Cigarette smoking and telomere length: A systematic review of 84 studies and meta-analysis

Environmental Research

Volumn 158, Issue , 2017, Pages 480-489

  Astuti, Yuliana ^a,b,c   Wardhana, Ardyan ^b,c   Watkins, Johnathan ^c   Wulaningsih, Wahyu ^b,c,d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b GADJAH MADA UNIVERSITY   (Indonesia)

^c Pilar Research and Education   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Ageing; Smoking; Telomere; Telomere length; Tobacco

Indexed keywords

AGING; CHROMOSOME; DOSE-RESPONSE RELATIONSHIP; HETEROGENEITY; LITERATURE REVIEW; META-ANALYSIS; PUBLIC HEALTH; RISK FACTOR; SMOKE; SMOKING;

AGING; APOPTOSIS; ARTICLE; DOSE RESPONSE; HEREDITY; LEUKOCYTE; OXIDATIVE STRESS; PRIORITY JOURNAL; SENESCENCE; SENSITIVITY ANALYSIS; SMOKING; SMOKING CESSATION; TELOMERE LENGTH; ADVERSE EFFECTS; DRUG EFFECTS; HUMAN; META ANALYSIS; PASSIVE SMOKING; RISK FACTOR; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING;

NICOTIANA TABACUM;

PASSIVE SMOKING;

HUMANS; RISK FACTORS; SMOKING; TELOMERE HOMEOSTASIS; TELOMERE SHORTENING; TOBACCO SMOKE POLLUTION;

EID: 85022030679     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2017.06.038     Document Type: Article

References (68)

1. Akbar, A.N., Vukmanovic-Stejic, M., Telomerase in T lymphocytes: use it and lose it?. J. Immunol. 178 (2007), 6689–6694.
2. Alexandrov, K., Rojas, M., Rolando, C., DNA damage by benzo(a)pyrene in human cells is increased by cigarette smoke and decreased by a filter containing rosemary extract, which lowers free radicals. Cancer Res. 66 (2006), 11938–11945, 10.1158/0008-5472.CAN-06-3277.
3. Alexandrov, L.B., Ju, Y.S., Haase, K., Van Loo, P., Martincorena, I., Nik-Zainal, S., Totoki, Y., Fujimoto, A., Nakagawa, H., Shibata, T., Campbell, P.J., Vineis, P., Phillips, D.H., Stratton, M.R., Mutational signatures associated with tobacco smoking in human cancer. Science 354:80- (2016), 618–622, 10.1126/science.aag0299.
4. Arheart, K.L., Lee, D.J., Fleming, L.E., LeBlanc, W.G., Dietz, N. a., McCollister, K.E., Wilkinson, J.D., Lewis, J.E., Clark, J.D., Davila, E.P., Bandiera, F.C., Erard, M.J., Accuracy of self-reported smoking and secondhand smoke exposure in the US workforce: the National Health and Nutrition Examination Surveys. J. Occup. Environ. Med., 50, 2008, 1414–1420, 10.1097/JOM.0b013e318188b90a.
5. Asami, S., Hirano, T., Yamaguchi, R., Tomioka, Y., Itoh, H., Kasai, H., Increase of a type of oxidative DNA damage, 8-hydroxyguanine, and its repair activity in human leukocytes by cigarette smoking. Cancer Res. 56 (1996), 2546–2549.
6. Aviv, A., Chen, W., Gardner, J.P., Kimura, M., Brimacombe, M., Cao, X., Srinivasan, S.R., Berenson, G.S., Leukocyte telomere dynamics: longitudinal findings among young adults in the Bogalusa heart study. Am. J. Epidemiol. 169 (2009), 323–329, 10.1093/aje/kwn338.
7. Aviv, A., Hunt, S.C., Lin, J., Cao, X., Kimura, M., Blackburn, E., Impartial comparative analysis of measurement of leukocyte telomere length/DNA content by Southern blots and qPCR. Nucleic Acids Res., 39, 2011, 10.1093/nar/gkr634.
8. Bernadotte, A., Mikhelson, V.M., Spivak, I.M., Markers of cellular senescence. Telomere shortening as a marker of cellular senescence. Aging (Albany NY) 8 (2016), 3–11, 10.18632/aging.100871.
9. Blackburn, E.H., Switching and signaling at the telomere. Cell 106 (2001), 661–673, 10.1016/S0092-8674(01)00492-5.
10. Block, G., Dietrich, M., Norkus, E., Jensen, C., Benowitz, N.L., Morrow, J.D., Hudes, M., Packer, L., Intraindividual variability of plasma antioxidants, markers of oxidative stress, C-reactive protein, cotinine, and other biomarkers. Epidemiol. (Camb., Mass) 17 (2006), 404–412, 10.1097/01.ede.0000220655.53323.e9.
11. Broer, L., Codd, V., Nyholt, D.R., Deelen, J., Mangino, M., Willemsen, G., Albrecht, E., Amin, N., Beekman, M., de Geus, E.J.C., Henders, A., Nelson, C.P., Steves, C.J., Wright, M.J., de Craen, A.J.M., Isaacs, A., Matthews, M., Moayyeri, A., Montgomery, G.W., Oostra, B.A., Vink, J.J.M., Spector, T.D., Slagboom, P.E., Martin, N.G., Samani, N.J., van Duijn, C.M., Boomsma, D.I., Meta-analysis of telomere length in 19 713 subjects reveals high heritability, stronger maternal inheritance and a paternal age effect. Eur. J. Hum. Genet. 21 (2013), 1163–1168, 10.1038/ejhg.2012.303.
12. Brouilette, S., Singh, R.K., Thompson, J.R., Goodall, A.H., Samani, N.J., White cell telomere length and risk of premature myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 23 (2003), 842–846, 10.1161/01.ATV.0000067426.96344.32.
13. Cech, T.R., Beginning to Understand the End of the Chromosome. Mod. Biopharm. Des. Dev. Optim. 1 (2008), 36–48, 10.1002/9783527620982.ch1.
14. Chen, W., Kimura, M., Kim, S., Cao, X., Srinivasan, S.R., Berenson, G.S., Kark, J.D., Aviv, A., 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. 66 A (2011), 312–319, 10.1093/gerona/glq223.
15. Crippa, A., Orsini, N., Dose-response meta-analysis of differences in means. BMC Med. Res. Methodol., 16, 2016, 91, 10.1186/s12874-016-0189-0.
16. Critical Appraisal Skills Programme, 2017. CASP Systematic Review Checklist. [WWW Document]. URL 〈http://www.casp-uk.net/checklists〉.
17. d'Adda di Fagagna, F., Reaper, P.M., Clay-Farrace, L., Fiegler, H., Carr, P., Von Zglinicki, T., Saretzki, G., Carter, N.P., Jackson, S.P., A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003), 194–198, 10.1038/nature02118.
18. Daniali, L., Benetos, A., Susser, E., Kark, J.D., Labat, C., Kimura, M., Desai, K.K., Granick, M., Aviv, A., Telomeres shorten at equivalent rates in somatic tissues of adults. Nat. Commun., 4, 2013, 1597, 10.1038/ncomms2602.
19. Dlouha, D., Maluskova, J., Kralova Lesna, I., Lanska, V., Hubacek, J.A., Comparison of the relative telomere length measured in leukocytes and eleven different human tissues. Physiol. Res. 63 (2014), S343–S350.
20. Egger, M., Davey Smith, G., Schneider, M., Minder, C., Bias in meta-analysis detected by a simple, graphical test. Br. Med. J. 315 (1997), 629–634, 10.1136/bmj.316.7129.469.
21. Eisenberg, D.T.A., An evolutionary review of human telomere biology: the thrifty telomere hypothesis and notes on potential adaptive paternal effects. Am. J. Hum. Biol. 23 (2011), 149–167, 10.1002/ajhb.21127.
22. Friedrich, U., Griese, E., Schwab, M., Fritz, P., Thon, K., Klotz, U., Telomere length in different tissues of elderly patients. Mech. Ageing Dev. 119 (2000), 89–99, 10.1016/S0047-6374(00)00173-1.
23. Fyhrquist, F., Silventoinen, K., Saijonmaa, O., Kontula, K., Devereux, R.B., de Faire, U., Os, I., Dahlöf, B., Telomere length and cardiovascular risk in hypertensive patients with left ventricular hypertrophy: the LIFE study. J. Hum. Hypertens. 25 (2011), 711–718, 10.1038/jhh.2011.57.
24. Gadalla, S.M., Cawthon, R., Giri, N., Alter, B.P., Savage, S.A., Telomere length in blood, buccal cells, and fibroblasts from patients with inherited bone marrow failure syndromes. Aging (Albany NY). 2 (2010), 867–874.
25. Gardner, M., Bann, D., Wiley, L., Cooper, R., Hardy, R., Nitsch, D., Martin-Ruiz, C., Shiels, P., Sayer, A.A., Barbieri, M., Bekaert, S., Bischoff, C., Brooks-Wilson, A., Chen, W., Cooper, C., Christensen, K., De Meyer, T., Deary, I., Der, G., Roux, A.D., Fitzpatrick, A., Hajat, A., Halaschek-Wiener, J., Harris, S., Hunt, S.C., Jagger, C., Jeon, H.S., Kaplan, R., Kimura, M., Lansdorp, P., Li, C., Maeda, T., Mangino, M., Nawrot, T.S., Nilsson, P., Nordfjall, K., Paolisso, G., Ren, F., Riabowol, K., Robertson, T., Roos, G., Staessen, J.A., Spector, T., Tang, N., Unryn, B., van der Harst, P., Woo, J., Xing, C., Yadegarfar, M.E., Park, J.Y., Young, N., Kuh, D., von Zglinicki, T., Ben-Shlomo, Y., Gender and telomere length: systematic review and meta-analysis. Exp. Gerontol. 51 (2014), 15–27, 10.1016/j.exger.2013.12.004.
26. Greenland, S., Longnecker, M.P., Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am. J. Epidemiol. 135 (1992), 1301–1309.
27. Griffith, J.D., Comeau, L., Rosenfield, S., Stansel, R.M., Bianchi, A., Moss, H., De Lange, T., Mammalian telomeres end in a large duplex loop. Cell 97 (1999), 503–514, 10.1016/S0092-8674(00)80760-6.
28. Harris, S.E., Martin-Ruiz, C., von Zglinicki, T., Starr, J.M., Deary, I.J., Telomere length and aging biomarkers in 70-year-olds: the Lothian Birth Cohort 1936. Neurobiol. Aging 33 (2012), 1486.e3–1486.e8, 10.1016/j.neurobiolaging.2010.11.013.
29. Higgins, J., Greenland, S., 2011. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0. The Cochrane Collaboration.
30. Higgins, J.P.T., Thompson, S.G., Deeks, J.J., Altman, D.G., Measuring inconsistency in meta-analyses. BMJ Br. Med. J. 327 (2003), 557–560, 10.1136/bmj.327.7414.557.
31. Hodes, R.J., Hathcock, K.S., Weng, N., Telomeres in T and B cells. Nat. Rev. Immunol. 2 (2002), 699–706, 10.1038/nri890.
32. Huda, N., Tanaka, H., Herbert, B.S., Reed, T., Gilley, D., Shared environmental factors associated with telomere length maintenance in elderly male twins. Aging Cell 6 (2007), 709–713, 10.1111/j.1474-9726.2007.00330.x.
33. Il'yasova, D., Hertz-Picciotto, I., Peters, U., Berlin, J.A., Poole, C., Choice of exposure scores for categorical regression in meta-analysis: a case study of a common problem. Cancer Causes Control 16 (2005), 383–388, 10.1007/s10552-004-5025-x.
34. Kimura, M., Hjelmborg, J.V.B., Gardner, J.P., Bathum, L., Brimacombe, M., Lu, X., Christiansen, L., Vaupel, J.W., Aviv, A., Christensen, K., Telomere length and mortality: a study of leukocytes in elderly danish twins. Am. J. Epidemiol. 167 (2008), 799–806, 10.1093/aje/kwm380.
35. Kingma, E.M., de Jonge, P., van der Harst, P., Ormel, J., Rosmalen, J.G.M., The Association between Intelligence and Telomere Length: a Longitudinal Population Based Study. PLoS One 7 (2012), 1–6, 10.1371/journal.pone.0049356.
36. Kirkwood, T.B., Holliday, R., 1979. The evolution of ageing and longevity. Proceedings R. Soc. London. Ser. B, Biol. Sci. 205, pp. 531–546.
37. Kuilman, T., Michaloglou, C., Mooi, W.J., Peeper, D.S., The essence of senescence. Genes Dev., 2010, 10.1101/gad.1971610.
38. Lakowa, N., Trieu, N., Flehmig, G., Lohmann, T., Sch??n, M.R., Dietrich, A., Zeplin, P.H., Langer, S., Stumvoll, M., Bl??her, M., Kl??ting, N., Telomere length differences between subcutaneous and visceral adipose tissue in humans. Biochem. Biophys. Res. Commun. 457 (2015), 426–432, 10.1016/j.bbrc.2014.12.122.
39. Lingner, J., Cooper, J., Cech, T., Telomerase and DNA end replication: no longer a lagging strand problem?. Science 269:80- (1995), 1533–1534, 10.1126/science.7545310.
40. Longhese, M.P., DNA damage response at functional and dysfunctional telomeres. Genes Dev. 22 (2008), 125–140, 10.1101/gad.1626908.
41. Martin-Ruiz, C.M., Baird, D., Roger, L., Boukamp, P., Krunic, D., Cawthon, R., Dokter, M.M., Van der Harst, P., Bekaert, S., De Meyer, T., Roos, G., Svenson, U., Codd, V., Samani, N.J., McGlynn, L., Shiels, P.G., Pooley, K.A., Dunning, A.M., Cooper, R., Wong, A., Kingston, A., von Zglinicki, T., Reproducibility of telomere length assessment: an international collaborative study. Int. J. Epidemiol. 44 (2015), 1673–1683, 10.1093/ije/dyu191.
42. Mather, K.A., Jorm, A.F., Parslow, R.A., Christensen, H., Is telomere length a biomarker of aging? A review. J. Gerontol. - Ser. A Biol. Sci. Med. Sci., 2011, 10.1093/gerona/glq180.
43. Mirabello, L., Huang, W.Y., Wong, J.Y.Y., Chatterjee, N., Reding, D., Crawford, E.D., De Vivo, I., Hayes, R.B., Savage, S.A., The association between leukocyte telomere length and cigarette smoking, dietary and physical variables, and risk of prostate cancer. Aging Cell 8 (2009), 405–413, 10.1111/j.1474-9726.2009.00485.x.
44. Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Altman, D.G., Antes, G., Atkins, D., Barbour, V., Barrowman, N., Berlin, J.A., Clark, J., Clarke, M., Cook, D., D'Amico, R., Deeks, J.J., Devereaux, P.J., Dickersin, K., Egger, M., Ernst, E., G??tzsche, P.C., Grimshaw, J., Guyatt, G., Higgins, J., Ioannidis, J.P.A., Kleijnen, J., Lang, T., Magrini, N., McNamee, D., Moja, L., Mulrow, C., Napoli, M., Oxman, A., Pham, B., Rennie, D., Sampson, M., Schulz, K.F., Shekelle, P.G., Tovey, D., Tugwell, P., Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement (Chinese edition). J. Chin. Integr. Med. 7 (2009), 889–896, 10.3736/jcim20090918.
45. Müezzinler, A., Mons, U., Dieffenbach, A.K., Butterbach, K., Saum, K.-U., Schick, M., Stammer, H., Boukamp, P., Holleczek, B., Stegmaier, C., Brenner, H., Smoking habits and leukocyte telomere length dynamics among older adults: results from the ESTHER cohort. Exp. Gerontol. 70 (2015), 18–25, 10.1016/j.exger.2015.07.002.
46. Mundstock, E., Sarria, E.E., Zatti, H., Mattos Louzada, F., Kich Grun, L., Herbert Jones, M., Guma, F.T.C.R., Mazzola, J., Epifanio, M., Stein, R.T., Barbé-Tuana, F.M., Mattiello, R., Effect of obesity on telomere length: systematic review and meta-analysis. Obesity, 2015, 10.1002/oby.21183.
47. Needham, B.L., Adler, N., Gregorich, S., Rehkopf, D., Lin, J., Blackburn, E.H., Epel, E.S., Socioeconomic status, health behavior, and leukocyte telomere length in the National Health and Nutrition Examination Survey, 1999–2002. Soc. Sci. Med. 85 (2013), 1–8, 10.1016/j.socscimed.2013.02.023.
48. Needham, B.L., Rehkopf, D., Adler, N., Gregorich, S., Lin, J., Blackburn, E.H., Epel, E.S., Leukocyte Telomere Length and Mortality in the National Health and Nutrition Examination Survey, 1999–2002. Epidemiology 26 (2015), 528–535, 10.1097/EDE.0000000000000299.
49. Nordfjäll, K., Svenson, U., Norrback, K.F., Adolfsson, R., Lenner, P., Roos, G., The individual blood cell telomere attrition rate is telomere length dependent. PLoS Genet., 5, 2009, 10.1371/journal.pgen.1000375.
50. O'Sullivan, R.J., Karlseder, J., Telomeres: protecting chromosomes against genome instability. Nat. Rev. Mol. Cell Biol. 11 (2010), 171–181, 10.1038/nrm2848.
51. Opresko, P.L., Fan, J., Danzy, S., Wilson, D.M., Bohr, V.A., Oxidative damage in telomeric DNA disrupts recognition by TRF1 and TRF2. Nucleic Acids Res. 33 (2005), 1230–1239, 10.1093/nar/gki273.
52. Patel, C.J., Manrai, A.K., Corona, E., Kohane, I.S., Systematic correlation of environmental exposure and physiological and self-reported behaviour factors with leukocyte telomere length. Int. J. Epidemiol., 2016, 10.1093/ije/dyw043.
53. Revesz, D., Milaneschi, Y., Verhoeven, J.E., Lin, J., Penninx, B.W., Longitudinal associations between metabolic syndrome components and telomere shortening. J. Clin. Endocrinol. Metab. 100 (2015), 3050–3059, 10.1210/jc.2015-1995.
54. Sanders, J.L., Newman, A.B., Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither?. Epidemiol. Rev. 35 (2013), 112–131, 10.1093/epirev/mxs008.
55. Starkweather, A.R., Alhaeeri, A.A., Montpetit, A., Brumelle, J., Filler, K., Montpetit, M., Mohanraj, L., Lyon, D.E., Jackson-Cook, C.K., An integrative review of factors associated with telomere length and implications for biobehavioral research. Nurs. Res. 63 (2014), 36–50, 10.1097/NNR.0000000000000009.
56. Sterne, J.A.C., Sutton, A.J., Ioannidis, J.P.A., Terrin, N., Jones, D.R., Lau, J., Carpenter, J., Rücker, G., Harbord, R.M., Schmid, C.H., Tetzlaff, J., Deeks, J.J., Peters, J., Macaskill, P., Schwarzer, G., Duval, S., Altman, D.G., Moher, D., Higgins, J.P.T., Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ, 343, 2011, d4002, 10.1136/bmj.d4002.
57. Stroup, D.F., Berlin, J.A., Morton, S.C., Olkin, I., Williamson, G.D., Rennie, D., Moher, D., Becker, B.J., Sipe, T.A., Thacker, S.B., Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283 (2000), 2008–2012.
58. Svenson, U., Nordfj??ll, K., Baird, D., Roger, L., Osterman, P., Hellenius, M.L., Roos, G., Blood cell telomere length is a dynamic feature. PLoS One, 2011, 6, 10.1371/journal.pone.0021485.
59. Tellechea, M., Pirola, C., The impact of hypertension on leukocyte telomere length: a systematic review and meta-analysis of human studies. J. Hum. Hypertens. Adv. Online Publ., 2016, 1–7, 10.1038/jhh.2016.45.
60. Thorne, D., Wilson, J., Kumaravel, T.S., Massey, E.D., McEwan, M., Measurement of oxidative DNA damage induced by mainstream cigarette smoke in cultured NCI-H292 human pulmonary carcinoma cells. Mutat. Res. - Genet. Toxicol. Environ. Mutagen. 673 (2009), 3–8, 10.1016/j.mrgentox.2008.11.008.
61. Van Steensel, B., Smogorzewska, A., De Lange, T., TRF2 protects human telomeres from end-to-end fusions. Cell 92 (1998), 401–413, 10.1016/S0092-8674(00)80932-0.
62. Verde, Z., Reinoso-Barbero, L., Chicharro, L., Garatachea, N., Resano, P., Sánchez-Hernández, I., Rodríguez González-Moro, J.M., Bandrés, F., Santiago, C., Gómez-Gallego, F., Effects of cigarette smoking and nicotine metabolite ratio on leukocyte telomere length. Environ. Res. 140 (2015), 488–494, 10.1016/j.envres.2015.05.008.
63. Verdun, R.E., Karlseder, J., Replication and protection of telomeres. Nature 447 (2007), 924–931, 10.1038/nature05976.
64. Von Zglinicki, T., Oxidative stress shortens telomeres. Trends Biochem. Sci., 2002, 10.1016/S0968-0004(02)02110-2.
65. Wallace, B.C., Dahabreh, I.J., Trikalinos, T. a., Lau, J., Trow, P., Schmid, C.H., Closing the gap between methodologists and end-users: R as a computational back-end. J. Stat. Softw. 49 (2012), 1–15, 10.18637/jss.v049.i05.
66. Wang, Y.-Y., Chen, A.-F., Wang, H.-Z., Xie, L.-Y., Sui, K.-X., Zhang, Q.-Y., Association of shorter mean telomere length with large artery stiffness in patients with coronary heart disease. Aging Male 14 (2011), 27–32, 10.3109/13685538.2010.529196.
67. Wulaningsih, W., Serrano, F.E.C., Utarini, A., Matsuguchi, T., Watkins, J., ResearchNetwork, for P, Smoking, second-hand smoke exposure and smoking cessation in relation to leukocyte telomere length and mortality. Oncotarget, 2016, 10.18632/oncotarget.11051.
68. Zhang, C., Lauderdale, D.S., Pierce, B.L., Sex-specific and time-varying associations between cigarette smoking and telomere length among older adults. Am. J. Epidemiol. 184 (2016), 922–932, 10.1093/aje/kww102.