Adipose tissue distribution from body MRI is associated with cross-sectional and longitudinal brain age in adults

Dani Beck; Ann-Marie G. de Lange; Dag Alnæs; Ivan I. Maximov; Mads L. Pedersen; Olof Dahlqvist Leinhard; Jennifer Linge; Rozalyn Simon; Geneviève Richard; Kristine M. Ulrichsen; Erlend S. Dørum; Knut K. Kolskår; Anne-Marthe Sanders; Adriano Winterton; Tiril P. Gurholt; Tobias Kaufmann; Nils Eiel Steen; Jan Egil Nordvik; Ole A. Andreassen; Lars T. Westlye

NeuroImage: Clinical (Jan 2022)

Adipose tissue distribution from body MRI is associated with cross-sectional and longitudinal brain age in adults

Dani Beck,
Ann-Marie G. de Lange,
Dag Alnæs,
Ivan I. Maximov,
Mads L. Pedersen,
Olof Dahlqvist Leinhard,
Jennifer Linge,
Rozalyn Simon,
Geneviève Richard,
Kristine M. Ulrichsen,
Erlend S. Dørum,
Knut K. Kolskår,
Anne-Marthe Sanders,
Adriano Winterton,
Tiril P. Gurholt,
Tobias Kaufmann,
Nils Eiel Steen,
Jan Egil Nordvik,
Ole A. Andreassen,
Lars T. Westlye

Affiliations

Dani Beck: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; Sunnaas Rehabilitation Hospital HT, Nesodden, Norway; Corresponding authors at: Department of Psychology, University of Oslo, PoBox 1094 Blindern, 0317 Oslo, Norway.
Ann-Marie G. de Lange: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; LREN, Centre for Research in Neurosciences-Department of Clinical Neurosciences, CHUV and University of Lausanne, Lausanne, Switzerland; Department of Psychiatry, University of Oxford, Warneford Hospital, Oxford, UK
Dag Alnæs: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Bjørknes College, Oslo, Norway
Ivan I. Maximov: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; Department of Health and Functioning, Western Norway University of Applied Sciences, Bergen, Norway
Mads L. Pedersen: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway
Olof Dahlqvist Leinhard: AMRA Medical AB, Linköping, Sweden; Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden; Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden
Jennifer Linge: AMRA Medical AB, Linköping, Sweden; Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden
Rozalyn Simon: AMRA Medical AB, Linköping, Sweden; Center for Medical Image Science and Visualization (CMIV), Linköping University, Linköping, Sweden; Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden
Geneviève Richard: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
Kristine M. Ulrichsen: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
Erlend S. Dørum: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
Knut K. Kolskår: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
Anne-Marthe Sanders: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
Adriano Winterton: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
Tiril P. Gurholt: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
Tobias Kaufmann: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychiatry and Psychotherapy, University of Tübingen, Germany
Nils Eiel Steen: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway
Jan Egil Nordvik: CatoSenteret Rehabilitation Center, Son, Norway
Ole A. Andreassen: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; KG Jebsen Centre for Neurodevelopmental Disorders, University of Oslo, Norway
Lars T. Westlye: NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Department of Psychology, University of Oslo, Norway; KG Jebsen Centre for Neurodevelopmental Disorders, University of Oslo, Norway; Corresponding authors at: Department of Psychology, University of Oslo, PoBox 1094 Blindern, 0317 Oslo, Norway.

Journal volume & issue: Vol. 33
p. 102949

Abstract

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There is an intimate body-brain connection in ageing, and obesity is a key risk factor for poor cardiometabolic health and neurodegenerative conditions. Although research has demonstrated deleterious effects of obesity on brain structure and function, the majority of studies have used conventional measures such as waist-to-hip ratio, waist circumference, and body mass index. While sensitive to gross features of body composition, such global anthropometric features fail to describe regional differences in body fat distribution and composition. The sample consisted of baseline brain magnetic resonance imaging (MRI) acquired from 790 healthy participants aged 18–94 years (mean ± standard deviation (SD) at baseline: 46.8 ± 16.3), and follow-up brain MRI collected from 272 of those individuals (two time-points with 19.7 months interval, on average (min = 9.8, max = 35.6). Of the 790 included participants, cross-sectional body MRI data was available from a subgroup of 286 participants, with age range 19–86 (mean = 57.6, SD = 15.6). Adopting a mixed cross-sectional and longitudinal design, we investigated cross-sectional body magnetic resonance imaging measures of adipose tissue distribution in relation to longitudinal brain structure using MRI-based morphometry (T1) and diffusion tensor imaging (DTI). We estimated tissue-specific brain age at two time points and performed Bayesian multilevel modelling to investigate the associations between adipose measures at follow-up and brain age gap (BAG) – the difference between actual age and the prediction of the brain’s biological age – at baseline and follow-up. We also tested for interactions between BAG and both time and age on each adipose measure. The results showed credible associations between T1-based BAG and liver fat, muscle fat infiltration (MFI), and weight-to-muscle ratio (WMR), indicating older-appearing brains in people with higher measures of adipose tissue. Longitudinal evidence supported interaction effects between time and MFI and WMR on T1-based BAG, indicating accelerated ageing over the course of the study period in people with higher measures of adipose tissue. The results show that specific measures of fat distribution are associated with brain ageing and that different compartments of adipose tissue may be differentially linked with increased brain ageing, with potential to identify key processes involved in age-related transdiagnostic disease processes.

Published in NeuroImage: Clinical

ISSN: 2213-1582 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General): Computer applications to medicine. Medical informatics; Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry: Neurology. Diseases of the nervous system
Website: http://www.journals.elsevier.com/neuroimage-clinical/

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