Cortical and subcortical brain structure in generalized anxiety disorder: findings from 28 research sites in the ENIGMA-Anxiety Working Group

Anita Harrewijn¹, Elise M Cardinale², Nynke A Groenewold³, Janna Marie Bas-Hoogendam^{4

5

6}, Moji Aghajani^{7

8}, Kevin Hilbert⁹, Narcis Cardoner^{10

11

12}, Daniel Porta-Casteràs^{10

11

12}, Savannah Gosnell¹³, Ramiro Salas¹³, Andrea P Jackowski¹⁴, Pedro M Pan¹⁴, Giovanni A Salum¹⁵, Karina S Blair¹⁶, James R Blair¹⁶, Mira Z Hammoud¹⁷, Mohammed R Milad¹⁷, Katie L Burkhouse¹⁸, K Luan Phan¹⁹, Heidi K Schroeder²⁰, Jeffrey R Strawn²⁰, Katja Beesdo-Baum²¹, Neda Jahanshad²², Sophia I Thomopoulos²², Randy Buckner^{23

24}, Jared A Nielsen^{23

24

25}, Jordan W Smoller²⁴, Jair C Soares²⁶, Benson Mwangi²⁶, Mon-Ju Wu²⁶, Giovana B Zunta-Soares²⁶, Michal Assaf^{27

28}, Gretchen J Diefenbach^{28

29}, Paolo Brambilla^{30

31}, Eleonora Maggioni³⁰, David Hofmann³², Thomas Straube³², Carmen Andreescu³³, Rachel Berta³³, Erica Tamburo³³, Rebecca B Price^{33

34}, Gisele G Manfro³⁵, Federica Agosta^{36

37}, Elisa Canu³⁶, Camilla Cividini^{36

37}, Massimo Filippi^{36

37

38

39

40}, Milutin Kostić^{41

42}, Ana Munjiza Jovanovic⁴¹, Bianca A V Alberton⁴³, Brenda Benson², Gabrielle F Freitag², Courtney A Filippi², Andrea L Gold⁴⁴, Ellen Leibenluft², Grace V Ringlein², Kathryn E Werwath², Hannah Zwiebel², André Zugman², Hans J Grabe^{45

46}, Sandra Van der Auwera^{45

46}, Katharina Wittfeld^{45

46}, Henry Völzke⁴⁷, Robin Bülow⁴⁸, Nicholas L Balderston⁴⁹, Monique Ernst⁵⁰, Christian Grillon⁵⁰, Lilianne R Mujica-Parodi⁵¹, Helena van Nieuwenhuizen⁵², Hugo D Critchley⁵³, Elena Makovac⁵⁴, Matteo Mancini⁵³, Frances Meeten⁵⁵, Cristina Ottaviani^{56

57}, Tali M Ball⁵⁸, Gregory A Fonzo⁵⁹, Martin P Paulus⁶⁰, Murray B Stein⁶¹, Raquel E Gur⁶², Ruben C Gur⁶², Antonia N Kaczkurkin⁶², Bart Larsen⁶², Theodore D Satterthwaite⁶², Jennifer Harper⁶³, Michael Myers⁶³, Michael T Perino⁶³, Chad M Sylvester⁶³, Qiongru Yu⁶³, Ulrike Lueken⁹, Dick J Veltman⁷, Paul M Thompson²², Dan J Stein⁶⁴, Nic J A Van der Wee^{4

6}, Anderson M Winkler^#², Daniel S Pine^#²

Affiliations

¹ Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA. anita.harrewijn@nih.gov.
² Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA.
³ Department of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, South Africa.
⁴ Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands.
⁵ Department of Developmental and Educational Psychology, Institute of Psychology, Leiden University, Leiden, The Netherlands.
⁶ Leiden Institute for Brain and Cognition, Leiden, The Netherlands.
⁷ Department of Psychiatry, Amsterdam UMC, location VUMC, Amsterdam, The Netherlands.
⁸ Department of Research & Innovation, GGZ InGeest, Amsterdam, The Netherlands.
⁹ Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany.
¹⁰ Department of Mental Health, University Hospital Parc Taulí-I3PT, Barcelona, Spain.
¹¹ Department of Psychiatry and Forensic Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain.
¹² Centro de Investigación Biomédica en Red de Salud Mental, Carlos III Health Institute, Madrid, Spain.
¹³ Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, USA.
¹⁴ LiNC, Department of Psychiatry, Federal University of São Paulo, São Paulo, Brazil.
¹⁵ Section on Negative Affect and Social Processes, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
¹⁶ Center for Neurobehavioral Research, Boys Town National Research Hospital, Boys Town, NE, USA.
¹⁷ Department of Psychiatry, NYU School of Medicine, New York University, New York, NY, USA.
¹⁸ Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
¹⁹ Department of Psychiatry and Behavioral Health, The Ohio State University, Columbus, OH, USA.
²⁰ Department of Psychiatry & Behavioral Neuroscience, University of Cincinnati, Cincinnati, OH, USA.
²¹ Behavioral Epidemiology, Institute of Clinical Psychology and Psychotherapy, Technische Universität Dresden, Dresden, Germany.
²² Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA.
²³ Center for Brain Science & Department of Psychology, Harvard University, Cambridge, MA, USA.
²⁴ Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA.
²⁵ Psychology Department & Neuroscience Center, Brigham Young University, Provo, USA.
²⁶ Center Of Excellence On Mood Disorders, Louis A. Faillace, MD, Department of Psychiatry and Behavioral Sciences, The University of Texas Health Science Center at Houston, Houston, TX, USA.
²⁷ Olin Neuropsychiatry Research Center, Institute of Living, Hartford Hospital, Hartford, CT, USA.
²⁸ Department of Psychiatry, Yale School of Medicine, New Haven, CT, USA.
²⁹ Anxiety Disorders Center, Institute of Living, Hartford Hospital, Hartford, CT, USA.
³⁰ Department of Neurosciences and Mental Health, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.
³¹ Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy.
³² Institute of Medical Psychology and Systems Neuroscience, University of Muenster, Muenster, Germany.
³³ Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA.
³⁴ Department Psychology, University of Pittsburgh, Pittsburgh, PA, USA.
³⁵ Anxiety Disorder Program, Hospital de Clínicas de Porto Alegre, Department of Psychiatry, Federal University of Rio Grande do Sul, Porto Alegre, Brazil.
³⁶ Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy.
³⁷ Vita-Salute San Raffaele University, Milan, Italy.
³⁸ Neurology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.
³⁹ Neurophysiology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.
⁴⁰ Neurorehabilitation Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.
⁴¹ Institute of Mental Health, University of Belgrade, Belgrade, Serbia.
⁴² Department of Psychiatry, School of Medicine, University of Belgrade, Belgrade, Serbia.
⁴³ Graduate Program in Electrical and Computer Engineering, Universidade Tecnológica Federal do Paraná, Curitiba, Puerto Rico, Brazil.
⁴⁴ Department of Psychiatry and Human Behavior, Brown University Warren Alpert Medical School, Providence, RI, USA.
⁴⁵ Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.
⁴⁶ German Center for Neurodegenerative Diseases (DZNE), Site Rostock/Greifswald, Greifswald, Germany.
⁴⁷ Institute for Community Medicine, University Medicine Greifswald, Greifswald, Germany.
⁴⁸ Institute for Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
⁴⁹ Center for Neuromodulation in Depression and Stress, University of Pennsylvania, Philadelphia, PA, USA.
⁵⁰ Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, Bethesda, MD, USA.
⁵¹ Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY, USA.
⁵² Department of Physics, Stony Brook University, Stony Brook, NY, USA.
⁵³ Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, Brighton, UK.
⁵⁴ Centre for Neuroimaging Science, Kings College London, London, UK.
⁵⁵ School of Psychology, University of Sussex, Brighton, UK.
⁵⁶ Department of Psychology, Sapienza University of Rome, Rome, Italy.
⁵⁷ IRCCS Santa Lucia Foundation, Rome, Italy.
⁵⁸ Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA.
⁵⁹ Department of Psychiatry and Behavioral Sciences, The University of Texas at Austin Dell Medical School, Austin, TX, USA.
⁶⁰ Laureate Institute for Brain Research, Tulsa, OK, USA.
⁶¹ Department of Psychiatry, School of Medicine and Herbert Wertheim School of Public Health, University of California, San Diego, La Jolla, CA, USA.
⁶² Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.
⁶³ Department of Psychiatry, Washington University, St. Louis, MO, USA.
⁶⁴ South African Medical Research Council Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, South Africa.

^# Contributed equally.

PMID: 34599145
PMCID: PMC8486763
DOI: 10.1038/s41398-021-01622-1

Cortical and subcortical brain structure in generalized anxiety disorder: findings from 28 research sites in the ENIGMA-Anxiety Working Group

Anita Harrewijn et al. Transl Psychiatry. 2021.

. 2021 Oct 1;11(1):502.

doi: 10.1038/s41398-021-01622-1.

Authors

Affiliations

¹ Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA. anita.harrewijn@nih.gov.
² Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA.
³ Department of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, South Africa.
⁴ Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands.
⁵ Department of Developmental and Educational Psychology, Institute of Psychology, Leiden University, Leiden, The Netherlands.
⁶ Leiden Institute for Brain and Cognition, Leiden, The Netherlands.
⁷ Department of Psychiatry, Amsterdam UMC, location VUMC, Amsterdam, The Netherlands.
⁸ Department of Research & Innovation, GGZ InGeest, Amsterdam, The Netherlands.
⁹ Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany.
¹⁰ Department of Mental Health, University Hospital Parc Taulí-I3PT, Barcelona, Spain.
¹¹ Department of Psychiatry and Forensic Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain.
¹² Centro de Investigación Biomédica en Red de Salud Mental, Carlos III Health Institute, Madrid, Spain.
¹³ Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, USA.
¹⁴ LiNC, Department of Psychiatry, Federal University of São Paulo, São Paulo, Brazil.
¹⁵ Section on Negative Affect and Social Processes, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.
¹⁶ Center for Neurobehavioral Research, Boys Town National Research Hospital, Boys Town, NE, USA.
¹⁷ Department of Psychiatry, NYU School of Medicine, New York University, New York, NY, USA.
¹⁸ Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.
¹⁹ Department of Psychiatry and Behavioral Health, The Ohio State University, Columbus, OH, USA.
²⁰ Department of Psychiatry & Behavioral Neuroscience, University of Cincinnati, Cincinnati, OH, USA.
²¹ Behavioral Epidemiology, Institute of Clinical Psychology and Psychotherapy, Technische Universität Dresden, Dresden, Germany.
²² Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey, CA, USA.
²³ Center for Brain Science & Department of Psychology, Harvard University, Cambridge, MA, USA.
²⁴ Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA.
²⁵ Psychology Department & Neuroscience Center, Brigham Young University, Provo, USA.
²⁶ Center Of Excellence On Mood Disorders, Louis A. Faillace, MD, Department of Psychiatry and Behavioral Sciences, The University of Texas Health Science Center at Houston, Houston, TX, USA.
²⁷ Olin Neuropsychiatry Research Center, Institute of Living, Hartford Hospital, Hartford, CT, USA.
²⁸ Department of Psychiatry, Yale School of Medicine, New Haven, CT, USA.
²⁹ Anxiety Disorders Center, Institute of Living, Hartford Hospital, Hartford, CT, USA.
³⁰ Department of Neurosciences and Mental Health, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milan, Italy.
³¹ Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy.
³² Institute of Medical Psychology and Systems Neuroscience, University of Muenster, Muenster, Germany.
³³ Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, USA.
³⁴ Department Psychology, University of Pittsburgh, Pittsburgh, PA, USA.
³⁵ Anxiety Disorder Program, Hospital de Clínicas de Porto Alegre, Department of Psychiatry, Federal University of Rio Grande do Sul, Porto Alegre, Brazil.
³⁶ Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, IRCCS San Raffaele Scientific Institute, Milan, Italy.
³⁷ Vita-Salute San Raffaele University, Milan, Italy.
³⁸ Neurology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.
³⁹ Neurophysiology Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.
⁴⁰ Neurorehabilitation Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy.
⁴¹ Institute of Mental Health, University of Belgrade, Belgrade, Serbia.
⁴² Department of Psychiatry, School of Medicine, University of Belgrade, Belgrade, Serbia.
⁴³ Graduate Program in Electrical and Computer Engineering, Universidade Tecnológica Federal do Paraná, Curitiba, Puerto Rico, Brazil.
⁴⁴ Department of Psychiatry and Human Behavior, Brown University Warren Alpert Medical School, Providence, RI, USA.
⁴⁵ Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.
⁴⁶ German Center for Neurodegenerative Diseases (DZNE), Site Rostock/Greifswald, Greifswald, Germany.
⁴⁷ Institute for Community Medicine, University Medicine Greifswald, Greifswald, Germany.
⁴⁸ Institute for Diagnostic Radiology and Neuroradiology, University Medicine Greifswald, Greifswald, Germany.
⁴⁹ Center for Neuromodulation in Depression and Stress, University of Pennsylvania, Philadelphia, PA, USA.
⁵⁰ Section on Neurobiology of Fear and Anxiety, National Institute of Mental Health, Bethesda, MD, USA.
⁵¹ Department of Biomedical Engineering, Stony Brook University, Stony Brook, NY, USA.
⁵² Department of Physics, Stony Brook University, Stony Brook, NY, USA.
⁵³ Department of Neuroscience, Brighton and Sussex Medical School, University of Sussex, Brighton, UK.
⁵⁴ Centre for Neuroimaging Science, Kings College London, London, UK.
⁵⁵ School of Psychology, University of Sussex, Brighton, UK.
⁵⁶ Department of Psychology, Sapienza University of Rome, Rome, Italy.
⁵⁷ IRCCS Santa Lucia Foundation, Rome, Italy.
⁵⁸ Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA.
⁵⁹ Department of Psychiatry and Behavioral Sciences, The University of Texas at Austin Dell Medical School, Austin, TX, USA.
⁶⁰ Laureate Institute for Brain Research, Tulsa, OK, USA.
⁶¹ Department of Psychiatry, School of Medicine and Herbert Wertheim School of Public Health, University of California, San Diego, La Jolla, CA, USA.
⁶² Department of Psychiatry, University of Pennsylvania, Philadelphia, PA, USA.
⁶³ Department of Psychiatry, Washington University, St. Louis, MO, USA.
⁶⁴ South African Medical Research Council Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry & Neuroscience Institute, University of Cape Town, Cape Town, South Africa.

^# Contributed equally.

PMID: 34599145
PMCID: PMC8486763
DOI: 10.1038/s41398-021-01622-1

Abstract

The goal of this study was to compare brain structure between individuals with generalized anxiety disorder (GAD) and healthy controls. Previous studies have generated inconsistent findings, possibly due to small sample sizes, or clinical/analytic heterogeneity. To address these concerns, we combined data from 28 research sites worldwide through the ENIGMA-Anxiety Working Group, using a single, pre-registered mega-analysis. Structural magnetic resonance imaging data from children and adults (5-90 years) were processed using FreeSurfer. The main analysis included the regional and vertex-wise cortical thickness, cortical surface area, and subcortical volume as dependent variables, and GAD, age, age-squared, sex, and their interactions as independent variables. Nuisance variables included IQ, years of education, medication use, comorbidities, and global brain measures. The main analysis (1020 individuals with GAD and 2999 healthy controls) included random slopes per site and random intercepts per scanner. A secondary analysis (1112 individuals with GAD and 3282 healthy controls) included fixed slopes and random intercepts per scanner with the same variables. The main analysis showed no effect of GAD on brain structure, nor interactions involving GAD, age, or sex. The secondary analysis showed increased volume in the right ventral diencephalon in male individuals with GAD compared to male healthy controls, whereas female individuals with GAD did not differ from female healthy controls. This mega-analysis combining worldwide data showed that differences in brain structure related to GAD are small, possibly reflecting heterogeneity or those structural alterations are not a major component of its pathophysiology.

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Conflict of interest statement

PMP has received speakers honoraria from Daiichi Sankyo, Libbs, Sandoz, Novartis, and Abbot. NJ is MPI of a research-related grant from Biogen Inc, for work unrelated to this manuscript. JCS is consultant for PFIZER, SUNOVIAN, SANOFI, JOHNSON & JOHNSON, Livanova, and Boehringer Ingelheim. FA is Section Editor of NeuroImage: Clinical; has received speaker honoraria from Philips, Novartis, and Biogen Idec; and receives or has received research supports from the Italian Ministry of Health, AriSLA (Fondazione Italiana di Ricerca per la SLA), and the European Research Council. EC has received research support from the Italian Ministry of Health. MF is Editor-in-Chief of the Journal of Neurology; received compensation for consulting services and/or speaking activities from Biogen Idec, Merck-Serono, Novartis, and Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Merck-Serono, Novartis, Teva Pharmaceutical Industries, Roche, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, and ARiSLA (Fondazione Italiana di Ricerca per la SLA). HJG has received travel grants and speakers honoraria from Fresenius Medical Care, Neuraxpharm, Servier, and Janssen Cilag as well as research funding from Fresenius Medical Care. GAF owns equity in Alto Neuroscience. MPP is an advisor to Spring Care, Inc., a behavioral health startup, he has received royalties for an article about methamphetamine in UpToDate. MBS has in the past 3 years been a consultant for Actelion, Acadia Pharmaceuticals, Aptinyx, Bionomics, BioXcel Therapeutics, Clexio, EmpowerPharm, Epivario, GW Pharmaceuticals, Janssen, Jazz Pharmaceuticals, Roche/Genentech, and Oxeia Biopharmaceuticals; and has stock options in Oxeia Biopharmaceuticals and Epivario. PMT received partial grant support from Biogen, Inc., for research unrelated to this manuscript; consulted for Kairos Venture Capital, Inc., on projects unrelated to this manuscript. DJS has received research grants and/or consultancy honoraria from Lundbeck and Sun. Material support (for IOL site, led by MA and GJD) was provided by Neuronetics. The remaining authors declare no competing interests.

Figures

**Fig. 1. Violin plots of the age distribution for all sites in the main analysis.**
ABCD Adolescent Brain Cognitive Development Study, BHRCS Brazilian High Risk Cohort Study, CMI-HBN Child Mind Institute Healthy Brain Network, IOL Institute of Living, SDAN Section on Development and Affective Neuroscience, SHIP Study of Health in Pomerania, UCSD University of California – San Diego, UPenn University of Pennsylvania, WashU Washington University.

**Fig. 2. Effect sizes from the main analysis for vertex-wise cortical surface area with the design that included global brain measures as nuisance variables.**
None of these was statistically significant.

**Fig. 3. Effect sizes from the main analysis for vertex-wise cortical thickness with the design that included global brain measures as nuisance variables.**
None of these was statistically significant.

Fig. 4. An interaction between generalized anxiety disorder (GAD) and sex in volume in the right ventral diencephalon was observed; male individuals with GAD showed greater volume (mm³) compared to male healthy controls, whereas there was no difference between the groups for females.
Figure shows data after nuisance variables have been considered (residuals). Average volume of the right ventral diencephalon across individuals with GAD and HC: 3988.6 mm³. Note: Error bars reflect standard error.

See this image and copyright information in PMC

References

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Cortical and subcortical brain structure in generalized anxiety disorder: findings from 28 research sites in the ENIGMA-Anxiety Working Group

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Cortical and subcortical brain structure in generalized anxiety disorder: findings from 28 research sites in the ENIGMA-Anxiety Working Group

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Abstract

Conflict of interest statement

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