Effects of Helicobacter infection on research: The case for eradication of Helicobacter from rodent research

Comparative Medicine

Volumn 59, Issue 1, 2009, Pages 10-17

  Chichlowski, Maciej ^a   Hale, Laura P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TRANSMISSION; BREAST CANCER; COLITIS; COLON TUMOR; EXPERIMENTAL MOUSE; GASTRITIS; HELICOBACTER INFECTION; HEPATITIS; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; INFECTION PREVENTION; LABORATORY INFECTION; LIVER CELL CARCINOMA; MEDICAL RESEARCH; MOUSE; NONHUMAN; ORGANISM COLONY; RELIABILITY; REVIEW;

ANIMAL HUSBANDRY; ANIMALS; ANIMALS, LABORATORY; ANTI-BACTERIAL AGENTS; CRICETINAE; DISEASE MODELS, ANIMAL; HELICOBACTER; HELICOBACTER INFECTIONS; HUMANS; MASS SCREENING; MICE; MURINAE; RATS; REPRODUCIBILITY OF RESULTS; RODENT DISEASES; RODENTIA;

EID: 63449117417     PISSN: 15320820     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (125)

1. Abad A. 2008. New drugs in the treatment of gastric tumors. Clir Transl Oncol 10:256-261.
2. Baele M, Decostere A, Vandamme P, Ceelen L, Hellemans A Mast J, Chiers K, Ducatelle R, Haesebrouck F. 2008. Isolation anc characterization of Helicobacter suis sp. nov. from pig stomachs. In J Syst Evol Microbiol 58:1350-1358.
3. Beckwith CS, Franklin CL, Hook RR Jr, Besch-Williford CL, Riley LK. 1997. Fecal pcr assay for diagnosis of Helicobacter infection ir laboratory rodents. J Clin Microbiol 35:1620-1623.
4. Bohr UR, Selgrad M, Ochmann C, Backert S, Konig W, Fenske A Wex T, Malfertheiner P. 2006. Prevalence and spread of enterohe patic Helicobacter species in mice reared in a specific-pathogen-free animal facility. J Clin Microbiol 44:738-742.
5. Bridgeford EC, Marini RP, Feng Y, Parry NM, Rickman B, Fox JG 2008. Gastric Helicobacter species as a cause of feline gastric lymphoma: a viable hypothesis. Vet Immunol Immunopathol 123:106-113
6. Burich A, Hershberg R, Waggie K, Zeng W, Brabb T, Westrich G Viney JL, Maggio-Price L. 2001. Helicobacter-induced inflammatory bowel disease in IL10- and T cell-deficient mice. Am J Physio Gastrointest Liver Physiol 281:G764-G778.
7. Burks AW, Laubach S, Jones SM. 2008. Oral tolerance, food allerg) and immunotherapy: implications for future treatment. J Allerg' Clin Immunol 121:1344-1350.
8. Campli CD, Gasbarrini A, Nucera E, Franceschi F, Ojetti V, Tore ES, Schiavino D, Pola P, Patriarca G, Gasbarrini G. 1998. Beneficia effects of Helicobacter pylori eradication on idiopathic chronic urticaria. Dig Dis Sci 43:1226-1229.
9. Chichlowski M, Sharp JM, Vanderford DA, Myles MH, Hale LP 2008. Helicobacter typhlonius and H. Rodentium differentially affec the severity of colon inflammation and inflammation-associated neoplasia in ILO-deficient mice. Comp Med 58:534-541.
10. Compton SR, Ball-Goodrich LJ, Zeiss CJ, Johnson LK, Johnson EA Macy JD. 2003. Pathogenesis of mouse hepatitis virus infection in gamma interferon-deficient mice is modulated by coinfection with Helicobacter hepaticus. Comp Med 53:197-206.
11. Corrado G, Luzzi I, Lucarelli S, Frediani T, Pacchiarotti C, Cavalier M, Rea P, Cardi E. 1998. Positive association between Helicobacte pylori infection and food allergy in children. Scand J Gastroenterc 33:1135-1139.
12. Correa P, Houghton J. 2007. Carcinogenesis of Helicobacter pylor. Gastroenterology 133:659-672.
13. Didierlaurent A, Ferrero I, Otten LA, Dubois B, Reinhardt M, Carlsen H, Blomhoff R, Akira S, Kraehenbuhl J-P, Sirard J-C. 2004. Flagellin promotes myeloid differentiation factor 88-dependent development of Th2-type response. J Immunol 172:6922-6930.
14. Balish E, Doetschman T. 2002. Elimination of colon cancer in germ-free transforming growth factor βi-deficient mice. Cancer Res 62:6362-6366.
15. + regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2 -deficient mice. Am J Pathol 162:691-702.
16. + regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res 63:6042-6050.
17. Farinha P, Gascoyne RD. 2005. Helicobacter pylori and MALT lymphoma. Gastroenterology 128:1579-1605.
18. Feng S, Ku K, Hodzic E, Lorenzana E, Freet K, Barthold SW. 2005. Differential detection of five mouse-infecting Helicobacter species by multiplex PCR. Clin Diagn Lab Immunol 12:531-536.
19. Figura N, Perrone A, Gennari C, Orlandini G, Bianciardi L, Giannace R, Vaira D, Vagliasinti M, Rottoli P. 1999. Food allergy and Helicobacter pylori infection. Ital J Gastroenterol Hepatol 31:186-191.
20. Foltz CJ, Fox JG, Cahill R, Murphy JC, Yan L, Shames B, Schauer DB. 1998. Spontaneous inflammatory bowel disease in multiple mutant mouse lines: association with colonization by Helicobacter hepaticus. Helicobacter 3:69-78.
21. Foltz CJ, Fox JG, Yan L, Shames B. 1995. Evaluation of antibiotic therapies for eradication of Helicobacter hepaticus. Antimicrob Agents Chemother 39:1292-1294.
22. Foltz CJ, Fox JG, Yan L, Shames B. 1996. Evaluation of various oral antimicrobial formulations for eradication of Helicobacter hepaticus. Lab Anim Sci 46:193-197.
23. Fox JG, Blanco M, Murphy JC, Taylor NS, Lee A, Kabok Z, Pappo J. 1993. Local and systemic immune responses in murine Helicobacter felis active chronic gastritis. Infect Immun 61:2309-2315.
24. Fox JG, Dewhirst FE, Shen Z, Feng Y, Taylor NS, Paster BJ, Ericson RL, Lau CN, Correa P, Araya JC, Roa I. 1998. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114:755-763.
25. Fox JG, Dewhirst FE, Eraser GJ, Paster BJ, Shames B, Murphy JC. 1994. Intracellular Campylobacter-like organism from ferrets and hamsters with proliferative bowel disease is a Desulfovibrio sp. J Clin Microbiol 32:1229-1237.
26. Fox JG, Dewhirst FE, Tully JG, Paster BJ, Yan L, Taylor NS, Collins MJ Jr, Gorelick PL, Ward JM. 1994. Helicobacter hepaticus sp. nov., a microaerophic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol 32:1238-1245.
27. Fox JG, Drolet R, Higgins R, Messier S, Yan L, Coleman BE, Paster BJ, Dewhirst FE. 1996. Helicobacter canis isolated from a dog liver with multifocal necrotizing hepatitis. J Clin Microbiol 34:2479-2482.
28. Fox JG, Gorelick PL, Kullberg MC, Ge Z, Dewhirst FE, Ward JM. 1999. A novel urease-negative Helicobacter species associated with colitis and typhlitis in IL10-deficient mice. Infect Immun 67:1757- 1762.
29. Fox JG, Handt L, Sheppard BJ, Xu S, Dewhirst FE, Motzel S, Klein H. 2001. Isolation of Helicobacter cinaedi from the colon, liver, and mesenteric lymph node of a rhesus monkey with chronic colitis and hepatitis. J Clin Microbiol 39:1580-1585.
30. Fox JG, Li X, Yan L, Cahill RJ, Hurley R, Lewis R, Murphy JC. 1996. Chronic proliferative hepatitis in A/JCr mice associated with persistent Helicobacter hepaticus infection: a model of Helicobacter- induced carcinogenesis. Infect Immun 64:1548-1558.
31. Fox JG, MacGregor J A, Shen Z, Li X, Lewis R, Dangler CA. 1998. Comparison of methods of identifying Helicobacter hepaticus in B6C3F1 mice used in a carcinogenesis bioassay. J Clin Microbiol 36:1382-1387.
32. Fox JG, Rogers AB, Whary MT, Taylor NS, Xu S, Feng Y, Keys S. 2004. Helicobacter bilis -associated hepatitis in outbred mice. Comp Med 54:571-577.
33. Fox JG, Shen Z, Xu S, Feng Y, Dangler CA, Dewhirst FE, Paster BJ, Cullen JM. 2002. Helicobacter marmotae sp. nov. isolated from livers of woodchucks and intestines of cats. J Clin Microbiol 40:2513-2519.
34. Fox JG, Yan L, Shames B, Campbell J, Murphy JC, Li X. 1996. Persistent hepatitis and enterocolitis in germf ree mice infected with Helicobacter hepaticus. Infect Immun 64:3673-3681.
35. Fox JG, Yan LL, Dewhirst FE, Paster BJ, Shames B, Murphy JC, Hayward A, Belcher JC, Mendes EN. 1995. Helicobacter bilis sp. nov., a novel Helicobacter species isolated from bile, livers, and intestines of aged, inbred mice. J Clin Microbiol 33:445-454.
36. Franklin CL, Beckwith CS, Livingston RS, Riley LK, Gibson SV, Besch-Williford CL, Hook RR Jr. 1996. Isolation of a novel Helicobacter species, Helicobacter cholecystus sp. nov., from the gallbladders of Syrian hamsters with cholangiofibrosis and centrilobular pancreatitis. J Clin Microbiol 34:2952-2958.
37. Franklin CL, Gorelick PL, Riley LK, Dewhirst FE, Livingston RS, Ward JM, Beckwith CS, Fox JG. 2001. Helicobacter typhlonius sp. nov., a novel murine urease-negative Helicobacter species. J Clin Microbiol 39:3920-3926.
38. Franklin CL, Riley LK, Livingston RS, Beckwith CS, Besch- Williford CL, Hook RRJ. 1998. Enterohepatic lesions in SCID mice infected with Helicobacter bilis. Lab Anim Sci 48:334-339.
39. Franklin CL, Riley LK, Livingston RS, Beckwith CS, Hook RR Jr, Besch-Williford CL, Hunziker R, Gorelick PL. 1999. Enteric lesions in SCID mice infected with 'Helicobacter typhlonicus,' a novel ureasenegative Helicobacter species. Lab Anim Sci 49:496-505.
40. Gaboriau-Routhiau V, Moreau MC. 1996. Gut flora allows recovery of oral tolerance to ovalbumin in mice after transient breakdown mediated by cholera toxin or Escherichia coli heat-labile enterotoxin. Pediatr Res 39:625-629.
41. Garcia A, Ihrig MM, Fry RC, Feng Y, Xu S, Boutin SR, Rogers AB, Muthupalani S, Samson LD, Fox JG. 2008. Genetic susceptibility to chronic hepatitis is inherited codominantly in Helicobacter hepaticus-infected AB6F1 and B6AF1 hybrid male mice, and progression to hepatocellular carcinoma is linked to hepatic expression of lipogenic genes and immune function-associated networks. Infect Immun 76:1866-1876.
42. Ge Z, Lee A, Whary MT, Rogers AB, Maurer KJ, Taylor NS, Schauer DB, Fox JG. 2008. Helicobacter hepaticus urease is not required for intestinal colonization but promotes hepatic inflammation in male A/JCr mice. Microb Pathog 45:18-24.
43. Ge Z, White DA, Whary MT, Fox JG. 2001. Fluorogenic PCR-based quantitative detection of a murine pathogen, Helicobacter hepaticus. J Clin Microbiol 39:2598-2602.
44. Goto K, Jiang W, Zheng Q, Oku Y, Kamiya H, Itoh T, Ito M. 2004. Epidemiology of Helicobacter infection in wild rodents in the Xinjiang-Uygur autonomous region of China. Curr Microbiol 49:221-223.
45. Hailey JR, Haseman JK, Bucher JR, Radovsky AE, Malarkey DE, Miller RT, Nyska A, Maronpot RR. 1998. Impact of Helicobacter hepaticus infection in B6C3F1 mice from 12 national toxicology program 2-year carcinogenesis studies. Toxicol Pathol 26:602-611.
46. -/- mice. Helicobacter 12:598-604.
47. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Vi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103.
48. Jiang H-Q, Kushnir N, Christine Thurnheer M, Bos NA, Cebra JJ. 2002. Monoassociation of SCID mice with Helicobacter muridarum, but not 4 other enterics, provokes IBD upon receipt of T cells. Gastroenterology 122:1346-1354.
49. Johansson SK, Feinstein RE, Johansson KE, Lindberg AV. 2006. Occurrence of Helicobacter species other than H. hepaticus in laboratory mice and rats in Sweden. Comp Med 56:110-113.
50. Kobayashi M, Lee H, Schaffer L, Gilmartin TJ, Head SR, Takaishi S, Wang TC, Nakayama J, Fukuda M. 2007. A distinctive set of genes is upregulated during the inflammation-carcinoma sequence in mouse stomach infected by Helicobacter felis. J Histochem Cytochem 55:263-274.
51. Kostomitsopoulos N, Donnelly H, Kostavasili I, Paronis E, Alexa- kos P, Karayannacos P. 2007. Eradication of Helicobacter bills and H. hepaticus from infected mice by using a medicated diet. Lab Anim (NY) 36:37-40.
52. Kuehl CJ, Wood HD, Marsh TL, Schmidt TM, Young VB. 2005. Colonization of the cecal mucosa by Helicobacter hepaticus impacts the diversity of the indigenous microbiota. Infect Immun 73:6952- 6961.
53. Laharie D, Ménard S, Asencio C, Vidal-Martinez T, Rullier A, Zerbib F, Candalh C, Megraud F, Heyman M, Matysiak-Budnik T. 2007. Effect of rebamipide on the colonic barrier in ILlO-deficient mice. Dig Dis Sci 52:84-92.
54. Lee A, Phillips MW, O'Rourke JL, Paster BJ, Dewhirst FE, Fraser GJ, Fox JG, Sly LI, Romaniuk PJ, Trust TJ. 1992. Helicobacter muridarum sp. nov., a microaerophilic helical bacterium with a novel ultrastructure isolated from the intestinal mucosa of rodents. Int ] Syst Bacterid 42:27-36.
55. Lee CW, Rickman B, Rogers AB, Ge Z, Wang TC, Fox JG. 2008. Helicobacter pylori eradication prevents progression of gastric cancer in hypergastrinemic INS-GAS mice. Cancer Res 68:3540-3548.
56. Li X, Fox JG, Whary MT, Yan L, Shames B, Zhao Z. 1998. SCID/ NCR mice naturally infected with Helicobacter hepaticus develop progressive hepatitis, proliferative typhlitis, and colitis. Infect Immun 66:5477-5484.
57. Livingston RS, Riley LK. 2003. Diagnostic testing of mouse and rat colonies for infectious agents. Lab Anim 32:44-51.
58. Livingston RS, Riley LK, Besch-Williford CL, Hook RR, Franklin CL. 1998. Transmission of Helicobacter hepaticus infection to sentinel mice by contaminated bedding. Lab Anim Sci 48:291-293.
59. Lodes MJ, Cong Y, Elson CO, Mohamath R, Landers CJ, Targan SR, Fort M, Hershberg RM. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 113:1296-1306.
60. Maggio-Price L, Bielefeldt-Ohmann H, Treuting P, Iritani BM, Zeng W, Nicks A, Tsang M, Shows D, Morrissey P, Viney JL. 2005. Dual infection with Helicobacter bills and Helicobacter hepaticus in pglycoprotein-deficient Mdr1a-/- mice results in colitis that progresses to dysplasia. Am J Pathol 166:1793-1806.
61. Maggio-Price L, Shows D, Waggie K, Burich A, Zeng W, Escobar S, Morrissey P, Viney JL. 2002. Helicobacter bills infection accelerates and H. hepaticus infection delays the development of colitis in multiple drug resistance-deficient (Mdr1a-/-) mice. Am J Pathol 160:739-751.
62. Maggio-Price L, Treuting P, Zeng W, Tsang M, Bielefeldt-Ohmann H, Iritani BM. 2006. Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res 66:828-838.
63. Mahler M, Bedigian HG, Burgett BL, Bates RJ, Hogan ME, Sund- berg JP. 1998. Comparison of 4 diagnostic methods for detection of Helicobacter species in laboratory mice. Lab Anim Sci 48:85-91.
64. + Tr cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 197:111-119.
65. Marshall B, Schoep T. 2007. Helicobacter pylori as a vaccine delivery system. Helicobacter 12 Suppl 2:75-79.
66. Marshall BJ, Warren JR. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 323:1311-1315.
67. Matsukura N, Yokomuro S, Yamada S, Tajiri T, Sundo T, Hadama T, Kamiya S, Naito Z, Fox JG. 2002. Association between Helicobacter bills in bile and biliary tract malignancies: H. bills in bile from Japanese and Thai patients with benign and malignant diseases in the biliary tract. Jpn J Cancer Res 93:842-847.
68. Matysiak-Budnik T, Hashimoto K, Heyman M, de Mascarel A, Desjeux JF, Mégraud F. 1999. Antral gastric permeability to antigens in mice is altered by infection with Helicobacter felis. Eur J Gastroenterol Hepatol 11:1371-1377.
69. Matysiak-Budnik T, Terpend K, Alain S, Sanson le Pors MJ, Desjeux JF, Megraud F, Heyman M. 1998. Helicobacter pylori alters exogenous antigen absorption and processing in a digestive tract epithelial cell line model. Infect Immun 66:5785-5791.
70. Matysiak-Budnik T, van Niel G, Megraud F, Mayo K, Bevilacqua C, Gaboriau-Kouthiau V, Moreau M-C, Heyman M. 2003. Gastric Helicobacter infection inhibits development of oral tolerance to food antigens in mice. Infect Immun 71:5219-5224.
71. Maurer KJ, Ihrig MM, Rogers AB, Ng V, Bouchard G, Leonard MR, Carey MC, Fox JG. 2005. Identification of cholelithogenic en- terohepatic Helicobacter species and their role in murine cholesterol gallstone formation. Gastroenterology 128:1023-1033.
72. + T cells in vivo. J Immunol 169:3914-3919.
73. Mendes EN, Queiroz DM, Dewhirst FE, Paster BJ, Moura SB, Fox JG. 1996. Helicobacter trogontum sp. nov. isolated from the rat intestine. Int J Syst Bacteriol 46:916-921.
74. Mera R, Fontham ETH, Bravo LE, Bravo JC, Piazuelo MB, Camargo MC, Correa P. 2005. Long-term follow-up of patients treated for Helicobacter pylori infection. Gut 54:1536-1540.
75. Moura SB, Mendes EN, Queiroz DM, Camargos ER, Evangelina M, Fonseca F, Rocha G A, Nicoli JR. 1998. Ultrastructure of Helicobacter trogontum in culture and in the gastrointestinal tract of gnotobiotic mice. J Med Microbiol 47:513-520.
76. Murakami K, Fujioka T, Nishizono A, Nagai J, Tokieda M, Kodama R, Kubota T, Nasu M. 1996. Atopic dermatitis successfully treated by eradication of Helicobacter pylori. J Gastroenterol 31:77-82.
77. Myles MH, Dieckgraefe BK, Criley JM, Franklin CL. 2007. Characterization of cecal gene expression in a differentially susceptible mouse model of bacterial-induced inflammatory bowel disease, lnflamm Bowel Dis 13:822-836.
78. Myles MH, Livingston RS, Franklin CL. 2004. Pathogenicity of Helicobacter rodentium in A/JCr and SCID mice. Comp Med 54:549- 557.
79. Nagamine CM, Rogers AB, Fox JG, Schauer DB. 2008. Helicobacter hepaticus promotes azoxymethane-initiated colon tumorigenesis in BALB/c ILl0-deficient mice. Int J Cancer 122:832-838.
80. min mouse. Infect Immun 76:2758-2766.
81. Nilsson H-O, Taneera J, Castedal M, Glatz E, Olsson R, Wadstrom T. 2000. Identification of Helicobacter pylori and other Helicobacter species by PCR, hybridization, and partial DNA sequencing in human liver samples from patients with primary sclerosing cholangitis or primary biliary cirrhosis. J Clin Microbiol 38:1072-1076.
82. Patterson MM, Schrenzel MD, Feng Y, Fox JG. 2000. Gastritis and intestinal metaplasia in Syrian hamsters infected with Helicobacter aurati and 2 other microaerobes. Vet Pathol 37:589-596.
83. Patterson MM, Schrenzel MD, Feng Y, Xu S, Dewhirst FE, Paster BJ, Thibodeau SA, Versalovic J, Fox JG. 2000. Helicobacter aurati sp. nov., a urease-positive Helicobacter species cultured from gastrointestinal tissues of Syrian hamsters. J Clin Microbiol 38:3722-3728.
84. Pellicano R, Ménard A, Rizzetto M, Mégraud F. 2008. Helicobacter species and liver diseases: association or causation? Lancet Infect Dis 8:254-260.
85. Powrie F. 1995. T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity 3:171-174.
86. Queiroz DM, Contigli C, Coimbra RS, Nogueira AM, Mendes EN, Rocha GA, Moura SB. 1992. Spiral bacterium associated with gastric, ileal, and caecal mucosa of mice. Lab Anim 26:288-294.
87. Rao VP, Poutahidis T, Ge Z, Nambiar PR, Boussahmain C, Wang YY, Horwitz BH, Fox JG, Erdman SE. 2006. Innate immune inflammatory response against enteric bacteria Helicobacter hepaticus induces mammary adenocarcinoma in mice. Cancer Res 66:7395-7400.
88. Riley LK, Franklin CL, Hook RR Jr, Besch-Williford C. 1996. Identification of murine Helicobacters by PCR and restriction enzyme analyses. J Clin Microbiol 34:942-946.
89. Robertson BR, O'Rourke JL, Vandamme P, On SLW, Lee A. 2001. Helicobacter ganmani sp. nov., a urease-negative anaerobe isolated from the intestines of laboratory mice. Int J Syst Evol Microbiol 51:1881-1889.
90. Rogers AB, Boutin SR, Whary MT, Sundina N, Ge Z, Cormier K, Fox JG. 2004. Progression of chronic hepatitis and preneoplasia in Helicobacter hepaticus-inlected A/JCr mice. Toxicol Pathol 32:668-677.
91. Rogers AB, Fox JG. 2004. Inflammation and cancer. I. Rodent models of infectious gastrointestinal and liver cancer. Am J Physiol Gastro- intest Liver Physiol 286:G361-G366.
92. Rogers AB, Theve EJ, Feng Y, Fry RC, Taghizadeh K, Clapp KM, Boussahmain C, Cormier KS, Fox JG. 2007. Hepatocellular carcinoma associated with liver-gender disruption in male mice. Cancer Res 67:11536-11546.
93. Rossi G, Romagnoli S, Lauretti L, Pancotto L, Taccini E, Rappuoli R, Del Giudice G, Ruggiero P. 2004. Helicobacter pylori infection negatively influences pregnancy outcome in a mouse model. Helicobacter 9:152-157.
94. Sanders CJ, Yu Y, Moore DA 3rd, Williams IR, Gewirtz AT. 2006. Humoral immune response to flagellin requires T cells and activation of innate immunity. J Immunol 177:2810-2818.
95. Scavizzi F, Raspa M. 2006. Helicobacter typhlonius was detected in the sex organs of 3mouse strains but did not transmit vertically. Lab Anim 40:70-79.
96. Schubert ML, Peura DA. 2008. Control of gastric acid secretion in health and disease. Gastroenterology 134:1842-1860.
97. Seok S, Park J, Cho S, Baek M, Lee H, Kim D, Yang K, Jang D, Han B, Nam K, Park J. 2005. Health surveillance of specific pathogen- free and conventionally housed mice and rats in Korea. Exp Anim 54:85-92.
98. Shames B, Fox JG, Dewhirst F, Yan L, Shen Z, Taylor NS. 1995. Identification of widespread Helicobacter hepaticus infection in feces in commercial mouse colonies by culture and PCR assay. J Clin Microbiol 33:2968-2972.
99. Sharp JM, Vanderford DA, Chichlowski M, H. MM, Hale LP. 2008. Helicobacter infection decreases reproductive success of ILl0-deficient mice. Comp Med 58:447-453.
100. Shen Z, Fox JG, Dewhirst FE, Paster BJ, Foltz CJ, Yan L, Shames B, Perry L. 1997. Helicobacter rodentium sp. nov., a urease-negative Helicobacter species isolated from laboratory mice. Int J Syst Bacteriol 47:627-634.
101. Shen Z, Xu S, Dewhirst FE, Paster BJ, Pena JA, Modlin IM, Kidd M, Fox JG. 2005. A novel enterohepatic Helicobacter species Helicobacter mastomyrinus isolated from the liver and intestine of rodents. Helicobacter 10:59-70.
102. Shomer NH, Dangler CA, Marini RP, Fox JG. 1998. Helicobacter bilis-Helicobacter rodentium coinfection associated with diarrhea in a colony of SCID mice. Lab Anim Sci 48:455-459.
103. Shomer NH, Dangler CA, Schrenzel MD, Whary MT, Xu S, Feng Y, Paster BJ, Dewhirst FE, Fox JG. 2001. Cholangiohepatitis and inflammatory bowel disease induced by a novel urease-negative Helicobacter species in A/J and tac:Icr:Hascidf RF mice. Exp Biol Med 226:420-428.
104. Simmons JH, Riley LK, Besch-Williford CL, Franklin CL. 2000. Helicobacter mesocricetorum sp. nov., a novel Helicobacter isolated from the feces of Syrian hamsters. J Clin Microbiol 38:1811-1817.
105. Sipowicz MA, Weghorst CM, Shiao YH, Buzard GS, Calvert RJ, Anver MR, Anderson LM, Rice JM. 1997. Lack of p53 and Ras mutations in Helicobacter hepaticus-induced liver tumors in A/JCr mice. Carcinogenesis 18:233-236.
106. Sitaraman SV, Klapproth J-M, Moore DA 3rd, Landers C, Targan S, Williams IR, Gewirtz AT. 2005. Elevated flagellin-specific immunoglobulins in Crohn disease. Am J Physiol Gastrointest Liver Physiol 288:G403-G406.
107. Stanley J, Linton D, Burnens AP, Dewhirst FE, On SL, Porter A, Owen RJ, Costas M. 1994. Helicobacter pullorum sp. novgenotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology 140:3441-3449.
108. Stills HF Jr, Hook RR Jr, Kinden DA. 1989. Isolation of a Campy- lobacter-like organism from healthy Syrian hamsters (Mesocricetus auratus). J Clin Microbiol 27:2497-2501.
109. Taylor NS, Xu S, Nambiar P, Dewhirst FE, Fox JG. 2007. Entero- hepatic Helicobacter species are prevalent in mice from commercial and academic institutions in Asia, Europe, and North America. J Clin Microbiol 45:2166-2172.
110. Theve EJ, Feng Y, Taghizadeh K, Cormier KS, Bell DR, Fox JG, Rogers AB. 2008. Sex hormone influence on hepatitis in young male A/JCr mice infected with Helicobacter hepaticus. Infect Immun 76:4071-4078.
111. Torrence AE, Brabb T, Viney JL, Bielefeldt-Ohmann H, Treuting P, Seamons A, Drivdahl R, Zeng W, Maggio-Price L. 2008. Serum biomarkers in a mouse model of bacterial-induced inflammatory bowel disease. Inflamm Bowel Dis 14:480-490.
112. van Es JH, Giles RH, Clevers HC. 2001. The many faces of the tumor suppressor gene APC. Exp Cell Res 264:126-134.
113. Visy B, Fust G, Bygum A, Bork K, Longhurst H, Bucher C, Bouil- let L, Cicardi M, Farkas H. 2007. Helicobacter pylori infection as a triggering factor of attacks in patients with hereditary angioedema. Helicobacter 12:251-257.
114. Vorobjova T, Nilsson I, Terjajev S, Granholm M, Lyyra M, Porkka T, Prükk T, Salupere R, Maaroos HI, Wadström T, Uibo R. 2006. Serum antibodies to enterohepatic Helicobacter spp. in patients with chronic liver diseases and in a population with high prevalence of H. pylori infection. Dig Liver Dis 38:171-176.
115. Ward JM, Anver MR, Haines DC, Benveniste RE. 1994. Chronic active hepatitis in mice caused by Helicobacter hepaticus. Am J Pathol 145:959-968.
116. Ward JM, Fox JG, Anver MR, Haines DC, George CV, Collins MJ Jr, Gorelick PL, Nagashima K, Gonda MA, Gilden RV, Tully JG, Russell RJ, Benvensite RE, Paster BJ, Dewhirst FE, Donovan JC, Anderson LM, Rice JM. 1994. Chronic active hepatitis and associated liver tumors in mice caused by a presistent bacterial infection with a novel Helicobacter species. J Natl Cancer Inst 86:1222-1227.
117. Watanabe K, Murakami K, Maeda K, FujiokaT, Nasu M, Nishizono A. 2002. Intraperitoneal immunization led to T cell hyporesponsiveness to Helicobacter pylori infection in mice. Microbiol Immunol 46:441-147.
118. Wedi B, Wagner S, Werfel T, Manns MP, Kapp A. 1998. Prevalence of Helicobacter pylori-associated gastritis in chronic urticaria. Int Arch Allergy Immunol 116:288-294.
119. Whary MT, Cline J, King A, Ge Z, Shen Z, Sheppard B, Fox JG. 2001. Long-term colonization levels of Helicobacter hepaticus in the cecum of hepatitis-prone A/JCr mice are significantly lower than those in hepatitis-resistant C57BL/6 mice. Comp Med 51:413-417.
120. Whary MT, Cline JH, King AE, Hewes KM, Chojnacky D, Salvarrey A, Fox JG. 2000. Monitoring sentinel mice for Helicobacter hepaticus, H. rodentium, and H. bilis infection by use of polymerase chain reaction analysis and serologic testing. Comp Med 50:436-443.
121. Whary MT, Fox JG. 2004. Natural and experimental Helicobacter infections. Comp Med 54:128-158.
122. Wong BC-Y, Lam SK, Wong WM, Chen JS, Zheng TT, Feng RE, Lai KC, Hu WHC, Yuen ST, Leung SY, Fong DYT, Ho J, Ching CK, Chen JS. 2004. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 291:187-194.
123. You WC, Brown LM, Zhang L, Li JY, Jin ML, Chang YS, Ma JL, Pan KF, Liu WD, Hu Y, Crystal-Mansour S, Pee D, Blot WJ, Fraumeni JF jr, Xu GW, Gail MH. 2006. Randomized double-blind factorial trial of 3 treatments to reduce the prevalence of precancerous gastric lesions. J Natl Cancer Inst 98:974-983.
124. Zhang L, Danon SJ, Grehan M, Chan V, Lee A, Mitchell H. 2005. Natural colonization with Helicobacter species and the development of inflammatory bowel disease in ILl0-deficient mice. Helicobacter 10:223-230.
125. Zhang L, Mitchell H. 2006. The roles of mucus-associated bacteria in inflammatory bowel disease. Drugs Today (Bare) 42:605-616.