Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study

Objective: The intricate neuroanatomical structure of the cerebellum is of longstanding interest in epilepsy, but has been poorly characterized within the current corticocentric models of this disease. We quantified cross-sectional regional cerebellar lobule volumes using structural magnetic resonan...

Descripción completa

Detalles Bibliográficos
Autores: Rummel C, Scheffler F, Severino, Mariasavina, Silva LS, Staba RJ, Stein DJ, Striano, Pasquale, Taylor PN, Thomopoulos SI, Thompson PM, Bender B, Tortora, Domenico, Brioschi R, Vaudano AE, Bürkle E, Weber B, Caligiuri ME, Wiest R, Cendes, Fernando, Winston, Gavin P, de Tisi J, Yasuda CL, Duncan, John S, Engel JP Jr, Foley S, Fortunato F, Kerestes R, Perry A, Vivash, Lucy, O'Brien TJ, Alvim MKM, Arienzo D, Aventurato ÍK, Ballerini A, Baltazar GF, Bargalló Alabart, Núria, Zheng H, McDonald CR, Sisodiya SM, Harding IH, Gambardella, Antonio, Giacomini T, Guerrini, Renzo, Hall G, Hamandi, Khalid, Ives-Deliperi V, João RB, Keller SS, Kleiser B, Labate, Angelo, Lenge, Matteo, Marotta C, Martin P, Mascalchi M, Meletti S, Owens-Walton C, Parodi CB, Pascual-Diaz, Saül, Powell D, Rao J, Rebsamen M, Reiter J, Riva A, Rüber T
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Universidad de Barcelona
Repositorio:Dipòsit Digital de la UB
OAI Identifier:oai:diposit.ub.edu:2445/226425
Acceso en línea:https://hdl.handle.net/2445/226425
Access Level:acceso abierto
Palabra clave:Epilèpsia
Cerebel
Imatges per ressonància magnètica
Epilepsy
Cerebellum
Magnetic resonance imaging
id ES_caa2d0dffb78a55a117b41bbfc68932d
oai_identifier_str oai:diposit.ub.edu:2445/226425
network_acronym_str ES
network_name_str España
repository_id_str
spelling Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy studyRummel CScheffler FSeverino, MariasavinaSilva LSStaba RJStein DJStriano, PasqualeTaylor PNThomopoulos SIThompson PMBender BTortora, DomenicoBrioschi RVaudano AEBürkle EWeber BCaligiuri MEWiest RCendes, FernandoWinston, Gavin Pde Tisi JYasuda CLDuncan, John SEngel JP JrFoley SFortunato FKerestes RPerry AVivash, LucyO'Brien TJAlvim MKMArienzo DAventurato ÍKBallerini ABaltazar GFBargalló Alabart, NúriaZheng HMcDonald CRSisodiya SMHarding IHGambardella, AntonioGiacomini TGuerrini, RenzoHall GHamandi, KhalidIves-Deliperi VJoão RBKeller SSKleiser BLabate, AngeloLenge, MatteoMarotta CMartin PMascalchi MMeletti SOwens-Walton CParodi CBPascual-Diaz, SaülPowell DRao JRebsamen MReiter JRiva ARüber TEpilèpsiaCerebelImatges per ressonància magnèticaEpilepsyCerebellumMagnetic resonance imagingObjective: The intricate neuroanatomical structure of the cerebellum is of longstanding interest in epilepsy, but has been poorly characterized within the current corticocentric models of this disease. We quantified cross-sectional regional cerebellar lobule volumes using structural magnetic resonance imaging in 1602 adults with epilepsy and 1022 healthy controls across 22 sites from the global ENIGMA-Epilepsy working group. Methods: A state-of-the-art deep learning-based approach was employed that parcellates the cerebellum into 28 neuroanatomical subregions. Linear mixed models compared total and regional cerebellar volume in (1) all epilepsies, (2) temporal lobe epilepsy with hippocampal sclerosis (TLE-HS), (3) nonlesional temporal lobe epilepsy, (4) genetic generalized epilepsy, and (5) extratemporal focal epilepsy (ETLE). Relationships were examined for cerebellar volume versus age at seizure onset, duration of epilepsy, phenytoin treatment, and cerebral cortical thickness. Results: Across all epilepsies, reduced total cerebellar volume was observed (d = .42). Maximum volume loss was observed in the corpus medullare (dmax = .49) and posterior lobe gray matter regions, including bilateral lobules VIIB (dmax = .47), crus I/II (dmax = .39), VIIIA (dmax = .45), and VIIIB (dmax = .40). Earlier age at seizure onset ( ηρ2max = .05) and longer epilepsy duration ( ηρ2max = .06) correlated with reduced volume in these regions. Findings were most pronounced in TLE-HS and ETLE, with distinct neuroanatomical profiles observed in the posterior lobe. Phenytoin treatment was associated with reduced posterior lobe volume. Cerebellum volume correlated with cerebral cortical thinning more strongly in the epilepsy cohort than in controls. Significance: We provide robust evidence of deep cerebellar and posterior lobe subregional gray matter volume loss in patients with chronic epilepsy. Volume loss was maximal for posterior subregions implicated in nonmotor functions, relative to motor regions of both the anterior and posterior lobe. Associations between cerebral and cerebellar changes, and variability of neuroanatomical profiles across epilepsy syndromes argue for more precise incorporation of cerebellar subregional damage into neurobiological models of epilepsy.John Wiley & Sons2024info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2445/226425Articles publicats en revistes (Medicina)reponame:Dipòsit Digital de la UBinstname:Universidad de BarcelonaInglésReproducció del document publicat a: https://doi.org/10.1111/epi.17881Epilepsia Open, 2024https://doi.org/10.1111/epi.17881cc-by-nc-nd (c) Kerestes R et al., 2024http://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:diposit.ub.edu:2445/2264252026-05-27T06:46:51Z
dc.title.none.fl_str_mv Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
title Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
spellingShingle Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
Rummel C
Epilèpsia
Cerebel
Imatges per ressonància magnètica
Epilepsy
Cerebellum
Magnetic resonance imaging
title_short Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
title_full Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
title_fullStr Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
title_full_unstemmed Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
title_sort Patterns of subregional cerebellar atrophy across epilepsy syndromes: An ENIGMA-Epilepsy study
dc.creator.none.fl_str_mv Rummel C
Scheffler F
Severino, Mariasavina
Silva LS
Staba RJ
Stein DJ
Striano, Pasquale
Taylor PN
Thomopoulos SI
Thompson PM
Bender B
Tortora, Domenico
Brioschi R
Vaudano AE
Bürkle E
Weber B
Caligiuri ME
Wiest R
Cendes, Fernando
Winston, Gavin P
de Tisi J
Yasuda CL
Duncan, John S
Engel JP Jr
Foley S
Fortunato F
Kerestes R
Perry A
Vivash, Lucy
O'Brien TJ
Alvim MKM
Arienzo D
Aventurato ÍK
Ballerini A
Baltazar GF
Bargalló Alabart, Núria
Zheng H
McDonald CR
Sisodiya SM
Harding IH
Gambardella, Antonio
Giacomini T
Guerrini, Renzo
Hall G
Hamandi, Khalid
Ives-Deliperi V
João RB
Keller SS
Kleiser B
Labate, Angelo
Lenge, Matteo
Marotta C
Martin P
Mascalchi M
Meletti S
Owens-Walton C
Parodi CB
Pascual-Diaz, Saül
Powell D
Rao J
Rebsamen M
Reiter J
Riva A
Rüber T
author Rummel C
author_facet Rummel C
Scheffler F
Severino, Mariasavina
Silva LS
Staba RJ
Stein DJ
Striano, Pasquale
Taylor PN
Thomopoulos SI
Thompson PM
Bender B
Tortora, Domenico
Brioschi R
Vaudano AE
Bürkle E
Weber B
Caligiuri ME
Wiest R
Cendes, Fernando
Winston, Gavin P
de Tisi J
Yasuda CL
Duncan, John S
Engel JP Jr
Foley S
Fortunato F
Kerestes R
Perry A
Vivash, Lucy
O'Brien TJ
Alvim MKM
Arienzo D
Aventurato ÍK
Ballerini A
Baltazar GF
Bargalló Alabart, Núria
Zheng H
McDonald CR
Sisodiya SM
Harding IH
Gambardella, Antonio
Giacomini T
Guerrini, Renzo
Hall G
Hamandi, Khalid
Ives-Deliperi V
João RB
Keller SS
Kleiser B
Labate, Angelo
Lenge, Matteo
Marotta C
Martin P
Mascalchi M
Meletti S
Owens-Walton C
Parodi CB
Pascual-Diaz, Saül
Powell D
Rao J
Rebsamen M
Reiter J
Riva A
Rüber T
author_role author
author2 Scheffler F
Severino, Mariasavina
Silva LS
Staba RJ
Stein DJ
Striano, Pasquale
Taylor PN
Thomopoulos SI
Thompson PM
Bender B
Tortora, Domenico
Brioschi R
Vaudano AE
Bürkle E
Weber B
Caligiuri ME
Wiest R
Cendes, Fernando
Winston, Gavin P
de Tisi J
Yasuda CL
Duncan, John S
Engel JP Jr
Foley S
Fortunato F
Kerestes R
Perry A
Vivash, Lucy
O'Brien TJ
Alvim MKM
Arienzo D
Aventurato ÍK
Ballerini A
Baltazar GF
Bargalló Alabart, Núria
Zheng H
McDonald CR
Sisodiya SM
Harding IH
Gambardella, Antonio
Giacomini T
Guerrini, Renzo
Hall G
Hamandi, Khalid
Ives-Deliperi V
João RB
Keller SS
Kleiser B
Labate, Angelo
Lenge, Matteo
Marotta C
Martin P
Mascalchi M
Meletti S
Owens-Walton C
Parodi CB
Pascual-Diaz, Saül
Powell D
Rao J
Rebsamen M
Reiter J
Riva A
Rüber T
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Epilèpsia
Cerebel
Imatges per ressonància magnètica
Epilepsy
Cerebellum
Magnetic resonance imaging
topic Epilèpsia
Cerebel
Imatges per ressonància magnètica
Epilepsy
Cerebellum
Magnetic resonance imaging
description Objective: The intricate neuroanatomical structure of the cerebellum is of longstanding interest in epilepsy, but has been poorly characterized within the current corticocentric models of this disease. We quantified cross-sectional regional cerebellar lobule volumes using structural magnetic resonance imaging in 1602 adults with epilepsy and 1022 healthy controls across 22 sites from the global ENIGMA-Epilepsy working group. Methods: A state-of-the-art deep learning-based approach was employed that parcellates the cerebellum into 28 neuroanatomical subregions. Linear mixed models compared total and regional cerebellar volume in (1) all epilepsies, (2) temporal lobe epilepsy with hippocampal sclerosis (TLE-HS), (3) nonlesional temporal lobe epilepsy, (4) genetic generalized epilepsy, and (5) extratemporal focal epilepsy (ETLE). Relationships were examined for cerebellar volume versus age at seizure onset, duration of epilepsy, phenytoin treatment, and cerebral cortical thickness. Results: Across all epilepsies, reduced total cerebellar volume was observed (d = .42). Maximum volume loss was observed in the corpus medullare (dmax = .49) and posterior lobe gray matter regions, including bilateral lobules VIIB (dmax = .47), crus I/II (dmax = .39), VIIIA (dmax = .45), and VIIIB (dmax = .40). Earlier age at seizure onset ( ηρ2max = .05) and longer epilepsy duration ( ηρ2max = .06) correlated with reduced volume in these regions. Findings were most pronounced in TLE-HS and ETLE, with distinct neuroanatomical profiles observed in the posterior lobe. Phenytoin treatment was associated with reduced posterior lobe volume. Cerebellum volume correlated with cerebral cortical thinning more strongly in the epilepsy cohort than in controls. Significance: We provide robust evidence of deep cerebellar and posterior lobe subregional gray matter volume loss in patients with chronic epilepsy. Volume loss was maximal for posterior subregions implicated in nonmotor functions, relative to motor regions of both the anterior and posterior lobe. Associations between cerebral and cerebellar changes, and variability of neuroanatomical profiles across epilepsy syndromes argue for more precise incorporation of cerebellar subregional damage into neurobiological models of epilepsy.
publishDate 2024
dc.date.none.fl_str_mv 2024
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/226425
url https://hdl.handle.net/2445/226425
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.1111/epi.17881
Epilepsia Open, 2024
https://doi.org/10.1111/epi.17881
dc.rights.none.fl_str_mv cc-by-nc-nd (c) Kerestes R et al., 2024
http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by-nc-nd (c) Kerestes R et al., 2024
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
dc.source.none.fl_str_mv Articles publicats en revistes (Medicina)
reponame:Dipòsit Digital de la UB
instname:Universidad de Barcelona
instname_str Universidad de Barcelona
reponame_str Dipòsit Digital de la UB
collection Dipòsit Digital de la UB
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869419497047195648
score 15,81155