Early seizures and temporal lobe trauma predict post-traumatic epilepsy

A longitudinal study

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, Paul M. Vespa, EpiBioS4Rx Study Group Investigators, Denes Agoston, Alicia Au, Michael J. Bell, Tom Bleck, Craig Branch, Manuel Buitrago Blanco, Ross Bullock & 41 others Brian T. Burrows, Jan Claassen, Robert Clarke, James Cloyd, Lisa Coles, Karen Crawford, Ramon Diaz-Arrastia, Dominique Duncan, Benjamin Ellingson, Jerome Engel, Brandon Foreman, Aristea Galanopoulou, Emily Gilmore, Grohn Olli, Neil Harris, Jed Hartings, Hirsch Lawrence, Martin Hunn, Nathalie Jette, Leigh Johnston, Nigel Jones, Andres Kanner, David McArthur, Martin Monti, Andrew Morokoff, Solomon Moshe, Wenzhu Mowrey, Terence O'Brien, Kristine O'Phelan, Asla Pitkanen, Rema Raman, Courtney Robertson, Eric Rosenthal, Sandy Shultz, Terrance Snutch, Richard Staba, Arthur Toga, Jack Van Horn, Paul Vespa, Frederick Willyerd, Lara Zimmermann

Research output: Contribution to journalReview ArticleResearchpeer-review

Abstract

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.

Original languageEnglish
Pages (from-to)115-121
Number of pages7
JournalNeurobiology of Disease
Volume123
DOIs
Publication statusPublished - 1 Mar 2019
Externally publishedYes

Keywords

  • Brain atrophy
  • Brain trauma
  • Coma
  • Post-traumatic epilepsy
  • Seizures
  • Status epilepticus

Cite this

Tubi, M. A., Lutkenhoff, E., Blanco, M. B., McArthur, D., Villablanca, P., Ellingson, B., ... Zimmermann, L. (2019). Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study. Neurobiology of Disease, 123, 115-121. https://doi.org/10.1016/j.nbd.2018.05.014
Tubi, Meral A. ; Lutkenhoff, Evan ; Blanco, Manuel Buitrago ; McArthur, David ; Villablanca, Pablo ; Ellingson, Benjamin ; Diaz-Arrastia, Ramon ; Van Ness, Paul ; Real, Courtney ; Shrestha, Vikesh ; Engel, Jerome ; Vespa, Paul M. ; EpiBioS4Rx Study Group Investigators ; Agoston, Denes ; Au, Alicia ; Bell, Michael J. ; Bleck, Tom ; Branch, Craig ; Buitrago Blanco, Manuel ; Bullock, Ross ; Burrows, Brian T. ; Claassen, Jan ; Clarke, Robert ; Cloyd, James ; Coles, Lisa ; Crawford, Karen ; Diaz-Arrastia, Ramon ; Duncan, Dominique ; Ellingson, Benjamin ; Engel, Jerome ; Foreman, Brandon ; Galanopoulou, Aristea ; Gilmore, Emily ; Olli, Grohn ; Harris, Neil ; Hartings, Jed ; Lawrence, Hirsch ; Hunn, Martin ; Jette, Nathalie ; Johnston, Leigh ; Jones, Nigel ; Kanner, Andres ; McArthur, David ; Monti, Martin ; Morokoff, Andrew ; Moshe, Solomon ; Mowrey, Wenzhu ; O'Brien, Terence ; O'Phelan, Kristine ; Pitkanen, Asla ; Raman, Rema ; Robertson, Courtney ; Rosenthal, Eric ; Shultz, Sandy ; Snutch, Terrance ; Staba, Richard ; Toga, Arthur ; Van Horn, Jack ; Vespa, Paul ; Willyerd, Frederick ; Zimmermann, Lara. / Early seizures and temporal lobe trauma predict post-traumatic epilepsy : A longitudinal study. In: Neurobiology of Disease. 2019 ; Vol. 123. pp. 115-121.
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title = "Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study",
abstract = "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.",
keywords = "Brain atrophy, Brain trauma, Coma, Post-traumatic epilepsy, Seizures, Status epilepticus",
author = "Tubi, {Meral A.} and Evan Lutkenhoff and Blanco, {Manuel Buitrago} and David McArthur and Pablo Villablanca and Benjamin Ellingson and Ramon Diaz-Arrastia and {Van Ness}, Paul and Courtney Real and Vikesh Shrestha and Jerome Engel and Vespa, {Paul M.} and {EpiBioS4Rx Study Group Investigators} and Denes Agoston and Alicia Au and Bell, {Michael J.} and Tom Bleck and Craig Branch and {Buitrago Blanco}, Manuel and Ross Bullock and Burrows, {Brian T.} and Jan Claassen and Robert Clarke and James Cloyd and Lisa Coles and Karen Crawford and Ramon Diaz-Arrastia and Dominique Duncan and Benjamin Ellingson and Jerome Engel and Brandon Foreman and Aristea Galanopoulou and Emily Gilmore and Grohn Olli and Neil Harris and Jed Hartings and Hirsch Lawrence and Martin Hunn and Nathalie Jette and Leigh Johnston and Nigel Jones and Andres Kanner and David McArthur and Martin Monti and Andrew Morokoff and Solomon Moshe and Wenzhu Mowrey and Terence O'Brien and Kristine O'Phelan and Asla Pitkanen and Rema Raman and Courtney Robertson and Eric Rosenthal and Sandy Shultz and Terrance Snutch and Richard Staba and Arthur Toga and {Van Horn}, Jack and Paul Vespa and Frederick Willyerd and Lara Zimmermann",
year = "2019",
month = "3",
day = "1",
doi = "10.1016/j.nbd.2018.05.014",
language = "English",
volume = "123",
pages = "115--121",
journal = "Neurobiology of Disease",
issn = "0969-9961",
publisher = "Elsevier",

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Tubi, MA, Lutkenhoff, E, Blanco, MB, McArthur, D, Villablanca, P, Ellingson, B, Diaz-Arrastia, R, Van Ness, P, Real, C, Shrestha, V, Engel, J, Vespa, PM, EpiBioS4Rx Study Group Investigators, Agoston, D, Au, A, Bell, MJ, Bleck, T, Branch, C, Buitrago Blanco, M, Bullock, R, Burrows, BT, Claassen, J, Clarke, R, Cloyd, J, Coles, L, Crawford, K, Diaz-Arrastia, R, Duncan, D, Ellingson, B, Engel, J, Foreman, B, Galanopoulou, A, Gilmore, E, Olli, G, Harris, N, Hartings, J, Lawrence, H, Hunn, M, Jette, N, Johnston, L, Jones, N, Kanner, A, McArthur, D, Monti, M, Morokoff, A, Moshe, S, Mowrey, W, O'Brien, T, O'Phelan, K, Pitkanen, A, Raman, R, Robertson, C, Rosenthal, E, Shultz, S, Snutch, T, Staba, R, Toga, A, Van Horn, J, Vespa, P, Willyerd, F & Zimmermann, L 2019, 'Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study', Neurobiology of Disease, vol. 123, pp. 115-121. https://doi.org/10.1016/j.nbd.2018.05.014

Early seizures and temporal lobe trauma predict post-traumatic epilepsy : A longitudinal study. / Tubi, Meral A.; Lutkenhoff, Evan; Blanco, Manuel Buitrago; McArthur, David; Villablanca, Pablo; Ellingson, Benjamin; Diaz-Arrastia, Ramon; Van Ness, Paul; Real, Courtney; Shrestha, Vikesh; Engel, Jerome; Vespa, Paul M.; EpiBioS4Rx Study Group Investigators; Agoston, Denes; Au, Alicia; Bell, Michael J.; Bleck, Tom; Branch, Craig; Buitrago Blanco, Manuel; Bullock, Ross; Burrows, Brian T.; Claassen, Jan; Clarke, Robert; Cloyd, James; Coles, Lisa; Crawford, Karen; Diaz-Arrastia, Ramon; Duncan, Dominique; Ellingson, Benjamin; Engel, Jerome; Foreman, Brandon; Galanopoulou, Aristea; Gilmore, Emily; Olli, Grohn; Harris, Neil; Hartings, Jed; Lawrence, Hirsch; Hunn, Martin; Jette, Nathalie; Johnston, Leigh; Jones, Nigel; Kanner, Andres; McArthur, David; Monti, Martin; Morokoff, Andrew; Moshe, Solomon; Mowrey, Wenzhu; O'Brien, Terence; O'Phelan, Kristine; Pitkanen, Asla; Raman, Rema; Robertson, Courtney; Rosenthal, Eric; Shultz, Sandy; Snutch, Terrance; Staba, Richard; Toga, Arthur; Van Horn, Jack; Vespa, Paul; Willyerd, Frederick; Zimmermann, Lara.

In: Neurobiology of Disease, Vol. 123, 01.03.2019, p. 115-121.

Research output: Contribution to journalReview ArticleResearchpeer-review

TY - JOUR

T1 - Early seizures and temporal lobe trauma predict post-traumatic epilepsy

T2 - A longitudinal study

AU - Tubi, Meral A.

AU - Lutkenhoff, Evan

AU - Blanco, Manuel Buitrago

AU - McArthur, David

AU - Villablanca, Pablo

AU - Ellingson, Benjamin

AU - Diaz-Arrastia, Ramon

AU - Van Ness, Paul

AU - Real, Courtney

AU - Shrestha, Vikesh

AU - Engel, Jerome

AU - Vespa, Paul M.

AU - EpiBioS4Rx Study Group Investigators

AU - Agoston, Denes

AU - Au, Alicia

AU - Bell, Michael J.

AU - Bleck, Tom

AU - Branch, Craig

AU - Buitrago Blanco, Manuel

AU - Bullock, Ross

AU - Burrows, Brian T.

AU - Claassen, Jan

AU - Clarke, Robert

AU - Cloyd, James

AU - Coles, Lisa

AU - Crawford, Karen

AU - Diaz-Arrastia, Ramon

AU - Duncan, Dominique

AU - Ellingson, Benjamin

AU - Engel, Jerome

AU - Foreman, Brandon

AU - Galanopoulou, Aristea

AU - Gilmore, Emily

AU - Olli, Grohn

AU - Harris, Neil

AU - Hartings, Jed

AU - Lawrence, Hirsch

AU - Hunn, Martin

AU - Jette, Nathalie

AU - Johnston, Leigh

AU - Jones, Nigel

AU - Kanner, Andres

AU - McArthur, David

AU - Monti, Martin

AU - Morokoff, Andrew

AU - Moshe, Solomon

AU - Mowrey, Wenzhu

AU - O'Brien, Terence

AU - O'Phelan, Kristine

AU - Pitkanen, Asla

AU - Raman, Rema

AU - Robertson, Courtney

AU - Rosenthal, Eric

AU - Shultz, Sandy

AU - Snutch, Terrance

AU - Staba, Richard

AU - Toga, Arthur

AU - Van Horn, Jack

AU - Vespa, Paul

AU - Willyerd, Frederick

AU - Zimmermann, Lara

PY - 2019/3/1

Y1 - 2019/3/1

N2 - 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.

AB - 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.

KW - Brain atrophy

KW - Brain trauma

KW - Coma

KW - Post-traumatic epilepsy

KW - Seizures

KW - Status epilepticus

UR - http://www.scopus.com/inward/record.url?scp=85049355471&partnerID=8YFLogxK

U2 - 10.1016/j.nbd.2018.05.014

DO - 10.1016/j.nbd.2018.05.014

M3 - Review Article

VL - 123

SP - 115

EP - 121

JO - Neurobiology of Disease

JF - Neurobiology of Disease

SN - 0969-9961

ER -

Tubi MA, Lutkenhoff E, Blanco MB, McArthur D, Villablanca P, Ellingson B et al. Early seizures and temporal lobe trauma predict post-traumatic epilepsy: A longitudinal study. Neurobiology of Disease. 2019 Mar 1;123:115-121. https://doi.org/10.1016/j.nbd.2018.05.014