Physical activity and risk of pancreatic cancer: a systematic review and meta-analysis

European Journal of Epidemiology

Volumn 30, Issue 4, 2015, Pages 279-298

  Behrens, Gundula ^a   Jochem, Carmen ^a   Schmid, Daniela ^a   Keimling, Marlen ^a   Ricci, Cristian ^a   Leitzmann, Michael F ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Meta analysis; Pancreatic cancer; Physical activity

Indexed keywords

BODY MASS; EXERCISE; FEMALE; HUMAN; MALE; META ANALYSIS; MOTOR ACTIVITY; PANCREATIC NEOPLASMS; RISK FACTOR; RISK REDUCTION;

BODY MASS INDEX; EXERCISE; FEMALE; HUMANS; MALE; MOTOR ACTIVITY; PANCREATIC NEOPLASMS; RISK FACTORS; RISK REDUCTION BEHAVIOR;

EID: 84930516622     PISSN: 03932990     EISSN: 15737284     Source Type: Journal    
DOI: 10.1007/s10654-015-0014-9     Document Type: Article

References (82)

1. Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, F B. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer, 2013. Available from: http://globocan.iarc.fr. Accessed on 20 June 2014.
2. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA. 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. Aune D, Greenwood DC, Chan DS, Vieira R, Vieira AR, Navarro Rosenblatt DA, Cade JE, Burley VJ, Norat T. Body mass index, abdominal fatness and pancreatic cancer risk: a systematic review and non-linear dose–response meta-analysis of prospective studies. Ann Oncol. 2012;23(4):843–52.
4. Zou L, Zhong R, Shen N, Chen W, Zhu B, Ke J, Lu X, Zhang T, Lou J, Wang Z, Liu L, Qi L, Miao X. Non-linear dose–response relationship between cigarette smoking and pancreatic cancer risk: evidence from a meta-analysis of 42 observational studies. Eur J Cancer. 2014;50(1):193–203.
5. Lucenteforte E, La Vecchia C, Silverman D, Petersen GM, Bracci PM, Ji BT, Bosetti C, Li D, Gallinger S, Miller AB, Bueno-de-Mesquita HB, Talamini R, Polesel J, Ghadirian P, Baghurst PA, Zatonski W, Fontham E, Bamlet WR, Holly EA, Gao YT, Negri E, Hassan M, Cotterchio M, Su J, Maisonneuve P, Boffetta P, Duell EJ. Alcohol consumption and pancreatic cancer: a pooled analysis in the International Pancreatic Cancer Case–Control Consortium (PanC4). Ann Oncol. 2012;23(2):374–82.
6. Larsson SC, Wolk A. Red and processed meat consumption and risk of pancreatic cancer: meta-analysis of prospective studies. Br J Cancer. 2012;106(3):603–7.
7. Elena JW, Steplowski E, Yu K, Hartge P, Tobias GS, Brotzman MJ, Chanock SJ, Stolzenberg-Solomon RZ, Arslan AA, Bueno-de-Mesquita HB, Helzlsouer K, Jacobs EJ, LaCroix A, Petersen G, Zheng W, Albanes D, Allen NE, Amundadottir L, Bao Y, Boeing H, Boutron-Ruault MC, Buring JE, Gaziano JM, Giovannucci EL, Duell EJ, Hallmans G, Howard BV, Hunter DJ, Hutchinson A, Jacobs KB, Kooperberg C, Kraft P, Mendelsohn JB, Michaud DS, Palli D, Phillips LS, Overvad K, Patel AV, Sansbury L, Shu XO, Simon MS, Slimani N, Trichopoulos D, Visvanathan K, Virtamo J, Wolpin BM, Zeleniuch-Jacquotte A, Fuchs CS, Hoover RN, Gross M. Diabetes and risk of pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Cancer Causes Control. 2013;24(1):13–25.
8. Rothwell PM, Fowkes FG, Belch JF, Ogawa H, Warlow CP, Meade TW. Effect of daily aspirin on long-term risk of death due to cancer: analysis of individual patient data from randomised trials. Lancet. 2011;377(9759):31–41.
9. Mann S, Beedie C, Balducci S, Zanuso S, Allgrove J, Bertiato F, Jimenez A. Changes in insulin sensitivity in response to different modalities of exercise: a review of the evidence. Diabetes Metab Res Rev. 2014;30(4):257–68.
10. Barte JC, Veldwijk J, Teixeira PJ, Sacks FM, Bemelmans WJ. Differences in weight loss across different BMI classes: a meta-analysis of the effects of interventions with diet and exercise. Int J Behav Med. 2014. doi:10.1007/s12529-013-9355-5. Accessed on 11 June 2014.
11. Cash SW, Beresford SA, Vaughan TL, Heagerty PJ, Bernstein L, White E, Neuhouser ML. Recent physical activity in relation to DNA damage and repair using the comet assay. J Phys Act Health. 2014;11(4):770–6.
12. Herder C, Peltonen M, Koenig W, Sutfels K, Lindstrom J, Martin S, Ilanne-Parikka P, Eriksson JG, Aunola S, Keinanen-Kiukaanniemi S, Valle TT, Uusitupa M, Kolb H, Tuomilehto J. Finnish Diabetes Prevention Study G. Anti-inflammatory effect of lifestyle changes in the Finnish Diabetes Prevention Study. Diabetologia. 2009;52(3):433–42.
13. Bao Y, Michaud DS. Physical activity and pancreatic cancer risk: a systematic review. Cancer Epidemiol Biomark Prev. 2008;17(10):2671–82.
14. O’Rorke MA, Cantwell MM, Cardwell CR, Mulholland HG, Murray LJ. Can physical activity modulate pancreatic cancer risk? A systematic review and meta-analysis. Int J Cancer. 2010;126(12):2957–68.
15. Norat T, Aune D, Vieira AR, Chan D, Navarro Rosenblatt D, Vieira R. The associations between food, nutrition and physical activity and the risk of pancreatic cancer. WCRF/AICR Systematic Literature Review Continuous Update Project Report, 2011. Accessed on 30 Jan 2014 under http://www.dietandcancerreport.org/cancer_resource_center/downloads/cu/Pancreatic-Cancer-SLR-2011.pdf.
16. Jiao L, Berrington de Gonzalez A, Hartge P, Pfeiffer RM, Park Y, Freedman DM, Gail MH, Alavanja MC, Albanes D, Beane Freeman LE, Chow WH, Huang WY, Hayes RB, Hoppin JA, Ji BT, Leitzmann MF, Linet MS, Meinhold CL, Schairer C, Schatzkin A, Virtamo J, Weinstein SJ, Zheng W, Stolzenberg-Solomon RZ. Body mass index, effect modifiers, and risk of pancreatic cancer: a pooled study of seven prospective cohorts. Cancer Causes Control. 2010;21(8):1305–14.
17. Michaud DS, Giovannucci E, Willett WC, Colditz GA, Stampfer MJ, Fuchs CS. Physical activity, obesity, height, and the risk of pancreatic cancer. JAMA. 2001;286(8):921–9.
18. Arem H, Moore SC, Park Y, Ballard-Barbash R, Hollenbeck A, Leitzmann M, Matthews CE. Physical activity and cancer-specific mortality in the NIH-AARP Diet and Health Study cohort. Int J Cancer. 2014;135(2):423–31.
19. Nöthlings U, Wilkens LR, Murphy SP, Hankin JH, Henderson BE, Kolonel LN. Body mass index and physical activity as risk factors for pancreatic cancer: the Multiethnic Cohort Study. Cancer Causes Control. 2007;18(2):165–75.
20. 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.
21. Calton BA, Stolzenberg-Solomon RZ, Moore SC, Schatzkin A, Schairer C, Albanes D, Leitzmann MF. A prospective study of physical activity and the risk of pancreatic cancer among women (United States). BMC Cancer. 2008;8:63.
22. Inoue M, Yamamoto S, Kurahashi N, Iwasaki M, Sasazuki S, Tsugane S. Japan Public Health Center-based Prospective Study G. 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.
23. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:2535.
24. Garfinkel L, Stellman SD. Mortality by relative weight and exercise. Cancer. 1988;62(8 Suppl):1844–50.
25. Robsahm TE, Hestvik UE, Veierod MB, Fagerlie A, Nystad W, Engebretsen L, Tretli S. Cancer risk in Norwegian world class athletes. Cancer Causes Control. 2010;21(10):1711–9.
26. 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.
27. Sormunen J, Backmand HM, Sarna S, Kujala UM, Kaprio J, Dyba T, Pukkala E. Lifetime physical activity and cancer incidence—A cohort study of male former elite athletes in Finland. J Sci Med Sport 2013. doi:10.1016/j.jsams.2013.10.239. Accessed on 20 Nov 2013.
28. 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.
29. 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.
30. Batty GD, Shipley MJ, Marmot M, Davey Smith G. Physical activity and cause-specific mortality in men: further evidence from the Whitehall Study. Eur J Epidemiol. 2001;17:863–9.
31. Batty GD, Kivimaki M, Morrison D, Huxley R, Smith GD, Clarke R, Marmot MG, Shipley MJ. Risk factors for pancreatic cancer mortality: extended follow-up of the original Whitehall Study. Cancer Epidemiol Biomark Prev. 2009;18(2):673–5.
32. 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(7):831–7.
33. 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.
34. Ji BT, Hatch MC, Chow WH, McLaughlin JK, Dai Q, Howe GR, Gao YT, Fraumeni JF Jr. Anthropometric and reproductive factors and the risk of pancreatic cancer: a case–control study in Shanghai, China. Int J Cancer. 1996;66(4):432–7.
35. Zhang Y, Cantor KP, Lynch CF, Zhu Y, Zheng T. Occupation and risk of pancreatic cancer: a population-based case–control study in Iowa. J Occup Environ Med. 2005;47(4):392–8.
36. Alguacil J, Kauppinen T, Porta M, Partanen T, Malats N, Kogevinas M, Benavides FG, Obiols J, Bernal F, Rifa J, Carrato A. Risk of pancreatic cancer and occupational exposures in Spain. Ann Occup Hyg. 2000;44(5):391–403.
37. Brenner DR, Wozniak MB, Feyt C, Holcatova I, Janout V, Foretova L, Fabianova E, Shonova O, Martinek A, Ryska M, Adamcakova Z, Flaska E, Moskal A, Brennan P, Scelo G. Physical activity and risk of pancreatic cancer in a central European multicenter case–control study. Cancer Causes Control. 2014;25(6):669–81.
38. Eberle CA, Bracci PM, Holly EA. Anthropometric factors and pancreatic cancer in a population-based case–control study in the San Francisco Bay area. Cancer Causes Control. 2005;16(10):1235–44.
39. Hanley AJ, Johnson KC, Villeneuve PJ, Mao Y. Canadian Cancer Registries Epidemiology Research G. Physical activity, anthropometric factors and risk of pancreatic cancer: results from the Canadian enhanced cancer surveillance system. Int J Cancer. 2001;94(1):140–7.
40. Inoue M, Tajima K, Takezaki T, Hamajima N, Hirose K, Ito H, Tominaga S. Epidemiology of pancreatic cancer in Japan: a nested case–control study from the Hospital-based Epidemiologic Research Program at Aichi Cancer Center (HERPACC). Int J Epidemiol. 2003;32(2):257–62.
41. 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.
42. Pelucchi C, Zucchetto A, Tavani A, Dal Maso L, Serraino D, La Vecchia C. Physical activity and pancreatic cancer risk. Int J Cancer. 2011;128(9):2243–5.
43. Santibanez M, Vioque J, Alguacil J, de la Hera MG, Moreno-Osset E, Carrato A, Porta M, Kauppinen T. Occupational exposures and risk of pancreatic cancer. Eur J Epidemiol. 2010;25(10):721–30.
44. Zhang J, Dhakal IB, Gross MD, Lang NP, Kadlubar FF, Harnack LJ, Anderson KE. Physical activity, diet, and pancreatic cancer: a population-based, case–control study in Minnesota. Nutr Cancer. 2009;61(4):457–65.
45. Batty GD, Shipley MJ, Kivimaki M, Marmot M, Smith GD. 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;20:661–9.
46. Berrington de Gonzalez A, Spencer EA, Bueno-de-Mesquita HB, Roddam A, Stolzenberg-Solomon R, Halkjaer J, Tjonneland A, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Boeing H, Pischon T, Linseisen J, Rohrmann S, Trichopoulou A, Benetou V, Papadimitriou A, Pala V, Palli D, Panico S, Tumino R, Vineis P, Boshuizen HC, Ocke MC, Peeters PH, Lund E, Gonzalez CA, Larranaga N, Martinez-Garcia C, Mendez M, Navarro C, Quiros JR, Tormo MJ, Hallmans G, Ye W, Bingham SA, Khaw KT, Allen N, Key TJ, Jenab M, Norat T, Ferrari P, Riboli E. Anthropometry, physical activity, and the risk of pancreatic cancer in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomark Prev. 2006;15(5):879–85.
47. Heinen MM, Verhage BA, Goldbohm RA, Lumey LH, van den Brandt PA. Physical activity, energy restriction, and the risk of pancreatic cancer: a prospective study in the Netherlands. Am J Clin Nutr. 2011;94(5):1314–23.
48. Isaksson B, Jonsson F, Pedersen NL, Larsson J, Feychting M, Permert J. Lifestyle factors and pancreatic cancer risk: a cohort study from the Swedish Twin Registry. Int J Cancer. 2002;98(3):480–2.
49. Jiao L, Mitrou PN, Reedy J, Graubard BI, Hollenbeck AR, Schatzkin A, Stolzenberg-Solomon R. A combined healthy lifestyle score and risk of pancreatic cancer in a large cohort study. Arch Intern Med. 2009;169(8):764–70.
50. Lee IM, Sesso HD, Oguma Y, Paffenbarger RS. Physical activity, body weight, and pancreatic cancer mortality. Br J Cancer. 2003;88(5):679–83.
51. Lin Y, Kikuchi S, Tamakoshi A, Yagyu K, Obata Y, Inaba Y, Kurosawa M, Kawamura T, Motohashi Y, Ishibashi T, Group JS. Obesity, physical activity and the risk of pancreatic cancer in a large Japanese cohort. Int J Cancer. 2007;120(12):2665–71.
52. Luo J, Iwasaki M, Inoue M, Sasazuki S, Otani T, Ye W, Tsugane S, Group JS. Body mass index, physical activity and the risk of pancreatic cancer in relation to smoking status and history of diabetes: a large-scale population-based cohort study in Japan—the JPHC study. Cancer Causes Control. 2007;18(6):603–12.
53. Nakamura K, Nagata C, Wada K, Tamai Y, Tsuji M, Takatsuka N, Shimizu H. Cigarette smoking and other lifestyle factors in relation to the risk of pancreatic cancer death: a prospective cohort study in Japan. Jpn J Clin Oncol. 2011;41(2):225–31.
54. Nilsen TI, Vatten LJ. A prospective study of lifestyle factors and the risk of pancreatic cancer in Nord-Trondelag, Norway. Cancer Causes Control. 2000;11(7):645–52.
55. Paffenbarger RS, Hyde RT, Wing AL. Physical activity and incidence of cancer in diverse populations: a preliminary report. Am J Clin Nutr. 1987;45:312–7.
56. Patel AV, Rodriguez C, Bernstein L, Chao A, Thurn MJ, Calle EE. Obesity, recreational physical activity, and risk of pancreatic cancer in a large US cohort. Cancer Epidemiol Biomark Prev. 2005;14(2):459–66.
57. Stevens RJ, Roddam AW, Spencer EA, Pirie KL, Reeves GK, Green J, Beral V. Million Women Study Collaborators. Factors associated with incident and fatal pancreatic cancer in a cohort of middle-aged women. Int J Cancer. 2009;124(10):2400–5.
58. Stolzenberg-Solomon R, Pietinen P, Taylor PR, Virtamo J, Albanes D. A prospective study of medical conditions, anthropometry, physical activity, and pancreatic cancer in male smokers (Finland). Cancer Causes Control. 2002;13:417–26.
59. Stolzenberg-Solomon RZ, Adams K, Leitzmann M, Schairer C, Michaud DS, Hollenbeck A, Schatzkin A, Silverman DT. Adiposity, physical activity, and pancreatic cancer in the National Institutes of Health-AARP Diet and Health Cohort. Am J Epidemiol. 2008;167(5):586–97.
60. Suzuki K. Health conditions and mortality in the Japan Collaborative Cohort Study for Evaluation of Cancer (JACC). Asian Pac J Cancer Prev. 2007;8:25–34.
61. Weiderpass E, Vainio H, Kauppinen T, Vasama-Neuvonen K, Partanen T, Pukkala E. Occupational exposures and gastrointestinal cancers among Finnish women. J Occup Environ Med. 2003;45(3):305–15.
62. Sinner PJ, Schmitz KH, Anderson KE, Folsom AR. Lack of association of physical activity and obesity with incident pancreatic cancer in elderly women. Cancer Epidemiol Biomark Prev. 2005;14(6):1571–3.
63. Waterbor J, Cole P, Delzell E, Andjelkovich D. The mortality experience of major-league baseball players. N Engl J Med. 1988;318(19):1278–80.
64. Monninkhof EM, Elias SG, Vlems FA, van der Tweel I, Schuit AJ, Voskuil DW, van Leeuwen FE. Tfpac. Physical activity and breast cancer: a systematic review. Epidemiology. 2007;18(1):137–57.
65. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.
66. 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.
67. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.
68. R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria, 2011.
69. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36:1–48.
70. Gasparrini A, Armstrong B, Kenward MG. Multivariate meta-analysis for non-linear and other multi-parameter associations. Stat Med. 2012;31(29):3821–39.
71. Jochem C, Leitzmann MF, Keimling M, Schmid D, Behrens G. Physical activity in relation to risk of hematologic cancers: a systematic review and meta-analysis. Cancer Epidemiol Biomark Prev. 2014;23(5):833–46.
72. Paluszkiewicz P, Smolinska K, Debinska I, Turski WA. Main dietary compounds and pancreatic cancer risk. The quantitative analysis of case–control and cohort studies. Cancer Epidemiol. 2012;36(1):60–7.
73. Huxley R, Ansary-Moghaddam A, Berrington de Gonzalez A, Barzi F, Woodward M. Type-II diabetes and pancreatic cancer: a meta-analysis of 36 studies. Br J Cancer. 2005;92(11):2076–83.
74. Gong Y, Li S, Tang Y, Mai C, Ba M, Jiang P, Tang H. Cholelithiasis and risk of pancreatic cancer: systematic review and meta-analysis of 21 observational studies. Cancer Causes Control 2014. doi:10.1007/s10552-014-0458-3. Accessed on 22 Oct 2014.
75. Zhu B, Zou L, Han J, Chen W, Shen N, Zhong R, Li J, Chen X, Liu C, Shi Y, Miao X. Parity and pancreatic cancer risk: evidence from a meta-analysis of twenty epidemiologic studies. Sci Rep. 2014;4:5313.
76. Jeon CY, Lokken RP, Hu FB, van Dam RM. Physical activity of moderate intensity and risk of type 2 diabetes: a systematic review. Diabetes Care. 2007;30(3):744–52.
77. Bouassida A, Chamari K, Zaouali M, Feki Y, Zbidi A, Tabka Z. Review on leptin and adiponectin responses and adaptations to acute and chronic exercise. Br J Sports Med. 2010;44(9):620–30.
78. Bao Y, Giovannucci EL, Kraft P, Stampfer MJ, Ogino S, Ma J, Buring JE, Sesso HD, Lee IM, Gaziano JM, Rifai N, Pollak MN, Cochrane BB, Kaklamani V, Lin JH, Manson JE, Fuchs CS, Wolpin BM. A prospective study of plasma adiponectin and pancreatic cancer risk in five US cohorts. J Natl Cancer Inst. 2013;105(2):95–103.
79. Guerra C, Collado M, Navas C, Schuhmacher AJ, Hernandez-Porras I, Canamero M, Rodriguez-Justo M, Serrano M, Barbacid M. Pancreatitis-induced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence. Cancer Cell. 2011;19(6):728–39.
80. Dite P, Hermanova M, Trna J, Novotny I, Ruzicka M, Liberda M, Bartkova A. The role of chronic inflammation: chronic pancreatitis as a risk factor of pancreatic cancer. Dig Dis. 2012;30(3):277–83.
81. Whitcomb D, Greer J. Germ-line mutations, pancreatic inflammation, and pancreatic cancer. Clin Gastroenterol Hepatol. 2009;7(11 Suppl):S29–34.
82. Clarkson PM, Thompson HS. Antioxidants: What role do they play in physical activity and health? Am J Clin Nutr. 2000;72(2 Suppl):637S–46S.