Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions

Abstract To see whether acute intraoperative recordings using stereo EEG (SEEG) electrodes can replace prolonged interictal intracranial EEG (iEEG) recording, making the process more efficient and safer, 10 min of iEEG were recorded following electrode implantation in 16 anesthetized patients, and 1...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Shennan A. Weiss, Richard J. Staba, Ashwini Sharan, Chengyuan Wu, Daniel Rubinstein, Sandhitsu Das, Zachary Waldman, Iren Orosz, Gregory Worrell, Jerome Engel, Michael R. Sperling
Formato: article
Lenguaje:EN
Publicado: Nature Portfolio 2021
Materias:
R
Q
Acceso en línea:https://doaj.org/article/57c5ac49e4a845d1a7cf614214a7d96f
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:57c5ac49e4a845d1a7cf614214a7d96f
record_format dspace
spelling oai:doaj.org-article:57c5ac49e4a845d1a7cf614214a7d96f2021-11-08T10:50:36ZAccuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions10.1038/s41598-021-00894-32045-2322https://doaj.org/article/57c5ac49e4a845d1a7cf614214a7d96f2021-11-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-00894-3https://doaj.org/toc/2045-2322Abstract To see whether acute intraoperative recordings using stereo EEG (SEEG) electrodes can replace prolonged interictal intracranial EEG (iEEG) recording, making the process more efficient and safer, 10 min of iEEG were recorded following electrode implantation in 16 anesthetized patients, and 1–2 days later during non-rapid eye movement (REM) sleep. Ripples on oscillations (RonO, 80–250 Hz), ripples on spikes (RonS), sharp-spikes, fast RonO (fRonO, 250–600 Hz), and fast RonS (fRonS) were semi-automatically detected. HFO power and frequency were compared between the conditions using a generalized linear mixed-effects model. HFO rates were compared using a two-way repeated measures ANOVA with anesthesia type and SOZ as factors. A receiver-operating characteristic (ROC) curve analysis quantified seizure onset zone (SOZ) classification accuracy, and the scalar product was used to assess spatial reliability. Resection of contacts with the highest rate of events was compared with outcome. During sleep, all HFOs, except fRonO, were larger in amplitude compared to intraoperatively (p < 0.01). HFO frequency was also affected (p < 0.01). Anesthesia selection affected HFO and sharp-spike rates. In both conditions combined, sharp-spikes and all HFO subtypes were increased in the SOZ (p < 0.01). However, the increases were larger during the sleep recordings (p < 0.05). The area under the ROC curves for SOZ classification were significantly smaller for intraoperative sharp-spikes, fRonO, and fRonS rates (p < 0.05). HFOs and spikes were only significantly spatially reliable for a subset of the patients (p < 0.05). A failure to resect fRonO areas in the sleep recordings trended the most sensitive and accurate for predicting failure. In summary, HFO morphology is altered by anesthesia. Intraoperative SEEG recordings exhibit increased rates of HFOs in the SOZ, but their spatial distribution can differ from sleep recordings. Recording these biomarkers during non-REM sleep offers a more accurate delineation of the SOZ and possibly the epileptogenic zone.Shennan A. WeissRichard J. StabaAshwini SharanChengyuan WuDaniel RubinsteinSandhitsu DasZachary WaldmanIren OroszGregory WorrellJerome EngelMichael R. SperlingNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-12 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Shennan A. Weiss
Richard J. Staba
Ashwini Sharan
Chengyuan Wu
Daniel Rubinstein
Sandhitsu Das
Zachary Waldman
Iren Orosz
Gregory Worrell
Jerome Engel
Michael R. Sperling
Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
description Abstract To see whether acute intraoperative recordings using stereo EEG (SEEG) electrodes can replace prolonged interictal intracranial EEG (iEEG) recording, making the process more efficient and safer, 10 min of iEEG were recorded following electrode implantation in 16 anesthetized patients, and 1–2 days later during non-rapid eye movement (REM) sleep. Ripples on oscillations (RonO, 80–250 Hz), ripples on spikes (RonS), sharp-spikes, fast RonO (fRonO, 250–600 Hz), and fast RonS (fRonS) were semi-automatically detected. HFO power and frequency were compared between the conditions using a generalized linear mixed-effects model. HFO rates were compared using a two-way repeated measures ANOVA with anesthesia type and SOZ as factors. A receiver-operating characteristic (ROC) curve analysis quantified seizure onset zone (SOZ) classification accuracy, and the scalar product was used to assess spatial reliability. Resection of contacts with the highest rate of events was compared with outcome. During sleep, all HFOs, except fRonO, were larger in amplitude compared to intraoperatively (p < 0.01). HFO frequency was also affected (p < 0.01). Anesthesia selection affected HFO and sharp-spike rates. In both conditions combined, sharp-spikes and all HFO subtypes were increased in the SOZ (p < 0.01). However, the increases were larger during the sleep recordings (p < 0.05). The area under the ROC curves for SOZ classification were significantly smaller for intraoperative sharp-spikes, fRonO, and fRonS rates (p < 0.05). HFOs and spikes were only significantly spatially reliable for a subset of the patients (p < 0.05). A failure to resect fRonO areas in the sleep recordings trended the most sensitive and accurate for predicting failure. In summary, HFO morphology is altered by anesthesia. Intraoperative SEEG recordings exhibit increased rates of HFOs in the SOZ, but their spatial distribution can differ from sleep recordings. Recording these biomarkers during non-REM sleep offers a more accurate delineation of the SOZ and possibly the epileptogenic zone.
format article
author Shennan A. Weiss
Richard J. Staba
Ashwini Sharan
Chengyuan Wu
Daniel Rubinstein
Sandhitsu Das
Zachary Waldman
Iren Orosz
Gregory Worrell
Jerome Engel
Michael R. Sperling
author_facet Shennan A. Weiss
Richard J. Staba
Ashwini Sharan
Chengyuan Wu
Daniel Rubinstein
Sandhitsu Das
Zachary Waldman
Iren Orosz
Gregory Worrell
Jerome Engel
Michael R. Sperling
author_sort Shennan A. Weiss
title Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
title_short Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
title_full Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
title_fullStr Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
title_full_unstemmed Accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
title_sort accuracy of high-frequency oscillations recorded intraoperatively for classification of epileptogenic regions
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/57c5ac49e4a845d1a7cf614214a7d96f
work_keys_str_mv AT shennanaweiss accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT richardjstaba accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT ashwinisharan accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT chengyuanwu accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT danielrubinstein accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT sandhitsudas accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT zacharywaldman accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT irenorosz accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT gregoryworrell accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT jeromeengel accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
AT michaelrsperling accuracyofhighfrequencyoscillationsrecordedintraoperativelyforclassificationofepileptogenicregions
_version_ 1718442618022526976