Epigenetic Signatures of Socioeconomic Status Across the Lifecourse

  • Silvia Stringhini
  • Paolo Vineis


In the last years, research has expanded with the aim of identifying the biological mechanisms through which socioeconomic factors are embedded. Indeed, if differences in the social environment are causally related to health, then they must express themselves in terms of variations in biological factors that are linked to health. The identification of these factors might be important for clarifying the complex mechanisms involved in the social distribution of diseases and for better targeting public health interventions. Epigenetics, and more specifically DNA methylation, is potentially one of the most important biological pathways through which socioeconomic factors are embedded. Here we propose a conceptual framework for the role of epigenetic modifications in the biological integration of socioeconomic factors and provide some examples from empirical studies.



This work was supported by a grant from the European Commission (Horizon 2020 grant no. 633666-LIFEPATH). Silvia Stringhini is supported by an Ambizione Grant (no. PZ00P3_147998) from the Swiss National Science Foundation (SNSF).


  1. Abel, Thomas. 2008. Cultural Capital and Social Inequality in Health. Journal of Epidemiology and Community Health 62 (7): e13.CrossRefGoogle Scholar
  2. Bartley, Mel, and Ian Plewis. 1997. Does Health-Selective Mobility Account for Socioeconomic Differences in Health? Evidence from England and Wales, 1971 to 1991. Journal of Health and Social Behavior 38 (4): 376–386.CrossRefGoogle Scholar
  3. Basham, J. Kaitlin, Vasudev R. Bhonde, Collin Kieffer, James B. Mack, Matthew Hess, Bryan E. Welm, and Ryan E. Looper. 2014. Bis-Aryloxadiazoles as Effective Activators of the Aryl Hydrocarbon Receptor. Bioorganic & Medicinal Chemistry Letters 24 (11): 2473–2476.CrossRefGoogle Scholar
  4. Borghol, Nada, Matthew Suderman, Wendy McArdle, Ariane Racine, Michael Hallett, Marcus Pembrey, Clyde Hertzman, Chris Power, and Moshe Szyf. 2012. Associations with Early-Life Socio-Economic Position in Adult DNA Methylation. International Journal of Epidemiology 41 (1): 62–74.CrossRefGoogle Scholar
  5. Bronnum-Hansen, Henrik, and Mikkel Baadsgaard. 2008. Increase in Social Inequality in Health Expectancy in Denmark. Scandinavian Journal of Public Health 36 (1): 44–51.CrossRefGoogle Scholar
  6. Carroll, E. Judith, Sheldon Cohen, and Anna L. Marsland. 2011. Early Childhood Socioeconomic Status is Associated with Circulating Interleukin-6 among Mid-Life Adults. Brain, Behavior, and Immunity 25 (7): 1468–1474.CrossRefGoogle Scholar
  7. Charafeddine, Rana, Herman Van Oyen, and Stefaan Demarest. 2009. Trends in Social Inequalities in Obesity: Belgium, 1997 to 2004. Preventive Medicine 48 (1): 54–58.CrossRefGoogle Scholar
  8. Chen, Edith, Sheldon Cohen, and Gregory E. Miller. 2010. How Low Socioeconomic Status Affects 2-Year Hormonal Trajectories in Children. Psychological Science: A Journal of the American Psychological Society / APS 21 (1): 31–37.CrossRefGoogle Scholar
  9. Chetty, Raj, Michael Stepner, Sarah Abraham, Shelby Lin, Benjamin Scuderi, Nicholas Turner, Augustin Bergeron, and David Cutler. 2016. The Association between Income and Life Expectancy in the United States, 2001–2014. Journal of the American Medical Association 315 (16): 1750–1766.CrossRefGoogle Scholar
  10. Cohen, Sheldon, William J. Doyle, and Andrew Baum. 2006a. Socioeconomic Status is Associated with Stress Hormones. Psychosomatic Medicine 68 (3): 414–420.CrossRefGoogle Scholar
  11. Cohen, Sheldon, Joseph E. Schwartz, Elissa Epel, Clemens Kirschbaum, Steve Sidney, and Teresa Seeman. 2006b. Socioeconomic Status, Race, and Diurnal Cortisol Decline in the Coronary Artery Risk Development in Young Adults (Cardia) Study. Psychosomatic Medicine 68 (1): 41–50.CrossRefGoogle Scholar
  12. Crimmins, Eileen, and Teresa Seeman. 2004. Integrating Biology into the Study of Health Disparities. Population and Development Review 30: 89–107.Google Scholar
  13. Dowd, Jennifer Beam, Anna Zajacova, and Allison Aiello. 2009. Early Origins of Health Disparities: Burden of Infection, Health, and Socioeconomic Status in U.S. Children. Social Science and Medicine 68 (4): 699–707.CrossRefGoogle Scholar
  14. Elovainio, Marko, Jane E. Ferrie, Archana Singh-Manoux, Martin Shipley, G. David Batty, Jenny Head, Mark Hamer, et al. 2011. Socioeconomic Differences in Cardiometabolic Factors: Social Causation or Health-Related Selection? Evidence from the Whitehall Ii Cohort Study, 1991–2004. American Journal of Epidemiology 174 (7): 779–789.CrossRefGoogle Scholar
  15. Espelt, Albert, Anton E. Kunst, Laia Palencia, Roberto Gnavi, and Carme Borrell. 2011. Twenty Years of Socio-Economic Inequalities in Type 2 Diabetes Mellitus Prevalence in Spain, 1987-2006. European Journal of Public Health 22: 765–771.CrossRefGoogle Scholar
  16. Fasanelli, Francesca, Laura Baglietto, Erica Ponzi, Florence Guida, Gianluca Campanella, Mattias Johansson, Kjell Grankvist, et al. 2015. Hypomethylation of Smoking-Related Genes is Associated with Future Lung Cancer in Four Prospective Cohorts. Nature Communications 6: 10192.CrossRefGoogle Scholar
  17. Fox, A. John, Peter O. Goldblatt, and David R. Jones. 1985. Social Class Mortality Differentials: Artefact, Selection or Life Circumstances? Journal of Epidemiology and Community Health 39 (1): 1–8.CrossRefGoogle Scholar
  18. Gianaros, Peter J., Jeffrey A. Horenstein, Sheldon Cohen, Karen A. Matthews, Sarah M. Brown, Janine D. Flory, Hugo D. Critchley, Stephen B. Manuck, and Ahmad R. Hariri. 2007. Perigenual Anterior Cingulate Morphology Covaries with Perceived Social Standing. Social Cognitive and Affective Neuroscience 2 (3): 161–173.CrossRefGoogle Scholar
  19. Gianaros, Peter J., Jeffrey A. Horenstein, Ahmad R. Hariri, Lei K. Sheu, Stephen B. Manuck, Karen A. Matthews, and Sheldon Cohen. 2008. Potential Neural Embedding of Parental Social Standing. Social Cognitive and Affective Neuroscience 3 (2): 91–96.CrossRefGoogle Scholar
  20. Gianaros, Peter J., and Stephen B. Manuck. 2010. Neurobiological Pathways Linking Socioeconomic Position and Health. Psychosomatic Medicine 72 (5): 450–461.CrossRefGoogle Scholar
  21. Giuliani, Cristina, Maria Giulia Bacalini, Marco Sazzini, Chiara Pirazzini, Claudio Franceschi, Paolo Garagnani, and Donata Luiselli. 2015. The Epigenetic Side of Human Adaptation: Hypotheses, Evidences and Theories. Annals of Human Biology 42 (1): 1–9.CrossRefGoogle Scholar
  22. Guida, Florence, Torkjel M. Sandanger, Raphaele Castagne, Gianluca Campanella, Silvia Polidoro, Domenico Palli, Vittorio Krogh, et al. 2015. Dynamics of Smoking-Induced Genome-Wide Methylation Changes with Time since Smoking Cessation. Human Molecular Genetics 24 (8): 2349–2359.CrossRefGoogle Scholar
  23. Hahn, E. Mark, Lenka L. Allan, and David H. Sherr. 2009. Regulation of Constitutive and Inducible Ahr Signaling: Complex Interactions Involving the Ahr Repressor. Biochemical Pharmacology 77 (4): 485–497.CrossRefGoogle Scholar
  24. Heard, Edith, and Robert A. Martienssen. 2014. Transgenerational Epigenetic Inheritance: Myths and Mechanisms. Cell 157 (1): 95–109.CrossRefGoogle Scholar
  25. Hertzman, Clyde, and Tom Boyce. 2010. How Experience Gets under the Skin to Create Gradients in Developmental Health. Annual Review of Public Health 31: 329–347. 3p following 47.CrossRefGoogle Scholar
  26. Horvath, Steve. 2013. DNA Methylation Age of Human Tissues and Cell Types. Genome Biology 14 (10): R115.CrossRefGoogle Scholar
  27. Imkampe, Anne K., and Martin C. Gulliford. 2011. Increasing Socio-Economic Inequality in Type 2 Diabetes Prevalence—Repeated Cross-Sectional Surveys in England 1994–2006. European Journal of Public Health 21 (4): 484–490.CrossRefGoogle Scholar
  28. James, William Philip T., Michael Nelson, Ann Ralph, and Simon Leather. 1997. Socioeconomic Determinants of Health: The Contribution of Nutrition to Inequalities in Health. British Medical Journal 314 (7093): 1545–1549.CrossRefGoogle Scholar
  29. Jemal, Ahmedin, Elizabeth Ward, Robert N. Anderson, Taylor Murray, and Michael J. Thun. 2008. Widening of Socioeconomic Inequalities in U.S. Death Rates, 1993-2001. PloS One 3 (5): e2181.CrossRefGoogle Scholar
  30. Kanjilal, Sanjat, Edward W. Gregg, Yiling J. Cheng, Ping Zhang, David E. Nelson, George Mensah, and Gloria L. Beckles. 2006. Socioeconomic Status and Trends in Disparities in 4 Major Risk Factors for Cardiovascular Disease among us Adults, 1971–2002. Archives of Internal Medicine 166 (21): 2348–2355.CrossRefGoogle Scholar
  31. Kelly-Irving, Michelle, Cyrille Delpierre, Anne-Cecile Schieber, Benoit Lepage, Christine Rolland, Anissa Afrite, Jean Pascal, Chantal Cases, Pierre Lombrail, and Thierry Lang. 2011. Do General Practitioners Overestimate the Health of Their Patients with Lower Education? Social Science and Medicine 73 (9): 1416–1421.CrossRefGoogle Scholar
  32. Kickbusch, Ilona S. 2001. Health Literacy: Addressing the Health and Education Divide. Health Promotion International 16 (3): 289–297.CrossRefGoogle Scholar
  33. Krieger, Nancy. 2005. Embodiment: A Conceptual Glossary for Epidemiology. Journal of Epidemiology and Community Health 59 (5): 350–355.CrossRefGoogle Scholar
  34. Ladd-Acosta, Christine, and M. Daniele Fallin. 2016. The Role of Epigenetics in Genetic and Environmental Epidemiology. Epigenomics 8 (2): 271–283.CrossRefGoogle Scholar
  35. Lantz, Paula M., James S. House, James M. Lepkowski, David R. Williams, Richard P. Mero, and Jieming Chen. 1998. Socioeconomic Factors, Health Behaviors, and Mortality: Results from a Nationally Representative Prospective Study of Us Adults. Journal of the American Medical Association 279 (21): 1703–1708.CrossRefGoogle Scholar
  36. Lantz, Paula M., James S. House, Richard P. Mero, and David R. Williams. 2005. Stress, Life Events, and Socioeconomic Disparities in Health: Results from the Americans’ Changing Lives Study. Journal of Health and Social Behavior 46 (3): 274–288.CrossRefGoogle Scholar
  37. Loucks, Eric B., Louise Pilote, John W. Lynch, Hugues Richard, Nisha D. Almeida, Emelia J. Benjamin, and Joanne M. Murabito. 2010. Life Course Socioeconomic Position is Associated with Inflammatory Markers: The Framingham Offspring Study. Social Science and Medicine 71 (1): 187–195.CrossRefGoogle Scholar
  38. Lynch, John W., George A. Kaplan, and Johana T. Salonen. 1997a. Why Do Poor People Behave Poorly? Variation in Adult Health Behaviours and Psychosocial Characteristics by Stages of the Socioeconomic Lifecourse. Social Science and Medicine 44 (6): 809–819.CrossRefGoogle Scholar
  39. Lynch, John W., George A. Kaplan, and Sarah J. Shema. 1997b. Cumulative Impact of Sustained Economic Hardship on Physical, Cognitive, Psychological, and Social Functioning. New England Journal of Medicine 337 (26): 1889–1895.CrossRefGoogle Scholar
  40. Lynch, John W., George Davey Smith, George A. Kaplan, and James S. House. 2000. Income Inequality and Mortality: Importance to Health of Individual Income, Psychosocial Environment, or Material Conditions. British Medical Journal 320 (7243): 1200–1204.CrossRefGoogle Scholar
  41. Mackenbach, Johan P., Ivana Kulhanova, Barbara Artnik, Matthias Bopp, Carme Borrell, Tom Clemens, Giuseppe Costa, et al. 2016. Changes in Mortality Inequalities over Two Decades: Register Based Study of European Countries. British Medical Journal 353: i1732.CrossRefGoogle Scholar
  42. Mackenbach, Johan P., Irina Stirbu, Albert-Jan Roskam, Maartje M. Schaap, Gwenn Menvielle, Mall Leinsalu, Anton Kunst, and Health the European Union Working Group on Socioeconomic Inequalities. 2008. Socioeconomic Inequalities in Health in 22 European Countries. New England Journal of Medicine 358 (23): 2468–2481.CrossRefGoogle Scholar
  43. Marmot, Michael G., Martin J. Shipley, and Geoffrey Rose. 1984. Inequalities in Death—Specific Explanations of a General Pattern? Lancet 1 (8384): 1003–1006.CrossRefGoogle Scholar
  44. Mathers, Colin D., and Dejan Loncar. 2006. Projections of Global Mortality and Burden of Disease from 2002 to 2030. PLoS Medicine 3 (11): e442.CrossRefGoogle Scholar
  45. Mayhew, Les, and David Smith. 2016. An Investigation into Inequalities in Adult Lifespan. London: Cass Business School, City University London, International Longevity Centre.Google Scholar
  46. McGuinness, Dagmara, Liane M. McGlynn, Paul C. Johnson, Alan MacIntyre, G. David Batty, Harry Burns, Jonathan Cavanagh, et al. 2012. Socio-Economic Status is Associated with Epigenetic Differences in the Psobid Cohort. International Journal of Epidemiology 41 (1): 151–160.CrossRefGoogle Scholar
  47. Miller, Gregory E., Edith Chen, Alexandra K. Fok, Hope Walker, Alvin Lim, Erin F. Nicholls, Steve Cole, and Michael S. Kobor. 2009. Low Early-Life Social Class Leaves a Biological Residue Manifested by Decreased Glucocorticoid and Increased Proinflammatory Signaling. Proceedings of the National Academy of Sciences of the United States of America 106 (34): 14716–14721.CrossRefGoogle Scholar
  48. Miller, Gregory E., Edith Chen, and Karen J. Parker. 2011. Psychological Stress in Childhood and Susceptibility to the Chronic Diseases of Aging: Moving toward a Model of Behavioral and Biological Mechanisms. Psychological Bulletin 137 (6): 959–997.CrossRefGoogle Scholar
  49. Mitchell, Richard, David Blane, and Mel Bartley. 2002. Elevated Risk of High Blood Pressure: Climate and the Inverse Housing Law. International Journal of Epidemiology 31 (4): 831–838.CrossRefGoogle Scholar
  50. Papoutsis, Andreas J., Ornella I. Selmin, Jamie L. Borg, and Donato F. Romagnolo. 2015. Gestational Exposure to the Ahr Agonist 2,3,7,8-Tetrachlorodibenzo-P-Dioxin Induces Brca-1 Promoter Hypermethylation and Reduces Brca-1 Expression in Mammary Tissue of Rat Offspring: Preventive Effects of Resveratrol. Molecular Carcinogenesis 54 (4): 261–269.CrossRefGoogle Scholar
  51. Pogribny, Igor P., and Frederick A. Beland. 2009. DNA Hypomethylation in the Origin and Pathogenesis of Human Diseases. Cellular and Molecular Life Sciences 66 (14): 2249–2261.CrossRefGoogle Scholar
  52. Power, Chris, Sharon Matthews, and Orly Manor. 1996. Inequalities in Self Rated Health in the 1958 Birth Cohort: Lifetime Social Circumstances or Social Mobility? British Medical Journal 313 (7055): 449–453.CrossRefGoogle Scholar
  53. Rang, Franka J., and Johannes Boonstra. 2014. Causes and Consequences of Age-Related Changes in DNA Methylation: A Role for Ros? Biology (Basel) 3 (2): 403–425.Google Scholar
  54. Ranjit, Nalini, Ana V. Diez-Roux, Steven Shea, Mary Cushman, Hanyu Ni, and Teresa Seeman. 2007. Socioeconomic Position, Race/Ethnicity, and Inflammation in the Multi-Ethnic Study of Atherosclerosis. Circulation 116 (21): 2383–2390.CrossRefGoogle Scholar
  55. Richmond, Rebecca C., Nicholas J. Timpson, and Thorkild I. Sorensen. 2015. Exploring Possible Epigenetic Mediation of Early-Life Environmental Exposures on Adiposity and Obesity Development. International Journal of Epidemiology 44 (4): 1191–1198.CrossRefGoogle Scholar
  56. Rutter, Michael. 2012. Achievements and Challenges in the Biology of Environmental Effects. Proceedings of the national Academy of Sciences USA 109 (Supplement 2): 17149–17153.CrossRefGoogle Scholar
  57. Shenker, Natalie S., Silvia Polidoro, Karin van Veldhoven, Carlotta Sacerdote, Fulvio Ricceri, Mark A. Birrell, Maria G. Belvisi, Robert Brown, Paolo Vineis, and James M. Flanagan. 2013a. Epigenome-Wide Association Study in the European Prospective Investigation into Cancer and Nutrition (Epic-Turin) Identifies Novel Genetic Loci Associated with Smoking. Human Molecular Genetics 22 (5): 843–851.CrossRefGoogle Scholar
  58. Shenker, Natalie S., Per Magne Ueland., Silvia Polidoro, Karin van Veldhoven, Fulvio Ricceri, Robert Brown, James M. Flanagan, and Paolo Vineis. DNA Methylation as a Long-Term Biomarker of Exposure to Tobacco Smoke Epidemiology 24, no. 5 (2013b): 712-716.CrossRefGoogle Scholar
  59. Siegrist, Johannes, and Michael Marmot. 2004. Health Inequalities and the Psychosocial Environment-Two Scientific Challenges. Social Science and Medicine 58 (8): 1463–1473.CrossRefGoogle Scholar
  60. Steptoe, Andrew, Alireza Shamaei-Tousi, Asa Gylfe, Brian Henderson, Sven Bergstrom, and Michael Marmot. 2007. Socioeconomic Status, Pathogen Burden and Cardiovascular Disease Risk. Heart 93 (12): 1567–1570.CrossRefGoogle Scholar
  61. Stringhini, Silvia, Aline Dugravot, Martin Shipley, Marcel Goldberg, Marie Zins, Mika Kivimaki, Michael Marmot, Severine Sabia, and Archana Singh-Manoux. 2011. Health Behaviours, Socioeconomic Status, and Mortality: Further Analyses of the British Whitehall Ii and the French Gazel Prospective Cohorts. PLoS Medicine 8 (2): e1000419.CrossRefGoogle Scholar
  62. Stringhini, Silvia, Silvia Polidoro, Carlotta Sacerdote, Rachel Kelly, Karin van Veldhoven, Claudia Agnoli, Sara Grioni, et al. 2015. Lifecourse Socioeconomic Status and DNA Methylation of Genes Regulating Inflammation. International Journal of Epidemiology 44 (4): 1320–1330.CrossRefGoogle Scholar
  63. Stringhini, Silvia, Adam G. Tabak, Tasnime N. Akbaraly, Severine Sabia, Martin J. Shipley, Michael G. Marmot, Eric J. Brunner, G. David Batty, Pascal Bovet, and Mika Kivimaki. 2012. Contribution of Modifiable Risk Factors to Social Inequalities in Type 2 Diabetes: Prospective Whitehall Ii Cohort Study. British Medical Journal 345: e5452.CrossRefGoogle Scholar
  64. Townsend, Peter, and Nicholas Davidson. 1982. Inequalities in Health: The Black Report. Harmondsworth: Penguin Books. Reprint, NOT IN FILE.Google Scholar
  65. Tung, Jenny, Luis B. Barreiro, Zachary P. Johnson, Kasper D. Hansen, Vasiliki Michopoulos, Donna Toufexis, Katelyn Michelini, Mark E. Wilson, and Yoav Gilad. 2012. Social Environment is Associated with Gene Regulatory Variation in the Rhesus Macaque Immune System. Proceedings of the National Academy of Sciences of the United States of America 109 (17): 6490–6495.CrossRefGoogle Scholar
  66. Valinluck, Victoria, Hsin-Hsao Tsai, Daniel K. Rogstad, Artur Burdzy, Adrian Bird, and Lawrence C. Sowers. 2004. Oxidative Damage to Methyl-Cpg Sequences Inhibits the Binding of the Methyl-Cpg Binding Domain (Mbd) of Methyl-Cpg Binding Protein 2 (Mecp2). Nucleic Acids Research 32 (14): 4100–4108.CrossRefGoogle Scholar
  67. van der Pol, Marjon. 2011. Health, Education and Time Preference. Health Economics 20 (8): 917–929.CrossRefGoogle Scholar
  68. van Doorslaer, Eddy, Cristina Masseria, Xander Koolman, and OECD Health Equity Research Group. 2006. Inequalities in Access to Medical Care by Income in Developed Countries. Canadian Medical Association Journal 174 (2): 177–183.CrossRefGoogle Scholar
  69. Vineis, Paolo, Karin van Veldhoven, Marc Chadeau-Hyam, and Toby J. Athersuch. 2013. Advancing the Application of Omics-Based Biomarkers in Environmental Epidemiology. Environmental and Molecular Mutagenesis 54 (7): 461–467.CrossRefGoogle Scholar
  70. Vineis, Paolo, Aristotelis Chatziioannou, Vincent T. Cunliffe, James M. Flanagan, Mark Hanson, Micheline Kirsch-Volders, and Soterios Kyrtopoulos. 2017. Epigenetic Memory in Response to Environmental Stressors. The FASEB Journal 31 (6): 2241–2251.CrossRefGoogle Scholar
  71. World Health Organisation. 2011. Rio Political Declaration on Social Determinants of Health, WHO (ed.). Rio de Janeiro, Brazil.Google Scholar

Copyright information

© The Author(s) 2018

Authors and Affiliations

  • Silvia Stringhini
    • 1
  • Paolo Vineis
    • 2
  1. 1.Institute of Social and Preventive Medicine (IUMSP), Lausanne University HospitalLausanneSwitzerland
  2. 2.School of Public Health, Imperial College LondonLondonUK

Personalised recommendations