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...
| Autores: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| 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 |
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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 |
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cc-by-nc-nd (c) Kerestes R et al., 2024 http://creativecommons.org/licenses/by-nc-nd/4.0/ |
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openAccess |
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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 |
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Universidad de Barcelona |
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Dipòsit Digital de la UB |
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Dipòsit Digital de la UB |
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1869419497047195648 |
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15,81155 |