Skip to main content

Helicobacter pylori Infection and High Dietary Salt Independently Induce Atrophic Gastritis and Intestinal Metaplasia in Commercially Available Outbred Mongolian Gerbils

Digestive Diseases and Sciences volume 48, pages 475–485 (2003)Cite this article

Abstract

Risk factors for development of gastric adenocarcinoma include high dietary salt and Helicobacter pylori infection. Few animal models exist for the laboratory investigation of these factors. We examined gastric pathology resulting from H. pylori infection and high dietary salt as independent variables in commercially available, outbred Mongolian gerbils. Gastric adenocarcinoma and its precursor lesion, intestinal metaplasia, have been previously reported in inbred Mongolian gerbils (MGS/Sea) infected either with clinical isolates of H. pylori or with the strain ATCC 43504. In contrast, we utilized outbred gerbils [Crl:(MON)] infected with the Sydney strain of H. pylori. After 37 weeks, five of five infected animals had atrophic gastritis and intestinal metaplasia. These lesions were similar in description and time of appearance to the lesions reported in inbred gerbils. Atrophic gastritis and intestinal metaplasia also developed in six of six uninfected, outbred gerbils fed a 2.5% salt diet for 56 weeks. In contrast to the H. pylori-infected animals, these lesions were present without concurrent gastric inflammation. The outbred Mongolian gerbil therefore provides an excellent animal model for the study of several gastric cancer risk factors.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Parkin DM, Pisani P, Ferlay J: Estimates of the worldwide incidence of eighteen major cancers in 1985. Int J Cancer 54:594-606, 1993

    Google Scholar 

  2. IARC: Schistosomes, liver flukes, and Helicobacter pylori. IARC Monogr Eval of Carcinog Risks to Hum 61:177-240, 1994

    Google Scholar 

  3. Sato T, Fukuyama T, Suzuki T, Takayanagi J: Studies of the causation of gastric cancer. The relation between gastric cancer mortality rate and salted food intake in several places in Japan. Bull Inst Public Health 8:187-193, 1959

    Google Scholar 

  4. Watanabe T, Tada M, Nagai H, Sasaki S, Nakao M: Helicobacter pylori infection induces cancer in Mongolian gerbils. Gastroenterology 115:642-648, 1998

    Google Scholar 

  5. Honda S, Fujioka T, Tokieda M, Satoh R, Nishizono A, Nasu M: Development of Helicobacter pylori-induced gastric carcinoma in Mongolian gerbils. Cancer Res 58:4255-4259, 1999

    Google Scholar 

  6. Hirayama F, Takagi S, Iwao E, Yokoyama Y, Haga K, Hanada S: Development of poorly differentiated adenocarcinoma and carcinoid due to long-term Helicobacter pylori colonization in Mongolian gerbils. J Gastroenterol 34:450-454, 1999

    Google Scholar 

  7. Ogura K, Maeda S, Nakao M, Watanabe T, Tada M, Kyutoku T, Yoshida H, Shiratori, Y, Omata M: Virulence factors of Helicobacter pylori responsible for gastric diseases in Mongolian gerbils. J Exp Med 192:1601-1610, 2000

    Google Scholar 

  8. Sugiyama A, Maruta F, Ikeno T, Ishida K, Kawasaki S, Katsuyama T, Shimizu N, Tatematsu M: Helicobacter pylori infection enhances N-methyl-N′-nitrosourea-induced stomach carcinogenesis in the Mongolian gerbil. Cancer Res 58:2067-2069, 1998

    Google Scholar 

  9. Honda S, Fujioka, T, Tokieda M, Gotoh T, Nishizono A, Nasu M: Gastric ulcer, atrophic gastritis, and intestinal metaplasia caused by Helicobacter pylori infection in Mongolian gerbils. Scand J Gastroenterol 33:454-460, 1998

    Google Scholar 

  10. Sawada Y, Yamamoto N, Sakagami T, Fukuda Y, Shimoyama T, Nishigami T, Uematsu K, Nakagawa K: Comparison of pathological changes in Helicobacter pylori-infected Mongolian gerbils and humans. J Gastroenterol 34 (suppl XI):55-60, 1999

    Google Scholar 

  11. Ikeno T, Ota H, Sugiyama A, Ishida K, Katsuyama T, Genta RM, Kawasaki S: Helicobacter pylori-induced chronic active gastritis, intestinal metaplasia, and gastric ulcer in Mongolian gerbils. Am J Pathol 154:951-960, 1999

    Google Scholar 

  12. Wirth HP, Beins MH, Yang M, Tham KT, Blaser MJ: Experimental infection of Mongolian gerbils with wild-type and mutant Helicobacter pylori strains. Infect Immun 66:4856-4866, 1998

    Google Scholar 

  13. Israel DA, Peek Jr RM: Pathogenesis of Helicobacter pylori-induced gastric inflammation. Alim Pharmacol Ther 9:1271-1290, 2001

    Google Scholar 

  14. Israel DA, Salama N, Arnold CN, Moss SF, Ando T, Wirth HP, Tham KT, Camorlinga M, Blaser MJ, Falkow S, Peek Jr RM: Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J Clin Invest 107:611-620, 2001

    Google Scholar 

  15. Lee A, O'Rourke J, Corazon de Ungria M, Robertson B, Daskalopoulos G, Dixon MF: A standardized model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386-1397, 1997

    Google Scholar 

  16. The EuroGast Study Group: Epidemiology of and risk factors for Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations. Gut 34:1672-1676, 1993

    Google Scholar 

  17. The Eurogast Study Group: An international association between Helicobacter pylori infection and gastric cancer. Lancet 341:1359-1362, 1993

    Google Scholar 

  18. Sakagami T, Dixon M, O'Rourke J, Howlett R, Alderuccio F, Vella J, Shimoyama T, Lee A: Atrophic gastric changes in both Helicobacter felis and Helicobacter pylori infected mice are host dependent and separate from antral gastritis. Gut 39:639-640, 1996

    Google Scholar 

  19. Neumann K, Maak S, Stuermer IW, von Lengerken G, Gattermann R: Low microsatellite variation in laboratory gerbils. J. Hered 92:71-74, 2001

    Google Scholar 

  20. Matsumoto S, Washizuka Y, Matsumoto Y, Tawara S, Ikeda, F, Yokota Y, Karita M: Induction of ulceration and severe gastritis in Mongolian gerbils by Helicobacter pylori infection. J Med Microbiol 46:391-397, 1997

    Google Scholar 

  21. DeKoster E, Buset M, Fernandes E, Willems D, Deprez C, Deltenre M, Galand P: Influence of sodium intake on gastric antrum and corpus mucosal cell proliferation status. Acta Gastroenterol Belg 56(suppl):54, 1993

    Google Scholar 

  22. Fox JG, Dangler CA, Taylor NS, King A, Koh TJ, Wang TC: High salt diet induces gastric epithelial hyperplasia and parietal cell loss and enhances Helicobacter pylori colonization in C57BL/6 mice. Cancer Res 59:4823-4828, 1999

    Google Scholar 

  23. Peek RM Jr, Wirth HP, Moss SF, Yang M, Abdalia AM, Tham KT, Zhang T, Tang LH, Modlin IM, Blaser MJ: Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils. Gastroenterology 118:48-59, 2000

    Google Scholar 

  24. Takashima M, Furuta T, Hanai H, Sugimura H, Kaneka E: Effect of Helicobacter pylori infection on gastric acid secretion and serum gastrin levels in Mongolian gerbils. Gut 48:765-773, 2001

    Google Scholar 

Download references

Authors
  1. Ingrid L. Bergin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barbara J. Sheppard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James G. Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bergin, I.L., Sheppard, B.J. & Fox, J.G. Helicobacter pylori Infection and High Dietary Salt Independently Induce Atrophic Gastritis and Intestinal Metaplasia in Commercially Available Outbred Mongolian Gerbils. Dig Dis Sci 48, 475–485 (2003). https://doi.org/10.1023/A:1022524313355

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022524313355

  • Helicobacter pylori
  • gerbil
  • salt
  • intestinal metaplasia
  • gastric cancer