Elsevier

Clinical Neurophysiology

Volume 127, Issue 1, January 2016, Pages 238-244
Clinical Neurophysiology

Intracranial EEG analysis in tumor-related epilepsy: Evidence of distant epileptic abnormalities

https://doi.org/10.1016/j.clinph.2015.06.028Get rights and content

Highlights

  • In most patients with TRE, at least part of SOSz lies distant from the tumor.

  • Resection of the brain tumor plus SOSz results in excellent seizure outcome.

  • On iEEG, interictal spikes are most abundant and sharpest in the peritumoral region.

Abstract

Objective

In patients with tumor-related epilepsy (TRE), surgery traditionally focuses on tumor resection; but identification and removal of associated epileptogenic zone may improve seizure outcome. Here, we study spatial relationship of tumor and seizure onset and early spread zone (SOSz). We also perform quantitative analysis of interictal epileptiform activities in patients with both TRE and non-lesional epilepsy in order to better understand the electrophysiological basis of epileptogenesis.

Methods

Twenty-five patients (11 with TRE and 14 with non-lesional epilepsy) underwent staged surgery using intracranial electrodes. Tumors were outlined on MRI and images were coregistered with post-implantation CT images. For each electrode, distance to the nearest tumor margin was measured. Electrodes were categorized based on distance from tumor and involvement in seizure. Quantitative EEG analysis studying frequency, amplitude, power, duration and slope of interictal spikes was performed.

Results

At least part of the SOSz was located beyond 1.5 cm from the tumor margin in 10/11 patients. Interictally, spike frequency and power were higher in the SOSz and spikes near tumor were smaller and less sharp. Interestingly, peritumoral electrodes had the highest spike frequencies and sharpest spikes, indicating greatest degree of epileptic synchrony. A complete resection of the SOSz resulted in excellent seizure outcome.

Conclusions

Seizure onset and early spread often involves brain areas distant from the tumor.

Significance

Utilization of epilepsy surgery approach for TRE may provide better seizure outcome and study of the intracranial EEG may provide insight into pathophysiology of TRE.

Introduction

About 30–50% of patients with brain tumors present with seizures (van Breemen et al., 2007). In patients with intrinsic low-grade gliomas and glioneuronal tumors, the incidence is >90% (Kurzwelly et al., 2010). Seizures can increase morbidity in these patients and hence, there is growing interest in developing methods, which achieve optimal seizure control along with aggressive tumor removal. Complete removal of the lesion results in better seizure control compared to subtotal excision, though not everyone becomes seizure-free (Chang et al., 2008, Englot et al., 2011). In fact, in a comprehensive systematic review of the literature of seizure outcomes in 1181 patients with tumor-related epilepsy (TRE) across 41 studies, only 43% of patients were seizure-free after subtotal tumor resection whereas 79% achieved seizure freedom following gross-total lesionectomy (Englot et al., 2012). Recently, use of tailored resection with intraoperative electrocorticography to identify electrographic abnormalities around tumor margin often yielded improved seizure outcome (Mikuni et al., 2006, Seo and Hong, 2003, Sugano et al., 2007). The prevailing thought is that the immediate peritumoral area shows the most frequent epileptiform activity, possibly due to microscopic tumor infiltration (Mikuni et al., 2006, Rassi-Neto et al., 1999, Weber et al., 1993). Most studies have focused on temporal lobe lesions and electrocorticography restricted to brief intraoperative period done under anesthesia, which may itself alter epileptiform activity.

In the present study, we combined brain tumor resection with a tailored two-stage surgical approach of prolonged extraoperative intracranial EEG (iEEG) monitoring used for epilepsy surgery to investigate the spatial relationship between the tumor and the SOSz. We also performed quantitative EEG (qEEG) analysis of interictal spikes in patients with TRE and compared the spike parameters to patients without lesions.

Section snippets

Patient data and EEG recordings

A total of 25 patients with intractable epilepsy, 11 patients with a primary brain tumor (metastatic brain tumors and suspected high-grade gliomas were excluded) and 14 patients with non-lesional epilepsy undergoing epilepsy surgery during the same time period, were included in the study. All patients underwent a two-staged surgery with implantation of arrays of subdural grids and depth electrodes. Prolonged (usually 5 days) extraoperative iEEG recordings were obtained using a 128-channel

Results

The majority of patients in the study had extratemporal or multilobar seizure onset (6/11 in TRE and 9/14 in non-lesional group). Isolated mesial temporal lobe seizure onset was observed in only 3 patients in TRE group and 2 patients in non-leisonal group. In eleven patients with TRE, a total of 693 intracranial electrodes were implanted (mean: 63; range: 38–96); while in the non-lesional group, a total of 1112 intracranial electrodes were implanted (mean: 79; range: 16–112) (Fig. 1B). In the

TRE overview

Adults with new-onset seizures commonly harbor brain tumors. Certain types of tumors, such as dysembryoplastic neuroepithelial tumors, oligodendrogliomas, and gangliogliomas are more likely to present with TRE (Japp et al., 2013, Mittal et al., 2008, Ruda et al., 2012). Conversely, high-grade neoplasms generally have a lower prevalence of TRE. One possible explanation is that development of seizures is a process that evolves over time and may not become operational in a rapidly-growing tumor.

Conflict of interest

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

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