Leukocyte Telomere Length in Relation to 17 Biomarkers of Cardiovascular Disease Risk: A Cross-Sectional Study of US Adults

1. Haycock PC, Heydon EE, Kaptoge S, Butterworth AS, Thompson A, Willeit P. Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. 2014.

2. Sanders JL, Newman AB. Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither? Epidemiologic reviews. 2013;35(1):112–31.

3. Fitzpatrick AL, Kronmal RA, Gardner JP, Psaty BM, Jenny NS, Tracy RP, et al. Leukocyte telomere length and cardiovascular disease in the cardiovascular health study. American Journal of Epidemiology. 2007;165(1):14–21. Epub 2006/10/18. doi: 10.1093/aje/kwj346 17043079.

4. Epel ES, Merkin SS, Cawthon R, Blackburn EH, Adler NE, Pletcher MJ, et al. The rate of leukocyte telomere shortening predicts mortality from cardiovascular disease in elderly men. Aging (Albany NY). 2009;1(1):81–8. Epub 2009/01/01. 20195384; PubMed Central PMCID: PMC2830080. doi: 10.18632/aging.100007

5. van der Harst P, van der Steege G, de Boer RA, Voors AA, Hall AS, Mulder MJ, et al. Telomere length of circulating leukocytes is decreased in patients with chronic heart failure. Journal of the American College of Cardiology. 2007;49(13):1459–64. doi: 10.1016/j.jacc.2007.01.027 17397675

6. Willeit P, Willeit J, Brandstätter A, Ehrlenbach S, Mayr A, Gasperi A, et al. Cellular aging reflected by leukocyte telomere length predicts advanced atherosclerosis and cardiovascular disease risk. Arteriosclerosis, thrombosis, and vascular biology. 2010;30(8):1649–56. doi: 10.1161/ATVBAHA.110.205492 20508208

7. Codd V, Nelson CP, Albrecht E, Mangino M, Deelen J, Buxton JL, et al. Identification of seven loci affecting mean telomere length and their association with disease. Nat Genet. 2013;45(4):422–7, 7e1-2. doi: 10.1038/ng.2528 23535734; PubMed Central PMCID: PMCPMC4006270.

8. Bekaert S, De Meyer T, Rietzschel ER, De Buyzere ML, De Bacquer D, Langlois M, et al. Telomere length and cardiovascular risk factors in a middle-aged population free of overt cardiovascular disease. Aging Cell. 2007;6(5):639–47. doi: 10.1111/j.1474-9726.2007.00321.x 17874998.

9. DeFries T, Avendano M, Glymour MM. Level and change in cognitive test scores predict risk of first stroke. J Am Geriatr Soc. 2009;57(3):499–505. Epub 2009/01/30. doi: 10.1111/j.1532-5415.2008.02132.x 19175440.

10. D’Mello MJ, Ross SA, Briel M, Anand SS, Gerstein H, Paré G. Association Between Shortened Leukocyte Telomere Length and Cardiometabolic Outcomes Systematic Review and Meta-Analysis. Circulation: Cardiovascular Genetics. 2015;8(1):82–90.

11. Guzzardi MA, Iozzo P, Salonen M, Kajantie E, Eriksson JG. Rate of telomere shortening and metabolic and cardiovascular risk factors: A longitudinal study in the 1934–44 Helsinki Birth Cohort Study. Annals of medicine. 2015;47(6):499–505. doi: 10.3109/07853890.2015.1074718 26339993

12. Lin J, Cheon J, Brown R, Coccia M, Puterman E, Aschbacher K, et al. Systematic and Cell Type-Specific Telomere Length Changes in Subsets of Lymphocytes. Journal of immunology research. 2016;2016.

13. McQuillan GM, Pan Q, Porter KS. Consent for genetic research in a general population: an update on the National Health and Nutrition Examination Survey experience. Genet Med. 2006;8(6):354–60. doi: 10.109701.gim.0000223552.70393.08 16778597.

14. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30(10):e47. Epub 2002/05/10. 12000852; PubMed Central PMCID: PMC115301.

15. 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(1–2):71–80. Epub 2009/10/20. doi: 10.1016/j.jim.2009.09.012 19837074; PubMed Central PMCID: PMC3280689.

16. Farzaneh-Far R, Lin J, Epel E, Lapham K, Blackburn E, Whooley MA. Telomere length trajectory and its determinants in persons with coronary artery disease: longitudinal findings from the heart and soul study. PLoS ONE. 2010;5(1):e8612. Epub 2010/01/15. doi: 10.1371/journal.pone.0008612 20072607; PubMed Central PMCID: PMC2797633.

17. Gunter EW, Lewis BG, Koncikowski SM. Laboratory Procedures Used for the Third National Health and Nutrition Examination Survey (NHANES III), 1988–1994. Hyattsville: National Center for Health Statistics, 1996.

18. Levey AS, Coresh J, Greene T, Stevens LA, Zhang YL, Hendriksen S, et al. Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Annals of internal medicine. 2006;145(4):247–54. 16908915

19. Grundy SM, Cleeman JI, Merz CNB, Brewer HB, Clark LT, Hunninghake DB, et al. Implications of recent clinical trials for the national cholesterol education program adult treatment panel III guidelines. Journal of the American College of Cardiology. 2004;44(3):720–32. doi: 10.1016/j.jacc.2004.07.001 15358046

20. Seshasai SRK, Kaptoge S, Thompson A, Di Angelantonio E, Gao P, Sarwar N, et al. Diabetes mellitus, fasting glucose, and risk of cause-specific death. The New England journal of medicine. 2011;364(9):829. doi: 10.1056/NEJMoa1008862 21366474

21. Gerstein HC. Glycosylated hemoglobin: finally ready for prime time as a cardiovascular risk factor. Annals of internal medicine. 2004;141(6):475–6. 15381522

22. Kuk JL, Ardern CI. Are metabolically normal but obese individuals at lower risk for all-cause mortality? Diabetes care. 2009;32(12):2297–9. doi: 10.2337/dc09-0574 19729521

23. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL, et al. Seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension. 2003;42(6):1206–52. doi: 10.1161/01.HYP.0000107251.49515.c2 14656957

24. Fox K, Borer JS, Camm AJ, Danchin N, Ferrari R, Sendon JLL, et al. Resting heart rate in cardiovascular disease. Journal of the American College of Cardiology. 2007;50(9):823–30. doi: 10.1016/j.jacc.2007.04.079 17719466

25. Diaz A, Bourassa MG, Guertin M-C, Tardif J-C. Long-term prognostic value of resting heart rate in patients with suspected or proven coronary artery disease. European heart journal. 2005;26(10):967–74. doi: 10.1093/eurheartj/ehi190 15774493

26. Buckley DI, Fu R, Freeman M, Rogers K, Helfand M. C-reactive protein as a risk factor for coronary heart disease: a systematic review and meta-analyses for the US Preventive Services Task Force. Annals of internal medicine. 2009;151(7):483–95. 19805771

27. Ernst E, Resch KL. Fibrinogen as a cardiovascular risk factor: a meta-analysis and review of the literature. Annals of Internal Medicine. 1993;118(12):956–63. 8489110

28. Shlipak MG, Sarnak MJ, Katz R, Fried LF, Seliger SL, Newman AB, et al. Cystatin C and the risk of death and cardiovascular events among elderly persons. New England Journal of Medicine. 2005;352(20):2049–60. doi: 10.1056/NEJMoa043161 15901858

29. Consortium CKDP. Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. The Lancet. 2010;375(9731):2073–81.

30. Levey AS, Eckardt KU, Tsukamoto Y, Levin A, Coresh J, Rossert J, et al. Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int. 2005;67(6):2089–100. doi: 10.1111/j.1523-1755.2005.00365.x 15882252.

31. Janssen I, Katzmarzyk PT, Ross R. Body mass index, waist circumference, and health risk: evidence in support of current National Institutes of Health guidelines. Archives of internal medicine. 2002;162(18):2074–9. 12374515

32. Williams DP, Going SB, Lohman TG, Harsha DW, Srinivasan SR, Webber LS, et al. Body fatness and risk for elevated blood pressure, total cholesterol, and serum lipoprotein ratios in children and adolescents. American journal of public health. 1992;82(3):358–63. 1536350

33. Loucks EB, Magnusson KT, Cook S, Rehkopf DH, Ford ES, Berkman LF. Socioeconomic position and the metabolic syndrome in early, middle, and late life: evidence from NHANES 1999–2002. Ann Epidemiol. 2007;17(10):782–90. doi: 10.1016/j.annepidem.2007.05.003 17697786.

34. Rehkopf DH, Berkman LF, Coull B, Krieger N. The non-linear risk of mortality by income level in a healthy population: US National Health and Nutrition Examination Survey mortality follow-up cohort, 1988–2001. BMC Public Health. 2008;8(1):383.

35. Stekhoven DJ, Bühlmann P. MissForest—non-parametric missing value imputation for mixed-type data. Bioinformatics. 2012;28(1):112–8. doi: 10.1093/bioinformatics/btr597 22039212

36. Waljee AK, Mukherjee A, Singal AG, Zhang Y, Warren J, Balis U, et al. Comparison of imputation methods for missing laboratory data in medicine. BMJ open. 2013;3(8):e002847. doi: 10.1136/bmjopen-2013-002847 23906948

37. Braveman PA, Cubbin C, Egerter S, Chideya S, Marchi KS, Metzler M, et al. Socioeconomic status in health research: one size does not fit all. JAMA. 2005;294(22):2879–88. Epub 2005/12/15. 294/22/2879 [pii] doi: 10.1001/jama.294.22.2879 16352796.

38. Von Hippel PT. Regression with missing Ys: An improved strategy for analyzing multiply imputed data. Sociological Methodology. 2007;37(1):83–117.

39. Sullivan TR, Salter AB, Ryan P, Lee KJ. Bias and Precision of the “Multiple Imputation, Then Deletion” Method for Dealing With Missing Outcome Data. American journal of epidemiology. 2015;182(6):528–34. doi: 10.1093/aje/kwv100 26337075

40. Lumley T. Survey: analysis of complex survey samples. R package version 3.28–2. 2012.

41. CDC. Analytic and Reporting Guidelines, The National Health and Nutrition Examination Survey Data Hyattsville: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2005 [cited 2007 October 28]. http://www.cdc.gov/nchs/data/nhanes/nhanes_03_04/nhanes_analytic_guidelines_dec_2005.pdf.

42. Rehkopf DH, Dow WH, Rosero-Bixby L, Lin J, Epel ES, Blackburn EH. Longer leukocyte telomere length in Costa Rica's Nicoya Peninsula: a population-based study. Exp Gerontol. 2013;48(11):1266–73. doi: 10.1016/j.exger.2013.08.005 23988653; PubMed Central PMCID: PMCPMC3819141.

43. Wood S. Generalized Additive Models: An Introduction with R. Carlin BP, Chatfield C, Tanner M, Zidek J, editors. Boca Raton: Chapman & Hall/CRC; 2006.

44. Yaari S, Even-Zohar S, Goldbourt U, Neufeld H. Associations of serum high density lipoprotein and total cholesterol with total, cardiovascular, and cancer mortality in a 7-year prospective study of 10 000 men. The Lancet. 1981;317(8228):1011–5.

45. Needham BL, Rehkopf D, Adler N, Gregorich S, Lin J, Blackburn EH, et al. Leukocyte telomere length and mortality in the National Health and Nutrition Examination Survey, 1999–2002. Epidemiology. 2015;26(4):528–35. doi: 10.1097/EDE.0000000000000299 26039272.

46. Müezzinler A, Zaineddin A, Brenner H. Body mass index and leukocyte telomere length in adults: a systematic review and meta‐analysis. Obesity Reviews. 2014;15(3):192–201. doi: 10.1111/obr.12126 24165286

47. O'Donovan A, Pantell MS, Puterman E, Dhabhar FS, Blackburn EH, Yaffe K, et al. Cumulative inflammatory load is associated with short leukocyte telomere length in the Health, Aging and Body Composition Study. PLoS ONE. 2011;6(5):e19687. doi: 10.1371/journal.pone.0019687 21602933

48. Rode L, Nordestgaard BG, Weischer M, Bojesen SE. Increased body mass index, elevated C-reactive protein, and short telomere length. The Journal of Clinical Endocrinology & Metabolism. 2014;99(9):E1671–E5.

49. Demissie S, Levy D, Benjamin E, Cupples L, Gardner J, Herbert A, et al. Insulin resistance, oxidative stress, hypertension, and leukocyte telomere length in men from the Framingham Heart Study. Aging cell. 2006;5(4):325–30. doi: 10.1111/j.1474-9726.2006.00224.x 16913878

50. Patel CJ, Manrai AK, Corona E, Kohane IS. Systematic correlation of environmental exposure and physiological and self-reported behaviour factors with leukocyte telomere length. International journal of epidemiology. 2016:dyw043.

51. Houben JM, Moonen HJ, van Schooten FJ, Hageman GJ. Telomere length assessment: biomarker of chronic oxidative stress? Free Radical Biology and Medicine. 2008;44(3):235–46. doi: 10.1016/j.freeradbiomed.2007.10.001 18021748

52. Testa R, Olivieri F, Sirolla C, Spazzafumo L, Rippo MR, Marra M, et al. Leukocyte telomere length is associated with complications of type 2 diabetes mellitus. Diabet Med. 2011;28(11):1388–94. doi: 10.1111/j.1464-5491.2011.03370.x 21692845.

53. 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(11):e79993. doi: 10.1371/journal.pone.0079993 24278229; PubMed Central PMCID: PMCPMC3836967.

54. Bonfigli AR, Spazzafumo L, Prattichizzo F, Bonafe M, Mensa E, Micolucci L, et al. Leukocyte telomere length and mortality risk in patients with type 2 diabetes. Oncotarget. 2016. doi: 10.18632/oncotarget.10615 27437767.

55. van der Harst P, Wong LS, de Boer RA, Brouilette SW, van der Steege G, Voors AA, et al. Possible association between telomere length and renal dysfunction in patients with chronic heart failure. The American journal of cardiology. 2008;102(2):207–10. doi: 10.1016/j.amjcard.2008.03.040 18602523

56. Melk A, Ramassar V, Helms LM, Moore R, Rayner D, Solez K, et al. Telomere shortening in kidneys with age. J Am Soc Nephrol. 2000;11(3):444–53. 10703668.

57. Zhao J, Zhu Y, Uppal K, Tran VT, Yu T, Lin J, et al. Metabolic profiles of biological aging in American Indians: the Strong Heart Family Study. Aging (Albany NY). 2014;6(3):176–86. doi: 10.18632/aging.100644 24799415; PubMed Central PMCID: PMCPMC4012935.