Skip to main content
SpringerLink
Log in

The association between physical activity and gastroesophageal cancer: systematic review and meta-analysis

  • REVIEW
  • Published:
European Journal of Epidemiology Aims and scope Submit manuscript

Abstract

Physical activity may decrease gastroesophageal cancer risk through a reduction of oxidative stress and decreased chronic inflammation, yet few epidemiologic studies have been able to report a clear inverse association between physical activity and gastroesophageal cancer. Because no meta-analysis has investigated the relation of physical activity to gastroesophageal cancer, we conducted a comprehensive systematic review and meta-analysis according to the PRISMA guidelines based on 24 studies with a total of 15,745 cases. When we compared high versus low physical activity levels and summarized associations according to anatomic site and tumor histology, risk reductions were evident for esophageal adenocarcinoma [relative risk (RR) = 0.79, 95 % confidence interval (CI) = 0.66–0.94], gastric cardia adenocarcinoma (RR = 0.83, 95 % CI = 0.69–0.99) and gastric non-cardia adenocarcinoma (RR = 0.72, 95 % CI = 0.62–0.84). The risk reduction for esophageal squamous cell carcinoma (RR = 0.94, 95 % CI = 0.41–2.16) became statistically significant (RR = 0.66, 95 % CI = 0.46–0.96) after excluding an influential study. The test for heterogeneity by gastroesophageal cancer subtype was statistically non-significant (p-difference = 0.71). The RR of total gastroesophageal cancer for high versus low physical activity was 0.82 (95 % CI = 0.74–0.90). A dose–response analysis of frequency of physical activity and total gastroesophageal cancer risk revealed that the greatest risk reduction was achieved among those engaging in moderate to vigorous physical activity five times per week (RR = 0.67, 95 % CI = 0.58–0.79). Our results provide support for an inverse relation of physical activity, in particular exercise frequency, to gastroesophageal cancer risk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.

    Article  PubMed  Google Scholar 

  2. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF et al. SEER cancer statistics review, 1975–2010, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2010/, based on November 2012 SEER data submission. 2013.

  3. Hur C, Miller M, Kong CY, Dowling EC, Nattinger KJ, Dunn M, et al. Trends in esophageal adenocarcinoma incidence and mortality. Cancer. 2013;119(6):1149–58.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Cancer Trends Progress Report—2011/2012. Update [database on the Internet]. National Cancer Institute, NIH, DHHS. 2012. Available from: http://progressreport.cancer.gov. Accessed 10 December 2013.

  5. Edgren G, Adami HO, Weiderpass E, Nyren O. A global assessment of the oesophageal adenocarcinoma epidemic. Gut. 2013;62(10):1406–14.

    Article  PubMed  Google Scholar 

  6. Tramacere I, La Vecchia C, Negri E. Tobacco smoking and esophageal and gastric cardia adenocarcinoma: a meta-analysis. Epidemiology. 2011;22(3):344–9.

    Article  PubMed  Google Scholar 

  7. Ladeiras-Lopes R, Pereira AK, Nogueira A, Pinheiro-Torres T, Pinto I, Santos-Pereira R, et al. Smoking and gastric cancer: systematic review and meta-analysis of cohort studies. Cancer Causes Control. 2008;19(7):689–701.

    Article  PubMed  Google Scholar 

  8. Islami F, Fedirko V, Tramacere I, Bagnardi V, Jenab M, Scotti L, et al. Alcohol drinking and esophageal squamous cell carcinoma with focus on light-drinkers and never-smokers: a systematic review and meta-analysis. Int J Cancer. 2011;129(10):2473–84.

    Article  PubMed  CAS  Google Scholar 

  9. Mahjub H, Sadri G. Association between alcohol consumption and gastric cancer: a meta-analysis. J Res Health Sci. 2007;7(2):63–72.

    PubMed  CAS  Google Scholar 

  10. Coleman HG, Murray LJ, Hicks B, Bhat SK, Kubo A, Corley DA, et al. Dietary fiber and the risk of precancerous lesions and cancer of the esophagus: a systematic review and meta-analysis. Nutr Rev. 2013;71(7):474–82.

    Article  PubMed  Google Scholar 

  11. Zhang Z, Xu G, Ma M, Yang J, Liu X. Dietary fiber intake reduces risk for gastric cancer: a meta-analysis. Gastroenterology. 2013;145(1):113 e3–20 e3.

    Google Scholar 

  12. Zhu H, Yang X, Zhang C, Zhu C, Tao G, Zhao L, et al. Red and processed meat intake is associated with higher gastric cancer risk: a meta-analysis of epidemiological observational studies. PLoS ONE. 2013;8(8):e70955.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  13. Choi Y, Song S, Song Y, Lee JE. Consumption of red and processed meat and esophageal cancer risk: meta-analysis. World J Gastroenterol. 2013;19(7):1020–9.

    Article  PubMed Central  PubMed  Google Scholar 

  14. Turati F, Tramacere I, La Vecchia C, Negri E. A meta-analysis of body mass index and esophageal and gastric cardia adenocarcinoma. Ann Oncol. 2013;24(3):609–17.

    Article  PubMed  CAS  Google Scholar 

  15. Huang W, Ren H, Ben Q, Cai Q, Zhu W, Li Z. Risk of esophageal cancer in diabetes mellitus: a meta-analysis of observational studies. Cancer Causes Control. 2012;23(2):263–72.

    Article  PubMed  Google Scholar 

  16. Yoon JM, Son KY, Eom CS, Durrance D, Park SM. Pre-existing diabetes mellitus increases the risk of gastric cancer: a meta-analysis. World J Gastroenterol. 2013;19(6):936–45.

    Article  PubMed Central  PubMed  Google Scholar 

  17. Lam TH, Ho SY, Hedley AJ, Mak KH, Leung GM. Leisure time physical activity and mortality in Hong Kong: case-control study of all adult deaths in 1998. Ann Epidemiol. 2004;14(6):391–8.

    Article  PubMed  Google Scholar 

  18. Ibiebele TI, Hughes MC, Whiteman DC, Webb PM. Dietary patterns and risk of oesophageal cancers: a population-based case-control study. Br J Nutr. 2012;107(8):1207–16.

    Article  PubMed  CAS  Google Scholar 

  19. 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(2):151–9.

    Article  PubMed  Google Scholar 

  20. Etemadi A, Golozar A, Kamangar F, Freedman ND, Shakeri R, Matthews C, et al. Large body size and sedentary lifestyle during childhood and early adulthood and esophageal squamous cell carcinoma in a high-risk population. Ann Oncol. 2012;23(6):1593–600.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  21. Jessri M, Rashidkhani B, Hajizadeh B, Jessri M, Kreiger N, Bajdik CD. Adherence to dietary recommendations and risk of esophageal squamous cell carcinoma: a case-control study in Iran. Ann Nutr Metab. 2011;59(2–4):166–75.

    Article  PubMed  CAS  Google Scholar 

  22. Brownson RC, Chang JC, Davis JR, Smith CA. Physical activity on the job and cancer in Missouri. Am J Public Health. 1991;81(5):639–42.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  23. Huerta JM, Navarro C, Chirlaque MD, Tormo MJ, Steindorf K, Buckland G, et al. Prospective study of physical activity and risk of primary adenocarcinomas of the oesophagus and stomach in the EPIC (European Prospective Investigation into Cancer and nutrition) cohort. Cancer Causes Control. 2010;21(5):657–69.

    Article  PubMed  Google Scholar 

  24. Leitzmann MF, Koebnick C, Freedman ND, Park Y, Ballard-Barbash R, Hollenbeck A, et al. Physical activity and esophageal and gastric carcinoma in a large prospective study. Am J Prev Med. 2009;36(2):112–9.

    Article  PubMed Central  PubMed  Google Scholar 

  25. Vigen C, Bernstein L, Wu AH. Occupational physical activity and risk of adenocarcinomas of the esophagus and stomach. Int J Cancer. 2006;118(4):1004–9.

    Article  PubMed  CAS  Google Scholar 

  26. Wannamethee SG, Shaper AG, Walker M. Physical activity and risk of cancer in middle-aged men. Br J Cancer. 2001;85(9):1311–6.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. 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.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Dar NA, Shah IA, Bhat GA, Makhdoomi MA, Iqbal B, Rafiq R, et al. Socioeconomic status and esophageal squamous cell carcinoma risk in Kashmir, India. Cancer Sci. 2013;104(9):1231–6.

    Article  PubMed  CAS  Google Scholar 

  29. Campbell PT, Sloan M, Kreiger N. Physical activity and stomach cancer risk: the influence of intensity and timing during the lifetime. Eur J Cancer. 2007;43(3):593–600.

    Article  PubMed  Google Scholar 

  30. 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(4):419–27.

    PubMed  Google Scholar 

  31. Inoue M, Yamamoto S, Kurahashi N, Iwasaki M, Sasazuki S, Tsugane S. 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(4):391–403.

    Article  PubMed  Google Scholar 

  32. Wen XY. Salt taste sensitivity, physical activity and gastric cancer. Asian Pac J Cancer Prev. 2010;11(6):1473–7.

    PubMed  Google Scholar 

  33. Batty GD, Shipley MJ, Kivimaki M, Marmot M. Davey Smith G. Walking pace, leisure time physical activity, and resting heart rate in relation to disease-specific mortality in London: 40 years follow-up of the original Whitehall study. An update of our work with professor Jerry N. Morris (1910–2009). Ann Epidemiol. 2010;20(9):661–9.

    Article  PubMed  Google Scholar 

  34. Boccia S, Persiani R, La Torre G, Rausei S, Arzani D, Gianfagna F, et al. Sulfotransferase 1A1 polymorphism and gastric cancer risk: a pilot case-control study. Cancer Lett. 2005;229(2):235–43.

    Article  PubMed  CAS  Google Scholar 

  35. 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(4):313–21.

    Article  PubMed  CAS  Google Scholar 

  36. 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(1 Suppl):312–7.

    PubMed  Google Scholar 

  37. Severson RK, Nomura AM, Grove JS, Stemmermann GN. A prospective analysis of physical activity and cancer. Am J Epidemiol. 1989;130(3):522–9.

    PubMed  CAS  Google Scholar 

  38. Sjödahl K, Jia C, Vatten L, Nilsen T, Hveem K, Lagergren J. Body mass and physical activity and risk of gastric cancer in a population-based cohort study in Norway. Cancer Epidemiol Biomarkers Prev. 2008;17(1):135–40.

    Article  PubMed  Google Scholar 

  39. Suwanrungruang K, Sriamporn S, Wiangnon S, Rangsrikajee D, Sookprasert A, Thipsuntornsak N, et al. Lifestyle-related risk factors for stomach cancer in northeast Thailand. Asian Pac J Cancer Prev. 2008;9(1):71–5.

    PubMed  Google Scholar 

  40. Watabe K, Nishi M, Miyake H, Hirata K. Lifestyle and gastric cancer: a case-control study. Oncol Rep. 1998;5(5):1191–4.

    PubMed  CAS  Google Scholar 

  41. Pennathur A, Gibson MK, Jobe BA, Luketich JD. Oesophageal carcinoma. Lancet. 2013;381(9864):400–12.

    Article  PubMed  Google Scholar 

  42. Gonzalez CA, Agudo A. Carcinogenesis, prevention and early detection of gastric cancer: where we are and where we should go. Int J Cancer. 2012;130(4):745–53.

    Article  PubMed  CAS  Google Scholar 

  43. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.

    Article  PubMed Central  PubMed  Google Scholar 

  44. Batty GD, Shipley MJ, Marmot M, Smith GD. Physical activity and cause-specific mortality in men: further evidence from the Whitehall study. Eur J Epidemiol. 2001;17(9):863–9.

    Article  PubMed  CAS  Google Scholar 

  45. Davey Smith G, Shipley MJ, Batty GD, Morris JN, Marmot M. Physical activity and cause-specific mortality in the Whitehall study. Public Health. 2000;114(5):308–15.

    Google Scholar 

  46. Arem H, Moore SC, Park Y, Ballard-Barbash R, Hollenbeck A, Leitzmann M et al. Physical activity and cancer-specific mortality in the NIH-AARP diet and health study cohort. Int J Cancer. 2013. doi:10.1002/ijc.28659.

  47. Monninkhof EM, Elias SG, Vlems FA, van der Tweel I, Schuit AJ, Voskuil DW, et al. Physical activity and breast cancer: a systematic review. Epidemiology. 2007;18(1):137–57.

    Article  PubMed  Google Scholar 

  48. Behrens G, Leitzmann MF. The association between physical activity and renal cancer: systematic review and meta-analysis. Br J Cancer. 2013;108(4):798–811.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  49. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.

    Article  PubMed  Google Scholar 

  50. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088–101.

    Article  PubMed  CAS  Google Scholar 

  51. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  52. Rota M, Bellocco R, Scotti L, Tramacere I, Jenab M, Corrao G, et al. Random-effects meta-regression models for studying nonlinear dose-response relationship, with an application to alcohol and esophageal squamous cell carcinoma. Stat Med. 2010;29(26):2679–87.

    Article  PubMed  Google Scholar 

  53. R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria: 2011.

  54. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36(3):1–48.

    Google Scholar 

  55. Gasparrini A, Armstrong B, Kenward MG. Multivariate meta-analysis for non-linear and other multi-parameter associations. Stat Med. 2012;31(29):3821–39.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  56. Cavaleiro-Pinto M, Peleteiro B, Lunet N, Barros H. Helicobacter pylori infection and gastric cardia cancer: systematic review and meta-analysis. Cancer Causes Control. 2011;22(3):375–87.

    Article  PubMed  Google Scholar 

  57. Kim JJ. Upper gastrointestinal cancer and reflux disease. J Gastric Cancer. 2013;13(2):79–85.

    Article  PubMed Central  PubMed  Google Scholar 

  58. Conteduca V, Sansonno D, Ingravallo G, Marangi S, Russi S, Lauletta G, et al. Barrett’s esophagus and esophageal cancer: an overview. Int J Oncol. 2012;41(2):414–24.

    PubMed  CAS  Google Scholar 

  59. Bosetti C, Rosato V, Gallus S, Cuzick J, La Vecchia C. Aspirin and cancer risk: a quantitative review to 2011. Ann Oncol. 2012;23(6):1403–15.

    Article  PubMed  CAS  Google Scholar 

  60. Abnet CC, Freedman ND, Kamangar F, Leitzmann MF, Hollenbeck AR, Schatzkin A. Non-steroidal anti-inflammatory drugs and risk of gastric and oesophageal adenocarcinomas: results from a cohort study and a meta-analysis. Br J Cancer. 2009;100(3):551–7.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  61. Kasapis C, Thompson PD. The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol. 2005;45(10):1563–9.

    Article  PubMed  CAS  Google Scholar 

  62. Rosenthal M, Haskell WL, Solomon R, Widstrom A, Reaven GM. Demonstration of a relationship between level of physical training and insulin-stimulated glucose utilization in normal humans. Diabetes. 1983;32(5):408–11.

    Article  PubMed  CAS  Google Scholar 

  63. Eliakim A, Brasel JA, Mohan S, Barstow TJ, Berman N, Cooper DM. Physical fitness, endurance training, and the growth hormone-insulin-like growth factor I system in adolescent females. J Clin Endocrinol Metab. 1996;81(11):3986–92.

    PubMed  CAS  Google Scholar 

  64. Eliakim A, Brasel JA, Mohan S, Wong WL, Cooper DM. Increased physical activity and the growth hormone-IGF-I axis in adolescent males. Am J Physiol. 1998;275(1 Pt 2):R308–14.

    PubMed  CAS  Google Scholar 

  65. Miyazaki H, Oh-ishi S, Ookawara T, Kizaki T, Toshinai K, Ha S, et al. Strenuous endurance training in humans reduces oxidative stress following exhausting exercise. Eur J Appl Physiol. 2001;84(1–2):1–6.

    Article  PubMed  CAS  Google Scholar 

  66. Cash SW, Beresford SA, Vaughan TL, Heagerty PJ, Bernstein L, White E et al. Recent physical activity in relation to DNA damage and repair using the comet assay. J Phys Act Health. 2013;PMID:23574930.

    Google Scholar 

  67. Steevens J, Schouten LJ, Goldbohm RA, van den Brandt PA. Alcohol consumption, cigarette smoking and risk of subtypes of oesophageal and gastric cancer: a prospective cohort study. Gut. 2010;59(1):39–48.

    Article  PubMed  CAS  Google Scholar 

  68. Tramacere I, Pelucchi C, Bagnardi V, Rota M, Scotti L, Islami F, et al. A meta-analysis on alcohol drinking and esophageal and gastric cardia adenocarcinoma risk. Ann Oncol. 2012;23(2):287–97.

    Article  PubMed  CAS  Google Scholar 

  69. Islami F, Ren JS, Taylor PR, Kamangar F. Pickled vegetables and the risk of oesophageal cancer: a meta-analysis. Br J Cancer. 2009;101(9):1641–7.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  70. Ren JS, Kamangar F, Forman D, Islami F. Pickled food and risk of gastric cancer—a systematic review and meta-analysis of English and Chinese literature. Cancer Epidemiol Biomarkers Prev. 2012;21(6):905–15.

    Article  PubMed  Google Scholar 

  71. Smith M, Zhou M, Whitlock G, Yang G, Offer A, Hui G, et al. Esophageal cancer and body mass index: results from a prospective study of 220,000 men in China and a meta-analysis of published studies. Int J Cancer. 2008;122(7):1604–10.

    Article  PubMed  CAS  Google Scholar 

  72. Wakui S, Motohashi M, Muto T, Takahashi H, Hano H, Jutabha P, et al. Sex-associated difference in estrogen receptor beta expression in N-methyl-N’-nitro-N-nitrosoguanidine-induced gastric cancers in rats. Comp Med. 2011;61(5):412–8.

    PubMed Central  PubMed  CAS  Google Scholar 

  73. Ueo H, Matsuoka H, Sugimachi K, Kuwano H, Mori M, Akiyoshi T. Inhibitory effects of estrogen on the growth of a human esophageal carcinoma cell line. Cancer Res. 1990;50(22):7212–5.

    PubMed  CAS  Google Scholar 

  74. Green J, Czanner G, Reeves G, Watson J, Wise L, Roddam A, et al. Menopausal hormone therapy and risk of gastrointestinal cancer: nested case-control study within a prospective cohort, and meta-analysis. Int J Cancer. 2012;130(10):2387–96.

    Article  PubMed  CAS  Google Scholar 

  75. Singh S, Edakkanambeth Varayil J, Devanna S, Murad MH, Iyer PG. Physical activity is associated with reduced risk of gastric cancer: a systematic review and meta-analysis. Cancer Prev Res (Phila). 2014;7(1):12–22.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Epidemiology and Preventive Medicine, University of Regensburg, Franz-Josef-Strauss-Allee 11, 93053, Regensburg, Germany

    Gundula Behrens, Carmen Jochem, Marlen Keimling, Cristian Ricci, Daniela Schmid & Michael Fred Leitzmann

Authors
  1. Gundula Behrens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carmen Jochem
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marlen Keimling
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristian Ricci
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniela Schmid
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Fred Leitzmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gundula Behrens.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 164 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Behrens, G., Jochem, C., Keimling, M. et al. The association between physical activity and gastroesophageal cancer: systematic review and meta-analysis. Eur J Epidemiol 29, 151–170 (2014). https://doi.org/10.1007/s10654-014-9895-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-014-9895-2

Keywords

Search

Navigation