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Localizing seizure onset zones in surgical epilepsy with neurostimulation deep learning

Graham W. Johnson, Leon Y. Cai, Derek J. Doss, Jasmine W. Jiang, Aarushi S. Negi, Saramati Narasimhan, Danika L. Paulo, Hernán F. J. González, Shawniqua Williams Roberson, Sarah K. Bick, Catie E. Chang, Victoria L. Morgan, Mark T. Wallace, and Dario J. Englot

OBJECTIVE

In drug-resistant temporal lobe epilepsy, automated tools for seizure onset zone (SOZ) localization that use brief interictal recordings could supplement presurgical evaluations and improve care. Thus, the authors sought to localize SOZs by training a multichannel convolutional neural network on stereoelectroencephalography (SEEG) cortico-cortical evoked potentials.

METHODS

The authors performed single-pulse electrical stimulation in 10 drug-resistant temporal lobe epilepsy patients implanted with SEEG. Using 500,000 unique poststimulation SEEG epochs, the authors trained a multichannel 1-dimensional convolutional neural network to determine whether an SOZ had been stimulated.

RESULTS

SOZs were classified with mean sensitivity of 78.1% and specificity of 74.6% according to leave-one-patient-out testing. To achieve maximum accuracy, the model required a 0- to 350-msec poststimulation time period. Post hoc analysis revealed that the model accurately classified unilateral versus bilateral mesial temporal lobe seizure onset, as well as neocortical SOZs.

CONCLUSIONS

This was the first demonstration, to the authors’ knowledge, that a deep learning framework can be used to accurately classify SOZs with single-pulse electrical stimulation–evoked responses. These findings suggest that accurate classification of SOZs relies on a complex temporal evolution of evoked responses within 350 msec of stimulation. Validation in a larger data set could provide a practical clinical tool for the presurgical evaluation of drug-resistant epilepsy.

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Clinical outcome of imaging-based programming for anterior thalamic nucleus deep brain stimulation

Brin E. Freund, Elena Greco, Lela Okromelidze, Julio Mendez, William O. Tatum IV, Sanjeet S. Grewal, and Erik H. Middlebrooks

OBJECTIVE

The authors hypothesized that the proximity of deep brain stimulator contacts to the anterior thalamic nucleus–mammillothalamic tract (ANT-MMT) junction determines responsiveness to treatment with ANT deep brain stimulation (DBS) in drug-resistant epilepsy and conducted this study to test that hypothesis.

METHODS

This retrospective study evaluated patients who had undergone ANT DBS electrode implantation and whose devices were programmed to stimulate nearest the ANT-MMT junction based on direct MRI visualization. The proximity of the active electrode to the ANT and the ANT-MMT junction was compared between responders (≥ 50% reduction in seizure frequency) and nonresponders. Linear regression was performed to assess the percentage of seizure reduction and distance to both the ANT and the ANT-MMT junction.

RESULTS

Four (57.1%) of 7 patients had ≥ 50% reduction in seizures. All 4 responders had at least one contact within 1 mm of the ANT-MMT junction, whereas the 3 patients with < 50% seizure improvement did not have a contact within 1 mm of the ANT-MMT junction. Additionally, the 4 responders demonstrated contact positioning closer to the ANT-MMT junction than the 3 nonresponders (mean distance from MMT: 0.7 mm on the left and 0.6 mm on the right in responders vs 3.0 mm on the left and 2.3 mm on the right in nonresponders). However, proximity of the electrode contact to any point in the ANT nucleus did not correlate with seizure reduction. Greater seizure improvement was correlated with a contact position closer to the ANT-MMT junction (R2 = 0.62, p = 0.04). Seizure improvement was not significantly correlated with proximity of the contact to any ANT border (R2 = 0.24, p = 0.26).

CONCLUSIONS

Obtained using a combination of direct visualization and targeted programming of the ANT-MMT junction, data in this study support the hypothesis that proximity to the ANT alone does not correlate with seizure reduction in ANT DBS, whereas proximity to the ANT-MMT junction does. These findings support the importance of direct targeting in ANT DBS, as well as imaging-informed programming. Additionally, the authors provide supportive evidence for future prospective trials using ANT-MMT junction for direct surgical targeting.

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The endoscopic anterior transmaxillary temporal pole approach for mesial temporal lobe epilepsies: a feasibility study

Jorge A. Gonzalez-Martinez, Hussam Abou-Al-Shaar, Arka N. Mallela, Michael M. McDowell, Luke Henry, David T. Fernandes Cabral, James Sweat, Alexandra Urban, Joanna Fong, Niravkumar Barot, James F. Castellano, Vijayalakshmi Rajasekaran, Anto Bagic, Carl H. Snyderman, and Paul A. Gardner

OBJECTIVE

In mesial temporal lobe epilepsy (MTLE), the ideal surgical approach to achieve seizure freedom and minimize morbidity is an unsolved question. Selective approaches to mesial temporal structures often result in suboptimal seizure outcomes. The authors report the results of a pilot study intended to evaluate the clinical feasibility of using an endoscopic anterior transmaxillary (eATM) approach for minimally invasive management of MTLEs.

METHODS

The study is a prospectively collected case series of four consecutive patients who underwent the eATM approach for the treatment of MTLE and were followed for a minimum of 12 months. All participants underwent an epilepsy workup and surgical care at a tertiary referral comprehensive epilepsy center and had medically refractory epilepsy. The noninvasive evaluations and intracranial recordings of these patients confirmed the presence of anatomically restricted epileptogenic zones located in the mesial temporal structures. Data on seizure freedom at 1 year, neuropsychological outcomes, diffusion tractography, and adverse events were collected and analyzed.

RESULTS

By applying the eATM technique and approaching the far anterior temporal lobe regions, mesial-basal resections of the temporal polar areas and mesial temporal structures were successfully achieved in all patients (2 with left-sided approaches, 2 with right-sided approaches). No neurological complications or neuropsychological declines were observed. All 4 patients achieved Engel class Ia outcome up to the end of the follow-up period (19, 15, 14, and 12 months). One patient developed hypoesthesia in the left V2 distribution but there were no other adverse events. The low degree of white matter injury from the eATM approach was analyzed using high-definition fiber tractography in 1 patient as a putative mechanism for preserving neuropsychological function.

CONCLUSIONS

The described series demonstrates the feasibility and potential safety profile of a novel approach for medically refractory MTLE. The study affirms the feasibility of performing efficacious mesial temporal lobe resections through an eATM approach.

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Stereo-electroencephalography–guided radiofrequency thermocoagulation in patients with MRI-negative focal epilepsy

Luísa Panadés-de Oliveira, Carmen Pérez-Enríquez, Ainara Barguilla, Klaus Langohr, Gerardo Conesa, Nazaret Infante, Alessandro Principe, and Rodrigo Rocamora

OBJECTIVE

Coupled with stereo-electroencephalography (SEEG), radiofrequency thermocoagulation (RFTC) has emerged as a therapeutic alternative for patients with refractory focal epilepsy, with proven safe but highly variable results across studies. The authors aimed to describe the outcomes and safety of SEEG-RFTC, focusing on patients with MRI-negative epilepsy.

METHODS

A retrospective observational study was conducted on patients evaluated by SEEG in the authors’ center. Of 84 total cases, 55 underwent RFTC, with 31 MRI-negative epilepsies that were ultimately included in the study. The primary outcome was freedom from disabling seizures at last follow-up. Secondary outcomes were reduction in seizure frequency (RFTC response = seizure frequency reduction > 50%), peri-interventional complications, and neuropsychological outcomes. Potential factors influencing post-RFTC outcome were considered by comparing different variables between responders and nonresponders.

RESULTS

The mean follow-up period was 30.9 months (range 7.1–69.8 months). Three patients underwent subsequent resection/laser interstitial thermal therapy within the 1st year after RFTC failure. All other patients completed a minimum follow-up period of 1 year. Fourteen patients (45.2%) showed at least a 50% reduction in seizure frequency (responders), and 8 were seizure free (25.8% of the whole cohort). One case showed a permanent complication not directly related to thermolesions. Most patients (76%) showed no significant cognitive decline. Electrically elicited seizures (EESs) were observed in all seizure-free patients and were more frequent in responders (p = 0.038). All patients who were seizure free at the 6-month visit maintained their status during long-term follow-up.

CONCLUSIONS

SEEG-RFTC is a safe procedure and leads to a good response in many cases of MRI-negative focal epilepsies. One-quarter of the patients were seizure free and almost one-half were responders at the last follow-up. Although these results are still far from those achieved through conventional resection, a nonnegligible proportion of patients may benefit from this one-stage and much less invasive approach. Factors associated with seizure outcome remain to be elucidated; however, responders were significantly more frequent among patients with EESs, and achieving 6 months of seizure freedom appears to predict a good long-term response. In addition, the positive predictive value of RFTC response may be a valuable factor in the decision to proceed to subsequent surgery.

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Asymmetry index in anatomically symmetrized FDG-PET for improved epileptogenic focus detection in pharmacoresistant epilepsy

Shameer Aslam, Natesan Damodaran, Ramiah Rajeshkannan, Manjit Sarma, Siby Gopinath, and Ashok Pillai

OBJECTIVE

Positron emission tomography (PET) imaging has assumed an essential role in the presurgical evaluation of epileptogenic foci in drug-resistant epilepsy by identifying the hypometabolic cerebral cortex. The authors herein designed a pilot study to test a novel technique of PET asymmetry after anatomical symmetrization coregistered to MRI (PASCOM), utilizing interhemispheric metabolic asymmetry on interictal fluorine 18–labeled fluorodeoxyglucose (FDG)-PET to better localize the epileptogenic zone.

METHODS

The authors analyzed interictal FDG-PET scans from 23 patients with drug-resistant epilepsy, mean (± SD) age 20.9 ± 13.1 years old, who had an Engel class I postsurgical outcome while followed up for > 12 months. T1-weighted and FLAIR MRI were used to create a patient-specific, structurally symmetrical template. The asymmetry index (AI) image was computed to detect the cerebral region of hypometabolism using different z-score threshold criteria to optimize sensitivity and specificity. The detected regions were compared with the resection cavity on postoperative MRI using predefined anatomical labels. PASCOM was compared with the visual analysis of FDG-PET by a nuclear medicine consultant blinded to other clinical data (VIS) and visual analysis during multidisciplinary team discussion (MDT). The efficacy of each technique was compared based on a performance score (S), sensitivity, specificity, and correct lateralization of epileptogenicity.

RESULTS

The mean S was maximum (1.30 ± 1.23) for AI images when thresholded at z > 4 and retaining the cluster of more than 100 voxels containing the peak AI value (Z4C) with 73.03% sensitivity and 96.43% specificity. The mean S was minimum for VIS (0.27 ± 0.31). The mean sensitivity was maximum for MDT (85.04%) and minimum for Z5C (AI images thresholded at z > 5 and clustered; 59.47%), whereas the mean specificity was maximum for Z5C (97.77%) and minimum for VIS (64.60%). Z3C (AI images thresholded at z > 3 and clustered) and Z4C were able to correctly identify the side of epileptogenicity in all the patients.

CONCLUSIONS

The PASCOM technique with a Z4C threshold had a maximum performance score with good sensitivity and specificity in localizing and lateralizing the epileptogenic zone. The described technique outperformed the conventional visual analysis of FDG-PET and hence warrants further prospective verification.

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Modern intracranial electroencephalography for epilepsy localization with combined subdural grid and depth electrodes with low and improved hemorrhagic complication rates

Anthony T. Lee, Noah M. Nichols, Benjamin A. Speidel, Joline M. Fan, Iahn Cajigas, Robert C. Knowlton, and Edward F. Chang

OBJECTIVE

Recent trends have moved from subdural grid electrocorticography (ECoG) recordings toward stereo-electroencephalography (SEEG) depth electrodes for intracranial localization of seizures, in part because of perceived morbidity from subdural grid and strip electrodes. For invasive epilepsy monitoring, the authors describe the outcomes of a hybrid approach, whereby patients receive a combination of subdural grids, strips, and frameless stereotactic depth electrode implantations through a craniotomy. Evolution of surgical techniques was employed to reduce complications. In this study, the authors review the surgical hemorrhage and functional outcomes of this hybrid approach.

METHODS

A retrospective review was performed of consecutive patients who underwent hybrid implantation from July 2012 to May 2022 at an academic epilepsy center by a single surgeon. Outcomes included hemorrhagic and nonhemorrhagic complications, neurological deficits, length of monitoring, and number of electrodes.

RESULTS

A total of 137 consecutive procedures were performed; 113 procedures included both subdural and depth electrodes. The number of depth electrodes and electrode contacts did not increase the risk of hemorrhage. A mean of 1.9 ± 0.8 grid, 4.9 ± 2.1 strip, and 3.0 ± 1.9 depth electrodes were implanted, for a mean of 125.1 ± 32 electrode contacts per patient. The overall incidence of hematomas over the study period was 5.1% (7 patients) and decreased significantly with experience and the introduction of new surgical techniques. The incidence of hematomas in the last 4 years of the study period was 0% (55 patients). Symptomatic hematomas were all delayed and extra-axial. These patients required surgical evacuation, and there were no cases of hematoma recurrence. All neurological deficits related to hematomas were temporary and were resolved at hospital discharge. There were 2 nonhemorrhagic complications. The mean duration of monitoring was 7.3 ± 3.2 days. Seizures were localized in 95% of patients, with 77% of patients eventually undergoing resection and 17% undergoing responsive neurostimulation device implantation.

CONCLUSIONS

In the authors’ institutional experience, craniotomy-based subdural and depth electrode implantation was associated with low hemorrhage rates and no permanent morbidity. The rate of hemorrhage can be nearly eliminated with surgical experience and specific techniques. The decision to use subdural electrodes or SEEG should be tailored to the patient’s unique pathology and surgeon experience.

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Arousal and salience network connectivity alterations in surgical temporal lobe epilepsy

Hernán F. J. González, Saramati Narasimhan, Sarah E. Goodale, Graham W. Johnson, Derek J. Doss, Danika L. Paulo, Victoria L. Morgan, Catie Chang, and Dario J. Englot

OBJECTIVE

It is poorly understood why patients with mesial temporal lobe epilepsy (TLE) have cognitive deficits and brain network changes that extend beyond the temporal lobe, including altered extratemporal intrinsic connectivity networks (ICNs). However, subcortical arousal structures project broadly to the neocortex, are affected by TLE, and thus may contribute to these widespread network effects. The authors’ objective was to examine functional connectivity (FC) patterns between subcortical arousal structures and neocortical ICNs, possible neurocognitive relationships, and FC changes after epilepsy surgery.

METHODS

The authors obtained resting-state functional magnetic resonance imaging (fMRI) in 50 adults with TLE and 50 controls. They compared nondirected FC (correlation) and directed FC (Granger causality laterality index) within the salience network, default mode network, and central executive network, as well as between subcortical arousal structures; these 3 ICNs were also compared between patients and controls. They also used an fMRI-based vigilance index to relate alertness to arousal center FC. Finally, fMRI was repeated in 29 patients > 12 months after temporal lobe resection.

RESULTS

Nondirected FC within the salience (p = 0.042) and default mode (p = 0.0008) networks, but not the central executive network (p = 0.79), was decreased in patients in comparison with controls (t-tests, corrected). Nondirected FC between the salience network and subcortical arousal structures (nucleus basalis of Meynert, thalamic centromedian nucleus, and brainstem pedunculopontine nucleus) was reduced in patients in comparison with controls (p = 0.0028–0.015, t-tests, corrected), and some of these connectivity abnormalities were associated with lower processing speed index, verbal comprehension, and full-scale IQ. Interestingly, directed connectivity measures suggested a loss of top-down influence from the salience network to the arousal nuclei in patients. After resection, certain FC patterns between the arousal nuclei and salience network moved toward control values in the patients, suggesting that some postoperative recovery may be possible. Although an fMRI-based vigilance measure suggested that patients exhibited reduced alertness over time, FC abnormalities between the salience network and arousal structures were not influenced by the alertness levels during the scans.

CONCLUSIONS

FC abnormalities between subcortical arousal structures and ICNs, such as the salience network, may be related to certain neurocognitive deficits in TLE patients. Although TLE patients demonstrated vigilance abnormalities, baseline FC perturbations between the arousal and salience networks are unlikely to be driven solely by alertness level, and some may improve after surgery. Examination of the arousal network and ICN disturbances may improve our understanding of the downstream clinical effects of TLE.