{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T18:27:05Z","timestamp":1791916025862,"version":"4.3.4"},"reference-count":40,"publisher":"Microbiology Society","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2010,10,1]]},"abstract":"<jats:p><jats:italic>Helicobacter marmotae<\/jats:italic>has been identified in the inflamed livers of Eastern woodchucks (<jats:italic>Marmota monax<\/jats:italic>) infected with woodchuck hepatitis virus (WHV), as well as from the livers of WHV-negative woodchucks. Because the majority of WHV-positive woodchucks with hepatic tumours were culture or PCR positive for this helicobacter, and WHV-negative woodchucks with<jats:italic>H. marmotae<\/jats:italic>had hepatitis, the bacterium may have a role in tumour promotion related to chronic inflammation. In this study, the type strain of<jats:italic>H. marmotae<\/jats:italic>was inoculated intraperitoneally into 48 male and female A\/J mice, a strain noted to be susceptible to<jats:italic>Helicobacter hepaticus<\/jats:italic>-induced liver tumours. Sixteen mice served as mock-dosed controls. At 6, 12 and 18 months post-inoculation (p.i.), there were statistically significant (<jats:italic>P<\/jats:italic>&lt;0.05) differences in mean inflammation scores for the caecum and proximal colon between experimentally infected and control mice. Differences in hepatic inflammation were significant (<jats:italic>P<\/jats:italic>&lt;0.05) at 6 and 12 months p.i. between the two groups but not at the 18 month time point. Two infected male mice had livers with severe hepatitis, and the liver samples were culture positive for<jats:italic>H. marmotae<\/jats:italic>. Serum IgG levels in the mice dosed with<jats:italic>H. marmotae<\/jats:italic>were elevated for the duration of the study. These results demonstrate that the woodchuck helicobacter can successfully colonize mice and cause enterohepatic disease. In the future, a mouse-adapted strain of<jats:italic>H. marmotae<\/jats:italic>could be selected to maximize colonization and lesion development. Such a woodchuck helicobacter-infected mouse model could be used to dissect potential mechanisms of microbial co-carcinogenesis involved in tumour development in woodchucks with WHV and in humans with hepatitis B virus.<\/jats:p>","DOI":"10.1099\/jmm.0.020479-0","type":"journal-article","created":{"date-parts":[[2010,7,9]],"date-time":"2010-07-09T02:26:33Z","timestamp":1278642393000},"page":"1235-1241","source":"Crossref","is-referenced-by-count":11,"title":["Experimental Helicobacter marmotae infection in A\/J mice causes enterohepatic disease"],"prefix":"10.1099","volume":"59","author":[{"given":"Mary M.","family":"Patterson","sequence":"first","affiliation":[{"name":"Division of Comparative Medicine, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Building 16-825, Cambridge, MA 02139, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arlin B.","family":"Rogers","sequence":"additional","affiliation":[{"name":"Division of Comparative Medicine, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Building 16-825, Cambridge, MA 02139, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James G.","family":"Fox","sequence":"additional","affiliation":[{"name":"Division of Comparative Medicine, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Building 16-825, Cambridge, MA 02139, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"345","reference":[{"key":"R1","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1128\/JCM.26.1.101-105.1988","article-title":"Characterization of an unclassified microaerophilic bacterium associated with gastroenteritis","volume":"26","author":"Archer","year":"1988","journal-title":"J Clin Microbiol"},{"key":"R2","doi-asserted-by":"crossref","first-page":"1916","DOI":"10.1128\/JCM.31.7.1916-1917.1993","article-title":"Novel Campylobacter -like organism resembling Helicobacter fennelliae isolated from a boy with gastroenteritis and from dogs","volume":"31","author":"Burnens","year":"1993","journal-title":"J Clin Microbiol"},{"key":"R3","doi-asserted-by":"crossref","first-page":"3126","DOI":"10.1128\/IAI.65.8.3126-3131.1997","article-title":"Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus","volume":"65","author":"Cahill","year":"1997","journal-title":"Infect Immun"},{"key":"R4","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1099\/0022-1317-49-6-525","article-title":"Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp","volume":"49","author":"Chien","year":"2000","journal-title":"J Med Microbiol"},{"key":"R5","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1128\/JCM.25.5.942-943.1987","article-title":"\u201c Campylobacter cinaedi \u201d bacteremia: case report and laboratory findings","volume":"25","author":"Cimolai","year":"1987","journal-title":"J Clin Microbiol"},{"key":"R6","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1016\/S0002-9440(10)63863-1","article-title":"CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice","volume":"162","author":"Erdman","year":"2003","journal-title":"Am J Pathol"},{"key":"R7","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1073\/pnas.0812347106","article-title":"Nitric oxide and TNF- \u03b1 trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus -infected, Rag2-deficient mice","volume":"106","author":"Erdman","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R8","first-page":"371","article-title":"Overview of Helicobacter pylori . 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carcinogenesis","volume":"64","author":"Fox","year":"1996b","journal-title":"Infect Immun"},{"key":"R12","doi-asserted-by":"crossref","first-page":"3673","DOI":"10.1128\/IAI.64.9.3673-3681.1996","article-title":"Persistent hepatitis and enterocolitis in germfree mice infected with Helicobacter hepaticus","volume":"64","author":"Fox","year":"1996c","journal-title":"Infect Immun"},{"key":"R13","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1177\/030098589703400308","article-title":"Helicobacter mustelae -associated gastric adenocarcinoma in ferrets ( Mustela putorius furo )","volume":"34","author":"Fox","year":"1997","journal-title":"Vet Pathol"},{"key":"R14","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/S0016-5085(98)70589-X","article-title":"Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic 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