Resection of ictal high-frequency oscillations leads to favorable surgical outcome in pediatric epilepsy

Abstract

Purpose: Intracranial electroencephalography (EEG) is performed as part of an epilepsy surgery evaluation when noninvasive tests are incongruent or the putative seizure-onset zone is near eloquent cortex. Determining the seizure-onset zone using intracranial EEG has been conventionally based on identification of specific ictal patterns with visual inspection. High-frequency oscillations (HFOs, >80 Hz) have been recognized recently as highly correlated with the epileptogenic zone. However, HFOs can be difficult to detect because of their low amplitude. Therefore, the prevalence of ictal HFOs and their role in localization of epileptogenic zone on intracranial EEG are unknown.

Methods: We identified 48 patients who underwent surgical treatment after the surgical evaluation with intracranial EEG, and 44 patients met criteria for this retrospective study. Results were not used in surgical decision making. Intracranial EEG recordings were collected with a sampling rate of 2,000 Hz. Recordings were first inspected visually to determine ictal onset and then analyzed further with time-frequency analysis. Forty-one (93%) of 44 patients had ictal HFOs determined with time-frequency analysis of intracranial EEG.

Key findings: Twenty-two (54%) of the 41 patients with ictal HFOs had complete resection of HFO regions, regardless of frequency bands. Complete resection of HFOs (n = 22) resulted in a seizure-free outcome in 18 (82%) of 22 patients, significantly higher than the seizure-free outcome with incomplete HFO resection (4/19, 21%).

Significance: Our study shows that ictal HFOs are commonly found with intracranial EEG in our population largely of children with cortical dysplasia, and have localizing value. The use of ictal HFOs may add more promising information compared to interictal HFOs because of the evidence of ictal propagation and followed by clinical aspect of seizures. Complete resection of HFOs is a favorable prognostic indicator for surgical outcome.

Figure 1

Nonlesional MRI (normal MRI) case. Ictal onset was followed by immediate spread to symptomatogenic zone in a 13-year-old left-handed girl with seizures since 8 years of age (A: showing partial number of electrodes; 49 of total 96 electrode placement, B1: expanded view of ICEEG at line in A, high-pass filtered at 40Hz; which approximately 250 msec before the clinical seizure onset, reveals the initial appearance of ictal HFO). After applying TFA through 1-min time window TFA analysis for each bandwidth (80–150, 150–300, 300–500 Hz) in 5-min segmentation before the initial seizure onset, HFOs were found (B2: 300–500 Hz, B3: 150–300 Hz) approximately 250 msec preceding clinical seizure onset defined by both video and muscle artifact seen in the electrocardiography electrode. Epilepsia © ILAE

Figure 2

Ictal ICEEG recording showing ictal HFOs (A1) and symptomatogenic onset (high pass, 40 Hz) (B1). Time frequency analysis (TFA) using short-time Fast Fourier Transform (STFT) revealed ictal HFOs (300–500 Hz) localized in anterior mesial frontal (AIH5) and superior-posterior (PIH2) with secondary spread to lateral direction (LAF31, LPF27) (A2, B2). Frequency domain analysis superimposed on the picture of 3D reconstructed interhemispheric strip and intraoperative photo with grid placement showing the propagation of HFOs (A3, B3). 3D reconstructed left hemisphere image showing the intracranial electrodes by coregistration of MRI and post–grid placement CT images (A4, B4). The red (A4) and orange (B4) circle indicate AIH5 and PHI2 electrodes, respectively, as the first electrodes of SOZ, and dark blue (A4) and light blue (B4) indicate LAF31 and LPF27, respectively, as the first electrodes of secondary spreading location. The each area defined by dotted line on A3 and B3 indicate the area of the SOZ and secondary spread area. The yellow lines in A3 and B3 indicate the resection margin. Post, posterior; Ant, anterior. Epilepsia © ILAE