Cortical and Subcortical Brain Alterations in Specific Phobia and Its Animal and Blood-Injection-Injury Subtypes: A Mega-Analysis From the ENIGMA Anxiety Working Group,American Journal of Psychiatry

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Cortical and Subcortical Brain Alterations in Specific Phobia and Its Animal and Blood-Injection-Injury Subtypes: A Mega-Analysis From the ENIGMA Anxiety Working Group
American Journal of Psychiatry ( IF 15.1 ) Pub Date : 2024-06-11 , DOI: 10.1176/appi.ajp.20230032
Kevin Hilbert ₁ , Ole Jonas Boeken ₁ , Till Langhammer ₁ , Nynke A Groenewold ₁ , Janna Marie Bas-Hoogendam ₁ , Moji Aghajani ₁ , André Zugman ₁ , Fredrik Åhs ₁ , Volker Arolt ₁ , Katja Beesdo-Baum ₁ , Johannes Björkstrand ₁ , Jennifer U Blackford ₁ , Laura Blanco-Hinojo ₁ , Joscha Böhnlein ₁ , Robin Bülow ₁ , Marta Cano ₁ , Narcis Cardoner ₁ , Xavier Caseras ₁ , Udo Dannlowski ₁ , Katharina Domschke ₁ , Lydia Fehm ₁ , Brandee Feola ₁ , Mats Fredrikson ₁ , Liesbet Goossens ₁ , Hans J Grabe ₁ , Dominik Grotegerd ₁ , Raquel E Gur ₁ , Alfons O Hamm ₁ , Anita Harrewijn ₁ , Ingmar Heinig ₁ , Martin J Herrmann ₁ , David Hofmann ₁ , Andrea P Jackowski ₁ , Andreas Jansen ₁ , Antonia N Kaczkurkin ₁ , Merel Kindt ₁ , Ellen N Kingsley ₁ , Tilo Kircher ₁ , Anna L Klahn ₁ , Katja Koelkebeck ₁ , Axel Krug ₁ , Harald Kugel ₁ , Bart Larsen ₁ , Elisabeth J Leehr ₁ , Lieselotte Leonhardt ₁ , Martin Lotze ₁ , Jürgen Margraf ₁ , Jarosław Michałowski ₁ , Markus Muehlhan ₁ , Igor Nenadić ₁ , Pedro M Pan ₁ , Paul Pauli ₁ , Wenceslao Peñate ₁ , Andre Pittig ₁ , Jens Plag ₁ , Jesus Pujol ₁ , Jan Richter ₁ , Francisco L Rivero ₁ , Giovanni A Salum ₁ , Theodore D Satterthwaite ₁ , Axel Schäfer ₁ , Judith Schäfer ₁ , Anne Schienle ₁ , Silvia Schneider ₁ , Elisabeth Schrammen ₁ , Koen Schruers ₁ , Stefan M Schulz ₁ , Esther Seidl ₁ , Rudolf M Stark ₁ , Frederike Stein ₁ , Benjamin Straube ₁ , Thomas Straube ₁ , Andreas Ströhle ₁ , Boris Suchan ₁ , Sophia I Thomopoulos ₁ , Carlos Ventura-Bort ₁ , Renee Visser ₁ , Henry Völzke ₁ , Albert Wabnegger ₁ , André Wannemüller ₁ , Julia Wendt ₁ , Julian Wiemer ₁ , Hans-Ulrich Wittchen ₁ , Katharina Wittfeld ₁ , Barry Wright ₁ , Yunbo Yang ₁ , Anna Zilverstand ₁ , Peter Zwanzger ₁ , Dick J Veltman ₁ , Anderson M Winkler ₁ , Daniel S Pine ₁ , Neda Jahanshad ₁ , Paul M Thompson ₁ , Dan J Stein ₁ , Nic J A Van der Wee ₁ , Ulrike Lueken ₁

Affiliation

Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany (Hilbert, Boeken, Langhammer, Fehm, Lueken); Department of Psychology, Health and Medical University Erfurt, Erfurt, Germany (Hilbert); German Center for Mental Health, Partner Site Berlin/Potsdam, Berlin, Germany (Lueken); Neuroscience Institute, Department of Psychiatry and Mental Health, University of Cape Town, and South African Medical Research Council Unit on Child and Adolescent Health, Department of Paediatrics and Child Health, Red Cross War Memorial Children's Hospital, University of Cape Town, Cape Town, South Africa (Groenewold); Department of Psychiatry, Leiden University Medical Center, Leiden, the Netherlands (Bas-Hoogendam, Van der Wee); Department of Developmental and Educational Psychology, Institute of Psychology, Leiden University, Leiden, the Netherlands (Bas-Hoogendam); Leiden Institute for Brain and Cognition, Leiden, the Netherlands (Bas-Hoogendam, Van der Wee); Forensic Family and Youth Care Studies, Institute of Education and Child Studies, Leiden University, Leiden, the Netherlands (Aghajani); Department of Psychiatry, Amsterdam UMC location VUMC, Amsterdam (Aghajani, Veltman); Emotion and Development Branch, NIMH, Bethesda, Md. (Zugman, Harrewijn, Pine); Department of Psychology and Social Work, Mid Sweden University, Östersund, Sweden (Åhs); Institute for Translational Psychiatry (Arolt, Böhnlein, Dannlowski, Grotegerd, Leehr, Schrammen), Institute of Medical Psychology and Systems Neuroscience (Hofmann, T. Straube), and University Clinic for Radiology (Kugel), University of Münster, Münster, Germany; Institute for Clinical Psychology and Psychotherapy, Behavioral Epidemiology, Technische Universität Dresden, Dresden, Germany (Beesdo-Baum); Department of Psychology, Lund University, Lund, Sweden (Björkstrand); Munroe-Meyer Institute, University of Nebraska Medical Center, Omaha (Blackford); MRI Research Unit, Department of Radiology, Hospital del Mar, and IMIM-CIBER de Salud Mental, Instituto de Salud Carlos III, Barcelona, Spain (Blanco-Hinojo, Pujol); Institute of Diagnostic Radiology and Neuroradiology (Bülow), Department of Psychiatry and Psychotherapy (Grabe, Wittfeld), Functional Imaging Unit, Diagnostic Radiology and Neuroradiology (Lotze), and Institute for Community Medicine (Völzke), University Medicine Greifswald, Greifswald, Germany; Institut de Recerca Sant Pau (IR SANT PAU), Barcelona, Spain (Cano, Cardoner); Department of Psychiatry and Forensic Medicine, Universitat Autonòma de Barcelona, Barcelona, Spain (Cardoner); Centro de Investigación Biomédica en Red de Salud Mental, Carlos III Health Institute, Madrid (Cano, Cardoner); Department of Psychiatry and Forensic Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain (Cardoner); Department of Psychological Medicine and Clinical Neurosciences, Cardiff University, Cardiff, U.K. (Caseras); Department of Psychiatry and Psychotherapy, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany (Domschke); Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, Tenn. (Feola); Department of Psychology, Uppsala University, Uppsala, Sweden (Fredrikson); Department of Psychiatry and Neuropsychology, Maastricht University Medical Center, Maastricht, the Netherlands (Goossens, Schruers); German Center for Neurodegenerative Diseases, Site Rostock/Greifswald, Greifswald, Germany (Grabe); Department of Psychiatry, University of Pennsylvania, Philadelphia (Gur, Satterthwaite); Department of Biological and Clinical Psychology, University of Greifswald, Greifswald, Germany (Hamm, Richter); Department of Psychology, Education, and Child Studies, Erasmus University Rotterdam, Rotterdam, the Netherlands (Harrewijn); Institute of Clinical Psychology and Psychotherapy, Technische Universität Dresden, Dresden, Germany (Heinig, Leonhardt, J. Schäfer); Department of Psychiatry, Psychosomatics, and Psychotherapy, Center of Mental Health, University Hospital Würzburg, Würzburg, Germany (Herrmann); Interdisciplinary Laboratory of Clinical Neuroscience and Department of Psychiatry, Federal University of São Paulo, São Paulo, Brazil (Jackowski, Pan); Department of Pediatrics, Masonic Institute for the Developing Brain, University of Minnesota, Minneapolis (Larsen); Core-Facility Brain Imaging, Faculty of Medicine (Jansen), and Department of Psychiatry (Krug, Nenadić, F. Stein), University of Marburg, Marburg, Germany; Department of Psychology, Vanderbilt University, Nashville, Tenn. (Kaczkurkin); Department of Psychology, University of Amsterdam, Amsterdam (Kindt, Visser); COMIC Research, Leeds and York Partnership NHS Foundation Trust, Leeds, U.K. (Kingsley); Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden (Klahn); LVR-University Hospital Essen, Department of Psychiatry and Psychotherapy, Faculty of Medicine, and Center for Translational Neuro- and Behavioral Sciences, University of Duisburg-Essen, Essen, North Rhine-Westphalia, Germany (Koelkebeck); Department of Psychiatry, University Hospital of Bonn, Bonn, Germany (Krug); Mental Health Research and Treatment Center, Faculty of Psychology, Ruhr-Universität Bochum, Bochum, Germany (Margraf); Laboratory of Affective Neuroscience in Poznan, SWPS University, Warsaw, Poland (Michałowski); Department of Psychology, Faculty of Human Sciences, and Institute for Cognitive and Affective Neuroscience, Medical School Hamburg, Hamburg, Germany (Muehlhan); Department of Psychology, University of Würzburg, Würzburg, Germany (Pauli, Schulz, Wiemer); Department of Clinical Psychology, Psychobiology, and Methodology, Universidad de La Laguna, San Cristóbal de La Laguna, Spain (Peñate, Rivero); Translational Psychotherapy, Institute of Psychology, University of Göttingen, Göttingen, Germany (Pittig); Department of Medicine, Health and Medical University, Potsdam, Germany (Plag); Department of Experimental Psychopathology, University of Hildesheim, Hildesheim, Germany (Richter); Department of Psychology, Faculty of Health Science, Universidad Europea de Canarias, La Orotava, Spain (Rivero); Section on Negative Affect and Social Processes, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil (Salum); Department of Psychology (A. Schäfer) and Department of Psychotherapy and Systems Neuroscience (Stark), Bender Institute of Neuroimaging, Justus Liebig University Giessen, and Center for Mind, Brain, and Behavior, Universities of Marburg and Giessen (A. Schäfer, Stark), Giessen, Germany; Department of Psychology, University of Graz, Graz, Austria (Schienle, Wabnegger); Clinical Child and Adolescent Psychology, Mental Health Research and Treatment Center, Faculty of Psychology, Ruhr-Universität Bochum, Bochum, Germany (Schneider); Department of Behavioral Medicine and Principles of Human Biology for the Health Sciences, Universität Trier, Trier, Germany (Schulz); Research Group Security and Privacy, Faculty of Computer Science, University of Vienna, Vienna (Seidl); Department of Psychiatry and Psychotherapy, University of Marburg, Marburg, Germany (Kircher, B. Straube, Yang); Department of Psychiatry and Neuroscience, Campus Charité Mitte, Charité-Universitätsmedizin Berlin, Berlin, Germany (Ströhle); Department of Psychology, Ruhr-Universität Bochum, Bochum, Germany (Suchan, Wannemüller); Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Marina del Rey (Thomopoulos, Jahanshad, Thompson); Department of Biological Psychology and Affective Science, Faculty of Human Sciences, University of Potsdam, Potsdam, Germany (Ventura-Bort, Wendt); Health Sciences, University of York, York, U.K. (Wright); Department of Psychiatry and Behavioral Sciences, University of Minnesota Medical School, Minneapolis (Zilverstand); KBO-Inn-Salzach-Klinikum, Wasserburg am Inn, Germany (Zwanzger); Department of Psychiatry and Psychotherapy, Ludwig Maximilians University of Munich, Munich, Germany (Zwanzger); Division of Human Genetics, School of Medicine, University of Texas Rio Grande Valley, Brownsville (Winkler); South African Medical Research Council Unit on Risk and Resilience in Mental Disorders, Neuroscience Institute, Department of Psychiatry and Mental Health, University of Cape Town, Cape Town, South Africa (D.J. Stein); Department of Education, Information, and Communications Technology and Learning, Østfold University College, Halden, Norway (Jackowski).

Objective:

Specific phobia is a common anxiety disorder, but the literature on associated brain structure alterations exhibits substantial gaps. The ENIGMA Anxiety Working Group examined brain structure differences between individuals with specific phobias and healthy control subjects as well as between the animal and blood-injection-injury (BII) subtypes of specific phobia. Additionally, the authors investigated associations of brain structure with symptom severity and age (youths vs. adults).

Methods:

Data sets from 31 original studies were combined to create a final sample with 1,452 participants with phobia and 2,991 healthy participants (62.7% female; ages 5–90). Imaging processing and quality control were performed using established ENIGMA protocols. Subcortical volumes as well as cortical surface area and thickness were examined in a preregistered analysis.

Results:

Compared with the healthy control group, the phobia group showed mostly smaller subcortical volumes, mixed surface differences, and larger cortical thickness across a substantial number of regions. The phobia subgroups also showed differences, including, as hypothesized, larger medial orbitofrontal cortex thickness in BII phobia (N=182) compared with animal phobia (N=739). All findings were driven by adult participants; no significant results were observed in children and adolescents.

Conclusions:

Brain alterations associated with specific phobia exceeded those of other anxiety disorders in comparable analyses in extent and effect size and were not limited to reductions in brain structure. Moreover, phenomenological differences between phobia subgroups were reflected in diverging neural underpinnings, including brain areas related to fear processing and higher cognitive processes. The findings implicate brain structure alterations in specific phobia, although subcortical alterations in particular may also relate to broader internalizing psychopathology.

中文翻译：

特定恐惧症及其动物和血液注射损伤亚型的皮质和皮质下大脑改变：来自 ENIGMA 焦虑工作组的大型分析

客观的：

特定恐惧症是一种常见的焦虑症，但有关相关大脑结构改变的文献存在很大差距。 ENIGMA 焦虑工作组检查了患有特定恐惧症的个体和健康对照受试者之间以及特定恐惧症的动物和血液注射损伤 (BII) 亚型之间的大脑结构差异。此外，作者还研究了大脑结构与症状严重程度和年龄（青少年与成人）的关联。

方法：

来自 31 项原始研究的数据集被合并起来，创建了一个最终样本，其中包括 1,452 名患有恐惧症的参与者和 2,991 名健康参与者（62.7% 为女性；年龄 5-90 岁）。使用既定的 ENIGMA 协议进行成像处理和质量控制。在预先注册的分析中检查皮质下体积以及皮质表面积和厚度。

结果：

与健康对照组相比，恐惧症组的皮质下体积大多较小，表面差异混合，并且在相当多的区域中皮质厚度较大。恐惧症亚组也显示出差异，包括如假设的那样，与动物恐惧症 (N=739) 相比，BII 恐惧症 (N=182) 的内侧眶额皮层厚度更大。所有研究结果均由成年参与者推动；在儿童和青少年中没有观察到显着的结果。