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      What we learn about bipolar disorder from large‐scale neuroimaging: Findings and future directions from the ENIGMA Bipolar Disorder Working Group

      review-article
      Author(s): 1 , , 2 , 3 , 4 , 5 , 6 , 1 , 6 , 7 , 3 , 8 , 9 , 10 , 11 , 10 , 12 , 13 , 14 , 15 , 4 , 16 , 4 , 17 , 14 , 15 , 18 , 19 , 20 , 21 , 22 , 10 , 1 , 10 , 23 , 13 , 14 , 23 , 24 , 8 , 25 , 26 , 27 , 28 , 10 , 29 , 25 , 30 , 21 , 1 , 31 , 4 , 32 , 3 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 44 , 25 , 30 , 51 , 52 , 33 , 34 , 53 , 54 , 55 , 56 , 57 , 37 , 51 , 58 , 59 , 60 , 14 , 17 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 25 , 30 , 67 , 70 , 37 , 71 , 72 , 73 , 74 , 75 , 76 , 75 , 77 , 78 , 78 , 79 , 71 , 80 , 58 , 81 , 82 , 83 , 84 , 43 , 44 , 70 , 78 , 85 , 86 , 87 , 79 , 88 , 89 , 90 , 67 , 35 , 91 , 92 , 43 , 44 , 93 , 94 , 33 , 34 , 93 , 67 , 70 , 95 , 70 , 96 , 97 , 33 , 34 , 33 , 34 , 98 , 96 , 99 , 100 , 101 , 102 , 79 , 75 , 76 , 103 , 3 , 8 , 104 , 105 , 106 , 58 , 107 , 108 , 109 , 110 , 111 , 98 , 102 , 112 , 113 , 114 , 1 , 3 , 4 , ENIGMA Bipolar Disorder Working Group
      Publication date (Electronic):
      Journal: Human Brain Mapping
      Publisher: John Wiley & Sons, Inc.
      Keywords: bipolar disorder, cortical surface area, cortical thickness, ENIGMA, mega‐analysis, meta‐analysis, MRI, neuroimaging, psychiatry, volume

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          Abstract

          MRI‐derived brain measures offer a link between genes, the environment and behavior and have been widely studied in bipolar disorder (BD). However, many neuroimaging studies of BD have been underpowered, leading to varied results and uncertainty regarding effects. The Enhancing Neuro Imaging Genetics through Meta‐Analysis (ENIGMA) Bipolar Disorder Working Group was formed in 2012 to empower discoveries, generate consensus findings and inform future hypothesis‐driven studies of BD. Through this effort, over 150 researchers from 20 countries and 55 institutions pool data and resources to produce the largest neuroimaging studies of BD ever conducted. The ENIGMA Bipolar Disorder Working Group applies standardized processing and analysis techniques to empower large‐scale meta‐ and mega‐analyses of multimodal brain MRI and improve the replicability of studies relating brain variation to clinical and genetic data. Initial BD Working Group studies reveal widespread patterns of lower cortical thickness, subcortical volume and disrupted white matter integrity associated with BD. Findings also include mapping brain alterations of common medications like lithium, symptom patterns and clinical risk profiles and have provided further insights into the pathophysiological mechanisms of BD. Here we discuss key findings from the BD working group, its ongoing projects and future directions for large‐scale, collaborative studies of mental illness.

          Abstract

          This review discusses the major challenges facing neuroimaging research of bipolar disorder and highlights the major accomplishments, ongoing challenges and future goals of the ENIGMA Bipolar Disorder Working Group.

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          Most cited references145

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          Diagnostic and Statistical Manual of Mental Disorders

          American Psychiatric Association (2013)
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            NIA-AA Research Framework: Toward a biological definition of Alzheimer’s disease

            Clifford R. Jack, David Bennett, Kaj Blennow … (2018)
            In 2011, the National Institute on Aging and Alzheimer’s Association created separate diagnostic recommendations for the preclinical, mild cognitive impairment, and dementia stages of Alzheimer’s disease. Scientific progress in the interim led to an initiative by the National Institute on Aging and Alzheimer’s Association to update and unify the 2011 guidelines. This unifying update is labeled a “research framework” because its intended use is for observational and interventional research, not routine clinical care. In the National Institute on Aging and Alzheimer’s Association Research Framework, Alzheimer’s disease (AD) is defined by its underlying pathologic processes that can be documented by postmortem examination or in vivo by biomarkers. The diagnosis is not based on the clinical consequences of the disease (i.e., symptoms/signs) in this research framework, which shifts the definition of AD in living people from a syndromal to a biological construct. The research framework focuses on the diagnosis of AD with biomarkers in living persons. Biomarkers are grouped into those of β amyloid deposition, pathologic tau, and neurodegeneration [AT(N)]. This ATN classification system groups different biomarkers (imaging and biofluids) by the pathologic process each measures. The AT(N) system is flexible in that new biomarkers can be added to the three existing AT(N) groups, and new biomarker groups beyond AT(N) can be added when they become available. We focus on AD as a continuum, and cognitive staging may be accomplished using continuous measures. However, we also outline two different categorical cognitive schemes for staging the severity of cognitive impairment: a scheme using three traditional syndromal categories and a six-stage numeric scheme. It is important to stress that this framework seeks to create a common language with which investigators can generate and test hypotheses about the interactions among different pathologic processes (denoted by biomarkers) and cognitive symptoms. We appreciate the concern that this biomarker-based research framework has the potential to be misused. Therefore, we emphasize, first, it is premature and inappropriate to use this research framework in general medical practice. Second, this research framework should not be used to restrict alternative approaches to hypothesis testing that do not use biomarkers. There will be situations where biomarkers are not available or requiring them would be counterproductive to the specific research goals (discussed in more detail later in the document). Thus, biomarker-based research should not be considered a template for all research into age-related cognitive impairment and dementia; rather, it should be applied when it is fit for the purpose of the specific research goals of a study. Importantly, this framework should be examined in diverse populations. Although it is possible that β-amyloid plaques and neurofibrillary tau deposits are not causal in AD pathogenesis, it is these abnormal protein deposits that define AD as a unique neurodegenerative disease among different disorders that can lead to dementia. We envision that defining AD as a biological construct will enable a more accurate characterization and understanding of the sequence of events that lead to cognitive impairment that is associated with AD, as well as the multifactorial etiology of dementia. This approach also will enable a more precise approach to interventional trials where specific pathways can be targeted in the disease process and in the appropriate people.
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              Biological Insights From 108 Schizophrenia-Associated Genetic Loci

              Stephan Ripke, Benjamin M. Neale, Aiden Corvin … (2015)
              Summary Schizophrenia is a highly heritable disorder. Genetic risk is conferred by a large number of alleles, including common alleles of small effect that might be detected by genome-wide association studies. Here, we report a multi-stage schizophrenia genome-wide association study of up to 36,989 cases and 113,075 controls. We identify 128 independent associations spanning 108 conservatively defined loci that meet genome-wide significance, 83 of which have not been previously reported. Associations were enriched among genes expressed in brain providing biological plausibility for the findings. Many findings have the potential to provide entirely novel insights into aetiology, but associations at DRD2 and multiple genes involved in glutamatergic neurotransmission highlight molecules of known and potential therapeutic relevance to schizophrenia, and are consistent with leading pathophysiological hypotheses. Independent of genes expressed in brain, associations were enriched among genes expressed in tissues that play important roles in immunity, providing support for the hypothesized link between the immune system and schizophrenia.
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                Author and article information

                Contributors
                Christopher R. K. Ching:
                ORCID: https://orcid.org/0000-0003-2921-3408
                cching47@gmail.com
                Bradley J. MacIntosh:
                ORCID: https://orcid.org/0000-0001-7300-2355
                bmac@sri.utoronto.ca
                Journal
                Journal ID (nlm-ta): Hum Brain Mapp
                Journal ID (iso-abbrev): Hum Brain Mapp
                Journal ID (doi): 10.1002/(ISSN)1097-0193
                Journal ID (publisher-id): HBM
                Title: Human Brain Mapping
                Publisher: John Wiley & Sons, Inc. (Hoboken, USA )
                ISSN (Print): 1065-9471
                ISSN (Electronic): 1097-0193
                Publication date (Electronic): 29 July 2020
                Publication date Collection: January 2022
                Volume: 43
                Issue: 1 , The ENIGMA Consortium: the first 10 years ( doiID: 10.1002/hbm.v43.1 )
                Pages: 56-82
                Affiliations
                [ 1 ] Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine University of Southern California Los Angeles California USA
                [ 2 ] Genentech, Inc. South San Francisco California USA
                [ 3 ] Norwegian Centre for Mental Disorders Research (NORMENT), Institute of Clinical Medicine, University of Oslo Oslo Norway
                [ 4 ] Division of Mental Health and Addicition, Oslo University Hospital Oslo Norway
                [ 5 ] Department of Psychiatry Dalhousie University Halifax Nova Scotia Canada
                [ 6 ] Faculty of Computer Science Dalhousie University Halifax Nova Scotia Canada
                [ 7 ] Department of Clinical Neuroscience Karolinska Institutet Stockholm Sweden
                [ 8 ] Department of Psychiatric Research Diakonhjemmet Hospital Oslo Norway
                [ 9 ] Center for Psychiatric Research, Department of Clinical Neuroscience Karolinska Institutet Stockholm Sweden
                [ 10 ] Department of Psychiatry, University Medical Center Utrecht Brain Center, University Medical Center Utrecht Utrecht University Utrecht The Netherlands
                [ 11 ] Centre for Neuroimaging & Cognitive Genomics (NICOG), Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine Nursing and Health Sciences National University of Ireland Galway Galway Ireland
                [ 12 ] Department of Psychiatry University of California La Jolla California USA
                [ 13 ] Desert‐Pacific MIRECC VA San Diego Healthcare San Diego California USA
                [ 14 ] INSERM U955, team 15 “Translational Neuro‐Psychiatry” Créteil France
                [ 15 ] Neurospin, CEA Paris‐Saclay, team UNIACT Gif‐sur‐Yvette France
                [ 16 ] National Institute of Mental Health Klecany Czech Republic
                [ 17 ] Norwegian Centre for Mental Disorders Research (NORMENT) Oslo University Hospital Oslo Norway
                [ 18 ] APHP Mondor University Hospitals, DMU IMPACT Créteil France
                [ 19 ] Department of Neuroscience and Physiology University of Gothenburg Gothenburg Sweden
                [ 20 ] Department of Medical Epidemiology and Biostatistics Karolinska Institutet Stockholm Sweden
                [ 21 ] Department for Psychiatry and Psychotherapy Charité Universitätsmedizin Berlin Berlin Germany
                [ 22 ] Department of Neurology with Experimental Neurology Charité Universitätsmedizin Berlin Berlin Germany
                [ 23 ] Bloorview Research Institute Holland Bloorview Kids Rehabilitation Hospital Toronto Ontario Canada
                [ 24 ] Departments of Psychology and Psychiatry University of Toronto Toronto Ontario Canada
                [ 25 ] Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS) Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM) Barcelona Spain
                [ 26 ] Early Psychosis: Interventions and Clinical‐detection (EPIC) lab, Department of Psychosis Studies Institute of Psychiatry, Psychology and Neuroscience, King's College London London UK
                [ 27 ] Stockholm Health Care Services Stockholm County Council Stockholm Sweden
                [ 28 ] Mood Disorders Unit (GRUDA), Hospital das Clinicas HCFMUSP, Faculdade de Medicina Universidade de São Paulo São Paulo SP Brazil
                [ 29 ] Department of Child and Adolescent Psychiatry/Psychology Erasmus Medical Center Rotterdam The Netherlands
                [ 30 ] Barcelona Bipolar Disorders and Depressive Unit, Hospital Clinic, Institute of Neurosciences University of Barcelona Barcelona Spain
                [ 31 ] College of Intelligence Science and Technology National University of Defense Technology Changsha China
                [ 32 ] Dell Medical School The University of Texas at Austin Austin Texas USA
                [ 33 ] FIDMAG Germanes Hospitalàries Research Foundation Barcelona Spain
                [ 34 ] CIBERSAM Madrid Spain
                [ 35 ] Milken Institute Center for Strategic Philanthropy Washington District of Columbia USA
                [ 36 ] Department of Psychiatry and Psychotherapy, Medical Faculty Technische Universität Dresden Dresden Germany
                [ 37 ] Department of Psychiatry University of Münster Münster Germany
                [ 38 ] Department of Psychiatry The University of Melbourne Melbourne Victoria Australia
                [ 39 ] The Florey Institute of Neuroscience and Mental Health The University of Melbourne Melbourne Victoria Australia
                [ 40 ] Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior University of California Los Angeles California USA
                [ 41 ] Department of Psychology University of California Los Angeles California USA
                [ 42 ] Section of Psychiatry, Department of Neurosciences, Biomedicine and Movement Sciences University of Verona Verona Italy
                [ 43 ] Vita‐Salute San Raffaele University Milan Italy
                [ 44 ] Division of Neuroscience, Psychiatry and Psychobiology Unit IRCCS San Raffaele Scientific Institute Milan Italy
                [ 45 ] Department of Pathophysiology and Transplantation University of Milan Milan Italy
                [ 46 ] IMPACT Institute – The Institute for Mental and Physical Health and Clinical Translation, School of Medicine, Barwon Health Deakin University Geelong Victoria Australia
                [ 47 ] The National Centre of Excellence in Youth Mental Health, Centre for Youth Mental Health, Florey Institute for Neuroscience and Mental Health and the Department of Psychiatry, The University of Melbourne Orygen Melbourne Victoria Australia
                [ 48 ] P1vital Ltd Wallingford UK
                [ 49 ] Department of Psychiatry University of Oxford Oxford UK
                [ 50 ] Mood Disorders Research Program Yale School of Medicine New Haven Connecticut USA
                [ 51 ] Psychosomatic and CL Psychiatry Oslo University Hospital Oslo Norway
                [ 52 ] Department of Neurosciences and Mental Health Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico Milan Italy
                [ 53 ] Department of Radiology Centre Hospitalier Universitaire Vaudois (CHUV) Lausanne Switzerland
                [ 54 ] Signal Processing Lab (LTS5), École Polytechnique Fédérale de Lausanne Lausanne Switzerland
                [ 55 ] MRC Centre for Neuropsychiatric Genetics and Genomics Cardiff University Cardiff UK
                [ 56 ] Melbourne Neuropsychiatry Centre, Department of Psychiatry University of Melbourne and Melbourne Health Melbourne Victoria Australia
                [ 57 ] Brain, Mind and Society Research Hub, Turner Institute for Brain and Mental Health, School of Psychological Sciences Monash University Clayton Victoria Australia
                [ 58 ] Research Group in Psychiatry GIPSI, Department of Psychiatry Faculty of Medicine, Universidad de Antioquia Medellín Colombia
                [ 59 ] Department of Psychology, School of Social Sciences and Arts City, University of London London UK
                [ 60 ] Department of Neuroimaging, Institute of Psychiatry, Psychology & Neuroscience King's College London London UK
                [ 61 ] Department of Neurology Oslo University Hospital Oslo Norway
                [ 62 ] Institute of Clinical Medicine University of Oslo Oslo Norway
                [ 63 ] Center for Neurobehavioral Genetics Los Angeles California USA
                [ 64 ] Greater Los Angeles Veterans Administration Los Angeles California USA
                [ 65 ] Centre for Brain Health University of British Columbia Vancouver British Columbia Canada
                [ 66 ] Department of Psychiatry Icahn School of Medicine at Mount Sinai New York New York USA
                [ 67 ] Neuroscience Research Australia Randwick New South Wales Australia
                [ 68 ] School of Medical Sciences University of New South Wales Sydney New South Wales Australia
                [ 69 ] Department of Psychiatry Boston Children's Hospital and Harvard Medical School Boston Massachusetts USA
                [ 70 ] School of Psychiatry University of New South Wales Sydney New South Wales Australia
                [ 71 ] Department of General Psychiatry Heidelberg University Heidelberg Germany
                [ 72 ] Department of Psychiatry, University Medical Center Groningen University of Groningen Groningen The Netherlands
                [ 73 ] Department of Psychiatry Service Hospitalo‐Universitaire, GHU Paris Psychiatrie & Neurosciences Paris France
                [ 74 ] Université de Paris Paris France
                [ 75 ] Neuroscience Institute University of Cape Town Cape Town South Africa
                [ 76 ] Department of Psychiatry and Mental Health University of Cape Town Cape Town South Africa
                [ 77 ] Core‐Facility Brainimaging, Faculty of Medicine University of Marburg Marburg Germany
                [ 78 ] Department of Psychiatry and Psychotherapy Philipps‐University Marburg Marburg Germany
                [ 79 ] Department of Psychiatry, Psychosomatic Medicine and Psychotherapy Goethe University Frankfurt Frankfurt Germany
                [ 80 ] Laboratory of Psychiatric Neuroimaging (LIM‐21), Departamento e Instituto de Psiquiatria Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo São Paulo SP Brazil
                [ 81 ] Mood Disorders Program Hospital Universitario Trastorno del Ánimo Medellín Colombia
                [ 82 ] Experimental Therapeutics and Molecular Pathophysiology Program, Department of Psychiatry UTHealth, University of Texas Houston Texas USA
                [ 83 ] Hurvitz Brain Sciences Sunnybrook Research Institute Toronto Ontario Canada
                [ 84 ] Department of Medical Biophysics University of Toronto Toronto Ontario Canada
                [ 85 ] University of Cincinnati Cincinnati Ohio USA
                [ 86 ] Universidade de São Paulo São Paulo SP Brazil
                [ 87 ] MEG Core Facility Bethesda Maryland USA
                [ 88 ] UCLA Center for Neurobehavioral Genetics Los Angeles California USA
                [ 89 ] Department of Psychiatry Erasmus Medical Center, Erasmus University Rotterdam The Netherlands
                [ 90 ] Department of Mental Disorder Research National Institute of Neuroscience, National Center of Neurology and Psychiatry Tokyo Japan
                [ 91 ] Department of Psychiatry University of Pittsburgh Pittsburgh Pennsylvania USA
                [ 92 ] Research Group Instituto de Alta Tecnología Médica (IATM) Medellín Colombia
                [ 93 ] University of Grenoble Alpes CHU Grenoble Alpes Grenoble France
                [ 94 ] INSERM U1216 ‐ Grenoble Institut des Neurosciences La Tronche France
                [ 95 ] Department of Psychiatry Amsterdam UMC, location AMC Amsterdam The Netherlands
                [ 96 ] Department of Psychiatry Radboud University Medical Center Nijmegen The Netherlands
                [ 97 ] Donders Institute for Brain, Cognition and Behavior Radboud University Nijmegen The Netherlands
                [ 98 ] Department of Psychiatry University of Pennsylvania Perelman School of Medicine Philadelphia Pennsylvania USA
                [ 99 ] West Region, Institute of Mental Health Singapore Singapore
                [ 100 ] Yong Loo Lin School of Medicine National University of Singapore Singapore Singapore
                [ 101 ] Center of Excellent on Mood Disorders UTHealth Houston Houston Texas USA
                [ 102 ] Department of Psychiatry and Behavioral Sciences UTHealth Houston Houston Texas USA
                [ 103 ] SAMRC Unit on Risk & Resilience in Mental Disorders University of Cape Town Cape Town South Africa
                [ 104 ] PROMENTA Research Center, Department of Psychology University of Oslo Oslo Norway
                [ 105 ] Papanikolaou General Hospital Thessaloniki Greece
                [ 106 ] Laboratory of Mechanics and Materials School of Engineering, Aristotle University Thessaloniki Greece
                [ 107 ] Department of Psychiatry Amsterdam UMC Amsterdam The Netherlands
                [ 108 ] Department of Neuropsychology and Clinical Psychology Johannes Gutenberg‐University Mainz Mainz Germany
                [ 109 ] Department of Psychology University of Oslo Oslo Norway
                [ 110 ] Norwegian Centre for Mental Disorders Research (NORMENT), Department of Mental Health and Addiction Oslo University Hospital Oslo Norway
                [ 111 ] Centre for Clinical Brain Sciences University of Edinburgh Edinburgh UK
                [ 112 ] Department of Psychiatry University of British Columbia Vancouver British Columbia Canada
                [ 113 ] Chief Experimental Therapeutics & Pathophysiology Branch Bethesda Maryland USA
                [ 114 ] Intramural Research Program National Institute of Mental Health Bethesda Maryland USA
                Author notes
                [*] [* ] Correspondence

                Christopher R. K. Ching, Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA.

                Email: cching47@ 123456gmail.com

                Author information
                https://orcid.org/0000-0003-2921-3408
                https://orcid.org/0000-0002-1272-7616
                https://orcid.org/0000-0003-0281-8458
                https://orcid.org/0000-0002-0363-4127
                https://orcid.org/0000-0002-8516-923X
                https://orcid.org/0000-0002-4749-6977
                https://orcid.org/0000-0002-9006-8863
                https://orcid.org/0000-0001-9759-2556
                https://orcid.org/0000-0001-7300-2355
                https://orcid.org/0000-0002-8569-7139
                https://orcid.org/0000-0002-2621-2920
                Article
                Publisher ID: HBM25098
                DOI: 10.1002/hbm.25098
                PMC ID: 8675426
                PubMed ID: 32725849
                SO-VID: 7f6ae031-e125-4bca-b2b3-1fe2e4a8544f
                Copyright © © 2020 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date revision received : 31 May 2020
                Date received : 31 March 2020
                Date accepted : 04 June 2020
                Page count
                Figures: 10, Tables: 0, Pages: 27, Words: 21469
                Categories
                Subject: Review Article
                Subject: Review Articles
                Custom metadata
                source-schema-version-number 2.0
                cover-date January 2022
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.7.0 mode:remove_FC converted:16.12.2021

                ScienceOpen disciplines: Neurology
                Keywords: bipolar disorder,cortical surface area,cortical thickness,enigma,mega‐analysis,meta‐analysis,mri,neuroimaging,psychiatry,volume
                Data availability:
                ScienceOpen disciplines: Neurology
                Keywords: bipolar disorder, cortical surface area, cortical thickness, enigma, mega‐analysis, meta‐analysis, mri, neuroimaging, psychiatry, volume

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