Neurostructural subgroup in 4291 individuals with schizophrenia identified using the subtype and stage inference algorithm

Yuchao Jiang, Cheng Luo, Jijun Wang, Lena Palaniyappan, Xiao Chang, Shitong Xiang, Jie Zhang, Mingjun Duan, Huan Huang, Christian Gaser, Kiyotaka Nemoto, Kenichiro Miura, Ryota Hashimoto, Lars T. Westlye, Genevieve Richard, Sara Fernandez-Cabello, Nadine Parker, Ole A. Andreassen, Tilo Kircher, Igor Nenadić, Frederike Stein, Florian Thomas-Odenthal, Lea Teutenberg, Paula Usemann, Udo Dannlowski, Tim Hahn, Dominik Grotegerd, Susanne Meinert, Rebekka Lencer, Yingying Tang, Tianhong Zhang, Chunbo Li, Weihua Yue, Yuyanan Zhang, Xin Yu, Enpeng Zhou, Ching-Po Lin, Shih-Jen Tsai, Amanda L. Rodrigue, David Glahn, Godfrey Pearlson, John Blangero, Andriana Karuk, Edith Pomarol-Clotet, Raymond Salvador, Paola Fuentes-Claramonte, María Ángeles Garcia-León, Gianfranco Spalletta, Fabrizio Piras, Daniela Vecchio, Nerisa Banaj, Jingliang Cheng, Zhening Liu, Jie Yang, Ali Saffet Gonul, Ozgul Uslu, Birce Begum Burhanoglu, Aslihan Uyar Demir, Kelly Rootes-Murdy, Vince D. Calhoun, Kang Sim, Melissa Green, Yann Quidé, Young Chul Chung, Woo-Sung Kim, Scott R. Sponheim, Caroline Demro, Ian S. Ramsay, Felice Iasevoli, Andrea Bartolomeis, Annarita Barone, Mariateresa Ciccarelli, Arturo Brunetti, Sirio Cocozza, Giuseppe Pontillo, Mario Tranfa, Min Tae M. Park, Matthias Kirschner, Foivos Georgiadis, Stefan Kaiser, Tamsyn E. Rheenen, Susan L. Rossell, Matthew Hughes, William Woods, Sean P. Carruthers, Philip Sumner, Elysha Ringin, Filip Spaniel, Antonin Skoch, David Tomecek, Philipp Homan, Stephanie Homan, Wolfgang Omlor, Giacomo Cecere, Dana D. Nguyen, Adrian Preda, Sophia I. Thomopoulos, Neda Jahanshad, Long-Biao Cui, Dezhong Yao, Paul M. Thompson, Jessica A. Turner, Theo G. M. Erp, Wei Cheng and Jianfeng Feng ()
Additional contact information
Yuchao Jiang: Fudan University
Cheng Luo: University of Electronic Science and Technology of China
Jijun Wang: Shanghai Jiao Tong University School of Medicine
Lena Palaniyappan: McGill University
Xiao Chang: Fudan University
Shitong Xiang: Fudan University
Jie Zhang: Fudan University
Mingjun Duan: University of Electronic Science and Technology of China
Huan Huang: University of Electronic Science and Technology of China
Christian Gaser: Jena University Hospital
Kiyotaka Nemoto: University of Tsukuba
Kenichiro Miura: National Institute of Mental Health, National Center of Neurology and Psychiatry
Ryota Hashimoto: National Institute of Mental Health, National Center of Neurology and Psychiatry
Lars T. Westlye: University of Oslo
Genevieve Richard: University of Oslo
Sara Fernandez-Cabello: University of Oslo
Nadine Parker: Oslo University Hospital & Institute of Clinical Medicine, University of Oslo
Ole A. Andreassen: Oslo University Hospital & Institute of Clinical Medicine, University of Oslo
Tilo Kircher: Philipps Universität Marburg
Igor Nenadić: Philipps Universität Marburg
Frederike Stein: Philipps Universität Marburg
Florian Thomas-Odenthal: Philipps Universität Marburg
Lea Teutenberg: Philipps Universität Marburg
Paula Usemann: Philipps Universität Marburg
Udo Dannlowski: University of Münster
Tim Hahn: University of Münster
Dominik Grotegerd: University of Münster
Susanne Meinert: University of Münster
Rebekka Lencer: University of Münster
Yingying Tang: Shanghai Jiao Tong University School of Medicine
Tianhong Zhang: Shanghai Jiao Tong University School of Medicine
Chunbo Li: Shanghai Jiao Tong University School of Medicine
Weihua Yue: Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital)
Yuyanan Zhang: Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital)
Xin Yu: Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital)
Enpeng Zhou: Peking University Institute of Mental Health, NHC Key Laboratory of Mental Health (Peking University), National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital)
Ching-Po Lin: National Yang Ming Chiao Tung University
Shih-Jen Tsai: Taipei Veterans General Hospital
Amanda L. Rodrigue: Boston Children’s Hospital, Harvard Medical School
David Glahn: Boston Children’s Hospital, Harvard Medical School
Godfrey Pearlson: Institute of Living
John Blangero: University of Texas of the Rio Grande Valley
Andriana Karuk: FIDMAG Germanes Hospitalàries Research Foundation
Edith Pomarol-Clotet: FIDMAG Germanes Hospitalàries Research Foundation
Raymond Salvador: FIDMAG Germanes Hospitalàries Research Foundation
Paola Fuentes-Claramonte: FIDMAG Germanes Hospitalàries Research Foundation
María Ángeles Garcia-León: FIDMAG Germanes Hospitalàries Research Foundation
Gianfranco Spalletta: IRCCS Santa Lucia Foundation
Fabrizio Piras: IRCCS Santa Lucia Foundation
Daniela Vecchio: IRCCS Santa Lucia Foundation
Nerisa Banaj: IRCCS Santa Lucia Foundation
Jingliang Cheng: The First Affiliated Hospital of Zhengzhou University
Zhening Liu: The Second Xiangya Hospital of Central South University
Jie Yang: The Second Xiangya Hospital of Central South University
Ali Saffet Gonul: SoCAT Lab
Ozgul Uslu: Ege University Institute of Health Sciences Department of Neuroscience
Birce Begum Burhanoglu: Ege University Institute of Health Sciences Department of Neuroscience
Aslihan Uyar Demir: SoCAT Lab
Kelly Rootes-Murdy: Emory University]
Vince D. Calhoun: Emory University]
Kang Sim: Institute of Mental Health
Melissa Green: University of New South Wales
Yann Quidé: University of New South Wales
Young Chul Chung: Jeonbuk National University Hospital
Woo-Sung Kim: Jeonbuk National University Hospital
Scott R. Sponheim: University of Minnesota
Caroline Demro: University of Minnesota
Ian S. Ramsay: University of Minnesota
Felice Iasevoli: University “Federico II”
Andrea Bartolomeis: University “Federico II”
Annarita Barone: University “Federico II”
Mariateresa Ciccarelli: University “Federico II”
Arturo Brunetti: University “Federico II”
Sirio Cocozza: University “Federico II”
Giuseppe Pontillo: University “Federico II”
Mario Tranfa: University “Federico II”
Min Tae M. Park: University of Toronto
Matthias Kirschner: University Hospitals of Geneva
Foivos Georgiadis: Psychiatric Hospital University of Zurich
Stefan Kaiser: University Hospitals of Geneva
Tamsyn E. Rheenen: University of Melbourne
Susan L. Rossell: Swinburne University
Matthew Hughes: Swinburne University
William Woods: Swinburne University
Sean P. Carruthers: Swinburne University
Philip Sumner: Swinburne University
Elysha Ringin: National Institute of Mental Health
Filip Spaniel: National Institute of Mental Health
Antonin Skoch: National Institute of Mental Health
David Tomecek: National Institute of Mental Health
Philipp Homan: University of Zurich
Stephanie Homan: Psychiatric University Hospital Zurich
Wolfgang Omlor: University of Zurich
Giacomo Cecere: University of Zurich
Dana D. Nguyen: University of California Irvine
Adrian Preda: University of California Irvine
Sophia I. Thomopoulos: University of Southern California
Neda Jahanshad: University of Southern California
Long-Biao Cui: Fourth Military Medical University
Dezhong Yao: University of Electronic Science and Technology of China
Paul M. Thompson: University of Southern California
Jessica A. Turner: Ohio State Wexner Medical Center
Theo G. M. Erp: University of California Irvine
Wei Cheng: Fudan University
Jianfeng Feng: Fudan University

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Machine learning can be used to define subtypes of psychiatric conditions based on shared biological foundations of mental disorders. Here we analyzed cross-sectional brain images from 4,222 individuals with schizophrenia and 7038 healthy subjects pooled across 41 international cohorts from the ENIGMA, non-ENIGMA cohorts and public datasets. Using the Subtype and Stage Inference (SuStaIn) algorithm, we identify two distinct neurostructural subgroups by mapping the spatial and temporal ‘trajectory’ of gray matter change in schizophrenia. Subgroup 1 was characterized by an early cortical-predominant loss with enlarged striatum, whereas subgroup 2 displayed an early subcortical-predominant loss in the hippocampus, striatum and other subcortical regions. We confirmed the reproducibility of the two neurostructural subtypes across various sample sites, including Europe, North America and East Asia. This imaging-based taxonomy holds the potential to identify individuals with shared neurobiological attributes, thereby suggesting the viability of redefining existing disorder constructs based on biological factors.

Date: 2024
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DOI: 10.1038/s41467-024-50267-3

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