Chapter 43 : Enterohepatic Helicobacter Species

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Enterohepatic Helicobacter Species, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818005/9781555812133_Chap43-1.gif /docserver/preview/fulltext/10.1128/9781555818005/9781555812133_Chap43-2.gif


Most of the members of the genus do not normally colonize the gastric mucosa, but instead thrive in the mucosal surfaces of the intestinal tract and/or the liver of humans, other mammals, and birds. A growing number of enterohepatic species have also been reported to be associated with gastroenteritis, hepatitis, and other disease states in humans and in other animal species. The significance of the enterohepatic species in human disease and the true prevalence of these organisms in human populations remain to be determined. Chronic active hepatitis leading to hepatocellular neoplasia was also observed in germ-free female Swiss Webster mice following experimental infection with , clearly establishing the organism as a murine pathogen. has been documented as a cause of acute diarrhea in otherwise healthy individuals; however, bacteremia without gastroenteritis is more frequently associated with and infection in immunocompromised patients with AIDS or other underlying conditions. and have been shown to infect birds and mammals. By microscopic visualization, was found to have a higher density of colonization in the ileum than the cecum or colon in conventional mice and rats. can infect the stomach of mice and cause gastritis. Sequencing of PCR-amplified 16S rRNA gene fragments has been used to show that enterohepatic species can infect the gallbladder of humans with chronic cholecystitis.

Citation: Schauer D. 2001. Enterohepatic Helicobacter Species, p 533-548. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch43

Key Concept Ranking

Restriction Fragment Length Polymorphism
Mice Chronic Active Hepatitis
16s rRNA Sequencing
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Transmission electron micrograph of H. hepaticus grown in pure culture (A), scanning electron micrograph of an organism with typical H. hepaticus ultrastructure in the intestine of a mouse (B), and transmission electron micrograph of H. hepaticus in the liver of a mouse (C). Bars, 1 µm. Originally from Fox and Lee ( ) (B) and Li et al. ( ) (C).

Citation: Schauer D. 2001. Enterohepatic Helicobacter Species, p 533-548. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch43
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Transmission electron micrographs of “H. rappini” grown in pure culture (A), and in an intestinal crypt in a mouse (B), and scanning electron micrograph of “H. rappini” on the mucosal surface of the intestine of a mouse (C). Bars, 1 µm. Originally from Schauer et al. ( ).

Citation: Schauer D. 2001. Enterohepatic Helicobacter Species, p 533-548. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch43
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Archer, J. R.,, S. Romero,, A. E. Ritchie,, M. E. Hamacher,, B. M. Steiner,, J. H. Bryner,, and R. F. Schell. 1988. Characterization of an unclassified microaerophilic bacterium associated with gastroenteritis. J. Clin. Microbiol. 26:101105.
2. Atabay, H. I.,, J. E. Corry,, and S. L. On. 1998. Identification of unusual Campylobacter-like isolates from poultry products as Helicobacter pullorum. J. Appl. Microbiol. 84: 10171024.
3. Avenaud, P.,, A. Marais,, L. Monteiro,, B. Le Bail,, P. Bioulac Sage,, C. Balabaud,, and F. Megraud. 2000. Detection of Helicobacter species in the liver of patients with and without primary liver carcinoma. Cancer 89:14311439.
4. Bracke, J. W.,, D. L. Cruden,, and A. J. Markovetz. 1979. Intestinal microbial flora of the American cockroach, Periplaneta americana L. Appl. Environ. Microbiol. 38:945955.
5. Bryner, J. H., 1988. Flexispira rappini, gen. nov., sp. nov. A motile, urease-producing rod similar to Campylobacter pyloridis, p. 440. In B. Kaijser, and E. Falsen (ed.), Campylobacter IV. Goterna, Kungalv, Sweden.
6. Bryner, J. H.,, A. E. Ritchie,, L. Pollet,, C. A. Kirkbride,, and J. E. Collins. 1987. Experimental infection and abortion of pregnant guinea pigs with a unique spirillum-like bacterium isolated from aborted ovine fetuses. Am. J. Vet. Res. 48: 9195.
7. Burman, W. J.,, D. L. Cohn,, R. R. Reves,, and M. L. Wilson. 1995. Multifocal cellulitis and monoarticular arthritis as manifestations of Helicobacter cinaedi bacteremia. Clin. Infect. Dis. 20:564570.
8. Burnens, A. P.,, J. Stanley,, R. Morgenstern,, and J. Nicolet. 1994. Gastroenteritis associated with Helicobacter pullorum. Lancet 344:15691570.
9. Burnens, A. P.,, J. Stanley,, U. B. Schaad,, and J. Nicolet. 1993. Novel Campylobacter-like organism resembling Helicobacter fennelliae isolated from a boy with gastroenteritis and from dogs. J. Clin. Microbiol. 31:19161917.
10. Cahill, R. J.,, C. J. Foltz,, J. G. Fox,, C. A. Dangler,, F. Powrie,, and D. B. Schauer. 1997. Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect. Immun. 65:31263131.
11. Canella, K. A.,, B. A. Diwan,, P. L. Gorelick,, P. J. Donovan,, M. A. Sipowicz,, K. S. Kasprzak,, C. M. Weghorst,, E. G. Snyderwine,, C. D. Davis,, L. K. Keefer,, S. A. Kyrtopoulos,, S. S. Hecht,, M. Wang,, L. M. Anderson,, and J. M. Rice. 1996. Liver tumorigenesis by Helicobacter hepaticus: considerations of mechanism. In Vivo 10:285292.
12. Chien, C. C.,, N. S. Taylor,, Z. Ge,, D. B. Schauer,, V. B. Young,, and J. G. Fox. 2000. Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp. J. Med. Microbiol. 49:525534.
13. Chin, E. Y.,, C. A. Dangler,, J. G. Fox,, and D. B. Schauer. 2000. Helicobacter hepaticus infection triggers inflammatory bowel disease in T cell receptor α β deficient mice. Comp. Med. 50:586594.
14. Chomarat, P.,, M. A. Sipowicz,, B. A. Diwan,, L. W. Fornwald,, Y. C. Awasthi,, M. R. Anver,, J. M. Rice,, L. M. Anderson,, and C. P. Wild. 1997. Distinct time courses of increase in cytochromes P450 1A2, 2A5 and glutathione S-transferases during the progressive hepatitis associated with Helicobacter hepaticus. Carcinogenesis 18:21792190.
15. Cimolai, N.,, M. J. Gill,, A. Jones,, B. Flores,, W. E. Stamm,, W. Laurie,, B. Madden,, and M. S. Shahrabadi. 1987. "Campylobacter cinaedi" bacteremia: case report and laboratory findings. J. Clin. Microbiol. 25:942943.
16. Crawshaw, T. R.,, and H. E. Fuller. 1994. Flexispira rappini suspected in ovine abortion. Vet. Rec. 134:507.
17. Cuccherini, B.,, K. Chua,, V. Gill,, S. Weir,, B. Wray,, D. Stewart,, D. Nelson,, L. Fuss,, and W. Strober. 2000. Bacteremia and skin/bone infections in two patients with X-linked agammaglobulinemia caused by an unusual organism related to Flexispiral/Helicobacter species. Clin. Immunol. 97: 121129.
18. Davis, C. P.,, J. S. McAllister,, and D. C. Savage. 1973. Microbial colonization of the intestinal epithelium in suckling mice. Infect. Immun. 7:666672.
19. Davis, C. P.,, D. Mulcahy,, A. Takeuchi,, and D. C. Savage. 1972. Location and description of spiral-shaped microorganisms in the normal rat cecum. Infect. Immun. 6:184192.
20. Dewhirst, F. E.,, C. C. Chien,, B. J. Paster,, R. L. Ericson,, R. P. Orcutt,, D. B. Schauer,, and J. G. Fox. 1999. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl. Environ. Microbiol. 65:32873292.
21. Dewhirst, F. E.,, J. G. Fox,, E. N. Mendes,, B. J. Paster,, C. E. Gates,, C. A. Kirkbride,, and K. A. Eaton. 2000. 'Flexispira rappini' strains represent at least 10 Helicobacter taxa. Int. J. Syst. Evol. Microbiol. 50:17811787.
22. Dewhirst, F. E.,, C. Seymour,, G. J. Fraser,, B. J. Paster,, and J. G. Fox. 1994. Phylogeny of Helicobacter isolates from bird and swine feces and description of Helicobacter pametensis sp. nov. Int. J. Syst. Bacterial. 44:553560.
23. Dieleman, L. A.,, A. Arends,, S. L. Tonkonogy,, M. S. Goerres,, D. W. Craft,, W. Grenther,, R. K. Sellon,, E. Balish,, and R. B. Sartor. 2000. Helicobacter hepaticus does not induce or potentiate colitis in interleukin-10-deficient mice. Infect. Immun. 68:51075113.
24. 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. 25:597605.
25. Eaton, K. A.,, F. E. Dewhirst,, B. J. Paster,, N. Tzellas,, B. E. Coleman,, J. Paola,, and R. Sherding. 1996. Prevalence and varieties of Helicobacter species in dogs from random sources and pet dogs: animal and public health implications. J. Clin. Microbiol. 34:31653170.
26. Erlandsen, S. L.,, and D. G. Chase. 1972. Paneth cell function: phagocytosis and intracellular digestion of intestinal microorganisms. II. Spiral microorganism. J. Ultrastruct. Res. 41: 319333.
27. Fleisch, F.,, A. Burnens,, R. Weber,, and R. Zbinden. 1998. Helicobacter species strain Mainz isolated from cultures of blood from two patients with AIDS. Clin. Infect. Dis. 26: 526527.
28. Flores, B. M.,, C. L. Fennell,, L. Kuller,, M. A. Bronsdon,, W. R. Morton,, and W. E. Stamm. 1990. Experimental infection of pig-tailed macaques (Macaca nemestrina) with Campylobacter cinaedi and Campylobacter fennelliae. Infect. Immun. 58:39473953.
29. Foley, J. E.,, S. L. Marks,, L. Munson,, A. Melli,, F. E. Dewhirst,, S. Yu,, Z. Shen,, and J. G. Fox. 1999. Isolation of Helicobacter canis from a colony of Bengal cats with endemic diarrhea. J. Clin. Microbiol. 37:32713275.
30. Foley, J. E.,, J. V. Solnick,, J. M. Lapointe,, S. Jang,, and N. C. Pedersen. 1998. Identification of a novel enteric Helicobacter species in a kitten with severe diarrhea. J. Clin. Microbiol. 36:908912.
31. Foltz, C. J.,, J. G. Fox,, R. Cahill,, J. C. Murphy,, L. Yan,, B. Shames,, and D. B. Schauer. 1998. Spontaneous inflammatory bowel disease in multiple mutant mouse lines: association with colonization by Helicobacter hepaticus. Helicobacter 3: 6978.
32. Foltz, C. J.,, J. G. Fox,, L. Yan,, and B. Shames. 1995. Evaluation of antibiotic therapies for eradication of Helicobacter hepaticus. Antimicrob. Agents Chemother. 39:12921294.
33. Foltz, C. J.,, J. G. Fox,, L. Yan,, and B. Shames. 1996. Evaluation of various oral antimicrobial formulations for eradication of Helicobacter hepaticus. Lab. Anim. Sci. 46:193197.
34. Foster, J. R. 1984. Bacterial infection of the common bile duct in chronic fascioliasis in the rat. J. Comp. Med. 94:175181.
35. Fox, J. G. 1997. The expanding genus of Helicobacter: pathogenic and zoonotic potential. Semin. Gastrointest. Dis. 8: 124141.
36. Fox, J. G.,, C. C. Chien,, F. E. Dewhirst,, B. J. Paster,, Z. Shen,, P. L. Melito,, D. L. Woodward,, and F. G. Rodgers. 2000. Helicobacter canadensis sp. nov. isolated from humans with diarrhea as an example of an emerging pathogen. J. Clin. Microbiol. 38:25462549.
37. Fox, J. G.,, F. E. Dewhirst,, Z. Shen,, Y. Feng,, N. S. Taylor,, B. J. Paster,, R. L. Ericson,, C. N. Lau,, P. Correa,, J. C. Araya,, and I. Roa. 1998. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 114:755763.
38. 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. 32:12381245.
39. Fox, J. G.,, R. Drolet,, R. Higgins,, S. Messier,, L. Yan,, B. E. Coleman,, B.J. Paster,, and F. E. Dewhirst. 1996. Helicobacter canis isolated from a dog liver with multifocal necrotizing hepatitis. J. Clin. Microbiol. 34:24792482.
40. Fox, J. G.,, P. L. Gorelick,, M. C. Kullberg,, Z. Ge,, F. E. Dewhirst,, and J. M. Ward. 1999. A novel urease-negative Helicobacter species associated with colitis and typhlitis in IL-10-deficient mice. Infect. Immun. 67:17571762.
41. Fox, J. G.,, and A. Lee. 1997. The role of Helicobacter species in newly recognized gastrointestinal tract diseases of animals. Lab. Anim. Sci. 47:222255.
42. Fox, J. G.,, X. Li,, L. Yan,, R. J. Cahill,, R. Hurley,, R. Lewis,, and J. C. Murphy. 1996. Chronic proliferative hepatitis in A/JCr mice associated with persistent Helicobacter hepaticus infection: a model of helicobacter-induced carcinogenesis. Infect. Immun. 64:15481558.
43. 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. 36:13821387.
44. Fox, J. G.,, L. Yan,, B. Shames,, J. Campbell,, J. C. Murphy,, and X. Li. 1996. Persistent hepatitis and enterocolitis in germ-free mice infected with Helicobacter hepaticus. Infect. Immun. 64:36733681.
45. Fox, J. G.,, L. 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. 33:445454.
46. Franklin, C. L.,, C. S. Beckwith,, R. S. Livingston,, L. K. Riley,, S. V. Gibson,, C. L. Besch-Williford,, and R. R. Hook, 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. 34:29522958.
47. Franklin, C. L.,, L. K. Riley,, R. S. Livingston,, C. S. Beckwith,, C. L. Besch-Williford,, and R. R. Hook, Jr. 1998. Enterohepatic lesions in SCID mice infected with Helicobacter bilis. Lab. Anim. Sci. 48:334339.
48. 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. 49:496505.
49. Gebhart, C. J.,, C. L. Fennell,, M. P. Murtaugh,, and W. E. Stamm. 1989. Campylobacter cinaedi is normal intestinal flora in hamsters. J. Clin. Microbiol. 27:16921694.
50. Gibson, J. R.,, M. A. Ferrus,, D. Woodward,, J. Xerry,, and R. J. Owen. 1999. Genetic diversity in Helicobacter pullorum from human and poultry sources identified by an amplified fragment length polymorphism technique and pulsed-field gel electrophoresis. J. Appl. Microbiol. 87:602610.
51. 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. 26:602611.
52. Haines, D. C.,, P. L. Gorelick,, J. K. Battles,, K. M. Pike,, R. J. Anderson,, J. G. Fox,, N. S. Taylor,, Z. Shen,, F. E. Dewhirst,, M. R. Anver,, and J. M. Ward. 1998. Inflammatory large bowel disease in immunodeficient rats naturally and experimentally infected with Helicobacter bilis. Vet. Pathol. 35: 202208.
53. Hampton, J. C. 1967. The effects of nitrogen mustard on the intestinal epithelium of the mouse. Radiat. Res. 30:576589.
54. Han, S.,, C. Schindel,, R. Genitsariotis,, E. Marker-Hermann,, S. Bhakdi,, and M. J. Maeurer. 2000. Identification of a unique Helicobacter species by 16S rRNA gene analysis in an abdominal abscess from a patient with X-linked hypogammaglobulinemia. J. Clin. Microbiol. 38:27402742.
55. Hsueh, P. R.,, L. J. Teng,, C. C. Hung,, Y. C. Chen,, P. C. Yang,, S. W. Ho,, and K. T. Luh. 1999. Septic shock due to Helicobacter fennelliae in a non-human immunodeficiency virus-infected heterosexual patient. J. Clin. Microbiol. 37:20842086.
56. Hung, C. C.,, P. R. Hsueh,, M. Y. Chen,, L. J. Teng,, Y. C. Chen,, K. T. Luh,, and C. Y. Chuang. 1997. Bacteremia caused by Helicobacter cinaedi in an AIDS patient. J. Formos. Med. Assoc. 96:558560.
57. Husmann, M.,, C. Gries,, P. Jehnichen,, T. Woelfel,, G. Gerken,, W. Ludwig,, and S. Bhakdi. 1994. Helicobacter sp. strain Mainz isolated from an AIDS patient with septic arthritis: case report and nonradioactive analysis of 16S rRNA sequence. J. Clin. Microbiol. 32:30373039.
58. Hutto, D. L.,, and M. J. Wannemuehler. 1999. A comparison of the morphologic effects of Serpulina hyodysenteriae or its beta-hemolysin on the murine cecal mucosa. Vet. Pathol. 36: 3747.
59. Jalava, K.,, S. L. W. On,, P. A. Vandamme,, I. Happonen,, A. Sukura,, and M. L. Hanninen. 1998. Isolation and identification of Helicobacter spp. from canine and feline gastric mucosa. Appl. Environ. Microbiol. 64:39984006.
60. Kawaguchi, M.,, T. Saito,, H. Ohno,, S. Midorikawa,, T. Sanji,, Y. Handa,, S. Morita,, H. Yoshida,, M. Tsurui,, R. Misaka,, T. Hirota,, M. Saito,, and K. Minami. 1996. Bacteria closely resembling Helicobacter pylori detected immunohistologi-cally and genetically in resected gallbladder mucosa. J. Gastroenterol. 31:294298.
61. Kiehlbauch, J. A.,, D. J. Brenner,, D. N. Cameron,, A. G. Steigerwalt,, J. M. Makowski,, C. N. Baker,, C. M. Patton,, and I. K. Wachsmuth. 1995. Genotypic and phenotypic characterization of Helicobacter cinaedi and Helicobacter fennelliae strains isolated from humans and animals. J. Clin. Microbiol. 33:29402947.
62. Kirkbride, C. A.,, C. E. Gates,, and J. E. Collins. 1986. Abortion in sheep caused by a nonclassified, anaerobic, flagellated bacterium. Am. J. Vet. Res. 47:259262.
63. Kirkbride, C. A.,, C. E. Gates,, J. E. Collins,, and A. E. Ritchie. 1985. Ovine abortion associated with an anaerobic bacterium. J. Am. Vet. Med. Assoc. 186:789791.
64. 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 in-terleukin-10 (IL-lO)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun. 66: 51575166.
65. Lasry, S.,, J. Simon,, A. Marais,, J. Pouchot,, P. Vinceneux,, and Y. Boussougant. 2000. Helicobacter cinaedi septic arthritis and bacteremia in an immunocompetent patient. Clin. Infect. Dis. 31:201202.
66. Lee, A.,, M. Chen,, N. Coltro,, J. O'Rourke,, S. Hazell,, P. Hu,, and Y. Li. 1993. Long term infection of the gastric mucosa with Helicobacter species does induce atrophic gastritis in an animal model of Helicobacter pylori infection. Zentralbl. Bakteriol. 280:3850.
67. 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. 42:2736.
68. 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. 66:54775484.
69. Lin, T. T.,, C. T. Yeh,, C. S. Wu,, and Y. F. Liaw. 1995. Detection and partial sequence analysis of Helicobacter pylori DNA in the bile samples. Dig. Dis. Sci. 40:22142219.
70. Livingston, R. S.,, L. K. Riley,, E. K. Steffen,, C. L. Besch-Williford,, R. R. Hook, Jr.,, and C. L. Franklin. 1997. Serodiagnosis of Helicobacter hepaticus infection in mice by an enzyme-linked immunosorbent assay. J. Clin. Microbiol. 35: 12361238.
71. Malarkey, D. E.,, T. V. Ton,, J. R. Hailey,, and T. R. Devereux. 1997. A PCR-RFLP method for the detection of Helicobacter hepaticus in frozen or fixed liver from B6C3F1 mice. Toxicol. Pathol. 25:606612.
72. Mammen, M. P., Jr.,, N. E. Aronson,, W. J. Edenfield,, and T. P. Endy. 1995. Recurrent Helicobacter cinaedi bacteremia in a patient infected with human immunodeficiency virus: case report. Clin. Infect. Dis. 21:1055.
73. Melito, P. L.,, D. L. Woodward,, K. A. Bernard,, L. Price,, R. Khakhria,, W. M. Johnson,, and F. G. Rodgers. 2000. Differentiation of clinical Helicobacter pullorum isolates from related Helicobacter and Campylobacter species. Helicobacter 5:142147.
74. Mendes, E. N.,, D. M. Queiroz,, F. E. Dewhirst,, B. J. Paster,, S. B. Moura,, and J. G. Fox. 1996. Helicobacter trogontum sp. nov., isolated from the rat intestine. Int. J. Syst. Bacterial. 46:916921.
75. 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. 47:513520.
76. Neiger, R.,, C. Dieterich,, A. Burnens,, A. Waldvogel,, I. Corthesy-Theulaz,, F. Halter,, B. Lauterburg,, and A. Schmassmann. 1998. Detection and prevalence of Helicobacter infection in pet cats. J. Clin. Microbiol. 36:634637.
77. Ng, V. L.,, W. K. Hadley,, C. L. Fennell,, B. M. Flores,, and W. E. Stamm. 1987. Successive bacteremias with "Campylobacter cinaedi" and "Campylobacter fennelliae" in a bisexual male. J. Clin. Microbiol. 25:20082009.
78. Nilsson, H. O.,, M. Castedal,, R. Olsson,, and T. Wadstrom. 1999. Detection of Helicobacter in the liver of patients with chronic cholestatic liver diseases. J. Physiol. Pharmacol. 50: 875882.
79. Nilsson, H. G.,, J. Taneera,, M. Castedal,, E. Glatz,, R. Olsson,, and T. Wadstrom. 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. 38:10721076.
80. Nilsson, I.,, S. Lindgren,, S. Eriksson,, and T. Wadstrom. 2000. Serum antibodies to Helicobacter hepaticus and Helicobacter pylori in patients with chronic liver disease. Gut 46:410414.
81. Nyska, A.,, R. R. Maronpot,, S. R. Eldridge,, J. K. Haseman,, and J. R. Hailey. 1997. Alteration in cell kinetics in control B6C3F1 mice infected with Helicobacter hepaticus. Toxicol. Pathol. 25:591596.
82. Orlicek, S. L.,, D. F. Welch,, and T. L. Kuhls. 1993. Septicemia and meningitis caused by Helicobacter cinaedi in a neonate. J. Clin. Microbiol. 31:569571.
83. Patterson, M. M.,, M. D. Schrenzel,, Y. Feng,, and J. G. Fox. 2000. Gastritis and intestinal metaplasia in Syrian hamsters infected with Helicobacter aurati and two other microaerobes. Vet. Pathol. 37:589596.
84. Patterson, M. M.,, M. D. Schrenzel,, Y. Feng,, S. Xu,, F. E. Dewhirst,, B. J. Paster,, S. A. Thibodeau,, J. Versalovic,, and J. G. Fox. 2000. Helicobacter aurati sp. nov., a urease-positive helicobacter species cultured from gastrointestinal tissues of Syrian hamsters. J. Clin. Microbiol. 38:37223728.
85. Phillips, M. W.,, and A. Lee. 1983. Isolation and characterization of a spiral bacterium from the crypts of rodent gastrointestinal tracts. Appl. Environ. Microbiol. 45:675683.
86. Pickett, C. L.,, and C. A. Whitehouse. 1999. The cytolethal distending toxin family. Trends Microbiol. 7:292297.
87. Queiroz, D. M.,, C. Contigli,, R. S. Coimbra,, A. M. Nogueira,, E. N. Mendes,, G. A. Rocha,, and S. B. Moura. 1992. Spiral bacterium associated with gastric, ileal and caecal mucosa of mice. Lab. Anim. 26:288294.
88. Ramljalc, D.,, A. B. Jones,, B. A. Diwan,, A. O. Perantoni,, J. F. Hochadel,, and L. M. Anderson. 1998. Epidermal growth factor and transforming growth factor-alpha-associated over-expression of cyclin Dl, Cdk4, and c-Myc during hepatocarcinogenesis in Helicobacter hepaticus-infected A/JCr mice. Cancer Res. 58:35903597.
89. 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: 942946.
90. Roe, I. H.,, J. T. Kim,, H. S. Lee,, and J. H. Lee. 1999. Detection of Helicobacter DNA in bile from bile duct diseases. J. Korean Med. Sci. 14:182186.
91. Romero, S.,, J. R. Archer,, M. E. Hamacher,, S. M. Bologna,, and R. F. Schell. 1988. Case report of an unclassified microaerophilic bacterium associated with gastroenteritis. J. Clin. Microbiol. 26:142143.
92. Rudi, J.,, A. Rudy,, M. Maiwald,, and W. Stremmel. 1999. Helicobacter sp. are not detectable in bile from German patients with biliary disease. Gastroenterology 116: 10161017.
93. Russell, R. J.,, D. C. Haines,, M. R. Anver,, J. K. Battles,, P. L. Gorelick,, L. L. Blumenauer,, M. A. Gonda,, and J. M. Ward. 1995. Use of antibiotics to prevent hepatitis and typhlitis in male scid mice spontaneously infected with Helicobacter hepaticus. Lab. Anim. Sci. 45:373378.
94. Sacks, L. V.,, A. M. Labriola,, V. J. Gill,, and F. M. Gordin. 1991. Use of ciprofloxacin for successful eradication of bacteremia due to Campylobacter cinaedi in a human immunodeficiency virus-infected person. Rev. Infect. Dis. 13: 10661068.
95. Saunders, K. E.,, Z. Shen,, F. E. Dewhirst,, B. J. Paster,, C. A. Dangler,, and J. G. Fox. 1999. Novel intestinal Helicobacter species isolated from cotton-top tamarins (Saguinus oedipus) with chronic colitis. J. Clin. Microbiol. 37:146151.
96. Schauer, D. B.,, N. Ghori,, and S. Falkow. 1993. Isolation and characterization of "Flexispira rappini" from laboratory mice. J. Clin. Microbiol. 31:27092714.
97. Sellon, R. K.,, S. Tonkonogy,, M. Schultz,, L. A. Dieleman,, W. Grenther,, E. Balish,, D. M. Rennick,, and R. B. Sartor. 1998. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleu-kin-10-deficient mice. Infect. Immun. 66:52245231.
98. Seymour, C.,, R. G. Lewis,, M. Kim,, D. F. Gagnon,, J. G. Fox,, F. E. Dewhirst,, and B. J. Paster. 1994. Isolation of Helicobacter strains from wild bird and swine feces. Appl. Environ. Microbiol. 60:10251028.
99. 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. 33:29682972.
100. Shen, Z.,, Y. Feng,, and J. G. Fox. 2000. Identification of enterohepatic Helicobacter species by restriction fragment-length polymorphism analysis of the 16S rRNA gene. Helicobacter 5:121128.
101. 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: 627634.
102. Shen, Z.,, D. B. Schauer,, H. L. Mobley,, and J. G. Fox. 1998. Development of a PCR-restriction fragment length polymorphism assay using the nucleotide sequence of the Helicobacter hepaticus urease structural genes ureAB. J. Clin. Microbiol. 36:24472453.
103. Shomer, N. H.,, C. A. Dangler,, R. P. Marini,, and J. G. Fox. 1998. Helicobacter bilislHelicobacter rodentium co-infection associated with diarrhea in a colony of scid mice. Lab. Anim. Sci. 48:455459.
104. Shomer, N. H.,, C. A. Dangler,, M. D. Schrenzel,, and J. G. Fox. 1997. Helicobacter bilis-'mduced inflammatory bowel disease in scid mice with defined flora. Infect. Immun. 65: 48584864.
105. Simmons, J. H.,, L. K. Riley,, C. L. Besch-Williford,, and C. L. Franklin. 2000. Helicobacter mesocricetorum sp. nov., a novel helicobacter isolated from the feces of Syrian hamsters. J. Clin. Microbiol. 38:18111817.
106. Sipowicz, M. A.,, P. Chomarat,, B. A. Diwan,, M. A. Anver,, Y. C. Awasthi,, J. M. Ward,, J. M. Rice,, K. S. Kasprzak,, C. P. Wild,, and L. M. Anderson. 1997. Increased oxidative DNA damage and hepatocyte overexpression of specific cytochrome P450 isoforms in hepatitis of mice infected with Helicobacter hepaticus. Am. J. Pathol. 151:933941.
107. Sipowicz, M. A.,, C. M. Weghorst,, Y. H. Shiao,, G. S. Buzard,, R. J. Calvert,, M. R. Anver,, L. M. Anderson,, and J. M. Rice. 1997. Lack of pS3 and ras mutations in Helicobacter hepaticus-induced liver tumors in A/JCr mice. Carcinogenesis 18: 233236.
108. Solnick, J. V.,, and D. B. Schauer. 2001. Emergence of the Helicobacter genus in the pathogenesis of gastrointestinal disease. Clin. Microbiol. Rev. 14:5997.
109. Sorlin, P.,, P. Vandamme,, J. Nortier,, B. Hoste,, C. Rossi,, S. Pavlof,, and M. J. Struelens. 1999. Recurrent "Flexispira rappini" bacteremia in an adult patient undergoing hemodialysis: case report. J. Clin. Microbiol. 37:13191323.
110. Stanley, J.,, D. Linton,, A. P. Burnens,, F. E. Dewhirst,, S. L. On,, A. Porter,, R.J. Owen,, and M. Costas. 1994. Helicobacter pullorum sp. nov.—genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology 140:34413449.
111. Stanley, J.,, D. Linton,, A. P. Burnens,, F. E. Dewhirst,, R. J. Owen,, A. Porter,, S. L. On,, and M. Costas. 1993. Helicobacter canis sp. nov., a new species from dogs: an integrated study of phenotype and genotype. J. Gen. Microbiol. 139:24952504.
112. Steinbrueckner, B.,, G. Haerter,, K. Pelz,, A. Burnens,, and M. Kist. 1998. Discrimination of Helicobacter pullorum and Campylobacter lari by analysis of whole cell fatty acid extracts. FEMS Microbiol. Lett. 168:209212.
113. Steinbrueckner, B.,, G. Haerter,, K. Pelz,, S. Weiner,, J. A. Rump,, W. Deissler,, S. Bereswill,, and M. Kist. 1997. Isolation of Helicobacter pullorum from patients with enteritis. Scand. J. Infect. Dis. 29:315318.
114. Sullivan, A. K.,, M. R. Nelson,, J. Walsh,, and B. G. Gazzard. 1997. Recurrent Helicobacter cinaedi cellulitis and bacteremia in a patient with HIV Infection. Int. J. STD AIDS. 8: 5960.
115. Taylor, N. S.,, J. G. Fox,, and L. Yan. 1995. In-vitro hepatotoxic factor in Helicobacter hepaticus, H. pylori and other Helicobacter species. J. Med. Microbiol. 42:4852.
116. Tee, W.,, B. N. Anderson,, B. C. Ross,, and B. Dwyer. 1987. Atypical Campylobacters associated with gastroenteritis. J. Clin. Microbiol. 25:12481252.
117. Tee, W.,, K. Leder,, E. Karroum,, and M. Dyall-Smith. 1998. "Flexispira rappini" bacteremia in a child with pneumonia. J. Clin. Microbiol. 36:16791682.
118. Tee, W.,, A. C. Street,, D. Spelman,, W. Munckhof,, and A. Mijch. 1996. Helicobacter cinaedi bacteraemia: varied clinical manifestations in three homosexual males. Scand. J. Infect. Dis. 28:199203.
119. Totten, P. A.,, C. L. Fennell,, F. C. Tenover,, J. M. Wezenberg,, P. L. Perine,, W. E. Stamm,, and K. K. Holmes. 1985. Campylobacter cinaedi (sp. nov.) and Campylobacter fennelliae (sp. nov.): two new Campylobacter species associated with enteric disease in homosexual men. J. Infect. Dis. 151:131139.
120. Trivett-Moore, N. L.,, W. D. Rawlinson,, M. Yuen,, and G. L. Gilbert. 1997. Helicobacter westmeadii sp. nov., a new species isolated from blood cultures of two AIDS patients. J. Clin. Microbiol. 35:11441150.
121. Truett, G. E.,, J. A. Walker,, and D. G. Baker. 2000. Eradication of infection with Helicobacter spp. by use of neonatal transfer. Comp. Med. 50:444451.
122. Vandamme, P.,, E. Falsen,, B. Pot,, K. Kersters,, and J. De Ley. 1990. Identification of Campylobacter cinaedi isolated from blood and feces of children and adult females. J. Clin. Microbiol. 28:10161020.
123. Vandamme, P.,, C. S. Harrington,, K. Jalava,, and S. L. On. 2000. Misidentifying helicobacters: the Helicobacter cinaedi example. J. Clin. Microbiol. 38:22612266.
124. van der Ven, A. J.,, B. J. Kullberg,, P. Vandamme,, and J. F. Meis. 1996. Helicobacter cinaedi bacteremia associated with localized pain but not with cellulitis. Clin. Infect. Dis. 22:710711.
125. von Freeden-Jeffry, U.,, N. Davidson,, R. Wiler,, M. Fort,, S. Burdach,, and R. Murray. 1998. IL-7 deficiency prevents development of a non-T cell non-B cell-mediated colitis. J. Immunol. 161:56735680.
126. Ward, J. M.,, M. R. Anver,, D. C. Haines,, and R. E. Benveniste. 1994. Chronic active hepatitis in mice caused by Helicobacter hepaticus. Am. J. Pathol. 145:959968.
127. 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. 46:1520.
128. Ward, J. M.,, R. E. Benveniste,, C. H. Fox,, J. K. Battles,, M. A. Gonda,, and J. G. Tully. 1996. Autoimmunity in chronic active Helicobacter hepatitis of mice. Serum antibodies and expression of heat shock protein 70 in liver. Am. J. Pathol. 148:509517.
129. 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. 86:12221227.
130. Weir, S.,, B. Cuccherini,, A. M. Whitney,, M. L. Ray,, J. P. MacGregor,, A. Steigerwalt,, M. I. Daneshvar,, R. Weyant,, B. Wray,, J. Steele,, W. Strober,, and V. I. Gill. 1999. Recurrent bacteremia caused by a "Flexispira"-like organism in a patient with X-linked (Bruton's) agammaglobulinemia. J. Clin. Microbiol. 37:24392445.
131. Weir, S. C.,, C. L. Gibert,, F. M. Gordin,, S. H. Fischer,, and V. J. Gill. 1999. An uncommon Helicobacter isolate from blood: evidence of a group of Helicobacter spp. pathogenic in AIDS patients. J. Clin. Microbiol. 37:27292733.
132. 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. 50:436443.
133. Whary, M. T.,, T. J. Morgan,, C. A. Dangler,, K. J. Gaudes,, N. S. Taylor,, and J. G. Fox. 1998. Chronic active hepatitis induced by Helicobacter hepaticus in the A/JCr mouse is associated with a Thl cell-mediated immune response. Infect. Immun. 66:31423148.
134. Young, V. B.,, C. C. Chien,, K. A. Knox,, N. S. Taylor,, D. B. Schauer,, and J. G. Fox. 2000. Cytolethal distending toxin in avian and human isolates of Helicobacter pullorum. J. Infect. Dis. 182:620623.
135. Young, V. B.,, K. A. Knox,, and D. B. Schauer. 2000. Cytolethal distending toxin sequence and activity in the enterohepatic pathogen Helicobacter hepaticus. Infect. Immun. 68: 184191.


Generic image for table
Table 1

Selected characteristics of enterohepatic Helicobacter speciesa

Citation: Schauer D. 2001. Enterohepatic Helicobacter Species, p 533-548. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch43

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error