Neural Fragility as an EEG Marker of the Seizure Onset Zone

AbstractOver 15 million epilepsy patients worldwide do not respond to drugs. Successful surgical treatment requires complete removal, or disconnection of the seizure onset zone (SOZ), brain region(s) where seizures originate. Unfortunately, surgical success rates vary between 30%-70% because no clinically validated biological marker of the SOZ exists. We develop and retrospectively validate a new EEG marker - neural fragility. We validate this new marker in a retrospective analysis of 91 patients by using neural fragility of the annotated SOZ as a metric to predict surgical outcomes. Fragility predicts 43/47 surgical failures with an overall prediction accuracy of 76%, compared to the accuracy of clinicians being 48% (successful outcomes). In failed outcomes, we identify fragile regions that were untreated. When compared to 20 EEG features proposed as SOZ markers, fragility outperformed in predictive power and interpretability suggesting neural fragility as an EEG fingerprint of the SOZ.One Sentence SummaryNeural fragility, an intracranial EEG biomarker for the seizure onset zone in drug-resistant epilepsy, predicts surgical outcomes with high accuracy.

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A novel HFO-based method for unsupervised localization of the seizure onset zone in drug-resistant epilepsy

2017 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) ◽

10.1109/embc.2017.8037008 ◽

2017 ◽

Cited By ~ 5

Author(s):

Paige M. Murphy ◽

Adam J. von Paternos ◽

Sabato Santaniello

Keyword(s):

Drug Resistant ◽

Seizure Onset ◽

Seizure Onset Zone ◽

Drug Resistant Epilepsy

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Comparison of Ictal Brain Perfusion SPECT With 99mTc-HMPAO Versus 99mTc-ECD for Identification of The Epileptic Seizure Onset Zone

10.21203/rs.3.rs-104415/v1 ◽

2020 ◽

Author(s):

Mariam Jaber ◽

Jila Taherpour ◽

Berthold Voges ◽

Ivayla Apostolova ◽

Thomas Sauvigny ◽

...

Keyword(s):

Brain Perfusion ◽

Drug Resistant ◽

Seizure Onset ◽

Tracer Injection ◽

Brain Perfusion Spect ◽

Temporal Epilepsy ◽

Large Patient ◽

Seizure Onset Zone ◽

Perfusion Spect ◽

Drug Resistant Epilepsy

Abstract Background: The chemical microspheres 99mTc-HMPAO and 99mTc-ECD are widely used as tracers in ictal brain perfusion SPECT for identification of the seizure onset zone (SOZ) in presurgical evaluation of patients with drug-resistant epilepsy and uncertainty of SOZ localization after standard diagnostic workup. For both tracers there are theoretical arguments to favor it over the other for this task. The aim of this study was to compare the performance of ictal brain perfusion SPECT between 99mTc-HMPAO and 99mTc-ECD in a rather large patient sample.Methods: The study retrospectively included 196 patients from clinical routine in whom ictal perfusion SPECT had been performed with stabilized 99mTc-HMPAO (n = 110) or 99mTc-ECD (n = 86). Lateralization and localization of the SOZ was obtained by the consensus of two independent readers who visually inspected the SPECT images retrospectively. Results: The 99mTc-HMPAO group and the 99mTc-ECD group were well matched with respect to age, sex, age at first seizure, duration of disease, seizure frequency, history of previous brain surgery, and findings of presurgical MRI. The tracer groups differed significantly with respect to the latency of tracer injection (median latency 4 s longer in the 99mTc-HMPAO group), duration of the seizure after tracer injection (25 s shorter in the 99mTc-HMPAO group), tracer dose (70 MBq higher in the 99mTc-HMPAO group), and delay of the SPECT acquisition after tracer injection (63 min longer in the 99mTc-HMPAO group). The fraction of lateralising ictal SPECT did not differ significantly between the 99mTc-HMPAO and the 99mTc-ECD group (65.5% versus 72.1%, p = 0.355). Sensitivity of ictal perfusion SPECT (independent of the tracer) for correct localization of the SOZ in 62 patients with temporal lobe epilepsy and at least worthwhile improvement (Engel scale ≤ III) 12 months after temporal epilepsy surgery was 63%.Conclusions: This study does not provide evidence to favor 99mTc-HMPAO or 99mTc-ECD for identification of the SOZ by ictal perfusion SPECT in patients with drug resistant epilepsy.

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A probabilistic approach for lateralization of seizure onset zone in drug-resistant epilepsy with bilateral cerebral pathology

Mathematical Biosciences ◽

10.1016/j.mbs.2016.04.006 ◽

2016 ◽

Vol 277 ◽

pp. 136-140

Author(s):

Ravindra Arya ◽

Siva Sivaganesan ◽

Katherine D. Holland ◽

Hansel M. Greiner ◽

Francesco T. Mangano ◽

...

Keyword(s):

Probabilistic Approach ◽

Drug Resistant ◽

Seizure Onset ◽

Seizure Onset Zone ◽

Cerebral Pathology ◽

Drug Resistant Epilepsy

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Interictal SEEG resting-state connectivity localizes seizure onset zone and predicts seizure outcome

10.1101/2021.12.30.21268524 ◽

2022 ◽

Author(s):

Haiteng Jiang ◽

Vasileios Kokkinos ◽

Shuai Ye ◽

Alexandra Urban ◽

Anto Bagic ◽

...

Keyword(s):

Information Flow ◽

Resting State ◽

Inhibitory Input ◽

Seizure Outcome ◽

Epileptogenic Zone ◽

Drug Resistant ◽

Seizure Onset ◽

Seizure Onset Zone ◽

Drug Resistant Epilepsy ◽

Resting State Connectivity

Stereotactic-electroencephalography (SEEG) is a common neurosurgical method to localize epileptogenic zone in drug resistant epilepsy patients and inform treatment recommendations. In the current clinical practice, localization of epileptogenic zone typically requires prolonged recordings to capture seizure, which may take days to weeks. Although epilepsy surgery has been proven to be effective in general, the percentage of unsatisfactory seizure outcomes is still concerning. We developed a method to identify the seizure onset zone (SOZ) and predict seizure outcome using short-time resting-state SEEG data. In a cohort of 43 drug resistant epilepsy patients, we estimated the information flow via directional connectivity and inferred the excitation-inhibition ratio from the 1/f power slope. We hypothesized that the antagonism of information flow at multiple frequencies between SOZ and non-SOZ underlying the relatively stable epilepsy resting state could be related to the disrupted excitation-inhibition balance. We found higher excitability in non-SOZ regions compared to the SOZ, with dominant information flow from non-SOZ to SOZ regions, probably reflecting inhibitory input from non-SOZ to prevent seizure initiation. Greater differences in information flow between SOZ and non-SOZ regions were associated with favorable seizure outcome. By integrating a balanced random forest model with resting-state connectivity, our method localized the SOZ with an accuracy of 85% and predicted the seizure outcome with an accuracy of 77% using clinically determined SOZ. Overall, our study suggests that brief resting-state SEEG data can significantly facilitate the identification of SOZ and may eventually predict seizure outcomes without requiring long-term ictal recordings.

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EEG source connectivity to localize the seizure onset zone in patients with drug resistant epilepsy

NeuroImage Clinical ◽

10.1016/j.nicl.2017.09.011 ◽

2017 ◽

Vol 16 ◽

pp. 689-698 ◽

Cited By ~ 27

Author(s):

Willeke Staljanssens ◽

Gregor Strobbe ◽

Roel Van Holen ◽

Vincent Keereman ◽

Stefanie Gadeyne ◽

...

Keyword(s):

Drug Resistant ◽

Seizure Onset ◽

Seizure Onset Zone ◽

Drug Resistant Epilepsy

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Intracranial EEG seizure onset-patterns correlate with high-frequency oscillations in patients with drug-resistant epilepsy

Epilepsy Research ◽

10.1016/j.eplepsyres.2016.09.009 ◽

2016 ◽

Vol 127 ◽

pp. 200-206 ◽

Cited By ~ 14

Author(s):

Taissa Ferrari-Marinho ◽

Piero Perucca ◽

Francois Dubeau ◽

Jean Gotman

Keyword(s):

High Frequency ◽

Drug Resistant ◽

Seizure Onset ◽

Intracranial Eeg ◽

High Frequency Oscillations ◽

Drug Resistant Epilepsy

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Overnight ictal magnetoencephalography

Neurology Clinical Practice ◽

10.1212/cpj.0000000000000937 ◽

2020 ◽

pp. 10.1212/CPJ.0000000000000937

Author(s):

Jeremy T. Moreau ◽

Elisabeth Simard-Tremblay ◽

Steffen Albrecht ◽

Bernard Rosenblatt ◽

Sylvain Baillet ◽

...

Keyword(s):

Epileptic Activity ◽

Added Value ◽

Drug Resistant ◽

Seizure Onset ◽

Presurgical Evaluation ◽

Seizure Onset Zone ◽

Drug Resistant Epilepsy

The added value of magnetoencephalography (MEG) in the presurgical evaluation for drug-resistant epilepsy is well-recognised 1-4. However, MEG remains mostly limited to analysis of interictal epileptic activity 1,5. Seizures are uncommonly captured due to logistical considerations despite mounting evidence of the value of ictal MEG in localising the seizure onset zone 5-7. Here we report the recording and analysis of ictal MEG recordings in two drug-resistant epilepsy presurgical candidates that spent a night sleeping in the MEG.

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Extratemporal surface EEG features do not preclude successful surgical outcomes in drug-resistant epilepsy patients with unitemporal MRI lesions

Epileptic Disorders ◽

10.1684/epd.2012.0527 ◽

2012 ◽

Vol 14 (3) ◽

pp. 275-289 ◽

Cited By ~ 3

Author(s):

Kyriakos Garganis ◽

Vasileios Kokkinos ◽

Basilios Zountsas

Keyword(s):

Surgical Outcomes ◽

Drug Resistant ◽

Drug Resistant Epilepsy ◽

Surface Eeg ◽

Eeg Features

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Influence of Time-Series Normalization, Number of Nodes, Connectivity and Graph Measure Selection on Seizure-Onset Zone Localization from Intracranial EEG

Brain Topography ◽

10.1007/s10548-018-0646-7 ◽

2018 ◽

Vol 31 (5) ◽

pp. 753-766 ◽

Cited By ~ 5

Author(s):

Pieter van Mierlo ◽

Octavian Lie ◽

Willeke Staljanssens ◽

Ana Coito ◽

Serge Vulliémoz

Keyword(s):

Time Series ◽

Seizure Onset ◽

Intracranial Eeg ◽

Seizure Onset Zone ◽

Graph Measure

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Spatial variation in high-frequency oscillation rates and amplitudes in intracranial EEG

Neurology ◽

10.1212/wnl.0000000000004998 ◽

2018 ◽

Vol 90 (8) ◽

pp. e639-e646 ◽

Cited By ~ 23

Author(s):

Hari Guragain ◽

Jan Cimbalnik ◽

Matt Stead ◽

David M. Groppe ◽

Brent M. Berry ◽

...

Keyword(s):

High Frequency ◽

Anatomic Variation ◽

Brain Regions ◽

Brain Atlas ◽

Reproducible Research ◽

High Frequency Oscillation ◽

Seizure Onset ◽

Frequency Oscillation ◽

Intracranial Eeg ◽

Seizure Onset Zone

ObjectiveTo assess the variation in baseline and seizure onset zone interictal high-frequency oscillation (HFO) rates and amplitudes across different anatomic brain regions in a large cohort of patients.MethodsSeventy patients who had wide-bandwidth (5 kHz) intracranial EEG (iEEG) recordings during surgical evaluation for drug-resistant epilepsy between 2005 and 2014 who had high-resolution MRI and CT imaging were identified. Discrete HFOs were identified in 2-hour segments of high-quality interictal iEEG data with an automated detector. Electrode locations were determined by coregistering the patient's preoperative MRI with an X-ray CT scan acquired immediately after electrode implantation and correcting electrode locations for postimplant brain shift. The anatomic locations of electrodes were determined using the Desikan-Killiany brain atlas via FreeSurfer. HFO rates and mean amplitudes were measured in seizure onset zone (SOZ) and non-SOZ electrodes, as determined by the clinical iEEG seizure recordings. To promote reproducible research, imaging and iEEG data are made freely available (msel.mayo.edu).ResultsBaseline (non-SOZ) HFO rates and amplitudes vary significantly in different brain structures, and between homologous structures in left and right hemispheres. While HFO rates and amplitudes were significantly higher in SOZ than non-SOZ electrodes when analyzed regardless of contact location, SOZ and non-SOZ HFO rates and amplitudes were not separable in some lobes and structures (e.g., frontal and temporal neocortex).ConclusionsThe anatomic variation in SOZ and non-SOZ HFO rates and amplitudes suggests the need to assess interictal HFO activity relative to anatomically accurate normative standards when using HFOs for presurgical planning.

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