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Original Investigation |

Interictal Scalp Electroencephalography and Intraoperative Electrocorticography in Magnetic Resonance Imaging–Negative Temporal Lobe Epilepsy Surgery

David B. Burkholder, MD1; Vlastimil Sulc, MD1,2; E. Matthew Hoffman, DO, PhD1; Gregory D. Cascino, MD1; Jeffrey W. Britton, MD1; Elson L. So, MD1; W. Richard Marsh, MD3; Fredric B. Meyer, MD3; Jamie J. Van Gompel, MD3; Caterina Giannini, MD, PhD4; C. Thomas Wass, MD5; Robert E. Watson Jr, MD, PhD6; Gregory A. Worrell, MD, PhD1,7
[+] Author Affiliations
1Department of Neurology, Mayo Clinic, Rochester, Minnesota
2International Clinical Research Center, St. Anne’s University Hospital, Brno, Czech Republic
3Department of Neurologic Surgery, Mayo Clinic, Rochester, Minnesota
4Department of Pathology, Mayo Clinic, Rochester, Minnesota
5Department of Anesthesiology, Mayo Clinic, Rochester, Minnesota
6Department of Radiology, Mayo Clinic, Rochester, Minnesota
7Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, Minnesota
JAMA Neurol. 2014;71(6):702-709. doi:10.1001/jamaneurol.2014.585.
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Importance  Scalp electroencephalography (EEG) and intraoperative electrocorticography (ECoG) are routinely used in the evaluation of magnetic resonance imaging–negative temporal lobe epilepsy (TLE) undergoing standard anterior temporal lobectomy with amygdalohippocampectomy (ATL), but the utility of interictal epileptiform discharge (IED) 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 brain regions generating IEDs on baseline intraoperative ECoG (P = .02) were associated with excellent outcomes in univariate analysis. Both were associated with excellent outcomes when analyzed with Cox proportional hazards (unilateral-only IEDs, relative risk = 0.31 [95% CI, 0.16-0.64]; complete resection of IEDs on baseline ECoG, relative risk = 0.39 [95% CI, 0.20-0.76]). Overall, 25 of 35 patients (71%) with both unilateral-only IEDs and complete resection of baseline ECoG IEDs had an excellent outcome.

Conclusions and Relevance  Unilateral-only IEDs on preoperative scalp EEG and complete resection of IEDs on baseline ECoG are associated with better outcomes following standard ATL in magnetic resonance imaging–negative TLE. Prospective evaluation is needed to clarify the use of ECoG in tailoring temporal lobectomy.

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Figure 1.
Patient Selection Process Through the Mayo Clinic Epilepsy Surgery Database

ECoG indicates electrocorticography; EEG, electroencephalography; iEEG, intraoperative electroencephalography; and MRI, magnetic resonance imaging.

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Figure 2.
Intraoperative Electrocorticography and Anterior Temporal Lobectomy

A, Schematic of standardized electrode configuration for intraoperative electrocorticography in patients undergoing anterior temporal lobectomy. Dashed lines indicate cortical resections at 30 mm (a), 40 mm (b), and 50 mm (c). B, Intraoperative electrocorticography recording. IFS indicates the 8-contact strip electrode used to record from the inferior frontal gyrus; ITS, the 8-contact strip electrode used to record from the inferior temporal gyrus; and STS, the 8-contact strip electrode used to record from the superior temporal gyrus. C, Schematic of standard anterior temporal lobectomy performed in all patients. The extent of lateral neocortical resection for the dominant and nondominant temporal lobe is shown. The mesial temporal structures, amygdala, hippocampus, and parahippocampus are also resected.

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Figure 3.
Log-Rank Kaplan-Meier Curves of Excellent Outcome Proportions

A, Bilateral independent interictal epileptiform discharges (IEDs) on scalp electroencephalography. B, Baseline electrocorticography (ECoG) IED resection, complete vs incomplete. C, Opioid-induced ECoG IED resection, complete vs incomplete. D, Location of ECoG IEDs, mesial only vs mesiolateral or lateral only.

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