Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study

Sara Larivière; Raúl Rodríguez-Cruces; Jessica Royer; Maria Eugenia Caligiuri; Antonio Gambardella; Luis Concha; Simon S. Keller; Fernando Cendes; Clarissa Yasuda; Leonardo Bonilha; Ezequiel Gleichgerrcht; Niels K. Focke; Martin Domin; Felix Von Podewills; Soenke Langner; Christian Rummel; Roland Wiest; Pascal Martin; Raviteja Kotikalapudi; Terence J. O'Brien; Benjamin Sinclair; Lucy Vivash; Patricia M. Desmond; Saud Alhusaini; Colin P. Doherty; Gianpiero L. Cavalleri; Norman Delanty; Reetta Kälviaïnen; Graeme D. Jackson; Magdalena Kowalczyk; Mario Mascalchi; Mira Semmelroch; Rhys H. Thomas; Hamid Soltanian-Zadeh; Esmaeil Davoodi-Bojd; Junsong Zhang; Matteo Lenge; Renzo Guerrini; Emanuele Bartolini; Khalid Hamandi; Sonya Foley; Bernd Weber; Chantal Depondt; Julie Absil; Sarah J.A. Carr; Eugenio Abela; Mark P. Richardson; Orrin Devinsky; Mariasavina Severino; Pasquale Striano; Domenico Tortora; Sean N. Hatton; Sjoerd B. Vos; John S. Duncan; Christopher D. Whelan; Paul M. Thompson; Sanjay M. Sisodiya; Andrea Bernasconi; Angelo Labate; Carrie R. McDonald; Neda Bernasconi; Boris C. Bernhardt

doi:10.1126/sciadv.abc6457

Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study

Sara Larivière, Raúl Rodríguez-Cruces, Jessica Royer, Maria Eugenia Caligiuri, Antonio Gambardella, Luis Concha, Simon S. Keller, Fernando Cendes, Clarissa Yasuda, Leonardo Bonilha, Ezequiel Gleichgerrcht, Niels K. Focke, Martin Domin, Felix Von Podewills, Soenke Langner, Christian Rummel, Roland Wiest, Pascal Martin, Raviteja Kotikalapudi, Terence J. O'BrienBenjamin Sinclair, Lucy Vivash, Patricia M. Desmond, Saud Alhusaini, Colin P. Doherty, Gianpiero L. Cavalleri, Norman Delanty, Reetta Kälviaïnen, Graeme D. Jackson, Magdalena Kowalczyk, Mario Mascalchi, Mira Semmelroch, Rhys H. Thomas, Hamid Soltanian-Zadeh, Esmaeil Davoodi-Bojd, Junsong Zhang, Matteo Lenge, Renzo Guerrini, Emanuele Bartolini, Khalid Hamandi, Sonya Foley, Bernd Weber, Chantal Depondt, Julie Absil, Sarah J.A. Carr, Eugenio Abela, Mark P. Richardson, Orrin Devinsky, Mariasavina Severino, Pasquale Striano, Domenico Tortora, Sean N. Hatton, Sjoerd B. Vos, John S. Duncan, Christopher D. Whelan, Paul M. Thompson, Sanjay M. Sisodiya, Andrea Bernasconi, Angelo Labate, Carrie R. McDonald, Neda Bernasconi, Boris C. Bernhardt

Research output: Contribution to journal › Article › peer-review

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Abstract

Epilepsy is increasingly conceptualized as a network disorder. In this cross-sectional mega-analysis, we integrated neuroimaging and connectome analysis to identify network associations with atrophy patterns in 1021 adults with epilepsy compared to 1564 healthy controls from 19 international sites. In temporal lobe epilepsy, areas of atrophy colocalized with highly interconnected cortical hub regions, whereas idiopathic generalized epilepsy showed preferential subcortical hub involvement. These morphological abnormalities were anchored to the connectivity profiles of distinct disease epicenters, pointing to temporo-limbic cortices in temporal lobe epilepsy and fronto-central cortices in idiopathic generalized epilepsy. Negative effects of age on atrophy further revealed a strong influence of connectome architecture in temporal lobe, but not idiopathic generalized, epilepsy. Our findings were reproduced across individual sites and single patients and were robust across different analytical methods. Through worldwide collaboration in ENIGMA-Epilepsy, we provided deeper insights into the macroscale features that shape the pathophysiology of common epilepsies.

Original language	English
Article number	eabc6457
Journal	Science advances
Volume	6
Issue number	47
DOIs	https://doi.org/10.1126/sciadv.abc6457
State	Published - 18 Nov 2020
Externally published	Yes

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Larivière, S., Rodríguez-Cruces, R., Royer, J., Caligiuri, M. E., Gambardella, A., Concha, L., Keller, S. S., Cendes, F., Yasuda, C., Bonilha, L., Gleichgerrcht, E., Focke, N. K., Domin, M., Podewills, F. V., Langner, S., Rummel, C., Wiest, R., Martin, P., Kotikalapudi, R., ... Bernhardt, B. C. (2020). Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study. Science advances, 6(47), Article eabc6457. https://doi.org/10.1126/sciadv.abc6457

@article{dfd2124dd8ad4b56ac18b20a6c58263f,

title = "Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study",

abstract = "Epilepsy is increasingly conceptualized as a network disorder. In this cross-sectional mega-analysis, we integrated neuroimaging and connectome analysis to identify network associations with atrophy patterns in 1021 adults with epilepsy compared to 1564 healthy controls from 19 international sites. In temporal lobe epilepsy, areas of atrophy colocalized with highly interconnected cortical hub regions, whereas idiopathic generalized epilepsy showed preferential subcortical hub involvement. These morphological abnormalities were anchored to the connectivity profiles of distinct disease epicenters, pointing to temporo-limbic cortices in temporal lobe epilepsy and fronto-central cortices in idiopathic generalized epilepsy. Negative effects of age on atrophy further revealed a strong influence of connectome architecture in temporal lobe, but not idiopathic generalized, epilepsy. Our findings were reproduced across individual sites and single patients and were robust across different analytical methods. Through worldwide collaboration in ENIGMA-Epilepsy, we provided deeper insights into the macroscale features that shape the pathophysiology of common epilepsies.",

author = "Sara Larivi{\`e}re and Ra{\'u}l Rodr{\'i}guez-Cruces and Jessica Royer and Caligiuri, {Maria Eugenia} and Antonio Gambardella and Luis Concha and Keller, {Simon S.} and Fernando Cendes and Clarissa Yasuda and Leonardo Bonilha and Ezequiel Gleichgerrcht and Focke, {Niels K.} and Martin Domin and Podewills, {Felix Von} and Soenke Langner and Christian Rummel and Roland Wiest and Pascal Martin and Raviteja Kotikalapudi and O'Brien, {Terence J.} and Benjamin Sinclair and Lucy Vivash and Desmond, {Patricia M.} and Saud Alhusaini and Doherty, {Colin P.} and Cavalleri, {Gianpiero L.} and Norman Delanty and Reetta K{\"a}lvia{\"i}nen and Jackson, {Graeme D.} and Magdalena Kowalczyk and Mario Mascalchi and Mira Semmelroch and Thomas, {Rhys H.} and Hamid Soltanian-Zadeh and Esmaeil Davoodi-Bojd and Junsong Zhang and Matteo Lenge and Renzo Guerrini and Emanuele Bartolini and Khalid Hamandi and Sonya Foley and Bernd Weber and Chantal Depondt and Julie Absil and Carr, {Sarah J.A.} and Eugenio Abela and Richardson, {Mark P.} and Orrin Devinsky and Mariasavina Severino and Pasquale Striano and Domenico Tortora and Hatton, {Sean N.} and Vos, {Sjoerd B.} and Duncan, {John S.} and Whelan, {Christopher D.} and Thompson, {Paul M.} and Sisodiya, {Sanjay M.} and Andrea Bernasconi and Angelo Labate and McDonald, {Carrie R.} and Neda Bernasconi and Bernhardt, {Boris C.}",

note = "Publisher Copyright: Copyright {\textcopyright} 2020 The Authors, some rights reserved;.",

year = "2020",

month = nov,

day = "18",

doi = "10.1126/sciadv.abc6457",

language = "English",

volume = "6",

journal = "Science advances",

issn = "2375-2548",

publisher = "American Association for the Advancement of Science",

number = "47",

}

Larivière, S, Rodríguez-Cruces, R, Royer, J, Caligiuri, ME, Gambardella, A, Concha, L, Keller, SS, Cendes, F, Yasuda, C, Bonilha, L, Gleichgerrcht, E, Focke, NK, Domin, M, Podewills, FV, Langner, S, Rummel, C, Wiest, R, Martin, P, Kotikalapudi, R, O'Brien, TJ, Sinclair, B, Vivash, L, Desmond, PM, Alhusaini, S, Doherty, CP, Cavalleri, GL, Delanty, N, Kälviaïnen, R, Jackson, GD, Kowalczyk, M, Mascalchi, M, Semmelroch, M, Thomas, RH, Soltanian-Zadeh, H, Davoodi-Bojd, E, Zhang, J, Lenge, M, Guerrini, R, Bartolini, E, Hamandi, K, Foley, S, Weber, B, Depondt, C, Absil, J, Carr, SJA, Abela, E, Richardson, MP, Devinsky, O, Severino, M, Striano, P, Tortora, D, Hatton, SN, Vos, SB, Duncan, JS, Whelan, CD, Thompson, PM, Sisodiya, SM, Bernasconi, A, Labate, A, McDonald, CR, Bernasconi, N & Bernhardt, BC 2020, 'Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study', Science advances, vol. 6, no. 47, eabc6457. https://doi.org/10.1126/sciadv.abc6457

TY - JOUR

T1 - Network-based atrophy modeling in the common epilepsies

T2 - A worldwide ENIGMA study

AU - Larivière, Sara

AU - Rodríguez-Cruces, Raúl

AU - Royer, Jessica

AU - Caligiuri, Maria Eugenia

AU - Gambardella, Antonio

AU - Concha, Luis

AU - Keller, Simon S.

AU - Cendes, Fernando

AU - Yasuda, Clarissa

AU - Bonilha, Leonardo

AU - Gleichgerrcht, Ezequiel

AU - Focke, Niels K.

AU - Domin, Martin

AU - Podewills, Felix Von

AU - Langner, Soenke

AU - Rummel, Christian

AU - Wiest, Roland

AU - Martin, Pascal

AU - Kotikalapudi, Raviteja

AU - O'Brien, Terence J.

AU - Sinclair, Benjamin

AU - Vivash, Lucy

AU - Desmond, Patricia M.

AU - Alhusaini, Saud

AU - Doherty, Colin P.

AU - Cavalleri, Gianpiero L.

AU - Delanty, Norman

AU - Kälviaïnen, Reetta

AU - Jackson, Graeme D.

AU - Kowalczyk, Magdalena

AU - Mascalchi, Mario

AU - Semmelroch, Mira

AU - Thomas, Rhys H.

AU - Soltanian-Zadeh, Hamid

AU - Davoodi-Bojd, Esmaeil

AU - Zhang, Junsong

AU - Lenge, Matteo

AU - Guerrini, Renzo

AU - Bartolini, Emanuele

AU - Hamandi, Khalid

AU - Foley, Sonya

AU - Weber, Bernd

AU - Depondt, Chantal

AU - Absil, Julie

AU - Carr, Sarah J.A.

AU - Abela, Eugenio

AU - Richardson, Mark P.

AU - Devinsky, Orrin

AU - Severino, Mariasavina

AU - Striano, Pasquale

AU - Tortora, Domenico

AU - Hatton, Sean N.

AU - Vos, Sjoerd B.

AU - Duncan, John S.

AU - Whelan, Christopher D.

AU - Thompson, Paul M.

AU - Sisodiya, Sanjay M.

AU - Bernasconi, Andrea

AU - Labate, Angelo

AU - McDonald, Carrie R.

AU - Bernasconi, Neda

AU - Bernhardt, Boris C.

PY - 2020/11/18

Y1 - 2020/11/18

N2 - Epilepsy is increasingly conceptualized as a network disorder. In this cross-sectional mega-analysis, we integrated neuroimaging and connectome analysis to identify network associations with atrophy patterns in 1021 adults with epilepsy compared to 1564 healthy controls from 19 international sites. In temporal lobe epilepsy, areas of atrophy colocalized with highly interconnected cortical hub regions, whereas idiopathic generalized epilepsy showed preferential subcortical hub involvement. These morphological abnormalities were anchored to the connectivity profiles of distinct disease epicenters, pointing to temporo-limbic cortices in temporal lobe epilepsy and fronto-central cortices in idiopathic generalized epilepsy. Negative effects of age on atrophy further revealed a strong influence of connectome architecture in temporal lobe, but not idiopathic generalized, epilepsy. Our findings were reproduced across individual sites and single patients and were robust across different analytical methods. Through worldwide collaboration in ENIGMA-Epilepsy, we provided deeper insights into the macroscale features that shape the pathophysiology of common epilepsies.

AB - Epilepsy is increasingly conceptualized as a network disorder. In this cross-sectional mega-analysis, we integrated neuroimaging and connectome analysis to identify network associations with atrophy patterns in 1021 adults with epilepsy compared to 1564 healthy controls from 19 international sites. In temporal lobe epilepsy, areas of atrophy colocalized with highly interconnected cortical hub regions, whereas idiopathic generalized epilepsy showed preferential subcortical hub involvement. These morphological abnormalities were anchored to the connectivity profiles of distinct disease epicenters, pointing to temporo-limbic cortices in temporal lobe epilepsy and fronto-central cortices in idiopathic generalized epilepsy. Negative effects of age on atrophy further revealed a strong influence of connectome architecture in temporal lobe, but not idiopathic generalized, epilepsy. Our findings were reproduced across individual sites and single patients and were robust across different analytical methods. Through worldwide collaboration in ENIGMA-Epilepsy, we provided deeper insights into the macroscale features that shape the pathophysiology of common epilepsies.

UR - http://www.scopus.com/inward/record.url?scp=85096408152&partnerID=8YFLogxK

U2 - 10.1126/sciadv.abc6457

DO - 10.1126/sciadv.abc6457

M3 - Article

C2 - 33208365

AN - SCOPUS:85096408152

SN - 2375-2548

VL - 6

JO - Science advances

JF - Science advances

IS - 47

M1 - eabc6457

ER -

Network-based atrophy modeling in the common epilepsies: A worldwide ENIGMA study

Abstract

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