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Tumor-associated epilepsy in patients with brain metastases: necrosis-to-tumor ratio forecasts postoperative seizure freedom.

ABSTRACT: Surgical resection is highly effective in the treatment of tumor-related epilepsy (TRE) in patients with brain metastases (BM). Nevertheless, some patients suffer from postoperative persistent epilepsy which negatively impacts health-related quality of life. Therefore, early identification of patients with potentially unfavorable seizure outcome after BM resection is important. Patients with TRE that had undergone surgery for BM at the authors' institution between 2013 and 2018 were analyzed with regard to preoperatively identifiable risk factors for unfavorable seizure outcome. Tumor tissue and tumor necrosis ratios were assessed volumetrically. According to the classification of the International League Against Epilepsy (ILAE), seizure outcome was categorized as favorable (ILAE 1) and unfavorable (ILAE 2-6) after 3 months in order to avoid potential interference with adjuvant cancer treatment. Among all 38 patients undergoing neurosurgical treatment for BM with concomitant TRE, 34 patients achieved a favorable seizure outcome (90%). Unfavorable seizure outcome was significantly associated with larger tumor volumes (p = 0.012), a midline shift > 7 mm (p = 0.025), and a necrosis/tumor volume ratio > 0.2 (p = 0.047). The present study identifies preoperatively collectable risk factors for unfavorable seizure outcome in patients with BM and TRE. This might enable to preselect for highly vulnerable patients with postoperative persistent epilepsy who might benefit from accompanying neuro-oncological expertise during further systemical treatment regimes.

SUBMITTER: Bahna M

PROVIDER: S-EPMC8827395 | biostudies-literature | 2022 Feb

REPOSITORIES: biostudies-literature

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Tumor-associated epilepsy in patients with brain metastases: necrosis-to-tumor ratio forecasts postoperative seizure freedom.

Bahna Majd M Heimann Muriel M Bode Christian C Borger Valeri V Eichhorn Lars L Güresir Erdem E Hamed Motaz M Herrlinger Ulrich U Ko Yon-Dschun YD Lehmann Felix F Potthoff Anna-Laura AL Radbruch Alexander A Schaub Christina C Surges Rainer R Weller Johannes J Vatter Hartmut H Schäfer Niklas N Schneider Matthias M Schuss Patrick P

Neurosurgical review 20210514 1

Surgical resection is highly effective in the treatment of tumor-related epilepsy (TRE) in patients with brain metastases (BM). Nevertheless, some patients suffer from postoperative persistent epilepsy which negatively impacts health-related quality of life. Therefore, early identification of patients with potentially unfavorable seizure outcome after BM resection is important. Patients with TRE that had undergone surgery for BM at the authors' institution between 2013 and 2018 were analyzed wit ...[more]

PMID: 33988803

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Project description:Alterations in brain networks may cause the lowering of the seizure threshold and hypersynchronization that underlie the recurrence of unprovoked seizures in epilepsy. The aim of this work is to estimate functional network characteristics, which may help predicting outcome of epilepsy surgery. Twenty patients were studied (11 females, 9 males, mean age 33 years) with scalp-recorded HD-EEG in resting state (eyes closed, no interictal discharges) before intracranial evaluation, which allowed the precise determination of the epileptogenic zone. Dipole source time courses in the brain were estimated using Weighted Minimum Norm Estimate based on HD-EEG signals. Information inflow and outflow of atlas-based brain regions were computed using partial directed connectivity. A set of graph measures for pairwise connections in standard EEG frequency bands was calculated. After epilepsy surgery 10 patients were seizure-free (Engel 1a) and 10 patients continued suffering from seizures (Engel outcome worse than 1a). Inflow of the regions containing the epileptogenic zone in the beta and delta frequency bands was significantly lower in patients who achieved seizure-freedom after surgery, compared with patients who continued to have seizures (p = 0.012, and p = 0.026, respectively). Average path length in the beta frequency band was significantly higher in patients who achieved seizure freedom (p = 0.012). In the delta frequency band, local efficiency and clustering coefficient were significantly higher in patients who achieved seizure freedom (0.033, 0.046). In patients who achieved seizure freedom after surgery, the preoperative analysis of the epileptic network exhibited stronger separation of the region containing the seizure onset zone, with less inflow of information. In contrast, shorter paths within the epileptic network may facilitate hypersynchronous neuronal activity and thus the recurrence of seizures in non-seizure free patients. This study supports the hypothesis that epileptic network properties might help to define suitable candidates for epilepsy surgery.

Project description:ObjectiveSeizure outcomes after brain surgery for drug-resistant epilepsy (DRE) are very heterogeneous and difficult to predict with models utilizing the current clinical, imaging, and electrophysiological variables. In this pilot study, we investigated whether genetic and molecular biomarkers (e.g., genomic, transcriptomic) can provide additional insight into differential response to surgery.MethodsPost-operative seizure-outcomes were collected at last follow-up (>6 months) for 201 adult patients with DRE who underwent surgery between 2004 and 2020. Resected tissue was sent for miRNA sequencing (n = 132) and mRNA sequencing (n = 135). Following the selection of 10 genes (SCN1A, NBEA, PTEN, GABRA1, LGL1, DEPDC5, IL1A, ABCB1, C3, CALHM1), we investigated SNPs in those 10 genes from previously acquired exome sequencing data (n = 106). Logistic regression was performed to test for associations between individual features (mRNAs, miRNAs, and SNPs) and post-operative seizure-outcome with an exploratory FDR P < 0.25 as the threshold for significance. Post-operative time-to-seizure analyses were performed for each SNP using a Cox proportional hazards model.ResultsThe majority of patients (83%) had temporal lobe epilepsy. Mean age at surgery was 38.3 years, and 56% were female. Three SNPs (rs10276036, rs11975994, rs1128503) in multi-drug resistance gene, ABCB1, were associated with post-operative seizure outcomes. Patients with alternate alleles in ABCB1 were more likely to be seizure-free at last follow-up (52-56% reduction in seizure recurrence; FDR P = 0.24). All three SNPs were in linkage disequilibrium and highly correlated with each other. Median post-operative time-to-seizure was 63 months for patients with 2 alternate alleles, 24-33 months with 1 alternate allele, and 10-11 months with 0 alternate alleles. These SNPs improved outcome prediction beyond MRI and sex alone. No independent miRNAs or mRNAs were significantly associated with seizure-outcome (P > 0.05). However, pathway analysis identified "cancer drug resistance by drug efflux" (mir-154 and mir-379) as enriched (P = 0.02), supporting the role of drug response genes in post-operative seizure recurrence.SignificanceABCB1 may have a role in epileptogenesis and surgery outcomes independent of its drug efflux activity necessitating further investigation. SNPs in ABCB1 may serve as independent predictors of post-operative outcome.

Dataset Information

Tumor-associated epilepsy in patients with brain metastases: necrosis-to-tumor ratio forecasts postoperative seizure freedom.

Publications

Tumor-associated epilepsy in patients with brain metastases: necrosis-to-tumor ratio forecasts postoperative seizure freedom.

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