High‐frequency oscillations mirror severity of human temporal lobe seizures

Abstract Objective Many patients with epilepsy have both focal and bilateral tonic‐clonic seizures (BTCSs), but it is largely unclear why ictal activity spreads only sometimes. Previous work indicates that interictal high‐frequency oscillations (HFOs), traditionally subdivided into ripples (80–250 H...

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Main Authors: Jan Schönberger, Nadja Birk, Daniel Lachner‐Piza, Matthias Dümpelmann, Andreas Schulze‐Bonhage, Julia Jacobs
Format: Article
Language:English
Published: Wiley 2019-12-01
Series:Annals of Clinical and Translational Neurology
Online Access:https://doi.org/10.1002/acn3.50941
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author Jan Schönberger
Nadja Birk
Daniel Lachner‐Piza
Matthias Dümpelmann
Andreas Schulze‐Bonhage
Julia Jacobs
author_facet Jan Schönberger
Nadja Birk
Daniel Lachner‐Piza
Matthias Dümpelmann
Andreas Schulze‐Bonhage
Julia Jacobs
author_sort Jan Schönberger
collection DOAJ
description Abstract Objective Many patients with epilepsy have both focal and bilateral tonic‐clonic seizures (BTCSs), but it is largely unclear why ictal activity spreads only sometimes. Previous work indicates that interictal high‐frequency oscillations (HFOs), traditionally subdivided into ripples (80–250 Hz) and fast ripples (250–500 Hz), are a promising biomarker of epileptogenicity. We aimed to investigate whether HFOs correlate with the emergence of seizure activity and whether they differ between focal seizures (FSs) with impaired awareness and BTCSs. Methods We retrospectively analyzed 15 FSs and 13 BTCSs from seven patients with mesial temporal lobe epilepsy, each of them with at least one BTCS and at least one FS. Representative intervals of intracranial electroencephalography from the seizure onset zone (SOZ) and remote non‐SOZ areas were selected to compare pre‐ictal, complex focal, tonic‐clonic, and postictal periods. Ripples and fast ripples were visually identified and their density, that is, percentage of time occupied by the respective events, computed. Results Ripple and fast ripple densities increased inside the SOZ after seizure onset (P < 0.01) and in remote areas after progression to BTCSs (P < 0.01). Postictal SOZ ripple density dropped below pre‐ictal levels (P < 0.001). Prior to onset of bilateral tonic‐clonic movements, ripple density inside the SOZ is higher in BTCSs than in FSs (P < 0.05). Interpretation Ripples and fast ripples correlate with onset and spread of ictal activity. Abundant ripples inside the SOZ may reflect the activation of specific neuronal networks related to imminent spread of seizure activity.
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spelling doaj.art-586d040ae9724e17b33ae56630dc1fdd2022-12-21T22:25:24ZengWileyAnnals of Clinical and Translational Neurology2328-95032019-12-016122479248810.1002/acn3.50941High‐frequency oscillations mirror severity of human temporal lobe seizuresJan Schönberger0Nadja Birk1Daniel Lachner‐Piza2Matthias Dümpelmann3Andreas Schulze‐Bonhage4Julia Jacobs5Universitätsklinikum Freiburg Epilepsiezentrum Breisacher Straße 64 79106 Freiburg im Breisgau GermanyUniversitätsklinikum Freiburg Epilepsiezentrum Breisacher Straße 64 79106 Freiburg im Breisgau GermanyUniversitätsklinikum Freiburg Epilepsiezentrum Breisacher Straße 64 79106 Freiburg im Breisgau GermanyUniversitätsklinikum Freiburg Epilepsiezentrum Breisacher Straße 64 79106 Freiburg im Breisgau GermanyUniversitätsklinikum Freiburg Epilepsiezentrum Breisacher Straße 64 79106 Freiburg im Breisgau GermanyUniversitätsklinikum Freiburg Epilepsiezentrum Breisacher Straße 64 79106 Freiburg im Breisgau GermanyAbstract Objective Many patients with epilepsy have both focal and bilateral tonic‐clonic seizures (BTCSs), but it is largely unclear why ictal activity spreads only sometimes. Previous work indicates that interictal high‐frequency oscillations (HFOs), traditionally subdivided into ripples (80–250 Hz) and fast ripples (250–500 Hz), are a promising biomarker of epileptogenicity. We aimed to investigate whether HFOs correlate with the emergence of seizure activity and whether they differ between focal seizures (FSs) with impaired awareness and BTCSs. Methods We retrospectively analyzed 15 FSs and 13 BTCSs from seven patients with mesial temporal lobe epilepsy, each of them with at least one BTCS and at least one FS. Representative intervals of intracranial electroencephalography from the seizure onset zone (SOZ) and remote non‐SOZ areas were selected to compare pre‐ictal, complex focal, tonic‐clonic, and postictal periods. Ripples and fast ripples were visually identified and their density, that is, percentage of time occupied by the respective events, computed. Results Ripple and fast ripple densities increased inside the SOZ after seizure onset (P < 0.01) and in remote areas after progression to BTCSs (P < 0.01). Postictal SOZ ripple density dropped below pre‐ictal levels (P < 0.001). Prior to onset of bilateral tonic‐clonic movements, ripple density inside the SOZ is higher in BTCSs than in FSs (P < 0.05). Interpretation Ripples and fast ripples correlate with onset and spread of ictal activity. Abundant ripples inside the SOZ may reflect the activation of specific neuronal networks related to imminent spread of seizure activity.https://doi.org/10.1002/acn3.50941
spellingShingle Jan Schönberger
Nadja Birk
Daniel Lachner‐Piza
Matthias Dümpelmann
Andreas Schulze‐Bonhage
Julia Jacobs
High‐frequency oscillations mirror severity of human temporal lobe seizures
Annals of Clinical and Translational Neurology
title High‐frequency oscillations mirror severity of human temporal lobe seizures
title_full High‐frequency oscillations mirror severity of human temporal lobe seizures
title_fullStr High‐frequency oscillations mirror severity of human temporal lobe seizures
title_full_unstemmed High‐frequency oscillations mirror severity of human temporal lobe seizures
title_short High‐frequency oscillations mirror severity of human temporal lobe seizures
title_sort high frequency oscillations mirror severity of human temporal lobe seizures
url https://doi.org/10.1002/acn3.50941
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