Physical activity is associated with reduced risk of esophageal cancer, particularly esophageal adenocarcinoma: a systematic review and meta-analysis

Siddharth Singh, Swapna Devanna, Jithinraj Edakkanambeth Varayil, Mohammad Hassan Murad, Prasad G Iyer, Siddharth Singh, Swapna Devanna, Jithinraj Edakkanambeth Varayil, Mohammad Hassan Murad, Prasad G Iyer

Abstract

Background: Physical activity has been inversely associated with risk of several cancers. We performed a systematic review and meta-analysis to evaluate the association between physical activity and risk of esophageal cancer (esophageal adenocarcinoma [EAC] and/or esophageal squamous cell carcinoma [ESCC]).

Methods: We conducted a comprehensive search of bibliographic databases and conference proceedings from inception through February 2013 for observational studies that examined associations between recreational and/or occupational physical activity and esophageal cancer risk. Summary adjusted odds ratio (OR) estimates with 95% confidence intervals (CI) were estimated using the random-effects model.

Results: The analysis included 9 studies (4 cohort, 5 case-control) reporting 1,871 cases of esophageal cancer among 1,381,844 patients. Meta-analysis demonstrated that the risk of esophageal cancer was 29% lower among the most physically active compared to the least physically active subjects (OR, 0.71; 95% CI, 0.57-0.89), with moderate heterogeneity (I2 = 47%). On histology-specific analysis, physical activity was associated with a 32% decreased risk of EAC (4 studies, 503 cases of EAC; OR, 0.68; 95% CI, 0.55-0.85) with minimal heterogeneity (I2 = 0%). There were only 3 studies reporting the association between physical activity and risk of ESCC with conflicting results, and the meta-analysis demonstrated a null association (OR, 1.10; 95% CI, 0.21-5.64). The results were consistent across study design, geographic location and study quality, with a non-significant trend towards a dose-response relationship.

Conclusions: Meta-analysis of published observational studies indicates that physical activity may be associated with reduced risk of esophageal adenocarcinoma. Lifestyle interventions focusing on increasing physical activity may decrease the global burden of EAC.

Figures

Figure 1
Figure 1
Flow diagram summarizing study identification and selection.
Figure 2
Figure 2
Physical activity and risk of esophageal cancer.
Figure 3
Figure 3
Physical activity and risk of esophageal adenocarcinoma.

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. doi: 10.3322/caac.20107.
    1. Lagergren J, Lagergren P. Recent developments in esophageal adenocarcinoma. CA Cancer J Clin. 2013;63(4):232–248. doi: 10.3322/caac.21185.
    1. Singh S, Singh AG, Singh PP, Murad MH, Iyer PG. Statins are associated with reduced risk of Esophageal Cancer, particularly in patients with Barrett’s Esophagus: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2013;11(6):620–629. doi: 10.1016/j.cgh.2012.12.036.
    1. Spechler SJ, Sharma P, Souza RF, Inadomi JM, Shaheen NJ. American Gastroenterological Association technical review on the management of Barrett’s esophagus. Gastroenterology. 2011;140(3):e18–e52. doi: 10.1053/j.gastro.2011.01.031. quiz e13.
    1. Liao LM, Vaughan TL, Corley DA, Cook MB, Casson AG, Kamangar F, Abnet CC, Risch HA, Giffen C, Freedman ND, Chow WH, Sadeghi S, Pandeya N, Whiteman DC, Murray LJ, Bernstein L, Gammon MD, Wu AH. Nonsteroidal anti-inflammatory drug use reduces risk of adenocarcinomas of the esophagus and esophagogastric junction in a pooled analysis. Gastroenterology. 2012;142(3):442–452. doi: 10.1053/j.gastro.2011.11.019. e445; quiz e422-443.
    1. Nguyen DM, El-Serag HB, Henderson L, Stein D, Bhattacharyya A, Sampliner RE. Medication usage and the risk of neoplasia in patients with Barrett’s esophagus. Clin Gastroenterol Hepatol. 2009;7(12):1299–1304. doi: 10.1016/j.cgh.2009.06.001.
    1. Research WCRFAIfC. Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective. Washington, DC: American Institute for Cancer Research; 2007.
    1. Boyle T, Keegel T, Bull F, Heyworth J, Fritschi L. Physical activity and risks of proximal and distal colon cancers: a systematic review and meta-analysis. J Natl Cancer Inst. 2012;104(20):1548–1561. doi: 10.1093/jnci/djs354.
    1. Singh PP, Singh S. Statins are associated with reduced risk of gastric cancer: a systematic review and meta-analysis. Ann Oncol. 2013;24(9):1721–1730.
    1. Moore SC, Gierach GL, Schatzkin A, Matthews CE. Physical activity, sedentary behaviours, and the prevention of endometrial cancer. Br J Cancer. 2010;103(7):933–938. doi: 10.1038/sj.bjc.6605902.
    1. Na HK, Oliynyk S. Effects of physical activity on cancer prevention. Ann N Y Acad Sci. 2011;1229:176–183. doi: 10.1111/j.1749-6632.2011.06105.x.
    1. McTiernan A. Mechanisms linking physical activity with cancer. Nat Rev Cancer. 2008;8(3):205–211. doi: 10.1038/nrc2325.
    1. 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):151–159. doi: 10.1016/j.canep.2010.09.004.
    1. Vigen C, Bernstein L, Wu AH. Occupational physical activity and risk of adenocarcinomas of the esophagus and stomach. Int J Cancer. 2006;118(4):1004–1009. doi: 10.1002/ijc.21419.
    1. Huerta JM, Navarro C, Chirlaque MD, Tormo MJ, Steindorf K, Buckland G, Carneiro F, Johnsen NF, Overvad K, Stegger J, Tjønneland A, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Boeing H, Kaaks R, Rohrmann S, Vigl M, Lagiou P, Trichopoulos D, Trichopoulou A, Bas Bueno-de-Mesquita H, Monninkhof EM, Numans ME, Peeters PH, Mattiello A, Pala V, Palli D, Tumino R, Vineis P. 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):657–669. doi: 10.1007/s10552-009-9493-x.
    1. Leitzmann MF, Koebnick C, Freedman ND, Park Y, Ballard-Barbash R, Hollenbeck A, Schatzkin A, Abnet CC. Physical activity and esophageal and gastric carcinoma in a large prospective study. Am J Prev Med. 2009;36(2):112–119. doi: 10.1016/j.amepre.2008.09.033.
    1. Thune I, Furberg AS. Physical activity and cancer risk: dose–response and cancer, all sites and site-specific. Med Sci Sports Exerc. 2001;33(6 Suppl):S530–S550. discussion S609-510.
    1. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–269. doi: 10.7326/0003-4819-151-4-200908180-00135. W264.
    1. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188. doi: 10.1016/0197-2456(86)90046-2.
    1. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560. doi: 10.1136/bmj.327.7414.557.
    1. Guyatt GH, Oxman AD, Kunz R, Woodcock J, Brozek J, Helfand M, Alonso-Coello P, Glasziou P, Jaeschke R, Akl EA, Akl EA, Norris S, Vist G, Dahm P, Shukla VK, Higgins J, Falck-Ytter Y, Schünemann HJ. GRADE Working Group. GRADE guidelines: 7. rating the quality of evidence–inconsistency. J Clin Epidemiol. 2011;64(12):1294–1302. doi: 10.1016/j.jclinepi.2011.03.017.
    1. Sterne JA, Egger M, Smith GD. Systematic reviews in health care: investigating and dealing with publication and other biases in meta-analysis. BMJ. 2001;323(7304):101–105. doi: 10.1136/bmj.323.7304.101.
    1. Wannamethee SG, Shaper AG, Walker M. Physical activity and risk of cancer in middle-aged men. Br J Cancer. 2001;85(9):1311–1316. doi: 10.1054/bjoc.2001.2096.
    1. Yun YH, Lim MK, Won YJ, Park SM, Chang YJ, Oh SW, Shin SA. Dietary preference, physical activity, and cancer risk in men: national health insurance corporation study. BMC Cancer. 2008;8:366. doi: 10.1186/1471-2407-8-366.
    1. Brownson RC, Chang JC, Davis JR, Smith CA. Physical activity on the job and cancer in Missouri. Am J Public Health. 1991;81(5):639–642. doi: 10.2105/AJPH.81.5.639.
    1. Balbuena L, Casson AG. Physical activity, obesity and risk for esophageal adenocarcinoma. Future Oncol. 2009;5(7):1051–1063. doi: 10.2217/fon.09.65.
    1. Etemadi A, Golozar A, Kamangar F, Freedman ND, Shakeri R, Matthews C, Islami F, Boffetta P, Brennan P, Abnet CC, Malekzadeh R, Dawsey SM. 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):1593–1600. doi: 10.1093/annonc/mdr494.
    1. Dar NA, Shah IA, Bhat GA, Makhdoomi MA, Iqbal B, Rafiq R, Nisar I, Bhat AB, Nabi S, Masood A, Shah SA, Lone MM, Zargar SA, Islami F, Boffetta P. Socioeconomic status and esophageal squamous cell carcinoma risk in Kashmir India. Cancer Sci. 2013;104(9):1231–1236. doi: 10.1111/cas.12210.
    1. Gao YT, McLaughlin JK, Blot WJ, Ji BT, Dai Q, Fraumeni JF Jr. Reduced risk of esophageal cancer associated with green tea consumption. J Natl Cancer Inst. 1994;86(11):855–858. doi: 10.1093/jnci/86.11.855.
    1. Whittemore AS, Paffenbarger RS Jr, Anderson K, Lee JE. Early precursors of site-specific cancers in college men and women. J Natl Cancer Inst. 1985;74(1):43–51.
    1. Lagergren J, Bergstrom R, Nyren O. Association between body mass and adenocarcinoma of the esophagus and gastric cardia. Ann Intern Med. 1999;130(11):883–890. doi: 10.7326/0003-4819-130-11-199906010-00003.
    1. Zhang ZF, Kurtz RC, Sun M, Karpeh M Jr, Yu GP, Gargon N, Fein JS, Georgopoulos SK, Harlap S. Adenocarcinomas of the esophagus and gastric cardia: medical conditions, tobacco, alcohol, and socioeconomic factors. Cancer Epidemiol Biomarkers Prev. 1996;5(10):761–768.
    1. Jessri M, Rashidkhani B, Hajizadeh B, Gotay C. Macronutrients, vitamins and minerals intake and risk of esophageal squamous cell carcinoma: a case–control study in Iran. Nutr J. 2011;10:137. doi: 10.1186/1475-2891-10-137.
    1. Hogervorst JG, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA. Dietary acrylamide intake is not associated with gastrointestinal cancer risk. J Nutr. 2008;138(11):2229–2236. doi: 10.3945/jn.108.092957.
    1. PJ DEJ, Wolters LM, Steyerberg EW, Vand H, Kusters JG, Kuipers EJ, Siersema PD. Environmental risk factors in the development of adenocarcinoma of the oesophagus or gastric cardia: a cross-sectional study in a Dutch cohort. Aliment Pharmacol Ther. 2007;26(1):31–39. doi: 10.1111/j.1365-2036.2007.03344.x.
    1. de Jonge PJ, Steyerberg EW, Kuipers EJ, Honkoop P, Wolters LM, Kerkhof M, van Dekken H, Siersema PD. Risk factors for the development of esophageal adenocarcinoma in Barrett’s esophagus. Am J Gastroenterol. 2006;101(7):1421–1429. doi: 10.1111/j.1572-0241.2006.00626.x.
    1. Sundelof M, Lagergren J, Ye W. Patient demographics and lifestyle factors influencing long-term survival of oesophageal cancer and gastric cardia cancer in a nationwide study in Sweden. Eur J Cancer. 2008;44(11):1566–1571. doi: 10.1016/j.ejca.2008.04.002.
    1. Wolin KY, Yan Y, Colditz GA, Lee IM. Physical activity and colon cancer prevention: a meta-analysis. Br J Cancer. 2009;100(4):611–616. doi: 10.1038/sj.bjc.6604917.
    1. Wolin KY, Tuchman H. Physical activity and gastrointestinal cancer prevention. Recent Results Cancer Res. 2011;186:73–100.
    1. Rubenstein JH, Kao JY, Madanick RD, Zhang M, Wang M, Spacek MB, Donovan JL, Bright SD, Shaheen NJ. Association of adiponectin multimers with Barrett’s oesophagus. Gut. 2009;58(12):1583–1589. doi: 10.1136/gut.2008.171553.
    1. Singh S, Sharma AN, Murad MH, Buttar NS, El-Serag HB, Katzka DA, Iyer PG. Central adiposity is associated with increased risk of esophageal inflammation, metaplasia, and adenocarcinoma: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2013;11(11):1399–1412. doi: 10.1016/j.cgh.2013.05.009.
    1. Duggan C, Onstad L, Hardikar S, Blount PL, Reid BJ, Vaughan TL. Association between markers of obesity and progression from Barrett’s esophagus to esophageal adenocarcinoma. Clin Gastroenterol Hepatol. 2013;11(8):934–943. doi: 10.1016/j.cgh.2013.02.017.
    1. Garcia JM, Splenser AE, Kramer J, Alsarraj A, Fitzgerald S, Ramsey D, El-Serag HB. Circulating inflammatory Cytokines and Adipokines are associated with increased risk of Barrett’s Esophagus: a case–control study. Clin Gastroenterol Hepatol. 2014;12(2):229–238. doi: 10.1016/j.cgh.2013.07.038.
    1. Inoue M, Tsugane S. Insulin resistance and cancer: epidemiological evidence. Endocr Relat Cancer. 2012;19(5):F1–F8. doi: 10.1530/ERC-12-0142.
    1. Friedenreich CM, Neilson HK, Lynch BM. State of the epidemiological evidence on physical activity and cancer prevention. Eur J Cancer. 2010;46(14):2593–2604. doi: 10.1016/j.ejca.2010.07.028.
    1. Deeb KK, Trump DL, Johnson CS. Vitamin D signalling pathways in cancer: potential for anticancer therapeutics. Nat Rev Cancer. 2007;7(9):684–700. doi: 10.1038/nrc2196.
    1. Shrank WH, Patrick AR, Brookhart MA. Healthy user and related biases in observational studies of preventive interventions: a primer for physicians. J Gen Intern Med. 2011;26(5):546–550. doi: 10.1007/s11606-010-1609-1.
    1. Nilsson M, Johnsen R, Ye W, Hveem K, Lagergren J. Lifestyle related risk factors in the aetiology of gastro-oesophageal reflux. Gut. 2004;53(12):1730–1735. doi: 10.1136/gut.2004.043265.
    1. Jozkow P, Wasko-Czopnik D, Medras M, Paradowski L. Gastroesophageal reflux disease and physical activity. Sports Med. 2006;36(5):385–391. doi: 10.2165/00007256-200636050-00002.
    1. Winzer BM, Paratz JD, Reeves MM, Whiteman DC. Exercise and the Prevention of Oesophageal Cancer (EPOC) study protocol: a randomized controlled trial of exercise versus stretching in males with Barrett’s oesophagus. BMC Cancer. 2010;10:292. doi: 10.1186/1471-2407-10-292.
    1. Kushi LH, Doyle C, McCullough M, Rock CL, Demark-Wahnefried W, Bandera EV, Gapstur S, Patel AV, Andrews K, Gansler T. American cancer society guidelines on nutrition and physical activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J Clin. 2012;62(1):30–67. doi: 10.3322/caac.20140.

Source: PubMed

3
Tilaa