A new cultivation method was successfully applied for the isolation of a hitherto uncultured spiral species associated with ulceration of the non-glandular stomach and gastritis in pigs and formerly described as ‘ Helicobacter suis’. Three isolates, HS1, HS2 and HS3, were subcultured from the stomach mucosa of three pigs after slaughter and were analysed using a polyphasic taxonomic approach. The novel isolates grew on biphasic culture plates or very moist agar bases in microaerobic conditions and exhibited urease, oxidase and catalase activities. Sequencing of the 16S rRNA gene, the 23S rRNA gene, the partial gene and partial genes confirmed that the strains present in the gastric mucosa of pigs constituted a separate taxon, corresponding to ‘’ type 1 strains as detected in the gastric mucosa of humans and other primates. For all genes sequenced, the highest sequence similarities were obtained with and , species isolated from the gastric mucosa of dogs and cats, which have also been detected in the human gastric mucosa and which are commonly referred to as ‘’ type 2. SDS-PAGE of whole-cell proteins of strains HS1, HS2 and HS3 differentiated them from other species of gastric origin. The results of the polyphasic taxonomic analysis confirmed that the novel isolates constitute a novel taxon corresponding to ‘’ type 1 strains from humans and to ‘ H. suis’ from pigs. The name sp. nov. is proposed for the novel isolates with the type strain HS1 (=LMG 23995=DSM 19735).


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  1. Ayles, H. L., Friendship, R. M. & Ball, R. O.(1996). Effect of dietary particle size on gastric ulcers, assessed by endoscopic examination, and relationship between ulcer severity and growth performance of individually fed pigs. Swine Health Prod 4, 211–216. [Google Scholar]
  2. Baele, M., Devriese, L. A. & Haesebrouck, F.(2001).Lactobacillus agilis is an important component of the pigeon crop flora. J Appl Microbiol 91, 488–491.[CrossRef] [Google Scholar]
  3. Baele, M., Van den Bulck, K., Decostere, A., Vandamme, P., Hanninen, M. L., Ducatelle, R. & Haesebrouck, F.(2004). Multiplex PCR assay for differentiation of Helicobacter felis, H. bizzozeronii, and H. salomonis. J Clin Microbiol 42, 1115–1122.[CrossRef] [Google Scholar]
  4. Baele, M., Haesebrouck, F., Vandamme, P., Van den Bulck, K., Gruntar, I., Mehle, J., Mast, J., Ducatelle, R. & Decostere, A.(2008).Helicobacter baculiformis sp. nov. isolated from feline stomach mucosa. Int J Syst Evol Microbiol 58, 357–364.[CrossRef] [Google Scholar]
  5. Barbosa, A. J. A., Silva, J. C. P., Nogueira, A. M. M. F., Paulino, E. & Miranda, C. R.(1995). Higher incidence of Gastrospirillum sp. in swine with gastric ulcer of the pars oesophagea. Vet Pathol 32, 134–139.[CrossRef] [Google Scholar]
  6. Cantet, F., Magras, C., Marais, A., Federighi, M. & Mégraud, F.(1999).Helicobacter species colonizing the pig stomach: molecular characterization and determination of prevalence. Appl Environ Microbiol 65, 4672–4676. [Google Scholar]
  7. Ceelen, L. M., Decostere, A., Van den Bulck, K., On, S. L., Baele, M., Ducatelle, R. & Haesebrouck, F.(2006).Helicobacter pullorum in chickens, Belgium. Emerg Infect Dis 12, 263–267.[CrossRef] [Google Scholar]
  8. Choi, Y. K., Han, J. H. & Joo, H. S.(2001). Identification of novel Helicobacter species in pig stomachs by PCR and partial sequencing. J Clin Microbiol 39, 3311–3315.[CrossRef] [Google Scholar]
  9. Coenye, T., Falsen, E., Vancanneyt, M., Hoste, B., Govan, J. R. W., Kersters, K. & Vandamme, P.(1999). Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol 49, 405–413.[CrossRef] [Google Scholar]
  10. De Groote, D., van Doorn, L.-J., Ducatelle, R., Verschuuren, A., Haesebrouck, F., Quint, W. G. V., Jalava, K. & Vandamme, P.(1999).Candidatus Helicobacter suis’, a gastric helicobacter from pigs, and its phylogenetic relatedness to other gastrospirilla. Int J Syst Bacteriol 49, 1769–1777.[CrossRef] [Google Scholar]
  11. De Groote, D., Ducatelle, R., van Doorn, L.-J., Tilmant, K., Verschuuren, A. & Haesebrouck, F.(2000). Detection of “Candidatus Helicobacter suis” in gastric samples of pigs by PCR: comparison with other invasive diagnostic techniques. J Clin Microbiol 38, 1131–1135. [Google Scholar]
  12. De Groote, D., Van Doorn, L. J., Van den Bulck, K., Vandamme, P., Vieth, M., Stolte, M., Debongnie, J. C., Burette, A., Haesebrouck, F. & Ducatelle, R.(2005). Detection of non-pylori Helicobacter species in “Helicobacter heilmannii”-infected humans. Helicobacter 10, 398–406.[CrossRef] [Google Scholar]
  13. Dewhirst, F. E., Fox, J. G. & On, S. L. W.(2000). Recommended minimal standards for describing new species of the genus Helicobacter. Int J Syst Evol Microbiol 50, 2231–2237.[CrossRef] [Google Scholar]
  14. Dewhirst, F. E., Shen, Z. L., Scimeca, M. S., Stokes, L. N., Boumenna, T., Chen, T. T., Paster, B. J. & Fox, J. G.(2005). Discordant 16S and 23S rRNA gene phylogenies for the genus Helicobacter: Implications for phylogenetic inference and systematics. J Bacteriol 187, 6106–6118.[CrossRef] [Google Scholar]
  15. Goddard, A. F., Logan, R. P. H., Atherton, J. C., Jenkins, D. & Spiller, R.(1997). Healing of duodenal ulcer after eradication of Helicobacter heilmannii. Lancet 349, 1815–1816. [Google Scholar]
  16. Grasso, G. M., Ripabelli, G., Sammarco, M. L., Ruberto, A. & Iannitto, G.(1996). Prevalence of Helicobacter-like organisms in porcine gastric mucosa: a study of swine slaughtered in Italy. Comp Immunol Microbiol Infect Dis 19, 213–217.[CrossRef] [Google Scholar]
  17. Gruntar, I., Mehle, J., Krt, B., Ocepek, M., Gombac, M., Cerne, M. & Pogacnik, M.(2003). New approaches in isolation of Helicobacter spp. from gastric mucosa in dogs. Int J Med Microbiol 293 (Suppl.), 65 [Google Scholar]
  18. Hänninen, M. L., Happonen, I., Saari, S. & Jalava, K.(1996). Culture and characteristics of Helicobacter bizzozeronii, a new canine gastric Helicobacter sp. Int J Syst Bacteriol 46, 160–166.[CrossRef] [Google Scholar]
  19. Hellemans, A., Decostere, A., Haesebrouck, F. & Ducatelle, R.(2005). Evaluation of antibiotic treatment for eradication of “Candidatus Helicobacter suis” in a mouse model. Antimicrob Agents Chemother 49, 4530–4535.[CrossRef] [Google Scholar]
  20. Hellemans, A., Decostere, A., Duchateau, L., De Bock, M., Haesebrouck, F. & Ducatelle, R.(2006). Protective immunization against “Candidatus Helicobacter suis” with heterologous antigens of H. pylori and H. felis. Vaccine 24, 2469–2476.[CrossRef] [Google Scholar]
  21. Hellemans, A., Chiers, K., Decostere, A., De Bock, M., Haesebrouck, F. & Ducatelle, R.(2007). Experimental infection of pigs with “Candidatus Helicobacter suis”. Vet Res Commun 31, 385–395. [Google Scholar]
  22. Houf, K., On, S. L. W., Coenye, T., Mast, J., Van Hoof, J. & Vandamme, P.(2005).Arcobacter cibarius sp nov., isolated from broiler carcasses. Int J Syst Evol Microbiol 55, 713–717.[CrossRef] [Google Scholar]
  23. Jalava, K., Kaartinen, M., Utriainen, M., Happonen, I. & Hanninen, M. L.(1997).Helicobacter salomonis sp. nov., a canine gastric Helicobacter sp. related to Helicobacter felis and Helicobacter bizzozeronii. Int J Syst Bacteriol 47, 975–982.[CrossRef] [Google Scholar]
  24. Jalava, K., On, S. L. W., Vandamme, P. A. R., Happonen, I., Sukura, A. & Hanninen, M. L.(1998). Isolation and identification of Helicobacter spp, from canine and feline gastric mucosa. Appl Environ Microbiol 64, 3998–4006. [Google Scholar]
  25. Jalava, K., On, S. L. W., Harrington, C. S., Andersen, L. P., Hanninen, M. L. & Vandamme, P.(2001). A cultured strain of “Helicobacter heilmannii,” a human gastric pathogen, identified as H. bizzozeronii: Evidence for zoonotic potential of Helicobacter. Emerg Infect Dis 7, 1036–1038.[CrossRef] [Google Scholar]
  26. Kokotovic, B. & On, S. L. W.(1999). High-resolution genomic fingerprinting of Campylobacter jejuni and Campylobacter coli by analysis of amplified fragment length polymorphisms. FEMS Microbiol Lett 173, 77–84.[CrossRef] [Google Scholar]
  27. Lee, A., Hazell, S. L., O'Rourke, J. & Kouprach, S.(1988). Isolation of a spiral-shaped bacterium from the cat stomach. Infect Immun 56, 2843–2850. [Google Scholar]
  28. Magras, C., Cantet, F., Koffi, G., Pilet, M.-F., Mégraud, F. & Federighi, M.(1999).Helicobacter sp. dans l'estomac des porcs charcutiers: un problème de santé publique? Journ Rech Porcine France 31, 395–399 (in French). [Google Scholar]
  29. Meining, A., Kroher, G. & Stolte, M.(1998). Animal reservoirs in the transmission of Helicobacter heilmannii. Results of a questionnaire-based study. Scand J Gastroenterol 33, 795–798.[CrossRef] [Google Scholar]
  30. Melnichouk, S. L., Friendship, R. M., Dewey, C. E., Bildfell, R. J. & Smart, N. L.(1999).Helicobacter-like organisms in the stomach of pigs with and without gastric ulceration. Swine Health Prod 7, 201–205. [Google Scholar]
  31. Mendes, E. N., Queiroz, D. M., Rocha, G. A., Moura, S. B., Leite, V. H. R. & Fonseca, M. E. F.(1990). Ultrastructure of a spiral micro-organism from pig gastric mucosa (“Gastrospirillum suis”). J Med Microbiol 33, 61–66.[CrossRef] [Google Scholar]
  32. Mendes, E. N., Queiroz, D. M., Rocha, G. A., Nogueira, A. M., Carvalho, A. C., Lage, A. P. & Barbosa, A. J.(1991). Histopathological study of porcine gastric mucosa with and without a spiral bacterium (“Gastrospirillum suis”). J Med Microbiol 35, 345–348.[CrossRef] [Google Scholar]
  33. Mikkonen, T. P., Karenlampi, R. I. & Hänninen, M. L.(2004). Phylogenetic analysis of gastric and enterohepatic Helicobacter species based on partial HSP60 gene sequences. Int J Syst Evol Microbiol 54, 753–758.[CrossRef] [Google Scholar]
  34. Mills, C. K. & Gherna, R. L.(1987). Hydrolysis of indoxyl acetate by Campylobacter species. J Clin Microbiol 25, 1560–1561. [Google Scholar]
  35. Morgner, A., Bayerdorffer, E., Meining, A., Stolte, M. & Kroher, G.(1995).Helicobacter heilmannii and gastric cancer. Lancet 346, 511–512. [Google Scholar]
  36. O'Rourke, J. L., Dixon, M. F., Jack, A., Enno, A. & Lee, A.(2004a).Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of ‘Helicobacter heilmannii’ infection. J Pathol 203, 896–903.[CrossRef] [Google Scholar]
  37. O'Rourke, J. L., Solnick, J. V., Neilan, B. A., Seidel, K., Hayter, R., Hansen, L. M. & Lee, A.(2004b). Description of ‘Candidatus Helicobacter heilmannii’ based on DNA sequence analysis of 16S rRNA and urease genes. Int J Syst Evol Microbiol 54, 2203–2211.[CrossRef] [Google Scholar]
  38. Owen, R. J., Costas, M., Morgan, D. D., On, S. L. W., Hill, L. R., Pearson, A. D. & Morgan, D. R.(1989). Strain variation in Campylobacter pylori detected by numerical analysis of one-dimensional electrophoretic protein patterns. Antonie van Leeuwenhoek 55, 253–267.[CrossRef] [Google Scholar]
  39. Park, J.-H., Lee, B.-J., Lee, Y.-S. & Park, J.-H.(2000). Association of tightly spiraled bacterial infection and gastritis in pigs. J Vet Med Sci 62, 725–729.[CrossRef] [Google Scholar]
  40. Park, J. H., Seok, S. H., Cho, S. A., Baek, M. W., Lee, H. Y., Kim, D. J. & Park, J. H.(2004). The high prevalence of Helicobacter sp. in porcine pyloric mucosa and its histopathological and molecular characteristics. Vet Microbiol 104, 219–225.[CrossRef] [Google Scholar]
  41. Pot, B., Devriese, L. A., Hommez, J., Miry, C., Vandemeulebroecke, K., Kersters, K. & Haesebrouck, F.(1994). Characterization and identification of Vagococcus fluvialis strains isolated from domestic animals. J Appl Bacteriol 77, 362–369.[CrossRef] [Google Scholar]
  42. Queiroz, D. M. M., Rocha, G. A., Mendes, E. N., Lage, A. P., Carvalho, A. C. T. & Barbosa, A. J. A.(1990). A spiral microorganism in the stomach of pigs. Vet Microbiol 24, 199–204.[CrossRef] [Google Scholar]
  43. Queiroz, D. M. M., Rocha, G. A., Mendes, E. N., Moura, S. B., Rocha De Oliveira, A. M. & Miranda, D.(1996). Association between Helicobacter and gastric ulcer disease of the pars oesophagea in swine. Gastroenterology 111, 19–27.[CrossRef] [Google Scholar]
  44. Roosendaal, R., Vos, J. H., Roumen, T., Van Vugt, R., Cattoli, G., Bart, A., Klaasen, H. L., Kuipers, E. J., Vandenbroucke-Grauls, C. M. & Kusters, J. G.(2000). Slaughter pigs are commonly infected by closely related but distinct gastric ulcerative lesion-inducing gastrospirilla. J Clin Microbiol 38, 2661–2664. [Google Scholar]
  45. Singhal, A. V. & Sepulveda, A. R.(2005).Helicobacter heilmannii gastritis. A case study with review of literature. Am J Surg Pathol 29, 1537–1539.[CrossRef] [Google Scholar]
  46. Solnick, J. V., O'Rourke, J., Lee, A., Paster, B. J., Dewhirst, F. E. & Tompkins, L. S.(1993). An uncultured gastric spiral organism is a newly identified Helicobacter in humans. J Infect Dis 168, 379–385.[CrossRef] [Google Scholar]
  47. Taneera, J., Moran, A. P., Hynes, S. O., Nilsson, H. O., Al-Soud, W. & Wadström, T.(2002). Influence of activated charcoal, porcine gastric mucin and β-cyclodextrin on the morphology and growth of intestinal and gastric Helicobacter spp. Microbiology 148, 677–684. [Google Scholar]
  48. Utriainen, M. & Hänninen, M.-L.(1998). Detection of Helicobacter-like bacteria in porcine gastric biopsy samples by amplification of 16S rRNA, ureB, vacA and cagA genes by PCR. Vet Res Commun 22, 373–383.[CrossRef] [Google Scholar]
  49. Van den Bulck, K., Decostere, A., Baele, M., Driessen, A., Debongnie, J. C., Burette, A., Stolte, M., Ducatelle, R. & Haesebrouck, F.(2005). Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs and cats. J Clin Microbiol 43, 2256–2260.[CrossRef] [Google Scholar]
  50. Van den Bulck, K., Decostere, A., Baele, M., Vandamme, P., Mast, J., Ducatelle, R. & Haesebrouck, F.(2006).Helicobacter cynogastricus sp. nov., isolated from the canine gastric mucosa. Int J Syst Evol Microbiol 56, 1559–1564.[CrossRef] [Google Scholar]
  51. Vandamme, P., Harrington, C. S., Jalava, K. & On, S. L.(2000). Misidentifying helicobacters: the Helicobacter cinaedi example. J Clin Microbiol 38, 2261–2266. [Google Scholar]
  52. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Fijters, A., Pot, J., Peleman, J. & other authors(1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23, 4407–4414.[CrossRef] [Google Scholar]

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vol. , part 6, pp. 1350 - 1358

Distance matrix analyses for the 16S rRNA, partial , 23S rRNA and partial gene sequences from strains. [ Combined PDF] 177 KB

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