1887

Abstract

A novel helicobacter, ‘’, was previously isolated from a colony of rhesus and cynomolgus monkeys in which diarrhoea from chronic idiopathic colitis was enzootic. A survey performed in a second colony of rhesus monkeys without a history of chronic diarrhoea determined that 57 % were faecal-culture positive for species. Ten years after the survey, one of the animals from which ‘’ had been isolated, a 23-year-old, intact male rhesus monkey (), presented with partial inappetence and progressive weight loss. Subsequent evaluation of the monkey revealed anaemia, hypoproteinaemia, hypoalbuminaemia and a palpable abdominal mass. Contrast radiography suggested partial intestinal obstruction. The animal was euthanized and a diagnosis was made of intestinal adenocarcinoma of the ileocaecocolic junction with metastasis to regional lymph nodes and liver. Microaerobic culture of caecal tissue yielded a helicobacter organism identified as ‘’ by 16S rRNA gene sequencing – the same species of bacteria isolated 10 years previously. The liver, small intestine and colon were also positive by PCR for species. Intestinal adenocarcinoma is the most common malignancy of aged macaques. Faeces or caecal tissue from five out of five monkeys that remained from the original cohort and that were colonized with ‘’ in the initial survey were positive for the organism. The apparent persistence of ‘’ in these animals, the isolation of the bacterium from animals with colitis and the recognition of the importance of inflammation in carcinogenesis raise the possibility of an aetiological role in the genesis of intestinal adenocarcinoma in aged rhesus monkeys.

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2010-08-01
2024-04-18
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References

  1. Berg R. D. 1995; Bacterial translocation from the gastrointestinal tract. Trends Microbiol 3:149–154 [CrossRef]
    [Google Scholar]
  2. Boivin G. P., Washington K., Yang K., Ward J. M., Pretlow T. P., Russell R., Besselsen D. G., Godfrey V. L., Doetschman T. other authors 2003; Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 124:762–777 [CrossRef]
    [Google Scholar]
  3. Cahill R. J., Foltz C. J., Fox J. G., Dangler C. A., Powrie F., Schauer D. B. 1997; Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus . Infect Immun 65:3126–3131
    [Google Scholar]
  4. Erdman S. E., Poutahidis T., Tomczak M., Rogers A. B., Cormier K., Plank B., Horwitz B. H., Fox J. G. 2003; CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 162:691–702 [CrossRef]
    [Google Scholar]
  5. 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. other authors 2009; Nitric oxide and TNF- α trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus -infected, Rag2-deficient mice. Proc Natl Acad Sci U S A 106:1027–1032 [CrossRef]
    [Google Scholar]
  6. Feagins L. A., Souza R. F., Spechler S. J. 2009; Carcinogenesis in IBD: potential targets for the prevention of colorectal cancer. Nat Rev Gastroenterol Hepatol 6:297–305 [CrossRef]
    [Google Scholar]
  7. Flores B. M., Fennell C. L., Kuller L., Bronsdon M. A., Morton W. R., Stamm W. E. 1990; Experimental infection of pig-tailed macaques ( Macaca nemestrina ) with Campylobacter cinaedi and Campylobacter fennelliae . Infect Immun 58:3947–3953
    [Google Scholar]
  8. Fox J. G., Wang T. C. 2007; Inflammation, atrophy, and gastric cancer. J Clin Invest 117:60–69 [CrossRef]
    [Google Scholar]
  9. Fox J. G., Dewhirst F. E., Tully J. G., Paster B. J., Yan L., Taylor N. S., Collins M. J. Jr, Gorelick P. L., Ward J. M. 1994; Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol 32:1238–1245
    [Google Scholar]
  10. Fox J. G., Li X., Yan L., Cahill R. J., Hurley R., Lewis R., Murphy J. C. 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
    [Google Scholar]
  11. Fox J. G., Handt L., Sheppard B. J., Xu S., Dewhirst F. E., Motzel S., Klein H. 2001a; 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 [CrossRef]
    [Google Scholar]
  12. Fox J. G., Handt L., Xu S., Shen Z., Dewhirst F. E., Paster B. J., Dangler C. A., Lodge K., Motzel S., Klein H. 2001b; Novel Helicobacter species isolated from rhesus monkeys with chronic idiopathic colitis. J Med Microbiol 50:421–429
    [Google Scholar]
  13. 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. other authors 2007; Isolation and characterization of a novel helicobacter species, “ Helicobacter macacae ”, from rhesus monkeys with and without chronic idiopathic colitis. J Clin Microbiol 45:4061–4063 [CrossRef]
    [Google Scholar]
  14. García A., Xu S., Dewhirst F. E., Nambiar P. R., Fox J. G. 2006; Enterohepatic Helicobacter species isolated from the ileum, liver and colon of a baboon with pancreatic islet amyloidosis. J Med Microbiol 55:1591–1595 [CrossRef]
    [Google Scholar]
  15. García Rodríguez L. A., Ruigómez A., Panés J. 2006; Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 130:1588–1594 [CrossRef]
    [Google Scholar]
  16. Ge Z., Schauer D. B., Fox J. G. 2008; In vivo virulence properties of bacterial cytolethal-distending toxin. Cell Microbiol 10:1599–1607 [CrossRef]
    [Google Scholar]
  17. Gout S., Huot J. 2008; Role of cancer microenvironment in metastasis: focus on colon cancer. Cancer Microenviron 1:69–83 [CrossRef]
    [Google Scholar]
  18. Gradel K. O., Nielsen H. L., Schonheyder H. C., Ejlertsen T., Kristensen B., Nielsen H. 2009; Increased short- and long-term risk of inflammatory bowel disease after Salmonella or Campylobacter gastroenteritis. Gastroenterology 137:495–501 [CrossRef]
    [Google Scholar]
  19. Haggerty T. D., Perry S., Sanchez L., Perez-Perez G., Parsonnet J. 2005; Significance of transiently positive enzyme-linked immunosorbent assay results in detection of Helicobacter pylori in stool samples from children. J Clin Microbiol 43:2220–2223 [CrossRef]
    [Google Scholar]
  20. Hussain S. P., Harris C. C. 2007; Inflammation and cancer: an ancient link with novel potentials. Int J Cancer 121:2373–2380 [CrossRef]
    [Google Scholar]
  21. Ihrig M., Schrenzel M. D., Fox J. G. 1999; Differential susceptibility to hepatic inflammation and proliferation in AXB recombinant inbred mice chronically infected with Helicobacter hepaticus . Am J Pathol 155:571–582 [CrossRef]
    [Google Scholar]
  22. 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 Res 66:828–838 [CrossRef]
    [Google Scholar]
  23. Maggio-Price L., Treuting P., Bielefeldt-Ohmann H., Seamons A., Drivdahl R., Zeng W., Lai L., Huycke M., Phelps S. other authors 2009; Bacterial infection of Smad3/Rag2 double-null mice with transforming growth factor- β dysregulation as a model for studying inflammation-associated colon cancer. Am J Pathol 174:317–329 [CrossRef]
    [Google Scholar]
  24. McKenna P., Hoffmann C., Minkah N., Aye P. P., Lackner A., Liu Z., Lozupone C. A., Hamady M., Knight R., Bushman F. D. 2008; The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 4:e20 [CrossRef]
    [Google Scholar]
  25. Porter C. K., Tribble D. R., Aliaga P. A., Halvorson H. A., Riddle M. S. 2008; Infectious gastroenteritis and risk of developing inflammatory bowel disease. Gastroenterology 135:781–786 [CrossRef]
    [Google Scholar]
  26. Poutahidis T., Haigis K. M., Rao V. P., Nambiar P. R., Taylor C. L., Ge Z., Watanabe K., Davidson A., Horwitz B. H. other authors 2007; Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma. Carcinogenesis 28:2614–2623 [CrossRef]
    [Google Scholar]
  27. Rodriguez N. A., Garcia K. D., Fortman J. D., Hewett T. A., Bunte R. M., Bennett B. T. 2002; Clinical and histopathological evaluation of 13 cases of adenocarcinoma in aged rhesus macaques ( Macaca mulatta . J Med Primatol 31:74–83 [CrossRef]
    [Google Scholar]
  28. Rogers A. B., Fox J. G. 2004; Inflammation and cancer. I. Rodent models of infectious gastrointestinal and liver cancer. Am J Physiol Gastrointest Liver Physiol 286:G361–G366 [CrossRef]
    [Google Scholar]
  29. 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 Microbiol 37:146–151
    [Google Scholar]
  30. Uno H., Alsum P., Zimbric M. L., Houser W. D., Thomson J. A., Kemnitz J. W. 1998; Colon cancer in aged captive rhesus monkeys ( Macaca mulatta ). Am J Primatol 44:19–27 [CrossRef]
    [Google Scholar]
  31. Valverde C. R., Tarara R. P., Griffey S. M., Roberts J. A. 2000; Spontaneous intestinal adenocarcinoma in geriatric macaques ( Macaca sp.). Comp Med 50:540–544
    [Google Scholar]
  32. Whary M. T., Fox J. G. 2004; Natural and experimental Helicobacter infections. Comp Med 54:128–158
    [Google Scholar]
  33. Zeller J., Takeuchi A. 1982; Infection of the colon of the rhesus monkey by spiral-shaped organisms. Vet Pathol Suppl 7:26–32
    [Google Scholar]
  34. Zhang L., Man S. M., Day A. S., Leach S. T., Lemberg D. A., Dutt S., Stormon M., Otley A., O'Loughlin E. V. other authors 2009; Detection and isolation of Campylobacter species other than C. jejuni from children with Crohn's disease. J Clin Microbiol 47:453–455 [CrossRef]
    [Google Scholar]
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