Clinical Applicability and Safety of Conventional Frame-Based Stereotactic Techniques for Stereoelectroencephalography

Article information

J Korean Neurosurg Soc. 2024;67(6):661-674
Publication date (electronic) : 2024 July 11
doi : https://doi.org/10.3340/jkns.2023.0246
1Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
2Division of Pediatric Neurology, Department of Pediatrics, Asan Medical Center Children’s Hospital, University of Ulsan College of Medicine, Seoul, Korea
3Department of Neurology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
Address for reprints : Seok Ho Hong Department of Neurological Surgery, Asan Medical Center, University of Ulsan College of Medicine, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Korea Tel : +82-2-3010-3558, Fax : +82-2-476-6738, E-mail : hongsound@gmail.com
Received 2023 December 18; Revised 2024 March 19; Accepted 2024 April 26.

Abstract

Objective

Stereoelectroencephalography (SEEG) is increasingly being recognized as an important invasive modality for presurgical evaluation of epilepsy. This study focuses on the clinical and technical considerations of SEEG investigations when using conventional frame-based stereotaxy, drawing on institutional experience and a comprehensive review of relevant literature.

Methods

This retrospective observational study encompassed the surgical implantation of 201 SEEG electrodes in 16 epilepsy patients using a frame-based stereotactic instrument at a single tertiary-level center. We provide detailed descriptions of the operative procedures and technical nuances for bilateral and multiple SEEG insertions, along with several illustrative cases. Additionally, we present a literature review on the technical aspects of the SEEG procedure, discussing its clinical implications and potential risks.

Results

Frame-based SEEG electrode placements were successfully performed through sagittal arc application, with the majority (81.2%) of cases being bilateral and involving up to 18 electrodes in a single operation. The median skin-to-skin operation time was 162 minutes (interquartile range [IQR], 145–200), with a median of 13 minutes (IQR, 12–15) per electrode placement for time efficiency. There were two occurrences (1.0%) of electrode misplacement and one instance (0.5%) of a postoperative complication, which manifested as a delayed intraparenchymal hemorrhage. Following SEEG investigation, 11 patients proceeded with surgical intervention, resulting in favorable seizure outcomes for nine (81.8%) and complete remission for eight cases (72.7%).

Conclusion

Conventional frame-based stereotactic techniques remain a reliable and effective option for bilateral and multiple SEEG electrode placements. While SEEG is a suitable approach for selected patients who are strong candidates for epilepsy surgery, it is important to remain vigilant concerning the potential risks of electrode misplacement and hemorrhagic complications.

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).

Fig. 1.

Sagittal application of the stereotactic arc and corresponding angle parameters in the Leksell stereotactic system. A : Lateral-right orientation of the stereotactic arc. B : Sagittal-posterior orientation of the stereotactic arc (for the target in the left hemisphere). For stereoelectroencephalography requiring multiple and bilateral electrode placements, anterior/posterior orientations of the stereotactic arc may be preferred to the common lateralleft orientation. In these configurations, the arc support is attached to the x-axis of the coordinate frame instead of the y-axis. Following the center-of-arc principle, the target coordinate remains unchanged, but the coordinate on the arc axis needs to be set to its appropriate index mark : lateral-left orientation and anterior orientation share the same index, while the index for posterior orientation is obtained by subtracting from 200 mm. For anterior/posterior orientations, the arc axis should be set as the y-axis, which entails an additional adjustment of 15 mm from the x-axis value used for lateral orientations. Additionally, the ‘arc’ and ‘ring’ angle parameters need to be exchanged to maintain the correct entry point, with posterior arch orientation being optimal for the left hemisphere and anterior orientation for the right hemisphere. To convert between anterior and posterior orientations, both the ‘arc’ and ‘ring’ angles are simply subtracted from 180°.

Fig. 2.

Operative techniques for multiple SEEG electrode placement using frame-based stereotactic system. A : Patient positioning and application of the stereotactic arc (Leksell®; Elekta AB, Stockholm, Sweden). This orientation of the stereotactic arc allows bilateral access under a single surgical drape, though it is worth noting that the arc apparatus may obscure some areas in the occipital region. B : Drilling into the skull using a twist drill. Pre-measured skull depth at the entry point ensures procedure safety. C : Dural puncture with a monopolar cautery. This step proceeds in a blind manner, and practitioners should be vigilant to avoid violations to the brain parenchyma and superficial vessels. D : Fixation of the anchor bolt (Depthalon®; PMT Co., Chanhassen, MN, USA). The depth for electrode advancement is determined by subtracting the measured length between the arc and the fixed anchor point from the working length (typically 190 mm in the demonstrated system).

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.

Patient demographics and clinical information

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.

Fig. 3.

Postoperative intracranial hemorrhage following SEEG. Pre- and postoperative MRIs and the SEEG planning are presented (case #16). A 49-year-old female with a history of encephalitis and status epilepticus was referred for surgical intervention due to drug-resistant focal epilepsy, despite being on five antiseizure medications. MRI scans revealed bilateral hippocampal sclerosis and sequalae of encephalitis (A). SEEG was conducted to explore both the bilateral mesial temporal and operculo-insular regions (B). Preoperative post-contrast MRIs showed that a trajectory for targeting the left hippocampus was designed to ensure safe entry into brain parenchyma without damaging adjacent vasculature (C, arrowheads). However, during the procedure the SEEG electrode deviated from the planned trajectory, likely due to brain shift, passing through the nearby sulci (D, arrowheads). Initially, the patient tolerated the procedure well and was sent to epilepsy monitoring unit for long-term SEEG monitoring. However, a week later, the patient developed global dysphasia, and a follow-up imaging scans revealed a delayed postoperative hemorrhage (E and F). SEEG : stereoelectroencephalography, MRI : magnetic resonance imaging.

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.

SEEG investigation and surgical outcomes

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).

Fig. 4.

Successful seizure control following SEEG-guided resective surgery. The figure illustrates pre- and postoperative MRIs, SEEG planning, and intraoperative gross inspections from a representative case (case #13). A 15-year-old male with a history of hypoxic-ischemic encephalopathy had bilateral frontal atrophy with encephalomalacia (A, arrowheads). His seizures, characterized by hyperkinetic movements occurring several times a day, remained intractable despite the use of four antiseizure medications, causing significant distress to his caregiver. SEEG monitoring was performed to assess the feasibility of resective surgery (B). During SEEG, seizures were observed to initiate at the left orbitofrontal (C, arrow) and anterior cingulate regions, corresponding to the structural lesion observed in the MRI. The patient underwent a left frontal lobectomy (D and E) and subsequently achieved seizure remission while also reducing the number of medications (Engel Ia). LOF : left orbitofrontal gyrus, LSF : left superior frontal gyrus, LMF : left middle frontal gyrus, LIF : left inferior frontal gyrus, SEEG : stereoelectroencephalography, MRI : magnetic resonance imaging.

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.

Review of technical aspects in SEEG procedures

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.

Notes

Conflicts of interest

No potential conflict of interest relevant to this article was reported.

Informed consent

This type of study does not require informed consent.

Author contributions

Conceptualization : JK, SHH; Data curation : JK, SHH, HJK, MSY, TSK, YSK, SAL; Writing - original draft : JK; Writing - review & editing : JK, SHH, HJK, MSY, TSK, YSK, SAL

Data sharing

Data are available from the corresponding author on reasonable request.

Preprint

None

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Article information Continued

Fig. 1.

Sagittal application of the stereotactic arc and corresponding angle parameters in the Leksell stereotactic system. A : Lateral-right orientation of the stereotactic arc. B : Sagittal-posterior orientation of the stereotactic arc (for the target in the left hemisphere). For stereoelectroencephalography requiring multiple and bilateral electrode placements, anterior/posterior orientations of the stereotactic arc may be preferred to the common lateralleft orientation. In these configurations, the arc support is attached to the x-axis of the coordinate frame instead of the y-axis. Following the center-of-arc principle, the target coordinate remains unchanged, but the coordinate on the arc axis needs to be set to its appropriate index mark : lateral-left orientation and anterior orientation share the same index, while the index for posterior orientation is obtained by subtracting from 200 mm. For anterior/posterior orientations, the arc axis should be set as the y-axis, which entails an additional adjustment of 15 mm from the x-axis value used for lateral orientations. Additionally, the ‘arc’ and ‘ring’ angle parameters need to be exchanged to maintain the correct entry point, with posterior arch orientation being optimal for the left hemisphere and anterior orientation for the right hemisphere. To convert between anterior and posterior orientations, both the ‘arc’ and ‘ring’ angles are simply subtracted from 180°.

Fig. 2.

Operative techniques for multiple SEEG electrode placement using frame-based stereotactic system. A : Patient positioning and application of the stereotactic arc (Leksell®; Elekta AB, Stockholm, Sweden). This orientation of the stereotactic arc allows bilateral access under a single surgical drape, though it is worth noting that the arc apparatus may obscure some areas in the occipital region. B : Drilling into the skull using a twist drill. Pre-measured skull depth at the entry point ensures procedure safety. C : Dural puncture with a monopolar cautery. This step proceeds in a blind manner, and practitioners should be vigilant to avoid violations to the brain parenchyma and superficial vessels. D : Fixation of the anchor bolt (Depthalon®; PMT Co., Chanhassen, MN, USA). The depth for electrode advancement is determined by subtracting the measured length between the arc and the fixed anchor point from the working length (typically 190 mm in the demonstrated system).

Fig. 3.

Postoperative intracranial hemorrhage following SEEG. Pre- and postoperative MRIs and the SEEG planning are presented (case #16). A 49-year-old female with a history of encephalitis and status epilepticus was referred for surgical intervention due to drug-resistant focal epilepsy, despite being on five antiseizure medications. MRI scans revealed bilateral hippocampal sclerosis and sequalae of encephalitis (A). SEEG was conducted to explore both the bilateral mesial temporal and operculo-insular regions (B). Preoperative post-contrast MRIs showed that a trajectory for targeting the left hippocampus was designed to ensure safe entry into brain parenchyma without damaging adjacent vasculature (C, arrowheads). However, during the procedure the SEEG electrode deviated from the planned trajectory, likely due to brain shift, passing through the nearby sulci (D, arrowheads). Initially, the patient tolerated the procedure well and was sent to epilepsy monitoring unit for long-term SEEG monitoring. However, a week later, the patient developed global dysphasia, and a follow-up imaging scans revealed a delayed postoperative hemorrhage (E and F). SEEG : stereoelectroencephalography, MRI : magnetic resonance imaging.

Fig. 4.

Successful seizure control following SEEG-guided resective surgery. The figure illustrates pre- and postoperative MRIs, SEEG planning, and intraoperative gross inspections from a representative case (case #13). A 15-year-old male with a history of hypoxic-ischemic encephalopathy had bilateral frontal atrophy with encephalomalacia (A, arrowheads). His seizures, characterized by hyperkinetic movements occurring several times a day, remained intractable despite the use of four antiseizure medications, causing significant distress to his caregiver. SEEG monitoring was performed to assess the feasibility of resective surgery (B). During SEEG, seizures were observed to initiate at the left orbitofrontal (C, arrow) and anterior cingulate regions, corresponding to the structural lesion observed in the MRI. The patient underwent a left frontal lobectomy (D and E) and subsequently achieved seizure remission while also reducing the number of medications (Engel Ia). LOF : left orbitofrontal gyrus, LSF : left superior frontal gyrus, LMF : left middle frontal gyrus, LIF : left inferior frontal gyrus, SEEG : stereoelectroencephalography, MRI : magnetic resonance imaging.

Table 1.

Patient demographics and clinical information

Case Sex/age (years) Onset age (duration) (years) Handedness Risk factors Neuropsychological condition Number of ASMs Seizure frequency (/months) Seizure type* Seizure location* Epilepsy type Preoperative imaging studies
Structural abnormality Perfusion (ictal SPECT) Metabolism (FDG-PET)
1 Female/38 9 (29) Rt. - ID 2 14 FIAS F3 (60), F4 (40) FLE, Lt. - ↑Rt. F/T/P/BG ↓Lt. F
2 Female/57 27 (30) Rt. - - 3 1.5 FTBTCS F8 (65), F7 (35) TLE, Bilat. Rt. HS ↑Bilat. T ↓Rt. T
3 Male/36 22 (14) Rt. Enceph. - 3 1.5 FIAS Sp1 (70), Sp2 (30) TLE, Lt. - ↑Lt. T ↓Lt. T
4 Female/30 27 (3) Rt. FC - 3 6.0 FTBTCS T7 (50), T8 (50) TLE, Lt. - ↑Lt. T ↓Rt. T
5 Male/26 14 (12) Rt. - ID 5 1.5 FIAS Sp2 (75), Sp1 (25) TLE, Rt. Rt. HS - ↓Rt. T
6 Male/15 8 (7) Lt. FC ID 4 30 FTBTCS C3 (50), C4 (50) DEE Lt. F EM - -
7 Female/25 20 (5) Rt. Enceph.; SE - 4 3.0 FTBTCS Sp2 (60), Sp1 (40) TLE, Rt. Rt. F DVA ↑Rt. T/BG ↓Rt. F/T/P
8 Male/35 21 (14) Rt. - - 3 1.0 FIAS Sp2 (100) TLE, Rt. Lt. HS ↑Lt. F/T/P/BG ↓Rt. F
9 Female/51 22 (29) Rt. - - 3 2.5 FIAS T8 (100) TLE, Rt. - - -
10 Male/46 36 (10) Rt. - - 4 1.5 FIAS T7/F7 (60), T8/F8 (40) TLE, Bilat. Bilat. O EM ↑Lt. T ↓Lt. T
11 Female/34 14 (20) Rt. FC - 3 4.0 FIAS T7/F3 (80), T8 (20) TLE, Lt. Lt. T EM, Lt. O CM - ↓Lt. T
12 Male/32 12 (20) Rt. Enceph. - 3 0.4 FTBTCS T7/F7 (67), T8/F8 (33) FLE, Bilat. - ↑Rt. F/T -
13 Male/15 3 (12) Ambidex. - ID 5 30 FIAS T7/F7 (67), T8/F8 (33) DEE Bilat. F EM - -
14 Female/32 15 (17) Rt. - - 3 1.5 FIAS Sp1 (60), Sp2 (40) TLE, Bilat. - ↑Lt. T/BG ↓Lt. T
15 Female/48 32 (16) Rt. - Depression 3 6.0 FIAS Sp2 (100) TLE, Rt. - ↑Rt. T ↓Rt. F/T/P
16 Female/49 39 (10) Rt. Enceph., SE - 5 1.5 FIAS Sp1 (60), Sp2 (40) TLE, Bilat. Bilat. HS ↑Rt. T ↓Bilat. T
*

Most common seizure characteristics recorded during scalp and sphenoidal video-electroencephalography monitoring.

ASM : antiseizure medication, SPECT : single-photon emission computerized tomography, FDG-PET : [18F]fluorodeoxyglucose positron emission tomography, Rt. : right, ID : intellectual disability, FIAS : focal impaired awareness seizure, FLE : frontal lobe epilepsy, Lt. : left, F : frontal, T : temporal, P : parietal, BG : basal ganglia, FBTCS : focal to bilateral tonic-clonic seizure, TLE : temporal lobe epilepsy, Bilat. : bilateral, HS : hippocampal sclerosis, Enceph. : encephalitis, FC : febrile convulsion, DEE : developmental and epileptic encephalopathy, EM : encephalomalacia, SE : status epilepticus, DVA : developmental venous anomaly, O : occipital, CM : cavernous malformation, Ambidex. : ambidextrous

Table 2.

SEEG investigation and surgical outcomes

Case Number of electrodes, Rt./Lt. Duration of monitoring (days) Number of recorded seizures* Ictal onset zone Localization Surgical intervention Histopathology Postop. follow-up (months) Seizure outcome ASM adjustment
1 0/9 10 10 (0) Lt. F (100) Lt. F Lt. F lobectomy Non-specific 16 IV No reduction
2 4/4 8 6 (2) Rt. MT (50), Lt. T (50) Bilat. T ANT-DBS - 16 II No reduction
3 5/7 11 23 (0) Lt. MT (96) Rt. MT (4) Lt. T Lt. ATL-AH Non-specific 13 Ia No reduction
4 8/3; 8/5 9; 11 41 (32); 19 (8) Rt. MT (67), Lt. MT (33) Bilat. T - - - - -
5 4/4 8 >99 (8) Rt. MT (100) Rt. T Rt. ATL-AH HS, SBH 17 Ia Reduction
6 0/9 6 13 (0) Lt. F (100) Lt. F Lt. F topectomy FCD IIa 12 Ia Reduction
7 12/6 12 12 (4) Lt. T/MT (58), Rt. T (42) Bilat. T - - - - -
8 6/6 16 4 (0) Rt. MT (100) Rt. T Rt. ATL Non-specific 10 Ia Reduction
9 7/1 12 27 (1) Rt. MT (100) Rt. T Rt. ATL-AH FCD I 4 Ia Reduction
10 6/8 11 12 (0) Lt. MT (58), Rt. MT (42) Bilat. T - - - - -
11 3/7 7 13 (0) Lt. T (85), Lt. MT (15) Lt. T Lt. ATL-AH EM 4 Ia No reduction
12 11/0 13 3 (3) Rt. F/OI (100) Rt. F Lt. F topectomy FCD I 5 III No reduction
13 3/11 8 >99 (100) Lt. F/C (100) Lt. F Lt. F lobectomy EM 4 Ia Reduction
14 7/9 12 9 (9) Lt. MT (89), Rt. T (11) Lt. T - - - - -
15 11/1 11 17 (0) Rt. MT (76), Rt. T (24) Rt. T Rt. ATL-AH HS, FCD IIIa <3 Ia Reduction
16 8/8 7 34 (0) Lt. T/MT (56), Rt. T/MT (44) Bilat. T - - - - -
*

Total number of seizures (number of secondary generalization).

Engel class at the last visit.

Stereoelectroencephalography was performed in two separate sessions for this patient.

SEEG : stereoelectroencephalography, Rt. : right, Lt. : left, Postop. : postoperative, ASM : antiseizure medication, F : frontal cortex, MT : mesial temporal region (amygdala and hippocampus), Bilat. : bilateral, T : temporal cortex, ANT-DBS : deep brain stimulation of the anterior nucleus of the thalamus, ATL-AH : anterior temporal lobectomy with amygdalohippocampectomy, HS : hippocampal sclerosis, SBH : subcortical band heterotopia (laminar heterotopia), FCD : focal cortical dysplasia, EM : encephalomalacia, OI : operculo-insular region, C : cingulate cortex

Table 3.

Review of technical aspects in SEEG procedures

Study Study population Stereotactic instruments Number of electrodes per case* Morbidity Electrode misplacement Accuracy measures
Time for electrode placement (minutes)
EPLE (mm) TPLE (mm)
Frame-based SEEG techniques
 González-Martínez et al. [19] (2016) Adult Leksell 13.3 (1367/103) 0.2% (3.0%) - 1.1 - 26.5 (352)
 van der Loo et al. [43] (2017) Adult Leksell 11.9 (902/76) 0.2% (2.6%) - 1.5 2.9 11.4 (136)
 Dewan et al. [14] (2018) Adult Customized 9.1 (137/15) - - 1.4±1.0 3.4±2.7 24.0 (207)
 Yu et al. [45] (2018) Adult Customized 6.5 (136/21) - - 1.2 (0.8–1.8) 4.5 (2.4–7.7) -
 Bourdillon et al. [5] (2018) Adult Talairach 12.6 (628/50) 0.2% (5.0%) 0.2% - 4.0±1.0 19.6 (246)
 D'Agostino et al. [12] (2020) Adult Customized 14.0 (182/13) 1.6% (23.1%) - 2.0 (1.2–2.9) 5.0 (3.0–6.9) 10.3 (144)
 Girgis et al. [17] (2020) Adult CRW 3.6 (36/10) - - - 7.0 -
 Zheng et al. [46] (2021) All Leksell 6.4 (90/14) 2.2% (14.3%) - 1.5±0.5 1.6±0.7 24.6 (153)
 Machetanz et al. [31] (2021) All BRW 7.6 (91/12) - - 1.5±0.6 1.5±0.8 15.1
 Kogias et al. [28] (2022) All Leksell 9.1 (136/15) 0.7% (6.7%) - 0.6 1.5 -
 This study All Leksell 11.8 (201/17) 0.5% (5.9%) 1.0% - - 13.0 (162)
Image-guided SEEG techniques
 Nowell et al. [34] (2014) Adult Medtronic 8.5 (187/22) 0.5% (4.5%) 6.4% - 3.7±2.2 16.1 (137)
 Hou et al. [21] (2016) Adult Medtronic 4.8 (173/36) 1.2% (5.6%) - - 2.0±1.0 19.4
 Verburg et al. [44] (2016) Adult Brainlab 12.7 (89/7) - - - 3.5 -
 Roessler et al. [36] (2016) Adult Brainlab 9.7 (58/6) - - 1.4±1.2 3.2±2.2 11.8 (115)
 Budke et al. [6] (2018) Pediatric Brainlab 7.4 (111/15) 0.9% (6.7%) - 3.6±1.8 2.9±1.5 15.7 (90)
 Sharma et al. [37] (2019) Pediatric Medtronic 10.9 (218/20) (n=6) - - 4.5 (2.8–6.1) 5.5 (4.0–6.4) -
 Kim et al. [26] (2020) All Medtronic 7.1 (177/25) - - - - 24.0 (173)
 Chen et al. [11] (2020) Pediatric Medtronic 4.5 (81/18) - - 2.0±0.6 2.6±0.6 -
 Girgis et al. [17] (2020) Adult Medtronic 3.5 (45/13) - 17.8% - 11.0 -
 Ladisich et al. [29] (2021) Adult Brainlab 10.5 (220/21) 0.5% (4.8%) 0.5% 3.2±2.4 2.7±2.0 -
 Vakharia et al. [41] (2021) Adult Medtronic 10.5 (168/16) - - 1.2±0.1 1.2±0.2 9.1 (202)
 Song et al. [38] (2021) Adult Brainlab 7.4 (141/19) - - 2.0±0.5 2.5±0.8 14.2
 Joris et al. [23] (2023) All Brainlab 8.5 (94/11) 1.1% (9.1%) 1.1% 4.2±2.5 4.1±2.5 18.6 (158)
Robot-assisted SEEG techniques
 Cardinale et al. [8] (2013) All Neuromate 13.3 (1567/118) 0.2% (3.2%) - 0.9 (0.6–1.4) 2.0 (1.4–3.0) 24.1 (320)
 González-Martínez et al. [19] (2016) Adult ROSA 12.3 (1245/101) 0.3% (4.0%) - 1.2 (0.8–1.8) 1.7 (1.2–2.3) 10.5 (130)
 Dorfer et al. [15] (2017) Adult iSYS1 5.8 (93/16) 1.1% (6.3%) - 1.3 1.5 15.7
 Cardinale et al. [9] (2017) Adult Neuromate 15.9 (127/8) - - 0.6 (0.3–0.9) 1.5 (1.1–2.4) -
 Candela-Cantó et al. [7] (2018) Pediatric Neuromate 11.7 (164/14) 1.2% (14.3%) - 1.6 (1.0–2.3) 1.8 (1.2–2.6) 35.4 (414)
 Bourdillon et al. [5] (2018) Adult Neuromate 11.3 (565/50) - 0.2% - 1.2±0.4 22.1 (250)
 McGovern et al. [32] (2019) Pediatric ROSA 12.4 (794/64) 0.1% (1.5%) - - - 9.6
 Sharma et al. [37] (2019) Pediatric ROSA 10.9 (218/20) (n=14) - - 1.1 (0.7–1.6) 0.7 (0.5–1.0) -
 Spyrantis et al. [39] (2019) All ROSA 9.0 (171/19) - - 1.9±1.1 2.6±1.7 -
 Kim et al. [26] (2020) All ROSA 10.2 (255/25) - - 1.4±0.8 3.1±2.0 12.4 (126)
 Bottan et al. [4] (2020) Adult Neuromate 2.4 (98/41) 1.5±1.2 2.3±1.5
 Zheng et al. [46] (2021) All SINO 10.7 (203/19) 2.0% (21.1%) - 1.4±0.5 1.5±0.4 13.7 (127)
 Machetanz et al. [31] (2021) All ROSA 8.6 (129/15) 0.8% (6.7%) - 0.7±0.5 1.6±0.8 9.1
 Bonda et al. [3] (2021) Pediatric ROSA 11.3 (261/23) - - - 4.5±3.5 6.6
 Vakharia et al. [41] (2021) Adult iSYS1 10.0 (160/16) - - 1.1±0.1 1.6±0.2 6.4 (176)
 Kandregula et al. [24] (2021) Adult Neuromate 12.8 (294/23) 0.7% (8.7%) - 1.5 (1.1–2.3) 2.3 (1.5–3.5) -
 Hines et al. [20] (2023) Adult Neuromate 13.8 (525/38) - - 1.2 (0.8–1.8) 2.4 (1.6–3.5) -
 Dedrickson et al. [13] (2023) Adult ExcelsiusGPS 11.0 (55/5) - - 1.6±1.2 - 14.2 (156)

A literature search on PubMed covered publications from 2013 to 2023. Selected studies that specifically reported clinical data on the safety, accuracy, and/or time efficiency of various stereotactic techniques were selectively reviewed and summarized, with duplicated data removed. Data are presented as either counts, percentages per electrode (per case), medians (interquartile range), or mean±standard deviation, depending on availability, unless noted otherwise. Some estimates are derived from calculations based on reported values.

*

Average number of electrodes per case (total number of electrodes / number of cases).

Morbidity rates are reported as specifically adherent to SEEG procedure.

Average procedure time per electrode (skin-to-skin operation time), as determined by dividing the operation time (either mean or median) by the average number of electrodes.

SEEG : stereoelectroencephalography, EPLE : entry point localization error, TPLE : target point localization error