Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study

Objective: Injury severity after traumatic brain injury (TBI) is a well-established risk factor for the development of post-traumatic epilepsy (PTE). However, whether lesion location influences the susceptibility of seizures and development of PTE longitudinally has yet to be defined. We hypothesize...

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Main Authors: Meral A. Tubi, Evan Lutkenhoff, Manuel Buitrago Blanco, David McArthur, Pablo Villablanca, Benjamin Ellingson, Ramon Diaz-Arrastia, Paul Van Ness, Courtney Real, Vikesh Shrestha, Jerome Engel, Jr., Paul M. Vespa
Format: Article
Language:English
Published: Elsevier 2019-03-01
Series:Neurobiology of Disease
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0969996118301529
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language English
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author Meral A. Tubi
Evan Lutkenhoff
Manuel Buitrago Blanco
David McArthur
Pablo Villablanca
Benjamin Ellingson
Ramon Diaz-Arrastia
Paul Van Ness
Courtney Real
Vikesh Shrestha
Jerome Engel, Jr.
Paul M. Vespa
spellingShingle Meral A. Tubi
Evan Lutkenhoff
Manuel Buitrago Blanco
David McArthur
Pablo Villablanca
Benjamin Ellingson
Ramon Diaz-Arrastia
Paul Van Ness
Courtney Real
Vikesh Shrestha
Jerome Engel, Jr.
Paul M. Vespa
Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study
Neurobiology of Disease
Brain trauma
Post-traumatic epilepsy
Coma
Seizures
Brain atrophy
Status epilepticus
author_facet Meral A. Tubi
Evan Lutkenhoff
Manuel Buitrago Blanco
David McArthur
Pablo Villablanca
Benjamin Ellingson
Ramon Diaz-Arrastia
Paul Van Ness
Courtney Real
Vikesh Shrestha
Jerome Engel, Jr.
Paul M. Vespa
author_sort Meral A. Tubi
title Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study
title_short Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study
title_full Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study
title_fullStr Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study
title_full_unstemmed Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study
title_sort early seizures and temporal lobe trauma predict post-traumatic epilepsy: a longitudinal study
publisher Elsevier
series Neurobiology of Disease
issn 1095-953X
publishDate 2019-03-01
description Objective: Injury severity after traumatic brain injury (TBI) is a well-established risk factor for the development of post-traumatic epilepsy (PTE). However, whether lesion location influences the susceptibility of seizures and development of PTE longitudinally has yet to be defined. We hypothesized that lesion location, specifically in the temporal lobe, would be associated with an increased incidence of both early seizures and PTE. As secondary analysis measures, we assessed the degree of brain atrophy and functional recovery, and performed a between-group analysis, comparing patients who developed PTE with those who did not develop PTE. Methods: We assessed early seizure incidence (n = 90) and longitudinal development of PTE (n = 46) in a prospective convenience sample of patients with moderate-severe TBI. Acutely, patients were monitored with prospective cEEG and a high-resolution Magnetic Resonance Imaging (MRI) scan for lesion location classification. Chronically, patients underwent a high-resolution MRI, clinical assessment, and were longitudinally monitored for development of epilepsy for a minimum of 2 years post-injury. Results: Early seizures, occurring within the first week post-injury, occurred in 26.7% of the patients (n = 90). Within the cohort of subjects who had evidence of early seizures (n = 24), 75% had a hemorrhagic temporal lobe injury on admission. For longitudinal analyses (n = 46), 45.7% of patients developed PTE within a minimum of 2 years post-injury. Within the cohort of subjects who developed PTE (n = 21), 85.7% had a hemorrhagic temporal lobe injury on admission and 38.1% had early (convulsive or non-convulsive) seizures on cEEG monitoring during their acute ICU stay. In a between-group analysis, patients with PTE (n = 21) were more likely than patients who did not develop PTE (n = 25) to have a hemorrhagic temporal lobe injury (p < 0.001), worse functional recovery (p = 0.003), and greater temporal lobe atrophy (p = 0.029). Conclusion: Our results indicate that in a cohort of patients with a moderate-severe TBI, 1) lesion location specificity (e.g. the temporal lobe) is related to both a high incidence of early seizures and longitudinal development of PTE, 2) early seizures, whether convulsive or non-convulsive in nature, are associated with an increased risk for PTE development, and 3) patients who develop PTE have greater chronic temporal lobe atrophy and worse functional outcomes, compared to those who do not develop PTE, despite matched injury severity characteristics. This study provides the foundation for a future prospective study focused on elucidating the mechanisms and risk factors for epileptogenesis.
topic Brain trauma
Post-traumatic epilepsy
Coma
Seizures
Brain atrophy
Status epilepticus
url http://www.sciencedirect.com/science/article/pii/S0969996118301529
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spelling doaj-b806683e22ca4726ab314fcbf945dbe72021-03-22T12:46:35ZengElsevierNeurobiology of Disease1095-953X2019-03-01123115121Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal studyMeral A. Tubi0Evan Lutkenhoff1Manuel Buitrago Blanco2David McArthur3Pablo Villablanca4Benjamin Ellingson5Ramon Diaz-Arrastia6Paul Van Ness7Courtney Real8Vikesh Shrestha9Jerome Engel, Jr.10Paul M. Vespa11Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, USC Keck School of Medicine, United StatesDepartment of Psychology, UCLA, United StatesDavid Geffen School of Medicine at UCLA, United StatesDavid Geffen School of Medicine at UCLA, United StatesDavid Geffen School of Medicine at UCLA, United StatesDavid Geffen School of Medicine at UCLA, United StatesDepartment of Neurology, University of Pennsylvania, United StatesDepartment of Neurology and Neurophysiology, Baylor College of Medicine, United StatesDavid Geffen School of Medicine at UCLA, United StatesDavid Geffen School of Medicine at UCLA, United StatesDavid Geffen School of Medicine at UCLA, United StatesDavid Geffen School of Medicine at UCLA, United States; Corresponding author at: David Geffen School of Medicine at UCLA Healthcare, 757 Westwood Blvd, RR 6236A, Los Angeles, CA 90095, United States.Objective: Injury severity after traumatic brain injury (TBI) is a well-established risk factor for the development of post-traumatic epilepsy (PTE). However, whether lesion location influences the susceptibility of seizures and development of PTE longitudinally has yet to be defined. We hypothesized that lesion location, specifically in the temporal lobe, would be associated with an increased incidence of both early seizures and PTE. As secondary analysis measures, we assessed the degree of brain atrophy and functional recovery, and performed a between-group analysis, comparing patients who developed PTE with those who did not develop PTE. Methods: We assessed early seizure incidence (n = 90) and longitudinal development of PTE (n = 46) in a prospective convenience sample of patients with moderate-severe TBI. Acutely, patients were monitored with prospective cEEG and a high-resolution Magnetic Resonance Imaging (MRI) scan for lesion location classification. Chronically, patients underwent a high-resolution MRI, clinical assessment, and were longitudinally monitored for development of epilepsy for a minimum of 2 years post-injury. Results: Early seizures, occurring within the first week post-injury, occurred in 26.7% of the patients (n = 90). Within the cohort of subjects who had evidence of early seizures (n = 24), 75% had a hemorrhagic temporal lobe injury on admission. For longitudinal analyses (n = 46), 45.7% of patients developed PTE within a minimum of 2 years post-injury. Within the cohort of subjects who developed PTE (n = 21), 85.7% had a hemorrhagic temporal lobe injury on admission and 38.1% had early (convulsive or non-convulsive) seizures on cEEG monitoring during their acute ICU stay. In a between-group analysis, patients with PTE (n = 21) were more likely than patients who did not develop PTE (n = 25) to have a hemorrhagic temporal lobe injury (p < 0.001), worse functional recovery (p = 0.003), and greater temporal lobe atrophy (p = 0.029). Conclusion: Our results indicate that in a cohort of patients with a moderate-severe TBI, 1) lesion location specificity (e.g. the temporal lobe) is related to both a high incidence of early seizures and longitudinal development of PTE, 2) early seizures, whether convulsive or non-convulsive in nature, are associated with an increased risk for PTE development, and 3) patients who develop PTE have greater chronic temporal lobe atrophy and worse functional outcomes, compared to those who do not develop PTE, despite matched injury severity characteristics. This study provides the foundation for a future prospective study focused on elucidating the mechanisms and risk factors for epileptogenesis.http://www.sciencedirect.com/science/article/pii/S0969996118301529Brain traumaPost-traumatic epilepsyComaSeizuresBrain atrophyStatus epilepticus