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Phase I trial: safety and feasibility of intracranial electroencephalography using hybrid subdural electrodes containing macro- and microelectrode arrays

Jamie J. Van Gompel, S. Matthew Stead, Caterina Giannini, Fredric B. Meyer, W. Richard Marsh, Todd Fountain, Elson So, Aaron Cohen-Gadol, Kendall H. Lee, and Gregory A. Worrell

Object

Cerebral cortex electrophysiology is poorly sampled using standard, low spatial resolution clinical intracranial electrodes. Adding microelectrode arrays to the standard clinical macroelectrode arrays increases the spatial resolution and may ultimately improve the clinical utility of intracranial electroencephalography (iEEG). However, the safety of hybrid electrode systems containing standard clinical macroelectrode and microelectrode arrays is not yet known. The authors report on their preliminary experience in 24 patients who underwent implantation of hybrid electrodes.

Methods

In this study, 24 consecutive patients underwent long-term iEEG monitoring with implanted hybrid depth and subdural grid and strip electrodes; both clinical macroelectrodes and research microelectrodes were used. The patients included 18 women and 6 men with an average age of 35 ± 12 years (range 21–65). The mean hospital stay was 11 ± 4 days (range 5–20), with mean duration of implantation 7.0 ± 3.2 days (range 3–15). Data from the 198 consecutive craniotomies for standard clinical subdural grid insertion (prior to surgery in the 24 patients described here) were used for comparison to investigate the relative risk of complications.

Results

Focal seizure identification and subsequent resection was performed in 20 patients. One patient underwent a subsequent operation after neurological deterioration secondary to cerebral swelling and a 5-mm subdural hematoma. There were no infections. The overall complication rate was 4.2% (only 1 patient had a complication), which did not significantly differ from the complication rate previously reported by the authors of 6.6% when standard subdural and depth intracranial electrodes were used. There were no deaths or permanent neurological deficits related to electrode implantation.

Conclusions

The authors demonstrate the use of hybrid subdural strip and grid electrodes containing high-density microwire arrays and standard clinical macroelectrodes. Hybrid electrodes provide high spatial resolution electrophysiology of the neocortex that is impossible with standard clinical iEEG. In this initial study in 24 patients, the complication rate is acceptable, and there does not appear to be increased risk associated with the use of hybrid electrodes compared with standard subdural and depth iEEG electrodes. More research is required to show whether hybrid electrode recordings will improve localization of epileptic foci and tracking the generation of neocortical seizures.

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Acute postoperative seizures following anterior temporal lobectomy for intractable partial epilepsy

Bhaskara Rao Malla, Terence J. O'Brien, Gregory D. Cascino, Elson L. So, Kurupath Radhakrishnan, Peter Silbert, and W. Richard Marsh

Recurrence of seizures immediately following epilepsy surgery can be emotionally devastating, and raises concerns about the chances of successfully attaining long-term seizure control. The goals of this study were to investigate the frequency of acute postoperative seizure (APOS) occurring in the 1st postoperative week following anterior temporal lobectomy (ATL) to identify potential risk factors and to determine their prognostic significance.

One hundred sixty consecutive patients who underwent an ATL for intractable nonlesional temporal lobe epilepsy were retrospectively studied. Acute postoperative seizures occurred in 32 patients (20%). None of the following factors were shown to be significantly associated with the occurrence of APOS: age at surgery, duration of epilepsy, side of surgery, extent of neocortical resection, electrocorticography findings, presence of mesial temporal sclerosis, and hippocampal volume measurements (p > 0.05). Patients who suffered from APOS overall had a lower rate of favorable outcome with respect to seizure control at the last follow-up examination than patients without APOS (62.5% compared with 83.6%, p < 0.05). The type of APOS was of prognostic importance, with patients whose APOS were similar to their preoperative habitual seizures having a significantly worse outcome than those whose APOS were auras or were focal motor and/or generalized tonic-clonic seizures (excellent outcome: 14.3%, 77.8%, and 75%, respectively, p < 0.05). Only patients who had APOS similar to preoperative habitual seizures were less likely to have an excellent outcome than patients without APOS (14.3% compared with 75%, p < 0.05). Timing of the APOS and identification of a precipitating factor were of no prognostic importance.

The findings of this study may be useful in counseling patients who suffer from APOS following ATL for temporal lobe epilepsy.

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Intracranial electroencephalography seizure onset patterns and surgical outcomes in nonlesional extratemporal epilepsy

Clinical article

Nicholas M. Wetjen, W. Richard Marsh, Fredric B. Meyer, Gregory D. Cascino, Elson So, Jeffrey W. Britton, S. Matthew Stead, and Gregory A. Worrell

Object

Patients with normal MR imaging (nonlesional) findings and medically refractory extratemporal epilepsy make up a disproportionate number of nonexcellent outcomes after epilepsy surgery. In this paper, the authors investigated the usefulness of intracranial electroencephalography (iEEG) in the identification of surgical candidates.

Methods

Between 1992 and 2002, 51 consecutive patients with normal MR imaging findings and extratemporal epilepsy underwent intracranial electrode monitoring. The implantation of intracranial electrodes was determined by seizure semiology, interictal and ictal scalp EEG, SPECT, and in some patients PET studies. The demographics of patients at the time of surgery, lobar localization of electrode implantation, duration of follow-up, and Engel outcome score were abstracted from the Mayo Rochester Epilepsy Surgery Database. A blinded independent review of the iEEG records was conducted for this study.

Results

Thirty-one (61%) of the 51 patients who underwent iEEG ultimately underwent resection for their epilepsy. For 28 (90.3%) of the 31 patients who had epilepsy surgery, adequate information regarding follow-up (> 1 year), seizure frequency, and iEEG recordings was available. Twenty-six (92.9%) of 28 patients had frontal lobe resections, and 2 had parietal lobe resections. The most common iEEG pattern at seizure onset in the surgically treated group was a focal high-frequency discharge (in 15 [53.6%] of 28 patients). Ten (35.7%) of the 28 surgically treated patients were seizure free. Fourteen (50%) had Engel Class I outcomes, and overall, 17 (60.7%) had significant improvement (Engel Class I and IIAB with ≥80% seizure reduction). Focal high-frequency oscillation at seizure onset was associated with Engel Class I surgical outcome (12 [85.7%] of 14 patients, p = 0.02), and it was uncommon in the nonexcellent outcome group (3 [21.4%] of 14 patients).

Conclusions

A focal high-frequency oscillation (> 20 Hz) at seizure onset on iEEG may identify patients with nonlesional extratemporal epilepsy who are likely to have an Engel Class I outcome after epilepsy surgery. The prospect of excellent outcome in nonlesional extratemporal lobe epilepsy prior to intracranial monitoring is poor (14 [27.5%] of 51 patients). However, iEEG can further stratify patients and help identify those with a greater likelihood of Engel Class I outcome after surgery.

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Subtraction ictal single-photon emission computed tomography coregistered to magnetic resonance imaging in evaluating the need for repeated epilepsy surgery

Nicholas M. Wetjen, Gregory D. Cascino, A. James Fessler, Elson L. So, Jeffrey R. Buchhalter, Brian P. Mullan, Terence J. O’Brien, Fredric B. Meyer, and W. Richard Marsh

Object

The aim of this study was to determine whether ictal single-photon emission computed tomography (SPECT) is useful in localizing the site of seizure onset in patients in whom surgery for intractable epilepsy failed and who are being considered for repeated surgery.

Methods

Subtraction ictal SPECT coregistered to magnetic resonance imaging (SISCOM) studies were retrospectively analyzed in 58 patients who were being evaluated for possible repeated resection for intractable partial epilepsy between January 1, 1996, and October 31, 1999. All patients had persistent seizures subsequent to an initial resection and underwent another excision. The SISCOM-demonstrated abnormalities were classified as concordant, discordant, or indeterminate, compared with the localization of the epileptogenic zone revealed on video electroencephalography monitoring. The ability of SISCOM to predict operative outcome was also determined in patients who had undergone repeated surgical procedures.

The SISCOM studies revealed a localized hyperperfused alteration in 46 (79%) of 58 patients. Forty-one (89%) of these 46 patients had a SISCOM-demonstrated alteration in the hemisphere of the previous epilepsy surgery. Imaging changes in 33 (72%) of the 46 patients were at the site of the previous focal cortical resection. Eight (17%) of the 46 had SISCOM-demonstrated abnormalities remote from the lobe in which surgery had been performed but in the ipsilateral hemisphere. The hyperperfusion focus was in the contralateral hemisphere in the remaining five patients (11%). The site of the epileptogenic zone was concordant with the SISCOM focus in 32 (70%) of 46 patients. Twenty-six patients underwent repeated resection and were followed up for a mean of 44 months thereafter; 11 of these patients (42%) had a significant reduction in seizure tendency. Only five patients (19%) were seizure free. Ten (50%) of 20 patients with a concordant SISCOM focus compared with none (0%) of three patients with a discordant focus had a favorable surgical outcome (p = 0.23).

Conclusions

The SISCOM method might be useful in the evaluation of, and the surgical planning for, patients with intractable partial epilepsy in whom previous resective treatment has failed and who are being considered for reoperation.

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Acute postoperative seizures following anterior temporal lobectomy for intractable partial epilepsy

Bhaskara Rao Malla, Terence J. O'Brien, Gregory D. Cascino, Elson L. So, Kurupath Radhakrishnan, Peter Silbert, and W. Richard Marsh

Object. Recurrence of seizures immediately following epilepsy surgery can be emotionally devastating, and raises concerns about the chances of successfully attaining long-term seizure control. The goals of this study were to investigate the frequency of acute postoperative seizures (APOS) occurring in the 1st postoperative week following anterior temporal lobectomy (ATL) to identify potential risk factors and to determine their prognostic significance.

Methods. One hundred sixty consecutive patients who underwent an ATL for intractable nonlesional temporal lobe epilepsy were retrospectively studied. Acute postoperative seizures occurred in 32 patients (20%). None of the following factors were shown to be significantly associated with the occurrence of APOS: age at surgery, duration of epilepsy, side of surgery, extent of neocortical resection, electrocorticography findings, presence of mesial temporal sclerosis, and hippocampal volume measurements (p > 0.05). Patients who suffered from APOS overall had a lower rate of favorable outcome with respect to seizure control at the last follow-up examination than patients without APOS (62.5% compared with 83.6%, p < 0.05). The type of APOS was of prognostic importance, with patients whose APOS were similar to their preoperative habitual seizures having a significantly worse outcome than those whose APOS were auras or were focal motor and/or generalized tonic—clonic seizures (excellent outcome: 14.3%, 77.8%, and 75%, respectively, p < 0.05). Only patients who had APOS similar to preoperative habitual seizures were less likely to have an excellent outcome than patients without APOS (14.3% compared with 75%, p < 0.05). Timing of the APOS and identification of a precipitating factor were of no prognostic importance.

Conclusions. The findings of this study may be useful in counseling patients who suffer from APOS following ATL for temporal lobe epilepsy.

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Reassessing the impact of intraoperative electrocorticography on postoperative outcome of patients undergoing standard temporal lobectomy for MRI-negative temporal lobe epilepsy

Sanjeet S. Grewal, Mohammed Ali Alvi, William J. Perkins, Gregory D. Cascino, Jeffrey W. Britton, David B. Burkholder, Elson So, Cheolsu Shin, Richard W. Marsh, Fredric B. Meyer, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Almost 30% of the patients with suspected temporal lobe epilepsy (TLE) have normal results on MRI. Success rates for resection of MRI-negative TLE are less favorable, ranging from 36% to 76%. Herein the authors describe the impact of intraoperative electrocorticography (ECoG) augmented by opioid activation and its effect on postoperative seizure outcome.

METHODS

Adult and pediatric patients with medically resistant MRI-negative TLE who underwent standardized ECoG at the time of their elective anterior temporal lobectomy (ATL) with amygdalohippocampectomy between 1990 and 2016 were included in this study. Seizure recurrence comprised the primary outcome of interest and was assessed using Kaplan-Meier and multivariable Cox regression analysis plots based on distribution of interictal epileptiform discharges (IEDs) recorded on scalp electroencephalography, baseline and opioid-induced IEDs on ECoG, and extent of resection.

RESULTS

Of the 1144 ATLs performed at the authors’ institution between 1990 and 2016, 127 (11.1%) patients (81 females) with MRI-negative TLE were eligible for this study. Patients with complete resection of tissue generating IED recorded on intraoperative ECoG were less likely to have seizure recurrence compared to those with incomplete resection on univariate analysis (p < 0.05). No difference was found in seizure recurrence between patients with bilateral independent IEDs and unilateral IEDs (p = 0.15), presence or absence of opioid-induced epileptiform activation (p = 0.61), or completeness of resection of tissue with opioid-induced IEDs on intraoperative ECoG (p = 0.41).

CONCLUSIONS

The authors found that incomplete resection of IED-generating tissue on intraoperative ECoG was associated with an increased chance of seizure recurrence. However, they found that induction of epileptiform activity with intraoperative opioid activation did not provide useful intraoperative data predictive of improving operative results for temporal lobectomy in MRI-negative epilepsy.