Cited by 624Genetics, Aging, and Longevity in Model OrganismsDementia and Cognitive Impairment ResearchFrailty in Older Adults

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Heterogeneous aging across multiple organ systems and prediction of chronic disease and mortality

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Tian, Ye Ella, Cropley, Vanessa, Maier, Andrea B., Lautenschlager, Nicola T., Breakspear, Michael, Zalesky, Andrew·2023·Nature Medicine

DOI 10.1038/s41591-023-02296-6

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Abstract

Biological aging of human organ systems reflects the interplay of age, chronic disease, lifestyle and genetic risk. Using longitudinal brain imaging and physiological phenotypes from the UK Biobank, we establish normative models of biological age for three brain and seven body systems. Here we find that an organ's biological age selectively influences the aging of other organ systems, revealing a multiorgan aging network. We report organ age profiles for 16 chronic diseases, where advanced biological aging extends from the organ of primary disease to multiple systems. Advanced body age associates with several lifestyle and environmental factors, leukocyte telomere lengths and mortality risk, and predicts survival time (area under the curve of 0.77) and premature death (area under the curve of 0.86). Our work reveals the multisystem nature of human aging in health and chronic disease. It may enable early identification of individuals at increased risk of aging-related morbidity and inform new strategies to potentially limit organ-specific aging in such individuals.

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Authors: Tian, Y. E., Cropley, V., Maier, A. B., Lautenschlager, N. T., Breakspear, M., & Zalesky, A.
Affiliations: The University of Melbourne (AU)
National University of Singapore (SG)
The Royal Melbourne Hospital (AU)
University of Newcastle Australia (AU)
Corresponding author: Tian, Ye Ella
Zalesky, Andrew
ORCID: Tian, Ye Ella
Cropley, Vanessa
Maier, Andrea B.
Lautenschlager, Nicola T.
Breakspear, Michael
Zalesky, Andrew
Venue: Nature Medicine
Publisher: Springer Science and Business Media LLC
Published: 2023-04-06
Volume: 29
Issue: 5
Pages: 1221-1231
ISSN: 1078-8956 (ISSN-L)
1546-170X
DOI: 10.1038/s41591-023-02296-6
OpenAlex: W4362674168
Cited by: 618
References: 106
Citations by year: 2026: 174 · 2025: 224 · 2024: 180 · 2023: 39
FWCI: 41.89
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Medicine (publishedVersion, other-oa)
medRxiv (acceptedVersion, cc-by)
PubMed (publishedVersion)
Minerva Access (University of Melbourne) (submittedVersion)
VU Research Portal (submittedVersion, other-oa)
NOVA (University of Newcastle Australia) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: U.S. Department of Defense (U01 AG024904, W81XWH, W81XWH-12-2-, W81XWH1220012, AG024904)
Foundation for the National Institutes of Health (W81XWH-12-2-0012, U01AG024904, AG024904)
Alzheimer's Association (U01 AG024904, W81XWH-12-2-0012)
Bristol-Myers Squibb (U01 AG024904, AG024904, W81XWH-12-2-0012)
Eli Lilly and Company (U01 AG024904, AG024904, W81XWH-12-2-0012)
Pfizer (AG024904, W81XWH-12-2-0012, U01 AG024904)
Biogen (W81XWH-12-2-0012, U01 AG024904, AG024904)
University of Southern California (W81XWH-12-2-0012, U01 AG024904)
F. Hoffmann-La Roche (W81XWH-12-2-0012, AG024904, U01 AG024904)
Meso Scale Diagnostics (U01 AG024904, AG024904, W81XWH-12-2-0012)
Alzheimer's Disease Neuroimaging Initiative
BioClinica (U01 AG024904, W81XWH-12-2-0012, AG024904)
Novartis Pharmaceuticals Corporation (W81XWH-12-2-0012, U01 AG024904, AG024904)
Northern California Institute for Research and Education (U01 AG024904, W81XWH-12-2-0012)
University of Oxford
Commonwealth Scientific and Industrial Research Organisation
Eisai (W81XWH-12-2-0012, U01 AG024904, AG024904)
Universitetet i Oslo
Servier (AG024904, W81XWH-12-2-0012, U01 AG024904)
H. Lundbeck A/S (U01 AG024904, AG024904, W81XWH-12-2-0012)
IXICO (AG024904, W81XWH-12-2-0012, U01 AG024904)
National Institutes of Health (3u01ag024904-10s2, W81XWH, W81XWH-12-2-0012, U01-AG024904, AG024904)
Genentech (W81XWH-12-2-0012, AG024904, U01 AG024904)
Canadian Institutes of Health Research (U01 AG024904, W81XWH-12-2-0012)
Medical Research Council (U01 AG024904, MC_PC_17228)
National Health and Medical Research Council (1095227, 1142801, 2008612, APP118153, 1177370, 1152623)
National Institute on Aging (U01-AG-024904, W81XWH-12-2–0012, AG 024904)
National Institute of Biomedical Imaging and Bioengineering (W81XWH-12-2-0012, U01 AG024904, AG024904)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Health Sciences › Medicine › Geriatrics and Gerontology › Frailty in Older Adults
Keywords: biological aging, biological age prediction, chronic disease, mortality prediction, brain aging, telomere length, lifestyle factors, normative model, survival prediction, premature mortality
MeSH terms: Aging, Brain, Chronic Disease, Humans, Leukocytes, Risk Factors

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