Skip to main content
Top
Published in: European Journal of Epidemiology 5/2018

Open Access 01-05-2018 | MORTALITY

Allostatic load and subsequent all-cause mortality: which biological markers drive the relationship? Findings from a UK birth cohort

Authors: Raphaële Castagné, Valérie Garès, Maryam Karimi, Marc Chadeau-Hyam, Paolo Vineis, Cyrille Delpierre, Michelle Kelly-Irving, for the Lifepath Consortium

Published in: European Journal of Epidemiology | Issue 5/2018

Login to get access

Abstract

The concept of allostatic load (AL) refers to the idea of a global physiological ‘wear and tear’ resulting from the adaptation to the environment through the stress response systems over the life span. The link between socioeconomic position (SEP) and mortality has now been established, and there is evidence that AL may capture the link between SEP and mortality. In order to quantitatively assess the role of AL on mortality, we use data from the 1958 British birth cohort including eleven year mortality in 8,113 adults. Specifically, we interrogate the hypothesis of a cumulative biological risk (allostatic load) reflecting 4 physiological systems potentially predicting future risk of death (N = 132). AL was defined using 14 biomarkers assayed in blood from a biosample collected at 44 years of age. Cox proportional hazard regression analysis revealed that higher allostatic load at 44 years old was a significant predictor of mortality 11 years later [HR = 3.56 (2.3 to 5.53)]. We found that this relationship was not solely related to early-life SEP, adverse childhood experiences and young adulthood health status, behaviours and SEP [HR = 2.57 (1.59 to 4.15)]. Regarding the ability of each physiological system and biomarkers to predict future death, our results suggest that the cumulative measure was advantageous compared to evaluating each physiological system sub-score and biomarker separately. Our findings add some evidence of a biological embodiment in response to stress which ultimately affects mortality.
Appendix
Available only for authorised users
Literature
2.
go back to reference Marmot M, Friel S, Bell R, Houweling TA, Taylor S. Closing the gap in a generation: health equity through action on the social determinants of health. Lancet. 2008;372:1661–9.CrossRefPubMed Marmot M, Friel S, Bell R, Houweling TA, Taylor S. Closing the gap in a generation: health equity through action on the social determinants of health. Lancet. 2008;372:1661–9.CrossRefPubMed
3.
go back to reference Mackenbach JP, Stirbu I, Roskam A-JR, Schaap MM, Menvielle G, Leinsalu M, et al. Socioeconomic Inequalities in health in 22 European Countries. N Engl J Med. 2008;358:2468–81.CrossRefPubMed Mackenbach JP, Stirbu I, Roskam A-JR, Schaap MM, Menvielle G, Leinsalu M, et al. Socioeconomic Inequalities in health in 22 European Countries. N Engl J Med. 2008;358:2468–81.CrossRefPubMed
4.
go back to reference Kuh D, Hardy R, Langenberg C, Richards M, Wadsworth MEJ. Mortality in adults aged 26–54 years related to socioeconomic conditions in childhood and adulthood: post war birth cohort study. BMJ. 2002;325:1076–80.CrossRefPubMedPubMedCentral Kuh D, Hardy R, Langenberg C, Richards M, Wadsworth MEJ. Mortality in adults aged 26–54 years related to socioeconomic conditions in childhood and adulthood: post war birth cohort study. BMJ. 2002;325:1076–80.CrossRefPubMedPubMedCentral
5.
go back to reference Blakely T, Atkinson J, Kiro C, Blaiklock A, D’Souza A. Child mortality, socioeconomic position, and one-parent families: independent associations and variation by age and cause of death. Int J Epidemiol. 2003;32:410–8.CrossRefPubMed Blakely T, Atkinson J, Kiro C, Blaiklock A, D’Souza A. Child mortality, socioeconomic position, and one-parent families: independent associations and variation by age and cause of death. Int J Epidemiol. 2003;32:410–8.CrossRefPubMed
6.
go back to reference Stringhini S, Carmeli C, Jokela M, Avendaño M, Muennig P, Guida F, et al. Socioeconomic status and the 25  ×  25 risk factors as determinants of premature mortality: a multicohort study and meta-analysis of 1·7 million men and women. Lancet Lond Engl. 2017;389:1229–37.CrossRef Stringhini S, Carmeli C, Jokela M, Avendaño M, Muennig P, Guida F, et al. Socioeconomic status and the 25  ×  25 risk factors as determinants of premature mortality: a multicohort study and meta-analysis of 1·7 million men and women. Lancet Lond Engl. 2017;389:1229–37.CrossRef
7.
go back to reference Stringhini S, Dugravot A, Shipley M, Goldberg M, Zins M, Kivimäki M, et al. Health behaviours, socioeconomic status, and mortality: further analyses of the British Whitehall II and the French Gazel prospective cohorts. PLoS Med. 2011;8:e1000419.CrossRefPubMedPubMedCentral Stringhini S, Dugravot A, Shipley M, Goldberg M, Zins M, Kivimäki M, et al. Health behaviours, socioeconomic status, and mortality: further analyses of the British Whitehall II and the French Gazel prospective cohorts. PLoS Med. 2011;8:e1000419.CrossRefPubMedPubMedCentral
8.
go back to reference Gallo V, Mackenbach JP, Ezzati M, Menvielle G, Kunst AE, Rohrmann S, et al. Social inequalities and mortality in Europe—results from a large multi-national cohort. PLoS ONE. 2012;7:e39013.CrossRefPubMedPubMedCentral Gallo V, Mackenbach JP, Ezzati M, Menvielle G, Kunst AE, Rohrmann S, et al. Social inequalities and mortality in Europe—results from a large multi-national cohort. PLoS ONE. 2012;7:e39013.CrossRefPubMedPubMedCentral
9.
go back to reference McEwen BS, Stellar E. Stress and the individual. Mechanisms leading to disease. Arch Intern Med. 1993;153:2093–101.CrossRefPubMed McEwen BS, Stellar E. Stress and the individual. Mechanisms leading to disease. Arch Intern Med. 1993;153:2093–101.CrossRefPubMed
10.
11.
go back to reference Seeman TE, Singer BH, Rowe JW, Horwitz RI, McEwen BS. Price of adaptation–allostatic load and its health consequences. MacArthur studies of successful aging. Arch Intern Med. 1997;157:2259–68.CrossRefPubMed Seeman TE, Singer BH, Rowe JW, Horwitz RI, McEwen BS. Price of adaptation–allostatic load and its health consequences. MacArthur studies of successful aging. Arch Intern Med. 1997;157:2259–68.CrossRefPubMed
12.
go back to reference McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm Behav. 2003;43:2–15.CrossRefPubMed McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm Behav. 2003;43:2–15.CrossRefPubMed
13.
go back to reference Juster R-P, McEwen BS, Lupien SJ. Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev. 2010;35:2–16.CrossRefPubMed Juster R-P, McEwen BS, Lupien SJ. Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev. 2010;35:2–16.CrossRefPubMed
14.
go back to reference Peters A, McEwen BS. Stress habituation, body shape and cardiovascular mortality. Neurosci Biobehav Rev. 2015;56:139–50.CrossRefPubMed Peters A, McEwen BS. Stress habituation, body shape and cardiovascular mortality. Neurosci Biobehav Rev. 2015;56:139–50.CrossRefPubMed
15.
go back to reference Delpierre C, Barboza-Solis C, Torrisani J, Darnaudery M, Bartley M, Blane D, et al. Origins of health inequalities: the case for Allostatic Load. Longitud Life Course Stud. 2016;7:79–103.CrossRef Delpierre C, Barboza-Solis C, Torrisani J, Darnaudery M, Bartley M, Blane D, et al. Origins of health inequalities: the case for Allostatic Load. Longitud Life Course Stud. 2016;7:79–103.CrossRef
16.
go back to reference Beckie TM. A systematic review of allostatic load, health, and health disparities. Biol Res Nurs. 2012;14:311–46.CrossRefPubMed Beckie TM. A systematic review of allostatic load, health, and health disparities. Biol Res Nurs. 2012;14:311–46.CrossRefPubMed
18.
go back to reference Blane D, Kelly-Irving M, D’Errico A, Bartley M, Montgomery S. Social-biological transitions: how does the social become biological? Longitud Life Course Stud. 2013;4:136–46. Blane D, Kelly-Irving M, D’Errico A, Bartley M, Montgomery S. Social-biological transitions: how does the social become biological? Longitud Life Course Stud. 2013;4:136–46.
19.
go back to reference Adler NE, Newman K. Socioeconomic disparities in health: pathways and policies. Health Aff Proj Hope. 2002;21:60–76.CrossRef Adler NE, Newman K. Socioeconomic disparities in health: pathways and policies. Health Aff Proj Hope. 2002;21:60–76.CrossRef
20.
go back to reference Gustafsson PE, Janlert U, Theorell T, Westerlund H, Hammarström A. Socioeconomic status over the life course and allostatic load in adulthood: results from the Northern Swedish Cohort. J Epidemiol Community Health. 2011;65:986–92.CrossRefPubMed Gustafsson PE, Janlert U, Theorell T, Westerlund H, Hammarström A. Socioeconomic status over the life course and allostatic load in adulthood: results from the Northern Swedish Cohort. J Epidemiol Community Health. 2011;65:986–92.CrossRefPubMed
21.
go back to reference Gustafsson PE, Janlert U, Theorell T, Westerlund H, Hammarström A. Social and material adversity from adolescence to adulthood and allostatic load in middle-aged women and men: results from the Northern Swedish Cohort. Ann Behav Med Publ Soc Behav Med. 2012;43:117–28.CrossRef Gustafsson PE, Janlert U, Theorell T, Westerlund H, Hammarström A. Social and material adversity from adolescence to adulthood and allostatic load in middle-aged women and men: results from the Northern Swedish Cohort. Ann Behav Med Publ Soc Behav Med. 2012;43:117–28.CrossRef
22.
go back to reference Barboza Solís C, Fantin R, Castagné R, Lang T, Delpierre C, Kelly-Irving M. Mediating pathways between parental socio-economic position and allostatic load in mid-life: findings from the 1958 British birth cohort. Soc Sci Med. 1982;2016(165):19–27. Barboza Solís C, Fantin R, Castagné R, Lang T, Delpierre C, Kelly-Irving M. Mediating pathways between parental socio-economic position and allostatic load in mid-life: findings from the 1958 British birth cohort. Soc Sci Med. 1982;2016(165):19–27.
23.
go back to reference Barboza Solís C, Kelly-Irving M, Fantin R, Darnaudéry M, Torrisani J, Lang T, et al. Adverse childhood experiences and physiological wear-and-tear in midlife: findings from the 1958 British birth cohort. Proc Natl Acad Sci USA. 2015;112:E738–46.CrossRefPubMedPubMedCentral Barboza Solís C, Kelly-Irving M, Fantin R, Darnaudéry M, Torrisani J, Lang T, et al. Adverse childhood experiences and physiological wear-and-tear in midlife: findings from the 1958 British birth cohort. Proc Natl Acad Sci USA. 2015;112:E738–46.CrossRefPubMedPubMedCentral
24.
go back to reference Barboza Solís C, Fantin R, Kelly-Irving M, Delpierre C. Physiological wear-and-tear and later subjective health in mid-life: Findings from the 1958 British birth cohort. Psychoneuroendocrinology. 2016;74:24–33.CrossRefPubMed Barboza Solís C, Fantin R, Kelly-Irving M, Delpierre C. Physiological wear-and-tear and later subjective health in mid-life: Findings from the 1958 British birth cohort. Psychoneuroendocrinology. 2016;74:24–33.CrossRefPubMed
25.
go back to reference Power C, Elliott J. Cohort profile: 1958 British birth cohort (National Child Development Study). Int J Epidemiol. 2006;35:34–41.CrossRefPubMed Power C, Elliott J. Cohort profile: 1958 British birth cohort (National Child Development Study). Int J Epidemiol. 2006;35:34–41.CrossRefPubMed
26.
go back to reference Elliott J, Johnson J, Shepherd P. Guide to the NCDS Biomedical Dataset.pdf. Lond Cent Longitud Stud Institute of Education. London; 2008. Elliott J, Johnson J, Shepherd P. Guide to the NCDS Biomedical Dataset.pdf. Lond Cent Longitud Stud Institute of Education. London; 2008.
27.
go back to reference Atherton K, Fuller E, Shepherd P, Strachan DP, Power C. Loss and representativeness in a biomedical survey at age 45 years: 1958 British birth cohort. J Epidemiol Community Health. 2008;62:216–23.CrossRefPubMed Atherton K, Fuller E, Shepherd P, Strachan DP, Power C. Loss and representativeness in a biomedical survey at age 45 years: 1958 British birth cohort. J Epidemiol Community Health. 2008;62:216–23.CrossRefPubMed
28.
go back to reference Seeman TE, McEwen BS, Rowe JW, Singer BH. Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. Proc Natl Acad Sci USA. 2001;98:4770–5.CrossRefPubMedPubMedCentral Seeman TE, McEwen BS, Rowe JW, Singer BH. Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. Proc Natl Acad Sci USA. 2001;98:4770–5.CrossRefPubMedPubMedCentral
29.
go back to reference Kelly-Irving M, Lepage B, Dedieu D, Bartley M, Blane D, Grosclaude P, et al. Adverse childhood experiences and premature all-cause mortality. Eur J Epidemiol. 2013;28:721–34.CrossRefPubMedPubMedCentral Kelly-Irving M, Lepage B, Dedieu D, Bartley M, Blane D, Grosclaude P, et al. Adverse childhood experiences and premature all-cause mortality. Eur J Epidemiol. 2013;28:721–34.CrossRefPubMedPubMedCentral
31.
go back to reference Team RC. A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical. Computing. 2014;73:3–36. Team RC. A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical. Computing. 2014;73:3–36.
32.
go back to reference Karlamangla AS, Singer BH, Seeman TE. Reduction in allostatic load in older adults is associated with lower all-cause mortality risk: MacArthur studies of successful aging. Psychosom Med. 2006;68:500–7.CrossRefPubMed Karlamangla AS, Singer BH, Seeman TE. Reduction in allostatic load in older adults is associated with lower all-cause mortality risk: MacArthur studies of successful aging. Psychosom Med. 2006;68:500–7.CrossRefPubMed
33.
go back to reference Borrell LN, Dallo FJ, Nguyen N. Racial/ethnic disparities in all-cause mortality in U.S. adults: the effect of allostatic load. Public Health Rep. Wash. DC 1974. 2010;125:810–6. Borrell LN, Dallo FJ, Nguyen N. Racial/ethnic disparities in all-cause mortality in U.S. adults: the effect of allostatic load. Public Health Rep. Wash. DC 1974. 2010;125:810–6.
34.
go back to reference Levine ME, Crimmins EM. A comparison of methods for assessing mortality risk. Am J Hum Biol Off J Hum Biol Counc. 2014;26:768–76.CrossRef Levine ME, Crimmins EM. A comparison of methods for assessing mortality risk. Am J Hum Biol Off J Hum Biol Counc. 2014;26:768–76.CrossRef
35.
go back to reference Howard JT, Sparks PJ. The effects of allostatic load on racial/ethnic mortality differences in the united states. Popul Res Policy Rev. 2016;35:421–43.CrossRef Howard JT, Sparks PJ. The effects of allostatic load on racial/ethnic mortality differences in the united states. Popul Res Policy Rev. 2016;35:421–43.CrossRef
36.
go back to reference Hwang A-C, Peng L-N, Wen Y-W, Tsai Y-W, Chang L-C, Chiou S-T, et al. Predicting all-cause and cause-specific mortality by static and dynamic measurements of allostatic load: a 10-year population-based cohort study in Taiwan. J Am Med Dir Assoc. 2014;15:490–6.CrossRefPubMed Hwang A-C, Peng L-N, Wen Y-W, Tsai Y-W, Chang L-C, Chiou S-T, et al. Predicting all-cause and cause-specific mortality by static and dynamic measurements of allostatic load: a 10-year population-based cohort study in Taiwan. J Am Med Dir Assoc. 2014;15:490–6.CrossRefPubMed
37.
go back to reference Robertson T, Beveridge G, Bromley C. Allostatic load as a predictor of all-cause and cause-specific mortality in the general population: Evidence from the Scottish Health Survey. PLoS ONE. 2017;12:e0183297.CrossRefPubMedPubMedCentral Robertson T, Beveridge G, Bromley C. Allostatic load as a predictor of all-cause and cause-specific mortality in the general population: Evidence from the Scottish Health Survey. PLoS ONE. 2017;12:e0183297.CrossRefPubMedPubMedCentral
38.
go back to reference McEwen BS, Seeman T. Protective and damaging effects of mediators of stress. Elaborating and testing the concepts of allostasis and allostatic load. Ann N Y Acad Sci. 1999;896:30–47.CrossRefPubMed McEwen BS, Seeman T. Protective and damaging effects of mediators of stress. Elaborating and testing the concepts of allostasis and allostatic load. Ann N Y Acad Sci. 1999;896:30–47.CrossRefPubMed
39.
go back to reference Johnson SC, Cavallaro FL, Leon DA. A systematic review of allostatic load in relation to socioeconomic position: poor fidelity and major inconsistencies in biomarkers employed. Soc Sci Med. 1982;2017(192):66–73. Johnson SC, Cavallaro FL, Leon DA. A systematic review of allostatic load in relation to socioeconomic position: poor fidelity and major inconsistencies in biomarkers employed. Soc Sci Med. 1982;2017(192):66–73.
40.
go back to reference Karlamangla AS, Singer BH, McEwen BS, Rowe JW, Seeman TE. Allostatic load as a predictor of functional decline. MacArthur studies of successful aging. J Clin Epidemiol. 2002;55:696–710.CrossRefPubMed Karlamangla AS, Singer BH, McEwen BS, Rowe JW, Seeman TE. Allostatic load as a predictor of functional decline. MacArthur studies of successful aging. J Clin Epidemiol. 2002;55:696–710.CrossRefPubMed
Metadata
Title
Allostatic load and subsequent all-cause mortality: which biological markers drive the relationship? Findings from a UK birth cohort
Authors
Raphaële Castagné
Valérie Garès
Maryam Karimi
Marc Chadeau-Hyam
Paolo Vineis
Cyrille Delpierre
Michelle Kelly-Irving
for the Lifepath Consortium
Publication date
01-05-2018
Publisher
Springer Netherlands
Published in
European Journal of Epidemiology / Issue 5/2018
Print ISSN: 0393-2990
Electronic ISSN: 1573-7284
DOI
https://doi.org/10.1007/s10654-018-0364-1

Other articles of this Issue 5/2018

European Journal of Epidemiology 5/2018 Go to the issue