Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation

Giovanni Fiorito; Silvia Polidoro; Pierre Antoine Dugué; Mika Kivimaki; Erica Ponzi; Giuseppe Matullo; Simonetta Guarrera; Manuela B. Assumma; Panagiotis Georgiadis; Soterios A. Kyrtopoulos; Vittorio Krogh; Domenico Palli; Salvatore Panico; Carlotta Sacerdote; Rosario Tumino; Marc Chadeau-Hyam; Silvia Stringhini; Gianluca Severi; Allison M. Hodge; Graham G. Giles; Riccardo Marioni; Richard Karlsson Linnér; Aisling M. O'Halloran; Rose A. Kenny; Richard Layte; Laura Baglietto; Oliver Robinson; Cathal McCrory; Roger L. Milne; Paolo Vineis

doi:10.1038/s41598-017-16391-5

Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation

Giovanni Fiorito
, Silvia Polidoro
, Pierre Antoine Dugué
, Mika Kivimaki
, Erica Ponzi
, Giuseppe Matullo
, Simonetta Guarrera
, Manuela B. Assumma
, Panagiotis Georgiadis
, Soterios A. Kyrtopoulos
, Vittorio Krogh
, Domenico Palli
, Salvatore Panico
, Carlotta Sacerdote
, Rosario Tumino
, Marc Chadeau-Hyam
, Silvia Stringhini
, Gianluca Severi
, Allison M. Hodge
, Graham G. Giles

Riccardo Marioni, Richard Karlsson Linnér, Aisling M. O'Halloran, Rose A. Kenny, Richard Layte, Laura Baglietto, Oliver Robinson, Cathal McCrory, Roger L. Milne, Paolo Vineis^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Low socioeconomic status (SES) is associated with earlier onset of age-related chronic conditions and reduced life-expectancy, but the underlying biomolecular mechanisms remain unclear. Evidence of DNA-methylation differences by SES suggests a possible association of SES with epigenetic age acceleration (AA). We investigated the association of SES with AA in more than 5,000 individuals belonging to three independent prospective cohorts from Italy, Australia, and Ireland. Low SES was associated with greater AA (β = 0.99 years; 95% CI 0.39,1.59; p = 0.002; comparing extreme categories). The results were consistent across different SES indicators. The associations were only partially modulated by the unhealthy lifestyle habits of individuals with lower SES. Individuals who experienced life-course SES improvement had intermediate AA compared to extreme SES categories, suggesting reversibility of the effect and supporting the relative importance of the early childhood social environment. Socioeconomic adversity is associated with accelerated epigenetic aging, implicating biomolecular mechanisms that may link SES to age-related diseases and longevity.

Original language	English
Article number	16266
Journal	Scientific Reports
Volume	7
Issue number	1
DOIs	https://doi.org/10.1038/s41598-017-16391-5
Publication status	Published - 1 Dec 2017

Funding

This research was supported by the ‘Lifepath’ grant to Paolo Vineis at Imperial College, London, Silvia Polidoro at the HuGeF Foundation, Silvia Stringhini at Lausanne’s University Hospital, Mika Kivimaki at University College London, Richard Layte and Cathal McCrory at the Trinity College Dublin, Dublin, Ireland (European Commission H2020 grant, Grant number: 633666). Giovanni Fiorito, Silvia Polidoro, Giuseppe Matullo and Simonetta Guarrera are supported by the Italian Institute for Genomic Medicine (IIGM), Torino, Italy with support from Compagnia di San Paolo. Silvia Stringhini is supported by the Swiss National Science Foundation (Ambizione Grant n° PZ00P3_147998). Laura Baglietto is supported by a Marie Curie International Incoming Fellowship within the 7th European Community Framework Programme. Panagiotis Georgiadis and Soterios A. Kyrtopoulos were supported by the European Union grant Envirogenomarkers (Grant number 226756). Mika Kivimaki is supported by the UK Medical Research Council (K013351) and NordForsk. The MCCS component of the work was funded by the Australian National Health and Medical Research Council, including project grant numbers 1011618, 1026892, 1026522, 1050198, 623206, and 1043616, and program grant numbers 209057 and 1074383.

Funders	Funder number
Italian Institute for Genomic Medicine
Compagnia di San Paolo
European Commission
Trinity College Dublin
NordForsk
Seventh Framework Programme	226756
Marie Curie International Incoming Fellowship
IIGM
Medical Research Council	MR/K013351/1, MR/M501669/1, K013351
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	147998, 167732, PZ00P3_147998
National Health and Medical Research Council	1026522, 209057, 1074383, 1011618, 1026892, 1050198, 623206
Horizon 2020 Framework Programme	633666
National Science Foundation	1043616

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Fiorito, G., Polidoro, S., Dugué, P. A., Kivimaki, M., Ponzi, E., Matullo, G., Guarrera, S., Assumma, M. B., Georgiadis, P., Kyrtopoulos, S. A., Krogh, V., Palli, D., Panico, S., Sacerdote, C., Tumino, R., Chadeau-Hyam, M., Stringhini, S., Severi, G., Hodge, A. M., ... Vineis, P. (2017). Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation. Scientific Reports, 7(1), Article 16266. https://doi.org/10.1038/s41598-017-16391-5

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title = "Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation",

abstract = "Low socioeconomic status (SES) is associated with earlier onset of age-related chronic conditions and reduced life-expectancy, but the underlying biomolecular mechanisms remain unclear. Evidence of DNA-methylation differences by SES suggests a possible association of SES with epigenetic age acceleration (AA). We investigated the association of SES with AA in more than 5,000 individuals belonging to three independent prospective cohorts from Italy, Australia, and Ireland. Low SES was associated with greater AA (β = 0.99 years; 95\% CI 0.39,1.59; p = 0.002; comparing extreme categories). The results were consistent across different SES indicators. The associations were only partially modulated by the unhealthy lifestyle habits of individuals with lower SES. Individuals who experienced life-course SES improvement had intermediate AA compared to extreme SES categories, suggesting reversibility of the effect and supporting the relative importance of the early childhood social environment. Socioeconomic adversity is associated with accelerated epigenetic aging, implicating biomolecular mechanisms that may link SES to age-related diseases and longevity.",

author = "Giovanni Fiorito and Silvia Polidoro and Dugu{\'e}, \{Pierre Antoine\} and Mika Kivimaki and Erica Ponzi and Giuseppe Matullo and Simonetta Guarrera and Assumma, \{Manuela B.\} and Panagiotis Georgiadis and Kyrtopoulos, \{Soterios A.\} and Vittorio Krogh and Domenico Palli and Salvatore Panico and Carlotta Sacerdote and Rosario Tumino and Marc Chadeau-Hyam and Silvia Stringhini and Gianluca Severi and Hodge, \{Allison M.\} and Giles, \{Graham G.\} and Riccardo Marioni and \{Karlsson Linn{\'e}r\}, Richard and O'Halloran, \{Aisling M.\} and Kenny, \{Rose A.\} and Richard Layte and Laura Baglietto and Oliver Robinson and Cathal McCrory and Milne, \{Roger L.\} and Paolo Vineis",

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doi = "10.1038/s41598-017-16391-5",

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Fiorito, G, Polidoro, S, Dugué, PA, Kivimaki, M, Ponzi, E, Matullo, G, Guarrera, S, Assumma, MB, Georgiadis, P, Kyrtopoulos, SA, Krogh, V, Palli, D, Panico, S, Sacerdote, C, Tumino, R, Chadeau-Hyam, M, Stringhini, S, Severi, G, Hodge, AM, Giles, GG, Marioni, R, Karlsson Linnér, R, O'Halloran, AM, Kenny, RA, Layte, R, Baglietto, L, Robinson, O, McCrory, C, Milne, RL & Vineis, P 2017, 'Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation', Scientific Reports, vol. 7, no. 1, 16266. https://doi.org/10.1038/s41598-017-16391-5

TY - JOUR

T1 - Social adversity and epigenetic aging

T2 - A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation

AU - Fiorito, Giovanni

AU - Polidoro, Silvia

AU - Dugué, Pierre Antoine

AU - Kivimaki, Mika

AU - Ponzi, Erica

AU - Matullo, Giuseppe

AU - Guarrera, Simonetta

AU - Assumma, Manuela B.

AU - Georgiadis, Panagiotis

AU - Kyrtopoulos, Soterios A.

AU - Krogh, Vittorio

AU - Palli, Domenico

AU - Panico, Salvatore

AU - Sacerdote, Carlotta

AU - Tumino, Rosario

AU - Chadeau-Hyam, Marc

AU - Stringhini, Silvia

AU - Severi, Gianluca

AU - Hodge, Allison M.

AU - Giles, Graham G.

AU - Marioni, Riccardo

AU - Karlsson Linnér, Richard

AU - O'Halloran, Aisling M.

AU - Kenny, Rose A.

AU - Layte, Richard

AU - Baglietto, Laura

AU - Robinson, Oliver

AU - McCrory, Cathal

AU - Milne, Roger L.

AU - Vineis, Paolo

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Low socioeconomic status (SES) is associated with earlier onset of age-related chronic conditions and reduced life-expectancy, but the underlying biomolecular mechanisms remain unclear. Evidence of DNA-methylation differences by SES suggests a possible association of SES with epigenetic age acceleration (AA). We investigated the association of SES with AA in more than 5,000 individuals belonging to three independent prospective cohorts from Italy, Australia, and Ireland. Low SES was associated with greater AA (β = 0.99 years; 95% CI 0.39,1.59; p = 0.002; comparing extreme categories). The results were consistent across different SES indicators. The associations were only partially modulated by the unhealthy lifestyle habits of individuals with lower SES. Individuals who experienced life-course SES improvement had intermediate AA compared to extreme SES categories, suggesting reversibility of the effect and supporting the relative importance of the early childhood social environment. Socioeconomic adversity is associated with accelerated epigenetic aging, implicating biomolecular mechanisms that may link SES to age-related diseases and longevity.

AB - Low socioeconomic status (SES) is associated with earlier onset of age-related chronic conditions and reduced life-expectancy, but the underlying biomolecular mechanisms remain unclear. Evidence of DNA-methylation differences by SES suggests a possible association of SES with epigenetic age acceleration (AA). We investigated the association of SES with AA in more than 5,000 individuals belonging to three independent prospective cohorts from Italy, Australia, and Ireland. Low SES was associated with greater AA (β = 0.99 years; 95% CI 0.39,1.59; p = 0.002; comparing extreme categories). The results were consistent across different SES indicators. The associations were only partially modulated by the unhealthy lifestyle habits of individuals with lower SES. Individuals who experienced life-course SES improvement had intermediate AA compared to extreme SES categories, suggesting reversibility of the effect and supporting the relative importance of the early childhood social environment. Socioeconomic adversity is associated with accelerated epigenetic aging, implicating biomolecular mechanisms that may link SES to age-related diseases and longevity.

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DO - 10.1038/s41598-017-16391-5

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VL - 7

JO - Scientific Reports

JF - Scientific Reports

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ER -

Social adversity and epigenetic aging: A multi-cohort study on socioeconomic differences in peripheral blood DNA methylation

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Funding

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