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. 2021 Apr;62(4):997-1004.
doi: 10.1111/epi.16845. Epub 2021 Feb 22.

Can we use intraoperative high-frequency oscillations to guide tumor-related epilepsy surgery?

Nicole E C van Klink  1 , Willemiek J E M Zweiphenning  1 , Cyrille H Ferrier  1 , Peter H Gosselaar  1 , Kai J Miller  1   2 , Eleonora Aronica  3   4 , Kees P J Braun  1 , Maeike Zijlmans  1   4
Affiliations

Can we use intraoperative high-frequency oscillations to guide tumor-related epilepsy surgery?

Nicole E C van Klink et al. Epilepsia. 2021 Apr.

Abstract

Objective: In people with low-grade intrinsic brain tumors, an epileptic focus is often located close to the lesion. High-frequency oscillations (HFOs) in electrocorticography (ECoG) might help to delineate this focus. We investigated the relationship between HFOs and low-grade brain tumors and their potential value for tumor-related epilepsy surgery.

Methods: We analyzed pre- and postresection intraoperative ECoG in 41 patients with refractory epilepsy and a low-grade lesion. Electrodes were designated as overlying the tumor, adjacent resected tissue (peritumoral), or outside the resection bed using magnetic resonance imaging (MRI) and intraoperative photographs. We then used a semiautomated approach to detect HFOs as either ripples (80-250 Hz) or fast ripples (250-500 Hz).

Results: The rate of fast ripples was higher in electrodes covering tumor and peritumoral tissue than outside the resection (p = .04). Mesiotemporal tumors showed more ripples (p = .002), but not more fast ripples (p = .07), than superficial tumors. Rates of fast ripples were higher in glioma and extraventricular neurocytoma than in ganglioglioma or dysembryoplastic neuroepithelial tumor (DNET). The rate of ripples and fast ripples in postresection ECoG was not higher in patients with residual tumor tissue on MRI than those without. The rate of ripples in postresection ECoG was higher in patients with good than bad seizure outcome (p = .03). Fast ripples outside the resection and in post-ECoG seem related to seizure recurrence.

Significance: Fast ripples in intraoperative ECoG can be used to help guide resection in tumor-related epilepsy surgery. Preresection fast ripples occur predominantly in epileptogenic tumor and peritumoral tissue. Fast ripple rates are higher in glioma and extraventricular neurocytoma than in ganglioglioma and DNET.

Keywords: corticography; epilepsy surgery; high-frequency oscillations; tumor-related epilepsy.

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Conflict of interest statement

None of the authors has any conflict of interest to disclose.

Figures

FIGURE 1
FIGURE 1
Example of electrode positions, tumor location (red), and resected area (green) in Patient 64, with a right fronto‐orbital tumor. The tumor and resected volumes were determined from the presurgical fluid‐attenuated inversion recovery magnetic resonance imaging (MRI) and the postsurgical T1 MRI, respectively. The electrode grid was positioned at Recording 1A first. After recording approximately 5 min of continuous background electrocorticogram, the grid was placed on Recording 1B for another 5 min of recording
FIGURE 2
FIGURE 2
Rates of ripple (A) and fast ripples (B) per electrode per minute in preresection electrocorticography in channels located on tumor tissue, on peritumoral tissue, and outside the resection. Patients with a mesiotemporal tumor are shown in green, and those with a superficial tumor shown in blue; average is shown in black. Ripple rates are not significantly different on tumor tissue, on peritumoral tissue, or outside the resection. Fast ripple rates in tumor and peritumoral tissue are higher than outside the resection (*p = .035)
FIGURE 3
FIGURE 3
Boxplots showing rates of ripples (A) and fast ripples (FR; B) per electrode (elec) per minute in preresection electrocorticography in different pathologies. Each box shows the 25th to 75th percentiles, with a thick line at the median. Whiskers point to the highest and lowest values no further than 1.5*interquartile range. Outliers are indicated by dots. The rate of ripples and the rate of FR on tumor were significantly different between the four pathology groups (χ2[3] = 9.47, p = .024 for ripples, χ2[3] = 17.75, p < .001 for FR). Post hoc analysis showed significantly higher rates of FR in extraventricular neurocytoma compared to ganglioglioma and dysembryoplastic neuroepithelial tumor (DNET), and in glioma compared to ganglioglioma
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