaud. Through rigorous monitoring with the SEEG approach, this interdisciplinary epilepsy team conceptualized a distinction between the epileptogenic zone and the irritative zone. This insight represented a marked divergence from the traditional approach, which guided resective surgery based on interictal discharges, now recognized to be related to the irritative zone [2].
Currently, SEEG is increasingly being recognized as an important modality for investigating epilepsy. This is attributed to its historical concept of characterizing the epileptogenic focus through the 3D analysis of seizure patterns, thereby providing valuable insights into the epileptogenic network [1]. With recent advancements in the conceptualization of epileptic syndromes as network disorders, there is a growing demand for comprehensive intracranial EEG investigations with high spatial resolution. Consequently, SEEG techniques have garnered significant interest, particularly due to their less invasive features when compared to traditional invasive techniques [27]. Nevertheless, the neurosurgical implementation of SEEG can be labor-intensive, involving time-consuming stereotactic planning and a substantial surgical workload [40]. Cases indicated for invasive studies typically require the exploration of multiple deep brain structures to investigate possible hypotheses regarding the localization of the epileptogenic focus, often necessitating the placement of up to 15 electrodes per case [22].
In the context of neurosurgical techniques, conventional frame-based stereotaxy has been widely validated for a variety of procedures, including deep brain stimulation (DBS) surgery, shunt operation, brain biopsies, aspiration of brain abscesses or hematomas, as well as depth electrode placement. However, there appears to be insufficient literature discussing the detailed operative procedures and technical nuances of SEEG, making it challenging for practitioners aiming to implement this important modality into their practice.
Our epilepsy team has embraced the SEEG approach for invasive EEG monitoring, using conventional frame-based stereotaxy instruments. In this paper, we describe our initial experiences with SEEG in the presurgical evaluation of epilepsy surgery over the past couple of years, with a particular focus on the neurosurgical and technical aspects beyond electrophysiological implications. We share our perspectives and practical insights on employing the SEEG approach with a frame-based system and discuss both advantages and potential concerns associated with SEEG investigation.
MATERIALS AND METHODS
Study approval
This research was approved by the Institutional Review Board of Asan Medical Center (project number 2024-0008). All methods were conducted in accordance with relevant guidelines and regulations.
Study population and data collection
This retrospective observational study encompassed patients with drug-resistant epilepsy who underwent invasive studies using SEEG techniques at a single tertiary-level center between 2022 and 2023. The clinical information of the study population was extracted from the institutional clinical data warehouse and electronic medical record system. We reviewed neuroimaging and neurosurgical planning data as well as intracranial EEG monitoring data. The seizure and epilepsy types were classified according to the 2017 International League Against Epilepsy (ILAE) classification [16].
Presurgical evaluation and SEEG planning
Each case with intractable epilepsy considered for surgical interventions was reviewed by a multidisciplinary epilepsy team, consisting of neurosurgeons, neuroradiologists, and adult and pediatric epileptology specialists. The non-invasive presurgical evaluation included continuous video-EEG monitoring, structural magnetic resonance imaging (MRI), ictal/interictal single-photon emission computerized tomography (SPECT), and positron emission tomography (PET). In cases where clinical EEG assessments were inconclusive or discordant with structural, physiological, and metabolic imaging findings, patients were recommended for a second-phase invasive evaluation. For those who opted for SEEG, functional MRI and the intracarotid sodium amobarbital procedure were conducted to confirm hemispheric dominance.
The SEEG planning primarily aimed to identify the margins of the epileptogenic zone and to assess resectability [22]. Stereotactic trajectories and target delineation were determined using high-resolution 3D T1-weighted images and dedicated neuroimaging software (Curry Neuroimaging Suite; Compumedics Neuroscan Ltd., Victoria, Australia and Brainlab Elements; Brainlab AG, Munich, Germany). Before planning the trajectories for electrode placement, neurosurgeons manually segmented major hypothetical epileptogenic or eloquent regions, such as the cingulate gyrus, short and long gyri of the insula, pre- and post-central gyri, and any areas with structural abnormalities suspected to be epileptogenic.
Operative procedures for stereotactic SEEG insertion
Surgical procedures utilized a coordinate frame and stereotactic arc system (Leksell Stereotactic System; Elekta AB, Stockholm, Sweden). Patients underwent post-contrast, high-resolution 3D MRI and CT scans after the frame was in place. The prepared electrode trajectories were then integrated into the stereotactic planning software (SurgiPlan; Elekta AB) to obtain the frame coordinates and arc parameters. The depth of skull for each trajectory was measured for subsequent use in skull anchoring. Each trajectory and entry point were thoroughly reviewed to ensure avoidance of intracranial vasculature along each path, with further refinements and adjustments being made before finalization.
For SEEG, we mounted the stereotactic arc in a sagittal configuration (Fig. 1). This approach allowed access to both sides of the brain under a single surgical draping, thereby eliminating the need for patient repositioning or frame reapplication throughout the entire procedure (Fig. 2A). Patients were positioned neutrally in a semi-sitting position without neck rotation under general anesthesia. After setting the frame arc, we made a half-centimeter scalp incision, followed by a twist drill at the entry point on the skull (Fig. 2B). Using a monopolar cautery through the drilled access, the dura was punctured while ensuring the brain parenchyma remained unviolated (Fig. 2C).
Originally, for conventional invasive studies involving depth electrodes, we used Spencer probe depth electrodes, characterized by a 1.1 mm diameter and 8-channel contacts, each sized at 2.4 mm with 5 mm spacing. For SEEG, however, we employed electrodes specifically designed for this purpose, featuring a reduced diameter for less invasive placement. We used electrodes with varying channel configurations, a 0.8 mm diameter, and a 2 mm contact length with 3.5 mm spacing (sEEG Depthalon Epilepsy Electrodes; PMT Co., Chanhassen, MN, USA). In this system, we first secured a skull anchor and then advanced a stylet-guided electrode through it to the desired length (Fig. 2D). Once the stylet was removed and the skull anchor cap was fastened, the procedure for each electrode concluded.
Unlike DBS surgery and other stereotactic procedures, the SEEG approach prioritizes covering regions around the electrode contacts within the trajectory, rather than precise electrode tip positioning. Therefore, we did not routinely employ fluoroscopic or cone-beam CT (e.g., O-arm) guidance for each electrode placement. The final positions of the electrodes were confirmed through postoperative standard CT scans.
Long-term SEEG monitoring and clinical assessment
Patients were admitted to the epilepsy monitoring unit (EMU) for continuous video-intracranial EEG monitoring. Postoperative high-resolution CT scans were performed to aid in anatomical mapping of the SEEG electrodes. Any unusual postoperative findings and complications that can lead to temporary or permanent neurological deficits were meticulously monitored. Safety data, including complications related to the procedure or the devices necessitating surgical interventions, were thoroughly investigated.
Patients were typically monitored for a minimum of 5 days and up to 2 weeks in EMU. Patients gradually discontinued or reduced the dosage of their antiseizure medications (ASMs) as necessary. Once recording a sufficient number of habitual seizures, patients underwent functional mapping with electrical stimulation. After completing long-term monitoring in the EMU, the electrodes were easily removed at the beside. Patients were eligible for discharge in the absence of postoperative complications. The results of clinical EEG assessments were reviewed and discussed by the interdisciplinary epilepsy team, which determined the optimal therapeutic options for each patient.
RESULTS
Baseline characteristics
This series comprises 16 patients, with a median age of 35 years (interquartile range [IQR], 29–47) (Table 1). Among these, two were pediatric patients, with the youngest being 15 years old. The median age of seizure onset was 21 years (IQR, 14–27), with a median disease duration of 14 years (IQR, 10–20). Most of the patients in this series had drug-resistant focal epilepsy, with one exception diagnosed with Lennox-Gastaut syndrome.
Electrode misplacement and hemorrhagic complications
A total of 201 SEEG electrodes were inserted across the 16 patients. Except for three patients, both hemispheres were investigated in all the remaining cases. The median time required to finalize SEEG trajectories was 89 minutes (IQR, 71–108). The median skin-to-skin operation time per case was 162 minutes (IQR, 145–200), which corresponds to 13 minutes (IQR, 12–15) for each SEEG electrode placement.
In this series, we encountered misplacement in two electrodes (1.0%). In one instance, an electrode was positioned in the subdural space, failing to penetrate the brain parenchyma. We chose not to revise this electrode, instead opting for its use in epicortical recording. In another case, we revised the electrode placement due to insufficient depth, which failed to reach the intended orbitofrontal region. This revision was carried out at the bedside under local anesthesia with aseptic preparation. A new stylet-guided electrode was simply reinserted into the preexisting skull anchor immediately after the removal of the corresponding electrode. This patient experienced minimal discomfort during the procedure.
We encountered one case (case #16) of procedure-related complications, which presented delayed intraparenchymal hemorrhage following venous infarction that occurred a week after the SEEG procedure (Fig. 3). This patient temporarily experienced dysphasia, which resolved over time.
Seizure localization and clinical outcomes following surgical interventions
A median of 13 seizure events (IQR, 8–24) were recorded during the SEEG monitoring, which lasted a median of 11 days (IQR, 8–12) (Table 2). Intracranial coverage encompassed the mesial temporal region in 94% of cases (bilateral in 81%) and the operculo-insular region in all cases (bilateral in 56%). The localized ictal onset zones mostly comprised temporal neocortex or mesial temporal regions, except four cases involving the cingulate or operculo-insular regions. The primary ictal onset zone was unilaterally localized in 10 patients, while the remaining six patients demonstrated multifocal or bilateral ictal onset.
Based on the SEEG investigation, 10 patients underwent resective surgery, while one underwent bilateral DBS of the anterior nucleus of the thalamus (ANT-DBS) surgery. During a median follow-up duration of 10 months (IQR, 4–14) for the 11 surgically treated patients, nine cases achieved favorable seizure outcomes, with eight of them attaining seizure remission at the last visit. One noteworthy clinical advantage of SEEG was its ability to delineate the ictal onset and early propagation zones, which provided crucial guidance for resective surgery and ultimately contributed to successful seizure remissions (Fig. 4).
DISCUSSION
In this study, we presented our institutional experience with SEEG using the conventional frame-based stereotactic techniques. There have been several studies discussing the technical aspects of SEEG procedures, including frame-based, image-guided, and robot-assisted approaches (Table 3). While frameless, image-guided neuronavigation has been utilized for similar purposes to frame-based stereotaxy, its accuracy and precision were not reported to be as high as those of frame-based techniques, particularly in SEEG procedures [17,37]. In contrast, recent advancements in robot-assisted SEEG techniques have been well-documented, with numerous studies accentuating their superiority over traditional methods [8,15,19]. Unlike these robot-assisted techniques, frame-based stereotaxy has faced limitations related to the number of SEEG electrode placements possible within the confines of prolonged operation time [19]. A previous study also noted that bilateral procedures required more time than unilateral cases [43]. Nevertheless, the use of sagittal arc applications can offer bilateral electrode insertion under a single surgical drape, thereby facilitating the planning of multiple electrodes in each case.
One of the inherent technical challenges associated with frame-based SEEG techniques is the presence of anatomical limitations that may restrict certain areas as the entry or target points, particularly in the occipital region. This issue becomes more pronounced in the majority of patients who require monitoring of the mesial temporal and temporopolar regions which lie in close proximity to the anterior end of the head. Given the standard frame’s working length along the y-axis is typically 12 cm, it may be insufficient to encompass the occipital pole in some cases. Consequently, the meticulous selection of patient positioning and the strategic approach during the SEEG planning become important. For example, in cases with suspected bilateral epileptic foci, the employment of the sagittal arc technique could greatly enhance efficiency by facilitating bilateral electrode insertion. Conversely, for patients with suspected unilateral extratemporal frontal or parieto-occipital foci, an axial arc orientation may offer a more suitable choice. This highlights the critical need for individualized planning tailored to the unique anatomical and clinical requirements of each patient. Moreover, understanding these nuances and adapting the procedural strategy accordingly can enhance the benefits of SEEG investigation.
Compared to traditional invasive study techniques, one significant advantage of minimal invasive SEEG electrodes lies in their simplified skull anchoring system. However, it is important to note that this simplicity might compromise the safety of electrode placement, as it does not allow for direct verification of brain penetration during blind insertion though the anchor. This could potentially affect minor superficial vessels that were not visualized in the preoperative MRI [10]. While numerous studies have underscored the safety of this technique [33,42], there are also reports documenting serious hemorrhagic complications leading to permanent neurological deficits [32]. Furthermore, such complications have manifested even in the cases without direct arterial injury [25], as illustrated in our case with delayed intraparenchymal hemorrhage. Given these associated risks, we advise that SEEG be reserved for selected patients who are strong candidates for epilepsy surgery and genuinely contemplating such interventions.
A major concern with this minimally invasive SEEG technique might be a potential risk for electrode misplacement from the originally intended trajectory. While other stereotactic procedures employ the frame arch system to reach the target point, the SEEG procedure is guided only up to the entry point for skull anchoring. The subsequent electrode trajectory to the target point is determined by the orientation of the skull anchor. Notably, we observed that electrodes anchored at oblique angles to the skull tended to be positioned less accurately, particularly when covering the orbitofrontal or temporopolar regions. These trajectories which were often chosen for cosmetic reasons to keep the entry points posterior to the hairline. Similar findings have been observed in existing literature, where the oblique skull angle was positively correlated with the entry and target point errors [8,43]. Another challenge is the excessive cerebrospinal fluid drainage during the procedure, which can considerably alter the entry point and trajectory due to brain shift. Consequently, we prefer to target the deeply located small structures earlier in the procedure than other trajectories. Nevertheless, operators should always be vigilant regarding the potential misplacement of each electrode. Intraoperative verification of electrode positioning through intraoperative imaging techniques could be helpful in certain cases.
In our experience, intracranial EEG recordings from SEEG have provided invaluable insights in identifying surgically remediable epilepsy cases, even in complex cases of developmental and epileptic encephalopathy. Through a comprehensive investigation covering all potential hypothetical epileptogenic foci, we precisely localized the surgical targets responsible for seizures, leading to a successful resection. This strategy could be more challenging with other invasive techniques that rely on epicortical recordings. A significant hurdle is the considerable burden placed on operators due to the need for repetitive electrode implantations at individual frame coordinates. Recent studies have indicated that robot-assisted SEEG is not only efficient but also highly accurate, suggesting its potential to become the standard procedure in the foreseeable future [18,42]. Meanwhile, from our perspective, the conventional frame-based techniques for bilateral and multiple SEEG electrode placement remain practical and advantageous options for certain patients.
Limitations and future directions
Thus far, our experience with SEEG has not yet included emerging therapeutic applications such as SEEG-guided radiofrequency thermocoagulation or MR-guided laser ablation [30]. These minimally invasive approaches hold potential as alternative treatment options for managing patients with refractory epilepsy. Future investigations to validate their feasibility, in comparison to established neurosurgical modalities, might expert influence on regulatory authorities across various countries to approve these applications for the management of epilepsy patients.
CONCLUSION
Conventional frame-based stereotactic techniques continue to be a reliable and effective option for the placement of bilateral and multiple SEEG electrodes. While SEEG is a suitable approach for selected patients who are strong candidates for epilepsy surgery, it is important to remain vigilant regarding potential risks of electrode misplacement and hemorrhagic complications.
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