Longitudinal Structural Brain Changes in Bipolar Disorder: A Multicenter Neuroimaging Study of 1232 Individuals by the ENIGMA Bipolar Disorder Working Group.


Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
15 03 2022
Historique:
received: 30 04 2021
revised: 24 08 2021
accepted: 10 09 2021
pubmed: 24 11 2021
medline: 20 4 2022
entrez: 23 11 2021
Statut: ppublish

Résumé

Bipolar disorder (BD) is associated with cortical and subcortical structural brain abnormalities. It is unclear whether such alterations progressively change over time, and how this is related to the number of mood episodes. To address this question, we analyzed a large and diverse international sample with longitudinal magnetic resonance imaging (MRI) and clinical data to examine structural brain changes over time in BD. Longitudinal structural MRI and clinical data from the ENIGMA (Enhancing Neuro Imaging Genetics through Meta Analysis) BD Working Group, including 307 patients with BD and 925 healthy control subjects, were collected from 14 sites worldwide. Male and female participants, aged 40 ± 17 years, underwent MRI at 2 time points. Cortical thickness, surface area, and subcortical volumes were estimated using FreeSurfer. Annualized change rates for each imaging phenotype were compared between patients with BD and healthy control subjects. Within patients, we related brain change rates to the number of mood episodes between time points and tested for effects of demographic and clinical variables. Compared with healthy control subjects, patients with BD showed faster enlargement of ventricular volumes and slower thinning of the fusiform and parahippocampal cortex (0.18 <d < 0.22). More (hypo)manic episodes were associated with faster cortical thinning, primarily in the prefrontal cortex. In the hitherto largest longitudinal MRI study on BD, we did not detect accelerated cortical thinning but noted faster ventricular enlargements in BD. However, abnormal frontocortical thinning was observed in association with frequent manic episodes. Our study yields insights into disease progression in BD and highlights the importance of mania prevention in BD treatment.

Sections du résumé

BACKGROUND
Bipolar disorder (BD) is associated with cortical and subcortical structural brain abnormalities. It is unclear whether such alterations progressively change over time, and how this is related to the number of mood episodes. To address this question, we analyzed a large and diverse international sample with longitudinal magnetic resonance imaging (MRI) and clinical data to examine structural brain changes over time in BD.
METHODS
Longitudinal structural MRI and clinical data from the ENIGMA (Enhancing Neuro Imaging Genetics through Meta Analysis) BD Working Group, including 307 patients with BD and 925 healthy control subjects, were collected from 14 sites worldwide. Male and female participants, aged 40 ± 17 years, underwent MRI at 2 time points. Cortical thickness, surface area, and subcortical volumes were estimated using FreeSurfer. Annualized change rates for each imaging phenotype were compared between patients with BD and healthy control subjects. Within patients, we related brain change rates to the number of mood episodes between time points and tested for effects of demographic and clinical variables.
RESULTS
Compared with healthy control subjects, patients with BD showed faster enlargement of ventricular volumes and slower thinning of the fusiform and parahippocampal cortex (0.18 <d < 0.22). More (hypo)manic episodes were associated with faster cortical thinning, primarily in the prefrontal cortex.
CONCLUSIONS
In the hitherto largest longitudinal MRI study on BD, we did not detect accelerated cortical thinning but noted faster ventricular enlargements in BD. However, abnormal frontocortical thinning was observed in association with frequent manic episodes. Our study yields insights into disease progression in BD and highlights the importance of mania prevention in BD treatment.

Identifiants

pubmed: 34809987
pii: S0006-3223(21)01597-3
doi: 10.1016/j.biopsych.2021.09.008
pii:
doi:

Types de publication

Journal Article Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

582-592

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2021 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Christoph Abé (C)

Department of Clinical Neuroscience, Osher Center, Karolinska Institutet, Stockholm, Sweden. Electronic address: christoph.abe@ki.se.

Christopher R K Ching (CRK)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, University of Southern California, Los Angeles, California.

Benny Liberg (B)

Department of Clinical Neuroscience, Osher Center, Karolinska Institutet, Stockholm, Sweden.

Alexander V Lebedev (AV)

Department of Clinical Neuroscience, Osher Center, Karolinska Institutet, Stockholm, Sweden.

Ingrid Agartz (I)

Department of Clinical Neuroscience, Centre for Psychiatric Research, Karolinska Institutet, Stockholm, Sweden; Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; KG Jebsen Centre for Neurodevelopmental Disorders, Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Department of Psychiatric Research, Diakonhjemmet Hospital, Oslo, Norway.

Theophilus N Akudjedu (TN)

Institute of Medical Imaging and Visualisation, Bournemouth University, Bournemouth, United Kingdom; Centre for Neuroimaging and Cognitive Genomics, Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine, Nursing, and Health Sciences, National University of Ireland, Galway, Ireland.

Martin Alda (M)

Department of Psychiatry, Dalhousie University, Halifax, Nova Scotia; National Institute of Mental Health, Klecany, Czech Republic.

Dag Alnæs (D)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Bjørknes College, Oslo, Norway.

Silvia Alonso-Lana (S)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain.

Francesco Benedetti (F)

Psychiatry and Clinical Psychobiology Unit, Division of Neuroscience, IRCCS Ospedale San Raffaele, Milano, Italy; University Vita-Salute San Raffaele, Milano, Italy; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Michael Berk (M)

Orygen, 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, Melbourne, Victoria, Australia; Department of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia; Deakin University, the Institute for Mental and Physical Health and Clinical Translation, School of Medicine, Barwon Health, Geelong, Victoria, Australia.

Erlend Bøen (E)

Unit of Psychosomatic and CL Psychiatry, Oslo University Hospital, Oslo, Norway.

Caterina Del Mar Bonnin (CDM)

Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Barcelona Bipolar Disorders and Depressive Unit, Hospital Clínic, Institute of Neurosciences, Barcelona, Spain; University of Barcelona, Barcelona, Spain.

Fabian Breuer (F)

Psychiatry and Clinical Psychobiology Unit, Division of Neuroscience, IRCCS Ospedale San Raffaele, Milano, Italy; University Vita-Salute San Raffaele, Milano, Italy; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Katharina Brosch (K)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Rachel M Brouwer (RM)

Department of Psychiatry, University Medical Center Utrecht Brain Center, Utrecht University, Utrecht, the Netherlands; Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.

Erick J Canales-Rodríguez (EJ)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Signal Processing Laboratory, École polytechnique fédérale de Lausanne, Lausanne, Switzerland.

Dara M Cannon (DM)

Centre for Neuroimaging and Cognitive Genomics, Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine, Nursing, and Health Sciences, National University of Ireland, Galway, Ireland.

Yann Chye (Y)

Turner Institute for Brain and Mental Health, School of Psychological Science and Monash Biomedical Imaging Facility, Monash University, Melbourne, Victoria, Australia.

Andreas Dahl (A)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Department of Psychology, University of Oslo, Oslo, Norway.

Orwa Dandash (O)

Department of Psychiatry, The University of Melbourne, Melbourne, Victoria, Australia.

Udo Dannlowski (U)

Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Katharina Dohm (K)

Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Torbjørn Elvsåshagen (T)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Department of Neurology, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.

Lukas Fisch (L)

Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Janice M Fullerton (JM)

School of Medical Sciences, University of New South Wales, Sydney, New South Wales, Australia; Neuroscience Research Australia, Sydney, New South Wales, Australia.

Jose M Goikolea (JM)

Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Barcelona Bipolar Disorders and Depressive Unit, Hospital Clínic, Institute of Neurosciences, Barcelona, Spain; University of Barcelona, Barcelona, Spain.

Dominik Grotegerd (D)

Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Beathe Haatveit (B)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Tim Hahn (T)

Department of Psychiatry, Dalhousie University, Halifax, Nova Scotia; National Institute of Mental Health, Klecany, Czech Republic; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Tomas Hajek (T)

Department of Psychiatry, Dalhousie University, Halifax, Nova Scotia; National Institute of Mental Health, Klecany, Czech Republic; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Walter Heindel (W)

Clinic for Radiology, University of Münster, Münster, Germany.

Martin Ingvar (M)

Department of Clinical Neuroscience, Osher Center, Karolinska Institutet, Stockholm, Sweden; Karolinska University Hospital, Department of Neuroradiology, Stockholm, Sweden.

Kang Sim (K)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore; Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore; West Region, Institute of Mental Health, Singapore, Singapore; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Tilo T J Kircher (TTJ)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Rhoshel K Lenroot (RK)

University of New Mexico, Albuquerque, New Mexico.

Ulrik F Malt (UF)

Department of Neurology, Oslo University Hospital, Oslo, Norway; Department of Psychiatry and Addiction, Section for C-L Psychiatry and Psychosomatics, Oslo University Hospital, Oslo, Norway.

Colm McDonald (C)

Centre for Neuroimaging and Cognitive Genomics, Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine, Nursing, and Health Sciences, National University of Ireland, Galway, Ireland.

Sean R McWhinney (SR)

Department of Psychiatry, Dalhousie University, Halifax, Nova Scotia.

Ingrid Melle (I)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Tina Meller (T)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Elisa M T Melloni (EMT)

Psychiatry and Clinical Psychobiology Unit, Division of Neuroscience, IRCCS Ospedale San Raffaele, Milano, Italy; University Vita-Salute San Raffaele, Milano, Italy.

Philip B Mitchell (PB)

School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.

Leila Nabulsi (L)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, University of Southern California, Los Angeles, California; Centre for Neuroimaging and Cognitive Genomics, Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine, Nursing, and Health Sciences, National University of Ireland, Galway, Ireland.

Igor Nenadić (I)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Nils Opel (N)

Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Bronwyn J Overs (BJ)

Neuroscience Research Australia, Sydney, New South Wales, Australia.

Francesco Panicalli (F)

Hospital general de Granollers, Barcelona, Spain; Benito Menni CASM, Barcelona, Spain.

Julia-Katharina Pfarr (JK)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Sara Poletti (S)

Psychiatry and Clinical Psychobiology Unit, Division of Neuroscience, IRCCS Ospedale San Raffaele, Milano, Italy.

Edith Pomarol-Clotet (E)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain.

Joaquim Radua (J)

Center for Psychiatric Research, Department of Clinical Neuroscience, Karolinska Institutet and Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden; Early Psychosis: Interventions and Clinical-detection lab, Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, United Kingdom; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Jonathan Repple (J)

Center for Psychiatric Research, Department of Clinical Neuroscience, Karolinska Institutet and Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden; Early Psychosis: Interventions and Clinical-detection lab, Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, United Kingdom; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Kai G Ringwald (KG)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Gloria Roberts (G)

School of Psychiatry, University of New South Wales, Sydney, New South Wales, Australia.

Elena Rodriguez-Cano (E)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Benito Menni CASM, Barcelona, Spain.

Raymond Salvador (R)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain.

Kelvin Sarink (K)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore; Yong Loo Lin School of Medicine, National University of Singapore, Singapore, Singapore; West Region, Institute of Mental Health, Singapore, Singapore; Institute for Translational Psychiatry, University of Münster, Münster, Germany.

Salvador Sarró (S)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Simon Schmitt (S)

FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany; Department of Psychiatry, Social Psychiatry and Psychotherapy, Hannover Medical School, Hannover, Germany.

Frederike Stein (F)

Department of Psychiatry and Psychotherapy, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain and Behavior, University of Marburg and Justus Liebig, University of Giessen, Giessen, Germany.

Chao Suo (C)

Turner Institute for Brain and Mental Health, School of Psychological Science and Monash Biomedical Imaging Facility, Monash University, Melbourne, Victoria, Australia.

Sophia I Thomopoulos (SI)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, University of Southern California, Los Angeles, California.

Giulia Tronchin (G)

Centre for Neuroimaging and Cognitive Genomics, Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine, Nursing, and Health Sciences, National University of Ireland, Galway, Ireland.

Eduard Vieta (E)

Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Barcelona Bipolar Disorders and Depressive Unit, Hospital Clínic, Institute of Neurosciences, Barcelona, Spain; University of Barcelona, Barcelona, Spain.

Lars T Westlye (LT)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; KG Jebsen Centre for Neurodevelopmental Disorders, Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Department of Psychology, University of Oslo, Oslo, Norway.

Adam G White (AG)

Djavad Mowafaghian Centre for Brain Health, Vancouver, British Columbia, Canada.

Lakshmi N Yatham (LN)

Department of Psychiatry, University of British Columbia, Vancouver, British Columbia, Canada.

Nathalia Zak (N)

Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Paul M Thompson (PM)

Imaging Genetics Center, Mark and Mary Stevens Institute for Neuroimaging and Informatics, University of Southern California, Los Angeles, California.

Ole A Andreassen (OA)

KG Jebsen Centre for Neurodevelopmental Disorders, Institute of Clinical Medicine, University of Oslo, Oslo, Norway; Norwegian Centre for Mental Disorders Research, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway; Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Mikael Landén (M)

Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden; Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.

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