Advertisement

European Journal of Epidemiology

, Volume 31, Issue 12, pp 1173–1190 | Cite as

Does smoking influence the physical activity and lung cancer relation? A systematic review and meta-analysis

  • Daniela Schmid
  • Cristian Ricci
  • Gundula Behrens
  • Michael F. Leitzmann
META-ANALYSIS

Abstract

Research suggests an inverse association between physical activity and lung cancer. However, whether the relation is modified by degree of smoking adjustment has not been summarized. We conducted a meta-analysis of physical activity and lung cancer focusing on evaluating whether smoking status and the degree of smoking adjustment influenced the association. Comparing high versus low physical activity levels from 25 observational studies yielded a lung cancer summary relative risk (RR) of 0.79 [95 % confidence interval (CI) = 0.72–0.87], with RRs of 0.87 (95 % CI = 0.80–0.94) for cohort studies and 0.57 (95 % CI = 0.46–0.71) for case–control studies. In further analyses restricted to cohort studies, physical activity was inversely related to lung cancer among former smokers (RR = 0.68, 95 % CI = 0.51–0.90) and current smokers (RR = 0.80, 95 % CI = 0.70–0.90), whereas the association was null among never smokers (RR = 1.05, 95 % CI = 0.78–1.40, p interaction = 0.26). The degree of smoking adjustment did not modify the association (p interaction = 0.73). Physical activity was unrelated to lung cancer among never smokers but it was inversely associated with lung cancer among former and current smokers. Although the physical activity and lung cancer relation was not modified by smoking status or degree of smoking adjustment, residual confounding by smoking remains a possible explanation for the relations observed.

Keywords

Physical activity Lung cancer Meta-analysis 

Notes

Acknowledgments

We thank Dr. Helge Knuettel from the library of the University of Regensburg for his assistance in the literature search.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflicts of interest.

Supplementary material

10654_2016_186_MOESM1_ESM.tif (259 kb)
Supplementary material 1 (TIFF 258 kb)
10654_2016_186_MOESM2_ESM.tif (197 kb)
Supplementary material 2 (TIFF 197 kb)
10654_2016_186_MOESM3_ESM.tif (197 kb)
Supplementary material 3 (TIFF 197 kb)

References

  1. 1.
    Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.CrossRefPubMedGoogle Scholar
  2. 2.
    World Health Organization. Cancer key facts. http://www.who.int/mediacentre/factsheets/fs297/en/. Accessed 10 Dec 2015.
  3. 3.
    Cornfield J, Haenszel W, Hammond EC, Lilienfeld AM, Shimkin MB, Wynder EL. Smoking and lung cancer: recent evidence and a discussion of some questions. 1959. Int J Epidemiol. 2009;38:1175–91.CrossRefPubMedGoogle Scholar
  4. 4.
    Jakes RW, Day NE, Patel B, Khaw KT, Oakes S, Luben R, et al. Physical inactivity is associated with lower forced expiratory volume in 1 second: European prospective investigation into cancer-norfolk prospective population study. Am J Epidemiol. 2002;156:139–47.CrossRefPubMedGoogle Scholar
  5. 5.
    Garcia-Aymerich J, Lange P, Benet M, Schnohr P, Anto JM. Regular physical activity modifies smoking-related lung function decline and reduces risk of chronic obstructive pulmonary disease: a population-based cohort study. Am J Respir Crit Care Med. 2007;175:458–63.CrossRefPubMedGoogle Scholar
  6. 6.
    Cheng YJ, Macera CA, Addy CL, Sy FS, Wieland D, Blair SN. Effects of physical activity on exercise tests and respiratory function. Br J Sports Med. 2003;37:521–8.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Sin DD, Jones RL, Mannino DM, Paul Man SF. Forced expiratory volume in 1 second and physical activity in the general population. Am J Med. 2004;117:270–3.CrossRefPubMedGoogle Scholar
  8. 8.
    Joshua AM, Boyer MJ, Subramanian R, Clarke SJ. Smoking reduction does work: resulting alterations in the incidence and histological subtypes of lung cancer in New South Wales in the last 20 years. Respirology. 2005;10:233–8.CrossRefPubMedGoogle Scholar
  9. 9.
    Tockman MS, Anthonisen NR, Wright EC, Donithan MG. Airways obstruction and the risk for lung cancer. Ann Intern Med. 1987;106:512–8.CrossRefPubMedGoogle Scholar
  10. 10.
    Zhong S, Ma T, Chen L, Chen W, Lv M, Zhang X, et al. Physical activity and risk of lung cancer: a meta-analysis. Clin J Sport Med. 2015;26:173–81.CrossRefGoogle Scholar
  11. 11.
    Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.CrossRefGoogle Scholar
  12. 12.
    Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 6 Feb 2014.
  13. 13.
    Kabat GC, Kim M, Hunt JR, Chlebowski RT, Rohan TE. Body mass index and waist circumference in relation to lung cancer risk in the women’s health initiative. Am J Epidemiol. 2008;168:158–69.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Thune I, Lund E. The influence of physical activity on lung-cancer risk: a prospective study of 81,516 men and women. Int J Cancer. 1997;70:57–62.CrossRefPubMedGoogle Scholar
  15. 15.
    Severson RK, Nomura AM, Grove JS, Stemmermann GN. A prospective analysis of physical activity and cancer. Am J Epidemiol. 1989;130:522–9.PubMedGoogle Scholar
  16. 16.
    Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.CrossRefPubMedGoogle Scholar
  17. 17.
    Egger M. Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRefPubMedGoogle Scholar
  19. 19.
    Albanes D, Blair A, Taylor PR. Physical activity and risk of cancer in the NHANES I population. Am J Public Health. 1989;79:744–50.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Kubik AK, Zatloukal P, Tomasek L, Petruzelka L. Lung cancer risk among Czech women: a case-control study. Prev Med. 2002;34:436–44.CrossRefPubMedGoogle Scholar
  21. 21.
    Lee IM, Sesso HD, Paffenbarger RS Jr. Physical activity and risk of lung cancer. Int J Epidemiol. 1999;28:620–5.CrossRefPubMedGoogle Scholar
  22. 22.
    Pukkala E, Kaprio J, Koskenvuo M, Kujala U, Sarna S. Cancer incidence among Finnish world class male athletes. Int J Sports Med. 2000;21:216–20.CrossRefPubMedGoogle Scholar
  23. 23.
    Sellers TA, Potter JD, Folsom AR. Association of incident lung cancer with family history of female reproductive cancers: the Iowa Women’s Health Study. Genet Epidemiol. 1991;8:199–208.CrossRefPubMedGoogle Scholar
  24. 24.
    Bak H, Christensen J, Thomsen BL, Tjonneland A, Overvad K, Loft S, et al. Physical activity and risk for lung cancer in a Danish cohort. Int J Cancer. 2005;116:439–44.CrossRefPubMedGoogle Scholar
  25. 25.
    Kubik A, Zatloukal P, Tomasek L, Pauk N, Havel L, Dolezal J, et al. Interactions between smoking and other exposures associated with lung cancer risk in women: diet and physical activity. Neoplasma. 2007;54:83–8.PubMedGoogle Scholar
  26. 26.
    Kubik A, Zatloukal P, Tomasek L, Pauk N, Petruzelka L, Plesko I. Lung cancer risk among nonsmoking women in relation to diet and physical activity. Neoplasma. 2004;51:136–43.PubMedGoogle Scholar
  27. 27.
    Kubik A, Zatloukal P, Tomasek L, Kriz J, Petruzelka L, Plesko I. Diet and the risk of lung cancer among women. A hospital-based case-control study. Neoplasma. 2001;48:262–6.PubMedGoogle Scholar
  28. 28.
    Paffenbarger RS Jr, Hyde RT, Wing AL. Physical activity and incidence of cancer in diverse populations: a preliminary report. Am J Clin Nutr. 1987;45:312–7.PubMedGoogle Scholar
  29. 29.
    Knekt P, Raitasalo R, Heliovaara M, Lehtinen V, Pukkala E, Teppo L, et al. Elevated lung cancer risk among persons with depressed mood. Am J Epidemiol. 1996;144:1096–103.CrossRefPubMedGoogle Scholar
  30. 30.
    Potter JD, Sellers TA, Folsom AR, McGovern PG. Alcohol, beer, and lung cancer in postmenopausal women. The Iowa Women’s Health Study. Ann Epidemiol. 1992;2:587–95.CrossRefPubMedGoogle Scholar
  31. 31.
    Paffenbarger RS Jr, Lee IM, Wing AL. The influence of physical activity on the incidence of site-specific cancers in college alumni. Adv Exp Med Biol. 1992;322:7–15.CrossRefPubMedGoogle Scholar
  32. 32.
    Kubik A, Zatloukal P, Tomasek L, Dolezal J, Syllabova L, Kara J, et al. A case-control study of lifestyle and lung cancer associations by histological types. Neoplasma. 2008;55:192–9.PubMedGoogle Scholar
  33. 33.
    Frisch RE, Wyshak G, Albright NL, Albright TE, Schiff I. Lower prevalence of non-reproductive system cancers among female former college athletes. Med Sci Sports Exerc. 1989;21:250–3.CrossRefPubMedGoogle Scholar
  34. 34.
    Alfano CM, Klesges RC, Murray DM, Bowen DJ, McTiernan A, Vander Weg MW, et al. Physical activity in relation to all-site and lung cancer incidence and mortality in current and former smokers. Cancer Epidemiol Biomark Prev. 2004;13:2233–41.Google Scholar
  35. 35.
    Land SR, Liu Q, Wickerham DL, Costantino JP, Ganz PA. Cigarette smoking, physical activity, and alcohol consumption as predictors of cancer incidence among women at high risk of breast cancer in the NSABP P-1 trial. Cancer Epidemiol Biomark Prev. 2014;23:823–32.CrossRefGoogle Scholar
  36. 36.
    Huang XE, Hirose K, Wakai K, Matsuo K, Ito H, Xiang J, et al. Comparison of lifestyle risk factors by family history for gastric, breast, lung and colorectal cancer. Asian Pac J Cancer Prev. 2004;5:419–27.PubMedGoogle Scholar
  37. 37.
    Laukkanen JA, Pukkala E, Rauramaa R, Makikallio TH, Toriola AT, Kurl S. Cardiorespiratory fitness, lifestyle factors and cancer risk and mortality in Finnish men. Eur J Cancer. 2010;46:355–63.CrossRefPubMedGoogle Scholar
  38. 38.
    Robsahm TE, Hestvik UE, Veierod MB, Fagerlie A, Nystad W, Engebretsen L, et al. Cancer risk in Norwegian world class athletes. Cancer Causes Control. 2010;21:1711–9.CrossRefPubMedGoogle Scholar
  39. 39.
    Soll-Johanning H, Bach E. Occupational exposure to air pollution and cancer risk among Danish urban mail carriers. Int Arch Occup Environ Health. 2004;77:351–6.CrossRefPubMedGoogle Scholar
  40. 40.
    Pukkala E, Poskiparta M, Apter D, Vihko V. Life-long physical activity and cancer risk among Finnish female teachers. Eur J Cancer Prev. 1993;2:369–76.CrossRefPubMedGoogle Scholar
  41. 41.
    Hallmarker U, James S, Michaelsson K, Arnlov J, Sandin F, Holmberg L. Cancer incidence in participants in a long-distance ski race (Vasaloppet, Sweden) compared to the background population. Eur J Cancer. 2015;51:558–68.CrossRefPubMedGoogle Scholar
  42. 42.
    Dosemeci M, Hayes RB, Vetter R, Hoover RN, Tucker M, Engin K, et al. Occupational physical activity, socioeconomic status, and risks of 15 cancer sites in Turkey. Cancer Causes Control. 1993;4:313–21.CrossRefPubMedGoogle Scholar
  43. 43.
    Brownson RC, Chang JC, Davis JR, Smith CA. Physical activity on the job and cancer in Missouri. Am J Pub Health. 1991;81:639–42.CrossRefGoogle Scholar
  44. 44.
    Colbert LH, Hartman TJ, Tangrea JA, Pietinen P, Virtamo J, Taylor PR, et al. Physical activity and lung cancer risk in male smokers. Int J Cancer. 2002;98:770–3.CrossRefPubMedGoogle Scholar
  45. 45.
    Inoue M, Yamamoto S, Kurahashi N, Iwasaki M, Sasazuki S, Tsugane S, et al. Daily total physical activity level and total cancer risk in men and women: results from a large-scale population-based cohort study in Japan. Am J Epidemiol. 2008;168:391–403.CrossRefPubMedGoogle Scholar
  46. 46.
    Lam TK, Moore SC, Brinton LA, Smith L, Hollenbeck AR, Gierach GL, et al. Anthropometric measures and physical activity and the risk of lung cancer in never-smokers: a prospective cohort study. PLoS One. 2013;8:e70672.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Lee IM, Paffenbarger RS Jr. Physical activity and its relation to cancer risk: a prospective study of college alumni. Med Sci Sports Exerc. 1994;26:831–7.CrossRefPubMedGoogle Scholar
  48. 48.
    Leitzmann MF, Koebnick C, Abnet CC, Freedman ND, Park Y, Hollenbeck A, et al. Prospective study of physical activity and lung cancer by histologic type in current, former, and never smokers. Am J Epidemiol. 2009;169:542–53.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Park S, Nam BH, Yang HR, Lee JA, Lim H, Han JT, et al. Individualized risk prediction model for lung cancer in Korean men. PLoS One. 2013;8:e54823.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Pletnikoff PP, Tuomainen TP, Laukkanen JA, Kauhanen J, Rauramaa R, Ronkainen K, et al. Cardiorespiratory fitness and lung cancer risk: a prospective population-based cohort study. J Sci Med Sport. 2015;19:98–102.CrossRefPubMedGoogle Scholar
  51. 51.
    Rundle A, Richie J, Steindorf K, Peluso M, Overvad K, Raaschou-Nielsen O, et al. Physical activity and lung cancer among non-smokers: a pilot molecular epidemiological study within EPIC. Biomarkers. 2010;15:20–30.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Schnohr P, Gronbaek M, Petersen L, Hein HO, Sorensen TI. Physical activity in leisure-time and risk of cancer: 14-year follow-up of 28,000 Danish men and women. Scand J Public Health. 2005;33:244–9.CrossRefPubMedGoogle Scholar
  53. 53.
    Sinner P, Folsom AR, Harnack L, Eberly LE, Schmitz KH. The association of physical activity with lung cancer incidence in a cohort of older women: the Iowa Women’s Health Study. Cancer Epidemiol Biomark Prev. 2006;15:2359–63.CrossRefGoogle Scholar
  54. 54.
    Sprague BL, Trentham-Dietz A, Klein BE, Klein R, Cruickshanks KJ, Lee KE, et al. Physical activity, white blood cell count, and lung cancer risk in a prospective cohort study. Cancer Epidemiol Biomark Prev. 2008;17:2714–22.CrossRefGoogle Scholar
  55. 55.
    Sormunen J, Backmand HM, Sarna S, Kujala UM, Kaprio J, Dyba T, et al. Lifetime physical activity and cancer incidence–a cohort study of male former elite athletes in Finland. J Sci Med Sport. 2014;17:479–84.CrossRefPubMedGoogle Scholar
  56. 56.
    Steenland K, Nowlin S, Palu S. Cancer incidence in the national health and nutrition survey I. Follow-up data: diabetes, cholesterol, pulse and physical activity. Cancer Epidemiol Biomark Prev. 1995;4:807–11.Google Scholar
  57. 57.
    Steindorf K, Friedenreich C, Linseisen J, Rohrmann S, Rundle A, Veglia F, et al. Physical activity and lung cancer risk in the European prospective investigation into cancer and nutrition cohort. Int J Cancer. 2006;119:2389–97.CrossRefPubMedGoogle Scholar
  58. 58.
    Wannamethee SG, Shaper AG, Walker M. Physical activity and risk of cancer in middle-aged men. Br J Cancer. 2001;85:1311–6.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Yun YH, Lim MK, Won YJ, Park SM, Chang YJ, Oh SW, et al. Dietary preference, physical activity, and cancer risk in men: national health insurance corporation study. BMC Cancer. 2008;8(366):17. doi: 10.1186/1471-2407-8-366.Google Scholar
  60. 60.
    Brizio ML, Hallal PC, Lee IM, Domingues MR. Physical activity and lung cancer: a case-control study in Brazil. J Phys Act Health. 2015;13:257–61.CrossRefPubMedGoogle Scholar
  61. 61.
    Kubik AK, Zatloukal P, Tomasek L, Pauk N, Havel L, Krepela E, et al. Dietary habits and lung cancer risk among non-smoking women. Eur J Cancer Prev. 2004;13:471–80.CrossRefPubMedGoogle Scholar
  62. 62.
    Lin Y, Cai L. Environmental and dietary factors and lung cancer risk among Chinese women: a case-control study in southeast China. Nutr Cancer. 2012;64:508–14.CrossRefPubMedGoogle Scholar
  63. 63.
    Mao Y, Pan S, Wen SW, Johnson KC. Canadian cancer registries epidemiology research G. Physical activity and the risk of lung cancer in Canada. Am J Epidemiol. 2003;158:564–75.CrossRefPubMedGoogle Scholar
  64. 64.
    Parent ME, Rousseau MC, El-Zein M, Latreille B, Desy M, Siemiatycki J. Occupational and recreational physical activity during adult life and the risk of cancer among men. Cancer Epidemiol. 2011;35:151–9.CrossRefPubMedGoogle Scholar
  65. 65.
    Schmidt A, Jung J, Ernstmann N, Driller E, Neumann M, Staratschek-Jox A, et al. The association between active participation in a sports club, physical activity and social network on the development of lung cancer in smokers: a case-control study. BMC Res Notes. 2012;5(2):9. doi: 10.1186/1756-0500-5-2.Google Scholar
  66. 66.
    Kaczynski AT, Manske SR, Mannell RC, Grewal K. Smoking and physical activity: a systematic review. Am J Health Behav. 2008;32:93–110.CrossRefPubMedGoogle Scholar
  67. 67.
    Yu H, Rohan T. Role of the insulin-like growth factor family in cancer development and progression. J Natl Cancer Inst. 2000;92:1472–89.CrossRefPubMedGoogle Scholar
  68. 68.
    Covas MI, Elosua R, Fito M, Alcantara M, Coca L, Marrugat J. Relationship between physical activity and oxidative stress biomarkers in women. Med Sci Sports Exerc. 2002;34:814–9.CrossRefPubMedGoogle Scholar
  69. 69.
    Elosua R, Molina L, Fito M, Arquer A, Sanchez-Quesada JL, Covas MI, et al. Response of oxidative stress biomarkers to a 16-week aerobic physical activity program, and to acute physical activity, in healthy young men and women. Atherosclerosis. 2003;167:327–34.CrossRefPubMedGoogle Scholar
  70. 70.
    McTiernan A. Mechanisms linking physical activity with cancer. Nat Rev Cancer. 2008;8:205–11.CrossRefPubMedGoogle Scholar
  71. 71.
    Shen H, Spitz MR, Qiao Y, Guo Z, Wang LE, Bosken CH, et al. Smoking, DNA repair capacity and risk of nonsmall cell lung cancer. Int J Cancer. 2003;107:84–8.CrossRefPubMedGoogle Scholar
  72. 72.
    Ryberg D, Hewer A, Phillips DH, Haugen A. Different susceptibility to smoking-induced DNA damage among male and female lung cancer patients. Cancer Res. 1994;54:5801–3.PubMedGoogle Scholar
  73. 73.
    Woods JA, Davis JM, Smith JA, Nieman DC. Exercise and cellular innate immune function. Med Sci Sports Exerc. 1999;31:57–66.CrossRefPubMedGoogle Scholar
  74. 74.
    Purdue MP, Gold L, Jarvholm B, Alavanja MC, Ward MH, Vermeulen R. Impaired lung function and lung cancer incidence in a cohort of Swedish construction workers. Thorax. 2007;62:51–6.CrossRefPubMedGoogle Scholar
  75. 75.
    Sun JY, Shi L, Gao XD, Xu SF. Physical activity and risk of lung cancer: a meta-analysis of prospective cohort studies. Asian Pac J Cancer Prev. 2012;13:3143–7.CrossRefPubMedGoogle Scholar
  76. 76.
    Buffart LM, Singh AS, van Loon EC, Vermeulen HI, Brug J, Chinapaw MJ. Physical activity and the risk of developing lung cancer among smokers: a meta-analysis. J Sci Med Sport. 2014;17:67–71.CrossRefPubMedGoogle Scholar
  77. 77.
    Tardon A, Lee WJ, Delgado-Rodriguez M, Dosemeci M, Albanes D, Hoover R, et al. Leisure-time physical activity and lung cancer: a meta-analysis. Cancer Causes Control. 2005;16:389–97.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    World Health Organization. Global recommendations on physical activity for health. 2010. http://whqlibdoc.who.int/publications/2010/9789241599979_eng.pdf. Accessed 09 May 2016.

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Daniela Schmid
    • 1
  • Cristian Ricci
    • 1
  • Gundula Behrens
    • 1
  • Michael F. Leitzmann
    • 1
  1. 1.Department of Epidemiology and Preventive MedicineUniversity of RegensburgRegensburgGermany

Personalised recommendations