1887

Abstract

( type 1) commonly infects nonhuman primates but its clinical importance is in question.

To characterize infection in a colony of rhesus macaques () used in cognitive neuroscience research.

Inquiries into the nature of in nonhuman primates are required to further define the organism’s virulence and the experimental animal’s gastric microbiome.

Animals with and without clinical signs of vomiting and abdominal pain (=5 and =16, respectively) were evaluated by histology, culture, PCR amplification and sequencing, fluorescent hybridization (FISH) and serology. Three of the five animals with clinical signs, an index case and two others, were evaluated before and after antimicrobial therapy.

The index animal had endoscopically visible ulcers and multifocal, moderate, chronic lymphoplasmacytic gastritis with intraglandular and luminal spiral bacteria. Antimicrobial therapy in the index animal achieved histologic improvement, elimination of endoscopically visible ulcers, and evident eradication but clinical signs persisted. In the other treated animals, gastritis scores were not consistently altered, gastric bacteria persisted, but vomiting and abdominal discomfort abated.

Nineteen of 21 animals were PCR positive for and five animals were also PCR positive for . Organisms were detected by FISH in 17 of 21 animals: 16S rRNA sequences of two of these were shown to be . Mild to moderate lymphoplasmacytic gastritis was seen in antrum, body and cardia, with antral gastritis more likely to be moderate than that of the body.

No clear association between the bacterial numbers of spp. and the degree of inflammation was observed. is prevalent in this colony of but its clinical importance remains unclear. This study corroborates many of the findings in earlier studies of infection in macaques but also identifies at least one animal in which gastritis and endoscopically visible gastric ulcers were strongly associated with infection. In this study, serology was an inadequate biomarker for endoscopic evaluation in diagnosis of infection.

Keyword(s): gastritis , helicobacter and macaque
Funding
This study was supported by the:
  • National Institutes of Health (Award P30 ES02109)
    • Principle Award Recipient: JamesG Fox
  • National Institutes of Health (Award P01 CA028842-29)
    • Principle Award Recipient: JamesG Fox
  • National Institutes of Health (Award T32 OD010978-27)
    • Principle Award Recipient: JamesG Fox
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/content/journal/jmm/10.1099/jmm.0.001315
2021-01-21
2021-10-25
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References

  1. Handt LK, Fox JG, Yan LL, Shen Z, Pouch WJ et al. Diagnosis of Helicobacter pylori infection in a colony of rhesus monkeys (Macaca mulatta). J Clin Microbiol 1997; 35:165–168 [View Article][PubMed]
    [Google Scholar]
  2. Reindel JF, Fitzgerald AL, Breider MA, Gough AW, Yan C et al. An epizootic of lymphoplasmacytic gastritis attributed to Helicobacter pylori infection in cynomolgus monkeys (Macaca fascicularis). Vet Pathol 1999; 36:1–13 [View Article][PubMed]
    [Google Scholar]
  3. Dubois A, Fiala N, Heman-Ackah LM, Drazek ES, Tarnawski A et al. Natural gastric infection with Helicobacter pylori in monkeys: a model for spiral bacteria infection in humans. Gastroenterology 1994; 106:1405–1417 [View Article][PubMed]
    [Google Scholar]
  4. Suerbaum S, Kraft C, Dewhirst FE, Fox JG. Helicobacter nemestrinae ATCC 49396T is a strain of Helicobacter pylori (Marshall et al. 1985) Goodwin et al. 1989, and Helicobacter nemestrinae (Bronsdon et al. 1991) is therefore a junior heterotypic synonym of Helicobacter pylori . Int J Syst Evol Microbiol 2002; 52:437–439 [View Article][PubMed]
    [Google Scholar]
  5. Kasai K, Kobayashi R. The stomach spirochete occurring in mammals. J Parasitol 1919; 6:1–10 [View Article]
    [Google Scholar]
  6. Doenges JL. Spirochetes in gastric glands of Macacus rhesus and humans without definite history of related disease. Exp Biol Med 1938; 38:536–538 [View Article]
    [Google Scholar]
  7. Flahou B, Haesebrouck F, Pasmans F, D'Herde K, Driessen A et al. Helicobacter suis causes severe gastric pathology in mouse and Mongolian gerbil models of human gastric disease. PLoS One 2010; 5:e14083 [View Article][PubMed]
    [Google Scholar]
  8. Blaecher C, Bauwens E, Tay A, Peters F, Dobbs S et al. A novel isolation protocol and probe-based RT-PCR for diagnosis of gastric infections with the zoonotic pathogen Helicobacter suis . Helicobacter 2017; 22:e12369 [View Article][PubMed]
    [Google Scholar]
  9. Berlamont H, Smet A, De Bruykere S, Boyen F, Ducatelle R et al. Antimicrobial susceptibility pattern of Helicobacter suis isolates from pigs and macaques. Vet Microbiol 2019; 239:108459 [View Article][PubMed]
    [Google Scholar]
  10. Martin ME, Bhatnagar S, George MD, Paster BJ, Canfield DR et al. The impact of Helicobacter pylori infection on the gastric microbiota of the rhesus macaque. PLoS One 2013; 8:e76375 [View Article][PubMed]
    [Google Scholar]
  11. Esmail MY, Bacon R, Swennes AG, Feng Y, Shen Z et al. Helicobacter species identified in captive sooty Mangabeys (Cercocebus atys) with metastatic gastric adenocarcinoma. Helicobacter 2016; 21:175–185 [View Article][PubMed]
    [Google Scholar]
  12. Haesebrouck F, Pasmans F, Flahou B, Chiers K, Baele M et al. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin Microbiol Rev 2009; 22:202–223 [View Article][PubMed]
    [Google Scholar]
  13. Baele M, Decostere A, Vandamme P, Ceelen L, Hellemans A et al. Isolation and characterization of Helicobacter suis sp. nov. from pig stomachs. Int J Syst Evol Microbiol 2008; 58:1350–1358 [View Article][PubMed]
    [Google Scholar]
  14. Smet A, Flahou B, D'Herde K, Vandamme P, Cleenwerck I et al. Helicobacter heilmannii sp. nov., isolated from feline gastric mucosa. Int J Syst Evol Microbiol 2012; 62:299–306 [View Article][PubMed]
    [Google Scholar]
  15. Joosten M, Linden S, Rossi M, Tay CY, Skoog E et al. Divergence between the highly virulent zoonotic pathogen Helicobacter heilmannii and its closest relative, the low virulent Helicobacter ailurogastricussp. nov. Infect Immun 2015; 84:293–306 [View Article][PubMed]
    [Google Scholar]
  16. Haesebrouck F, Pasmans F, Flahou B, Smet A, Vandamme P et al. Non-Helicobacter pylori Helicobacter species in the human gastric mucosa: a proposal to introduce the terms H. heilmannii sensu lato and sensu stricto. Helicobacter 2011; 16:339–340 [View Article][PubMed]
    [Google Scholar]
  17. De Cooman L, Flahou B, Houf K, Smet A, Ducatelle R et al. Survival of Helicobacter suis bacteria in retail pig meat. Int J Food Microbiol 2013; 166:164–167 [View Article][PubMed]
    [Google Scholar]
  18. De Cooman L, Houf K, Smet A, Flahou B, Ducatelle R et al. Presence of Helicobacter suis on pork carcasses. Int J Food Microbiol 2014; 187:73–76 [View Article][PubMed]
    [Google Scholar]
  19. Flahou B, Rossi M, Bakker J, Langermans JA, Heuvelman E et al. Evidence for a primate origin of zoonotic Helicobacter suis colonizing domesticated pigs. ISME J 2018; 12:77–86 [View Article][PubMed]
    [Google Scholar]
  20. Perkins SE, Fox JG, Marini RP, Shen Z, Dangler CA et al. Experimental infection in cats with a cagA+ human isolate of Helicobacter pylori . Helicobacter 1998; 3:225–235 [View Article][PubMed]
    [Google Scholar]
  21. Joosten M, Flahou B, Meyns T, Smet A, Arts J et al. Case report: Helicobacter suis infection in a pig veterinarian. Helicobacter 2013; 18:392–396 [View Article][PubMed]
    [Google Scholar]
  22. Fox JG, Dewhirst FE, Shen Z, Feng Y, Taylor NS et al. Hepatic Helicobacter species identified in bile and gallbladder tissue from Chileans with chronic cholecystitis. Gastroenterology 1998; 114:755–763 [View Article][PubMed]
    [Google Scholar]
  23. Bickley J, Owen RJ, Fraser AG, Pounder RE. Evaluation of the polymerase chain reaction for detecting the urease C gene of Helicobacter pylori in gastric biopsy samples and dental plaque. J Med Microbiol 1993; 39:338–344 [View Article][PubMed]
    [Google Scholar]
  24. Dewhirst FE, Chien CC, Paster BJ, Ericson RL, Orcutt RP et al. Phylogeny of the defined murine microbiota: altered Schaedler flora . Appl Environ Microbiol 1999; 65:3287–3292 [View Article][PubMed]
    [Google Scholar]
  25. Shen Z, Xu S, Dewhirst FE, Paster BJ, Pena JA et al. A novel enterohepatic Helicobacter species 'Helicobacter mastomyrinus' isolated from the liver and intestine of rodents. Helicobacter 2005; 10:59–70 [View Article][PubMed]
    [Google Scholar]
  26. Bridgeford EC, Marini RP, Feng Y, Parry NM, Rickman B et al. Gastric helicobacter species as a cause of feline gastric lymphoma: a viable hypothesis. Vet Immunol Immunopathol 2008; 123:106–113 [View Article][PubMed]
    [Google Scholar]
  27. Trebesius K, Adler K, Vieth M, Stolte M, Haas R. Specific detection and prevalence of Helicobacter heilmannii-like organisms in the human gastric mucosa by fluorescent in situ hybridization and partial 16S ribosomal DNA sequencing. J Clin Microbiol 2001; 39:1510–1516 [View Article][PubMed]
    [Google Scholar]
  28. Chan V, Crocetti G, Grehan M, Zhang L, Danon S et al. Visualization of Helicobacter species within the murine cecal mucosa using specific fluorescence in situ hybridization. Helicobacter 2005; 10:114–124 [View Article][PubMed]
    [Google Scholar]
  29. Whary MT, Morgan TJ, Dangler CA, Gaudes KJ, Taylor NS et al. Chronic active hepatitis induced by Helicobacter hepaticus in the A/JCr mouse is associated with a Th1 cell-mediated immune response. Infect Immun 1998; 66:3142–3148 [View Article][PubMed]
    [Google Scholar]
  30. Dubois A, Tarnawski A, Newell DG, Fiala N, Dabros W et al. Gastric injury and invasion of parietal cells by spiral bacteria in rhesus monkeys. Gastroenterology 1991; 100:884–891 [View Article]
    [Google Scholar]
  31. Sato T, Takeuchi A. Infection by spirilla in the stomach of the rhesus monkey. Vet Pathol Suppl 1982; 7:17–25 [View Article][PubMed]
    [Google Scholar]
  32. Bosschem I, Flahou B, Bakker J, Heuvelman E, Langermans JA et al. Comparative virulence of in vitro -cultured primate- and pig-associated Helicobacter suis strains in a BALB/c mouse and a Mongolian gerbil model. Helicobacter 2017; 22:e12349 [View Article]
    [Google Scholar]
  33. Rogers AB, Fox JG. Inflammation and cancer. I. rodent models of infectious gastrointestinal and liver cancer. Am J Physiol Gastrointest Liver Physiol 2004; 286:G361–G366 [View Article][PubMed]
    [Google Scholar]
  34. Poh AR, O'Donoghue RJ, Ernst M, Putoczki TL. Mouse models for gastric cancer: matching models to biological questions. J Gastroenterol Hepatol 2016; 31:1257–1272 [View Article][PubMed]
    [Google Scholar]
  35. Boonjakuakul JK, Canfield DR, Solnick JV. Comparison of Helicobacter pylori virulence gene expression in vitro and in the rhesus macaque. Infect Immun 2005; 73:4895–4904 [View Article][PubMed]
    [Google Scholar]
  36. Skoog EC, Deck SL, Entwistle HD, Hansen LM, Solnick JV. Characterization of the CAG pathogenicity island in Helicobacter pylori from naturally infected rhesus macaques. FEMS Microbiol Lett 2016; 363:fnw275 [View Article][PubMed]
    [Google Scholar]
  37. Marini RP, Muthupalani S, Shen Z, Buckley EM, Alvarado C et al. Persistent infection of rhesus monkeys with 'Helicobacter macacae' and its isolation from an animal with intestinal adenocarcinoma. J Med Microbiol 2010; 59:961–969 [View Article][PubMed]
    [Google Scholar]
  38. Lertpiriyapong K, Handt L, Feng Y, Mitchell TW, Lodge KE et al. Pathogenic properties of enterohepatic Helicobacter spp. isolated from rhesus macaques with intestinal adenocarcinoma. J Med Microbiol 2014; 63:1004–1016 [View Article][PubMed]
    [Google Scholar]
  39. Fox JG, Handt L, Sheppard BJ, Xu S, Dewhirst FE et al. Isolation of Helicobacter cinaedi from the colon, liver, and mesenteric lymph node of a rhesus monkey with chronic colitis and hepatitis. J Clin Microbiol 2001; 39:1580–1585 [View Article][PubMed]
    [Google Scholar]
  40. Fox JG, Handt L, Xu S, Shen Z, Dewhirst FE et al. Novel Helicobacter species isolated from rhesus monkeys with chronic idiopathic colitis. J Med Microbiol 2001; 50:421–429 [View Article][PubMed]
    [Google Scholar]
  41. Hoang TT, Wheeldon TU, Bengtsson C, Phung DC, Sorberg M et al. Enzyme-linked immunosorbent assay for Helicobacter pylori needs adjustment for the population investigated. J Clin Microbiol 2004; 42:627–630 [View Article][PubMed]
    [Google Scholar]
  42. Bergin IL, Chien CC, Marini RP, Fox JG. Isolation and characterization of Corynebacterium ulcerans from cephalic implants in macaques. Comp Med 2000; 50:530–535[PubMed]
    [Google Scholar]
  43. Frydman GH, Marini RP, Bakthavatchalu V, Biddle KE, Muthupalani S et al. Local and systemic changes associated with long-term, percutaneous, static implantation of titanium alloys in Rhesus macaques (Macaca mulatta). Comp Med 2017; 67:165–175[PubMed]
    [Google Scholar]
  44. Mégraud F, Lehours P, Vale FF. The history of Helicobacter pylori: from phylogeography to paleomicrobiology. Clin Microbiol Infect 2016; 22:922–927 [View Article][PubMed]
    [Google Scholar]
  45. Smet A, Yahara K, Rossi M, Tay A, Backert S et al. Macroevolution of gastric Helicobacter species unveils interspecies admixture and time of divergence. ISME J 2018; 12:2518–2531 [View Article][PubMed]
    [Google Scholar]
  46. Liu H, Merrell DS, Semino-Mora C, Goldman M, Rahman A et al. Diet synergistically affects Helicobacter pylori-induced gastric carcinogenesis in nonhuman primates. Gastroenterology 2009; 137:1367–1379 [View Article][PubMed]
    [Google Scholar]
  47. Murakami K, Fujioka T, Kodama M, Honda S, Okimoto T et al. Analysis of p53 mutations and Helicobacter pylori infection in human and animal models. J Gastroenterol 2002; 37 Suppl 13:1–5 [View Article][PubMed]
    [Google Scholar]
  48. Dieterich C, Wiesel P, Neiger R, Blum A, Corthésy-Theulaz I. Presence of multiple "Helicobacter heilmannii" strains in an individual suffering from ulcers and in his two cats. J Clin Microbiol 1998; 36:1366–1370 [View Article][PubMed]
    [Google Scholar]
  49. Goddard AF, Logan RP, Atherton JC, Jenkins D, Spiller RC. Healing of duodenal ulcer after eradication of Helicobacter heilmannii . Lancet 1997; 349:1815–1816 [View Article][PubMed]
    [Google Scholar]
  50. Heilmann KL, Borchard F. Gastritis due to spiral shaped bacteria other than Helicobacter pylori: clinical, histological, and ultrastructural findings. Gut 1991; 32:137–140 [View Article][PubMed]
    [Google Scholar]
  51. Solnick JV. Clinical significance of Helicobacter species other than Helicobacter pylori . Clin Infect Dis 2003; 36:349–354 [View Article][PubMed]
    [Google Scholar]
  52. Jalava K, On SL, Harrington CS, Andersen LP, Hänninen ML et al. A cultured strain of "Helicobacter heilmannii," a human gastric pathogen, identified as H. bizzozeronii: evidence for zoonotic potential of Helicobacter . Emerg Infect Dis 2001; 7:1036–1038 [View Article][PubMed]
    [Google Scholar]
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