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Cancer Causes & Control

, Volume 25, Issue 11, pp 1543–1551 | Cite as

Cholelithiasis and risk of pancreatic cancer: systematic review and meta-analysis of 21 observational studies

  • Yuanfeng Gong
  • Siying Li
  • Yunqiang Tang
  • Cong Mai
  • Mingchen Ba
  • Peng Jiang
  • Hui Tang
Original paper

Abstract

Purpose

To investigate the association between cholelithiasis and risk of pancreatic cancer (PaC).

Methods

We identified eligible studies in MEDLINE and EMBASE up to August 1, 2013 and the reference lists of original studies and review articles on this topic. Summary relative risks (SRRs) with their 95 % confidence intervals (CIs) were calculated with a random-effects model.

Results

Twenty-one studies (15 case–control studies, 6 cohort studies) met eligibility criteria. The current data suggest that cholelithiasis is associated with a 25 % excess risk of PaC (SRRs = 1.25, 95 % CI 1.10–1.41; test for heterogeneity p = 0.006, I 2 = 47.6 %). In subgroup analysis of timing of exposure, seven of eight studies in patients whose diagnosis of cholelithiasis made more than specified year (5, 3, 2, or 1 year) prior to cancer diagnosis showed no association for PaC, while all three studies in patients diagnosed less than specified year before cancer diagnosis showed a positive association. There was no publication bias in the present meta-analysis.

Conclusion

This meta-analysis supports the hypothesis that a history of cholelithiasis may significantly increase PaC risk, particularly in Asian countries. However, the positive association disappeared over time, suggesting that cholelithiasis may be the early symptoms of PaC.

Keywords

Cholelithiasis Pancreatic cancer Systematic review Meta-analysis Relative risks 

Abbreviations

PaC

Pancreatic cancer

OR

Odds ratio

RR

Relative risk

HR

Hazard ratio

SRRs

Summary relative risks

CI

Confidence intervals

BMI

Body mass index

DM

Diabetes mellitus

Notes

Acknowledgments

This work was supported by a grant from the Scientific Study Project Foundation of Guangzhou medical University (No. 2013A43).

Conflict of interest

The authors have declared that no competing interests exist.

References

  1. 1.
    Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistics, 2014. CA Cancer J Clin 64:9–29PubMedCrossRefGoogle Scholar
  2. 2.
    StatBite (2010) U.S. pancreatic cancer rates. J Natl Cancer Inst 102:1822Google Scholar
  3. 3.
    Gudjonsson B (1987) Cancer of the pancreas. 50 years of surgery. Cancer 60:2284–2303PubMedCrossRefGoogle Scholar
  4. 4.
    Yeo CJ, Abrams RA, Grochow LB, Sohn TA, Ord SE et al (1997) Pancreaticoduodenectomy for pancreatic adenocarcinoma: postoperative adjuvant chemoradiation improves survival: a prospective, single-institution experience. Ann Surg 225(621–633):633–636Google Scholar
  5. 5.
    Iodice S, Gandini S, Maisonneuve P, Lowenfels AB (2008) Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbecks Arch Surg 393:535–545PubMedCrossRefGoogle Scholar
  6. 6.
    Larsson SC, Orsini N, Wolk A (2007) Body mass index and pancreatic cancer risk: a meta-analysis of prospective studies. Int J Cancer 120:1993–1998PubMedCrossRefGoogle Scholar
  7. 7.
    Li D, Morris JS, Liu J, Hassan MM, Day RS et al (2009) Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA 301:2553–2562PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Lowenfels AB, Maisonneuve P, Cavallini G, Ammann RW, Lankisch PG et al (1993) Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N Engl J Med 328:1433–1437PubMedCrossRefGoogle Scholar
  9. 9.
    Hart AR, Kennedy H, Harvey I (2008) Pancreatic cancer: a review of the evidence on causation. Clin Gastroenterol Hepatol 6:275–282PubMedCrossRefGoogle Scholar
  10. 10.
    Malka D, Hammel P, Maire F, Rufat P, Madeira I et al (2002) Risk of pancreatic adenocarcinoma in chronic pancreatitis. Gut 51:849–852PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Gupta S, Vittinghoff E, Bertenthal D, Corley D, Shen H et al (2006) New-onset diabetes and pancreatic cancer. Clin Gastroenterol Hepatol 4(1366–1372):1301Google Scholar
  12. 12.
    Lin G, Zeng Z, Wang X, Wu Z, Wang J et al (2012) Cholecystectomy and risk of pancreatic cancer: a meta-analysis of observational studies. Cancer Causes Control 23:59–67PubMedCrossRefGoogle Scholar
  13. 13.
    Zhou Y, Zhou Q, Lin Q, Chen R, Gong Y et al (2013) Evaluation of risk factors for extrahepatic cholangiocarcinoma: ABO blood group, hepatitis B virus and their synergism. Int J Cancer 133:1867–1875PubMedCrossRefGoogle Scholar
  14. 14.
    Shrikhande SV, Barreto SG, Singh S, Udwadia TE, Agarwal AK (2010) Cholelithiasis in gallbladder cancer: coincidence, cofactor, or cause! Eur J Surg Oncol 36:514–519PubMedCrossRefGoogle Scholar
  15. 15.
    Mack TM, Yu MC, Hanisch R, Henderson BE (1986) Pancreas cancer and smoking, beverage consumption, and past medical history. J Natl Cancer Inst 76:49–60PubMedGoogle Scholar
  16. 16.
    Lin RS, Kessler II (1981) A multifactorial model for pancreatic cancer in man. Epidemiologic evidence. JAMA 245:147–152PubMedCrossRefGoogle Scholar
  17. 17.
    Chen YK, Yeh JH, Lin CL, Peng CL, Sung FC et al (2014) Cancer risk in patients with cholelithiasis and after cholecystectomy: a nationwide cohort study. J Gastroenterol 49:923–931Google Scholar
  18. 18.
    Coughlin SS, Calle EE, Patel AV, Thun MJ (2000) Predictors of pancreatic cancer mortality among a large cohort of United States adults. Cancer Causes Control 11:915–923PubMedCrossRefGoogle Scholar
  19. 19.
    Chow WH, Johansen C, Gridley G, Mellemkjaer L, Olsen JH et al (1999) Gallstones, cholecystectomy and risk of cancers of the liver, biliary tract and pancreas. Br J Cancer 79:640–644PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Cuzick J, Babiker AG (1989) Pancreatic cancer, alcohol, diabetes mellitus and gall-bladder disease. Int J Cancer 43:415–421PubMedCrossRefGoogle Scholar
  21. 21.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012PubMedCrossRefGoogle Scholar
  22. 22.
    Manousos O, Trichopoulos D, Koutselinis A, Papadimitriou C, Polychronopoulou A et al (1981) Epidemiologic characteristics and trace elements in pancreatic cancer in Greece. Cancer Detect Prev 4:439–442PubMedGoogle Scholar
  23. 23.
    Wells GA, Shea B, O’connel D (2010) The Newcastle–Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa, Ottawa Health Research InstituteGoogle Scholar
  24. 24.
    Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30PubMedGoogle Scholar
  25. 25.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRefGoogle Scholar
  26. 26.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Sterne JA, Egger M (2001) Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 54:1046–1055PubMedCrossRefGoogle Scholar
  28. 28.
    Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463PubMedCrossRefGoogle Scholar
  29. 29.
    Farrow DC, Davis S (1990) Risk of pancreatic cancer in relation to medical history and the use of tobacco, alcohol and coffee. Int J Cancer 45:816–820PubMedCrossRefGoogle Scholar
  30. 30.
    Jain M, Howe GR, St LP, Miller AB (1991) Coffee and alcohol as determinants of risk of pancreas cancer: a case–control study from Toronto. Int J Cancer 47:384–389PubMedCrossRefGoogle Scholar
  31. 31.
    Bueno DMH, Maisonneuve P, Moerman CJ, Walker AM (1992) Aspects of medical history and exocrine carcinoma of the pancreas: a population-based case–control study in The Netherlands. Int J Cancer 52:17–23CrossRefGoogle Scholar
  32. 32.
    Kalapothaki V, Tzonou A, Hsieh CC, Toupadaki N, Karakatsani A et al (1993) Tobacco, ethanol, coffee, pancreatitis, diabetes mellitus, and cholelithiasis as risk factors for pancreatic carcinoma. Cancer Causes Control 4:375–382PubMedCrossRefGoogle Scholar
  33. 33.
    Gullo L, Pezzilli R, Morselli-Labate AM (1996) Risk of pancreatic cancer associated with cholelithiasis, cholecystectomy, or gastrectomy. Dig Dis Sci 41:1065–1068PubMedCrossRefGoogle Scholar
  34. 34.
    Kokic NZ, Adanja JB, Vlajinac DH, Marinkovic PJ, Colovic BR et al (1996) Case–control study of pancreatic cancer in Serbia, Yugoslavia. Neoplasma 43:353–356PubMedGoogle Scholar
  35. 35.
    Schattner A, Fenakel G, Malnick SD (1997) Cholelithiasis and pancreatic cancer. A case–control study. J Clin Gastroenterol 25:602–604CrossRefGoogle Scholar
  36. 36.
    Ko AH, Wang F, Holly EA (2007) Pancreatic cancer and medical history in a population-based case–control study in the San Francisco Bay Area, California. Cancer Causes Control 18:809–819PubMedCrossRefGoogle Scholar
  37. 37.
    Maisonneuve P, Lowenfels AB, Bueno-de-Mesquita HB, Ghadirian P, Baghurst PA et al (2010) Past medical history and pancreatic cancer risk: results from a multicenter case–control study. Ann Epidemiol 20:92–98PubMedCrossRefGoogle Scholar
  38. 38.
    Lipworth L, Zucchetto A, Bosetti C, Franceschi S, Talamini R et al (2011) Diabetes mellitus, other medical conditions and pancreatic cancer: a case–control study. Diabetes Metab Res Rev 27:255–261PubMedCrossRefGoogle Scholar
  39. 39.
    Tavani A, Rosato V, Di Palma F, Bosetti C, Talamini R et al (2012) History of cholelithiasis and cancer risk in a network of case–control studies. Ann Oncol 23:2173–2178PubMedCrossRefGoogle Scholar
  40. 40.
    Wu Q, Chen G, Wu WM, Zhou L, You L et al (2012) Metabolic syndrome components and risk factors for pancreatic adenocarcinoma: a case–control study in China. Digestion 86:294–301PubMedCrossRefGoogle Scholar
  41. 41.
    Stolzenberg-Solomon RZ, Pietinen P, Taylor PR, Virtamo J, Albanes D (2002) A prospective study of medical conditions, anthropometry, physical activity, and pancreatic cancer in male smokers (Finland). Cancer Causes Control 13:417–426PubMedCrossRefGoogle Scholar
  42. 42.
    Schernhammer ES, Michaud DS, Leitzmann MF, Giovannucci E, Colditz GA et al (2002) Gallstones, cholecystectomy, and the risk for developing pancreatic cancer. Br J Cancer 86:1081–1084PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Lin Y, Tamakoshi A, Kawamura T, Inaba Y, Kikuchi S et al (2002) Risk of pancreatic cancer in relation to alcohol drinking, coffee consumption and medical history: findings from the Japan collaborative cohort study for evaluation of cancer risk. Int J Cancer 99:742–746PubMedCrossRefGoogle Scholar
  44. 44.
    Agrawal S, Jonnalagadda S (2000) Gallstones, from gallbladder to gut. Management options for diverse complications. Postgrad Med 108(143–146):149–153Google Scholar
  45. 45.
    Huang J, Chang CH, Wang JL, Kuo HK, Lin JW et al (2009) Nationwide epidemiological study of severe gallstone disease in Taiwan. BMC Gastroenterol 9:63PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Watanapa P, Williamson RC (1993) Experimental pancreatic hyperplasia and neoplasia: effects of dietary and surgical manipulation. Br J Cancer 67:877–884PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Yuanfeng Gong
    • 1
  • Siying Li
    • 2
  • Yunqiang Tang
    • 1
  • Cong Mai
    • 1
  • Mingchen Ba
    • 1
  • Peng Jiang
    • 1
  • Hui Tang
    • 1
  1. 1.Department of Hepatobiliary SurgeryAffiliated Cancer Hospital of Guangzhou Medical UniversityGuangzhouChina
  2. 2.Department of NeurologyThird Affiliated Hospital of Guangzhou Medical UniversityGuangzhouChina

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