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The stereotactic approach for mapping epileptic networks: a prospective study of 200 patients

Clinical article

Demitre Serletis, Juan Bulacio, William Bingaman, Imad Najm, and Jorge González-Martínez

Object

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.

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在一段4年,作者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.

InJournal of Neurosurgery Volume 121 (2014): Issue 5 (Nov 2014)

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Connectivity of the frontal and anterior insular network: a cortico-cortical evoked potential study

Rei Enatsu, Jorge Gonzalez-Martinez, Juan Bulacio, John C. Mosher, Richard C. Burgess, Imad Najm, and Dileep R. Nair

OBJECT

The frontal and insular fiber network in humans remains largely unknown. This study investigated the connectivity of the frontal and anterior insular network in humans using cortico-cortical evoked potential (CCEP).

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这包括回顾性分析18例with medically intractable focal epilepsy who underwent stereoelectroencephalography and CCEP. Alternating 1-Hz electrical stimuli were delivered to parts of the frontal lobe and anterior insula (prefrontal cortex [PFC], ventrolateral and dorsolateral premotor area [vPM and dPM, respectively], presupplementary motor area [pre-SMA], SMA, frontal operculum, and anterior insula). A total of 40–60 stimuli were averaged in each trial to obtain CCEP responses. The distribution of CCEP was evaluated by calculating the root mean square of CCEP responses.

RESULTS

Stimulation of the PFC elicited prominent CCEP responses in the medial PFC and PMs over the ipsilateral hemisphere. Stimulation of the vPM and dPM induced CCEP responses in the ipsilateral frontoparietal areas. Stimulation of the pre-SMA induced CCEP responses in the ipsilateral medial and lateral frontal areas and contralateral pre-SMA, whereas stimulation of the SMA induced CCEP responses in the bilateral frontoparietal areas. Stimulation of the frontal operculum induced CCEP responses in the ipsilateral insula and temporal operculum. CCEPs were observed in the ipsilateral medial, lateral frontal, and frontotemporal operculum in the anterior insular stimulation. Stimulation of the vPM and SMA led to the network in the dominant hemisphere being more developed.

CONCLUSIONS

Various regions within the frontal lobe and anterior insula were linked to specific ipsilateral and contralateral regions, which may reflect distinct functional roles.

InJournal of Neurosurgery Volume 125 (2016): Issue 1 (Jul 2016)

Open access

Radiofrequency ablation during stereoelectroencephalography: from diagnostic tool to therapeutic intervention. Illustrative case

Demitre Serletis, Juan Bulacio, Justin Bingaman, Elham Abushanab, Stephen P. Harasimchuk, Richard Rammo, Silvia Neme-Mercante, and William Bingaman

BACKGROUND

Radiofrequency thermocoagulation (RFTC) during intracranial stereoelectroencephalography (sEEG) was first described as a safe technique for creating lesions of epileptic foci in 2004. Since that time, the method has been applied as a diagnostic and/or palliative intervention. Although widely practiced in European epilepsy surgical programs, the technique has not been popularized in the United States given the lack of Food and Drug Administration (FDA)–approved technologies permitting safe usage of in situ sEEG electrodes for this purpose.

OBSERVATIONS

The authors present a case report of a young female patient with refractory left neocortical temporal lobe epilepsy undergoing sEEG electrode implantation, who underwent sEEG-guided RFTC via a stereotactic temperature-sensing pallidotomy probe. Although used as a diagnostic step in her workup, the patient has remained seizure-free for nearly 18 months.

LESSONS

The use of in situ sEEG electrodes for RFTC remains limited in the United States. In this context, this case highlights a safe alternative and temporizing approach to performing diagnostic sEEG-guided RFTC, using a temperature-sensing pallidotomy probe to create small, precise stereotactic lesions. The authors caution careful consideration of this technique as a temporary work-around solution while also highlighting the rising need for new FDA-approved technologies for safe RFTC through in situ temperature-sensing sEEG electrodes.

InJournal of Neurosurgery: Case Lessons Volume 6 (2023): Issue 7 (Aug 2023)

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癫痫outcom的决定因素e after resective surgery following stereoelectroencephalography

Juan C. Bulacio, James Bena, Piradee Suwanpakdee, Dileep Nair, Ajay Gupta, Andreas Alexopoulos, William Bingaman, and Imad Najm

OBJECTIVE

The aim of this study was to investigate seizure outcomes after resective epilepsy surgery following stereoelectroencephalography (SEEG), including group characteristics, comparing surgical and nonsurgical groups and assess predictors of time to seizure recurrence.

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Clinical and EEG data of 536 consecutive patients who underwent SEEG at Cleveland Clinic Epilepsy Center between 2009 and 2017 were reviewed. The primary outcome was defined as complete seizure freedom since the resective surgery, discounting any auras or seizures that occurred within the 1st postoperative week. In addition, the rate of seizure freedom based on Engel classification was determined in patients with follow-up of ≥ 1 year. Presumably significant outcome variables were first identified using univariate analysis, and Cox proportional hazards modeling was used to identify outcome predictors.

RESULTS

Of 527 patients satisfying study criteria, 341 underwent resective surgery. Complete and continuous seizure freedom after surgery was achieved in 55.5% of patients at 1 year postoperatively, 44% of patients at 3 years, and 39% of patients at 5 years. As a secondary outcome point, 58% of patients achieved Engel class I seizure outcome for at least 1 year at last follow-up. Among surgical outcome predictors, in multivariate model analysis, the seizure recurrence rate by type of resection (p = 0.039) remained statistically significant, with the lowest risk of recurrence occurring after frontal and temporal lobe resections compared with multilobar and posterior quadrant surgeries. Patients with a history of previous resection (p = 0.006) and bilateral implantations (p = 0.023) were more likely to have seizure recurrence. The absence of an MRI abnormality prior to resective surgery did not significantly affect seizure outcome in this cohort.

CONCLUSIONS

This large, single-center series shows that resective surgery leads to continuous seizure freedom in a group of patients with complex and severe pharmacoresistant epilepsy after SEEG evaluation. In addition, up to 58% of patients achieved seizure freedom at last follow-up. The authors’ results suggest that SEEG is equally effective in patients with frontal and temporal lobe epilepsy with or without MRI identified lesions.

InJournal of Neurosurgery Volume 136: Issue 6 (Jun 2022)

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Stereotactic placement of depth electrodes in medically intractable epilepsy

Technical note

Jorge Gonzalez-Martinez, Jeffrey Mullin, Sumeet Vadera, Juan Bulacio, Gwyneth Hughes, Stephen Jones, Rei Enatsu, and Imad Najm

Object

Despite its long-reported successful record, with almost 60 years of clinical use, the technical complexity regarding the placement of stereoelectroencephalography (SEEG) depth electrodes may have contributed to the limited widespread application of the technique in centers outside Europe. The authors report on a simplified and novel SEEG surgical technique in the extraoperative mapping of refractory focal epilepsy.

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The proposed technique was applied in patients with medically refractory focal epilepsy. Data regarding general demographic information, method of electrode implantation, time of implantation, number of implanted electrodes, seizure outcome after SEEG-guided resections, and complications were prospectively collected.

Results

From March 2009 to April 2012, 122 patients underwent SEEG depth electrode implantation at the Cleveland Clinic Epilepsy Center in which the authors' technique was used. There were 65 male and 57 female patients whose mean age was 33 years (range 5–68 years). The group included 21 pediatric patients (younger than 18 years). Planning and implantations were performed in a single stage. The time for planning was, on average, 33 minutes (range 20–47 minutes), and the time for implantation was, on average, 107 minutes (range 47–150 minutes). Complications related to the SEEG technique were observed in 3 patients. The calculated risk of complications per electrode was 0.18%. The seizure-free rate after SEEG-guided resections was 62% in a mean follow-up period of 12 months.

Conclusions

The authors report on a safe, simplified, and less time-consuming method of SEEG depth electrode implantation, using standard and widely available surgical tools, making the technique a reasonable option for extraoperative monitoring of patients with medically intractable epilepsy in centers lacking the Talairach stereotactic armamentarium.

In开云手机版app下载安装最新版神经外科杂志》卷120开云体育app官方网站下载入口(2014):问题3(Mar 2014)

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The impact of skull thickness on pediatric stereoencephalography electrode implantation and technical considerations

Ansh Desai, Akshay Sharma, Swetha J. Sundar, Jason K. Hsieh, Efstathios Kondylis, Arpan Patel, Juan Bulacio, Ajay Gupta, Lara Jehi, and William Bingaman

OBJECTIVE

One consideration in pediatric stereoencephalography (SEEG) is decreased skull thicknesses compared with adults, which may limit traditional bolt-based anchoring of electrodes. The authors aimed to investigate the safety profile, complication rates, and technical adaptations of placing SEEG electrodes in pediatric patients.

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The authors retrospectively reviewed all patients aged 12 years or younger at the time of SEEG implantation at their institution. Postimplantation CT scans were used to measure skull thickness at the entry point of each SEEG lead. Postimplantation lead accuracy was also assessed.

RESULTS

Fifty-three patients were reviewed. The median skull thickness was 4.1 (interquartile range [IQR] 3.15–5.2) mm. There were 5 total complications: 1 retained bolt fragment, 3 asymptomatic subdural hematomas, and 1 asymptomatic intracranial hemorrhage. Median radial error from the lead target was 3.5 (IQR 2.24–5.25) mm. Linear regression analysis revealed that increasing skull thickness decreased the deviation from the intended target, implying an improved accuracy to target at thicker skull entry points; this trended towards improved accuracy, but did not achieve statistical significance (p = 0.54).

CONCLUSIONS

This study found a 1.9% hardware complication rate and a 9.4% asymptomatic hemorrhage rate. Suturing electrodes to the scalp may represent a reasonable option if there are concerns of young age or a thin skull. These data indicate that invasive SEEG evaluation is safe among patients 12 years old or younger.

InJournal of Neurosurgery: Pediatrics Publish Before Print

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Determinants of epileptogenic zone identification and seizure outcome in children with refractory epilepsy undergoing stereoelectroencephalography

Jason K. Hsieh, Swetha J. Sundar, Elaine Lu, Ansh Desai, Ajay Gupta, Ahsan N. Moosa, William Bingaman, Lara Jehi, and Juan Bulacio

OBJECTIVE

The objective of this paper was to investigate the factors associated with successful epileptogenic zone (EZ) identification and postsurgical seizure freedom in pediatric patients with drug-resistant epilepsy who underwent first-time stereoelectroencephalography (SEEG).

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The authors conducted a retrospective cohort study of all consecutive patients younger than 18 years of age at the time of recommendation for invasive evaluation with SEEG who were treated from July 2009 to June 2020. The authors excluded patients who had undergone failed prior resective epilepsy surgery or prior intracranial electrode evaluation for seizure localization. For their primary outcome, the authors evaluated the relationship between clinical and radiographic factors and successful identification of a putative EZ. For their secondary outcome, the authors investigated whether these factors had a significant relationship with seizure freedom (according to the Engel classification) at last follow-up.

RESULTS

The authors included 101 patients in this study. SEEG was safe, with no major morbidity or mortality experienced. The population was complex, with an MRI lesion present in less than 40% of patients and patients as young as 2.9 years included. A proposed EZ was identified in 88 (87%) patients. Patients with an older onset of epilepsy (OR 1.20/year, p = 0.04) or epilepsy etiology suspected to be due to a developmental lesion (OR 8.38, p = 0.02) were more likely to have proposed EZ identification. Patients with a preimplantation bilateral seizure-onset hypothesis (OR 0.29, p = 0.047) and those who underwent longer periods of monitoring (OR 0.86/day, p = 0.006) were somewhat less likely to have proposed EZ identification. The presence of an MRI lesion was a positive factor on secondary analyses (OR 4.18, p = 0.049; 1-tailed test). Fifty percent of patients who underwent surgical treatment with resection or laser ablation achieved Engel class I outcomes, in contrast to 0% of patients who underwent neuromodulation. Patients with a preimplantation hypothesis in the frontal/parietal lobes had increased odds of seizure freedom compared with patients with a hypothesis in other locations (OR 3.64, p = 0.01).

CONCLUSIONS

Pediatric SEEG is safe and often identifies a proposed resectable EZ. These results suggest that SEEG is effective in patients with frontal/parietal preimplantation hypothesis, with or without identified lesions on MRI.

InJournal of Neurosurgery: Pediatrics Publish Before Print

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