Brain aging patterns in a large and diverse cohort of 49,482 individuals.


Journal

Nature medicine
ISSN: 1546-170X
Titre abrégé: Nat Med
Pays: United States
ID NLM: 9502015

Informations de publication

Date de publication:
15 Aug 2024
Historique:
received: 31 12 2023
accepted: 20 06 2024
medline: 16 8 2024
pubmed: 16 8 2024
entrez: 15 8 2024
Statut: aheadofprint

Résumé

Brain aging process is influenced by various lifestyle, environmental and genetic factors, as well as by age-related and often coexisting pathologies. Magnetic resonance imaging and artificial intelligence methods have been instrumental in understanding neuroanatomical changes that occur during aging. Large, diverse population studies enable identifying comprehensive and representative brain change patterns resulting from distinct but overlapping pathological and biological factors, revealing intersections and heterogeneity in affected brain regions and clinical phenotypes. Herein, we leverage a state-of-the-art deep-representation learning method, Surreal-GAN, and present methodological advances and extensive experimental results elucidating brain aging heterogeneity in a cohort of 49,482 individuals from 11 studies. Five dominant patterns of brain atrophy were identified and quantified for each individual by respective measures, R-indices. Their associations with biomedical, lifestyle and genetic factors provide insights into the etiology of observed variances, suggesting their potential as brain endophenotypes for genetic and lifestyle risks. Furthermore, baseline R-indices predict disease progression and mortality, capturing early changes as supplementary prognostic markers. These R-indices establish a dimensional approach to measuring aging trajectories and related brain changes. They hold promise for precise diagnostics, especially at preclinical stages, facilitating personalized patient management and targeted clinical trial recruitment based on specific brain endophenotypic expression and prognosis.

Identifiants

pubmed: 39147830
doi: 10.1038/s41591-024-03144-x
pii: 10.1038/s41591-024-03144-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIA NIH HHS
ID : RF1 AG054409
Pays : United States

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature America, Inc.

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Auteurs

Zhijian Yang (Z)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Graduate Group in Applied Mathematics and Computational Science, University of Pennsylvania, Philadelphia, PA, USA.
GE Healthcare, Bellevue, WA, USA.

Junhao Wen (J)

Laboratory of AI and Biomedical Science (LABS), Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, USA.

Guray Erus (G)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Sindhuja T Govindarajan (ST)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Randa Melhem (R)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Elizabeth Mamourian (E)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Yuhan Cui (Y)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Dhivya Srinivasan (D)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Ahmed Abdulkadir (A)

Laboratory for Research in Neuroimaging, Department of Clinical Neurosciences, Lausanne University Hospital (CHUV) and University of Lausanne, Lausanne, Switzerland.

Paraskevi Parmpi (P)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Katharina Wittfeld (K)

Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.

Hans J Grabe (HJ)

Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.
Site Rostock/Greifswald, German Center for Neurodegenerative Diseases (DZNE), Greifswald, Germany.

Robin Bülow (R)

Institute of Diagnostic Radiology and Neuroradiology, University of Greifswald, Greifswald, Germany.

Stefan Frenzel (S)

Department of Psychiatry and Psychotherapy, University Medicine Greifswald, Greifswald, Germany.

Duygu Tosun (D)

Department of Radiology and Biomedical Imaging, University of California, San Francisco, San Francisco, CA, USA.

Murat Bilgel (M)

Laboratory of Behavioral Neuroscience, National Institute on Aging, National Institutes of Health, Baltimore, MD, USA.

Yang An (Y)

Laboratory of Behavioral Neuroscience, National Institute on Aging, National Institutes of Health, Baltimore, MD, USA.

Dahyun Yi (D)

Institute of Human Behavioral Medicine, Medical Research Center Seoul National University, Seoul, Republic of Korea.

Daniel S Marcus (DS)

Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, MO, USA.

Pamela LaMontagne (P)

Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, MO, USA.

Tammie L S Benzinger (TLS)

Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, MO, USA.

Susan R Heckbert (SR)

Cardiovascular Health Research Unit and Department of Epidemiology, University of Washington, Seattle, WA, USA.

Thomas R Austin (TR)

Cardiovascular Health Research Unit and Department of Epidemiology, University of Washington, Seattle, WA, USA.

Shari R Waldstein (SR)

Department of Psychology, University of Maryland, Baltimore County, Baltimore, MD, USA.

Michele K Evans (MK)

Health Disparities Research Section, Laboratory of Epidemiology and Population Sciences, NIA/NIH/IRP, Baltimore, MD, USA.

Alan B Zonderman (AB)

Health Disparities Research Section, Laboratory of Epidemiology and Population Sciences, NIA/NIH/IRP, Baltimore, MD, USA.

Lenore J Launer (LJ)

Neuroepidemiology Section, Intramural Research Program, National Institute on Aging, Bethesda, MD, USA.

Aristeidis Sotiras (A)

Department of Radiology and Institute for Informatics, Data Science & Biostatistics, Washington University in St. Louis, St. Louis, MO, USA.

Mark A Espeland (MA)

Department of Internal Medicine, Wake Forest University School of Medicine, Winston-Salem, NC, USA.

Colin L Masters (CL)

Florey Institute, The University of Melbourne, Parkville, Victoria, Australia.

Paul Maruff (P)

Florey Institute, The University of Melbourne, Parkville, Victoria, Australia.

Jurgen Fripp (J)

CSIRO Health and Biosecurity, Australian e-Health Research Centre CSIRO, Brisbane, Queensland, Australia.

Arthur W Toga (AW)

Laboratory of Neuro Imaging, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine of USC, University of Southern California, Los Angeles, CA, USA.

Sid O'Bryant (S)

Institute for Translational Research University of North Texas Health Science Center, Fort Worth, TX, USA.

Mallar M Chakravarty (MM)

Computational Brain Anatomy (CoBrA) Laboratory, Cerebral Imaging Center, Douglas Mental Health University Institute, McGill University, Verdun, Quebec, Canada.

Sylvia Villeneuve (S)

McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada.

Sterling C Johnson (SC)

Wisconsin Alzheimer's Institute, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA.

John C Morris (JC)

Knight Alzheimer Disease Research Center, Dept of Neurology, Washington University School of Medicine, St. Louis, MO, USA.

Marilyn S Albert (MS)

Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA.

Kristine Yaffe (K)

Departments of Neurology, Psychiatry and Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, CA, USA.

Henry Völzke (H)

Institute for Community Medicine, University Medicine Greifswald, Greifswald, Germany.

Luigi Ferrucci (L)

Translational Gerontology Branch, Longitudinal Studies Section, National Institute on Aging, National Institutes of Health, MedStar Harbor Hospital, Baltimore, MD, USA.

R Nick Bryan (R)

Department of Radiology, University of Pennsylvania, Philadelphia, PA, USA.

Russell T Shinohara (RT)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, & Informatics, University of Pennsylvania, Philadelphia, PA, USA.

Yong Fan (Y)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Mohamad Habes (M)

Neuroimage Analytics Laboratory and Biggs Institute Neuroimaging Core, Glenn Biggs Institute for Neurodegenerative Disorders, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA.

Paris Alexandros Lalousis (PA)

Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.

Nikolaos Koutsouleris (N)

Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK.
Section for Precision Psychiatry, Department of Psychiatry and Psychotherapy, Ludwig-Maximilian-University Munich, Munich, Germany.

David A Wolk (DA)

Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

Susan M Resnick (SM)

Laboratory of Behavioral Neuroscience, National Institute on Aging, National Institutes of Health, Baltimore, MD, USA.

Haochang Shou (H)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Penn Statistics in Imaging and Visualization Center, Department of Biostatistics, Epidemiology, & Informatics, University of Pennsylvania, Philadelphia, PA, USA.

Ilya M Nasrallah (IM)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
Department of Radiology, University of Pennsylvania, Philadelphia, PA, USA.

Christos Davatzikos (C)

Artificial Intelligence in Biomedical Imaging Laboratory (AIBIL), Center for and Data Science for Integrated Diagnostics (AI2D), Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. Christos.Davatzikos@pennmedicine.upenn.edu.

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