Chronic psychosocial and financial burden accelerates 5-year telomere shortening: findings from the Coronary Artery Risk Development in Young Adults Study.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
06
04
2018
accepted:
21
05
2019
revised:
09
05
2019
pubmed:
29
8
2019
medline:
17
3
2021
entrez:
29
8
2019
Statut:
ppublish
Résumé
Leukocyte telomere length, a marker of immune system function, is sensitive to exposures such as psychosocial stressors and health-maintaining behaviors. Past research has determined that stress experienced in adulthood is associated with shorter telomere length, but is limited to mostly cross-sectional reports. We test whether repeated reports of chronic psychosocial and financial burden is associated with telomere length change over a 5-year period (years 15 and 20) from 969 participants in the Coronary Artery Risk Development in Young Adults (CARDIA) Study, a longitudinal, population-based cohort, ages 18-30 at time of recruitment in 1985. We further examine whether multisystem resiliency, comprised of social connections, health-maintaining behaviors, and psychological resources, mitigates the effects of repeated burden on telomere attrition over 5 years. Our results indicate that adults with high chronic burden do not show decreased telomere length over the 5-year period. However, these effects do vary by level of resiliency, as regression results revealed a significant interaction between chronic burden and multisystem resiliency. For individuals with high repeated chronic burden and low multisystem resiliency (1 SD below the mean), there was a significant 5-year shortening in telomere length, whereas no significant relationships between chronic burden and attrition were evident for those at moderate and higher levels of resiliency. These effects apply similarly across the three components of resiliency. Results imply that interventions should focus on establishing strong social connections, psychological resources, and health-maintaining behaviors when attempting to ameliorate stress-related decline in telomere length among at-risk individuals.
Identifiants
pubmed: 31455861
doi: 10.1038/s41380-019-0482-5
pii: 10.1038/s41380-019-0482-5
pmc: PMC7044034
mid: NIHMS1530061
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1141-1153Subventions
Organisme : NIMH NIH HHS
ID : T32 MH019391
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201300026C
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201300025C
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201300027C
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201300029C
Pays : United States
Organisme : NHLBI NIH HHS
ID : R00 HL109247
Pays : United States
Organisme : NHLBI NIH HHS
ID : K99 HL109247
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268200900041C
Pays : United States
Organisme : NHLBI NIH HHS
ID : HHSN268201300028C
Pays : United States
Références
Richardson S, Shaffer JA, Falzon L, Krupka D, Davidson KW, Edmondson D. Meta-analysis of perceived stress and its association with incident coronary heart disease. Am J Cardiol. 2012;110:1711–6.
pubmed: 22975465
pmcid: 3511594
Cohen S, Janicki-Deverts D, Miller GE. Psychological stress and disease. J Am Med Assoc. 2007;298:1685–7.
Yusuf S, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case–control study. Lancet. 2004;364:937–52.
Aldwin CM, et al. Do stress trajectories predict mortality in older men? Longitudinal findings from the VA normative aging study. J Aging Res. 2011;2011:896109.
pubmed: 21961066
pmcid: 3180855
Miller GE, Chen E, Cole SW. Health psychology: developing biologically plausible models linking the social world and physical health. Annu Rev Psychol. 2009;60:501–24.
pubmed: 19035829
Gouin JP, Hantsoo L, Kiecolt-Glaser JK. Immune dysregulation and chronic stress among older adults: a review. Neuroimmunomodulation. 2008;15:251–9.
pubmed: 19047802
pmcid: 2676338
Blackburn EH. Telomere states and cell fates. Nature. 2000;408:53–56.
pubmed: 11081503
Campisi J, di Fagagna FD. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007;8:729–40.
pubmed: 17667954
Sahin E, Depinho RA. Axis of ageing: telomeres, p53 and mitochondria. Nat Rev Mol Cell Biol. 2012;13:397–404.
pubmed: 22588366
pmcid: 3718675
Jaskelioff M, et al. Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature. 2011;469:102–6.
pubmed: 21113150
Haycock PC, et al. Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2014;349:g4227.
pubmed: 25006006
pmcid: 4086028
Codd V, et al. Identification of seven loci affecting mean telomere length and their association with disease. Nat Genet. 2013;45:422–7.
pubmed: 23535734
pmcid: 4006270
Wentzensen IM, Mirabello L, Pfeiffer RM, Savage SA. The association of telomere length and cancer: a meta-analysis. Cancer Epidemiol Biomark Prev. 2011;20:1238–50.
Ma H, et al. Shortened telomere length is associated with increased risk of cancer: a meta-analysis. PLoS ONE. 2011;6:e20466.
pubmed: 21695195
pmcid: 3112149
Zhao J, Miao K, Wang H, Ding H, Wang DW. Association between telomere length and type 2 diabetes mellitus: a meta-analysis. PLoS ONE. 2013;8:e79993.
pubmed: 24278229
pmcid: 3836967
Rode L, Bojesen SE, Weischer M, Vestbo J, Nordestgaard BG. Short telomere length, lung function and chronic obstructive pulmonary disease in 46,396 individuals. Thorax. 2013;68:429–35.
pubmed: 23268483
Zhan Y, et al. Telomere length shortening and Alzheimer disease—a Mendelian randomization study. JAMA Neurol. 2015;72:1202–3.
pubmed: 26457630
Cawthon RM, Smith KR, O’Brien E, Sivatchenko A, Kerber RA. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet. 2003;361:393–5.
pubmed: 12573379
Epel ES, et al. The rate of leukocyte telomere shortening predicts mortality from cardiovascular disease in elderly men. Aging. 2009;1:81–88.
Glei DA, Goldman N, Weinstein M, Risques RA. Shorter ends, faster end? Leukocyte telomere length and mortality among older Taiwanese. J Gerontol A Biol Sci Med Sci. 2014; glu191. https://doi.org/10.1093/gerona/glu191 .
Kimura M, et al. Telomere length and mortality: a study of leukocytes in elderly Danish twins. Am J Epidemiol. 2008;167:799–806.
pubmed: 18270372
pmcid: 3631778
Bakaysa SL, et al. Telomere length predicts survival independent of genetic influences. Aging Cell. 2007;6:769–74.
pubmed: 17925004
Deelen J, et al. Leukocyte telomere length associates with prospective mortality independent of immune-related parameters and known genetic markers. Int J Epidemiol. 2014;43:878–86.
pubmed: 24425829
pmcid: 4052133
Schaefer C, et al. Demographic and behavioral influences on telomere length and relationship with all-cause mortality: early results from the Kaiser Permanente Research Program on Genes, Environ, Health (RPGEH). Clin Med Res. 2013;11:146–146.
pmcid: 3788534
Bendix L, et al. Longitudinal changes in leukocyte telomere length and mortality in humans. J Gerontol A Biol Sci Med Sci. 2014;69:231–9.
pubmed: 24149432
Svensson J, et al. Leukocyte telomere length is not associated with mortality in older men. Exp Gerontol. 2014;57:6–12.
pubmed: 24793325
Duggan C, et al. Change in peripheral blood leukocyte telomere length and mortality in breast cancer survivors. J Natl Cancer Inst. 2014;106:dju035.
pubmed: 24627273
pmcid: 3982887
Njajou OT, et al. Association between telomere length, specific causes of death, and years of healthy life in health, aging, and body composition, a population-based cohort study. J Gerontol Ser A Biol Sci Med Sci. 2009;64:860–4.
Rode L, Nordestgaard BG, Bojesen SE. Peripheral blood leukocyte telomere length and mortality among 64,637 individuals from the general population. J Natl Cancer Inst. 2015;107:djv074.
pubmed: 25862531
Damjanovic AK, et al. Accelerated telomere erosion is associated with a declining immune function of caregivers of Alzheimer’s disease patients. J Immunol. 2007;179:4249–54.
pubmed: 17785865
pmcid: 2262924
Epel ES, et al. Accelerated telomere shortening in response to life stress. Proc Natl Acad Sci USA. 2004;101:17312–5.
pubmed: 15574496
Humphreys J, et al. Telomere shortening in formerly abused and never abused women. Biol Res Nurs. 2012;14:115–23.
pubmed: 21385798
Ala-Mursula L, et al. Long-term unemployment is associated with short telomeres in 31-year-old men: an observational study in the Northern Finland birth cohort 1966. PLoS ONE. 2013;8:e80094.
pubmed: 24278245
pmcid: 3835859
Litzelman K, et al. Association between informal caregiving and cellular aging in the survey of the health of Wisconsin: the role of caregiving characteristics, stress, and strain. Am J Epidemiol. 2014;179:1340–52.
pubmed: 24780842
pmcid: 4036217
Ahola K, et al. Work-related exhaustion and telomere length: a population-based study. PLoS ONE. 2012;7:e40186.
pubmed: 22808115
pmcid: 3394788
Pepper, GV, Bateson, M & Nettle, D. Telomeres as integrative markers of exposure to stress and adversity: a systematic review and meta-analysis. 2018 bioRxiv 320150. https://doi.org/10.1101/320150 .
Puterman E, et al. Lifespan adversity and later adulthood telomere length in the nationally representative US Health and Retirement Study. Proc Natl Acad Sci USA. 2016;113:E6335–E6342.
pubmed: 27698131
Verhoeven JE, van Oppen P, Puterman E, Elzinga B, Penninx BWJH. The association of early and recent psychosocial life stress with leukocyte telomere length. Psychosom Med. 2015;77:882–91.
pubmed: 26374947
Puterman E, Lin J, Krauss J, Blackburn EH, Epel ES. Determinants of telomere attrition over 1 year in healthy older women: stress and health behaviors matter. Mol Psychiatry. 2015;20:529–35.
pubmed: 25070535
Taylor SE, Seeman TE. Psychosocial resources and the SES-health relationship. Ann N Y Acad Sci. 1999;896:210–25.
pubmed: 10681899
Taylor SE, Kemeny ME, Reed GM, Bower JE, Gruenewald TL. Psychological resources, positive illusions, and health. Am Psychol. 2000;55:99–109.
pubmed: 11392870
Cohen S, Wills TAS. Stress, social support, and the buffering hypothesis. Psychol Bull. 1985;98:310–57.
pubmed: 3901065
Hamer M. Psychosocial stress and cardiovascular disease risk: the role of physical activity. Psychosom Med. 2012;74:896–903.
pubmed: 23107839
Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24:385–96.
pubmed: 6668417
Puterman E, et al. The power of exercise: buffering the effect of chronic stress on telomere length. PLoS ONE. 2010;5:e10837.
Puterman E, et al. Aerobic exercise lengthens telomeres and reduces stress in family caregivers: a randomized controlled trial—Curt Richter Award Paper 2018. Psychoneuroendocrinology. 2018. https://doi.org/10.1016/J.PSYNEUEN.2018.08.002 .
Liu JJW, Reed M, Girard TA. Advancing resilience: an integrative, multi-system model of resilience. Personal Individ Differ. 2017;111:111–8.
Puterman E, Epel ES. An intricate dance: life experience, multisystem resiliency, and rate of telomere decline throughout the lifespan. Soc Personal Psychol Compass. 2012;6:807–25.
pubmed: 23162608
pmcid: 3496269
Puterman E, et al. Multisystem resiliency moderates the major depression-telomere length association: findings from the heart and soul study. Brain Behav Immun. 2013;33:65–73.
pubmed: 23727245
Friedman GD, et al. CARDIA: study design, recruitment, and some characteristics of the examined subjects. J Clin Epidemiol. 1988;41:1105–16.
pubmed: 3204420
Cohen S, et al. Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Psychosom Med. 2006;68:41–50.
pubmed: 16449410
Scheier MF, Carver CS, Bridges MW. Distinguishing optimism from neuroticism (and trait anxiety, self-mastery, and self-esteem): a reevaluation of the Life Orientation Test. J Personal Soc Psychol. 1994;67:1063.
Pearlin LI, Schooler C. The structure of coping. J Health Soc Behav. 1978;19:2–212.
pubmed: 649936
Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30:e47.
pubmed: 12000852
pmcid: 115301
Lin J, et al. Analyses and comparisons of telomerase activity and telomere length in human T and B cells: insights for epidemiology of telomere maintenance. J Immunol Methods. 2010;352:71–80.
pubmed: 19837074
Enders CK. A primer on the use of modern missing-data methods in psychosomatic medicine research. Psychosom Med. 2006;68:427–36.
pubmed: 16738075
Schlomer GL, Bauman S, Card NA. Best practices for missing data management in counseling psychology. J Couns Psychol. 2010;57:1–10.
pubmed: 21133556
Glickman ME, Rao SR, Schultz MR. False discovery rate control is a recommended alternative to Bonferroni-type adjustments in health studies. J Clin Epidemiol. 2014;67:850–7.
pubmed: 24831050
Seeman TE, McEwen B, Rowe J, Singer B. Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. Proc Natl Acad Sci USA. 2001;98:4770–5.
pubmed: 11287659
Geronimus AT. The weathering hypothesis and the health of African-American women and infants: evidence and speculations. Ethn Dis. 1992;2:207–21.
pubmed: 1467758
Tomiyama AJ, et al. Does cellular aging relate to patterns of allostasis? An examination of basal and stress reactive HPA axis activity and telomere length. Physiol Behav. 2011. https://doi.org/10.1016/j.physbeh.2011.11.016 .
Epel ES, et al. Cell aging in relation to stress arousal and cardiovascular disease risk factors. Psychoneuroendocrinology. 2006;31:277–87.
pubmed: 16298085
Parks CG, et al. Telomere length, current perceived stress, and urinary stress hormones in women. Cancer Epidemiol Biomark Prev. 2009;18:551–60.
Steptoe A, Hamer M, Lin J, Blackburn EH, Erusalimsky JD. The longitudinal relationship between cortisol responses to mental stress and leukocyte telomere attrition. J Clin Endocrinol Metab. 2016; 2016–3035. https://doi.org/10.1210/jc.2016-3035 .
Charles ST, Piazza JR, Mogle J, Sliwinski MJ, Almeida DM. The wear and tear of daily stressors on mental health. Psychol Sci. 2013;24:733–41.
pubmed: 23531486
pmcid: 3654031
Piazza JR, Charles ST, Sliwinski MJ, Mogle J, Almeida DM. Affective reactivity to daily stressors and long-term risk of reporting a chronic physical health condition. Ann Behav Med. 2013;45:110–20.
pubmed: 23080393
pmcid: 3626280
Mroczek DK, et al. Emotional reactivity and mortality: longitudinal findings from the VA normative aging study. J Gerontol B Psychol Sci Soc Sci. 2013. https://doi.org/10.1093/geronb/gbt107 .
Epel ES, et al. More than a feeling: a unified view of stress measurement for population science. Front Neuroendocrinol. 2018. https://doi.org/10.1016/j.yfrne.2018.03.001 .
Puterman E, An EE. Intricate dance: life experience, multisystem resiliency, and rate of telomere decline throughout the lifespan. Soc Personal Psychol Compass. 2012;6:807–25.
pubmed: 23162608
pmcid: 3496269
Mezuk B, et al. “White Box” epidemiology and the social neuroscience of health behaviors. Soc Ment Health. 2013;3:79–95.
Schafer MH, Ferraro KF, Mustillo SA. Children of misfortune: early adversity and cumulative inequality in perceived life trajectories. AJS. 2011;116:1053.
pubmed: 21648247
pmcid: 3149822
Surtees PG, et al. Life stress, emotional health, and mean telomere length in the European prospective investigation into cancer (EPIC)—Norfolk population study. J Gerontol Ser a-Biol Sci Med Sci. 2011;66:1152–62.
Jodczyk S, Fergusson DM, Horwood LJ, Pearson JF, Kennedy MA. No association between mean telomere length and life stress observed in a 30 year birth cohort. PLoS ONE. 2014;9:e97102.
pubmed: 24816913
pmcid: 4016252
Steenstrup T, Hjelmborg JVB, Kark JD, Christensen K, Aviv A. The telomere lengthening conundrum-artifact or biology? Nucleic Acids Res. 2013;41:e131.
pubmed: 23671336
pmcid: 3905906
Verhoeven JE, Lin J, Révész D, Wolkowitz OM, Penninx BWJH, et al. Unresolved issues in longitudinal telomere length research: response to susser. Am J Psychiatry. 2016;173:1147–9.
pubmed: 27798998
Svenson U, et al. Blood cell telomere length is a dynamic feature. PLoS ONE. 2011;6:e21485.
pubmed: 21720548
pmcid: 3123359
Chen W, et al. Longitudinal versus cross-sectional evaluations of leukocyte telomere length dynamics: age-dependent telomere shortening is the rule. J Gerontol Ser A Biol Sci Med Sci. 2011;66:312–9.
Verhoeven JE, et al. Depression, telomeres and mitochondrial DNA: between- and within-person associations from a 10-year longitudinal study. Mol Psychiatry. 2017. https://doi.org/10.1038/mp.2017.48 .
Révész D, et al. Associations between cellular aging markers and metabolic syndrome: findings from the cardia study. J Clin Endocrinol Metab. 2018;103:148–57.
Lauderdale DS, Knutson KL, Yan LL, Liu K, Rathouz PJ. Self-reported and measured sleep duration: how similar are they? Epidemiology. 2008;19:838–45.
pubmed: 18854708
pmcid: 2785092
Booth M. Assessment of physical activity: an international perspective. Res Q Exerc Sport. 2000;71:S114–20.
pubmed: 10925833
Adam TC, Epel ES. Stress, eating, and the reward system. Physiol Behav. 2007;91:449–58.
pubmed: 17543357
Schuit AJ, van Loon AJM, Tijhuis M, Ocké M. Clustering of lifestyle risk factors in a general adult population. Prev Med. 2002;35:219–24.
pubmed: 12202063
Poortinga W. The prevalence and clustering of four major lifestyle risk factors in an English adult population. Prev Med. 2007;44:124–8.
pubmed: 17157369
Sun Q, et al. Healthy lifestyle and leukocyte telomere length in U.S. women. PloS ONE. 2012;7:e38374.