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

doi:10.1016/j.nicl.2022.102949

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

Neuroimage Clin. 2022:33:102949. doi: 10.1016/j.nicl.2022.102949. Epub 2022 Jan 27.

Authors

Dani Beck¹, Ann-Marie G de Lange², Dag Alnæs³, Ivan I Maximov⁴, Mads L Pedersen⁵, Olof Dahlqvist Leinhard⁶, Jennifer Linge⁷, Rozalyn Simon⁶, Geneviève Richard⁸, Kristine M Ulrichsen⁹, Erlend S Dørum⁹, Knut K Kolskår⁹, Anne-Marthe Sanders⁹, Adriano Winterton⁸, Tiril P Gurholt⁸, Tobias Kaufmann¹⁰, Nils Eiel Steen⁸, Jan Egil Nordvik¹¹, Ole A Andreassen¹², Lars T Westlye¹³

Affiliations

¹ 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. Electronic address: dani.beck@psykologi.uio.no.
² 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.
³ NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway; Bjørknes College, Oslo, Norway.
⁴ 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.
⁵ 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.
⁶ 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.
⁷ AMRA Medical AB, Linköping, Sweden; Department of Health, Medicine, and Caring Sciences, Linköping University, Linköping, Sweden.
⁸ NORMENT, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Norway.
⁹ 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.
¹⁰ 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.
¹¹ CatoSenteret Rehabilitation Center, Son, Norway.
¹² 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.
¹³ 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. Electronic address: l.t.westlye@psykologi.uio.no.

Abstract

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.

Keywords: Adipose tissue; Brain age; DTI; MRI; Obesity; T1.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Adult
Aged
Aged, 80 and over
Bayes Theorem
Body Fat Distribution*
Body Mass Index
Brain / diagnostic imaging
Cross-Sectional Studies
Diffusion Tensor Imaging*
Humans
Magnetic Resonance Imaging
Middle Aged
Tissue Distribution
Young Adult