Socioeconomic status, health behavior, and leukocyte telomere length in the National Health and Nutrition Examination Survey, 1999-2002

Social Science and Medicine

Volumn 85, Issue , 2013, Pages 1-8

  Needham, Belinda L ^a   Adler, Nancy ^b   Gregorich, Steven ^b   Rehkopf, David ^c   Lin, Jue ^d   Blackburn, Elizabeth H ^d   Epel, Elissa S ^b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell aging; Health behavior; Socioeconomic status; Telomere length; United States

Indexed keywords

EDUCATIONAL ATTAINMENT; ETHNICITY; HEALTH SURVEY; PUBLIC HEALTH; SOCIOECONOMIC STATUS;

ADULT; AFRICAN AMERICAN; AGED; ARTICLE; BODY MASS; CELL AGING; DRINKING; ETHNIC DIFFERENCE; HEALTH BEHAVIOR; HEALTH SURVEY; HIGH SCHOOL STUDENT; HUMAN; INCOME; LEUKOCYTE; NATIONAL HEALTH AND NUTRITION EXAMINATION SURVEY; RACE DIFFERENCE; SMOKING; SOCIAL STATUS; TELOMERE;

ADULT; AFRICAN AMERICANS; AGED; AGED, 80 AND OVER; ALCOHOL DRINKING; BIOLOGICAL MARKERS; BODY MASS INDEX; CELL AGING; CROSS-SECTIONAL STUDIES; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; HEALTH BEHAVIOR; HUMANS; LEUKOCYTES; MALE; MIDDLE AGED; NUTRITION SURVEYS; SEDENTARY LIFESTYLE; SMOKING; SOCIAL CLASS; TELOMERE; UNITED STATES; YOUNG ADULT;

UNITED STATES;

EID: 84876163913     PISSN: 02779536     EISSN: 18735347     Source Type: Journal    
DOI: 10.1016/j.socscimed.2013.02.023     Document Type: Article

References (82)

1. Adams J., Martin-Ruiz C., Pearce M., White M., Parker L., von Zglinicki T. No association between socio-economic status and white blood cell telomere length. Aging Cell 2007, 6:125-128.
2. Adler N., Pantell M., O'Donovan A., Blackburn E., Cawthon R., Koster A., et al. Educational attainment and late life telomere length in the Health, Aging and Body Composition Study. Brain, Behavior, and Immunity 2013, 27(1):15-21.
3. Adler N.E., Rehkopf D.H. US disparities in health: descriptions, causes, and mechanisms. Annual Review of Public Health 2008, 29:235-252.
4. Adler N.E., Stewart J. Health disparities across the lifespan: meaning, methods, and mechanisms. Annals of the New York Academy of Sciences 2010, 1186:5-23.
5. Allsopp R., Vaziri H., Patterson C., et al. Telomere length predicts replicative capacity of human fibroblasts. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:10114-10118.
6. Armanios M., Blackburn E.H. The telomere syndromes. Nature Reviews Genetics 2012, 13:693-704.
7. Aubert G., Lansdorp P.M. Telomeres and aging. Physiological Reviews 2008, 88:557-579.
8. Aviv A. The epidemiology of human telomeres: faults and promises. Journal of Gerontology Series A: Biological Sciences and Medical Sciences 2008, 63:979-983.
9. Aviv A., Chen W., Gardner J.P., Kimura M., Brimacombe M., Cao X., et al. Leukocyte telomere dynamics: longitudinal findings among young adults in the Bogalusa Heart Study. American Journal of Epidemiology 2009, 169:323-329.
10. Aviv A., Valdes A., Spector T. Human telomere biology: pitfalls of moving from the laboratory to epidemiology. International Journal of Epidemiology 2006, 35:1424-1429.
11. Bakaysa S., Mucci L., Slagbloom P., Boomsma D., McClearn G., Johansson B., et al. Telomere length predicts survival independent of genetic influences. Aging Cell 2007, 6:769-774.
12. Baron R.M., Kenny D.A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality & Social Psychology 1986, 51:1173-1182.
13. Barrett E.L.B., Richardson D.S. Sex differences in telomeres and lifespan. Aging Cell 2011, 10:913-921.
14. Batty G.D., Wang Y., Brouilette S.W., Shiels P., Packard C., Moore J., et al. Socioeconomic status and telomere length: the West of Scotland Coronary Prevention Study. Journal of Epidemiology and Community Health 2009, 63:839-841.
15. Bernardes de Jesus B., Vera E., Schneeberger K., Tejera A.M., Ayuso E., Bosch F., et al. Telomerase gene therapy in adult and old mice delays aging and increases longevity without increasing cancer. EMBO Molecular Medicine 2012, 4:691-704.
16. Blackburn E. The telomere and telomerase: nucleic acid-protein complexes acting in a telomere homeostasis system. A review. Biochemistry (Moscow) 1997, 62:1196-1201.
17. Blackburn E. Telomere states and cell fates. Nature 2000, 408:53-56.
18. Blackburn E. Telomeres and telomerase: their mechanisms of action and the effects of altering their functions. FEBS Letters 2005, 579:859-862.
19. Blasco M.A. Telomeres and human disease: ageing, cancer and beyond. Nature Reviews Genetics 2005, 6:611-622.
20. Braveman P., Cubbin C., Egerter S., Chideya S., Marchi K., Metzler M., et al. Socioeconomic status in health research: one size does not fit all. Journal of the American Medical Association 2005, 294:2879-2888.
21. Card D., Krueger A. School quality and black-white relative earnings: a direct assessment. The Quarterly Journal of Economics 1992, 197:151-200.
22. Carroll J.E., Diez-Roux A.V., Adler N.E., Seeman T.E. Socioeconomic factors and leukocyte telomere length in a multi-ethnic sample: findings from the multi-ethnic study of atherosclerosis (MESA). Brain, Behavior, and Immunity 2013, 28:108-114.
23. Cawthon R.M. Telomere measurement by quantitative PCR. Nucleic Acids Research 2002, 30.
24. Cawthon R., Smith K., O'Brien E., Sivatchenko A., Kerber R. Association between telomere length in blood and mortality in people aged 60 years or older. Lancet 2003, 361:393-395.
25. Cherkas L., Aviv A., Valdes A., Hunkin J., Gardner J., Surdulescu L., et al. The effects of social status on biological aging as measured by white-blood-cell telomere length. Aging Cell 2006, 5:361-365.
26. Choi J., Fauce S., Effros R. Reduced telomerase activity in human T lymphocytes exposed to cortisol. Brain, Behavior, and Immunity 2008, 22:600-605.
27. Cohen S., Schwartz J., Epel E., Kirschbaum C., Sidney S., Seeman T. Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Psychosomatic Medicine 2006, 68:41-50.
28. Conley D. Being black, living in the red: Race, wealth, and social policy in America 1999, University of California Press, Berkeley.
29. Damjanovic A., Yang Y., Glaser R., Kiecolt-Glaser J., Nguyen H., Laskowski B., et al. Accelerated telomere erosion is associated with a declining immune function of caregivers of Alzheimer's disease patients. Journal of Immunology 2007, 179:4249-4254.
30. Demissie S., Levy D., Benjamin E.J., Cupples L.A., Gardner J.P., Herbert A., et al. Insulin resistance, oxidative stress, hypertension, and leukocyte telomere length in men from the Framingham Heart Study. Aging Cell 2006, 5:325-330.
31. Der G., Batty G.D., Benzeval M., Deary I.J., Green M.J., McGlynn L., et al. Is telomere length a biomarker for aging: cross-sectional evidence from the west of Scotland?. PLoS One 2012, 7:e45166.
32. Diez Roux A., Ranjit N., Jenny N., Shea S., Cushman M., Fitzpatrick A., et al. Race/ethnicity and telomere length in the Multi-Ethnic Study of Atherosclerosis. Aging Cell 2009, 8(3):251-257.
33. Drury S., Theall K., Gleason M., Smyke A., De Vivo I., Wong J., et al. Telomere length and early severe social deprivation: linking early adversity and cellular aging. Molecular Psychiatry 2012, 17:719-727.
34. Du M., Prescott J., Kraft P., Han J., Giovannucci E., Hankinson S.E., et al. Physical activity, sedentary behavior, and leukocyte telomere length in women. American Journal of Epidemiology 2012, 175:414-422.
35. Edo M., Andres V. Aging, telomeres, and atherosclerosis. Cardiovascular Research 2005, 66:213-221.
36. Effros R. T cell replicative senescence: pleiotropic effects on human aging. Annals of the New York Academy of Sciences 2004, 1019:123-126.
37. Effros R., Dagarag M., Spaulding C., Man J. The role of CD8+ T-cell replicative senescence in human aging. Immunological Reviews 2005, 205:147-157.
38. Epel E.S., Blackburn E.H., Lin J., Dhabhar F.S., Adler N.E., Morrow J.D., et al. Accelerated telomere shortening in response to life stress. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:17312-17315.
39. Ford E.S., Zhao G., Tsai J., Li C. Low-risk lifestyle behaviors and all-cause mortality: findings from the National Health and Nutrition Examination Survey III Mortality Study. American Journal of Public Health 2011, 101:1922-1929.
40. Freedman D.S., Gates L., Flanders W.D., Van Assendelft O.W., Barboriak J.J., Joesoef M.R., et al. Black/white differences in leukocyte subpopulations in men. International Journal of Epidemiology 1997, 26:757-764.
41. Frenck R., Blackburn E., Shannon K. The rate of telomere sequence loss in human leukocytes varies with age. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:5607-5610.
42. Geronimus A.T., Hicken M., Keene D., Bound J. "Weathering" and age patterns of allostatic load scores among blacks and whites in the United States. American Journal of Public Health 2006, 96:826-833.
43. Geronimus A.T., Hicken M.T., Pearson J.A., Seashols S.J., Brown K.L., Cruz T.D. Do US black women experience stress-related accelerated biological aging?: a novel theory and first population-based test of black-white differences in telomere length. Human Nature 2010, 21:19-38.
44. Hunt S., Chen W., Gardner J., Kimura M., Srinivasan S., Eckfeldt J., et al. Leukocyte telomeres are longer in African Americans than in whites: the NHLBI Family Heart Study and the Bogalusa Heart Study. Aging Cell 2008, 7(4):451-458.
45. Iacobucci D. Mediation analysis and categorical variables: the final frontier. Journal of Consumer Psychology 2012, 22:582-594.
46. Iwama H., Ohyashiki K., Ohyashiki J.H., Hayashi S., Yahata N., Ando K., et al. Telomeric length and telomerase activity vary with age in peripheral blood cells obtained from normal individuals. Human Genetics 1998, 102:397-402.
47. Janicki-Deverts D., Cohen S., Adler N., Schwartz J., Matthews K., Seeman T. Socioeconomic status is related to urinary catecholamines in the Coronary Artery Risk Development in Young Adults (CARDIA) study. Psychosomatic Medicine 2007, 69:514-520.
48. Jaskelioff M., Muller F.L., Paik J.H., Thomas E., Jiang S., Adams A.C., et al. Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 2011, 469:102-106.
49. Kananen L., Surakka I., Pirkola S., Suvisaari J., Lonnqvist J., Peltonen L., et al. Childhood adversities are associated with shorter telomere length at adult age both in individuals with an anxiety disorder and controls. PLoS One 2010, 5:e10826.
50. Khaw K.T., Wareham N., Bingham S., Welch A., Luben R., Day N. Combined impact of health behaviours and mortality in men and women: the EPIC-Norfolk prospective population study. PLoS Medicine 2008, 5:e12.
51. Kim S., Parks C.G., DeRoo L.A., Chen H., Taylor J.A., Cawthon R.M., et al. Obesity and weight gain in adulthood and telomere length. Cancer Epidemiology, Biomarkers and Prevention 2009, 18:816-820.
52. Krieger N., Williams D., Moss N. Measuring social class in US public health research: concepts, methodologies, and guidelines. Annual Review of Public Health 1997, 18:341-378.
53. Lee M., Martin H., Firpo M.A., Demerath E.W. Inverse association between adiposity and telomere length: the Fels Longitudinal Study. American Journal of Human Biology 2011, 23:100-106.
54. Lin J., Epel E., Cheon J., Kroenke C., Sinclair E., Bigos M., et al. Analyses and comparisons of telomerase activity and telomere length in human T and B cells: insights for epidemiology of telomere maintenance. Journal of Immunological Methods 2010, 352:71-80.
55. Ludlow A.T., Roth S.M. Physical activity and telomere biology: exploring the link with aging-related disease prevention. Journal of Aging Research 2011, 2011:790378.
56. Lynch J., Kaplan G. Socioeconomic position. Social epidemiology 2000, 13-35. Oxford, New York. L.F. Berkman, I. Kawachi (Eds.).
57. McEwen B. Protective and damaging effects of stress mediators. New England Journal of Medicine 1998, 338:171-179.
58. McGrath M., Wong J.Y., Michaud D., Hunter D.J., De Vivo I. Telomere length, cigarette smoking, and bladder cancer risk in men and women. Cancer Epidemiology, Biomarkers and Prevention 2007, 16:815-819.
59. Mannino D., Aguayo S., Petty T., Redd S. Low lung function and incident lung cancer in the United States. Archives of Internal Medicine 2003, 163:1475-1480.
60. National Center for Health Statistics Analytic and reporting guidelines: The National Health and Nutrition Examination Survey (NHANES) 2006, National Center for Health Statistics, Centers for Disease Control and Prevention, Hyattsville, MD.
61. Needham B.L., Fernandez J.R., Lin J., Epel E.S., Blackburn E.H. Socioeconomic status and cell aging in children. Social Science & Medicine 2012, 74:1948-1951.
62. Olovnikov A.M. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. Journal of Theoretical Biology 1973, 41:181-190.
63. Paternoster R., Brame R., Mazerolle P., Piquero A. Using the correct statistical test for the quality of regression coefficients. Criminology 1998, 36:859-866.
64. Pavanello S., Hoxha M., Dioni L., Bertazzi P.A., Snenghi R., Nalesso A., et al. Shortened telomeres in individuals with abuse in alcohol consumption. International Journal of Cancer 2011, 129:983-992.
65. Robertson T., Batty G.D., Der G., Fenton C., Shiels P.G., Benzeval M. Is socioeconomic status associated with biological aging as measured by telomere length?. Epidemiologic Reviews 2012, 7(7):e41805.
66. Robertson T., Batty G.D., Der G., Green M.J., McGlynn L.M., McIntyre A., et al. Is telomere length socially patterned? Evidence from the West of Scotland Twenty-07 Study. PLoS One 2012, 7:e41805.
67. Sabin R.J., Anderson R.M. Cellular Senescence - its role in cancer and the response to ionizing radiation. Genome Integrity 2011, 2:7.
68. Samani N., Boultby R., Butler R., Thompson J., Goodall A. Telomere shortening in atherosclerosis. Lancet 2001, 358:472-473.
69. Shiels P.G., McGlynn L.M., MacIntyre A., Johnson P.C., Batty G.D., Burns H., et al. Accelerated telomere attrition is associated with relative household income, diet and inflammation in the pSoBid cohort. PLoS One 2011, 6:e22521.
70. Sloan R., Huang M., Sidney S., Liu K., Williams O., Seeman T. Socioeconomic status and health: is parasympathetic nervous system activity an intervening mechanism?. International Journal of Epidemiology 2005, 34:309-315.
71. Steptoe A., Hamer M., Butcher L., Lin J., Brydon L., Kivimaki M., et al. Educational attainment but not measures of current socioeconomic circumstances are associated with leukocyte telomere length in healthy older men and women. Brain, Behavior, and Immunity 2011, 25:1292-1298.
72. Strandberg T.E., Saijonmaa O., Tilvis R.S., Pitkala K.H., Strandberg A.Y., Miettinen T.A., et al. Association of telomere length in older men with mortality and midlife body mass index and smoking. Journals of Gerontology Series A: Biological Sciences and Medical Sciences 2011, 66:815-820.
73. Surtees P.G., Wainwright N.W., Pooley K.A., Luben R.N., Khaw K.T., Easton D.F., et al. Educational attainment and mean leukocyte telomere length in women in the European Prospective Investigation into Cancer (EPIC)-Norfolk population study. Brain, Behavior, and Immunity 2012, 26:414-418.
74. Tyrka A.R., Price L.H., Kao H.T., Porton B., Marsella S.A., Carpenter L.L. Childhood maltreatment and telomere shortening: preliminary support for an effect of early stress on cellular aging. Biological Psychiatry 2010, 67:531-534.
75. Tzanetakou I.P., Katsilambros N.L., Benetos A., Mikhailidis D.P., Perrea D.N. "Is obesity linked to aging?": adipose tissue and the role of telomeres. Ageing Research Reviews 2012, 11:220-229.
76. Valdes A., Andrew T., Gardner J., et al. Obesity, cigarette smoking, and telomere length in women. Lancet 2005, 366:662-664.
77. Vittinghoff E., Glidden D.V., Shiboski S.C., McCulloch C.E. Regression methods in biostatistics 2012, Springer, New York.
78. Weischer M., Bojesen S.E., Cawthon R.M., Freiberg J.J., Tybjaerg-Hansen A., Nordestgaard B.G. Short telomere length, myocardial infarction, ischemic heart disease, and early death. Arteriosclerosis, Thrombosis, and Vascular Biology 2012, 32:822-829.
79. Williams D.R., Collins C. US socioeconomic and racial differences in health: patterns and explanations. Annual Review of Sociology 1995, 349-386.
80. Zee R.Y., Castonguay A.J., Barton N.S., Germer S., Martin M. Mean leukocyte telomere length shortening and type 2 diabetes mellitus: a case-control study. Translational Research 2010, 155:166-169.
81. von Zglinicki T., Saretzki G., Docke W., Lotze C. Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence?. Experimental Cell Research 1995, 220:186-193.
82. Zhu H., Wang X., Gutin B., Davis C.L., Keeton D., Thomas J., et al. Leukocyte telomere length in healthy Caucasian and African-American adolescents: relationships with race, sex, adiposity, adipokines, and physical activity. Journal of Pediatrics 2011, 158:215-220.