Prevalence and spread of enterohepatic Helicobacter species in mice reared in a specific-pathogen-free animal facility

Journal of Clinical Microbiology

Volumn 44, Issue 3, 2006, Pages 738-742

  Bohr, U R M ^a   Selgrad, M ^a   Ochmann, C ^a   Backert, S ^a   Konig W ^a   Fenske, A ^a   Wex, T ^a   Malfertheiner, P ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ANIMAL EXPERIMENT; ANIMAL WELFARE; ARTICLE; BACTERIAL TRANSMISSION; CONTROLLED STUDY; FECES ANALYSIS; FILTER; HELICOBACTER; HELICOBACTER HEPATICUS; HELICOBACTER INFECTION; HELICOBACTER TYPHLONICUS; MASS SCREENING; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMAL HUSBANDRY; ANIMALS; BASE SEQUENCE; DNA, BACTERIAL; FECES; HELICOBACTER; HELICOBACTER INFECTIONS; HEPATITIS, ANIMAL; INFLAMMATORY BOWEL DISEASES; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; SPECIFIC PATHOGEN-FREE ORGANISMS;

ANIMALIA; BACTERIA (MICROORGANISMS); CRICETINAE; HELICOBACTER; HELICOBACTER GANMANI; HELICOBACTER HEPATICUS; HELICOBACTER TYPHLONIUS; HELICOBACTERACEAE;

EID: 33644884761     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.44.3.738-742.2006     Document Type: Article

References (41)

1. Bohr, U. R. M., B. Glasbrenner, A. Primus, A. Zagoura, T. Wex, and P. Malfertheiner. 2004. Identification of enterohepatic Helicobacter species in patients suffering from inflammatory bowel disease. J. Clin. Microbiol. 42:2766-2768.
2. Bohr, U. R. M., A. Primus, A. Zagoura, B. Glasbrenner, T. Wex, and P. Malferthelner. 2002. A group-specific PCR assay for the detection of Helicobacteraceae in human gut. Helicobacter 7:378-383.
3. Bohr, U. R. M., I. Segal, A. Primus, T. Wex, H. Hassan, R. Ally, and P. Malfertheiner. 2003. Detection of a putative novel Wolinella species in patients suffering from squamous cell carcinoma of the esophagus. Helicobacter 8:608-612.
4. Compton, S. R., L. J. Ball-Goodrich, C. J. Zeiss, L. K. Johnson, E. A. Johnson, and J. D. Macy. 2003. Pathogenesis of mouse hepatitis virus infection in gamma interferon-deficient mice is modulated by co-infection with Helicobacter hepaticus. Comp. Med. 53:197-206.
5. Diwan, B. A., J. M. Ward, D. Ramljak, and L. M. Anderson. 1997. Promotion by Helicobacter hepaticus-induced hepatitis of hepatic tumors initiated by N-nitrosodimethylamine in male A/JCr mice. Toxicol. Pathol. 25:597-605.
6. Fox, J. G., F. E. Dewhirst, J. G. Tully, B. J. Paster, L. Yan, N. S. Taylor, M. J. Collins, Jr., P. L. Gorelick, and J. M. Ward. 1994. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J. Clin. Microbiol. 32:1238-1245.
7. Fox, J. G, J. A. MacGregor, Z. Shen, X. Li, R. Lewis, and C. A. Dangler. 1998. Comparison of methods of identifying Helicobacter hepaticus in B6C3F1 mice used in a carcinogenesis bioassay. J. Clin. Microbiol. 36:1382-1387.
8. Fox, J. G., A. B. Rogers, M. T. Whary, N. S. Taylor, S. Xu, Y. Feng, and S. Keys. 2004. Helicobacter bilis-associated hepatitis in outbred mice. Comp. Med. 54:571-577.
9. Fox, J. G., L. Yan, F. E. Dewhirst, B. J. Paster, B. Shames, J. C. Murphy, A. Hayward, J. C. Belcher, and E. N. Mendes. 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.
10. Fox, J. G., L. Yan, B. Shames, J. Campbell, J. C. Murphy, and X. Li. 1996. Persistent hepatitis and enterocolitis in germfree mice infected with Helicobacter hepaticus. Infect. Immun. 64:3673-3681.
11. Franklin, C. L., L. K. Riley, R. S. Livingston, C. S. Beckwitb, C. L. Besch-Williford, and R. R. Hook, Jr. 1998. Enterohepatic lesions in SCID mice infected with Helicobacter bilis. Lab. Anim. Sci. 48:334-339.
12. Franklin, C. L., L. K. Riley, R. S. Livingston, C. S. Beckwith, R. R. Hook, Jr., C. L. Besch-Williford, R. Hunziker, and P. L. Gorelick. 1999. Enteric lesions in SCID mice infected with "Helicobacter typhlonicus," a novel urease-negative Helicobacter species. Lab. Anim. Sci. 49:496-505.
13. Goto, K., H. Ohashi, A. Takakura, and T. Itoh. 2000. Current status of Helicobacter contamination of laboratory mice, rats, gerbils, and house musk shrews in Japan. Curr. Microbiol. 41:161-166.
14. Hailey, J. R., J. K. Haseman, J. R. Bucher, A. E. Radovsky, D. E. Malarkey, R. T. Miller, A. Nyska, and R. R. Maronpot. 1998. Impact of Helicobacter hepaticus infection in B6C3F1 mice from twelve National Toxicology Program two-year carcinogenesis studies. Toxicol. Pathol. 26:602-611.
15. Jiang, H. Q., N. Kushnir, M. C. Thurnheer, N. A. Bos, and J. J. Cebra. 2002. Monoassociation of SCID mice with Helicobacter muridarum, but not four other enterics, provokes IBD upon receipt of T cells. Gastroenterology 122:1346-1354.
16. Kullberg, M. C., J. M. Ward, P. L. Gorelick, P. Caspar, S. Hieny, A. Cheever, D. Jankovic, and A. Sher. 1998. 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. 66:5157-5166.
17. Lee, A., M. W. Phillips, J. L. O'Rourke, B. J. Paster, F. E. Dewhirst, G. J. Fraser, J. G. Fox, L. I. Sly, P. J. Romaniuk, T. J. Trust, and S. Kouprach. 1992. Helicobacter muridarum sp. nov., a microaerophilic helical bacterium with a novel ultrastructure isolated from the intestinal mucosa of rodents. Int. J. Syst. Bacteriol. 42:27-36.
18. Li, X., J. G. Fox, M. T. Whary, L. Yan, B. Shames, and Z. Zhao. 1998. SCID/NCr mice naturally infected with Helicobacter hepaticus develop progressive hepatitis, proliferative typhlitis, and colitis. Infect. Immun. 66:5477-5484.
19. Livingston, R. S., L. K. Riley, C. L. Besch-Williford, R. R. Hook, Jr., and C. L. Franklin. 1998. Transmission of Helicobacter hepaticus infection to sentinel mice by contaminated bedding. Lab. Anim. Sci. 48:291-293.
20. -/-) mice. Am. J. Pathol. 160:739-751.
21. Maurer, K. J., M. M. Ihrig, A. B. Rogers, V. Ng, G. Bouchard, M. R. Leonard, M. C. Carey, and J. G. Fox. 2005. Identification of cholelithogenic enterohepatic Helicobacter species and their role in murine cholesterol gallstone formation. Gastroenterology 128:1023-1033.
22. Moura, S. B., E. N. Mendes, D. M. Queiroz, E. R. Camargos, M. Evangelina, F. Fonseca, G. A. Rocha, and J. R. Nicoli. 1998. Ultrastructure of Helicobacter trogontum in culture and in the gastrointestinal tract of gnotobiotic mice. J. Med. Microbiol. 47:513-520.
23. Myles, M. H., R. S. Livingston, and C. L. Franklin. 2004. Pathogenicity of Helicobacter rodentium in A/JCr and SCID mice. Comp. Med. 54:549-557.
24. Nicklas, W., P. Baneux, R. Boot, T. Decelle, A. A. Deeny, M. Fumanelli, B. Illgen-Wilcke, and the Federation of European Laboratory Animal Science Associations Working Group on Health Monitoring of Rodent and Rabbit Colonies. 2002. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab. Anim. 36:20-42.
25. Nilsson, H. O., I. S. Ouis, U. Stenram, A. Ljungh, A. P. Moran, T. Wadstrom, and W. A. Al-Soud. 2004. High prevalence of Helicobacter species detected in laboratory mouse strains by multiplex PCR-denaturing gradient gel electrophoresis and pyrosequencing. J. Clin. Microbiol. 42:3781-3788.
26. Reuter, J. D., and R. C. Dysko. 2003. Quality assurance / surveillance monitoring programs for rodent colonies, p. 1-13. In J. D. Reuter and M. A. Suckow (ed.), Laboratory animal medicine and management. International Veterinary Information Service, Ithaca, N.Y.
27. Riley, L. K., C. L. Franklin, R. R. Hook, Jr., and C. Besch-Williford. 1996. Identification of murine helicobacters by PCR and restriction enzyme analyses. J. Clin. Microbiol. 34:942-946.
28. Robertson, B. R., J. L. O'Rourke, P. Vandamme, S. L. On, and A. Lee. 2001. Helicobacter ganmani sp. nov., a urease-negative anaerobe isolated from the intestines of laboratory mice. Int. J. Syst. Evol. Microbiol. 51:1881-1889.
29. Seok, S., J. Park, S. Cho, M. Baek, H. Lee, D. Kim, K. Yang, D. Jang, B. Han, K. Nam, and J. Park. 2005. Health surveillance of specific pathogen-free and conventionally-housed mice and rats in Korea. Exp. Anim. 54:85-92.
30. Shames, B., J. G. Fox, F. Dewhirst, L. Yan, Z. Shen, and N. S. Taylor. 1995. Identification of widespread Helicobacter hepaticus infection in feces in commercial mouse colonies by culture and PCR assay. J. Clin. Microbiol. 33:2968-2972.
31. Shen, Z., J. G. Fox, F. E. Dewhirst, B. J. Paster, C. J. Foltz, L. Yan, B. Shames, and L. Perry. 1997. Helicobacter rodentium sp. nov., a urease-negative Helicobacter species isolated from laboratory mice. Int. J. Syst. Bacteriol. 47:627-634.
32. Shen, Z., S. Xu, F. E. Dewhirst, B. J. Paster, J. A. Pena, I. M. Modlin, M. Kidd, and J. G. Fox. 2005. A novel enterohepatic Helicobacter species "Helicobacter mastomyrinus" isolated from the liver and intestine of rodents. Helicobacter 10:59-70.
33. Shomer, N. H., C. A. Dangler, M. D. Schrenzel, and J. G. Fox. 1997. Helicobacter bilis-induced inflammatory bowel disease in SCID mice with defined flora. Infect. Immun. 65:4858-4864.
34. Shomer, N. H., C. A. Dangler, M. D. Schrenzel, M. T. Whary, S. Xu, Y. Feng, B. J. Paster, F. E. Dewhirst, and J. G. Fox. 2001. Cholangiohepatitis and inflammatory bowel disease induced by a novel urease-negative Helicobacter species in A/J. and Tac:ICR:HascidfRF mice. Exp. Biol. Med. 226:420-428.
35. Simmons, J. H., L. K. Riley, C. L. Besch-Williford, and C. L. Franklin. 2000. Helicobacter mesocricetotum sp. nov., a novel Helicobacter isolated from the feces of Syrian hamsters. J. Clin. Microbiol. 38:1811-1817.
36. Ward, J. M., M. R. Anver, D. C. Haines, J. M. Melhorn, P. Gorelick, L. Yan, and J. G. Fox. 1996. Inflammatory large bowel disease in immunodeficient mice naturally infected with Helicobacter hepaticus. Lab. Anim. Sci. 46:15-20.
37. Ward, J. M., J. G. Fox, M. R. Anver, D. C. Haines, C. V. George, M. J. Collins, Jr., P. L. Gorelick, K. Nagashima, M. A. Gonda, R. V. Gilden, J. G. Tully, R. J. Russell, R. E. Benveniste, B. J. Paster, F. E. Dewhirst, J. C. Donovan, L. M. Anderson, and J. M. Rice. 1994. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J. Natl. Cancer Inst. 86:1222-1227.
38. Whary, M. T., J. H. Cline, A. E. King, C. A. Corcoran, S. Xu, and J. G. Fox. 2000. Containment of Helicobacter hepaticus by use of husbandry practices. Comp. Med. 50:78-81.
39. Whary, M. T., J. Cline, A. King, Z. Ge, Z. Shen, B. Sheppard, and J. G. Fox. 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.
40. Whary, M. T., J. H. Cline, A. E. King, K. M. Hewes, D. Chojnacky, A. Salvarrey, and J. G. Fox. 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.
41. Zhang, L., S. J. Danon, M. Grehan, V. Chan, A. Lee, and H. Mitchell. 2005. Natural colonization with Helicobacter species and the development of inflammatory bowel disease in interleukin-10-deficient mice. Helicobacter 10:223-230.