1887

Abstract

Several enterohepatic spp. (EHS) have been isolated from cats. Despite the reported association between EHS infection and intestinal neoplasia in other species, this association has not been explored in cats. In this study, 55 non-haematopoietic feline intestinal carcinoma cases were histopathologically evaluated. In contrast with prior reports, large intestinal (LI) carcinoma was observed with greater frequency (61 %) relative to small intestinal (SI) carcinoma (35 %). There was a significant association between intestinal location and animal gender. Of males examined, 83 % had LI carcinoma, while no such trend was observed in females. Previously described associations between Siamese breed and intestinal carcinoma could not be definitively confirmed, although the Siamese breed may be predisposed to SI carcinoma location. Of all carcinomas examined in this study, 62 % were classified as adenocarcinoma, although mucinous adenocarcinoma (28 %) and solid carcinoma (11 %) were also identified. Tumours were all moderately or poorly differentiated. When considered by intestinal location and histopathologic classification, LI adenocarcinoma was associated with significantly advanced mean age (13 years) when compared to SI adenocarcinoma and LI mucinous adenocarcinoma (mean, 9 years in both cases), which were also frequently encountered. To determine whether EHS might play a role in feline intestinal neoplasia, genus- and species-specific fluorescence hybridization was performed. Of these carcinoma cases, 56 % were positive for spp. and one or more species-specific assay for , or . The presence of EHS was significantly associated with both LI location (68 %) and mucinous adenocarcinoma (92 %). These findings suggest a role for intestinal bacteria in non-haematopoietic feline intestinal neoplasia.

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2016-08-01
2020-07-03
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References

  1. Abidi M. Z., Wilhelm M. P., Neff J. L., Hughes J. G., Cunningham S. A., Patel R.. 2013; Helicobacter canis bacteremia in a patient with fever of unknown origin. J Clin Microbiol51:1046–1048 [CrossRef][PubMed]
    [Google Scholar]
  2. Beisele M., Shen Z., Parry N., Mobley M., Taylor N. S., Buckley E., Abedin M. Z., Dewhirst F. E., Fox J. G.. 2011; Helicobacter marmotae and novel Helicobacter and Campylobacter species isolated from the livers and intestines of prairie dogs. J Med Microbiol60:1366–1374 [CrossRef][PubMed]
    [Google Scholar]
  3. Bridgeford E. C., Marini R. P., Feng Y., Parry N. M., Rickman B., Fox J. G.. 2008; Gastric Helicobacter species as a cause of feline gastric lymphoma: a viable hypothesis. Vet Immunol Immunopathol123:106–113 [CrossRef][PubMed]
    [Google Scholar]
  4. Burnens A. P., Stanley J., Schaad U. B., Nicolet J.. 1993; Novel Campylobacter-like organism resembling Helicobacter fennelliae isolated from a boy with gastroenteritis and from dogs. J Clin Microbiol31:1916–1917[PubMed]
    [Google Scholar]
  5. Casswall T. H., Németh A., Nilsson I., Wadström T., Nilsson H. O.. 2010; Helicobacter species DNA in liver and gastric tissues in children and adolescents with chronic liver disease. Scand J Gastroenterol45:160–167 [CrossRef][PubMed]
    [Google Scholar]
  6. Castiglioni V., Vailati Facchini R., Mattiello S., Luini M., Gualdi V., Scanziani E., Recordati C.. 2012; Enterohepatic Helicobacter spp. in colonic biopsies of dogs: molecular, histopathological and immunohistochemical investigations. Vet Microbiol159:107–114 [CrossRef][PubMed]
    [Google Scholar]
  7. Chan V., Crocetti G., Grehan M., Zhang L., Danon S., Lee A., Mitchell H.. 2005; Visualization of Helicobacter species within the murine cecal mucosa using specific fluorescence in situ hybridization. Helicobacter10:114–124 [CrossRef][PubMed]
    [Google Scholar]
  8. Chien C. C., Taylor N. S., Ge Z., Schauer D. B., Young V. B., Fox J. G.. 2000; Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp. J Med Microbiol49:525–534 [CrossRef][PubMed]
    [Google Scholar]
  9. Cribb A. E.. 1988; Feline gastrointestinal adenocarcinoma: a review and retrospective study. Can Vet J29:709–712[PubMed]
    [Google Scholar]
  10. Erdman S. E., Poutahidis T., Tomczak M., Rogers A. B., Cormier K., Plank B., Horwitz B. H., Fox J. G.. 2003a; CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol162:691–702 [CrossRef][PubMed]
    [Google Scholar]
  11. Erdman S. E., Rao V. P., Poutahidis T., Ihrig M. M., Ge Z., Feng Y., Tomczak M., Rogers A. B., Horwitz B. H., Fox J. G.. 2003b; CD4(+)CD25(+) regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res63:6042–6050
    [Google Scholar]
  12. Erdman S. E., Rao V. P., Poutahidis T., Rogers A. B., Taylor C. L., Jackson E. A., Ge Z., Lee C. W., Schauer D. B. et al. 2009; Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice. Proc Natl Acad Sci U S A106:1027–1032 [CrossRef][PubMed]
    [Google Scholar]
  13. Foley J. E., Marks S. L., Munson L., Melli A., Dewhirst F. E., Yu S., Shen Z., Fox J. G.. 1999; Isolation of Helicobacter canis from a colony of bengal cats with endemic diarrhea. J Clin Microbiol37:3271–3275[PubMed]
    [Google Scholar]
  14. Fox J. G., Drolet R., Higgins R., Messier S., Yan L., Coleman B. E., Paster B. J., Dewhirst F. E.. 1996a; Helicobacter canis isolated from a dog liver with multifocal necrotizing hepatitis. J Clin Microbiol34:2479–2482
    [Google Scholar]
  15. Fox J. G., Yan L., Shames B., Campbell J., Murphy J. C., Li X.. 1996b; Persistent hepatitis and enterocolitis in germfree mice infected with Helicobacter hepaticus . Infect Immun64:3673–3681
    [Google Scholar]
  16. Fox J. G., Dewhirst F. E., Shen Z., Feng Y., Taylor N. S., Paster B. J., Ericson R. L., Lau C. N., Correa P. et al. 1998; Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology114:755–763 [CrossRef][PubMed]
    [Google Scholar]
  17. Fox J. G., Gorelick P. L., Kullberg M. C., Ge Z., Dewhirst F. E., Ward J. M.. 1999; A novel urease-negative Helicobacter species associated with colitis and typhlitis in IL-10-deficient mice. Infect Immun67:1757–1762[PubMed]
    [Google Scholar]
  18. Fox J. G., Handt L., Xu S., Shen Z., Dewhirst F. E., Paster B. J., Dangler C. A., Lodge K., Motzel S., Klein H.. 2001; Novel Helicobacter species isolated from rhesus monkeys with chronic idiopathic colitis. J Med Microbiol50:421–429 [CrossRef][PubMed]
    [Google Scholar]
  19. Fox J. G., Shen Z., Xu S., Feng Y., Dangler C. A., Dewhirst F. E., Paster B. J., Cullen J. M.. 2002; Helicobacter marmotae sp. nov. isolated from livers of woodchucks and intestines of cats. J Clin Microbiol40:2513–2519 [CrossRef][PubMed]
    [Google Scholar]
  20. Fox J. G., Boutin S. R., Handt L. K., Taylor N. S., Xu S., Rickman B., Marini R. P., Dewhirst F. E., Paster B. J. et al. 2007; Isolation and characterization of a novel helicobacter species, "Helicobacter macacae," from rhesus monkeys with and without chronic idiopathic colitis. J Clin Microbiol45:4061–4063 [CrossRef][PubMed]
    [Google Scholar]
  21. Fox J. G., Ge Z., Whary M. T., Erdman S. E., Horwitz B. H.. 2011; Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol4:22–30 [CrossRef][PubMed]
    [Google Scholar]
  22. Gerrard J., Alfredson D., Smith I.. 2001; Recurrent bacteremia and multifocal lower limb cellulitis due to Helicobacter-like organisms in a patient with X-linked hypogammaglobulinemia. Clin Infect Dis33:E116118 [CrossRef][PubMed]
    [Google Scholar]
  23. Knutson C. G., Mangerich A., Zeng Y., Raczynski A. R., Liberman R. G., Kang P., Ye W., Prestwich E. G., Lu K. et al. 2013; Chemical and cytokine features of innate immunity characterize serum and tissue profiles in inflammatory bowel disease. Proc Natl Acad Sci U S A110:E23322341 [CrossRef][PubMed]
    [Google Scholar]
  24. Kosovsky J. E., Matthiesen D. T., Patnaik A. K.. 1988; Small intestinal adenocarcinoma in cats: 32 cases (1978–1985). J Am Vet Med Assoc192:233–235[PubMed]
    [Google Scholar]
  25. Kullberg M. C., Ward J. M., Gorelick P. L., Caspar P., Hieny S., Cheever A., Jankovic D., Sher A.. 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 Immun66:5157–5166[PubMed]
    [Google Scholar]
  26. Leemann C., Gambillara E., Prod'hom G., Jaton K., Panizzon R., Bille J., Francioli P., Greub G., Laffitte E. et al. 2006; First case of bacteremia and multifocal cellulitis due to Helicobacter canis in an immunocompetent patient. J Clin Microbiol44:4598–4600 [CrossRef][PubMed]
    [Google Scholar]
  27. Lertpiriyapong K., Handt L., Feng Y., Mitchell T. W., Lodge K. E., Shen Z., Dewhirst F. E., Muthupalani S., Fox J. G.. 2014; Pathogenic properties of enterohepatic Helicobacter spp. isolated from rhesus macaques with intestinal adenocarcinoma. J Med Microbiol63:1004–1016 [CrossRef][PubMed]
    [Google Scholar]
  28. Li X., Fox J. G., Whary M. T., Yan L., Shames B., Zhao Z.. 1998; SCID/NCr mice naturally infected with Helicobacter hepaticus develop progressive hepatitis, proliferative typhlitis, and colitis. Infect Immun66:5477–5484[PubMed]
    [Google Scholar]
  29. Lingeman C. H., Garner F. M.. 1972; Comparative study of intestinal adenocarcinomas of animals and man. J Natl Cancer Inst48:325–346[PubMed]
    [Google Scholar]
  30. Maggio-Price L., Treuting P., Zeng W., Tsang M., Bielefeldt-Ohmann H., Iritani B. M.. 2006; Helicobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice. Cancer Res66:828–838 [CrossRef][PubMed]
    [Google Scholar]
  31. Mangerich A., Knutson C. G., Parry N. M., Muthupalani S., Ye W., Prestwich E., Cui L., McFaline J. L., Mobley M. et al. 2012; Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci U S A109:E18201829 [CrossRef][PubMed]
    [Google Scholar]
  32. Marini R. P., Muthupalani S., Shen Z., Buckley E. M., Alvarado C., Taylor N. S., Dewhirst F. E., Whary M. T., Patterson M. M., Fox J. G.. 2010; Persistent infection of rhesus monkeys with ‘Helicobacter macacae' and its isolation from an animal with intestinal adenocarcinoma. J Med Microbiol59:961–969 [CrossRef][PubMed]
    [Google Scholar]
  33. Matsukura N., Yokomuro S., Yamada S., Tajiri T., Sundo T., Hadama T., Kamiya S., Naito Z., Fox J. G.. 2002; Association between Helicobacter bilis in bile and biliary tract malignancies: H. bilis in bile from Japanese and Thai patients with benign and malignant diseases in the biliary tract. Jpn J Cancer Res93:842–847 [CrossRef][PubMed]
    [Google Scholar]
  34. Nagamine C. M., Sohn J. J., Rickman B. H., Rogers A. B., Fox J. G., Schauer D. B.. 2008; Helicobacter hepaticus infection promotes colon tumorigenesis in the BALB/c-Rag2(−/−) Apc(Min/+) mouse. Infect Immun76:2758–2766 [CrossRef][PubMed]
    [Google Scholar]
  35. Patnaik A. K., Liu S. K., Johnson G. F.. 1976; Feline intestinal adenocarcinoma. A clinicopathologic study of 22 cases. Vet Pathol13:1–10[PubMed]
    [Google Scholar]
  36. Patterson M. M., Rogers A. B., Fox J. G.. 2010; Experimental Helicobacter marmotae infection in A/J mice causes enterohepatic disease. J Med Microbiol59:1235–1241 [CrossRef][PubMed]
    [Google Scholar]
  37. Prag J., Blom J., Krogfelt K. A.. 2007; Helicobacter canis bacteraemia in a 7-month-old child. FEMS Immunol Med Microbiol50:264–267 [CrossRef][PubMed]
    [Google Scholar]
  38. Rissetto K., Villamil J. A., Selting K. A., Tyler J., Henry C. J.. 2011; Recent trends in feline intestinal neoplasia: an epidemiologic study of 1,129 cases in the veterinary medical database from 1964 to 2004. J Am Anim Hosp Assoc47:28–36 [CrossRef][PubMed]
    [Google Scholar]
  39. Rossi M., Hänninen M. L., Revez J., Hannula M., Zanoni R. G.. 2008; Occurrence and species level diagnostics of Campylobacter spp., enteric Helicobacter spp. and Anaerobiospirillum spp. in healthy and diarrheic dogs and cats. Vet Microbiol129:304–314 [CrossRef][PubMed]
    [Google Scholar]
  40. Saunders K. E., Shen Z., Dewhirst F. E., Paster B. J., Dangler C. A., Fox J. G.. 1999; Novel intestinal Helicobacter species isolated from cotton-top tamarins (Saguinus oedipus) with chronic colitis. J Clin Microbiol37:146–151[PubMed]
    [Google Scholar]
  41. Shen Z., Feng Y., Dewhirst F. E., Fox J. G.. 2001; Coinfection of enteric Helicobacter spp. and Campylobacter spp. in cats. J Clin Microbiol39:2166–2172 [CrossRef][PubMed]
    [Google Scholar]
  42. Shen Z., Feng Y., Rogers A. B., Rickman B., Whary M. T., Xu S., Clapp K. M., Boutin S. R., Fox J. G.. 2009; Cytolethal distending toxin promotes Helicobacter cinaedi-associated typhlocolitis in interleukin-10-deficient mice. Infect Immun77:2508–2516 [CrossRef][PubMed]
    [Google Scholar]
  43. Shen Z., Sheh A., Young S. K., Abouelliel A., Ward D. V., Earl A. M., Fox J. G.. 2014; Draft genome sequences of six enterohepatic Helicobacter species isolated from humans and one from rhesus macaques. Genome Announc2:e00857-14 [CrossRef][PubMed]
    [Google Scholar]
  44. Stanley J., Linton D., Burnens A. P., Dewhirst F. E., Owen R. J., Porter A., On S. L., Costas M.. 1993; Helicobacter canis sp. nov., a new species from dogs: an integrated study of phenotype and genotype. J Gen Microbiol139:2495–2504 [CrossRef][PubMed]
    [Google Scholar]
  45. Tankovic J., Smati M., Lamarque D., Delchier J. C.. 2011; First detection of Helicobacter canis in chronic duodenal ulcerations from a patient with Crohn's disease. Inflamm Bowel Dis17:1830–1831 [CrossRef][PubMed]
    [Google Scholar]
  46. Turk M. A., Gallina A. M., Russell T. S.. 1981; Nonhematopoietic gastrointestinal neoplasia in cats: a retrospective study of 44 cases. Vet Pathol18:614–620[PubMed][CrossRef]
    [Google Scholar]
  47. Whary M. T., Fox J. G.. 2004; Natural and experimental Helicobacter infections. Comp Med54:128–158[PubMed]
    [Google Scholar]
  48. Young V. B., Knox K. A., Pratt J. S., Cortez J. S., Mansfield L. S., Rogers A. B., Fox J. G., Schauer D. B.. 2004; In vitro and in vivo characterization of Helicobacter hepaticus cytolethal distending toxin mutants. Infect Immun72:2521–2527 [CrossRef][PubMed]
    [Google Scholar]
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