Association of Cortical Stimulation-Induced Seizure With Surgical Outcome in Patients With Focal Drug-Resistant Epilepsy

Abstract

Importance: Cortical stimulation is used during presurgical epilepsy evaluation for functional mapping and for defining the cortical area responsible for seizure generation. Despite wide use of cortical stimulation, the association between cortical stimulation-induced seizures and surgical outcome remains unknown.

Objective: To assess whether removal of the seizure-onset zone resulting from cortical stimulation is associated with a good surgical outcome.

Design, setting, and participants: This cohort study used data from 2 tertiary epilepsy centers: Montreal Neurological Institute in Montreal, Quebec, Canada, and Grenoble-Alpes University Hospital in Grenoble, France. Participants included consecutive patients (n = 103) with focal drug-resistant epilepsy who underwent stereoelectroencephalography between January 1, 2007, and January 1, 2017. Participant selection criteria were cortical stimulation during implantation, subsequent open surgical procedure with a follow-up of 1 or more years, and complete neuroimaging data sets for superimposition between intracranial electrodes and the resection.

Main outcomes and measures: Cortical stimulation-induced typical electroclinical seizures, the volume of the surgical resection, and the percentage of resected electrode contacts inducing a seizure or encompassing the cortical stimulation-informed and spontaneous seizure-onset zones were identified. These measures were correlated with good (Engel class I) and poor (Engel classes II-IV) surgical outcomes. Electroclinical characteristics associated with cortical stimulation-induced seizures were analyzed.

Results: In total, 103 patients were included, of whom 54 (52.4%) were female, and the mean (SD) age was 31 (11) years. Fifty-nine patients (57.3%) had cortical stimulation-induced seizures. The percentage of patients with cortical stimulation-induced electroclinical seizures was higher in the good outcome group than in the poor outcome group (31 of 44 [70.5%] vs 28 of 59 [47.5%]; P = .02). The percentage of the resected contacts encompassing the cortical stimulation-informed seizure-onset zone correlated with surgical outcome (median [range] percentage in good vs poor outcome: 63.2% [0%-100%] vs 33.3% [0%-84.6%]; Spearman ρ = 0.38; P = .003). A similar result was observed for spontaneous seizures (median [range] percentage in good vs poor outcome: 57.1% [0%-100%] vs 32.7% [0%-100%]; Spearman ρ = 0.32; P = .002). Longer elapsed time since the most recent seizure was associated with a higher likelihood of inducing seizures (>24 hours: 64.7% vs <24 hours: 27.3%; P = .04).

Conclusions and relevance: Seizure induction by cortical stimulation appears to identify the epileptic generator as reliably as spontaneous seizures do; this finding might lead to a more time-efficient intracranial presurgical investigation of focal epilepsy as the need to record spontaneous seizures is reduced.

Figure 1.. Patient Selection Flowchart

Incomplete data for most patients meant that the preimplantation, implantation, or postimplantation neuroimaging did not fit the inclusion criteria (slices of <2 mm). The rate of good surgical outcome (Engel class I) was 42.7% in patients included in the study and 41.9% in patients excluded (P = .91). CHUGA indicates Grenoble-Alpes University Hospital; MNI, Montreal Neurological Institute; and SEEG, stereoelectroencephalography.

Figure 2.. Percentages of Resected Volumes in Patients With Good or Poor Surgical Outcome

Comparable results were found for all 3 measures showing statistically significant differences depending on the outcome. CS indicates cortical stimulation. ^aSpearman ρ = 0.32; P = .002. ^bSpearman ρ = 0.38; P = .003. ^cSpearman ρ = 0.40; P < .002.

Figure 3.. Proportion of Resected Contacts in Patients With Good or Poor Surgical Outcome

A, Examples of Engel class I or good surgical outcome in patients 61, 134, 70, and 81. B, Examples of Engel class IV or poor surgical outcome in patients 260, 255, 180, and 231. For each patient, the coronal, sagittal, and axial planes of the presurgical magnetic resonance imaging are shown. The contacts of the seizure-onset zone informed by cortical stimulation are reconstructed as red dots, and the resection cavity is superimposed in white. The examples illustrate that in patients with good surgical outcome, a higher proportion of the contacts were removed compared with patients with poor outcome. The patient on the second row of panel B had a seizure-onset zone that involved both the left frontal and temporal lobes (the contacts are not visible in the selected planes). The decision to perform a left frontal lobe resection was based on clinical considerations. Its outcome at 1-year of follow-up was an Engel class IV.

Figure 4.. Comparison in Outcomes Between Spontaneous Seizure and Cortical Stimulation–Induced Seizure in 2 Patient Examples

A and C, Stereoelectroencephalographic (SEEG) recording of patient 217, who had a good surgical outcome. B and D, SEEG recording of patient 260, with poor surgical outcome. Because of functional limitations, only part of the seizure-onset zone was removed in patient 260, as opposed to patient 217. Blue arrows point to the beginning of the cortical stimulation (CS). Contacts RLa 4-6 in patient 217 and contacts LFug 4-6 in patient 260 were stimulated (using 50 Hz). Even though the seizure-onset patterns show differences, the seizure-inducing channels (labeled in red) were similar. LA indicates left amygdala; LCp, left cingulate posterior; LFug, left fusiform gyrus; LH, left hippocampus; LHp, left hippocampus posterior; LOi, left occipital inferior; LOs, left occipital superior; LPC, left precuneus; RA, right amygdala; RCAg, right angular gyrus; RCSMg, right supramarginal gyrus; RH, right hippocampus; RLa, right lesional anterior; RLp, right lesional posterior; RPs, right parietal superior.