Cancer Causes & Control

, Volume 23, Issue 8, pp 1279–1288

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

  • Yuanfeng Gong
  • Quanbo Zhou
  • Yu Zhou
  • Qing Lin
  • Bing Zeng
  • Rufu Chen
  • Zhihua Li
Original paper



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


We identified eligible studies in Medline and EMBASE up to 11 February 2012 and the reference lists of original studies and review articles on this topic. Summary relative risks with their 95 % confidence intervals were calculated with a random-effects model. Between-study heterogeneity was assessed using Cochran Q and I2 statistics.


Fifteen studies (11 case–control studies and 4 cohort studies) met eligibility criteria. The current data suggest that gastrectomy is associated with a 54 % excess risk of PaC (SRRs = 1.54; 95 % CI, 1.25–1.90; test for heterogeneity Q = 17.94, p < 0.001, I2 = 22 %). There was no publication bias in the present meta-analysis.


A significant increased risk of PaC exists in patients who have undergone gastrectomy, particularly those receiving Billroth II resection with a long postoperative interval.


Gastrectomy Pancreatic cancer Systematic review Meta-analysis Relative risks 



Pancreatic cancer


Odds ratio


Relative risk


Hazard ratio


Summary relative risks


Confidence intervals


Body mass index


Diabetes mellitus


  1. 1.
    Siegel R, Ward E, Brawley O, Jemal A (2011) Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 61(4):212–236. doi:10.3322/caac.20121 PubMedCrossRefGoogle Scholar
  2. 2.
    StatBite. U.S. pancreatic cancer rates (2010) J Natl Cancer Inst 102(24):1822. doi:10.1093/jnci/djq517 Google Scholar
  3. 3.
    Zervos EE, Rosemurgy AS, Al-Saif O, Durkin AJ (2004) Surgical management of early-stage pancreatic cancer. Cancer Control 11(1):23–31PubMedGoogle Scholar
  4. 4.
    Gudjonsson B (1987) Cancer of the pancreas. 50 years of surgery. Cancer 60(9):2284–2303PubMedCrossRefGoogle Scholar
  5. 5.
    Yeo CJ, Abrams RA, Grochow LB, Sohn TA, Ord SE, Hruban RH, Zahurak ML, Dooley WC, Coleman J, Sauter PK, Pitt HA, Lillemoe KD, Cameron JL (1997) Pancreaticoduodenectomy for pancreatic adenocarcinoma: postoperative adjuvant chemoradiation improves survival. A prospective, single-institution experience. Ann Surg 225(5):621–633, 633–636Google Scholar
  6. 6.
    Hassan MM, Bondy ML, Wolff RA, Abbruzzese JL, Vauthey JN, Pisters PW, Evans DB, Khan R, Chou TH, Lenzi R, Jiao L, Li D (2007) Risk factors for pancreatic cancer: case-control study. Am J Gastroenterol 102(12):2696–2707. doi:10.1111/j.1572-0241.2007.01510.x PubMedCrossRefGoogle Scholar
  7. 7.
    Lynch SM, Vrieling A, Lubin JH, Kraft P, Mendelsohn JB, Hartge P, Canzian F, Steplowski E, Arslan AA, Gross M, Helzlsouer K, Jacobs EJ, LaCroix A, Petersen G, Zheng W, Albanes D, Amundadottir L, Bingham SA, Boffetta P, Boutron-Ruault MC, Chanock SJ, Clipp S, Hoover RN, Jacobs K, Johnson KC, Kooperberg C, Luo J, Messina C, Palli D, Patel AV, Riboli E, Shu XO, Rodriguez SL, Thomas G, Tjonneland A, Tobias GS, Tong E, Trichopoulos D, Virtamo J, Ye W, Yu K, Zeleniuch-Jacquette A, Bueno-de-Mesquita HB, Stolzenberg-Solomon RZ (2009) Cigarette smoking and pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Am J Epidemiol 170(4):403–413. doi:10.1093/aje/kwp134 PubMedCrossRefGoogle Scholar
  8. 8.
    Vrieling A, Bueno-de-Mesquita HB, Boshuizen HC, Michaud DS, Severinsen MT, Overvad K, Olsen A, Tjonneland A, Clavel-Chapelon F, Boutron-Ruault MC, Kaaks R, Rohrmann S, Boeing H, Nothlings U, Trichopoulou A, Moutsiou E, Dilis V, Palli D, Krogh V, Panico S, Tumino R, Vineis P, van Gils CH, Peeters PH, Lund E, Gram IT, Rodriguez L, Agudo A, Larranaga N, Sanchez MJ, Navarro C, Barricarte A, Manjer J, Lindkvist B, Sund M, Ye W, Bingham S, Khaw KT, Roddam A, Key T, Boffetta P, Duell EJ, Jenab M, Gallo V, Riboli E (2010) Cigarette smoking, environmental tobacco smoke exposure and pancreatic cancer risk in the European prospective investigation into cancer and nutrition. Int J Cancer 126(10):2394–2403. doi:10.1002/ijc.24907 PubMedGoogle Scholar
  9. 9.
    Larsson SC, Orsini N, Wolk A (2007) Body mass index and pancreatic cancer risk: a meta-analysis of prospective studies. Int J Cancer 120(9):1993–1998. doi:10.1002/ijc.22535 PubMedCrossRefGoogle Scholar
  10. 10.
    Li D, Morris JS, Liu J, Hassan MM, Day RS, Bondy ML, Abbruzzese JL (2009) Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA 301(24):2553–2562. doi:10.1001/jama.2009.886 PubMedCrossRefGoogle Scholar
  11. 11.
    Mancuso TF, El-Attar AA (1967) Cohort study of workers exposed to betanaphthylamine and benzidine. J Occup Med 9(6):277–285PubMedGoogle Scholar
  12. 12.
    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 (2012) Alcohol consumption and pancreatic cancer: a pooled analysis in the International Pancreatic Cancer Case-Control Consortium (PanC4). Ann Oncol 23(2):374–382. doi:10.1093/annonc/mdr120 PubMedCrossRefGoogle Scholar
  13. 13.
    Gupta S, Vittinghoff E, Bertenthal D, Corley D, Shen H, Walter LC, McQuaid K (2006) New-onset diabetes and pancreatic cancer. Clin Gastroenterol Hepatol 4(11):1366–1372, 1301. doi:10.1016/j.cgh.2006.06.024 Google Scholar
  14. 14.
    Lowenfels AB, Maisonneuve P, Cavallini G, Ammann RW, Lankisch PG, Andersen JR, Dimagno EP, Andren-Sandberg A, Domellof L (1993) Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N Engl J Med 328(20):1433–1437. doi:10.1056/NEJM199305203282001 PubMedCrossRefGoogle Scholar
  15. 15.
    Malka D, Hammel P, Maire F, Rufat P, Madeira I, Pessione F, Levy P, Ruszniewski P (2002) Risk of pancreatic adenocarcinoma in chronic pancreatitis. Gut 51(6):849–852PubMedCrossRefGoogle Scholar
  16. 16.
    Bracci PM, Wang F, Hassan MM, Gupta S, Li D, Holly EA (2009) Pancreatitis and pancreatic cancer in two large pooled case-control studies. Cancer Causes Control 20(9):1723–1731. doi:10.1007/s10552-009-9424-x PubMedCrossRefGoogle Scholar
  17. 17.
    Tersmette AC, Giardiello FM, Tytgat GN, Offerhaus GJ (1995) Carcinogenesis after remote peptic ulcer surgery: the long-term prognosis of partial gastrectomy. Scand J Gastroenterol Suppl 212:96–99PubMedCrossRefGoogle Scholar
  18. 18.
    Caygill CP, Hill MJ, Hall CN, Kirkham JS, Northfield TC (1987) Increased risk of cancer at multiple sites after gastric surgery for peptic ulcer. Gut 28(8):924–928PubMedCrossRefGoogle Scholar
  19. 19.
    Ross AH, Smith MA, Anderson JR, Small WP (1982) Late mortality after surgery for peptic ulcer. N Engl J Med 307(9):519–522. doi:10.1056/NEJM198208263070902 PubMedCrossRefGoogle Scholar
  20. 20.
    Mack TM, Yu MC, Hanisch R, Henderson BE (1986) Pancreas cancer and smoking, beverage consumption, and past medical history. J Natl Cancer Inst 76(1):49–60PubMedGoogle Scholar
  21. 21.
    Stolzenberg-Solomon RZ, Blaser MJ, Limburg PJ, Perez-Perez G, Taylor PR, Virtamo J, Albanes D (2001) Helicobacter pylori seropositivity as a risk factor for pancreatic cancer. J Natl Cancer Inst 93(12):937–941PubMedCrossRefGoogle Scholar
  22. 22.
    Conter RL, Converse JO, McGarrity TJ, Koch KL (1990) Afferent loop obstruction presenting as acute pancreatitis and pseudocyst: case reports and review of the literature. Surgery 108(1):22–27PubMedGoogle Scholar
  23. 23.
    Nakao K, Fujiwara Y, Itoh R, Nakagawa K, Yamamura T (2003) Afferent loop obstruction with pancreatitis after distal partial gastrectomy with B-II reconstruction added Braun anastomosis for cancer of the stomach. Hepatogastroenterology 50(51):893–896PubMedGoogle Scholar
  24. 24.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–2012PubMedCrossRefGoogle Scholar
  25. 25.
    Kalapothaki V, Tzonou A, Hsieh CC, Toupadaki N, Karakatsani A, Trichopoulos D (1993) Tobacco, ethanol, coffee, pancreatitis, diabetes mellitus, and cholelithiasis as risk factors for pancreatic carcinoma. Cancer Causes Control 4(4):375–382PubMedCrossRefGoogle Scholar
  26. 26.
    Offerhaus GJ, Giardiello FM, Moore GW, Tersmette AC (1987) Partial gastrectomy: a risk factor for carcinoma of the pancreas? Hum Pathol 18(3):285–288PubMedCrossRefGoogle Scholar
  27. 27.
    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(8):809–819. doi:10.1007/s10552-007-9024-6 PubMedCrossRefGoogle Scholar
  28. 28.
    Stael VHC, Anderson H, Ahsberg K, Huldt B (1997) The significance of ulcer disease on late mortality after partial gastric resection. Eur J Gastroenterol Hepatol 9(1):33–40CrossRefGoogle Scholar
  29. 29.
    Inokuchi K, Tokudome S, Ikeda M, Kuratsune M, Ichimiya H, Kaibara N, Ikejiri T, Oka N (1984) Mortality from carcinoma after partial gastrectomy. Gann 75(7):588–594PubMedGoogle Scholar
  30. 30.
    Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Accessed on 21 Feb 2012Google Scholar
  31. 31.
    Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30PubMedGoogle Scholar
  32. 32.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558. doi:10.1002/sim.1186 PubMedCrossRefGoogle Scholar
  33. 33.
    Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. doi:10.1136/bmj.327.7414.557 PubMedCrossRefGoogle Scholar
  34. 34.
    La Vecchia C, Negri E, D’Avanzo B, Ferraroni M, Gramenzi A, Savoldelli R, Boyle P, Franceschi S (1990) Medical history, diet and pancreatic cancer. Oncology 47(6):463–466PubMedCrossRefGoogle Scholar
  35. 35.
    Silverman DT, Schiffman M, Everhart J, Goldstein A, Lillemoe KD, Swanson GM, Schwartz AG, Brown LM, Greenberg RS, Schoenberg JB, Pottern LM, Hoover RN, Fraumeni JJ (1999) Diabetes mellitus, other medical conditions and familial history of cancer as risk factors for pancreatic cancer. Br J Cancer 80(11):1830–1837. doi:10.1038/sj.bjc.6690607 PubMedCrossRefGoogle Scholar
  36. 36.
    Gullo L, Pezzilli R, Morselli-Labate AM (1996) Risk of pancreatic cancer associated with cholelithiasis, cholecystectomy, or gastrectomy. Dig Dis Sci 41(6):1065–1068PubMedCrossRefGoogle Scholar
  37. 37.
    Lee CT, Chang FY, Lee SD (1996) Risk factors for pancreatic cancer in orientals. J Gastroenterol Hepatol 11(5):491–495PubMedCrossRefGoogle Scholar
  38. 38.
    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(1):17–23CrossRefGoogle Scholar
  39. 39.
    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(5):816–820PubMedCrossRefGoogle Scholar
  40. 40.
    Wynder EL, Mabuchi K, Maruchi N, Fortner JG (1973) A case control study of cancer of the pancreas. Cancer 31(3):641–648PubMedCrossRefGoogle Scholar
  41. 41.
    Maringhini A, Thiruvengadam R, Melton LR, Hench VS, Zinsmeister AR, DiMagno EP (1987) Pancreatic cancer risk following gastric surgery. Cancer 60(2):245–247PubMedCrossRefGoogle Scholar
  42. 42.
    Tascilar M, van Rees BP, Sturm PD, Tytgat GN, Hruban RH, Goodman SN, Giardiello FM, Offerhaus GJ, Tersmette AC (2002) Pancreatic cancer after remote peptic ulcer surgery. J Clin Pathol 55(5):340–345PubMedCrossRefGoogle Scholar
  43. 43.
    Luo J, Nordenvall C, Nyren O, Adami HO, Permert J, Ye W (2007) The risk of pancreatic cancer in patients with gastric or duodenal ulcer disease. Int J Cancer 120(2):368–372. doi:10.1002/ijc.22123 PubMedCrossRefGoogle Scholar
  44. 44.
    Mills PK, Beeson WL, Abbey DE, Fraser GE, Phillips RL (1988) Dietary habits and past medical history as related to fatal pancreas cancer risk among adventists. Cancer 61(12):2578–2585PubMedCrossRefGoogle Scholar
  45. 45.
    Ilias EJ (2011) What is the role of gastrectomy in the treatment of peptic ulcer? Rev Assoc Med Bras 57(1):9PubMedCrossRefGoogle Scholar
  46. 46.
    Fischer L, Hildebrandt C, Bruckner T, Kenngott H, Linke GR, Gehrig T, Buchler MW, Muller-Stich BP (2012) Excessive weight loss after sleeve gastrectomy: a systematic review. Obes Surg. doi:10.1007/s11695-012-0616-1
  47. 47.
    Roe IH, Kim JT, Lee HS, Lee JH (1999) Detection of Helicobacter DNA in bile from bile duct diseases. J Korean Med Sci 14(2):182–186PubMedGoogle Scholar
  48. 48.
    Trikudanathan G, Philip A, Dasanu CA, Baker WL (2011) Association between Helicobacter pylori infection and pancreatic cancer. A cumulative meta-analysis. JOP 12(1):26–31PubMedGoogle Scholar
  49. 49.
    Risch HA (2012) Pancreatic cancer: Helicobacter pylori colonization, N-nitrosamine exposures, and ABO blood group. Mol Carcinog 51(1):109–118. doi:10.1002/mc.20826 PubMedCrossRefGoogle Scholar
  50. 50.
    Bair MJ, Wu MS, Chang WH, Shih SC, Wang TE, Chen CJ, Lin CC, Liu CY, Chen MJ (2009) Spontaneous clearance of Helicobacter pylori colonization in patients with partial gastrectomy: correlates with operative procedures and duration after operation. J Formos Med Assoc 108(1):13–19. doi:10.1016/S0929-6646(09)60027-9 PubMedCrossRefGoogle Scholar
  51. 51.
    Kim JW (2008) NSAID-induced gastroenteropathy. Korean J Gastroenterol 52(3):134–141PubMedGoogle Scholar
  52. 52.
    Hiraishi H, Yamagata M, Yoneda M, Shimada T (2007) Guideline for prophylaxis and treatment of NSAID-associated gastric ulcerations. Nihon Rinsho 65(10):1812–1817PubMedGoogle Scholar
  53. 53.
    Bosetti C, Gallus S, La Vecchia C (2009) Aspirin and cancer risk: a summary review to 2007. Recent Results Cancer Res 181:231–251PubMedCrossRefGoogle Scholar
  54. 54.
    Tan XL, Reid LK, Bamlet WR, Oberg AL, Robinson DP, Anderson KE, Petersen GM (2011) Aspirin, nonsteroidal anti-inflammatory drugs, acetaminophen, and pancreatic cancer risk: a clinic-based case-control study. Cancer Prev Res (Phila) 4(11):1835–1841. doi:10.1158/1940-6207.CAPR-11-0146 CrossRefGoogle Scholar
  55. 55.
    Sansom C (2002) Pancreatic-cancer risk increased by peptic-ulcer surgery. Lancet Oncol 3(6):326CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Yuanfeng Gong
    • 1
  • Quanbo Zhou
    • 1
  • Yu Zhou
    • 1
  • Qing Lin
    • 1
  • Bing Zeng
    • 1
  • Rufu Chen
    • 1
  • Zhihua Li
    • 2
  1. 1.Department of Hepatobiliary Surgery, Sun Yat-Sen Memorial HospitalSun Yat-Sen UniversityGuangzhouChina
  2. 2.Department of Oncology, Sun Yat-Sen Memorial HospitalSun Yat-Sen UniversityGuangzhouChina

Personalised recommendations