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Research Original Investigation Interictal Scalp Electroencephalography and Intraoperative Electrocorticography in Magnetic Resonance Imaging–Negative Temporal Lobe Epilepsy Surgery David B. Burkholder, MD; Vlastimil Sulc, MD; E. Matthew Hoffman, DO, PhD; Gregory D. Cascino, MD; Jeffrey W. Britton, MD; Elson L. So, MD; W. Richard Marsh, MD; Fredric B. Meyer, MD; Jamie J. Van Gompel, MD; Caterina Giannini, MD, PhD; C. Thomas Wass, MD; Robert E. Watson Jr, MD, PhD; Gregory A. Worrell, MD, PhD Editorial page 681 IMPORTANCE Scalp electroencephalography (EEG) and intraoperative electrocorticography Supplemental content at (ECoG) are routinely used in the evaluation of magnetic resonance imaging–negative jamaneurology.com temporal lobe epilepsy (TLE) undergoing standard anterior temporal lobectomy with CME Quiz at amygdalohippocampectomy (ATL), but the utility of interictal epileptiform discharge (IED) jamanetworkcme.com identification and its role in outcome are poorly defined. OBJECTIVES To determine whether the following are associated with surgical outcomes in patients with magnetic resonance imaging–negative TLE who underwent standard ATL: (1) unilateral-only IEDs on preoperative scalp EEG; (2) complete resection of tissue generating IEDs on ECoG; (3) complete resection of opioid-induced IEDs recorded on ECoG; and (4) location of IEDs recorded on ECoG. DESIGN, SETTING, AND PARTICIPANTS Data were gathered through retrospective medical record review at a tertiary referral center. Adult and pediatric patients with TLE who underwent standard ATL between January 1, 1990, and October 15, 2010, were considered for inclusion. Inclusion criteria were magnetic resonance imaging–negative TLE, standard ECoG performed at the time of surgery, and a minimum follow-up of 12 months. Univariate analysis was performed using log-rank time-to-event analysis. Variables reaching significance with log-rank testing were further analyzed using Cox proportional hazards. MAIN OUTCOMES AND MEASURES Excellent or nonexcellent outcome at time of last follow-up. An excellent outcome was defined as Engel class I and a nonexcellent outcome as Engel classes II through IV. RESULTS Eighty-seven patients met inclusion criteria, with 48 (55%) achieving an excellent outcome following ATL. Unilateral IEDs on scalp EEG (P = .001) and complete resection of Author Affiliations: Department of Neurology, Mayo Clinic, Rochester, brain regions generating IEDs on baseline intraoperative ECoG (P = .02) were associated with Minnesota (Burkholder, Sulc, excellent outcomes in univariate analysis. Both were associated with excellent outcomes Hoffman, Cascino, Britton, So, when analyzed with Cox proportional hazards (unilateral-only IEDs, relative risk = 0.31 Worrell); International Clinical Research Center, St. Anne’s [95% CI, 0.16-0.64]; complete resection of IEDs on baseline ECoG, relative risk = 0.39 University Hospital, Brno, Czech [95% CI, 0.20-0.76]). Overall, 25 of 35 patients (71%) with both unilateral-only IEDs and Republic (Sulc); Department of complete resection of baseline ECoG IEDs had an excellent outcome. Neurologic Surgery, Mayo Clinic, Rochester, Minnesota (Marsh, Meyer, Van Gompel); Department of CONCLUSIONS AND RELEVANCE Unilateral-only IEDs on preoperative scalp EEG and complete Pathology, Mayo Clinic, Rochester, resection of IEDs on baseline ECoG are associated with better outcomes following standard Minnesota (Giannini); Department ATL in magnetic resonance imaging–negative TLE. Prospective evaluation is needed to clarify of Anesthesiology, Mayo Clinic, Rochester, Minnesota (Wass); the use of ECoG in tailoring temporal lobectomy. Department of Radiology, Mayo Clinic, Rochester, Minnesota (Watson); Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, Minnesota (Worrell). Corresponding Author: Gregory A. Worrell, MD, PhD, Department of Neurology, Mayo Clinic, 200 First St JAMA Neurol. 2014;71(6):702-709. doi:10.1001/jamaneurol.2014.585 SW, Rochester, MN 55905 Published online April 28, 2014. ([email protected]). 702 jamaneurology.com Copyright 2014 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 MRI-Negative Temporal Lobe Epilepsy Surgery Original Investigation Research he prognosis for surgery in magnetic resonance Figure 1. Patient Selection Process Through the Mayo Clinic Epilepsy imaging (MRI)–negative temporal lobe epilepsy (TLE) Surgery Database T is less favorable than lesional epilepsy. Previous stud- ies demonstrate a favorable postoperative outcome in 36% to 1289 Patients with epilepsy 76% of patients with MRI-negative TLE.1-8 Many factors have and ECoG or iEEG been associated with a favorable outcome in MRI-negative 1,4,9-11 Excluded: TLE, but there has been little improvement in postop- 844 Lesional MRI erative outcomes.12,13 Both scalp and intracranial electroen- 101 Previous surgery 147 Extratemporal cephalography (EEG) play an important role in the selection of surgical candidates. While unilateral or localized ictal onset 197 on scalp EEG has been associated with good outcomes,11,14 Patients with MRI-negative temporal lobe epilepsy the role of interictal epileptiform discharges (IEDs) in out- comes is less clear. Intraoperative electrocorticography (ECoG) is commonly 90 107 performed prior to resection at comprehensive epilepsy cen- Unilateral temporal seizure Prolonged iEEG onset on scalp EEG, surgery monitoring performed ters. However, its prognostic value in TLE surgery is unclear. performed immediately Some data suggest ECoG may be useful in tailoring the surgi- 15-17 Excluded: cal approach or in selecting patients who may be able to 49 Excluded: Surgery not performed 23 bypass prolonged intracranial monitoring and proceed to 22 Inadequate follow-up Bilateral onset surgery.15 Other studies have not supported its use in the evalu- 16 Poorly localized onset 7 Patients refused surgery 18,19 ation or prognosis of surgical patients with TLE. The use 2 Eloquent onset 1 of ECoG in epilepsy surgery specifically for MRI-negative TLE Multifocal onset 87 Total included 27 Nonstandard ECoG has not been extensively evaluated. Most studies have fo- patients 12 Modified surgery cused on ECoG in lesional epilepsy including mesial tempo- 17,20,21 ral sclerosis (MTS), contained heterogeneous patient ECoG indicates electrocorticography; EEG, electroencephalography; groups,9,16-18,22 or involved relatively small numbers of iEEG, intraoperative electroencephalography; and MRI, magnetic resonance patients.10,15 imaging. To clarify the role of interictal EEG and intraoperative ECoG in the surgical management of MRI-negative TLE, we per- formed a multivariate analysis of 4 EEG findings and surgical longed intracranial monitoring, regardless of laterality. Pa- outcomes in this population, including unilateral-only or bi- tients with poorly localized or indeterminate seizure onset or lateral independent IEDs on preoperative scalp EEG, com- with semiology concerning for eloquent cortex involvement plete resection of baseline ECoG IEDs, complete resection of underwent prolonged intracranial EEG monitoring. Patients opioid-induced ECoG IEDs, and location of ECoG IEDs. were excluded if they underwent surgery without standard in- traoperative ECoG, regardless of other testing. All data were obtained through retrospective medical record review.Data col- Methods lected included sex, age at epilepsy onset, age at surgery, his- tory of febrile seizures in childhood, days monitored with scalp Patients EEG, pursuit of intracranial monitoring, side of seizure focus Approval for this study was obtained from the Mayo Clinic In- and resection, cortical resection size, time of seizure recur- stitutional Review Board. Patients who underwent compre- rence, and time of last follow-up. Electrophysiological data in- hensive epilepsy evaluation between January 1, 1990, and Oc- cluded the presence of unilateral-only or bilateral indepen- tober 15, 2010, were identified from the Mayo Clinic Epilepsy dent IEDs on presurgical scalp EEG, active contacts during Surgery Database (Figure 1). Informed consent was waived ow- baseline ECoG, active contacts during opioid-induced ECoG, ing to the retrospective design of the study. Adult and pediat- and location of ECoG IEDs (mesial only, mesiolateral, or lat- ric patients were included if they had medically resistant TLE, eral neocortex only). normal MRI findings, no prior neurologic surgery, standard- ized ECoG at the time of surgery, and at least 12 months of post- Imaging operative follow-up. Follow-up included any office visit or di- A standard epilepsy protocol was performed on all patients rect correspondence from the patient (telephone call or written using 1.5-T or 3-T MRI scanners. These included 4-mm coro- correspondence) documented in the medical record that out- nal fluid-attenuated inversion recovery and high-resolution lined the patient’s seizure outcome. All patients underwent a 1.6-mm T1-weighted slices cut perpendicularly through the hip- comprehensive evaluation including a seizure-protocol MRI, pocampal axis and standard T2-weighted sequences. Quanti- prolonged scalp EEG monitoring, and preneuropsychological tative hippocampal volumes were performed on patients with and postneuropsychological assessment. For most of the study suspected subtle hippocampal atrophy.23 Imaging was re- period, patients with unilateral temporal lobe seizure onset on viewed at the time it was performed by board-certified neu- scalp EEG and semiology not suggestive
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