A Novel Framework for Network-Targeted Neuropsychiatric Deep Brain Stimulation

Neurosurgery 89:E116–E121, 2021

Deep brain stimulation (DBS) has emerged as a promising therapy for neuropsychiatric illnesses, including depression and obsessive-compulsive disorder, but has shown inconsistent results in prior clinical trials. We propose a shift away from the empirical paradigm for developing new DBS applications, traditionally based on testing brain targets with conventional stimulation paradigms. Instead, we propose a multimodal approach centered on an individualized intracranial investigation adapted from the epilepsy monitoring experience, which integrates comprehensive behavioral assessment, such as the Research Domain Criteria proposed by the National Institutes of Mental Health. In this paradigm-shifting approach, we combine readouts obtained from neurophysiology, behavioral assessments, and self-report during broad exploration of stimulation parameters and behavioral tasks to inform the selection of ideal DBS parameters. Such an approach not only provides a foundational understanding of dysfunctional circuits underlying symptom domains in neuropsychiatric conditions but also aims to identify generalizable principles that can ultimately enable individualization and optimization of therapy without intracranial monitoring.

Robot-assisted stereoelectroencephalography in children

J Neurosurg Pediatr 23:288–296, 2019

The goal in the study was to describe the clinical outcomes associated with robot-assisted stereoelectroencephalography (SEEG) in children.

METHODS The authors performed a retrospective, single-center study in consecutive children with medically refractory epilepsy who were undergoing robot-assisted SEEG. Kaplan-Meier survival analysis was used to calculate the probability of seizure freedom. Both univariate and multivariate methods were used to analyze the preoperative and operative factors associated with seizure freedom.

RESULTS Fifty-seven children underwent a total of 64 robot-assisted procedures. The patients’ mean age was 12 years, an average of 6.4 antiepileptic drugs (AEDs) per patient had failed prior to implantation, and in 56% of the patients the disease was considered nonlesional. On average, children had 12.4 electrodes placed per implantation, with an implantation time of 9.6 minutes per electrode and a 10-day postoperative stay. SEEG analysis yielded a definable epileptogenic zone in 51 (89%) patients; 42 (74%) patients underwent surgery, half of whom were seizure free at last follow-up, 19.6 months from resection. In a multivariate generalized linear model, resective surgery, older age, and shorter SEEGrelated hospital length of stay were associated with seizure freedom. In a Cox proportional hazards model including only the children who underwent resective surgery, older age was the only significant factor associated with seizure freedom. Complications related to bleeding were the major contributors to morbidity. One patient (1.5%) had a symptomatic hemorrhage resulting in a permanent neurological deficit.

CONCLUSIONS The authors report one of the largest pediatric-specific SEEG series demonstrating that the modern surgical management of medically refractory epilepsy in children can lead to seizure freedom in many patients, while also highlighting the challenges posed by this difficult patient population.

 

Stereoelectroencephalography in insular epilepsy

J Neurosurg 128:1147–1157, 2018

Insular epilepsy is relatively rare; however, exploring the insular cortex when preoperative workup raises the suspicion of insular epilepsy is of paramount importance for accurate localization of the epileptogenic zone and achievement of seizure freedom. The authors review their clinical experience with stereoelectroencephalography (SEEG) electrode implantation in patients with medically intractable epilepsy and suspected insular involvement.

METHODS A total of 198 consecutive cases in which patients underwent SEEG implantation with a total of 1556 electrodes between June 2009 and April 2013 were reviewed. The authors identified patients with suspected insular involvement based on seizure semiology, scalp EEG data, and preoperative imaging (MRI, PET, and SPECT or magnetoencephalography [MEG]). Patients with at least 1 insular electrode based on the postoperative 3D reconstruction of CT fused with the preoperative MRI were included.

RESULTS One hundred thirty-five patients with suspected insular epilepsy underwent insular implantation of a total of 303 electrodes (1–6 insular electrodes per patient) with a total of 562 contacts. Two hundred sixty-eight electrodes (88.5%) were implanted orthogonally through the frontoparietal or temporal operculum (420 contacts). Thirty-five electrodes (11.5%) were implanted by means of an oblique trajectory either through a frontal or a parietal entry point (142 contacts). Nineteen patients (14.07%) had insular electrodes placed bilaterally. Twenty-three patients (17.04% of the insular implantation group and 11.6% of the whole SEEG cohort) were confirmed by SEEG to have ictal onset zones in the insula. None of the patients experienced any intracerebral hemorrhage related to the insular electrodes. After insular resection, 5 patients (33.3%) had Engel Class I outcomes, 6 patients (40%) had Engel Class II, 3 patients (20%) had Engel Class III, and 1 patient (6.66%) had Engel Class IV.

CONCLUSIONS Insula exploration with stereotactically placed depth electrodes is a safe technique. Orthogonal electrodes are implanted when the hypothesis suggests opercular involvement; however, oblique electrodes allow a higher insular sampling rate.

 

Stereoelectroencephalography Using Magnetic Resonance Angiography for Avascular Trajectory Planning

Neurosurgery 81:688–695, 2017

Stereoelectroencephalography (SEEG) requires high-quality angiographic studies because avascular trajectory planning is a prerequisite for the safety of this procedure. Some epilepsy surgery groups have begun to use computed tomography angiography and magnetic resonance T1-weighted sequence with contrast enhancement for this purpose.

OBJECTIVE: To present the first series of patients with avascular trajectory planning of SEEG based on magnetic resonance angiography (MRA).

METHODS: Thirty-six SEEG explorations for drug-resistant focal epilepsy were performed from January 2013 to December 2015. A retrospective analysis of this consecutive surgical series was then performed. Magnetic resonance imaging included MRA with a modified contrast-enhanced magnetic resonance venography (MRV) protocol with a short acquisition delay, which allowed simultaneous arterial and venous visualization. Our criteria for satisfactoryMRAwere the visualization of at least first-order branches of the angular artery, paracentral and calcarine artery, and third-order tributaries of the superficial Sylvian vein, vein of Labbe, and vein of Trolard.

RESULTS: Thirty-four patients underwent 36 SEEG explorations with 369 electrodes carrying 4321 contacts. Contrast-enhanced MRA using the MRV protocol was judged satisfactory for SEEG planning in all explorations. Postoperative complications were not observed in our series of 36 SEEG explorations, which included 50 transopercular insular trajectories.

CONCLUSION: MRA using an MRV protocol may be applied for avascular trajectory planning during SEEG procedures. This technique provides a simultaneous visualization of cortical arteries and veins without the need for additional radiation exposure or intraarterial catheter placement.

 

The stereotactic approach for mapping epileptic networks

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J Neurosurg 121:1239–1246, 2014

Stereoelectroencephalography (SEEG) is a methodology that permits accurate 3D in vivo electroclinical recordings of epileptiform activity. Among other general indications for invasive intracranial electroencephalography (EEG) monitoring, its advantages include access to deep cortical structures, its ability to localize the epileptogenic zone when subdural grids have failed to do so, and its utility in the context of possible multifocal seizure onsets with the need for bihemispheric explorations. In this context, the authors present a brief historical overview of the technique and report on their experience with 2 SEEG techniques (conventional Leksell frame-based stereotaxy and frameless stereotaxy under robotic guidance) for the purpose of invasively monitoring difficult-to-localize refractory focal epilepsy.

Methods. Over a period of 4 years, the authors prospectively identified 200 patients with refractory epilepsy who collectively underwent 2663 tailored SEEG electrode implantations for invasive intracranial EEG monitoring and extraoperative mapping. The first 122 patients underwent conventional Leksell frame-based SEEG electrode placement; the remaining 78 patients underwent frameless stereotaxy under robotic guidance, following acquisition of a stereotactic ROSA robotic device at the authors’ institution. Electrodes were placed according to a preimplantation hypothesis of the presumed epileptogenic zone, based on a standardized preoperative workup including video-EEG monitoring, MRI, PET, ictal SPECT, and neuropsychological assessment. Demographic features, seizure semiology, number and location of implanted SEEG electrodes, and location of the epileptogenic zone were recorded and analyzed for all patients. For patients undergoing subsequent craniotomy for resection, the type of resection and procedure-related complications were prospectively recorded. These results were analyzed and correlated with pathological diagnosis and postoperative seizure outcomes.

Results. The epileptogenic zone was confirmed by SEEG in 154 patients (77%), of which 134 (87%) underwent subsequent craniotomy for epileptogenic zone resection. Within this cohort, 90 patients had a minimum follow-up of at least 12 months; therein, 61 patients (67.8%) remained seizure free, with an average follow-up period of 2.4 years. The most common pathological diagnosis was focal cortical dysplasia Type I (55 patients, 61.1%). Per electrode, the surgical complications included wound infection (0.08%), hemorrhagic complications (0.08%), and a transient neurological deficit (0.04%) in a total of 5 patients (2.5%). One patient (0.5%) ultimately died due to intracerebral hematoma directly ensuing from SEEG electrode placement.

Conclusions. Based on these results, SEEG methodology is safe, reliable, and effective. It is associated with minimal morbidity and mortality, and serves as a practical, minimally invasive approach to extraoperative localization of the epileptogenic zone in patients with refractory epilepsy.

Tailored Unilobar and Multilobar Resections for Orbitofrontal-Plus Epilepsy

Tailored Unilobar and Multilobar Resections for Orbitofrontal-Plus Epilepsy

Neurosurgery 75:388–397, 2014

Surgery for frontal lobe epilepsy often has poor results, likely because of incomplete resection of the epileptogenic zone.

OBJECTIVE: To present our experience with a series of patients manifesting 2 different anatomo-electro-clinical patterns of refractory orbitofrontal epilepsy, necessitating different surgical approaches for resection in each group.

METHODS: Eleven patients with refractory epilepsy involving the orbitofrontal region were consecutively identified over 3 years in whom stereoelectroencephalography identified the epileptogenic zone. All patients underwent preoperative evaluation, stereoelectroencephalography, and postoperative magnetic resonance imaging. Demographic features, seizure semiology, imaging characteristics, location of the epileptogenic zone, surgical resection site, and pathological diagnosis were analyzed. Surgical outcome was correlated with type of resection.

RESULTS: Five patients exhibited orbitofrontal plus frontal epilepsy with the epileptogenic zone consistently residing in the frontal lobe; after surgery, 4 patients were free of disabling seizures (Engel I) and 1 patient improved (Engel II). The remaining 6 patients had multilobar epilepsy with the epileptogenic zone located in the orbitofrontal cortex associated with the temporal polar region (orbitofrontal plus temporal polar epilepsy). After surgery, all 6 patients were free of disabling seizures (Engel I). Pathology confirmed focal cortical dysplasia in all patients. We report no complications or mortalities in this series.

CONCLUSION: Our findings highlight the importance of differentiating between orbitofrontal plus frontal and orbitofrontal plus temporal polar epilepsy in patients afflicted with seizures involving the orbitofrontal cortex. For identified cases of orbitofrontal plus temporal polar epilepsy, a multilobar resection including the temporal pole may lead to improved postoperative outcomes with minimal morbidity or mortality.

Stereoelectroencephalography: Surgical Methodology, Safety, and Stereotactic Application Accuracy in 500 Procedures

Stereoelectroencephalography___Surgical

Neurosurgery 72:353–366, 2013

Stereoelectroencephalography (SEEG) methodology, originally developed by Talairach and Bancaud, is progressively gaining popularity for the presurgical invasive evaluation of drug-resistant epilepsies.

OBJECTIVE: To describe recent SEEG methodological implementations carried out in our center, to evaluate safety, and to analyze in vivo application accuracy in a consecutive series of 500 procedures with a total of 6496 implanted electrodes.

METHODS: Four hundred nineteen procedures were performed with the traditional 2- step surgical workflow, which was modified for the subsequent 81 procedures. The new workflow entailed acquisition of brain 3-dimensional angiography and magnetic resonance imaging in frameless and markerless conditions, advanced multimodal planning, and robot-assisted implantation. Quantitative analysis for in vivo entry point and target point localization error was performed on a sub–data set of 118 procedures (1567 electrodes).

RESULTS: The methodology allowed successful implantation in all cases. Major complication rate was 12 of 500 (2.4%), including 1 death for indirect morbidity. Median entry point localization error was 1.43 mm (interquartile range, 0.91-2.21 mm) with the traditional workflow and 0.78 mm (interquartile range, 0.49-1.08 mm) with the new one (P , 2.2 · 10216). Median target point localization errors were 2.69 mm (interquartile range, 1.89-3.67 mm) and 1.77 mm (interquartile range, 1.25-2.51 mm; P, 2.2 · 10216), respectively.

CONCLUSION: SEEG is a safe and accurate procedure for the invasive assessment of the epileptogenic zone. Traditional Talairach methodology, implemented by multimodal planning and robot-assisted surgery, allows direct electrical recording from superficial and deep-seated brain structures, providing essential information in the most complex cases of drug-resistant epilepsy.

Stereoelectroencephalography: Surgical Methodology, Safety, and Stereotactic Application Accuracy in 500 Procedures

Stereoelectroencephalography- Surgical Methodology, Safety, and Stereotactic Application Accuracy in 500 Procedures

Neurosurgery 72:353–366, 2013

Stereoelectroencephalography (SEEG) methodology, originally developed by Talairach and Bancaud, is progressively gaining popularity for the presurgical invasive evaluation of drug-resistant epilepsies.

OBJECTIVE: To describe recent SEEG methodological implementations carried out in our center, to evaluate safety, and to analyze in vivo application accuracy in a consecutive series of 500 procedures with a total of 6496 implanted electrodes.

METHODS: Four hundred nineteen procedures were performed with the traditional 2- step surgical workflow, which was modified for the subsequent 81 procedures. The new workflow entailed acquisition of brain 3-dimensional angiography and magnetic resonance imaging in frameless and markerless conditions, advanced multimodal planning, and robot-assisted implantation. Quantitative analysis for in vivo entry point and target point localization error was performed on a sub–data set of 118 procedures (1567 electrodes).

RESULTS: The methodology allowed successful implantation in all cases. Major complication rate was 12 of 500 (2.4%), including 1 death for indirect morbidity. Median entry point localization error was 1.43 mm (interquartile range, 0.91-2.21 mm) with the traditional workflow and 0.78 mm (interquartile range, 0.49-1.08 mm) with the new one (P < 2.2 · 10*16). Median target point localization errors were 2.69 mm (interquartile range, 1.89-3.67 mm) and 1.77 mm (interquartile range, 1.25-2.51 mm; P< 2.2 · 10*16), respectively.

CONCLUSION: SEEG is a safe and accurate procedure for the invasive assessment of the epileptogenic zone. Traditional Talairach methodology, implemented by multimodal planning and robot-assisted surgery, allows direct electrical recording from superficial and deep-seated brain structures, providing essential information in the most complex cases of drug-resistant epilepsy.