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. GilesRiccardo 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

?Italian In?titutefor Genomic Medicine(IIGM,former HuGeF),Via Nizza 笃砀 –, 眃瘃眃?簁?T?Dureinp,a Irttamlye. nt of Medical Science? – Univer?ityof Turin, C.So, Dogliotti, 眃稀 - 眃瘃眃砃?簁Canc eItra Elyp. idemiology& Intelligence Divi?ion, Cancer Council of Victoria, 簃眃笀 St Kilda Road, Melbourne, Victoria, 礃瘃瘃稁 ?ACeuntrtarelia f.o r Epidemiology and Bio?tati?tic?, Melbourne School of Population and Global Health, The Univer?ity of Melbourne, Parkville Victoria, 礃瘃眃瘁 Aut?rDaelipaa. rtment of Epidemiologyand PublicHealth – Univer?ityCollege London, 省眃缀 Torrington Place, London, WC 眀E 簀BT, United Kingdom?In.t itu te of Evolutionary Biology and Environmental Studie?, Univer?ity of Zürich, Winterthurer?tra??e 眃缃瘁 Zürich, Switzer?lIanntdit.u te of Biology, Medicinal Chemitry , and Biotechnology, National Hellenic Re?earch Foundation,Leof. Va?ileo? Kon?tantinou ?縁?Athen?, ??? ??F?on,dGarzeieocnee. IRCCS – I?tituto Nazionale dei Tumori, Via Venezian ?, ? ? ? ? ?, Mi?lIatni ,tIuttaoly p. er lo Studio e la Prevenzione Oncologica (ISPO Tocana), Via Co?imo Il Vecchio, 码 笃瘃眃礃缁 Flore眃?nDceep, aItratmly.e nt of Clinical Medicine and Surgery, Univer?ity of Naple? Federico II, Cor?o Umberto I, 稃瘁 縃瘃眃礃縁 N眃?aPpileed, mItoanlyt .R eference Centre for Epidemiologyand Cancer Prevention(CPOPiemonte), Via Santena 紁 眃瘃眃砃簁 T眃?uCrainn,c Ietar lRy.e gitry and Hi?topathology Department, ‘Civic – M. P. Arezzo’ Ho?pital, ASP Ragu?a, Piazza Igea, 省 缃紃眃瘃瘁 Ra眃?gMuaR, CI-taly. PHE CentreforEnvironment andHealth,ImperialCollegeLondon,St. Mary’ Campu? Paddington,W??PG,London, United Kingdom. 眃?In?titute of Social and Preventive Medicine Lau?anne Univer?ity Ho?pital (CHUV), Rue du Bugnon 稃簁 眃瘃眃省 Lau?anne, Sw眃?iItnzeerrlamndU. 眃瘃眃縁 Center for Re?earch in Epidemiology and Population Health (CESP),Gu?taveRou??y In?titute,???rueEdouardVaillant,?????,Villejuif Ce?dCe?exn,Ftrreanfocre G. enomic and ExperimentalMedicine– Univer?ity ofEdinburgh,CreweRoad,EH ??XU,Edinburgh,UnitedKingdom?D?. epartment of Complex Trait Genetic?, Center for Neurogenomic? and Cognitive Re?earch (CNCR), Neuro?cience Campu? Am?terdam (NCA), VU Univer?ity Am?terdam, De Boelelaan, ? ? ? ?-? ? ? ? ? ? ? ? HV, Am?terdam, The Netherland?. ?T?rinity College Dublin, Dublin, Ireland, UK. ?De? partment of Clinical and Experimental Medicine, Univer?ity of Pi?a, Lungarno Antonio Pacinotti, 稃礁 笃簃眃砃簁 Pi?a, Italy. Giovanni Fiorito, Silvia Polidoro, Cathal McCrory, Roger L. Milne and Paolo Vinei? contributied equally to thi? work. Corre?pondence and reque?t? for material? ?hould be addre??ed to P.V. (email: p.vinei? 㬀imperial.ac.uk )

Funders	Funder number
7th European Community Framework Programme
Australian National Health and Medical Research Council	1026522, 1043616, 209057, 1074383, 1011618, 1026892, 1050198, 623206
European Commission H2020
IIGM
Italian Institute for Genomic Medicine
UK Medical Research Council	K013351
Compagnia di San Paolo
Seventh Framework Programme	633666, 226756
European Commission
Trinity College Dublin
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung	PZ00P3_147998
NordForsk

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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

@article{de51b4a40896413c8849b78f9b5fdfc0,

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",

year = "2017",

month = dec,

day = "1",

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

language = "English",

volume = "7",

journal = "Scientific Reports",

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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

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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.

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

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