A comparison of methods to harmonize cortical thickness measurements across scanners and sites.

Journal: NeuroImage

Volume: 261

Issue: 

Year of Publication: 2022

Affiliated Institutions:  Brain Imaging and Analysis Center, Duke University, Durham, NC, USA.; Department of Veteran Affairs (VA) Mid-Atlantic Mental Illness Research, Education and Clinical Center, Durham, NC, USA.; Department of Psychology, The Education University of Hong Kong, Hong Kong, China. Brain Imaging and Analysis Center, Duke University, Durham, NC, USA.; Department of Veteran Affairs (VA) Mid-Atlantic Mental Illness Research, Education and Clinical Center, Durham, NC, USA. National Center for PTSD, VA Boston Healthcare System, Boston, MA, USA.; Department of Psychiatry, Boston University School of Medicine, Boston, MA, USA.; Biomedical Genetics, Boston University School of Medicine, Boston, MA, USA.; Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA. Department of Psychiatry, University of Toledo, Toledo, OH, USA. Department of Psychiatry, University of Toledo, Toledo, OH, USA.; Psychiatry Neuroimaging Laboratory, Brigham & Women's Hospital, Boston, MA, USA. Psychiatry Neuroimaging Laboratory, Brigham & Women's Hospital, Boston, MA, USA.; Imaging Genetics Center, Mark & Mary Stevens Neuroimaging & Informatics Institute, Keck School of Medicine of USC, Marina del Rey, CA, USA.; Department of Neurology, University of Utah, Salt Lake City, UT, USA.; Stanford Neurodevelopment, Affect, and Psychopathology Laboratory, Stanford, CA, USA. Imaging Genetics Center, Mark & Mary Stevens Neuroimaging & Informatics Institute, Keck School of Medicine of USC, Marina del Rey, CA, USA. Department of Psychiatry, Amsterdam University Medical Centers, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.; Donders Institute for Brain, Cognition and Behavior, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, The Netherlands. Department of Psychiatry, Amsterdam University Medical Centers, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands. Department of Psychiatry, Amsterdam University Medical Centers, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.; Department of Psychiatry, Amsterdam University Medical Centers, VU University Medical Center, VU University, Amsterdam, The Netherlands. Department of Psychiatry, Columbia University Medical Center, New York, NY, USA.; New York State Psychiatric Institute, New York, NY, USA. Del Monte Institute for Neuroscience, University of Rochester Medical Center, Rochester, NY, USA.; Department of Psychiatry, Columbia University Medical Center, New York, NY, USA.; New York State Psychiatric Institute, New York, NY, USA. University Medical Centre Charité, Berlin, Germany. Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, USA. Department of Psychiatry, University of California San Diego, La Jolla, CA, USA. Psychiatry Neuroimaging Laboratory, Brigham & Women's Hospital, Boston, MA, USA.; Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Ludwig-Maximilians-Universität, Munich, Germany. Health Services Research Center, University of California, San Diego, La Jolla, CA, USA. Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands.; Leiden Institute for Brain and Cognition, Leiden, The Netherlands. Department of Psychiatry, Leiden University Medical Center, Leiden, The Netherlands. Department of Psychosomatic Medicine and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Heidelberg, Germany. Department of Psychiatry, Harvard Medical School, Boston, MA, USA.; Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA. Institute for Technology in Psychiatry, McLean Hospital, Harvard University, Belmont, MA, USA. Department of Psychiatry, Harvard Medical School, Boston, MA, USA.; Center for Depression, Anxiety, and Stress Research, McLean Hospital, Belmont, MA, USA. Institute of Medical Psychology and Systems Neuroscience, University of Münster, Münster, Germany. Brain Dynamics Centre, Westmead Institute of Medical Research, University of Sydney, Westmead, NSW, Australia. Department of Psychology, University of Sydney, Westmead, NSW, Australia. Laboratory for Traumatic Stress Studies, Chinese Academy of Sciences Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China. SA MRC Unit on Risk & Resilience in Mental Disorders, Department of Psychiatry and Neuroscience Institute, University of Cape Town, Cape Town, South Africa. Department of Experimental Clinical and Health Psychology, Ghent University, Ghent, Belgium. Department of Psychology, University of Washington, Seattle, WA, USA. Department of Radiology, University of Washington, Seattle, WA, USA. Department of Radiology, Washington University, St. Louis, MO, USA. Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, SD, USA.; Center for Brain and Behavior Research, University of South Dakota, Vermillion, SD, USA.; Sioux Falls VA Health Care System, Sioux Falls, SD, USA. Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, SD, USA.; Center for Brain and Behavior Research, University of South Dakota, Vermillion, SD, USA.; Brain Health Research Centre, Department of Anatomy, University of Otago, Dunedin, New Zealand. Center for Brain and Behavior Research, University of South Dakota, Vermillion, SD, USA.; Department of Psychology, University of South Dakota, Vermillion, SD, USA. Sioux Falls VA Health Care System, Sioux Falls, SD, USA.; Department of Psychology, University of South Dakota, Vermillion, SD, USA. Department of Radiology, Psychiatry, and Biomedical Engineering, University of Iowa, Iowa City, IA, USA. Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA. Department of Psychiatry, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa. Minneapolis VA Health Care System, Minneapolis, MN, USA.; Department of Psychiatry, University of Minnesota, Minneapolis, MN, USA. Center for Healthy Minds, University of Wisconsin-Madison, Madison, WI, USA. Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA. Department of Surgery, Division of Trauma and Acute Care Surgery, Medical College of Wisconsin, Milwaukee, WI, USA. Department of Psychology, Marquette University, Milwaukee, WI, USA. Division of Clinical Neuroscience, National Center for PTSD, West Haven, CT, USA.; Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA. Department of Psychiatry, Amsterdam University Medical Centers, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.; ARQ National Psychotrauma Centre, Diemen, The Netherlands. Department of Psychiatry, Amsterdam University Medical Center, location VUMC, Amsterdam, The Netherlands. Healthy Childhood Brain Development Developmental Traumatology Research Program, Department of Psychiatry and Behavioral Sciences, Duke University, Durham, NC, USA. Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, MI, USA. Department of Clinical Psychology, University of Groningen, Groningen, The Netherlands. Psychiatry Neuroimaging Laboratory, Brigham & Women's Hospital, Boston, MA, USA.; VA Boston Healthcare System, Brockton Division, Brockton, MA, USA. Department of Psychiatry, Harvard Medical School, Boston, MA, USA.; Division of Women's Mental Health, McLean Hospital, Belmont, MA, USA. School of Psychology, University of New South Wales, Sydney, NSW, Australia. Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, SD, USA.; Center for Brain and Behavior Research, University of South Dakota, Vermillion, SD, USA.; Sioux Falls VA Health Care System, Sioux Falls, SD, USA.; Civil Aerospace Medical Institute, US Federal Aviation Administration, Oklahoma City, OK, USA. Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA. Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA.; Mental Health Service Line, Jesse Brown VA Chicago Health Care System, Chicago, IL, USA. Department of Psychology, Harvard University, Cambridge, MA, USA. Center for Healthy Minds, University of Wisconsin-Madison, Madison, WI, USA.; Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA.; Department of Psychology, University of Wisconsin-Madison, Madison, WI, USA. Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, WI, USA. Veterans Integrated Service Network- Center of Excellence for Research on Returning War Veterans, Waco, TX, USA.; Department of Psychology and Neuroscience, Baylor University, Waco, TX, USA.; Center for Vital Longevity, School of Behavioral and Brain Sciences, University of Texas at Dallas, Dallas, TX, USA.; Department of Psychiatry and Behavioral Science, Texas A&M University Health Science Center, Bryan, TX, USA. Department of Psychiatry and Behavioral Health, Pennsylvania State University, Hershey, PA, USA. Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.; VA Palo Alto Health Care System, Palo Alto, CA, USA. Department of Psychiatry and Behavioral Science, Texas A&M University, College Station, TX, USA. Clinical Translational Neuroscience Laboratory, Department of Psychiatry and Human Behavior, University of California Irvine, Irvine, CA, USA.; Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA, USA. School of Psychology, The University of New South Wales, Sydney, NSW, Australia.; Neuroscience Research Australia, Randwick, NSW, Australia. Department of Mathematics and Statistics, University of Toledo, Toledo, OH, USA. Brain Imaging and Analysis Center, Duke University, Durham, NC, USA.; Department of Veteran Affairs (VA) Mid-Atlantic Mental Illness Research, Education and Clinical Center, Durham, NC, USA.. Electronic address: rajendra.morey@duke.edu.

Abstract summary 

Results of neuroimaging datasets aggregated from multiple sites may be biased by site-specific profiles in participants' demographic and clinical characteristics, as well as MRI acquisition protocols and scanning platforms. We compared the impact of four different harmonization methods on results obtained from analyses of cortical thickness data: (1) linear mixed-effects model (LME) that models site-specific random intercepts (LME), (2) LME that models both site-specific random intercepts and age-related random slopes (LME), (3) ComBat, and (4) ComBat with a generalized additive model (ComBat-GAM). Our test case for comparing harmonization methods was cortical thickness data aggregated from 29 sites, which included 1,340 cases with posttraumatic stress disorder (PTSD) (6.2-81.8 years old) and 2,057 trauma-exposed controls without PTSD (6.3-85.2 years old). We found that, compared to the other data harmonization methods, data processed with ComBat-GAM was more sensitive to the detection of significant case-control differences (Χ(3) = 63.704, p < 0.001) as well as case-control differences in age-related cortical thinning (Χ(3) = 12.082, p = 0.007). Both ComBat and ComBat-GAM outperformed LME methods in detecting sex differences (Χ(3) = 9.114, p = 0.028) in regional cortical thickness. ComBat-GAM also led to stronger estimates of age-related declines in cortical thickness (corrected p-values < 0.001), stronger estimates of case-related cortical thickness reduction (corrected p-values < 0.001), weaker estimates of age-related declines in cortical thickness in cases than controls (corrected p-values < 0.001), stronger estimates of cortical thickness reduction in females than males (corrected p-values < 0.001), and stronger estimates of cortical thickness reduction in females relative to males in cases than controls (corrected p-values < 0.001). Our results support the use of ComBat-GAM to minimize confounds and increase statistical power when harmonizing data with non-linear effects, and the use of either ComBat or ComBat-GAM for harmonizing data with linear effects.

Authors & Co-authors:  Sun Delin D Rakesh Gopalkumar G Haswell Courtney C CC Logue Mark M Baird C Lexi CL O'Leary Erin N EN Cotton Andrew S AS Xie Hong H Tamburrino Marijo M Chen Tian T Dennis Emily L EL Jahanshad Neda N Salminen Lauren E LE Thomopoulos Sophia I SI Rashid Faisal F Ching Christopher R K CRK Koch Saskia B J SBJ Frijling Jessie L JL Nawijn Laura L van Zuiden Mirjam M Zhu Xi X Suarez-Jimenez Benjamin B Sierk Anika A Walter Henrik H Manthey Antje A Stevens Jennifer S JS Fani Negar N van Rooij Sanne J H SJH Stein Murray M Bomyea Jessica J Koerte Inga K IK Choi Kyle K van der Werff Steven J A SJA Vermeiren Robert R J M RRJM Herzog Julia J Lebois Lauren A M LAM Baker Justin T JT Olson Elizabeth A EA Straube Thomas T Korgaonkar Mayuresh S MS Andrew Elpiniki E Zhu Ye Y Li Gen G Ipser Jonathan J Hudson Anna R AR Peverill Matthew M Sambrook Kelly K Gordon Evan E Baugh Lee L Forster Gina G Simons Raluca M RM Simons Jeffrey S JS Magnotta Vincent V Maron-Katz Adi A du Plessis Stefan S Disner Seth G SG Davenport Nicholas N Grupe Daniel W DW Nitschke Jack B JB deRoon-Cassini Terri A TA Fitzgerald Jacklynn M JM Krystal John H JH Levy Ifat I Olff Miranda M Veltman Dick J DJ Wang Li L Neria Yuval Y De Bellis Michael D MD Jovanovic Tanja T Daniels Judith K JK Shenton Martha M van de Wee Nic J A NJA Schmahl Christian C Kaufman Milissa L ML Rosso Isabelle M IM Sponheim Scott R SR Hofmann David Bernd DB Bryant Richard A RA Fercho Kelene A KA Stein Dan J DJ Mueller Sven C SC Hosseini Bobak B Phan K Luan KL McLaughlin Katie A KA Davidson Richard J RJ Larson Christine L CL May Geoffrey G Nelson Steven M SM Abdallah Chadi G CG Gomaa Hassaan H Etkin Amit A Seedat Soraya S Harpaz-Rotem Ilan I Liberzon Israel I van Erp Theo G M TGM Quidé Yann Y Wang Xin X Thompson Paul M PM Morey Rajendra A RA

Study Outcome 

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Statistics
Citations :  Agarwal P, Shroff G, Malhotra P, 2013. Approximate incremental big-data harmonization. In: 2013 IEEE International Congress on Big Data, pp. 118–125.
Authors :  99
Identifiers
Doi : 10.1016/j.neuroimage.2022.119509
SSN : 1095-9572
Study Population
Males,Females
Mesh Terms
Adolescent
Other Terms
ComBat;ComBat-GAM;Cortical Thickness;Data Harmonization;General Additive Model;Linear Mixed-Effects Model;PTSD;Scanner Effects;Site Effects
Study Design
Case Study,Cross Sectional Study
Study Approach
Country of Study
Publication Country
United States