Official reprint from UpToDate®
www.uptodate.com ©2016 UpToDate®

Association between Helicobacter pylori infection and gastrointestinal malignancy

Section Editor
Mark Feldman, MD, MACP, AGAF, FACG
Deputy Editor
Shilpa Grover, MD, MPH


Since the discovery of Helicobacter pylori in the 1980s, much has been learned about this gram-negative spiral bacteria and its associated disease states. In 1994, the National Institutes of Health Consensus Conference recognized H. pylori as a cause of gastric and duodenal ulcers. Later that year, the International Agency for Research on Cancer declared H. pylori to be a group I human carcinogen for gastric adenocarcinoma [1]. There is also evidence that H. pylori infection is a risk factor for gastric mucosa-associated lymphomas (MALT lymphomas). (See "Clinical presentation and diagnosis of primary gastrointestinal lymphomas".)

Despite these clear associations, there is marked individual variability in the outcomes of H. pylori infection, with most patients having a non-neoplastic rather than neoplastic process. H. pylori infection is associated with a complex interaction between genetic, environmental, and bacterial factors, which potentially explains the different outcomes possible following infection. Until these factors are better defined and their interactions better understood, practitioners should limit testing for and treating H. pylori to those situations where there is evidence to support a clinical benefit.


Gastric cancer is one of the most common causes of cancer-related death in the world [2] (see "Epidemiology of gastric cancer"). Gastric cancers can be categorized by site of occurrence: gastroesophageal junction, proximal stomach, and distal stomach (body and antrum). In the 1930s in the United States, distal cancers were the most common. Over the subsequent 70 years, the incidence of gastric cancer has fallen primarily due to a reduction in distal cancers. In comparison, an increase in the incidence of gastroesophageal junction and proximal cancers has been noted during the past several decades [3,4]. These observations suggest that gastroesophageal and proximal gastric cancers share a common pathogenesis, which is distinct from that of distal cancers [5].

Adenocarcinomas, which accounts for more than 90 percent of tumors arising in the stomach, are of two distinct morphologic types: intestinal-type and diffuse. A sequence of steps with phenotypic changes in the gastric mucosa has been hypothesized as a model for carcinogenesis of intestinal type adenocarcinomas: superficial gastritis; chronic atrophic gastritis; intestinal metaplasia (picture 1); dysplasia; and finally carcinoma (algorithm 1) [6]. No similar sequence has been described for the diffuse type. (See "Pathology and molecular pathogenesis of gastric cancer".)

H. pylori can cause chronic active gastritis and atrophic gastritis, early steps in the carcinogenesis sequence [7,8]. In animal models, H. pylori infection has induced gastric adenocarcinoma [9]. Furthermore, a number of studies in humans have demonstrated a clear association between H. pylori infection and gastric adenocarcinoma [10-12]. The link has been demonstrated in both the intestinal and diffuse subtypes of gastric cancer [10,13].


Subscribers log in here

To continue reading this article, you must log in with your personal, hospital, or group practice subscription. For more information or to purchase a personal subscription, click below on the option that best describes you:
Literature review current through: Sep 2016. | This topic last updated: May 3, 2016.
The content on the UpToDate website is not intended nor recommended as a substitute for medical advice, diagnosis, or treatment. Always seek the advice of your own physician or other qualified health care professional regarding any medical questions or conditions. The use of this website is governed by the UpToDate Terms of Use ©2016 UpToDate, Inc.
  1. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994; 61:1.
  2. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011; 61:69.
  3. Blot WJ, Devesa SS, Kneller RW, Fraumeni JF Jr. Rising incidence of adenocarcinoma of the esophagus and gastric cardia. JAMA 1991; 265:1287.
  4. Powell J, McConkey CC. Increasing incidence of adenocarcinoma of the gastric cardia and adjacent sites. Br J Cancer 1990; 62:440.
  5. Fuchs CS, Mayer RJ. Gastric carcinoma. N Engl J Med 1995; 333:32.
  6. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process--First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52:6735.
  7. Siurala M, Varis K, Wiljasalo M. Studies of patients with atrophic gastritis: a 10-15-year follow-up. Scand J Gastroenterol 1966; 1:40.
  8. Kimura K. Chronological transition of the fundic-pyloric border determined by stepwise biopsy of the lesser and greater curvatures of the stomach. Gastroenterology 1972; 63:584.
  9. Watanabe T, Tada M, Nagai H, et al. Helicobacter pylori infection induces gastric cancer in mongolian gerbils. Gastroenterology 1998; 115:642.
  10. Huang JQ, Sridhar S, Chen Y, Hunt RH. Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 1998; 114:1169.
  11. Eslick GD, Lim LL, Byles JE, et al. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol 1999; 94:2373.
  12. Persson C, Jia Y, Pettersson H, et al. H. pylori seropositivity before age 40 and subsequent risk of stomach cancer: a glimpse of the true relationship? PLoS One 2011; 6:e17404.
  13. Hansson LR, Engstrand L, Nyrén O, Lindgren A. Prevalence of Helicobacter pylori infection in subtypes of gastric cancer. Gastroenterology 1995; 109:885.
  14. Parsonnet J, Vandersteen D, Goates J, et al. Helicobacter pylori infection in intestinal- and diffuse-type gastric adenocarcinomas. J Natl Cancer Inst 1991; 83:640.
  15. Guarner J, Mohar A, Parsonnet J, Halperin D. The association of Helicobacter pylori with gastric cancer and preneoplastic gastric lesions in Chiapas, Mexico. Cancer 1993; 71:297.
  16. An international association between Helicobacter pylori infection and gastric cancer. The EUROGAST Study Group. Lancet 1993; 341:1359.
  17. Parsonnet J, Friedman GD, Vandersteen DP, et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 1991; 325:1127.
  18. Nomura A, Stemmermann GN, Chyou PH, et al. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med 1991; 325:1132.
  19. Forman D, Newell DG, Fullerton F, et al. Association between infection with Helicobacter pylori and risk of gastric cancer: evidence from a prospective investigation. BMJ 1991; 302:1302.
  20. Hansen S, Melby KK, Aase S, et al. Helicobacter pylori infection and risk of cardia cancer and non-cardia gastric cancer. A nested case-control study. Scand J Gastroenterol 1999; 34:353.
  21. Uemura N, Okamoto S, Yamamoto S, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001; 345:784.
  22. de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 2012; 13:607.
  23. Crowe SE. Helicobacter infection, chronic inflammation, and the development of malignancy. Curr Opin Gastroenterol 2005; 21:32.
  24. El-Omar EM, Carrington M, Chow WH, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000; 404:398.
  25. El-Omar EM, Rabkin CS, Gammon MD, et al. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 2003; 124:1193.
  26. Garza-González E, Bosques-Padilla FJ, El-Omar E, et al. Role of the polymorphic IL-1B, IL-1RN and TNF-A genes in distal gastric cancer in Mexico. Int J Cancer 2005; 114:237.
  27. Furuta T, El-Omar EM, Xiao F, et al. Interleukin 1beta polymorphisms increase risk of hypochlorhydria and atrophic gastritis and reduce risk of duodenal ulcer recurrence in Japan. Gastroenterology 2002; 123:92.
  28. El-Omar EM, Carrington M, Chow WH, et al. The role of interleukin-1 polymorphisms in the pathogenesis of gastric cancer. Nature 2001; 412:99.
  29. Lu W, Pan K, Zhang L, et al. Genetic polymorphisms of interleukin (IL)-1B, IL-1RN, IL-8, IL-10 and tumor necrosis factor {alpha} and risk of gastric cancer in a Chinese population. Carcinogenesis 2005; 26:631.
  30. Rad R, Dossumbekova A, Neu B, et al. Cytokine gene polymorphisms influence mucosal cytokine expression, gastric inflammation, and host specific colonisation during Helicobacter pylori infection. Gut 2004; 53:1082.
  31. Ding SZ, Minohara Y, Fan XJ, et al. Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 2007; 75:4030.
  32. Xia HH, Talley NJ. Apoptosis in gastric epithelium induced by Helicobacter pylori infection: implications in gastric carcinogenesis. Am J Gastroenterol 2001; 96:16.
  33. Moss SF, Calam J, Agarwal B, et al. Induction of gastric epithelial apoptosis by Helicobacter pylori. Gut 1996; 38:498.
  34. Jones NL, Shannon PT, Cutz E, et al. Increase in proliferation and apoptosis of gastric epithelial cells early in the natural history of Helicobacter pylori infection. Am J Pathol 1997; 151:1695.
  35. Wagner S, Beil W, Westermann J, et al. Regulation of gastric epithelial cell growth by Helicobacter pylori: offdence for a major role of apoptosis. Gastroenterology 1997; 113:1836.
  36. Jones NL, Day AS, Jennings HA, Sherman PM. Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect Immun 1999; 67:4237.
  37. Correa P, Miller MJ. Helicobacter pylori and gastric atrophy--cancer paradoxes. J Natl Cancer Inst 1995; 87:1731.
  38. Lauwers GY, Scott GV, Hendricks J. Immunohistochemical evidence of aberrant bcl-2 protein expression in gastric epithelial dysplasia. Cancer 1994; 73:2900.
  39. Varro A, Noble PJ, Pritchard DM, et al. Helicobacter pylori induces plasminogen activator inhibitor 2 in gastric epithelial cells through nuclear factor-kappaB and RhoA: implications for invasion and apoptosis. Cancer Res 2004; 64:1695.
  40. Peek RM Jr, Moss SF, Tham KT, et al. Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis. J Natl Cancer Inst 1997; 89:863.
  41. Raju D, Hussey S, Ang M, et al. Vacuolating cytotoxin and variants in Atg16L1 that disrupt autophagy promote Helicobacter pylori infection in humans. Gastroenterology 2012; 142:1160.
  42. Müller A. Multistep activation of the Helicobacter pylori effector CagA. J Clin Invest 2012; 122:1192.
  43. Houghton J, Stoicov C, Nomura S, et al. Gastric cancer originating from bone marrow-derived cells. Science 2004; 306:1568.
  44. Tsugane S, Tei Y, Takahashi T, et al. Salty food intake and risk of Helicobacter pylori infection. Jpn J Cancer Res 1994; 85:474.
  45. Fox JG, Dangler CA, Taylor NS, et al. High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res 1999; 59:4823.
  46. Lee SA, Kang D, Shim KN, et al. Effect of diet and Helicobacter pylori infection to the risk of early gastric cancer. J Epidemiol 2003; 13:162.
  47. Machida-Montani A, Sasazuki S, Inoue M, et al. Association of Helicobacter pylori infection and environmental factors in non-cardia gastric cancer in Japan. Gastric Cancer 2004; 7:46.
  48. Nozaki K, Shimizu N, Inada K, et al. Synergistic promoting effects of Helicobacter pylori infection and high-salt diet on gastric carcinogenesis in Mongolian gerbils. Jpn J Cancer Res 2002; 93:1083.
  49. Yu LZ, Gao HJ, Bai JF, et al. Expression of COX-2 proteins in gastric mucosal lesions. World J Gastroenterol 2004; 10:292.
  50. van Rees BP, Saukkonen K, Ristimäki A, et al. Cyclooxygenase-2 expression during carcinogenesis in the human stomach. J Pathol 2002; 196:171.
  51. Lim HY, Joo HJ, Choi JH, et al. Increased expression of cyclooxygenase-2 protein in human gastric carcinoma. Clin Cancer Res 2000; 6:519.
  52. Kaise M, Miwa J, Suzuki N, et al. Inducible nitric oxide synthase gene promoter polymorphism is associated with increased gastric mRNA expression of inducible nitric oxide synthase and increased risk of gastric carcinoma. Eur J Gastroenterol Hepatol 2007; 19:139.
  53. Toyoda T, Tsukamoto T, Hirano N, et al. Synergistic upregulation of inducible nitric oxide synthase and cyclooxygenase-2 in gastric mucosa of Mongolian gerbils by a high-salt diet and Helicobacter pylori infection. Histol Histopathol 2008; 23:593.
  54. González CA, López-Carrillo L. Helicobacter pylori, nutrition and smoking interactions: their impact in gastric carcinogenesis. Scand J Gastroenterol 2010; 45:6.
  55. Kwon HJ, Won YS, Nam KT, et al. Vitamin D₃ upregulated protein 1 deficiency promotes N-methyl-N-nitrosourea and Helicobacter pylori-induced gastric carcinogenesis in mice. Gut 2012; 61:53.
  56. Sobala GM, Schorah CJ, Sanderson M, et al. Ascorbic acid in the human stomach. Gastroenterology 1989; 97:357.
  57. Plasma vitamin concentrations in patients with intestinal metaplasia and in controls. UK Subgroup of the ECP-EURONUT-IM Study Group. Eur J Cancer Prev 1992; 1:177.
  58. You WC, Zhang L, Gail MH, et al. Gastric dysplasia and gastric cancer: Helicobacter pylori, serum vitamin C, and other risk factors. J Natl Cancer Inst 2000; 92:1607.
  59. Block G. Vitamin C and cancer prevention: the epidemiologic evidence. Am J Clin Nutr 1991; 53:270S.
  60. Feiz HR, Mobarhan S. Does vitamin C intake slow the progression of gastric cancer in Helicobacter pylori-infected populations? Nutr Rev 2002; 60:34.
  61. Ikeda F, Doi Y, Yonemoto K, et al. Hyperglycemia increases risk of gastric cancer posed by Helicobacter pylori infection: a population-based cohort study. Gastroenterology 2009; 136:1234.
  62. Cho Y, Lee DH, Oh HS, et al. Higher prevalence of obesity in gastric cardia adenocarcinoma compared to gastric non-cardia adenocarcinoma. Dig Dis Sci 2012; 57:2687.
  63. Yang P, Zhou Y, Chen B, et al. Overweight, obesity and gastric cancer risk: results from a meta-analysis of cohort studies. Eur J Cancer 2009; 45:2867.
  64. Sierra R, Muñoz N, Peña AS, et al. Antibodies to Helicobacter pylori and pepsinogen levels in children from Costa Rica: comparison of two areas with different risks for stomach cancer. Cancer Epidemiol Biomarkers Prev 1992; 1:449.
  65. Hansson LE, Nyrén O, Hsing AW, et al. The risk of stomach cancer in patients with gastric or duodenal ulcer disease. N Engl J Med 1996; 335:242.
  66. Tsugane S, Kabuto M, Imai H, et al. Helicobacter pylori, dietary factors, and atrophic gastritis in five Japanese populations with different gastric cancer mortality. Cancer Causes Control 1993; 4:297.
  67. Azuma T, Ito S, Sato F, et al. The role of the HLA-DQA1 gene in resistance to atrophic gastritis and gastric adenocarcinoma induced by Helicobacter pylori infection. Cancer 1998; 82:1013.
  68. Lu H, Hsu PI, Graham DY, Yamaoka Y. Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology 2005; 128:833.
  69. Rood JC, Ruiz B, Fontham ET, et al. Helicobacter pylori-associated gastritis and the ascorbic acid concentration in gastric juice. Nutr Cancer 1994; 22:65.
  70. La Vecchia C, Negri E, Franceschi S, Gentile A. Family history and the risk of stomach and colorectal cancer. Cancer 1992; 70:50.
  71. Inoue M, Tajima K, Yamamura Y, et al. Family history and subsite of gastric cancer: data from a case-referent study in Japan. Int J Cancer 1998; 76:801.
  72. Brenner H, Arndt V, Stürmer T, et al. Individual and joint contribution of family history and Helicobacter pylori infection to the risk of gastric carcinoma. Cancer 2000; 88:274.
  73. El-Omar EM, Oien K, Murray LS, et al. Increased prevalence of precancerous changes in relatives of gastric cancer patients: critical role of H. pylori. Gastroenterology 2000; 118:22.
  74. Lee YC, Chiang TH, Chou CK, et al. Association Between Helicobacter pylori Eradication and Gastric Cancer Incidence: A Systematic Review and Meta-analysis. Gastroenterology 2016; 150:1113.
  75. Parsonnet J, Harris RA, Hack HM, Owens DK. Modelling cost-effectiveness of Helicobacter pylori screening to prevent gastric cancer: a mandate for clinical trials. Lancet 1996; 348:150.
  76. Fendrick AM, Chernew ME, Hirth RA, et al. Clinical and economic effects of population-based Helicobacter pylori screening to prevent gastric cancer. Arch Intern Med 1999; 159:142.
  77. Talley NJ, Fock KM, Moayyedi P. Gastric Cancer Consensus conference recommends Helicobacter pylori screening and treatment in asymptomatic persons from high-risk populations to prevent gastric cancer. Am J Gastroenterol 2008; 103:510.
  78. Malfertheiner P, Megraud F, O'Morain CA, et al. Management of Helicobacter pylori infection--the Maastricht IV/ Florence Consensus Report. Gut 2012; 61:646.
  79. Chey WD, Wong BC, Practice Parameters Committee of the American College of Gastroenterology. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol 2007; 102:1808.
  80. Freeman C, Berg JW, Cutler SJ. Occurrence and prognosis of extranodal lymphomas. Cancer 1972; 29:252.
  81. Isaacson PG. Gastrointestinal lymphomas and lymphoid hyperplasias. In: Neoplastic Haematolpathology, Knowles DM (Ed), Williams & Wilkins, Baltimore 1992. p.953.
  82. Clark EA, Ledbetter JA. How B and T cells talk to each other. Nature 1994; 367:425.
  83. Lydyard P, Grossi C. Secondary lymphoid organs and tissues. In: Immunology, 4th ed, Roitt I, Brostoff J, Male D (Eds), Mosby, London 1996. p.31.
  84. D'Elios MM, Amedei A, Manghetti M, et al. Impaired T-cell regulation of B-cell growth in Helicobacter pylori--related gastric low-grade MALT lymphoma. Gastroenterology 1999; 117:1105.
  85. Zucca E, Bertoni F, Roggero E, et al. Molecular analysis of the progression from Helicobacter pylori-associated chronic gastritis to mucosa-associated lymphoid-tissue lymphoma of the stomach. N Engl J Med 1998; 338:804.
  86. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 1991; 338:1175.
  87. Parsonnet J, Hansen S, Rodriguez L, et al. Helicobacter pylori infection and gastric lymphoma. N Engl J Med 1994; 330:1267.
  88. Eck M, Schmausser B, Haas R, et al. MALT-type lymphoma of the stomach is associated with Helicobacter pylori strains expressing the CagA protein. Gastroenterology 1997; 112:1482.
  89. Chang CS, Chen LT, Yang JC, et al. Isolation of a Helicobacter pylori protein, FldA, associated with mucosa-associated lymphoid tissue lymphoma of the stomach. Gastroenterology 1999; 117:82.
  90. Mazzucchelli L, Blaser A, Kappeler A, et al. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J Clin Invest 1999; 104:R49.
  91. Stolte M, Kroher G, Meining A, et al. A comparison of Helicobacter pylori and H. heilmannii gastritis. A matched control study involving 404 patients. Scand J Gastroenterol 1997; 32:28.
  92. Lin WC, Tsai HF, Kuo SH, et al. Translocation of Helicobacter pylori CagA into Human B lymphocytes, the origin of mucosa-associated lymphoid tissue lymphoma. Cancer Res 2010; 70:5740.
  93. Morgner A, Lehn N, Andersen LP, et al. Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology 2000; 118:821.
  94. Wotherspoon AC, Doglioni C, Diss TC, et al. Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet 1993; 342:575.
  95. Savio A, Franzin G, Wotherspoon AC, et al. Diagnosis and posttreatment follow-up of Helicobacter pylori-positive gastric lymphoma of mucosa-associated lymphoid tissue: histology, polymerase chain reaction, or both? Blood 1996; 87:1255.
  96. Weber DM, Dimopoulos MA, Anandu DP, et al. Regression of gastric lymphoma of mucosa-associated lymphoid tissue with antibiotic therapy for Helicobacter pylori. Gastroenterology 1994; 107:1835.
  97. Roggero E, Zucca E, Pinotti G, et al. Eradication of Helicobacter pylori infection in primary low-grade gastric lymphoma of mucosa-associated lymphoid tissue. Ann Intern Med 1995; 122:767.
  98. Carlson SJ, Yokoo H, Vanagunas A. Progression of gastritis to monoclonal B-cell lymphoma with resolution and recurrence following eradication of Helicobacter pylori. JAMA 1996; 275:937.
  99. Steinbach G, Ford R, Glober G, et al. Antibiotic treatment of gastric lymphoma of mucosa-associated lymphoid tissue. An uncontrolled trial. Ann Intern Med 1999; 131:88.
  100. Fischbach W, Goebeler-Kolve ME, Dragosics B, et al. Long term outcome of patients with gastric marginal zone B cell lymphoma of mucosa associated lymphoid tissue (MALT) following exclusive Helicobacter pylori eradication therapy: experience from a large prospective series. Gut 2004; 53:34.
  101. Okame M, Takaya S, Sato H, et al. Complete regression of early-stage gastric diffuse large B-cell lymphoma in an HIV-1-infected patient following Helicobacter pylori eradication therapy. Clin Infect Dis 2014; 58:1490.
  102. Breuer-Katschinski B, Nemes K, Marr A, et al. Helicobacter pylori and the risk of colonic adenomas. Colorectal Adenoma Study Group. Digestion 1999; 60:210.
  103. Aydin A, Karasu Z, Zeytinoglu A, et al. Colorectal adenomateous polyps and Helicobacter pylori infection. Am J Gastroenterol 1999; 94:1121.
  104. Meucci G, Tatarella M, Vecchi M, et al. High prevalence of Helicobacter pylori infection in patients with colonic adenomas and carcinomas. J Clin Gastroenterol 1997; 25:605.
  105. Shmuely H, Passaro D, Figer A, et al. Relationship between Helicobacter pylori CagA status and colorectal cancer. Am J Gastroenterol 2001; 96:3406.
  106. Sonnenberg A, Genta RM. Helicobacter pylori is a risk factor for colonic neoplasms. Am J Gastroenterol 2013; 108:208.
  107. Moss SF, Neugut AI, Garbowski GC, et al. Helicobacter pylori seroprevalence and colorectal neoplasia: evidence against an association. J Natl Cancer Inst 1995; 87:762.
  108. Siddheshwar RK, Muhammad KB, Gray JC, Kelly SB. Seroprevalence of Helicobacter pylori in patients with colorectal polyps and colorectal carcinoma. Am J Gastroenterol 2001; 96:84.
  109. Robertson DJ, Sandler RS, Ahnen DJ, et al. Gastrin, Helicobacter pylori, and colorectal adenomas. Clin Gastroenterol Hepatol 2009; 7:163.
  110. Zhang Y, Hoffmeister M, Weck MN, et al. Helicobacter pylori infection and colorectal cancer risk: evidence from a large population-based case-control study in Germany. Am J Epidemiol 2012; 175:441.
  111. Hong SN, Lee SM, Kim JH, et al. Helicobacter pylori infection increases the risk of colorectal adenomas: cross-sectional study and meta-analysis. Dig Dis Sci 2012; 57:2184.
  112. Selgrad M, Bornschein J, Kandulski A, et al. Helicobacter pylori but not gastrin is associated with the development of colonic neoplasms. Int J Cancer 2014; 135:1127.
  113. Stolzenberg-Solomon RZ, Blaser MJ, Limburg PJ, et al. Helicobacter pylori seropositivity as a risk factor for pancreatic cancer. J Natl Cancer Inst 2001; 93:937.
  114. Raderer M, Wrba F, Kornek G, et al. Association between Helicobacter pylori infection and pancreatic cancer. Oncology 1998; 55:16.
  115. Risch HA, Yu H, Lu L, Kidd MS. ABO blood group, Helicobacter pylori seropositivity, and risk of pancreatic cancer: a case-control study. J Natl Cancer Inst 2010; 102:502.
  116. Trikudanathan G, Philip A, Dasanu CA, Baker WL. Association between Helicobacter pylori infection and pancreatic cancer. A cumulative meta-analysis. JOP 2011; 12:26.
  117. Xiao M, Wang Y, Gao Y. Association between Helicobacter pylori infection and pancreatic cancer development: a meta-analysis. PLoS One 2013; 8:e75559.
  118. Risch HA. Etiology of pancreatic cancer, with a hypothesis concerning the role of N-nitroso compounds and excess gastric acidity. J Natl Cancer Inst 2003; 95:948.
  119. Chang JS, Tsai CR, Chen LT. Medical risk factors associated with cholangiocarcinoma in Taiwan: a population-based case-control study. PLoS One 2013; 8:e69981.
  120. Bulajic M, Maisonneuve P, Schneider-Brachert W, et al. Helicobacter pylori and the risk of benign and malignant biliary tract disease. Cancer 2002; 95:1946.
  121. Pandey M, Shukla M. Helicobacter species are associated with possible increase in risk of hepatobiliary tract cancers. Surg Oncol 2009; 18:51.
  122. Boonyanugomol W, Chomvarin C, Sripa B, et al. Helicobacter pylori in Thai patients with cholangiocarcinoma and its association with biliary inflammation and proliferation. HPB (Oxford) 2012; 14:177.
  123. Murphy G, Michel A, Taylor PR, et al. Association of seropositivity to Helicobacter species and biliary tract cancer in the ATBC study. Hepatology 2014; 60:1963.