Advertisement

European Journal of Epidemiology

, Volume 30, Issue 4, pp 279–298 | Cite as

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

  • Gundula Behrens
  • Carmen Jochem
  • Daniela Schmid
  • Marlen Keimling
  • Cristian Ricci
  • Michael F. Leitzmann
META-ANALYSIS

Abstract

Physical activity may prevent pancreatic cancer by regulating body weight and decreasing insulin resistance, DNA damage, and chronic inflammation. Previous meta-analyses found inconsistent evidence for a protective effect of physical activity on pancreatic cancer but those studies did not investigate whether the association between physical activity and pancreatic cancer varies by smoking status, body mass index (BMI), or level of consistency of physical activity over time. To address these issues, we conducted an updated meta-analysis following the PRISMA guidelines among 30 distinct studies with a total of 10,501 pancreatic cancer cases. Random effects meta-analysis of cohort studies revealed a weak, statistically significant reduction in pancreatic cancer risk for high versus low levels of physical activity (relative risk (RR) 0.93, 95 % confidence interval (CI) 0.88–0.98). By comparison, case–control studies yielded a stronger, statistically significant risk reduction (RR 0.78, 95 % CI 0.66–0.94; p-difference by study design = 0.07). When focusing on cohort studies, physical activity summary risk estimates appeared to be more pronounced for consistent physical activity over time (RR 0.86, 95 % CI 0.76–0.97) than for recent past physical activity (RR 0.95, 95 % CI 0.90–1.01) or distant past physical activity (RR 0.95, 95 % CI 0.79–1.15, p-difference by timing in life of physical activity = 0.36). Physical activity summary risk estimates did not differ by smoking status or BMI. In conclusion, physical activity is not strongly associated with pancreatic cancer risk, and the relation is not modified by smoking status or BMI level. While overall findings were weak, we did find some suggestion of potential pancreatic cancer risk reduction with consistent physical activity over time.

Keywords

Physical activity Pancreatic cancer Meta-analysis 

Supplementary material

10654_2015_14_MOESM1_ESM.docx (293 kb)
Supplementary material 1 (DOCX 292 kb)

References

  1. 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. 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. 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.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  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.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. 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. 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.PubMedCentralCrossRefGoogle Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. 13.
    Bao Y, Michaud DS. Physical activity and pancreatic cancer risk: a systematic review. Cancer Epidemiol Biomark Prev. 2008;17(10):2671–82.CrossRefGoogle Scholar
  14. 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.PubMedGoogle Scholar
  15. 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. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 24.
    Garfinkel L, Stellman SD. Mortality by relative weight and exercise. Cancer. 1988;62(8 Suppl):1844–50.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.PubMedCrossRefGoogle Scholar
  27. 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. 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.PubMedCrossRefGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.PubMedCrossRefGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. 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.PubMedCrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 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.PubMedCrossRefGoogle Scholar
  49. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  50. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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.PubMedCrossRefGoogle Scholar
  53. 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.PubMedCrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. 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.PubMedGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. 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.PubMedCrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.PubMedGoogle Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. 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.CrossRefGoogle Scholar
  63. 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.PubMedCrossRefGoogle Scholar
  64. 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.PubMedCrossRefGoogle Scholar
  65. 65.
    Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.PubMedCrossRefGoogle Scholar
  66. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  67. 67.
    Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.PubMedCrossRefGoogle Scholar
  68. 68.
    R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria, 2011.Google Scholar
  69. 69.
    Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36:1–48.Google Scholar
  70. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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.PubMedCrossRefGoogle Scholar
  73. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  74. 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. 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.PubMedCentralPubMedGoogle Scholar
  76. 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.PubMedCrossRefGoogle Scholar
  77. 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.PubMedCrossRefGoogle Scholar
  78. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  79. 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.PubMedCrossRefGoogle Scholar
  80. 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.PubMedCrossRefGoogle Scholar
  81. 81.
    Whitcomb D, Greer J. Germ-line mutations, pancreatic inflammation, and pancreatic cancer. Clin Gastroenterol Hepatol. 2009;7(11 Suppl):S29–34.PubMedCrossRefGoogle Scholar
  82. 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.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

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

Personalised recommendations