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Outcomes of cingulate epilepsy surgery: insights from an institutional and patient-level systematic review and meta-analysis

Panagiotis Kerezoudis, Rohin Singh, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Due to their deep and medial location, range of seizure semiologies, and poor localization on ictal electroencephalography (EEG), cingulate gyrus seizures can be difficult to diagnose and treat. The aim of this study was to review the available evidence on postoperative outcomes after cingulate epilepsy surgery.

METHODS

A comprehensive literature search of the PubMed/MEDLINE, Ovid Embase, Ovid Scopus, and Cochrane Library databases was conducted to identify studies that investigated postoperative outcomes of patients with cingulate epilepsy. Seizure freedom at the last follow-up (at least 12 months) was the primary endpoint. The literature search was supplemented by the authors’ institutional series (4 patients).

RESULTS

Twenty-one studies were identified, yielding a total of 105 patients (68 with lesional epilepsy [65%]). Median age at surgery was 23 years, and 56% of patients were male. Median epilepsy duration was 7.5 years. Invasive EEG recording was performed on 69% of patients (53% of patients with lesional epilepsy and 97% of those with nonlesional epilepsy, p < 0.001). The most commonly resected region was the anterior cingulate (55%), followed by the posterior (17%) and middle (14%) cingulate. Lesionectomy alone was performed in 9% of patients. Additional extracingulate treatment was performed in 54% of patients (53% of patients with lesional epilepsy vs 57% of those with nonlesional epilepsy, p = 0.87). The most common pathology was cortical dysplasia (54%), followed by low-grade neoplasm (29%) and gliosis (8%). Seizure freedom was noted in 72% of patients (median follow-up 24 months). A neurological deficit was noted in 27% of patients (24% had temporary deficit), with the most common deficit being motor weakness (13%) followed by supplementary motor area syndrome (9.5%). Univariate survival analysis revealed significantly greater probability of seizure freedom in patients with lesional epilepsy (p = 0.015, log-rank test).

CONCLUSIONS

Surgical treatment of drug-resistant focal epilepsy originating from the cingulate gyrus is safe, leads to low rates of permanent adverse effects, and leads to high rates of long-term seizure freedom in carefully selected patients. These data may serve as a benchmark for surgical counseling of patients with cingulate epilepsy.

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Electrocorticography-guided resection of temporal cavernoma: is electrocorticography warranted and does it alter the surgical approach?

Clinical article

Jamie J. Van Gompel, Jesus Rubio, Gregory D. Cascino, Gregory A. Worrell, and Fredric B. Meyer

Object

Cavernous hemangiomas associated with epilepsy present an interesting surgical dilemma in terms of whether one should perform a pure lesionectomy or tailored resection, especially in the temporal lobe given the potential for cognitive damage. This decision is often guided by electrocorticography (ECoG), despite the lack of data regarding its value in cavernoma surgery. The purpose of the present study was several-fold: first, to determine the epilepsy outcome following resection of cavernomas in all brain regions; second, to evaluate the usefulness of ECoG in guiding surgical decision making; and third, to determine the optimum surgical approach for temporal lobe cavernomas.

Methods

The authors identified from their surgical database 173 patients who had undergone resection of cavernomas. One hundred two of these patients presented with epilepsy, and 61 harbored temporal lobe cavernomas. Preoperatively, all patients were initially evaluated by an epileptologist. The mean follow-up was 37 months.

Results

Regardless of the cavernoma location, surgery resulted in an excellent seizure control rate: Engel Class I outcome in 88% of patients at 2 years postoperatively. Of 61 patients with temporal lobe cavernomas, the mesial structures were involved in 35. Among the patients with temporal lobe cavernomas, those who underwent ECoG typically had a more extensive parenchymal resection rather than a lesionectomy (p < 0.0001). The use of ECoG in cases of temporal lobe cavernomas resulted in a superior seizure-free outcome: 79% (29 patients) versus 91% (23 patients) of patients at 6 months postresection, 77% (22 patients) versus 90% (20 patients) at 1 year, and 79% (14 patients) versus 83% (18 patients) at 2 years without ECoG versus with ECoG, respectively.

Conclusions

The surgical removal of cavernomas most often leads to an excellent epilepsy outcome. In cases of temporal lobe cavernomas, the more extensive the ECoG-guided resection, the better the seizure outcome. In addition to upholding the concept of kindling, the data in this study support the use of ECoG in temporal lobe cavernoma surgery in patients presenting with epilepsy.

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Patient-assessed satisfaction and outcome after microsurgical resection of cavernomas causing epilepsy

Jamie J. Van Gompel, W. Richard Marsh, Fredric B. Meyer, and Gregory A. Worrell

Object

Microsurgical resection of supratentorial cavernomas associated with intractable epilepsy is performed frequently. Despite its common occurrence, little is known about patient perceptions of microsurgical resection for cavernomas. This survey study was performed to investigate patient perceived outcome after surgery for cavernomas associated with intractable epilepsy.

Methods

The authors' surgical database was searched for cavernoma resection performed between 1971 and July of 2006. Of the initial 173 patients identified, 102 met criteria for medically intractable seizures. These 102 patients were then mailed a survey to determine follow-up and patient satisfaction. Thirty-nine surveys were returned as undeliverable, and 30 (48%) of the remaining 63 patients responded.

Results

The average age at surgery for patients responding to this survey was 40 ± 16 years compared with 35 ± 15 years for all 102 patients. At prolonged follow-up, 87% of patients reported being seizure-free. Of those with seizures, 2 (7%) reported being nearly seizure-free (rare disabling seizures), 2 (7%) believed they had a worthwhile improvement in seizure frequency, and no patient (0%) in this series believed they did not have a worthwhile improvement in seizure frequency. Ninety percent of responders stated they definitely, and 10% probably, would have surgery again. No patient responded that they probably or definitely would not have epilepsy surgery. Mean clinical follow-up was 36 ± 8 months and survey follow-up was 97 ± 13 months for these 30 patients. Use of the mail-in survey increased follow-up length 2.7 times longer compared with clinical follow-up.

Conclusions

It is clear from this select group of survey responders that patients undergoing surgery for cavernomas associated with medically intractable epilepsy are happy they underwent surgery (100%) and had excellent surgical outcomes (87% seizure-free) at prolonged follow-up of 97 ± 13 months. These survey results support that microsurgical resection for cavernomas is highly effective and significantly improves these patients' quality of life.

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Differences in functional connectivity profiles as a predictor of response to anterior thalamic nucleus deep brain stimulation for epilepsy: a hypothesis for the mechanism of action and a potential biomarker for outcomes

Erik H. Middlebrooks, Sanjeet S. Grewal, Matthew Stead, Brian N. Lundstrom, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Deep brain stimulation (DBS) of the anterior nucleus of the thalamus (ANT) is a promising therapy for refractory epilepsy. Unfortunately, the variability in outcomes from ANT DBS is not fully understood. In this pilot study, the authors assess potential differences in functional connectivity related to the volume of tissue activated (VTA) in ANT DBS responders and nonresponders as a means for better understanding the mechanism of action and potentially improving DBS targeting.

METHODS

This retrospective analysis consisted of 6 patients who underwent ANT DBS for refractory epilepsy. Patients were classified as responders (n = 3) if their seizure frequency decreased by at least 50%. The DBS electrodes were localized postoperatively and VTAs were computationally generated based on DBS programming settings. VTAs were used as seed points for resting-state functional MRI connectivity analysis performed using a control dataset. Differences in cortical connectivity to the VTA were assessed between the responder and nonresponder groups.

RESULTS

The ANT DBS responders showed greater positive connectivity with the default mode network compared to nonresponders, including the posterior cingulate cortex, medial prefrontal cortex, inferior parietal lobule, and precuneus. Interestingly, there was also a consistent anticorrelation with the hippocampus seen in responders that was not present in nonresponders.

CONCLUSIONS

Based on their pilot study, the authors observed that successful ANT DBS in patients with epilepsy produces increased connectivity in the default mode network, which the authors hypothesize increases the threshold for seizure propagation. Additionally, an inhibitory effect on the hippocampus mediated through increased hippocampal γ-aminobutyric acid (GABA) concentration may contribute to seizure suppression. Future studies are planned to confirm these findings.

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Stereotactic electroencephalography with temporal grid and mesial temporal depth electrode coverage: does technique of depth electrode placement affect outcome?

Clinical article

Jamie J. Van Gompel, Fredric B. Meyer, W. Richard Marsh, Kendall H. Lee, and Gregory A. Worrell

Object

Intracranial monitoring for temporal lobe seizure localization to differentiate neocortical from mesial temporal onset seizures requires both neocortical subdural grids and hippocampal depth electrode implantation. There are 2 basic techniques for hippocampal depth electrode implantation. This first technique uses a stereotactically guided 8-contact depth electrode directed along the long axis of the hippocampus to the amygdala via an occipital bur hole. The second technique involves direct placement of 2 or 3 4-contact depth electrodes perpendicular to the temporal lobe through the middle temporal gyrus and overlying subdural grid. The purpose of this study was to determine whether one technique was superior to the other by examining monitoring success and complications.

Methods

Between 1997 and 2005, 41 patients underwent invasive seizure monitoring with both temporal subdural grids and depth electrodes placed in 2 ways. Patients in Group A underwent the first technique, and patients in Group B underwent the second technique.

Results

Group A consisted of 26 patients and Group B 15 patients. There were no statistically significant differences between Groups A and B regarding demographics, monitoring duration, seizure localization, or outcome (Engel classification). There was a statistically significant difference at the point in time at which these techniques were used: Group A represented more patients earlier in the series than Group B (p < 0.05). The complication rate attributable to the grids and depth electrodes was 0% in each group. It was more likely that the depth electrodes were placed through the grid if there was a prior resection and the patient was undergoing a new evaluation (p < 0.05). Furthermore, Group A procedures took significantly longer than Group B procedures.

Conclusions

In this patient series, there was no difference in efficacy of monitoring, complications, or outcome between hippocampal depth electrodes placed laterally through temporal grids or using an occipital bur hole stereotactic approach. Placement of the depth electrodes perpendicularly through the grids and middle temporal gyrus is technically more practical because multiple head positions and redraping are unnecessary, resulting in shorter operative times with comparable results.

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Surgical approaches to refractory central lobule epilepsy: a systematic review on the role of resection, ablation, and stimulation in the contemporary era

Panagiotis Kerezoudis, Brian N. Lundstrom, Fredric B. Meyer, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Epilepsy originating from the central lobule (i.e., the primary sensorimotor cortex) is a challenging entity to treat given its involvement of eloquent cortex. The objective of this study was to review available evidence on treatment options for central lobule epilepsy.

METHODS

A comprehensive literature search (PubMed/Medline, EMBASE, and Scopus) was conducted for studies (1990 to date) investigating postoperative outcomes for central lobule epilepsy. The primary and secondary endpoints were seizure freedom at last follow-up and postoperative neurological deficit, respectively. The following procedures were included: open resection, multiple subpial transections (MSTs), laser and radiofrequency ablation, deep brain stimulation (DBS), responsive neurostimulation (RNS), and continuous subthreshold cortical stimulation (CSCS).

RESULTS

A total of 52 studies and 504 patients were analyzed. Most evidence was based on open resection, yielding a total of 400 patients (24 studies), of whom 62% achieved seizure freedom at a mean follow-up of 48 months. A new or worsened motor deficit occurred in 44% (permanent in 19%). Forty-six patients underwent MSTs, of whom 16% achieved seizure freedom and 30% had a neurological deficit (permanent in 12%). There were 6 laser ablation cases (cavernomas in 50%) with seizure freedom in 4 patients and 1 patient with temporary motor deficit. There were 5 radiofrequency ablation cases, with 1 patient achieving seizure freedom, 2 patients each with Engel class III and IV outcomes, and 2 patients with motor deficit. The mean seizure frequency reduction at the last follow-up was 79% for RNS (28 patients), 90% for CSCS (15 patients), and 73% for DBS (4 patients). There were no cases of temporary or permanent neurological deficit in the CSCS or DBS group.

CONCLUSIONS

This review highlights the safety and efficacy profile of resection, ablation, and stimulation for refractory central lobe epilepsy. Resection of localized regions of epilepsy onset zones results in good rates of seizure freedom (62%); however, nearly 20% of patients had permanent motor deficits. The authors hope that this review will be useful to providers and patients when tailoring decision-making for this intricate pathology.

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Outcomes of epilepsy surgery in the older population: not too old, not too late

Panagiotis Kerezoudis, Rohin Singh, Veronica Parisi, Gregory A. Worrell, Kai J. Miller, W. Richard Marsh, and Jamie J. Van Gompel

OBJECTIVE

The prevalence of epilepsy in the older adult population is increasing. While surgical intervention in younger patients is supported by level I evidence, the safety and efficacy of epilepsy surgery in older individuals is less well established. The aim of this study was to evaluate seizure freedom rates and surgical outcomes in older epilepsy patients.

METHODS

The authors’ institutional electronic database was queried for patients older than 50 who had undergone epilepsy surgery during 2002–2018. Cases were grouped into 50–59, 60–69, and 70+ years old. Seizure freedom at the last follow-up constituted the primary outcome of interest. The institutional analysis was supplemented by a literature review and meta-analysis (random effects model) of all published studies on this topic as well as by an analysis of complication rates, mortality rates, and cost data from a nationwide administrative database (Vizient Inc., years 2016–2019).

RESULTS

A total of 73 patients (n = 16 for 50–59 years, n = 47 for 60–69, and n = 10 for 70+) were treated at the authors’ institution. The median age was 63 years, and 66% of the patients were female. At a median follow-up of 24 months, seizure freedom was 73% for the overall cohort, 63% for the 50–59 group, 77% for the 60–69 group, and 70% for the 70+ group. The literature search identified 15 additional retrospective studies (474 cases). Temporal lobectomy was the most commonly performed procedure (73%), and mesial temporal sclerosis was the most common pathology (52%), followed by nonspecific gliosis (19%). The pooled mean follow-up was 39 months (range 6–114.8 months) with a pooled seizure freedom rate of 65% (95% CI 59%–72%). On multivariable meta-regression analysis, an older mean age at surgery (coefficient [coeff] 2.1, 95% CI 1.1–3.1, p < 0.001) and the presence of mesial temporal sclerosis (coeff 0.3, 95% CI 0.1–0.6, p = 0.015) were the most important predictors of seizure freedom. Finally, analysis of the Vizient database revealed mortality rates of 0.5%, 1.1%, and 9.6%; complication rates of 7.1%, 10.1%, and 17.3%; and mean hospital costs of $31,977, $34,586, and $40,153 for patients aged 50–59, 60–69, and 70+ years, respectively.

CONCLUSIONS

While seizure-free outcomes of epilepsy surgery are excellent, there is an expected increase in morbidity and mortality with increasing age. Findings in this study on the safety and efficacy of epilepsy surgery in the older population may serve as a useful guide during preoperative decision-making and patient counseling.

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Insular epilepsy surgery: lessons learned from institutional review and patient-level meta-analysis

Panagiotis Kerezoudis, Rohin Singh, Anshit Goyal, Gregory A. Worrell, W. Richard Marsh, Jamie J. Van Gompel, and Kai J. Miller

OBJECTIVE

Insular lobe epilepsy is a challenging condition to diagnose and treat. Due to anatomical intricacy and proximity to eloquent brain regions, resection of epileptic foci in that region can be associated with significant postoperative morbidity. The aim of this study was to review available evidence on postoperative outcomes following insular epilepsy surgery.

METHODS

A comprehensive literature search (PubMed/MEDLINE, Scopus, Cochrane) was conducted for studies investigating the postoperative outcomes for seizures originating in the insula. Seizure freedom at last follow-up (at least 12 months) comprised the primary endpoint. The authors also present their institutional experience with 8 patients (4 pediatric, 4 adult).

RESULTS

A total of 19 studies with 204 cases (90 pediatric, 114 adult) were identified. The median age at surgery was 23 years, and 48% were males. The median epilepsy duration was 8 years, and 17% of patients had undergone prior epilepsy surgery. Epilepsy was lesional in 67%. The most common approach was transsylvian (60%). The most commonly resected area was the anterior insular region (n = 42, 21%), whereas radical insulectomy was performed in 13% of cases (n = 27). The most common pathology was cortical dysplasia (n = 68, 51%), followed by low-grade neoplasm (n = 16, 12%). In the literature, seizure freedom was noted in 60% of pediatric and 69% of adult patients at a median follow-up of 29 months (75% and 50%, respectively, in the current series). A neurological deficit occurred in 43% of cases (10% permanent), with extremity paresis comprising the most common deficit (n = 35, 21%), followed by facial paresis (n = 32, 19%). Language deficits were more common in left-sided approaches (24% vs 2%, p < 0.001). Univariate analysis for seizure freedom revealed a significantly higher proportion of patients with lesional epilepsy among those with at least 12 months of follow-up (77% vs 59%, p = 0.032).

CONCLUSIONS

These findings may serve as a benchmark when tailoring decision-making for insular epilepsy, and may assist surgeons in their preoperative discussions with patients. Although seizure freedom rates are quite high with insular epilepsy treatment, the associated morbidity needs to be weighed against the potential for seizure freedom.

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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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Chronic subthreshold cortical stimulation for adult drug-resistant focal epilepsy: safety, feasibility, and technique

Panagiotis Kerezoudis, Sanjeet S. Grewal, Matthew Stead, Brian Nils Lundstrom, Jeffrey W. Britton, Cheolsu Shin, Gregory D. Cascino, Benjamin H. Brinkmann, Gregory A. Worrell, and Jamie J. Van Gompel

OBJECTIVE

Epilepsy surgery is effective for lesional epilepsy, but it can be associated with significant morbidity when seizures originate from eloquent cortex that is resected. Here, the objective was to describe chronic subthreshold cortical stimulation and evaluate its early surgical safety profile in adult patients with epilepsy originating from seizure foci in cortex that is not amenable to resection.

METHODS

Adult patients with focal drug-resistant epilepsy underwent intracranial electroencephalography monitoring for evaluation of resection. Those with seizure foci in eloquent cortex were not candidates for resection and were offered a short therapeutic trial of continuous subthreshold cortical stimulation via intracranial monitoring electrodes. After a successful trial, electrodes were explanted and permanent stimulation hardware was implanted.

RESULTS

Ten patients (6 males) who underwent chronic subthreshold cortical stimulation between 2014 and 2016 were included. Based on radiographic imaging, intracranial pathologies included cortical dysplasia (n = 3), encephalomalacia (n = 3), cortical tubers (n = 1), Rasmussen encephalitis (n = 1), and linear migrational anomaly (n = 1). The duration of intracranial monitoring ranged from 3 to 20 days. All patients experienced an uneventful postoperative course and were discharged home with a median length of stay of 10 days. No postoperative surgical complications developed (median follow-up length 7.7 months). Seizure severity and seizure frequency improved in all patients.

CONCLUSIONS

The authors’ institutional experience with this small group shows that chronic subthreshold cortical stimulation can be safely and effectively performed in appropriately selected patients without postoperative complications. Future investigation will provide further insight to recently published results regarding mechanism and efficacy of this novel and promising intervention.