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Brain Structure in Acutely Underweight and Partially Weight-Restored Individuals With Anorexia Nervosa: A Coordinated Analysis by the ENIGMA Eating Disorders Working Group

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Esther Walton, Fabio Bernardoni, Victoria Luise Batury, Klaas Bahnsen, Sara Larivière, Giovanni Abbate-Daga, Susana Andres-Perpiña, Lasse Bang, Amanda Bischoff-Grethe, Samantha J. Brooks, Iain C. Campbell, Giammarco Cascino, Josefina Castro-Fornieles, Enrico Collantoni, Federico D'Agata, Brigitte Dahmen, Unna N. Danner, Angela Favaro, Jamie D. Feusner, Guido K.W. Frank & 39 more Hans Christoph Friederich, John L. Graner, Beate Herpertz-Dahlmann, Andreas Hess, Stefanie Horndasch, Allan S. Kaplan, Lisa Katrin Kaufmann, Walter H. Kaye, Sahib S. Khalsa, Kevin S. LaBar, Luca Lavagnino, Luisa Lazaro, Renzo Manara, Amy E. Miles, Gabriella F. Milos, Alessio Maria Monteleone, Palmiero Monteleone, Benson Mwangi, Owen O'Daly, Jose Pariente, Julie Roesch, Ulrike H. Schmidt, Jochen Seitz, Megan E. Shott, Joe J. Simon, Paul A.M. Smeets, Christian K. Tamnes, Elena Tenconi, Sophia I. Thomopoulos, Annemarie A. van Elburg, Aristotle N. Voineskos, Georg G. von Polier, Christina E. Wierenga, Nancy L. Zucker, Neda Jahanshad, Joseph A. King, Paul M. Thompson, Laura A. Berner, Stefan Ehrlich

Original languageEnglish
Pages (from-to)730-738
Number of pages9
JournalBiological psychiatry
Volume92
Issue number9
DOIs
Accepted/In press2022
Published1 Nov 2022

Bibliographical note

Funding Information: This work was supported by the Carus Promotionskolleg (to KB), Ministerio de Igualdad (Grant No. 234/09 [to SA-P]), Generalitat de Catalunya (Grant No. 2009 SGR 1119 [to SA-P and LLaz] and Grant No. 2017 SGR 4881 [to JC-F]), National Institutes of Health (Grant No. R21MH86017 [to AB-G and CEW], Grant No. R01MH113588 [to AB-G, WHK, and CEW], Grant No. RC1MH088678 [to JLG, KSL, NLZ, and JAK], and Grant No. R01MH042984-17A1 [to WHK]), Biomedical Research Centre (to ICC), Alicia Koplowitz Foundation (Grant No. DN040546 [to JC-F]), German Ministry for Education and Research (Grant Nos. 01GV0602 and 01GV0623 [to BD, BH-D, JSS, and GGvP]), National Institute of Mental Health (Grant Nos. R01MH105662 and R01MH093535 [to JDF], Grant Nos. K23MH080135 and R01MH096777 [to GKWF and MES], Grant No. K23MH112949 [to SSK], and Grant No. K23MH118418 [to LAB]), Centre for Addiction and Mental Health Alternative Funding Plan Innovation Fund (to ASK, AEM, and ANV), Swiss Anorexia Nervosa Foundation (Project No. 19-12 [to L-KK and GFM] and Project No. 57-16 [to JJS] and to SE), Palatin Foundation (to L-KK and GFM), Gottfried and Julia Bangerter-Rhyner-Foundation (to L-KK and GFM), Weston A. Price Foundation (to WHK), Carlos III Research Institute of the Spanish Ministry of Health (Grant No. FIS PI040829 [to LLaz]), National Institute for Health Research Mental Health Biomedical Research Centre at the South London and Maudsley NHS Foundation Trust and King's College London (ICC, OO, and UHS), German Research Foundation (Grant Nos. SI 2087/2-1 and BR 4852/1-1 [to JJS] and Grant Nos. EH 367/5-1 and EH 367/7-1 [to SE]), Research Council of Norway (Grant Nos. 288083 and 223273 [to CKT]), South-Eastern Norway Regional Health Authority (Grant Nos. 2019069, 2021070, and 500189 [to CKT]), National Institute of Health Research Senior Investigator Award (to UHS), NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (to LAB), and Technische Universität Dresden SFB 940 (to SE). This work was further supported by the European Union Horizon 2020 EarlyCause project (Grant No. 848158 [to EW]). The ENIGMA Working Group acknowledges the National Institutes of Health Big Data to Knowledge award for foundational support and consortium development (Grant No. U54 EB020403 [to PMT]). All data produced in the present study are available upon reasonable request to the authors. The authors report no biomedical financial interests or potential conflicts of interest. Funding Information: This work was supported by the Carus Promotionskolleg (to KB), Ministerio de Igualdad (Grant No. 234/09 [to SA-P]), Generalitat de Catalunya (Grant No. 2009 SGR 1119 [to SA-P and LLaz] and Grant No. 2017 SGR 4881 [to JC-F]), National Institutes of Health (Grant No. R21MH86017 [to AB-G and CEW], Grant No. R01MH113588 [to AB-G, WHK, and CEW], Grant No. RC1MH088678 [to JLG, KSL, NLZ, and JAK], and Grant No. R01MH042984-17A1 [to WHK]), Biomedical Research Centre (to ICC), Alicia Koplowitz Foundation (Grant No. DN040546 [to JC-F]), German Ministry for Education and Research (Grant Nos. 01GV0602 and 01GV0623 [to BD, BH-D, JSS, and GGvP]), National Institute of Mental Health (Grant Nos. R01MH105662 and R01MH093535 [to JDF], Grant Nos. K23MH080135 and R01MH096777 [to GKWF and MES], Grant No. K23MH112949 [to SSK], and Grant No. K23MH118418 [to LAB]), Centre for Addiction and Mental Health Alternative Funding Plan Innovation Fund (to ASK, AEM, and ANV), Swiss Anorexia Nervosa Foundation (Project No. 19-12 [to L-KK and GFM] and Project No. 57-16 [to JJS] and to SE), Palatin Foundation (to L-KK and GFM), Gottfried and Julia Bangerter-Rhyner-Foundation (to L-KK and GFM), Weston A. Price Foundation (to WHK), Carlos III Research Institute of the Spanish Ministry of Health (Grant No. FIS PI040829 [to LLaz]), National Institute for Health Research Mental Health Biomedical Research Centre at the South London and Maudsley NHS Foundation Trust and King’s College London (ICC, OO, and UHS), German Research Foundation (Grant Nos. SI 2087/2-1 and BR 4852/1-1 [to JJS] and Grant Nos. EH 367/5-1 and EH 367/7-1 [to SE]), Research Council of Norway (Grant Nos. 288083 and 223273 [to CKT]), South-Eastern Norway Regional Health Authority (Grant Nos. 2019069 , 2021070 , and 500189 [to CKT]), National Institute of Health Research Senior Investigator Award (to UHS), NARSAD Young Investigator Grant from the Brain and Behavior Research Foundation (to LAB), and Technische Universität Dresden SFB 940 (to SE). This work was further supported by the European Union Horizon 2020 EarlyCause project (Grant No. 848158 [to EW]). Funding Information: The ENIGMA Working Group acknowledges the National Institutes of Health Big Data to Knowledge award for foundational support and consortium development (Grant No. U54 EB020403 [to PMT]). Publisher Copyright: © 2022 Society of Biological Psychiatry

King's Authors

Abstract

Background: The pattern of structural brain abnormalities in anorexia nervosa (AN) is still not well understood. While several studies report substantial deficits in gray matter volume and cortical thickness in acutely underweight patients, others find no differences, or even increases in patients compared with healthy control subjects. Recent weight regain before scanning may explain some of this heterogeneity. To clarify the extent, magnitude, and dependencies of gray matter changes in AN, we conducted a prospective, coordinated meta-analysis of multicenter neuroimaging data. Methods: We analyzed T1-weighted structural magnetic resonance imaging scans assessed with standardized methods from 685 female patients with AN and 963 female healthy control subjects across 22 sites worldwide. In addition to a case-control comparison, we conducted a 3-group analysis comparing healthy control subjects with acutely underweight AN patients (n = 466) and partially weight-restored patients in treatment (n = 251). Results: In AN, reductions in cortical thickness, subcortical volumes, and, to a lesser extent, cortical surface area were sizable (Cohen's d up to 0.95), widespread, and colocalized with hub regions. Highlighting the effects of undernutrition, these deficits were associated with lower body mass index in the AN sample and were less pronounced in partially weight-restored patients. Conclusions: The effect sizes observed for cortical thickness deficits in acute AN are the largest of any psychiatric disorder investigated in the ENIGMA (Enhancing Neuro Imaging Genetics through Meta Analysis) Consortium to date. These results confirm the importance of considering weight loss and renutrition in biomedical research on AN and underscore the importance of treatment engagement to prevent potentially long-lasting structural brain changes in this population.

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