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

Giovanni Fiorito, Cathal McCrory, Oliver Robinson, Cristian Carmeli, Carolina Ochoa Rosales, Yan Zhang, Elena Colicino, Pierre Antoine Dugué, Fanny Artaud, Gareth J. McKay, Ayoung Jeong, Pashupati P. Mishra, Therese H. Nøst, Vittorio Krogh, Salvatore Panico, Carlotta Sacerdote, Rosario Tumino, Domenico Palli, Giuseppe Matullo, Simonetta Guarrera & 33 others Martina Gandini, Murielle Bochud, Emmanouil Dermitzakis, Taulant Muka, Joel Schwartz, Pantel S. Vokonas, Allan Just, Allison M. Hodge, Graham G. Giles, Melissa C. Southey, Mikko A. Hurme, Ian Young, Amy Jayne McKnight, Sonja Kunze, Melanie Waldenberger, Annette Peters, Lars Schwettmann, Eiliv Lund, Andrea Baccarelli, Roger L. Milne, Rose A. Kenny, Alexis Elbaz, Hermann Brenner, Frank Kee, Trudy Voortman, Nicole Probst-Hensch, Terho Lehtimäki, Paul Elliot, Silvia Stringhini, Paolo Vineis, Silvia Polidoro, the BIOS Consortium, the LIFEPATH consortium

Research output: Contribution to journalArticleResearchpeer-review

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.

Original languageEnglish
Pages (from-to)2045-2070
Number of pages26
JournalAging
Volume11
Issue number7
DOIs
Publication statusPublished - 15 Apr 2019

Keywords

  • Biological aging
  • Education
  • Epigenetic clocks
  • Socioeconomic position

Cite this

Fiorito, G., McCrory, C., Robinson, O., Carmeli, C., Rosales, C. O., Zhang, Y., ... the LIFEPATH consortium (2019). Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging: A multi-cohort analysis. Aging, 11(7), 2045-2070. https://doi.org/10.18632/aging.101900
Fiorito, Giovanni ; McCrory, Cathal ; Robinson, Oliver ; Carmeli, Cristian ; Rosales, Carolina Ochoa ; Zhang, Yan ; Colicino, Elena ; Dugué, Pierre Antoine ; Artaud, Fanny ; McKay, Gareth J. ; Jeong, Ayoung ; Mishra, Pashupati P. ; Nøst, Therese H. ; Krogh, Vittorio ; Panico, Salvatore ; Sacerdote, Carlotta ; Tumino, Rosario ; Palli, Domenico ; Matullo, Giuseppe ; Guarrera, Simonetta ; Gandini, Martina ; Bochud, Murielle ; Dermitzakis, Emmanouil ; Muka, Taulant ; Schwartz, Joel ; Vokonas, Pantel S. ; Just, Allan ; Hodge, Allison M. ; Giles, Graham G. ; Southey, Melissa C. ; Hurme, Mikko A. ; Young, Ian ; McKnight, Amy Jayne ; Kunze, Sonja ; Waldenberger, Melanie ; Peters, Annette ; Schwettmann, Lars ; Lund, Eiliv ; Baccarelli, Andrea ; Milne, Roger L. ; Kenny, Rose A. ; Elbaz, Alexis ; Brenner, Hermann ; Kee, Frank ; Voortman, Trudy ; Probst-Hensch, Nicole ; Lehtimäki, Terho ; Elliot, Paul ; Stringhini, Silvia ; Vineis, Paolo ; Polidoro, Silvia ; the BIOS Consortium ; the LIFEPATH consortium. / Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging : A multi-cohort analysis. In: Aging. 2019 ; Vol. 11, No. 7. pp. 2045-2070.
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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",
author = "Giovanni Fiorito and Cathal McCrory and Oliver Robinson and Cristian Carmeli and Rosales, {Carolina Ochoa} and Yan Zhang and Elena Colicino and Dugu{\'e}, {Pierre Antoine} and Fanny Artaud and McKay, {Gareth J.} and Ayoung Jeong and Mishra, {Pashupati P.} and N{\o}st, {Therese H.} and Vittorio Krogh and Salvatore Panico and Carlotta Sacerdote and Rosario Tumino and Domenico Palli and Giuseppe Matullo and Simonetta Guarrera and Martina Gandini and Murielle Bochud and Emmanouil Dermitzakis and Taulant Muka and Joel Schwartz and Vokonas, {Pantel S.} and Allan Just and Hodge, {Allison M.} and Giles, {Graham G.} and Southey, {Melissa C.} and Hurme, {Mikko A.} and Ian Young and McKnight, {Amy Jayne} and Sonja Kunze and Melanie Waldenberger and Annette Peters and Lars Schwettmann and Eiliv Lund and Andrea Baccarelli and Milne, {Roger L.} and Kenny, {Rose A.} and Alexis Elbaz and Hermann Brenner and Frank Kee and Trudy Voortman and Nicole Probst-Hensch and Terho Lehtim{\"a}ki and Paul Elliot and Silvia Stringhini and Paolo Vineis and Silvia Polidoro and {the BIOS Consortium} and {the LIFEPATH consortium}",
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Fiorito, G, McCrory, C, Robinson, O, Carmeli, C, Rosales, CO, Zhang, Y, Colicino, E, Dugué, PA, Artaud, F, McKay, GJ, Jeong, A, Mishra, PP, Nøst, TH, Krogh, V, Panico, S, Sacerdote, C, Tumino, R, Palli, D, Matullo, G, Guarrera, S, Gandini, M, Bochud, M, Dermitzakis, E, Muka, T, Schwartz, J, Vokonas, PS, Just, A, Hodge, AM, Giles, GG, Southey, MC, Hurme, MA, Young, I, McKnight, AJ, Kunze, S, Waldenberger, M, Peters, A, Schwettmann, L, Lund, E, Baccarelli, A, Milne, RL, Kenny, RA, Elbaz, A, Brenner, H, Kee, F, Voortman, T, Probst-Hensch, N, Lehtimäki, T, Elliot, P, Stringhini, S, Vineis, P, Polidoro, S, the BIOS Consortium & the LIFEPATH consortium 2019, 'Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging: A multi-cohort analysis' Aging, vol. 11, no. 7, pp. 2045-2070. https://doi.org/10.18632/aging.101900

Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging : A multi-cohort analysis. / Fiorito, Giovanni; McCrory, Cathal; Robinson, Oliver; Carmeli, Cristian; Rosales, Carolina Ochoa; Zhang, Yan; Colicino, Elena; Dugué, Pierre Antoine; Artaud, Fanny; McKay, Gareth J.; Jeong, Ayoung; Mishra, Pashupati P.; Nøst, Therese H.; Krogh, Vittorio; Panico, Salvatore; Sacerdote, Carlotta; Tumino, Rosario; Palli, Domenico; Matullo, Giuseppe; Guarrera, Simonetta; Gandini, Martina; Bochud, Murielle; Dermitzakis, Emmanouil; Muka, Taulant; Schwartz, Joel; Vokonas, Pantel S.; Just, Allan; Hodge, Allison M.; Giles, Graham G.; Southey, Melissa C.; Hurme, Mikko A.; Young, Ian; McKnight, Amy Jayne; Kunze, Sonja; Waldenberger, Melanie; Peters, Annette; Schwettmann, Lars; Lund, Eiliv; Baccarelli, Andrea; Milne, Roger L.; Kenny, Rose A.; Elbaz, Alexis; Brenner, Hermann; Kee, Frank; Voortman, Trudy; Probst-Hensch, Nicole; Lehtimäki, Terho; Elliot, Paul; Stringhini, Silvia; Vineis, Paolo; Polidoro, Silvia; the BIOS Consortium; the LIFEPATH consortium.

In: Aging, Vol. 11, No. 7, 15.04.2019, p. 2045-2070.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging

T2 - A multi-cohort analysis

AU - Fiorito, Giovanni

AU - McCrory, Cathal

AU - Robinson, Oliver

AU - Carmeli, Cristian

AU - Rosales, Carolina Ochoa

AU - Zhang, Yan

AU - Colicino, Elena

AU - Dugué, Pierre Antoine

AU - Artaud, Fanny

AU - McKay, Gareth J.

AU - Jeong, Ayoung

AU - Mishra, Pashupati P.

AU - Nøst, Therese H.

AU - Krogh, Vittorio

AU - Panico, Salvatore

AU - Sacerdote, Carlotta

AU - Tumino, Rosario

AU - Palli, Domenico

AU - Matullo, Giuseppe

AU - Guarrera, Simonetta

AU - Gandini, Martina

AU - Bochud, Murielle

AU - Dermitzakis, Emmanouil

AU - Muka, Taulant

AU - Schwartz, Joel

AU - Vokonas, Pantel S.

AU - Just, Allan

AU - Hodge, Allison M.

AU - Giles, Graham G.

AU - Southey, Melissa C.

AU - Hurme, Mikko A.

AU - Young, Ian

AU - McKnight, Amy Jayne

AU - Kunze, Sonja

AU - Waldenberger, Melanie

AU - Peters, Annette

AU - Schwettmann, Lars

AU - Lund, Eiliv

AU - Baccarelli, Andrea

AU - Milne, Roger L.

AU - Kenny, Rose A.

AU - Elbaz, Alexis

AU - Brenner, Hermann

AU - Kee, Frank

AU - Voortman, Trudy

AU - Probst-Hensch, Nicole

AU - Lehtimäki, Terho

AU - Elliot, Paul

AU - Stringhini, Silvia

AU - Vineis, Paolo

AU - Polidoro, Silvia

AU - the BIOS Consortium

AU - the LIFEPATH consortium

PY - 2019/4/15

Y1 - 2019/4/15

N2 - 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.

AB - 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.

KW - Biological aging

KW - Education

KW - Epigenetic clocks

KW - Socioeconomic position

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U2 - 10.18632/aging.101900

DO - 10.18632/aging.101900

M3 - Article

VL - 11

SP - 2045

EP - 2070

JO - Aging

JF - Aging

SN - 1945-4589

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Fiorito G, McCrory C, Robinson O, Carmeli C, Rosales CO, Zhang Y et al. Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging: A multi-cohort analysis. Aging. 2019 Apr 15;11(7):2045-2070. https://doi.org/10.18632/aging.101900