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Aging (Albany NY). 2019 Apr 14;11(7):2045-2070. doi: 10.18632/aging.101900.

Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging: a multi-cohort analysis.

Fiorito G1,2, McCrory C3,2, Robinson O4,2, Carmeli C5,2, Rosales CO6,7,2, Zhang Y8,2, Colicino E9,2, Dugué PA10,11,12,2, Artaud F13,2, McKay GJ14,2, Jeong A15,16,2, Mishra PP17,2, Nøst TH18,19,2, Krogh V20, Panico S21, Sacerdote C22, Tumino R23, Palli D24, Matullo G1,25, Guarrera S1,25, Gandini M26, Bochud M5, Dermitzakis E5, Muka T6,27, Schwartz J28, Vokonas PS29, Just A9, Hodge AM10,11, Giles GG10,11,12, Southey MC10,12,30, Hurme MA31, Young I14, McKnight AJ14, Kunze S32,33, Waldenberger M32,33,34, Peters A32,33,34,35, Schwettmann L36,37,38, Lund E18,38, Baccarelli A39,38, Milne RL10,11,12,38, Kenny RA3,38, Elbaz A13,38, Brenner H8,40,38, Kee F14,38, Voortman T6,38, Probst-Hensch N15,16,38, Lehtimäki T17,38, Elliot P4,38, Stringhini S5,41,38, Vineis P4,38, Polidoro S1,38; BIOS Consortium; Lifepath consortium42.

Author information

1
Italian Institute for Genomic Medicine (IIGM), Turin, Italy.
2
Equal contribution.
3
The Irish Longitudinal Study on Ageing, Trinity College Dublin, Dublin, Ireland.
4
MRC-PHE Centre for Environment and Health, Imperial College London, London, UK.
5
Institute of Social and Preventive Medicine, Lausanne University Hospital (CHUV), Lausanne, Switzerland.
6
Department of Epidemiology, Erasmus University Medical Center, Rotterdam, the Netherlands.
7
Centro de Vida Saludable de la Universidad de Concepción, Concepción, Chile.
8
Division of Clinical Epidemiology and Aging Research, German Cancer Research Center (DKFZ), Heidelberg, Germany.
9
Icahn School of Medicine, Mount Sinai, New York, NY 10029, USA.
10
Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, Australia.
11
Centre for Epidemiology and Biostatistics, School of Population and Global Health, The University of Melbourne, Victoria, Australia.
12
Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
13
CESP, Faculté de Médecine - Université Paris-Sud, Faculté de Médecine, UVSQ, Institut National de la Santé et de la Recherche Médicale, -, Université Paris, Saclay, France.
14
Centre for Public Health, Queen's University Belfast, Belfast, Northern Ireland.
15
Swiss Tropical and Public Health Institute, Basel, Switzerland.
16
University of Basel, Basel, Switzerland.
17
Department of Clinical Chemistry, Fimlab Laboratories, and Finnish Cardiovascular Research Center - Tampere, Faculty of Medicine and Health Technology, Tampere University, Tampere, 33520, Finland.
18
Department of Community Medicine, Faculty of Health Sciences, UiT-The Arctic University of Norway, Tromsø, Norway.
19
NILU Norwegian Institute for Air Research, The Fram Centre, Tromsø, Norway.
20
Fondazione IRCCS - Istituto Nazionale dei Tumori, Milan, Italy.
21
Department of Clinical Medicine and Surgery, University of Naples Federico II, Naples, Italy.
22
Piedmont Reference Centre for Epidemiology and Cancer Prevention (CPO Piemonte), Turin, Italy.
23
Cancer Registry and Histopathology Department, 'Civic - M. P. Arezzo' Hospital, ASP Ragusa, Ragusa, Italy.
24
Istituto per lo Studio, la Prevenzione e la Rete Oncologica (ISPRO Toscana), Florence, Italy.
25
Department of Medical Sciences, University of Torino, Torino, Italy.
26
Environmental Epidemiological Unit, Regional Environmental Protection Agency, Piedmont Region, Torino, Italy.
27
Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland.
28
Department of Environmental Health and Department of Epidemiology, Harvard T.H. School of Public Health, Boston, MA 02115, USA.
29
Department of Epidemiology, Boston University School of Public Health, Boston, MA 02115, USA.
30
Department of Clinical Pathology, The University of Melbourne, Melbourne, Australia.
31
Department of Microbiology and Immunology, Faculty of Medicine and Health Technology, Tampere University, Tampere, 33014, Finland.
32
Research Unit of Molecular Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.
33
Institute of Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Germany.
34
German Center for Cardiovascular Research (DZHK), Munich, Germany.
35
Ludwig-Maximilians-Universität München, Munich, Germany.
36
Institute of Health Economics and Health Care Management, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Neuherberg, D-85764, Germany.
37
Department of Economics, Martin Luther University Halle-Wittenberg, Halle, Germany.
38
Equal senior researcher.
39
Department of Environmental Health Sciences, Columbia University Mailman School of Public Health, New York, NY 10032, USA.
40
Network Aging Research, University of Heidelberg, Heidelberg, Germany.
41
Unit of Population Epidemiology, Primary Care Division, Geneva University Hospitals, Geneva, Switzerland.
42
See ACKNOWLEDGMENTS AND FUNDING.

Abstract

Differences in health status by socioeconomic position (SEP) tend to be more evident at older ages, suggesting the involvement of a biological mechanism responsive to the accumulation of deleterious exposures across the lifespan. DNA methylation (DNAm) has been proposed as a biomarker of biological aging that conserves memory of endogenous and exogenous stress during life.We examined the association of education level, as an indicator of SEP, and lifestyle-related variables with four biomarkers of age-dependent DNAm dysregulation: the total number of stochastic epigenetic mutations (SEMs) and three epigenetic clocks (Horvath, Hannum and Levine), in 18 cohorts spanning 12 countries.The four biological aging biomarkers were associated with education and different sets of risk factors independently, and the magnitude of the effects differed depending on the biomarker and the predictor. On average, the effect of low education on epigenetic aging was comparable with those of other lifestyle-related risk factors (obesity, alcohol intake), with the exception of smoking, which had a significantly stronger effect.Our study shows that low education is an independent predictor of accelerated biological (epigenetic) aging and that epigenetic clocks appear to be good candidates for disentangling the biological pathways underlying social inequalities in healthy aging and longevity.

KEYWORDS:

biological aging; education; epigenetic clocks; socioeconomic position

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