Immunogenicity and pathogenicity of Helicobacter infections of veterinary animals

Veterinary Immunology and Immunopathology

Volumn 122, Issue 3-4, 2008, Pages 191-203

  Harbour, Stacey ^a   Sutton, Philip ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Bacterial pathogens; Helicobacter; Immunopathology; Zoonotic infections

Indexed keywords

ANIMAL WELFARE; BACTERIAL INFECTION; BACTERIAL TRANSMISSION; BIRD; CAT; DISEASE ASSOCIATION; DOG; ENTERITIS; EXPERIMENTAL MODEL; FARM ANIMAL; GALLSTONE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HEPATITIS; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOPATHOLOGY; INFLAMMATION; INTESTINE INFECTION; MAMMAL; NEOPLASM; NONHUMAN; PATHOGENESIS; PATHOGENICITY; REVIEW; TH1 CELL;

ANIMALS; ANIMALS, DOMESTIC; BIRDS; CATS; DOGS; HELICOBACTER; HELICOBACTER INFECTIONS;

ANIMALIA; AVES; BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI; MAMMALIA;

EID: 40849095897     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2007.12.003     Document Type: Review

References (138)

1. Akhiani A.A., Pappo J., Kabok Z., Schon K., Gao W., Franzen L.E., and Lycke N. Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells. J. Immunol. 169 (2002) 6977-6984
2. Andersen-Nissen E., Smith K.D., Strobe K.L., Barrett S.L., Cookson B.T., Logan S.M., and Aderem A. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 9247-9252
3. Bamford K.B., Fan X.J., Crowe S.E., Leary J.F., Gourley W.K., Luthra G.K., Brooks E.G., Graham D.Y., Reyes V.E., and Ernst P.B. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114 (1998) 482-492
4. Berg D.J., Davidson N., Kuhn R., Muller W., Menon S., Holland G., Thompson-Snipes L., Leach M.W., and Rennick D. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J. Clin. Invest. 98 (1996) 1010-1020
5. Bryner J.H., Ritchie A.E., Pollet L., Kirkbride C.A., and Collins J.E. Experimental infection and abortion of pregnant guinea pigs with a unique spirillum-like bacterium isolated from aborted ovine fetuses. Am. J. Vet. Res. 48 (1987) 91-95
6. Burich A., Hershberg R., Waggie K., Zeng W.P., Brabb T., Westrich G., Viney J.L., and Maggio-Price L. Helicobacter-induced inflammatory bowel disease in IL-10-and T cell-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281 (2001) G764-G778
7. Cahill R.J., Foltz C.J., Fox J.G., Dangler C.A., Powrie F., and Schauer D.B. Inflammatory bowel disease-an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect. Immun. 65 (1997) 3126-3131
8. Carvalho F., Seruca R., David L., Amorim A., Seixas M., Bennett E., Clausen H., and Sobrinhosimoes M. Muc1 gene polymorphism and gastric cancer-an epidemiological study. Glycoconjugate J. 14 (1997) 107-111
9. Ceelen L., Decostere A., Martel A., Pasmans F., and Haesebrouck F. First report of Helicobacter pullorum in the faeces of a diarrhoeic psittacine bird (Psephotus haematogaster). Vet. Rec. 159 (2006) 389-390
10. Ceelen L., Decostere A., Verschraegen G., Ducatelle R., and Haesebrouck F. Prevalence of Helicobacter pullorum among patients with gastrointestinal disease and clinically healthy persons. J. Clin. Microbiol. 43 (2005) 2984-2986
11. Ceelen L.M., Decostere A., Chiers K., Ducatelle R., Maes D., and Haesebrouck F. Pathogenesis of Helicobacter pullorum infections in broilers. Int. J. Food Microbiol. 116 (2007) 207-213
12. Claesson M.H., Rudolphi A., Kofoed S., Poulsen S.S., and Reimann J. CD4+ T lymphocytes injected into severe combined immunodeficient (SCID) mice lead to an inflammatory and lethal bowel disease. Clin. Exp. Immunol. 104 (1996) 491-500
13. Coldham, T., 2004. The detection and characterisation of Helicobacter species in Australian marsupials. Ph.D. Thesis. University of New South Wales, Sydney.
14. De Bock M., Van den Bulck K., Hellemans A., Daminet S., Coche J.C., Debongnie J.C., Decostere A., Haesebrouck F., and Ducatelle R. Peptic ulcer disease associated with Helicobacter felis in a dog owner. Eur. J. Gastroenterol. Hepatol. 19 (2007) 79-82
15. De Groote D., van Doorn L.J., Ducatelle R., Verschuuren A., Haesebrouck F., Quint W.G.V., Jalava K., and Vandamme P. 'Candidatus Helicobacter suis', a gastric helicobacter from pigs, and its phylogenetic relatedness to other gastrospirilla. Int. J. Syst. Bacteriol. 49 (1999) 1769-1777
16. De Groote D., van Doorn L.J., Ducatelle R., Verschuuren A., Tilmant K., Quint W.G.V., Haesebrouck F., and Vandamme P. Phylogenetic characterization of 'Candidatus Helicobacter bovis', a new gastric helicobacter in cattle. Int. J. Syst. Bacteriol. 49 (1999) 1707-1715
17. Dewhirst F.E., Fox J.G., Mendes E.N., Paster B.J., Gates C.E., Kirkbride C.A., and Eaton K.A. 'Flexispira rappini' strains represent at least 10 Helicobacter taxa. Int. J. Syst. Evol. Microbiol. 50 (2000) 1781-1787
18. Dewhirst F.E., Seymour C., Fraser G.J., Paster B.J., and Fox J.G. Phylogeny of Helicobacter isolates from bird and swine feces and description of Helicobacter pametensis sp. nov. Int. J. Syst. Bacteriol. 44 (1994) 553-560
19. Dicken B.J., Bigam D.L., Cass C., Mackey J.R., Joy A.A., and Hamilton S.M. Gastric adenocarcinoma: review and considerations for future directions. Ann. Surg. 241 (2005) 27-39
20. Dore M.P., Bilotta M., Vaira D., Manca A., Massarelli G., Leandro G., Atzei A., Pisanu G., Graham D.Y., and Realdi G. High prevalence of Helicobacter pylori infection in shepherds. Dig. Dis. Sci. 44 (1999) 1161-1164
21. Dore M.P., Sepulveda A.R., El-Zimaity H., Yamaoka Y., Osato M.S., Mototsugu K., Nieddu A.M., Realdi G., and Graham D.Y. Isolation of Helicobacter pylori from sheep-implications for transmission to humans. Am. J. Gastroenterol. 96 (2001) 1396-1401
22. Dore M.P., Sepulveda A.R., Osato M.S., Realdi G., and Graham D.Y. Helicobacter pylori in sheep milk. Lancet 354 (1999) 132
23. Eaton K.A., Dewhirst F.E., Radin M.J., Fox J.G., Paster B.J., Krakowka S., and Morgan D.R. Helicobacter acinonyx sp. nov., isolated from cheetahs with gastritis. Int. J. Syst. Bacteriol. 43 (1993) 99-106
24. Eaton K.A., Mefford M., and Thevenot T. The role of T cell subsets and cytokines in the pathogenesis of Helicobacter pylori gastritis in mice. J. Immunol. 166 (2001) 7456-7461
25. El-Omar E.M., Carrington M., Chow W.H., McColl K.E.L., Bream J.H., Young H.A., Herrera J., Lissowska J., Yuan C.C., Rothman N., Lanyon G., Martin M., Fraumeni J.F., and Rabkin C.S. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 404 (2000) 398-402
26. El-Omar E.M., Rabkin C.S., Gammon M.D., Vaughan T.L., Risch H.A., Schoenberg J.B., Stanford J.L., Mayne S.T., Goedert J., Blot W.J., Fraumeni Jr. J.F., and Chow W.H. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 124 (2003) 1193-1201
27. Erdman S.E., Poutahidis T., Tomczak M., Rogers A.B., Cormier K., Plank B., Horwitz B.H., and Fox J.G. CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am. J. Pathol. 162 (2003) 691-702
28. Erginsoy S.D., Sozmen M., Ozcan K., and Tuzcu M. Occurrence of Helicobacter infection in the gastric mucosa of free-living red foxes (Vulpes vulpes). J. Wildl. Dis. 40 (2004) 548-554
29. Foley J.E., Marks S.L., Munson L., Melli A., Dewhirst F.E., Yu S.L., Shen Z.L., and Fox J.G. Isolation of Helicobacter canis from a colony of Bengal cats with endemic diarrhea. J. Clin. Microbiol. 37 (1999) 3271-3275
30. Foley J.E., Solnick J.V., Lapointe J.M., Jang S., and Pedersen N.C. Identification of a novel enteric Helicobacter species in a kitten with severe diarrhea. J. Clin. Microbiol. 36 (1998) 908-912
31. Fox J.G. The non-H. pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50 (2002) 273-283
32. Fox J.G., Blanco M., Murphy J.C., Taylor N.S., Lee A., Kabok Z., and Pappo J. Local and systemic immune responses in murine Helicobacter felis active chronic gastritis. Infect. Immun. 61 (1993) 2309-2315
33. Fox J.G., Correa P., Taylor N.S., Lee A., Otto G., Murphy J.C., and Rose R. Helicobacter mustelae-associated gastritis in ferrets. An animal model of Helicobacter pylori gastritis in humans. Gastroenterology 99 (1990) 352-361
34. Fox J.G., Dewhirst F.E., Tully J.G., Paster B.J., Yan L., Taylor N.S., Collins Jr. M.J., Gorelick P.L., and Ward J.M. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J. Clin. Microbiol. 32 (1994) 1238-1245
35. Fox J.G., Handt L., Sheppard B.J., Xu S., Dewhirst F.E., Motzel S., and Klein I. Isolation of Helicobacter cinaedi from the colon, liver, and mesenteric lymph node of a rhesus monkey with chronic colitis and hepatitis. J. Clin. Microbiol. 39 (2001) 1580-1585
36. Fox J.G., Perkins S., Yan L., Shen Z., Attardo L., and Pappo J. Local immune response in Helicobacter pylori-infected cats and identification of H. pylori in saliva, gastric fluid and faeces. Immunology 88 (1996) 400-406
37. Fox J.G., Shen Z., Xu S., Feng Y., Dangler C.A., Dewhirst F.E., Paster B.J., and Cullen J.M. Helicobacter marmotae sp. nov. isolated from livers of woodchucks and intestines of cats. J. Clin. Microbiol. 40 (2002) 2513-2519
38. Fox J.G., Taylor N.S., Howe S., Tidd M., Xu S., Paster B.J., and Dewhirst F.E. Helicobacter anseris sp. nov. and Helicobacter brantae sp. nov., isolated from feces of resident Canada geese in the greater Boston area. Appl. Environ. Microbiol. 72 (2006) 4633-4637
39. Fox J.G., Yan L., Shames B., Campbell J., Murphy J.C., and Li X. Persistent hepatitis and enterocolitis in germfree mice infected with Helicobacter hepaticus. Infect. Immun. 64 (1996) 3673-3681
40. Fox J.G., Yan L.L., Dewhirst F.E., Paster B.J., Shames B., Murphy J.C., Hayward A., Belcher J.C., and Mendes E.N. Helicobacter bilis sp. nov., a novel Helicobacter species isolated from bile, livers, and intestines of aged, inbred mice. J. Clin. Microbiol. 33 (1995) 445-454
41. Franklin C.L., Beckwith C.S., Livingston R.S., Riley L.K., Gibson S.V., Beschwilliford C.L., and Hook R.R. Isolation of a novel helicobacter species, Helicobacter cholecystus sp. nov., from the gallbladders of syrian hamsters with cholangiofibrosis and centrilobular pancreatitis. J. Clin. Microbiol. 34 (1996) 2952-2958
42. Franklin C.L., Gorelick P.L., Riley L.K., Dewhirst F.E., Livingston R.S., Ward J.M., Beckwith C.S., and Fox J.G. Helicobacter typhlonius sp. nov., a novel murine urease-negative Helicobacter species. J. Clin. Microbiol. 39 (2001) 3920-3926
43. Franklin C.L., Riley L.K., Livingston R.S., Beckwith C.S., Beschwilliford C.L., and Hook R.R. Enterohepatic lesions in scid mice infected with Helicobacter bilis. Lab. Anim. Sci. 48 (1998) 334-339
44. Fujimura S., Kawamura T., Kato S., Tateno H., and Watanabe A. Detection of Helicobacter pylori in cow's milk. Lett. Appl. Microbiol. 35 (2002) 504-507
45. Gewirtz A.T., Yu Y., Krishna U.S., Israel D.A., Lyons S.L., and Peek Jr. R.M. Helicobacter pylori flagellin evades toll-like receptor 5-mediated innate immunity. J. Infect. Dis. 189 (2004) 1914-1920
46. Gibson L.A. Gastric ulceration in pigs. Vet. Rec. 106 (1980) 109-110
47. Gibson W.W. Ulceration of the abomasum associated with calf scour and diet texture. Vet. Rec. 83 (1968) 472-473
48. Grasso G.M., Ripabelli G., Sammarco M.L., Ruberto A., and Iannitto G. Prevalence of Helicobacter-like organisms in porcine gastric mucosa-a study of swine slaughtered in Italy. Comp. Immunol. Microbiol. Infect. Dis. 19 (1996) 213-217
49. Gueneau P., Fuenmayor J., Aristimuno O.C., Cedeno S., Baez E., Reyes N., Michelangeli F., and Dominguez-Bello M.G. Are goats naturally resistant to gastric Helicobacter infection?. Vet. Microbiol. 84 (2002) 115-121
50. Hamir A.N., Stasko J., and Rupprecht C.E. Observation of Helicobacter-like organisms in gastric mucosa of grey foxes (Urocyon cinereoargenteus) and bobcats (Lynx rufus). Can. J. Vet. Res. 68 (2004) 154-156
51. Happonen I., Saari S., Castren L., Tyni O., Hanninen M.L., and Westermarck E. Occurrence and topographical mapping of gastric Helicobacter-like organisms and their association with histological changes in apparently healthy dogs and cats. Zentralblatt Fur Veterinarmedizin Reihe A 43 (1996) 305-315
52. Harper C.G., Feng Y., Xu S., Taylor N.S., Kinsel M., Dewhirst F.E., Paster B.J., Greenwell M., Levine G., Rogers A., and Fox J.G. Helicobacter cetorum sp. nov., a urease-positive Helicobacter species isolated from dolphins and whales. J. Clin. Microbiol. 40 (2002) 4536-4543
53. Harper C.M., Xu S., Feng Y., Dunn J.L., Taylor N.S., Dewhirst F.E., and Fox J.G. Identification of novel Helicobacter spp. from a beluga whale. Appl. Environ. Microbiol. 68 (2002) 2040-2043
54. Hellmig S., Fischbach W., Goebeler-Kolve M.E., Folsch U.R., Hampe J., and Schreiber S. A functional promotor polymorphism of TNF-alpha is associated with primary gastric B-cell lymphoma. Am. J. Gastroenterol. 100 (2005) 2644-2649
55. Hepburn, R., 2004. Investigation into the presence of Helicobacter in the equine stomach by urease testing and polymerase chain reaction and further investigation into the application of the 13C-urea blood test to the horse. Masters Thesis. Virginia Polytechnic Institute and State University, Leesburg.
56. Hill J.E., Khanolkar S.S., and Stadtlander C. Gastric ulcer associated with a Helicobacter-like organism in a cougar (Felis concolor). Vet. Pathol. 34 (1997) 50-51
57. Hue S., Ahern P., Buonocore S., Kullberg M.C., Cua D.J., McKenzie B.S., Powrie F., and Maloy K.J. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203 (2006) 2473-2483
58. Ishihara S., Rumi M.A., Kadowaki Y., Ortega-Cava C.F., Yuki T., Yoshino N., Miyaoka Y., Kazumori H., Ishimura N., Amano Y., and Kinoshita Y. Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J. Immunol. 173 (2004) 1406-1416
59. Jakob W., Stolte M., Valentin A., and Schroder H.D. Demonstration of Helicobacter pylori-like organisms in the gastric mucosa of captive exotic carnivores. J. Comp. Pathol. 116 (1997) 21-33
60. Jalava K., On S.L.W., Harrington C.S., Andersen L.P., Hanninen M.L., and Vandamme P. A cultured strain of "Helicobacter heilmannii," a human gastric pathogen, identified as H. bizzozeronii: evidence for zoonotic potential of Helicobacter. Emerg. Infect. Dis. 7 (2001) 1036-1038
61. Jalava K., On S.L.W., Vandamme P.A.R., Happonen I., Sukura A., and Hanninen M.L. Isolation and identification of Helicobacter spp., from canine and feline gastric mucosa. Appl. Environ. Microbiol. 64 (1998) 3998-4006
62. Kamradt A.E., Greiner M., Ghiara P., and Kaufmann S.H.E. Helicobacter pylori infection in wild-type and cytokine-deficient C57BL/6 and BALB/c mouse mutants. Microbes Infect. 2 (2000) 593-597
63. Kawahara T., Teshima S., Oka A., Sugiyama T., Kishi K., and Rokutan K. Type I Helicobacter pylori lipopolysaccharide stimulates toll-like receptor 4 and activates mitogen oxidase 1 in gastric pit cells. Infect. Immun. 69 (2001) 4382-4389
64. Kinsel M.J., Briggs M.B., Venzke K., Forge O., and Murnane R.D. Gastric spiral bacteria and intramuscular sarcocysts in African lions from Namibia. J. Wildl. Dis. 34 (1998) 317-324
65. Kinsel M.J., Kovarik P., and Murnane R.D. Gastric spiral bacteria in small felids. J. Zoo Wildl. Med. 29 (1998) 214-220
66. Kirkbride C.A., Gates C.E., and Collins J.E. Abortion in sheep caused by a nonclassified, anaerobic, flagellated bacterium. Am. J. Vet. Res. 47 (1986) 259-262
67. Kirkbride C.A., Gates C.E., Collins J.E., and Ritchie A.E. Ovine abortion associated with an anaerobic bacterium. J. Am. Vet. Med. Assoc. 186 (1985) 789-791
68. Krakowka S., and Ellis J. Reproduction of severe gastroesophageal ulcers (GEU) in gnotobiotic swine infected with porcine Helicobacter pylori-like bacteria. Vet. Pathol. 43 (2006) 956-962
69. Kuhn R., Lohler J., Rennick D., Rajewsky K., and Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75 (1993) 263-274
70. Kullberg M.C., Jankovic D., Feng C.G., Hue S., Gorelick P.L., McKenzie B.S., Cua D.J., Powrie F., Cheever A.W., Maloy K.J., and Sher A. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203 (2006) 2485-2494
71. Kullberg M.C., Rothfuchs A.G., Jankovic D., Caspar P., Wynn T.A., Gorelick P.L., Cheever A.W., and Sher A. Helicobacter hepaticus-induced colitis in interleukin-10-deficient mice: cytokine requirements for the induction and maintenance of intestinal inflammation. Infect. Immun. 69 (2001) 4232-4241
72. Kullberg M.C., Ward J.M., Gorelick P.L., Caspar P., Hieny S., Cheever A., Jankovic D., and Sher A. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun. 66 (1998) 5157-5166
73. Lavelle J.P., Landas S., Mitros F.A., and Conklin J.L. Acute gastritis associated with spiral organisms from cats. Dig. Dis. Sci. 39 (1994) 744-750
74. Lee A., Fox J.G., Otto G., and Murphy J. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology 99 (1990) 1315-1323
75. Lee A., Hazell S.L., O'Rourke J., and Kouprach S. Isolation of a spiral-shaped bacterium from the cat stomach. Infect. Immun. 56 (1988) 2843-2850
76. Lee A., Krakowka S., Fox J.G., Otto G., Eaton K.A., and Murphy J.C. Role of Helicobacter felis in chronic canine gastritis. Vet. Pathol. 29 (1992) 487-494
77. Lee S.K., Stack A., Katzowitsch E., Aizawa S.I., Suerbaum S., and Josenhans C. Helicobacter pylori flagellins have very low intrinsic activity to stimulate human gastric epithelial cells via TLR5. Microbes Infect. 5 (2003) 1345-1356
78. Leemann C., Gambillara E., Prod'hom G., Jaton K., Panizzon R., Bille J., Francioli P., Greub G., Laffitte E., and Tarr P.E. First case of bacteremia and multifocal cellulitis due to Helicobacter canis in an immunocompetent patient. J. Clin. Microbiol. 44 (2006) 4598-4600
79. Li X.T., Fox J.G., Whary M.T., Yan L.L., Shames B., and Zhao Z.B. SCID/NCr mice naturally infected with Helicobacter hepaticus develop progressive hepatitis, proliferative typhlitis, and colitis. Infect. Immun. 66 (1998) 5477-5484
80. Mackie J.T., and O'Rourke J.L. Gastritis associated with Helicobacter-like organisms in baboons. Vet. Pathol. 40 (2003) 563-566
81. Maloy K.J., Salaun L., Cahill R., Dougan G., Saunders N.J., and Powrie F. CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197 (2003) 111-119
82. Mandell L., Moran A.P., Cocchiarella A., Houghton J., Taylor N., Fox J.G., Wang T.C., and Kurt-Jones E.A. Intact gram-negative Helicobacter pylori, Helicobacter felis, and Helicobacter hepaticus bacteria activate innate immunity via toll-like receptor 2 but not toll-like receptor 4. Infect. Immun. 72 (2004) 6446-6454
83. Marshall B.J. Unidentified curved bacillus on gastric epithelium in active chronic gastritis. Lancet 1 (1983) 1273-1275
84. Matsumoto Y., Blanchard T.G., Drakes M.L., Basu M., Redline R.W., Levine A.D., and Czinn S.J. Eradication of Helicobacter pylori and resolution of gastritis in the gastric mucosa of IL-10-deficient mice. Helicobacter 10 (2005) 407-415
85. Maurer K.J., Ihrig M.M., Rogers A.B., Ng V., Bouchard G., Leonard M.R., Carey M.C., and Fox J.G. Identification of cholelithogenic enterohepatic helicobacter species and their role in murine cholesterol gallstone formation. Gastroenterology 128 (2005) 1023-1033
86. McGuckin M.A., Every A.L., Skene C.D., Linden S.K., Chionh Y.T., Swierczak A., McAuley J., Harbour S., Kaparakis M., Ferrero R., and Sutton P. Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis. Gastroenterology 133 (2007) 1210-1218
87. Meining A., Kroher G., and Stolte M. Animal reservoirs in the transmission of Helicobacter heilmannii-results of a questionnaire-based study. Scand. J. Gastroenterol. 33 (1998) 795-798
88. Mendes E.N., Queiroz D.M., Rocha G.A., Nogueira A.M., Carvalho A.C., Lage A.P., and Barbosa A.J. Histopathological study of porcine gastric mucosa with and without a spiral bacterium ("Gastrospirillum suis"). J. Med. Microbiol. 35 (1991) 345-348
89. Mohammadi M., Czinn S., Redline R., and Nedrud J. Helicobacter-specific cell-mediated immune responses display a predominant Th1 phenotype and promote a delayed-type hypersensitivity response in the stomachs of mice. J. Immunol. 156 (1996) 4729-4738
90. Mohammadi M., Redline R., Nedrud J., and Czinn S. Role of the host in pathogenesis of Helicobacter-associated gastritis-H. felis infection of inbred and congenic mouse strains. Infect. Immun. 64 (1996) 238-245
91. Morgner A., Lehn N., Andersen L.P., Thiede C., Bennedsen M., Trebesius K., Neubauer B., Neubauer A., Stolte M., and Bayerdorffer E. Helicobacter heilmannii-associated primary gastric low-grade MALT lymphoma: complete remission after curing the infection. Gastroenterology 118 (2000) 821-828
92. Moyaert H., Decostere A., Vandamme P., Debruyne L., Mast J., Baele M., Ceelen L., Ducatelle R., and Haesebrouck F. Helicobacter equorum sp. nov., a urease-negative Helicobacter species isolated from horse faeces. Int. J. Syst. Evol. Microbiol. 57 (2007) 213-218
93. Moyaert H., Haesebrouck F., Baele M., Picavet T., Ducatelle R., Chiers K., Ceelen L., and Decostere A. Prevalence of Helicobacter equorum in faecal samples from horses and humans. Vet. Microbiol. 121 (2007) 378-383
94. Nambiar P.R., Kirchain S., and Fox J.G. Gastritis-associated adenocarcinoma and intestinal metaplasia in a Syrian hamster naturally infected with Helicobacter species. Vet. Pathol. 42 (2005) 386-390
95. Neiger R., and Simpson K.W. Helicobacter infection in dogs and cats: facts and fiction. J. Vet. Int. Med. 14 (2000) 125-133
96. Neubauer C., and Hess M. Tissue tropism of Helicobacter pullorum in specific pathogen-free chickens determined by culture and nucleic acid detection. Avian Dis. 50 (2006) 620-623
97. Nilsson H.O., Ouis I.S., Stenram U., Ljungh A., Moran A.P., Wadstrom T., and Al-Soud W.A. High prevalence of Helicobacter species detected in laboratory mouse strains by multiplex PCR-denaturing gradient gel electrophoresis and pyrosequencing. J. Clin. Microbiol. 42 (2004) 3781-3788
98. Norris C.R., Marks S.L., Eaton K.A., Torabian S.Z., Munn R.J., and Solnick J.V. Healthy cats are commonly colonized with "Helicobacter heilmannii" that is associated with minimal gastritis. J. Clin. Microbiol. 37 (1999) 189-194
99. On S.L.W. Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: current status, future prospects and immediate concerns. J. Appl. Microbiol. 90 (2001) 1S-15S
100. O'Rourke J.L., Dixon M.F., Jack A., Enno A., and Lee A. Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of 'Helicobacter heilmannii' infection. J. Pathol. 203 (2004) 896-903
101. O'Rourke J.L., Solnick J.V., Neilan B.A., Seidel K., Hayter R., Hansen L.M., and Lee A. Description of 'Candidatus Helicobacter heilmannii' based on DNA sequence analysis of 16S rRNA and urease genes. Int. J. Syst. Evol. Microbiol. 54 (2004) 2203-2211
102. Park J.H., Lee B.J., and Lee Y.S. Association of tightly spiralled bacterial infection and gastritis in pigs. J. Vet. Med. Sci. 62 (2000) 725-729
103. Powrie F., Leach M.W., Mauze S., Caddle L.B., and Coffman R.L. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C.B-17 scid mice. Int. Immunol. 5 (1993) 1461-1471
104. Rad R., Brenner L., Krug A., Voland P., Mages J., Lang R., Schwendy S., Reindl W., Dossumbekova A., Ballhorn W., Wagner H., Schmid R.M., Bauer S., and Prinz C. Toll-like receptor-dependent activation of antigen-presenting cells affects adaptive immunity to Helicobacter pylori. Gastroenterology 133 (2007) 150-163
105. Rossi G., Fortuna D., Pancotto L., Renzoni G., Taccini E., Ghiara P., Rappuoli R., and Del Giudice G. Immunohistochemical study of lymphocyte populations infiltrating the gastric mucosa of beagle dogs experimentally infected with Helicobacter pylori. Infect. Immun. 68 (2000) 4769-4772
106. Roth K.A., Kapadia S.B., Martin S.M., and Lorenz R.G. Cellular immune responses are essential for the development of Helicobacter felis-associated gastric pathology. J. Immunol. 163 (1999) 1490-1497
107. Sadlack B., Merz H., Schorle H., Schimpl A., Feller A.C., and Horak I. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell 75 (1993) 253-261
108. Sakagami T., Dixon M., O'Rourke J., Howlett R., Alderuccio F., Vella J., Shimoyama T., and Lee A. Atrophic gastric changes in both Helicobacter felis and Helicobacter pylori infected mice are host dependent and separate from antral gastritis. Gut 39 (1996) 639-648
109. Sakagami T., Vella J., Dixon M.F., O'Rourke J., Radcliff F., Sutton P., Shimoyama T., Beagley K., and Lee A. The endotoxin of Helicobacter pylori is a modulator of host-dependent gastritis. Infect. Immun. 65 (1997) 3310-3316
110. Schauer D.B., Ghori N., and Falkow S. Isolation and characterisation of "Flexispira rappini" from laboratory mice. J. Clin. Microbiol. 31 (1993) 2709-2714
111. Schroder H.D., Ludwig C., Jakob W., Reischl U., Stolte M., and Lehn N. Chronic gastritis in tigers associated with Helicobacter acinonyx. J. Comp. Pathol. 119 (1998) 67-73
112. Sellon R.K., Tonkonogy S., Schultz M., Dieleman L.A., Grenther W., Balish E., Rennick D.M., and Sartor R.B. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66 (1998) 5224-5231
113. Shen Z., Fox J.G., Dewhirst F.E., Paster B.J., Foltz C.J., Yan L., Shames B., and Perry L. Helicobacter rodentium sp. nov., a urease-negative helicobacter species isolated from laboratory mice. Int. J. Syst. Bacteriol. 47 (1997) 627-634
114. Shomer N.H., Dangler C.A., Marini R.P., and Fox J.G. Helicobacter bilis Helicobacter rodentium co-infection associated with diarrhea in a colony of scid mice. Lab. Anim. Sci. 48 (1998) 455-459
115. Shomer N.H., Dangler C.A., Schrenzel M.D., and Fox J.G. Helicobacter bilis-induced inflammatory bowel disease in SCID mice with defined flora. Infect. Immun. 65 (1997) 4858-4864
116. Simmons J.H., Riley L.K., Besch-Williford C.L., and Franklin C.L. Helicobacter mesocricetorum sp. nov., a novel helicobacter isolated from the feces of Syrian hamsters. J. Clin. Microbiol. 38 (2000) 1811-1817
117. Simpson K.W., Strauss-Ayali D., Scanziani E., Straubinger R.K., McDonough P.L., Straubinger A.F., Chang Y.F., Domeneghini C., Arebi N., and Calam J. Helicobacter felis infection is associated with lymphoid follicular hyperplasia and mild gastritis but normal gastric secretory function in cats. Infect. Immun. 68 (2000) 779-790
118. Simpson K.W., Strauss-Ayali D., Straubinger R.K., Scanziani E., McDonough P.L., Straubinger A.F., Chang Y.F., Esteves M.I., Fox J.G., Domeneghini C., Arebi N., and Calam O. Helicobacter pylori infection in the cat: evaluation of gastric colonization, inflammation and function. Helicobacter 6 (2001) 1-14
119. Smith Jr. M.F., Mitchell A., Li G., Ding S., Fitzmaurice A.M., Ryan K., Crowe S., and Goldberg J.B. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J. Biol. Chem. 278 (2003) 32552-32560
120. Smythies L.E., Waites K.B., Lindsey J.R., Harris P.R., Ghiara P., and Smith P.D. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-γ, gene-deficient mice. J. Immunol. 165 (2000) 1022-1029
121. Stanley J., Linton D., Burnens A.P., Dewhirst F.E., On S.L.W., Porter A., Owen R.J., and Costas M. Helicobacter pullorum sp. nov.-genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology (UK) 140 (1994) 3441-3449
122. Stanley J., Linton D., Burnens A.P., Dewhirst F.E., Owen R.J., Porter A., On S.L.W., and Costas M. Helicobacter canis sp. nov., a new species from dogs-an integrated study of phenotype and genotype. J. Gen. Microbiol. 139 (1993) 2495-2504
123. Strauss-Ayali D., Scanziani E., Deng D., and Simpson K.W. Helicobacter spp. infection in cats: evaluation of the humoral immune response and prevalence of gastric Helicobacter spp. Vet. Microbiol. 79 (2001) 253-265
124. Sutton P., Kolesnikow T., Danon S., Wilson J., and Lee A. Dominant nonresponsiveness to Helicobacter pylori infection is associated with production of interleukin 10 but not gamma interferon. Infect. Immun. 68 (2000) 4802-4804
125. Sutton P., Wilson J., Genta R., Torrey D., Savinainen A., Pappo J., and Lee A. A genetic basis for atrophy: dominant non-responsiveness and helicobacter induced gastritis in F-1 hybrid mice. Gut 45 (1999) 335-340
126. Taylor N.S., Xu S., Nambiar P., Dewhirst F.E., and Fox J.G. Enterohepatic helicobacter species are prevalent in mice from commercial and academic institutions in Asia, Europe, and North America. J. Clin. Microbiol. 45 (2007) 2166-2172
127. Thomson M.A., Storey P., Greer R., and Cleghorn G.J. Canine-human transmission of Gastrospirillum hominis. Lancet 343 (1994) 1605-1607
128. Turutoglu H., and Mudul S. Investigation of Helicobacter pylori in raw sheep milk samples. J. Vet. Med. B Infect. Dis. Vet. Public Health 49 (2002) 308-309
129. Van den Bulck K., Decostere A., Baele M., Driessen A., Debongnie J.C., Burette A., Stolte M., Ducatelle R., and Haesebrouck F. Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats. J. Clin. Microbiol. 43 (2005) 2256-2260
130. Van den Bulck K., Decostere A., Baele M., Vandamme P., Mast J., Ducatelle R., and Haesebrouck F. Helicobacter cynogastricus sp. nov., isolated from the canine gastric mucosa. Int. J. Syst. Evol. Microbiol. 56 (2006) 1559-1564
131. Vinall L.E., King M., Novelli M., Green C.A., Daniels G., Hilkens J., Sarner M., and Swallow D.M. Altered expression and allelic association of the hypervariable membrane mucin MUC1 in Helicobacter pylori gastritis. Gastroenterology 123 (2002) 41-49
132. Waldenstrom J., On S.L., Ottvall R., Hasselquist D., Harrington C.S., and Olsen B. Avian reservoirs and zoonotic potential of the emerging human pathogen Helicobacter canadensis. Appl. Environ. Microbiol. 69 (2003) 7523-7526
133. Ward J.M., Anver M.R., Haines D.C., and Benveniste R.E. Chronic active hepatitis in mice caused by Helicobacter hepaticus. Am. J. Pathol. 145 (1994) 959-968
134. Ward J.M., Fox J.G., Anver M.R., Haines D.C., George C.V., Collins M.J., Gorelick P.L., Nagashima K., Gonda M.A., Gilden R.V., Tully J.G., Russell R.J., Benveniste R.E., Paster B.J., Dewhirst F.E., Donovan J.C., Anderson L.M., and Rice J.M. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J. Natl Cancer Inst. 86 (1994) 1222-1227
135. Warren J.R. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1 (1983) 1273
136. Weber A.F., Hasa O., and Sautter J.H. Some observations concerning the presence of spirilla in the fundic glands of dogs and cats. Am. J. Vet. Res. 19 (1958) 677-680
137. Weber A.F., and Schmittdiel E.F. Electron microscopic and bacteriologic studies of spirilla isolated from the fundic stomachs of cats and dogs. Am. J. Vet. Res. 23 (1962) 422-427
138. Whary M.T., Morgan T.J., Dangler C.A., Gaudes K.J., Taylor N.S., and Fox J.G. Chronic active hepatitis induced by Helicobacter hepaticus in the A/JCr mouse is associated with a Th1 cell-mediated immune response. Infect. Immun. 66 (1998) 3142-3148