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. 1991 Jun;59(6):1875–1880. doi: 10.1128/iai.59.6.1875-1880.1991

Helicobacter mustelae-induced gastritis and elevated gastric pH in the ferret (Mustela putorius furo).

J G Fox 1, G Otto 1, N S Taylor 1, W Rosenblad 1, J C Murphy 1
PMCID: PMC257936  PMID: 2037349

Abstract

Helicobacter mustelae has been cultured from the stomachs of ferrets with chronic gastritis; the lesions in the stomach have many of the same histological features seen in H. pylori gastritis in humans. To determine whether H. mustelae-negative ferrets with normal gastric mucosa were susceptible to colonization and whether gastritis developed after infection, four H. mustelae-negative ferrets treated with cimetidine were inoculated orally on two successive days with 3 ml (1.5 x 10(8) CFU) of H. mustelae; eight age-matched H. mustelae-negative ferrets served as controls. All four ferrets became colonized; H. mustelae persisted through week 24 of the study, as determined by positive gastric culture, tissue urease, and Warthin-Starry staining of gastric tissue. Superficial gastritis developed in the oxyntic gastric mucosa, and a full-thickness gastritis, composed primarily of lymphocytes and plasma cells plus small numbers of neutrophils and eosinophils, was present in the antrum. The inflammation was accompanied by an elevation of immunoglobulin G antibody to H. mustelae. At 4 weeks post-inoculation, the four infected (experimental) ferrets developed an elevated gastric pH (4.0 to 5.2) for 2 weeks. The eight control ferrets did not have gastritis; H. mustelae could not be demonstrated in gastric tissue via culture, nor was there an immune response to the bacteria. In ferrets, H. mustelae readily colonizes the stomach and produces a gastritis, a significant immune response, and, like H. pylori infection in humans, a transient elevated gastric pH after Helicobacter infection.

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Selected References

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  1. Barthel J. S., Westblom T. U., Havey A. D., Gonzalez F., Everett E. D. Gastritis and Campylobacter pylori in healthy, asymptomatic volunteers. Arch Intern Med. 1988 May;148(5):1149–1151. [PubMed] [Google Scholar]
  2. Baskerville A., Newell D. G. Naturally occurring chronic gastritis and C pylori infection in the rhesus monkey: a potential model for gastritis in man. Gut. 1988 Apr;29(4):465–472. doi: 10.1136/gut.29.4.465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cantorna M. T., Balish E. Inability of human clinical strains of Helicobacter pylori to colonize the alimentary tract of germfree rodents. Can J Microbiol. 1990 Apr;36(4):237–241. doi: 10.1139/m90-041. [DOI] [PubMed] [Google Scholar]
  4. Cave D. R., Vargas M. Effect of a Campylobacter pylori protein on acid secretion by parietal cells. Lancet. 1989 Jul 22;2(8656):187–189. doi: 10.1016/s0140-6736(89)90372-3. [DOI] [PubMed] [Google Scholar]
  5. Chen X. G., Correa P., Offerhaus J., Rodriguez E., Janney F., Hoffmann E., Fox J., Hunter F., Diavolitsis S. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am J Clin Pathol. 1986 Nov;86(5):575–582. doi: 10.1093/ajcp/86.5.575. [DOI] [PubMed] [Google Scholar]
  6. Czinn S. J., Dahms B. B., Jacobs G. H., Kaplan B., Rothstein F. C. Campylobacter-like organisms in association with symptomatic gastritis in children. J Pediatr. 1986 Jul;109(1):80–83. doi: 10.1016/s0022-3476(86)80579-0. [DOI] [PubMed] [Google Scholar]
  7. Engstrand L., Gustavsson S., Jörgensen A., Schwan A., Scheynius A. Inoculation of barrier-born pigs with Helicobacter pylori: a useful animal model for gastritis type B. Infect Immun. 1990 Jun;58(6):1763–1768. doi: 10.1128/iai.58.6.1763-1768.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fox J. G., Cabot E. B., Taylor N. S., Laraway R. Gastric colonization by Campylobacter pylori subsp. mustelae in ferrets. Infect Immun. 1988 Nov;56(11):2994–2996. doi: 10.1128/iai.56.11.2994-2996.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fox J. G., Correa P., Taylor N. S., Lee A., Otto G., Murphy J. C., Rose R. Helicobacter mustelae-associated gastritis in ferrets. An animal model of Helicobacter pylori gastritis in humans. Gastroenterology. 1990 Aug;99(2):352–361. doi: 10.1016/0016-5085(90)91016-y. [DOI] [PubMed] [Google Scholar]
  10. Fox J. G., Correa P., Taylor N. S., Zavala D., Fontham E., Janney F., Rodriguez E., Hunter F., Diavolitsis S. Campylobacter pylori-associated gastritis and immune response in a population at increased risk of gastric carcinoma. Am J Gastroenterol. 1989 Jul;84(7):775–781. [PubMed] [Google Scholar]
  11. Fox J. G., Edrise B. M., Cabot E. B., Beaucage C., Murphy J. C., Prostak K. S. Campylobacter-like organisms isolated from gastric mucosa of ferrets. Am J Vet Res. 1986 Feb;47(2):236–239. [PubMed] [Google Scholar]
  12. Fox J. G., Lee A. Gastric campylobacter-like organisms: their role in gastric disease of laboratory animals. Lab Anim Sci. 1989 Nov;39(6):543–553. [PubMed] [Google Scholar]
  13. Fox J. G., Lee A., Otto G., Taylor N. S., Murphy J. C. Helicobacter felis gastritis in gnotobiotic rats: an animal model of Helicobacter pylori gastritis. Infect Immun. 1991 Mar;59(3):785–791. doi: 10.1128/iai.59.3.785-791.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Graham D. Y., Alpert L. C., Smith J. L., Yoshimura H. H. Iatrogenic Campylobacter pylori infection is a cause of epidemic achlorhydria. Am J Gastroenterol. 1988 Sep;83(9):974–980. [PubMed] [Google Scholar]
  15. Hazell S. L., Borody T. J., Gal A., Lee A. Campylobacter pyloridis gastritis I: Detection of urease as a marker of bacterial colonization and gastritis. Am J Gastroenterol. 1987 Apr;82(4):292–296. [PubMed] [Google Scholar]
  16. Henry G. A., Long P. H., Burns J. L., Charbonneau D. L. Gastric spirillosis in beagles. Am J Vet Res. 1987 May;48(5):831–836. [PubMed] [Google Scholar]
  17. Krakowka S., Morgan D. R., Kraft W. G., Leunk R. D. Establishment of gastric Campylobacter pylori infection in the neonatal gnotobiotic piglet. Infect Immun. 1987 Nov;55(11):2789–2796. doi: 10.1128/iai.55.11.2789-2796.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee A., Fox J. G., Otto G., Murphy J. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology. 1990 Nov;99(5):1315–1323. doi: 10.1016/0016-5085(90)91156-z. [DOI] [PubMed] [Google Scholar]
  19. Lee A., Hazell S. L., O'Rourke J., Kouprach S. Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun. 1988 Nov;56(11):2843–2850. doi: 10.1128/iai.56.11.2843-2850.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lockard V. G., Boler R. K. Ultrastructure of a spiraled microorganism in the gastric mucosa of dogs. Am J Vet Res. 1970 Aug;31(8):1453–1462. [PubMed] [Google Scholar]
  21. Marshall B. J., Armstrong J. A., McGechie D. B., Glancy R. J. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust. 1985 Apr 15;142(8):436–439. doi: 10.5694/j.1326-5377.1985.tb113443.x. [DOI] [PubMed] [Google Scholar]
  22. Marshall B. J., Barrett L. J., Prakash C., McCallum R. W., Guerrant R. L. Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid. Gastroenterology. 1990 Sep;99(3):697–702. doi: 10.1016/0016-5085(90)90957-3. [DOI] [PubMed] [Google Scholar]
  23. Marshall B. J., Warren J. R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1984 Jun 16;1(8390):1311–1315. doi: 10.1016/s0140-6736(84)91816-6. [DOI] [PubMed] [Google Scholar]
  24. McNulty C. A., Dent J. C., Curry A., Uff J. S., Ford G. A., Gear M. W., Wilkinson S. P. New spiral bacterium in gastric mucosa. J Clin Pathol. 1989 Jun;42(6):585–591. doi: 10.1136/jcp.42.6.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Morris A., Nicholson G. Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol. 1987 Mar;82(3):192–199. [PubMed] [Google Scholar]
  26. Otto G., Fox J. G., Wu P. Y., Taylor N. S. Eradication of Helicobacter mustelae from the ferret stomach: an animal model of Helicobacter (Campylobacter) pylori chemotherapy. Antimicrob Agents Chemother. 1990 Jun;34(6):1232–1236. doi: 10.1128/aac.34.6.1232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Radin M. J., Eaton K. A., Krakowka S., Morgan D. R., Lee A., Otto G., Fox J. Helicobacter pylori gastric infection in gnotobiotic beagle dogs. Infect Immun. 1990 Aug;58(8):2606–2612. doi: 10.1128/iai.58.8.2606-2612.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ramsey E. J., Carey K. V., Peterson W. L., Jackson J. J., Murphy F. K., Read N. W., Taylor K. B., Trier J. S., Fordtran J. S. Epidemic gastritis with hypochlorhydria. Gastroenterology. 1979 Jun;76(6):1449–1457. [PubMed] [Google Scholar]
  29. Rauws E. A., Tytgat G. N. Cure of duodenal ulcer associated with eradication of Helicobacter pylori. Lancet. 1990 May 26;335(8700):1233–1235. doi: 10.1016/0140-6736(90)91301-p. [DOI] [PubMed] [Google Scholar]
  30. Sato T., Takeuchi A. Infection by spirilla in the stomach of the rhesus monkey. Vet Pathol Suppl. 1982 Sep;19 (Suppl 7):17–25. [PubMed] [Google Scholar]

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