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In vivo studies of emergent issues in gastric Helicobacter pathogenesis and epidemiology

  • J. G. Fox
Chapter

Abstract

Since the original description of the bacterium by Warren and Marshall in 1983, Helicobacter pylori is now causally linked to a variety of pathological conditions of the human stomach, such as chronic gastritis, peptic ulcer disease, gastric adenocarcinoma and, most recently, gastric mucosa-associated lymphoid tissue lymphoma1–6. The discovery of H. pylori, and its emerging importance in gastric disease, has generated an enormous interest in dissecting the pathogenesis and epidemiology of H. pylori infection7,8. Early studies failed to establish H. pylori in animal models and, surprisingly, Koch’s postulates were initially fulfilled in two human volunteers9–11. These individuals suffered bouts of acute gastric symptomatology a few days after oral challenge with H. pylori, and in one of them a persistent gastritis was established10,11.

Keywords

Gastric Mucosa Pylorus Infection Clinical Cure Pylorus Strain Pylorus Isolate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Marshall BJ, Warren JR. Unidentified curved bacillus on gastric epithelium in active chronic gastritis. Lancet. 1983;1:1273–5.Google Scholar
  2. 2.
    Correa P, Fox JG, Fontham E. Helicobacter pylori and gastric carcinoma: serum antibody prevalence in populations with contrasting cancer risks. Cancer. 1990;66:2569–74.PubMedCrossRefGoogle Scholar
  3. 3.
    Graham DY. Campylobacter pylori and peptic ulcer disease. Gastroenterology. 1989;96:615–23.PubMedGoogle Scholar
  4. 4.
    Graham DY, Lew GM, Klein PD et al. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer: a randomized controlled study. Ann Intern Med. 1992;116:705–8.PubMedGoogle Scholar
  5. 5.
    Parsonnet J, Friedman GD, Vandersteen DP. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991;325:1127–31.PubMedCrossRefGoogle Scholar
  6. 6.
    Parsonnet J, Hanson S, Rodriguez L. Helicobacter pylori infection and gastric MALT lymphoma. N Engl J Med. 1994;330:1267–71.PubMedCrossRefGoogle Scholar
  7. 7.
    Blaser MJ. Helicobacter pylori: its role in disease. J Clin Infect. 1992;15:386–93.CrossRefGoogle Scholar
  8. 8.
    Lee A, Fox JG, Hazell S. Pathogenicity of Helicobacter pylori: a perspective. Infect Immun. 1993; 61:1601–10.PubMedGoogle Scholar
  9. 9.
    Fox JG. In vivo models of gastric Helicobacter infections. In: Hunt RH, Tytgat G, editors. Helicobacter pylori: Basic mechanisms to clinical cure. Dordrecht: Kluwer; 1994:3–27.Google Scholar
  10. 10.
    Marshall BJ, Armstrong JA, McGechie B, Glancy RJ. Attempt to fulfill Koch’s postulates for pyloric Campylobacter. Med J Aust. 1985;142:436–9.PubMedGoogle Scholar
  11. 11.
    Morris A, Nicholson G. Ingestion of Campylopyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol. 1987;82:192–9.PubMedGoogle Scholar
  12. 12.
    Krakowka S, Morgan DR, Kraft WG et al. Establishment of gastric Campylobacter pylori infection in the neonatal gnotobiotic piglet. Infect Immun. 1987;55:2789–96.PubMedGoogle Scholar
  13. 13.
    Yoshihiro F, Yamamoto I, Tonokatsu Y, Tamura K, Shimoyama T. Inoculation of animals with human Helicobacter pylori and long-term investigation of Helicobacter pylori-associated gastritis. Eur J Gastroenterol Hepatol. 1992;4:S39–44.Google Scholar
  14. 14.
    Cantorna MT, Balish E. Inability of human clinical isolates of Helicobacter pylori to colonize the alimentary tract of germ-free rodents. Can J Microbiol. 1990;36:237–41.PubMedCrossRefGoogle Scholar
  15. 15.
    Fox JG, Otto G, Murphy JC et al. Gastric colonization of the ferret with Helicobacter species: natural and experimental infections. Rev Infect Dis. 1991;13(Suppl. 8):S671–80.PubMedCrossRefGoogle Scholar
  16. 16.
    Bronsdon MA, Goodwin CS, Sly LI. Helicobacter nemestrinae sp. nov., a spiral bacterium found in the stomach of a pigtailed macaque (Macaca nemestrina). Int J Syst Bacteriol. 1991;41:148–53.PubMedCrossRefGoogle Scholar
  17. 17.
    Eaton KA, Dewhirst FE, Radin MJ. Helicobacter acinonyx sp. nov., isolated from cheetahs with gastritis. Int J Syst Bacteriol. 1993;43:99–106.PubMedCrossRefGoogle Scholar
  18. 18.
    Fox JG, Taylor NS, Edmonds P. Campylobacter pylori subspecies mustelae subsp. nov. isolated from the gastric mucosa of ferrets (Mustela putorius furo), and an emended description of Campylobacter pylori. Int J Syst Bacteriol. 1988;38:367–70.CrossRefGoogle Scholar
  19. 19.
    Fox JG, Chilvers T, Goodwin CS. Campylobacter mustelae, a new species resulting from the elevation of Campylobacter pylori subsp. mustelae to species status. Int J Syst Bacteriol. 1989;39:301–3.CrossRefGoogle Scholar
  20. 20.
    Lee A, Hazell SL, O’Rourke J. Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun. 1988;56:2843–50.PubMedGoogle Scholar
  21. 21.
    Paster BJ, Lee A, Fox JG. Phylogeny of Helicobacter felis sp. nov., Helicobacter mustelae, and related bacteria. Int J Syst Bacteriol. 1991;41:31–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Hanninen ML, Happonen I, Saari S. Culture and characteristics of Helicobacter bizzozeronii, a new canine gastric Helicobacter sp. Int J Syst Bacteriol. 1996;46:160–6.PubMedCrossRefGoogle Scholar
  23. 23.
    Lambert JR, Borromes M, Pinkard KJ et al. Colonization of gnotobiotic piglets with Campylobacter pyloridis — an animal model? [letter]. J Infect Dis. 1987; 155:1344.PubMedCrossRefGoogle Scholar
  24. 24.
    Radin JM, Eaton KA, Krakowka S et al. Helicobacter pylori infection in gnotobiotic beagle dogs. Infect Immun. 1990;58:2606–12.PubMedGoogle Scholar
  25. 25.
    Baskerville A, Newell DG. Naturally occurring chronic gastritis and C. pylori infection in the rhesus monkey: a potential model for gastritis in man. Gut. 1988;29:465–72.PubMedCrossRefGoogle Scholar
  26. 26.
    Dubois A, Fiala N, Heman-Ackah LM. Natural gastric infection with Helicobacter pylori in monkeys: a model for spiral bacteria infection in humans. Gastroenterology. 1994; 106:1405–17.PubMedGoogle Scholar
  27. 27.
    Handt LK, Fox JG, Dewhirst FE et al. Helicobacter pylori isolated from the domestic cat: public health implications. Infect Immun. 1994;62:2367–74.PubMedGoogle Scholar
  28. 28.
    Handt LK, Fox JG, Stalis IH et al. Characterization of feline Helicobacter pylori strains and associated gastritis in a colony of domestic cats. J Clin Microbiol. 1995;33:2280–9.PubMedGoogle Scholar
  29. 29.
    Karita M, Kouchiyama T, Okita K, Nakazawa T. New small animal model for human gastric Helicobacter pylori infection: success in both nude and euthymic mice. Am J Gastroenterol. 1991; 86:1596–603.PubMedGoogle Scholar
  30. 30.
    Karita M, Li Q, Cantero D, Okita K. Establishment of a small animal model for human H. pylori infection using germ-free mouse. Am J Gastroenterol. 1994;89:208–13.PubMedGoogle Scholar
  31. 31.
    Marchetti M, Arico B, Burroni D, Figura N, Rappuoli R, Ghiara P. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science. 1995;267:1655–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Fox JG, Batchelder M, Marini RP et al. Helicobacter pylori induced gastritis in the domestic cat. Infect Immun. 1995;63:2674–81.PubMedGoogle Scholar
  33. 33.
    Finlay BB, Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989;53:210–30.PubMedGoogle Scholar
  34. 34.
    Eaton KA, Morgan DR, Krakowka S. Campylobacter pylori virulence factors in gnotobiotic piglets. Infect Immun. 1989;57:1119–25.PubMedGoogle Scholar
  35. 35.
    Leying H, Suerbaum S, Geis G, Haas R. Cloning and genetic characterization of a Helicobacter pylori flagellin gene. Mol Microbiol. 1992;6:2863–74.PubMedCrossRefGoogle Scholar
  36. 36.
    Kostrzynska M, Betts JD, Austin JW, Trust TJ. Identification, characterization, and spatial localization of two flagellin species in Helicobacter pylori flagella. J Bacteriol. 1991;173:937–46.PubMedGoogle Scholar
  37. 37.
    Suerbaum S, Josenhans D, Labigne A. Cloning and genetic characterization of the Helicobacter pylori and Helicobacter mustelae flaB flagellin genes and construction of H. pylori flaA- and flaB-negative mutants by electroporation-mediated allelic exchange. J Bacteriol. 1993,175:3278–88.PubMedGoogle Scholar
  38. 38.
    Haas R, Meyer JF, Putten JPMV. Aflagellated mutants of Helicobacter pylori generated by genetic transformation of naturally competent strains using transposon shuttle mutagenesis. Mol Microbiol. 1993;8:753–60.PubMedCrossRefGoogle Scholar
  39. 39.
    Josenhans C, Labigne A, Suerbaum S. Comparative ultrastructural and functional studies of Helicobacter pylori and Helicobacter mustelae flagellin mutants: both flagellin subunits, FlaA and FlaB, are necessary for full motility in Helicobacter species. J Bacteriol. 1995;177:3010–20.PubMedGoogle Scholar
  40. 40.
    Eaton K, Suerbaum S, Josenhans C, Krakowka S. Colonization of gnotobiotic piglets by H. pylori deficient in two flagellin genes. Infect Immun. 1996;64:2445–8.PubMedGoogle Scholar
  41. 41.
    Hazell SL, Lee A, Brady L et al. Campylobacter pyloridis and gastritis: association with intercellular spaces and adaption to an environment of mucus as important factors in colonization of the gastric epithelium. J Infect Dis. 1986;153:658–63.PubMedCrossRefGoogle Scholar
  42. 42.
    Hazell SL, Lee A. Campylobacter pyloridis, urease, hydrogen ion back diffusion and gastric ulcers. Lancet. 1986;2:15–17.PubMedCrossRefGoogle Scholar
  43. 43.
    Eaton KA, Brooks CL, Morgan DR, Krakowka S. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect Immun. 1991;59:2470–5.PubMedGoogle Scholar
  44. 44.
    Labigne A, Cussac V, Courcoux P. Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity. J Bacteriol. 1992;173:1920–31.Google Scholar
  45. 45.
    Ferrero RL, Cussav C, Courcoux P, Labigne A. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol. 1992;174:4212–17.PubMedGoogle Scholar
  46. 46.
    Eaton KA, Krakowka S. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. Infect Immun. 1994;62:3604–7.PubMedGoogle Scholar
  47. 47.
    Tsuda M, Karita M, Morshed MG, Okira K, Nakazawa T. A urease-negative mutant of Helicobacter pylori constructed by allelic exchange mutagenesis lacks the ability to colonize the nude mouse stomach. Infect Immun. 1994;62:3586–9.PubMedGoogle Scholar
  48. 48.
    Leunk RD, Johnson PT, David BC, Kraft WG, Morgan DR. Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J Med Microbiol. 1988;26:93–9.PubMedCrossRefGoogle Scholar
  49. 49.
    Figura N, Guglielmetti P, Rossolini A et al. Cytotoxin production by Campylobacter pylori strains isolated from patients with peptic ulcers and from patients with chronic gastritis only. J Clin Microbiol. 1989;27:225–6.PubMedGoogle Scholar
  50. 50.
    Fox JG, Correa P, Taylor NS et al. High prevalence and persistence of cytotoxin-positive Helicobacter pylori strains in a population at increased risk of gastric cancer. Am J Gastroenterol. 1992;87:1554–60.PubMedGoogle Scholar
  51. 51.
    Cover TJ, Vaughn SG, Cao P, Blaser MJ. Potentiation of Helicobacter pylori vacuolating toxin activity by nicotine and other weak bases. J Infect Dis. 1992; 166:1073–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Covacci A, Censini S, Bugnoli M et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci USA. 1993;90:5791–5.PubMedCrossRefGoogle Scholar
  53. 53.
    Tummuru MK, Cover TL, Blaser MJ. Cloning and expression of a high molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxicity. Infect Immun. 1993;61:1799–809.PubMedGoogle Scholar
  54. 54.
    Papini E, Bugnoli M, Bernard MD, Figura N, Rappuoli R, Montecucco C. Bafilomycin-Al inhibits Helicobacter pylori-induced vacuolization of HeLa cells. Mol Microbiol. 1993;7:323–7.PubMedCrossRefGoogle Scholar
  55. 55.
    Schmitt W, Haas R. Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the Ig A protease type of exported protein. Mol Microbiol. 1994;12:307–19.PubMedCrossRefGoogle Scholar
  56. 56.
    Eaton KA, Cover T, Tummuru MKR, Blaser MJ, Krakowka S. The role of vacuolating cytotoxin in gastritis due to H. pylori in gnotobiotic piglets, abstr 2434. In: Abstracts of the Meeting of the American Gastroenterological Association 1996. American Gastroenterological Association, San Francisco, CA.Google Scholar
  57. 57.
    Ghiara P, Marchetti M, Blaser MJ, et al. Role of the Helicobacter pylori virulence factor vacuolating cytotoxin, CagA, and urease in a mouse model of disease. Infect Immun. 1995;63:4154–60.PubMedGoogle Scholar
  58. 58.
    Phadnis SH, Liver D, Janzon L, Normark S, Westblom TU. Pathological significance and molecular characterization of the vacuolating toxin gene of Helicobacter pylori. Infect Immun. 1994;62:1557–65.PubMedGoogle Scholar
  59. 59.
    Telford JL, Dell’Orco M, Burroni D et al. Molecular analysis of the Helicobacter pylori cytotoxin gene. Eur J Gastroenterol Hepatol. 1993;5:S22–4.Google Scholar
  60. 60.
    Telford JL, Ghiara P, Dell’Orco M et al. Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J Exp Med. 1994; 179:1653–8.PubMedCrossRefGoogle Scholar
  61. 61.
    Sobóla GM, Crabtree JE, Dixon MF et al. Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentration. Gut. 1991;32:1415–18.CrossRefGoogle Scholar
  62. 62.
    Mitchell HM, Hazell SL, Kolesnikow R, Mitchell J, Frommer D. Antigen recognition during progression from acute to chronic infection with a azgA-positive strain of Helicobacter pylori. Infect Immun. 1996;64:1166–72.PubMedGoogle Scholar
  63. 63.
    McColm AA, Bagshaw J, O’Malley C, McLaren A. Development of a mouse model of gastric colonisation with Helicobacter pylori. Gut. 1995;37(Suppl. 1);A50.CrossRefGoogle Scholar
  64. 64.
    Kleanthous H, Tibbitts T, Bakios TJ et al. In vivo selection of a highly adapted H. pylori isolate and the development of an H. pylori mouse model for studying vaccine efficacy and attenuating lesions. Gut. 1995;37(Suppl. 1);A94.Google Scholar
  65. 65.
    Fox JG, Edrise BM, Cabot E et al. Campylobacter-Wke organisms isolated from gastric mucosa of ferrets. Am J Vet Res. 1986;47:236–9.PubMedGoogle Scholar
  66. 66.
    Fox JG, Cabot EB, Taylor NS et al. Gastric colonization of Campylobacter pylori subsp. mustelae in ferrets. Infect Immun. 1988;56:2994–6.PubMedGoogle Scholar
  67. 67.
    Fox JG, Correa P, Taylor NS et al. Helicobacter mustelae associated gastritis in ferrets: an animal model of Helicobacter pylori gastritis in humans. Gastroenterology. 1990;99:352–61.PubMedGoogle Scholar
  68. 68.
    Gottfried MR, Washington K, Harrell LJ. Helicobacter pylori-like microorganisms and chronic active gastritis in ferrets. Am J Gastroenterol. 1990;85:813–18.PubMedGoogle Scholar
  69. 69.
    Tompkins DS, Wyatt JI, Rathbone BJ et al. The characterization and pathological significance of gastric Campylobacter-like organisms in the ferret: a model for chronic gastritis? Epidemiol Infect. 1988;101:269–78.PubMedCrossRefGoogle Scholar
  70. 70.
    Morris A, Thomasen L, Tasman-Jones C et al. Failure to detect gastric Campylobacter-like organisms in a group of ferrets in New Zealand. NZ Med J. 1988; 101:275.Google Scholar
  71. 71.
    O’Rourke J, Lee A, Fox JG. An ultrastructural study of Helicobacter mustelae: evidence of a specific association with gastric mucosa. J Med Microbiol. 1992;36:420–7.PubMedCrossRefGoogle Scholar
  72. 72.
    Chen XG, Correa P, Offerhaus J et al. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am J Clin Pathol. 1986;86:575–82.PubMedGoogle Scholar
  73. 73.
    Gold BD, Huesca M, Sherman PM et al. Helicobacter mustelae and Helicobacter pylori bind to common lipid receptors in vitro. Infect Immun. 1993;61:2632–8.PubMedGoogle Scholar
  74. 74.
    Gold B, Dytoc M, Huesca M et al. Comparison of Helicobacter mustelae and Helicobacter pylori adhesion to eukaryotic cells in vitro. Gastroenterology. 1995;109:692–700.PubMedCrossRefGoogle Scholar
  75. 75.
    Gold BD, Islur P, Policova Z, Czinn S, Neumann AW, Sherman PM. Surface properties of H. mustelae and ferret gastrointestinal mucosa. Clin Invest Med. 1996;19:92–100.PubMedGoogle Scholar
  76. 76.
    Northfield TC. Decreased hydrophobicity of gastroduodenal mucosa due to H. pylori infection in humans. In: Hunt RH, Tytgat G, editors. Helicobacter pylori: basic mechanisms to clinical cure. Dordrecht: Kluwer; 1994:139–47.Google Scholar
  77. 77.
    O’Toole PW, Austin JW, Trust TJ. Identification and molecular characterization of a major ring-forming surface protein from the gastric pathogen Helicobacter mustelae. Mol Microbiol. 1994; 11:349–61.PubMedCrossRefGoogle Scholar
  78. 78.
    Kay WW, Trust TJ. Form and function of the regular surface array of Aeromonas salmonicida. Experientia. 1991;47:412–14.PubMedGoogle Scholar
  79. 79.
    Schauer DB, Fox JG. Examining the surface of a gastric pathogen. Trends Microbiol. 1994;2:219–20.PubMedCrossRefGoogle Scholar
  80. 80.
    Solnick J, Josenhans C, Suerbaum S, Tompkins L, Labigne A. Construction and characterization of an isogenic urease-negative mutant of Helicobacter mustelae. Infect Immun. 1995;63:3718–23.PubMedGoogle Scholar
  81. 81.
    Andrutis KA, Fox JG, Schauer DB et al. Identification of a cagA gene in Helicobacter mustelae. Gut. 1995;37(Suppl. 1):A30.CrossRefGoogle Scholar
  82. 82.
    Andrutis KA, Fox JG, Josenhans C, Suerbaum S. Infection of the ferret stomach by isogenic flagellar mutant strains of Helicobacter mustelae, abstr 1203. In: Abstracts of the Meeting of the American Gastroenterological Association 1996. American Gastroenterological Association, San Francisco, CA.Google Scholar
  83. 83.
    Andrutis KA, Fox JG, Schauer DB et al. Inability of an isogenic urease-negative mutant strain of Helicobacter mustelae to colonize the ferret stomach. Infect Immun. 1995;63:3722–5.PubMedGoogle Scholar
  84. 84.
    Perkins SE, Fox JG, Walsh JH. Helicobacter mustelae associated hypergastrinemia in ferrets (Mustelae putorius furo). Am J Vet Res. 1996;57:147–50.PubMedGoogle Scholar
  85. 85.
    Fox JG, Paster BJ, Dewhirst FE et al. Helicobacter mustelae isolation from feces of ferrets: evidence to support fecal-oral transmission of a gastric Helicobacter. Infect Immun. 1992; 60:606–11.PubMedGoogle Scholar
  86. 86.
    Fox JG, Otto G, Taylor NS et al. Helicobacter mustelae-induced gastritis and elevated gastric pH in the ferret (Mustela putorius furo). Infect Immun. 1991;59:1875–80.PubMedGoogle Scholar
  87. 87.
    Fox JG, Blanco M, Yan L et al. Role of gastric pH in isolation of Helicobacter mustelae from the feces of ferrets. Gastroenterology. 1993;104:86–92.PubMedGoogle Scholar
  88. 88.
    Thomas JE, Gibson GR, Darboe MK et al. Isolation of Helicobacter pylori from human feces. Lancet. 1992;340:1194–5.PubMedCrossRefGoogle Scholar
  89. 89.
    Kelly SM, Pitcher MCL, Farmery SM et al. Isolation of Helicobacter pylori from feces of patients with dyspepsia in the United Kingdom. Gastroenterology. 1994; 107:1671–4.PubMedGoogle Scholar
  90. 90.
    Doenges JL. Spirochetes in the gastric glands of macacas rhesus and of man without related disease. Arch Pathol. 1939;27:469–77.Google Scholar
  91. 91.
    Bronsdon MA, Schoenknecht FD. Campylobacter pylori isolated from the stomach of the monkey, Macaca nemistrina. J Clin Microbiol. 1988,26:1725–8.PubMedGoogle Scholar
  92. 92.
    Newell DG, Hudson MJ, Baskerville A. Isolation of a gastric Campylobacter-like organism from the stomach of four rhesus monkeys, and identification as Campylobacter pylori. J Med Microbiol. 1988;27:41–4.PubMedCrossRefGoogle Scholar
  93. 93.
    Curry A, Jones DM, Eldridge J. Spiral organism in the baboon stomach. Lancet. 1987;2:634–5.PubMedCrossRefGoogle Scholar
  94. 94.
    Euler AR, Zurenko GE, Moe JB et al. Evaluation of two monkey species (Macaca mulatta and Macaca fascicularis) as possible models for human Helicobacter pylori disease. J Clin Microbiol. 1990;28:2285–90.PubMedGoogle Scholar
  95. 95.
    Dubois A, Tarnawski A, Newell DG et al. Gastric injury and invasion of parietal cells by spiral bacteria in rhesus monkeys: are gastritis and hyperchlorhydria infectious diseases? Gastroenterology. 1991;100:884–91.PubMedGoogle Scholar
  96. 96.
    Sly LI, Bronsdon MA, Bowman JP et al. The phylogenetic position of Helicobacter nemestrinae. Int J Syst Bacteriol. 1993;43:386–7.PubMedCrossRefGoogle Scholar
  97. 97.
    Drazek ES, Dubois A, Holmes RK. Characterization and presumptive identification of Helicobacter pylori isolates from rhesus monkeys. J Clin Microbiol. 1994;32:1799–804.PubMedGoogle Scholar
  98. 98.
    Akopyants NS, Eaton KA, Berg DE. Adaptive mutation and cocolonization during Helicobacter pylori infection of gnotobiotic piglets. Infect Immun. 1995;63:116–21.PubMedGoogle Scholar
  99. 99.
    Hazell SL, Eichberg JW, Lee RD et al. Selection of the chimpanzee over the baboon as a model for Helicobacter pylori infection. Gastroenterology. 1992; 103:848–54.PubMedGoogle Scholar
  100. 100.
    Fujioka T, Shuto R, Kodama R et al. Experimental model for chronic gastritis with Helicobacter pylori: long term follow up study in H. pylori-infected Japanese macaques. Eur J Gastroenterol Hepatol. 1993;S1:S73–7.Google Scholar
  101. 101.
    Fukuda Y, Yamamoto I, Tonokatsu Y et al. Inoculation of rhesus monkeys with human Helicobacter pylori: a long-term investigation on gastric mucosa by endoscopy. Dig Endosc. 1992;4:19–30.CrossRefGoogle Scholar
  102. 102.
    Shuto R, Fujioka T, Kubota I et al. Experimental gastritis induced by Helicobacter pylori in Japanese monkeys. Infect Immun. 1993;61:933–9.PubMedGoogle Scholar
  103. 103.
    Fujiyama K, Fujioka T, Murakami K et al. Effects of Helicobacter pylori on gastric mucosal defense factors in Japanese monkeys. J Gastroenterol. 1995;30:441–6.PubMedCrossRefGoogle Scholar
  104. 104.
    Heilmann KL, Borchard F. Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut. 1991;32:137–40.PubMedCrossRefGoogle Scholar
  105. 105.
    Stolte M, Wellens E, Bethke B. Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scand J Gastroenterol. 1994;29:1061–4.PubMedCrossRefGoogle Scholar
  106. 106.
    Fox JG, Perkins S, Shen Z et al. Local immune response in Helicobacter pylori infected cats and identification of H. pylori in saliva, gastric fluid and feces. Immunology. 1996;88:400–6.PubMedCrossRefGoogle Scholar
  107. 107.
    Otto G, Hazell SH, Fox JG et al. Animal and public health implications of gastric colonization of cats by Helicobacter-like organisms. J Clin Microbiol. 1994;32:1043–9.PubMedGoogle Scholar
  108. 108.
    Henry GA, Long PH, Burns JL et al. Gastric spirillosis in beagles. Am J Vet Res. 1987;48:831–6.PubMedGoogle Scholar
  109. 109.
    Eaton KA, Radin MJ, Kramer L et al. Epizoonotic gastritis associated with gastric spiral bacilli in cheetahs (Acinonyx jubatus). Vet Pathol. 1993;30:55–63.PubMedCrossRefGoogle Scholar
  110. 110.
    Lockard VG, Boler RK. Ultrastructure of a spiraled microorganism in the gastric mucosa of dogs. Am J Vet Res. 1970;31:1453–62.PubMedGoogle Scholar
  111. 111.
    Lavelle JP, Landas S, Mitros FA et al. Acute gastritis associated with spiral organisms from cats. Dig Dis Sci. 1994;39:744–50.PubMedCrossRefGoogle Scholar
  112. 112.
    Salomon H. Über das Spirillum des Säugetiermagens und sein Verhalten zu den Belegzellen. Zentralbl Baketeriol Parasitenkd Infektionskr Hyg Abt. 1898; 119:422–41.Google Scholar
  113. 113.
    Lee A, Fox JG, Otto G et al. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology. 1990;99:1315–23.PubMedGoogle Scholar
  114. 114.
    Fox JG, Blanco M, Murphy JC et al. Local and systemic immune response in murine Helicobacter felis active chronic gastritis. Infect Immun. 1993;61:2309–15.PubMedGoogle Scholar
  115. 115.
    Mohammadi M, Redline R, Nedrud J et al. Role of the host in pathogenesis of Helicobacter-associated gastritis: H. felis infection of inbred and congenic mouse strains. Infect Immun. 1996;64:238–45.PubMedGoogle Scholar
  116. 116.
    Sakagami T, Shimoyama T, O’Rourke J et al. Back to the host: severity of inflammation induced by Helicobacter felis in different strains of mice. Am J Gastroenterol. 1994;89:1345 (abstract 241).Google Scholar
  117. 117.
    Fox JG, Li X, Cahill RJ et al. Hypertrophic gastropathy in Helicobacter felis infected wild type C57B1/6 mice and p53 hemizygous transgenic mice. Gastroenterology. 1996; 110:155–66.PubMedCrossRefGoogle Scholar
  118. 118.
    Enno A, O’Rourke JL, Howlett CR, Jack A, Dixon MF, Lee A. MALToma-like lesions in the murine gastric mucosa after long-term infection with Helicobacter felis. Am J Pathol. 1995; 147:217–23.PubMedGoogle Scholar
  119. 119.
    Chen M-H, Lee A, Hazell S et al. Immunisation against gastric Helicobacter infection in a mouse/Helicobacter felis model [letter]. Lancet. 1992;339:1120–1.PubMedCrossRefGoogle Scholar
  120. 120.
    Czinn SJ, Cai A, Nedrud JG. Protection of germ-free mice from infection by Helicobacter felis after active oral or passive IgA immunization. Vaccine. 1993; 11:637–42.PubMedCrossRefGoogle Scholar
  121. 121.
    Ferrero RL, Thieberge JM, Huerre M, Labigne A. Recombinant antigens prepared from the urease subunits of Helicobacter spp.: evidence of protection in a mouse model of gastric infection. Infect Immun. 1994;62:4981–9.PubMedGoogle Scholar
  122. 122.
    Michetti P, Corthesy-Theulaz I, Davin C et al. Immunization of BALB/c mice against Helicobacter felis infection with Helicobacter pylori urease. Gastroenterology. 1994; 107:1002–11.PubMedGoogle Scholar
  123. 123.
    Pappo J, Thomas W, Kabok Z, Taylor NS, Murphy JC, Fox JG. Effect of oral immunization with recombinant urease on murine Helicobacter felis gastritis. Infect Immun. 1995;63:1246–53.PubMedGoogle Scholar
  124. 124.
    Doidge C, Gust I, Lee A. Therapeutic immunization against Helicobacter infection (letter). Lancet. 1994;343:914–5.PubMedCrossRefGoogle Scholar
  125. 125.
    Engstrand L, Rosberg K, Hubinette R, Berglindh T, Rolfsen W, Gustavsson S. Topographic mapping of Helicobacter pylori colonization in long-term infected pigs. Infect Immun. 1992; 60:653–6.PubMedGoogle Scholar
  126. 126.
    Eaton KA, Morgan DR, Krakowka S. Persistence of Helicobacter pylori in conventionalized piglets. J Infect Dis. 1990; 161:1299–301.PubMedCrossRefGoogle Scholar
  127. 127.
    Eaton KA, Radin MJ, Krakowka S. Animal model of gastric ulcer due to bacterial gastritis in mice. Vet Pathol. 1995;32:489–97.PubMedCrossRefGoogle Scholar
  128. 128.
    Fox JG, Otto G, Lee A, Taylor NS, Murphy JC. Helicobacter felis gastritis in gnotobiotic rats: an animal model of H. pylori gastritis. Infect Immun. 1991;59:785–91.PubMedGoogle Scholar
  129. 129.
    Lee A, Krakowka S, Fox JG, Otto G, Murphy JC. Helicobacter felis as a cause of lympho-reticular hyperplasia in the dog stomach. Vet Pathol. 1992;29:487–94.PubMedCrossRefGoogle Scholar
  130. 130.
    Takagi H, Jhappan C, Sharp R, Merlino G. Hypertrophic gastropathy resembling Menetrier’s disease in transgenic mice overexpressing transforming growth factor α in the stomach. J Clin Invest. 1992;90:1161–7.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers and Axcan Pharma 1996

Authors and Affiliations

  • J. G. Fox

There are no affiliations available

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