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      White matter disturbances in major depressive disorder: a coordinated analysis across 20 international cohorts in the ENIGMA MDD working group

      research-article
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      Molecular Psychiatry
      Nature Publishing Group UK
      Neuroscience, Depression

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          Abstract

          Alterations in white matter (WM) microstructure have been implicated in the pathophysiology of major depressive disorder (MDD). However, previous findings have been inconsistent, partially due to low statistical power and the heterogeneity of depression. In the largest multi-site study to date, we examined WM anisotropy and diffusivity in 1305 MDD patients and 1602 healthy controls (age range 12–88 years) from 20 samples worldwide, which included both adults and adolescents, within the MDD Working Group of the Enhancing Neuroimaging Genetics through Meta-Analysis (ENIGMA) consortium. Processing of diffusion tensor imaging (DTI) data and statistical analyses were harmonized across sites and effects were meta-analyzed across studies. We observed subtle, but widespread, lower fractional anisotropy (FA) in adult MDD patients compared with controls in 16 out of 25 WM tracts of interest (Cohen’s d between 0.12 and 0.26). The largest differences were observed in the corpus callosum and corona radiata. Widespread higher radial diffusivity (RD) was also observed (all Cohen’s d between 0.12 and 0.18). Findings appeared to be driven by patients with recurrent MDD and an adult age of onset of depression. White matter microstructural differences in a smaller sample of adolescent MDD patients and controls did not survive correction for multiple testing. In this coordinated and harmonized multisite DTI study, we showed subtle, but widespread differences in WM microstructure in adult MDD, which may suggest structural disconnectivity in MDD.

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          Most cited references37

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          Demyelination increases radial diffusivity in corpus callosum of mouse brain.

          Myelin damage, as seen in multiple sclerosis (MS) and other demyelinating diseases, impairs axonal conduction and can also be associated with axonal degeneration. Accurate assessments of these conditions may be highly beneficial in evaluating and selecting therapeutic strategies for patient management. Recently, an analytical approach examining diffusion tensor imaging (DTI) derived parameters has been proposed to assess the extent of axonal damage, demyelination, or both. The current study uses the well-characterized cuprizone model of experimental demyelination and remyelination of corpus callosum in mouse brain to evaluate the ability of DTI parameters to detect the progression of myelin degeneration and regeneration. Our results demonstrate that the extent of increased radial diffusivity reflects the severity of demyelination in corpus callosum of mouse brain affected by cuprizone treatment. Subsequently, radial diffusivity decreases with the progression of remyelination. Furthermore, radial diffusivity changes were specific to the time course of changes in myelin integrity as distinct from axonal injury, which was detected by betaAPP immunostaining and shown to be most extensive prior to demyelination. Radial diffusivity offers a specific assessment of demyelination and remyelination, as distinct from acute axonal damage.
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            Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry.

            Magnetic resonance imaging volumetry studies report inverted U-patterns with increasing white-matter (WM) volume into middle age suggesting protracted WM maturation compared with the cortical gray matter. Diffusion tensor imaging (DTI) is sensitive to degree and direction of water permeability in biological tissues, providing in vivo indices of WM microstructure. The aim of this cross-sectional study was to delineate age trajectories of WM volume and DTI indices in 430 healthy subjects ranging 8-85 years of age. We used automated regional brain volume segmentation and tract-based statistics of fractional anisotropy, mean, and radial diffusivity as markers of WM integrity. Nonparametric regressions were used to fit the age trajectories and to estimate the timing of maximum development and deterioration in aging. Although the volumetric data supported protracted growth into the sixth decade, DTI indices plateaued early in the fourth decade across all tested regions and then declined slowly into late adulthood followed by an accelerating decrease in senescence. Tractwise and voxel-based analyses yielded regional differences in development and aging but did not provide ample evidence in support of a simple last-in-first-out hypothesis of life-span changes.
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              • Article: not found

              Methodological considerations on tract-based spatial statistics (TBSS).

              Having gained a tremendous amount of popularity since its introduction in 2006, tract-based spatial statistics (TBSS) can now be considered as the standard approach for voxel-based analysis (VBA) of diffusion tensor imaging (DTI) data. Aiming to improve the sensitivity, objectivity, and interpretability of multi-subject DTI studies, TBSS includes a skeletonization step that alleviates residual image misalignment and obviates the need for data smoothing. Although TBSS represents an elegant and user-friendly framework that tackles numerous concerns existing in conventional VBA methods, it has limitations of its own, some of which have already been detailed in recent literature. In this work, we present general methodological considerations on TBSS and report on pitfalls that have not been described previously. In particular, we have identified specific assumptions of TBSS that may not be satisfied under typical conditions. Moreover, we demonstrate that the existence of such violations can severely affect the reliability of TBSS results. With TBSS being used increasingly, it is of paramount importance to acquaint TBSS users with these concerns, such that a well-informed decision can be made as to whether and how to pursue a TBSS analysis. Finally, in addition to raising awareness by providing our new insights, we provide constructive suggestions that could improve the validity and increase the impact of TBSS drastically.
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                Author and article information

                Contributors
                laurasvanvelzen@gmail.com
                Journal
                Mol Psychiatry
                Mol. Psychiatry
                Molecular Psychiatry
                Nature Publishing Group UK (London )
                1359-4184
                1476-5578
                30 August 2019
                30 August 2019
                2020
                : 25
                : 7
                : 1511-1525
                Affiliations
                [1 ]Department of Psychiatry, Amsterdam UMC, The Netherlands
                [2 ]GRID grid.488501.0, Orygen, The National Centre of Excellence in Youth Mental Health, ; Parkville, Australia
                [3 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Centre for Youth Mental Health, , The University of Melbourne, ; Melbourne, Australia
                [4 ]ISNI 000000041936754X, GRID grid.38142.3c, Department of Psychiatry, Beth Israel Deaconess Medical Center, , Harvard Medical School, ; Boston, MA USA
                [5 ]ISNI 000000041936754X, GRID grid.38142.3c, Psychiatry Neuroimaging Laboratory, Brigham and Women’s Hospital, , Harvard Medical School, ; Boston, MA USA
                [6 ]ISNI 0000 0001 2156 6853, GRID grid.42505.36, Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, , University of Southern California, ; Marina del Rey, CA USA
                [7 ]ISNI 0000 0004 0407 1981, GRID grid.4830.f, Cognitive Neuroscience Center, University Medical Center Groningen, , University of Groningen, ; Groningen, The Netherlands
                [8 ]FSSBI “Scientific Research Institute of Physiology & Basic Medicine”, Laboratory of Affective, Cognitive & Translational Neuroscience, Novosibirsk, Russia
                [9 ]ISNI 0000000121896553, GRID grid.4605.7, Department of Neuroscience, , Novosibirsk State University, ; Novosibirsk, Russia
                [10 ]University of Münster, Institute of Clinical Radiology, Münster, Germany
                [11 ]ISNI 0000 0001 2172 9288, GRID grid.5949.1, Department of Psychiatry, , University of Münster, ; Münster, Germany
                [12 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, Department of Psychiatry, , The University of Melbourne, ; Melbourne, VIC Australia
                [13 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, The Florey Institute of Neuroscience and Mental Heatlh, , The University of Melbourne, Melbourne, ; VIC, Australia
                [14 ]ISNI 0000000121896553, GRID grid.4605.7, Lab. of Experimental & Translational Neuroscience, , Novosibirsk State University, ; Novosibirsk, Russia
                [15 ]ISNI 0000 0004 1936 9705, GRID grid.8217.c, Department of Psychiatry and Trinity Institute of Neuroscience, , Trinity College Dublin, ; Dublin, Ireland
                [16 ]North Dublin Mental Health Services, Dublin, Ireland
                [17 ]ISNI 0000 0001 2297 6811, GRID grid.266102.1, Department of Psychiatry, , University of California, ; San Francisco, CA USA
                [18 ]ISNI 0000 0004 0472 0419, GRID grid.255986.5, Department of Biomedical Sciences, , Florida State University, ; Tallahassee, FL USA
                [19 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, Institute for Molecular Bioscience, , The University of Queensland, ; Brisbane, QLD Australia
                [20 ]ISNI 0000000419368657, GRID grid.17635.36, Department of Psychiatry and Behavioral Sciences, , The University of Minnesota, ; Minneapolis, MN USA
                [21 ]ISNI 0000 0001 1018 4307, GRID grid.5807.a, Department of Psychiatry and Psychotherapy, , Otto von Guericke University, ; Madgeburg, Germany
                [22 ]German Center for Neurodegenerative Disease, Magdeburg, Germany
                [23 ]ISNI 0000000419368956, GRID grid.168010.e, Department of Psychology, , Stanford University, ; Stanford, CA USA
                [24 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Department of Psychiatry, , University of Cape Town, ; Cape Town, South Africa
                [25 ]Department of Psychiatry, Interdisciplinary Center Psychopathology and Emotion regulation (ICPE), University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
                [26 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, Division of Psychiatry, , University of Edinburgh, ; Edinburgh, UK
                [27 ]ISNI 0000 0004 1936 834X, GRID grid.1013.3, Youth Mental Health Team, Brain and Mind Centre, , University of Sydney, ; Camperdown, Australia
                [28 ]ISNI 0000000419368956, GRID grid.168010.e, Department of Psychiatry & Behavioral Sciences, , Stanford University, ; Stanford, CA USA
                [29 ]ISNI 0000 0004 1936 9756, GRID grid.10253.35, Department of Psychiatry, , University of Marburg, ; Marburg, Germany
                [30 ]ISNI 0000000419368657, GRID grid.17635.36, Department of Psychology, , The University of Minnesota, ; Minneapolis, MN USA
                [31 ]ISNI 0000 0001 2175 4264, GRID grid.411024.2, Maryland Psychiatric Research Center, Department of Psychiatry, , University of Maryland School of Medicine, ; Baltimore, MD USA
                [32 ]Sunshine Coast Mind and Neuroscience—Thompson Institute, Birtinya, QLD Australia
                [33 ]ISNI 0000 0004 0469 9592, GRID grid.414752.1, Research Division, , Institute of Mental Health, ; Singapore, Singapore
                [34 ]ISNI 0000 0001 2248 7639, GRID grid.7468.d, Division of Mind and Brain Research, Department of Psychiatry and Psychotherapy CCM, Charité—Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, , Humboldt-Universität zu Berlin, and Berlin Institute of Health, ; Berlin, Germany
                [35 ]ISNI 0000 0001 1018 4307, GRID grid.5807.a, Department of Neurology, , University of Magdeburg, ; Magdeburg, Germany
                [36 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Psychiatry and Paediatrics, , University of Calgary, ; Calgary, Canada
                [37 ]Strategic Clinical Network for Addictions and Mental Health, Calgary, Canada
                [38 ]ISNI 0000 0001 2294 1395, GRID grid.1049.c, QIMR Berghofer Medical Research Institute, ; Brisbane, QLD Australia
                [39 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, Centre for Cognitive Ageing and Cognitive Epidemiology, , University of Edinburgh, ; Edinburgh, UK
                [40 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Department of Neuroscience, , University of Calgary, ; Calgary, Canada
                [41 ]ISNI 0000 0001 0684 7358, GRID grid.413571.5, Alberta Children’s Hospital Research Institute, ; Calgary, Canada
                [42 ]Department of Psychiatry, Institute of Biomedical Research Sant Pau, Barcelona, Spain
                [43 ]ISNI 0000 0004 1762 4012, GRID grid.418264.d, CIBERSAM, ; Madrid, Spain
                [44 ]GRID grid.7080.f, Universitat Autònoma de Barcelona, ; Barcelona, Spain
                [45 ]ISNI 0000 0001 2214 904X, GRID grid.11956.3a, SAMRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry, , Stellenbosch University, ; Cape Town, South Africa
                [46 ]Center for Depression, Anxiety, and Stress Research, McLean Hospital, Harvard Medical School, Belmont, MA, USA
                [47 ]ISNI 0000 0000 9497 5095, GRID grid.419548.5, Max Planck Institute of Psychiatry, ; Munich, Germany
                [48 ]ISNI 0000 0001 2190 4373, GRID grid.7700.0, Department of Psychiatry, , University of Heidelberg, ; Heidelberg, Germany
                [49 ]ISNI 0000 0004 0469 9592, GRID grid.414752.1, West Region and Research Division, , Institute of Mental Health, ; Singapore, Singapore
                [50 ]ISNI 0000 0001 2180 6431, GRID grid.4280.e, Yong Loo Lin School of Medicine, , National University of Singapore, ; Singapore, Singapore
                [51 ]ISNI 0000 0001 2224 0361, GRID grid.59025.3b, Lee Kong Chian School of Medicine, , Nanyang Technological University, ; Singapore, Singapore
                [52 ]SAMRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry & Neuroscience Institute, University of Cape Town, South Africa
                [53 ]Mental Health Research Center, Moscow, Russia
                [54 ]ISNI 0000000089452978, GRID grid.10419.3d, Curium-LUMC Child and Adolescent Psychiatry, , Leiden University Medical Center, ; Leiden, The Netherlands
                [55 ]Leiden Institute for Brain and Cognition, Leiden, The Netherlands
                [56 ]ISNI 0000 0001 2312 1970, GRID grid.5132.5, Institute of Psychology, , Leiden University, ; Leiden, The Netherlands
                [57 ]ISNI 0000 0004 1770 5832, GRID grid.157927.f, Instituto ITACA, , Universitat Politècnica de València, ; València, Spain
                [58 ]ISNI 0000 0001 2190 1447, GRID grid.10392.39, Department of Psychiatry and Psychotherapy, , University of Tübingen, ; Tubingen, Germany
                [59 ]ISNI 0000000089452978, GRID grid.10419.3d, Department of Psychiatry, , Leiden University Medical Center, ; Leiden, The Netherlands
                [60 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, Queensland Brain Institute, , The University of Queensland, ; Brisbane, QLD Australia
                [61 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, Centre for Advanced Imaging, , The University of Queensland, ; Brisbane, QLD Australia
                [62 ]GRID grid.484519.5, Amsterdam Neuroscience, ; Amsterdam, The Netherlands
                Author information
                http://orcid.org/0000-0001-6548-426X
                http://orcid.org/0000-0002-5146-0096
                http://orcid.org/0000-0002-4051-3682
                http://orcid.org/0000-0002-1135-4141
                http://orcid.org/0000-0002-0731-9626
                http://orcid.org/0000-0003-4069-8020
                http://orcid.org/0000-0002-0198-4588
                http://orcid.org/0000-0003-3806-2218
                http://orcid.org/0000-0001-7218-7810
                http://orcid.org/0000-0002-9260-5490
                http://orcid.org/0000-0002-9403-6121
                http://orcid.org/0000-0002-2780-3327
                http://orcid.org/0000-0002-4505-8869
                http://orcid.org/0000-0001-7133-4970
                http://orcid.org/0000-0003-4401-8950
                Article
                477
                10.1038/s41380-019-0477-2
                7055351
                31471575
                9c1e5e46-481c-4473-adc7-b8d243ee6a0c
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 23 August 2018
                : 15 April 2019
                : 10 May 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000874, Brain and Behavior Research Foundation (Brain & Behavior Research Foundation);
                Award ID: R01MH085734
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100009670, National Alliance for Research on Schizophrenia and Depression (NARSAD);
                Award ID: P41 RR008079
                Award Recipient :
                Funded by: This work was funded by the German Research Foundation (SFB-TRR58, Projects C09 and Z02 to UD) and the Interdisciplinary Center for Clinical Research (IZKF) of the medical faculty of Münster (grant Dan3/012/17 to UD)
                Funded by: This study was supported by Science Foundation Ireland through a Stokes Professorhip grant to TF
                Funded by: FundRef https://doi.org/10.13039/100000025, U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH);
                Award ID: R01MH59259
                Award ID: R37101495
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: 0801700
                Award ID: DGE-1147470
                Award Recipient :
                Funded by: Professor Ian Hickie has been a Commissioner in Australia’s National Mental Health Commission since 2012. He is the Co-Director, Health and Policy at the Brain and Mind Centre (BMC) University of Sydney. The BMC operates an early-intervention youth services at Camperdown under contract to headspace. Professor Hickie has previously led community-based and pharmaceutical industry-supported (Wyeth, Eli Lily, Servier, Pfizer, AstraZeneca) projects focused on the identification and better management of anxiety and depression. He was a member of the Medical Advisory Panel for Medibank Private until October 2017, a Board Member of Psychosis Australia Trust and a member of Veterans Mental Health Clinical Reference group. He is the Chief Scientific Advisor to, and an equity shareholder in, Innowell. Innowell has been formed by the University of Sydney and PwC to deliver the $30m Australian Government-funded ‘Project Synergy’. Project Synergy is a three year program for the transformation of mental health services through the use of innovative technologies
                Funded by: This work was supported by the Brain and Behavior Research Foundation (formerly NARSAD) to T.T.Y.; the National Institute of Mental Health (R01MH085734 to T.T.Y..; K01MH117442 to T.C.H.) and by the American Foundation for Suicide Prevention (PDF-1-064-13) to T.C.H.
                Funded by: This work was funded by the German Research Foundation (DFG, grant FOR2107 DA1151/5-1 and DA1151/5-2 to UD; KI 588/14-1, KI 588/14-2 to TK; KR 3822/7-1, KR 3822/7-2 to AK; JA 1890/7-1, JA 1890/7-2 to AJ)
                Funded by: The study was funded by the National Institute of Mental Health (K23MH090421), the National Alliance for Research on Schizophrenia and Depression, the University of Minnesota Graduate School, the Minnesota Medical Foundation, and the Biotechnology Research Center (P41 RR008079 to the Center for Magnetic Resonance Research)
                Funded by: The study was funded by SFB 779.
                Funded by: This study has received funding from the European Community's Seventh Framework Programme (FP7/2007-2013). This paper reflects only the author’s views and the European Union is not liable for any use that may be made of the information contained therein. This work was also supported by a Wellcome Trust Strategic Award.
                Funded by: The infrastructure for the NESDA study (www.nesda.nl) is funded through the Geestkracht program of the Netherlands Organisation for Health Research and Development (Zon-Mw, grant number 10-000-1002) and is supported by participating universities (VU University Medical Center, GGZ inGeest, Arkin, Leiden University Medical Center, GGZ Rivierduinen, University Medical Center Groningen) and mental health care organizations, see www.nesda.nl.
                Funded by: "This study was funded by two grants of the Fondo de Investigación Sanitaria (FIS: PI 10/00372; FIS: 13/1057)from the Instituto de Salud Carlos III, by the Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM). The author is funded through ‘Miguel Servet’ research contract (CP16- 0020), co-financed by the European Regional Development Fund (ERDF) (2016–2019)."
                Funded by: MPIP: The MPIP Sample comprises patients included in the Recurrent Unipolar Depression (RUD) Case-Control study at the clinic of the Max Planck Institute of Psychiatry, Munich, German. The RUD study was supported by GlaxoSmithKline.We wish to acknowledge the patients and control subjects that have particiaped int the study. We thank Rosa Schirmer, Elke Schreiter, Reinhold Borschke and Ines Eidner for image acquisition and data preparation, and Anna Oliynyk for quality checks. We thank Dorothee P. Auer and F. Holsboer for initiation of the RUD study.
                Funded by: This work was supported by the National Healthcare Group Research Grant (SIG/15012) awarded to KS.
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                © Springer Nature Limited 2020

                Molecular medicine
                neuroscience,depression
                Molecular medicine
                neuroscience, depression

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