A meta-analysis of deep brain structural shape and asymmetry abnormalities in 2,833 individuals with schizophrenia compared with 3,929 healthy volunteers via the ENIGMA Consortium,Human Brain Mapping

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A meta-analysis of deep brain structural shape and asymmetry abnormalities in 2,833 individuals with schizophrenia compared with 3,929 healthy volunteers via the ENIGMA Consortium
Human Brain Mapping ( IF 4.8 ) Pub Date : 2021-09-08 , DOI: 10.1002/hbm.25625
Boris A Gutman _{1,

2} , Theo G M van Erp _{3,

4} , Kathryn Alpert ₅ , Christopher R K Ching ₆ , Dmitry Isaev ₇ , Anjani Ragothaman ₈ , Neda Jahanshad ₆ , Arvin Saremi ₆ , Artemis Zavaliangos-Petropulu ₆ , David C Glahn ₉ , Li Shen ₁₀ , Shan Cong ₁₀ , Dag Alnaes ₁₁ , Ole Andreas Andreassen ₁₁ , Nhat Trung Doan ₁₁ , Lars T Westlye _{11,

12} , Peter Kochunov ₁₃ , Theodore D Satterthwaite ₁₄ , Daniel H Wolf ₁₄ , Alexander J Huang ₃ , Charles Kessler ₃ , Andrea Weideman ₃ , Dana Nguyen ₁₅ , Bryon A Mueller ₁₆ , Lawrence Faziola ₁₇ , Steven G Potkin ₁₇ , Adrian Preda ₁₇ , Daniel H Mathalon _{18,

19} , Juan Bustillo ₂₀ , Vince Calhoun _{21,

22} , Judith M Ford _{19,

23} , Esther Walton ₂₄ , Stefan Ehrlich ₂₅ , Giuseppe Ducci ₂₆ , Nerisa Banaj ₂₇ , Fabrizio Piras ₂₇ , Federica Piras ₂₇ , Gianfranco Spalletta _{27,

28} , Erick J Canales-Rodríguez ₂₉ , Paola Fuentes-Claramonte ₂₉ , Edith Pomarol-Clotet ₂₉ , Joaquim Radua _{29,

30} , Raymond Salvador ₂₉ , Salvador Sarró ₂₉ , Erin W Dickie ₃₁ , Aristotle Voineskos ₃₁ , Diana Tordesillas-Gutiérrez ₃₂ , Benedicto Crespo-Facorro ₃₃ , Esther Setién-Suero ₃₄ , Jacqueline Mayoral van Son ₃₃ , Stefan Borgwardt _{35,

36} , Fabienne Schönborn-Harrisberger ₃₅ , Derek Morris ₃₇ , Gary Donohoe ₃₈ , Laurena Holleran ₃₈ , Dara Cannon ₃₉ , Colm McDonald ₃₉ , Aiden Corvin _{40,

41} , Michael Gill _{40,

41} , Geraldo Busatto Filho ₄₂ , Pedro G P Rosa ₄₂ , Mauricio H Serpa ₄₂ , Marcus V Zanetti _{42,

43} , Irina Lebedeva ₄₄ , Vasily Kaleda ₄₅ , Alexander Tomyshev ₄₄ , Tim Crow ₄₆ , Anthony James ₄₆ , Simon Cervenka ₄₇ , Carl M Sellgren ₄₈ , Helena Fatouros-Bergman ₄₇ , Ingrid Agartz ₁₁ , Fleur Howells _{49,

50} , Dan J Stein _{49,

50,

51} , Henk Temmingh ₄₉ , Anne Uhlmann _{49,

52} , Greig I de Zubicaray ₅₃ , Katie L McMahon ₅₄ , Margie Wright ₅₅ , Derin Cobia _{5,

56} , John G Csernansky ₅ , Paul M Thompson ₆ , Jessica A Turner ₅₇ , Lei Wang _{5,

58}

Affiliation

Department of Biomedical Engineering, Illinois Institute of Technology, Chicago, Illinois, USA.
Institute for Information Transmission Problems (Kharkevich Institute), Moscow, Russia.
Clinical Translational Neuroscience Laboratory, Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, California, USA.
Center for the Neurobiology of Learning and Memory, University of California Irvine, Irvine, California, USA.
Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Imaging Genetics Center, Mark & Mary Stevens Neuroimaging & Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
Department of Biomedical Engineering, Duke University, Durham, North Carolina, USA.
Department of biomedical engineering, Oregon Health and Science university, Portland, Oregon, USA.
Department of Psychiatry, Boston Children's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
Department of Psychology, University of Oslo, Oslo, Norway.
Department of Psychiatry, University of Maryland School of Medicine, Baltimore, Maryland, USA.
Department of Psychiatry, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA.
Department of Pediatrics, University of California Irvine, Irvine, California, USA.
Department of Psychiatry and Behavioral Sciences, University of Minnesota, Minneapolis, Minnesota, USA.
Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, California, USA.
Department of Psychiatry and Weill Institute for Neurosciences, University of California San Francisco, San Francisco, California, USA.
Judith Ford Mental Health, VA San Francisco Healthcare System, San Francisco, California, USA.
Departments of Psychiatry & Neuroscience, University of New Mexico, Albuquerque, New Mexico, USA.
Tri-institutional Center for Translational Research in Neuroimaging and Data Science (TReNDS) [Georgia State University, Georgia Institute of Technology], Emory University, Atlanta, Georgia, USA.
Department of Electrical and Computer Engineering, The University of New Mexico, Albuquerque, New Mexico, USA.
Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, California, USA.
Department of Psychology, University of Bath, Bath, UK.
Division of Psychological & Social Medicine and Developmental Neurosciences, Faculty of Medicine, TU-Dresden, Dresden, Germany.
Mental Health Department, ASL Roma1 DSM, Rome, Italy.
Laboratory of Neuropsychiatry, IRCCS Santa Lucia Foundation, Rome, Italy.
Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas, USA.
FIDMAG Germanes Hospitalàries Research Foundation, CIBERSAM, Barcelona, Spain.
Institut d'Investigacions Biomdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
Centre for Addiction and Mental Health (CAMH), Toronto, Canada.
Department of Radiology, IDIVAL, Marqués de Valdecilla University Hospital, Santander, Spain.
University Hospital Virgen del Rocio, IBiS, University of Sevilla, CIBERSAM, Sevilla, Spain.
University Hospital Marqués de Valdecilla, IDIVAL, CIBERSAM, Santander, Spain.
Department of Psychiatry, University of Basel, Basel, Switzerland.
Department of Psychiatry and Psychotherapy, University of Lübeck, Lübeck, Germany.
Centre for Neuroimaging and Cognitive Genomics, Discipline of Biochemistry, National University of Ireland Galway, Galway, Ireland.
Centre for Neuroimaging and Cognitive Genomics, School of Psychology, National University of Ireland Galway, Galway, Ireland.
Clinical Neuroimaging Laboratory, Centre for Neuroimaging and Cognitive Genomics, National University of Ireland Galway, Galway, Ireland.
Neuropsychiatric Genetics Research Group, Department of Psychiatry, Trinity College Dublin, Dublin, Ireland.
Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland.
Laboratory of Psychiatric Neuroimaging (LIM-21), Departamento e Instituto de Psiquiatria, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.
Hospital Sirio-Libanes, Sao Paulo, SP, Brazil.
Laboratory of Neuroimaging and Multimodal Analysis, Mental Health Research Center, Moscow, Russia.
Department of Endogenous Mental Disorders, Mental Health Research Center, Moscow, Russia.
Department of Psychiatry, University of Oxford, Oxford, UK.
Centre for Psychiatry Reserach, Department of Clinical Neuroscience, Karolinska Institutet, & Stockholm Health Care Services, Region Stockholm, Stockholm, Sweden.
Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden.
Department of Psychiatry and Mental Health, Faculty of Health Sciences, University of Cape Town, Cape Town, WC, South Africa.
Neuroscience Institute, University of Cape Town, Cape Town, WC, South Africa.
SA MRC Unit on Risk & Resilience in Mental Disorders, University of Cape Town, Cape Town, WC, South Africa.
Department of Child and Adolescent Psychiatry, TU Dresden, Germany.
School of Psychology, Faculty of Health, Queensland University of Technology (QUT), Brisbane, QLD, Australia.
School of Clinical Sciences, Queensland University of Technology (QUT), Brisbane, QLD, Australia.
Queensland Brain Institute, University of Queensland, Brisbane, QLD, Australia.
Department of Psychology and Neuroscience Center, Brigham Young University, Provo, Utah, USA.
Psychology & Neuroscience, Georgia State University, Atlanta, Georgia, USA.
Department of Psychiatry and Behavioral Health, Ohio State University Wexner Medical Center, Columbus, Ohio, USA.

Schizophrenia is associated with widespread alterations in subcortical brain structure. While analytic methods have enabled more detailed morphometric characterization, findings are often equivocal. In this meta-analysis, we employed the harmonized ENIGMA shape analysis protocols to collaboratively investigate subcortical brain structure shape differences between individuals with schizophrenia and healthy control participants. The study analyzed data from 2,833 individuals with schizophrenia and 3,929 healthy control participants contributed by 21 worldwide research groups participating in the ENIGMA Schizophrenia Working Group. Harmonized shape analysis protocols were applied to each site's data independently for bilateral hippocampus, amygdala, caudate, accumbens, putamen, pallidum, and thalamus obtained from T1-weighted structural MRI scans. Mass univariate meta-analyses revealed more-concave-than-convex shape differences in the hippocampus, amygdala, accumbens, and thalamus in individuals with schizophrenia compared with control participants, more-convex-than-concave shape differences in the putamen and pallidum, and both concave and convex shape differences in the caudate. Patterns of exaggerated asymmetry were observed across the hippocampus, amygdala, and thalamus in individuals with schizophrenia compared to control participants, while diminished asymmetry encompassed ventral striatum and ventral and dorsal thalamus. Our analyses also revealed that higher chlorpromazine dose equivalents and increased positive symptom levels were associated with patterns of contiguous convex shape differences across multiple subcortical structures. Findings from our shape meta-analysis suggest that common neurobiological mechanisms may contribute to gray matter reduction across multiple subcortical regions, thus enhancing our understanding of the nature of network disorganization in schizophrenia.

中文翻译：

通过 ENIGMA 联盟对 2,833 名精神分裂症患者与 3,929 名健康志愿者进行的深部大脑结构形状和不对称异常的荟萃分析

精神分裂症与皮层下大脑结构的广泛改变有关。虽然分析方法已经实现了更详细的形态表征，但结果往往模棱两可。在这项荟萃分析中，我们采用统一的 ENIGMA 形状分析协议来协作研究精神分裂症患者和健康对照参与者之间的皮层下大脑结构形状差异。该研究分析了 2,833 名精神分裂症患者和 3,929 名健康对照参与者的数据，这些数据由参与 ENIGMA 精神分裂症工作组的 21 个全球研究小组提供。从 T1 加权结构 MRI 扫描获得的双侧海马、杏仁核、尾状核、伏隔核、壳核、苍白球和丘脑的数据独立应用于每个部位的协调形状分析协议。大规模单变量荟萃分析显示，与对照组相比，精神分裂症患者的海马、杏仁核、伏隔核和丘脑的形状差异更大，壳核和苍白球的形状差异更大，并且尾状核的凹凸形状均有差异。与对照组相比，在精神分裂症患者的海马、杏仁核和丘脑中观察到夸张的不对称模式，而腹侧纹状体、腹侧和背侧丘脑的不对称性减弱。我们的分析还表明，较高的氯丙嗪剂量当量和增加的阳性症状水平与多个皮质下结构的连续凸形差异模式相关。

更新日期：2021-09-08

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