1887

Abstract

Molecular typing and virulence markers were used to evaluate the genetic profiles and virulence potential of 106 strains. Of these strains, 71 were bio-serotype 4/O : 3, isolated from human and animal clinical material, and 35 were of biotype 1A or 2 and of diverse serotypes, isolated from food in Brazil between 1968 and 2000. Drug resistance was also investigated. All the strains were resistant to three or more drugs. The isolates showed a virulence-related phenotype in the aesculin, pyrazinamidase and salicin tests, except for the food isolates, only two of which were positive for these tests. For the other phenotypic virulence determinants (autoagglutination, Ca dependence and Congo red absorption), the strains showed a diverse behaviour. The , and A genes were detected in all human and animal strains, while all the food isolates were positive for , and 3 % of them positive for and A. The presence of F was variable in the three groups of strains. The strains were better discriminated by PFGE than by enterobacterial repetitive intergenic consensus PCR (ERIC-PCR). A higher genomic similarity was observed among the 4/O : 3 strains, isolated from human and animal isolates, than among the food strains, with the exception of two food strains possessing the virulence genes and grouped close to the 4/O : 3 strains by ERIC-PCR. Unusually, the results revealed the virulence potential of a bio-serotype 1A/O : 10 strain, suggesting that food contaminated with biotype 1A may cause infection. This also suggests that ERIC-PCR may be used as a tool to reveal clues about the virulence potential of strains. Furthermore, the results also support the hypothesis that animals may act as reservoirs of for human infections in Brazil, an epidemiological aspect that has not been investigated in this country, confirming data from other parts of the world.

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2006-11-01
2019-11-13
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References

  1. Aleksic, S. & Bockemühl, J. ( 1999; ). Yersinia and other enterobacteriaceae. In Manual of Clinical Microbiology, 7th edn, pp. 483–496. Edited by K. V. Forrest, J. H. Jorgensen, & P. R. Murray. Washington, DC: American Society for Microbiology.
  2. Andersen, J. K. & Saunders, N. A. ( 1990; ). Epidemiological typing of Yersinia enterocolitica by analysis of restriction fragment length polymorphism with a cloned ribosomal RNA gene. J Med Microbiol 32, 179–187.[CrossRef]
    [Google Scholar]
  3. Bauab, T. M., Corrêa, E. F. & Falcão, D. P. ( 1995; ). Evaluation of different techniques for the differentiation of pathogenic and non pathogenic strains of Yersinia enterocolitica. Rev Microbiol 26, 106–111.
    [Google Scholar]
  4. Blumberg, H. M., Kiehlbauch, J. A. & Wachsmuth, I. K. ( 1991; ). Molecular epidemiology of Yersinia enterocolitica O : 3 infections: use of chromosomal DNA restriction fragment length polymorphism of rRNA genes. J Clin Microbiol 29, 2368–2374.
    [Google Scholar]
  5. Bottone, E. J. ( 1999; ). Yersinia enterocolitica: overview and epidemiologic correlates. Microb Infect 1, 323–333.[CrossRef]
    [Google Scholar]
  6. Carniel, E. ( 1995; ). Chromosomal virulence factors of Yersinia: an update. Contrib Microbiol Immunol 3, 218–224.
    [Google Scholar]
  7. Carniel, E. ( 2001; ). The Yersinia high-pathogenicity island: an iron-uptake island. Microb Infect 3, 561–569.[CrossRef]
    [Google Scholar]
  8. Cornelis, G. R., Boland, A., Boyd, A. P., Geuijen, C., Iriarte, M., Neyt, C., Sory, M.-P. & Stainier, I. ( 1998; ). The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 62, 1315–1352.
    [Google Scholar]
  9. Covone, M. G., Brocchi, M., Palla, E., Dias da Silveira, W., Rappuoli, R. & Galeotti, C. L. ( 1998; ). Levels of expression and immunogenicity of attenuated Salmonella enterica serovar Typhimurium strains expressing Escherichia coli mutant heat-labile enterotoxin. Infect Immun 66, 224–231.
    [Google Scholar]
  10. Falcão, D. P. ( 1987; ). Yersiniosis in Brazil. Summary of the data received at the Reference Laboratory for Yersinia in Brazil. Contrib Microbiol Immunol 9, 68–75.
    [Google Scholar]
  11. Falcão, D. P. ( 1991; ). Occurrence of Yersinia spp. in foods in Brazil. Int J Food Microbiol 14, 179–182.[CrossRef]
    [Google Scholar]
  12. Falcão, J. P., Falcão, D. P., Correa, E. F. & Brocchi, M. ( 2003; ). A virulence study of Yersinia enterocolitica O : 3 isolated from sick humans and animals in Brazil using PCR and phenotypic tests. Adv Exp Med Biol 529, 341–343.
    [Google Scholar]
  13. Falcão, J. P., Brocchi, M., Proença-Módena, J. L., Acrani, G. O., Correa, E. F. & Falcão, D. P. ( 2004; ). Virulence characteristics and epidemiology of Yersinia enterocolitica and Yersiniae other than Y. pseudotuberculosis and Y. pestis isolated from water and sewage. J Appl Microbiol 96, 1230–1236.[CrossRef]
    [Google Scholar]
  14. Farmer, J. J., III, Carter, G. P., Miller, V. L., Falkow, S. & Wachsmuth, I. K. ( 1992; ). Pyrazinamidase, CR-MOX agar, salicin fermentation-esculin hydrolysis, and d-xylose fermentation for identifying pathogenic serotypes of Yersinia enterocolitica. J Clin Microbiol 30, 2589–2594.
    [Google Scholar]
  15. Fredriksson-Ahomaa, M. & Korkeala, H. ( 2003; ). Low occurrence of pathogenic Yersinia enterocolitica in clinical, food and environmental samples: a methodological problem. Clin Microbiol Rev 16, 220–229.[CrossRef]
    [Google Scholar]
  16. Fredriksson-Ahomaa, M., Autio, T. & Korkeala, H. ( 1999; ). Efficient subtyping of Yersinia enterocolitica bioserotype 4/O : 3 with pulsed-field gel eletrophoresis. Lett Appl Microbiol 29, 308–312.[CrossRef]
    [Google Scholar]
  17. Fredriksson-Ahomaa, M., Hallanvuo, S., Korte, T., Siitonen, A. & Korkeala, H. ( 2001; ). Correspondence of genotypes of sporadic Yersinia enterocolitica bioserotype 4/O : 3 strains from human and porcine sources. Epidemiol Infect 127, 37–47.
    [Google Scholar]
  18. Fredriksson-Ahomaa, M., Koch, U., Klemm, C., Bucher, M. & Stolle, A. ( 2004; ). Different genotypes of Yersinia enterocolitica 4/O : 3 strains widely distributed in butcher shops in the Munich area. Int J Food Microbiol 95, 89–94.[CrossRef]
    [Google Scholar]
  19. Fredriksson-Ahomaa, M., Stolle, A., Siitonen, A. & Korkeala, H. ( 2006; ). Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O : 3 originate mainly from pigs. J Med Microbiol 55, 747–749.[CrossRef]
    [Google Scholar]
  20. Grant, T., Bennett-Wood, V. & Robins-Browne, R. M. ( 1998; ). Identification of virulence-associated characteristics in clinical isolates of Yersinia enterocolitica lacking classical virulence markers. Infect Immun 66, 1113–1120.
    [Google Scholar]
  21. Greenwood, M. H. & Hooper, W. L. ( 1990; ). Excretion of Yersinia spp. associated with consumption of pasteurized milk. Epidemiol Infect 104, 345–350.[CrossRef]
    [Google Scholar]
  22. Guiyoule, A., Rasoamanna, B., Buchrieser, C., Michel, P., Chanteau, S. & Carniel, E. ( 1997; ). Recent emergence of new variants of Yersinia pestis in Madagascar. J Clin Microbiol 35, 2826–2833.
    [Google Scholar]
  23. Hunter, P. R. & Gaston, M. A. ( 1998; ). Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J Clin Microbiol 26, 2465–2466.
    [Google Scholar]
  24. Ibrahim, A., Liesack, W., Griffiths, M. W. & Robins-Browne, R. M. ( 1997; ). Development of a highly specific assay for rapid identification of pathogenic strains of Yersinia enterocolitica based on PCR amplification of Yersinia heat-stable enterotoxin gene (yst). J Clin Microbiol 35, 1636–1638.
    [Google Scholar]
  25. Iteman, L., Guiyoule, A. & Carniel, E. ( 1996; ). Comparison of three molecular methods for typing and subtyping pathogenic Yersinia enterocolitica strains. J Med Microbiol 45, 48–56.[CrossRef]
    [Google Scholar]
  26. Kandolo, K. & Wauters, G. ( 1985; ). Pyrazinamidase activity in Yersinia enterocolitica and related organisms. J Clin Microbiol 21, 980–982.
    [Google Scholar]
  27. Kapperund, G. T., Nesbakken, T., Aleksic, S. & Mollaret, H. H. ( 1990; ). Comparison of restriction endonuclease analysis and phenotypic typing methods for differentiation of Y. enterocolitica isolates. J Clin Microbiol 28, 1125–1131.
    [Google Scholar]
  28. Lambertz, S. T. & Danielsson-Tham, M. L. ( 2005; ). Identification and characterization of pathogenic Yersinia enterocolitica isolates by PCR and pulsed-field gel electrophoresis. Appl Environ Microbiol 71, 3674–3681.[CrossRef]
    [Google Scholar]
  29. Liu, S. L., Hessel, A. & Sanderson, K. E. ( 1993; ). The XbaI-BlnI-CeuI genomic cleavage map of Salmonella typhimurium LT2 determined by double digestion, end labelling, and pulsed-field gel electrophoresis. J Bacteriol 175, 4104–4120.
    [Google Scholar]
  30. Lobato, M. J., Landeras, E., Gonzales-Hevia, M. A. & Mendonza, M. C. ( 1998; ). Genetic heterogeneity of clinical strains of Yersinia enterocolitica traced by ribotyping and relationships between ribotypes, serotypes, and biotypes. J Clin Microbiol 36, 3297–3301.
    [Google Scholar]
  31. McIntyre, M. & Nnochiri, E. ( 1986; ). A case of hospital-acquired Yersinia enterocolitica gastroenteritis. J Hosp Infect 7, 299–301.[CrossRef]
    [Google Scholar]
  32. Morris, J. G., Jr, Prado, V., Ferreccio, C., Robins-Browne, R. M., Bordun, A.-M., Cayazzo, M., Kay, B. A. & Levine, M. M. ( 1991; ). Yersinia enterocolitica isolated from two cohorts of young children in Santiago, Chile: incidence of and lack of correlation between illness and proposed virulence factors. J Clin Microbiol 29, 2784–2788.
    [Google Scholar]
  33. Najdenski, H., Iteman, I. & Carniel, E. ( 1994; ). Efficient subtyping of pathogenic Yersinia enterocolitica strains by pulsed-field gel electrophoresis. J Clin Microbiol 32, 2913–2921.
    [Google Scholar]
  34. Nakajima, H., Inoue, M., Mori, T., Itoh, K.-I., Arakawa, A. & Watanabe, H. ( 1992; ). Detection and identification of Yersinia pseudotuberculosis and pathogenic Yersinia enterocolitica by an improved polymerase chain reaction method. J Clin Microbiol 30, 2484–2486.
    [Google Scholar]
  35. National Commitee for Clinical Laboratory Standards ( 2001; ). Performance Standard for Antimicrobial Susceptibility Testing. Approved standard M100-S11. Wayne, PA: National Commitee for Clinical Laboratory Standards.
  36. Nesbakken, T., Kapperud, G., Sorum, H. & Dommarsnes, K. ( 1987; ). Structural variability of 40–50 MDa virulence plasmids from Yersinia enterocolitica. Acta Pathol Microbiol Immunol Scand 95, 167–173.
    [Google Scholar]
  37. Nesbakken, T., Kapperud, G., Dommarsnes, K., Skurnik, M. & Hornes, E. ( 1991; ). Comparative study of a DNA hybridization method and two isolation procedures for detection of Yersinia enterocolitica O : 3 in naturally contaminated pork products. Appl Environ Microbiol 57, 389–394.
    [Google Scholar]
  38. Nicolle, P., Mollaret, H. H. & Brault, J. ( 1976; ). Nouveaux resultats sur la lysotypie de Yersinia enterocolitica portant sur plus de 4000 souches d'origines diverses. Rev Epidemiol Santé Publique 24, 479–496 (in French).
    [Google Scholar]
  39. Rasmussen, H. N., Rasmussen, O. F., Andersen, J. K. & Olsen, J. E. ( 1994; ). Specific detection of pathogenic Yersinia enterocolitica by two-step PCR using hot-start and DMSO. Mol Cell Probes 8, 99–108.[CrossRef]
    [Google Scholar]
  40. Ratnam, S., Mercer, E., Picco, B., Parsons, S. & Butler, R. ( 1982; ). A nosocomial outbreak of diarrheal disease due to Yersinia enterocolitica serotype O 5, biotype 1. J Infect Dis 145, 242–247.[CrossRef]
    [Google Scholar]
  41. Riley, G. & Toma, S. ( 1989; ). Detection of pathogenic Yersinia enterocolitica by using Congo red-magnesium oxalate agar medium. J Clin Microbiol 27, 213–214.
    [Google Scholar]
  42. Robins-Browne, R. M. ( 2001; ). Yersinia enterocolitica. In Food Microbiology Fundamentals and Frontiers, pp. 215–245. Edited by M. P. Doyle, L. R. Beuchat & T. J. Montiville. Washington, DC: American Society for Microbiology.
  43. Sachdeva, P. & Virdi, J. S. ( 2004; ). Repetitive elements sequence (REP/ERIC)-PCR based genotyping of clinical and environmental strains of Yersinia enterocolitica biotype 1A reveal existence of limited number of clonal groups. FEMS Microbiol Lett 240, 193–201.[CrossRef]
    [Google Scholar]
  44. Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B. & Erlich, H. A. ( 1988; ). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487–491.[CrossRef]
    [Google Scholar]
  45. Saken, E., Roggenkamp, A., Aleksic, S. & Heeseman, J. ( 1994; ). Characterisation of pathogenic Yersinia enterocolitica serogroups by pulsed-field gel electrophoresis of genomic NotI restriction fragments. J Med Microbiol 41, 329–338.[CrossRef]
    [Google Scholar]
  46. Salyers, A. A. & Whitt, D. D. ( 2002; ). Yersinia pestis, the cause of plague, and its relatives. In Bacterial Pathogenesis: a Molecular Approach. Edited by A. A. Salyers & D. D. Whitt. Washington DC: American Society for Microbiology.
  47. Sambrook, J. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  48. Singh, I. & Virdi, J. S. ( 2004; ). Production of Yersinia stable toxin (YST) and distribution of yst genes in biotype 1A strains of Yersinia enterocolitica. J Med Microbiol 53, 1065–1068.[CrossRef]
    [Google Scholar]
  49. Stock, I. & Wiedemann, B. ( 1999; ). An in-vitro study of the antimicrobial susceptibilities of Yersinia enterocolitica and the definition of a database. J Antimicrob Chemother 43, 37–45.
    [Google Scholar]
  50. Stock, I., Heisig, P. & Wiedemann, B. ( 2000; ). Beta-lactamase expression in Yersinia enterocolitica biovars 1A, 1B, and 3. J Med Microbiol 49, 403–408.
    [Google Scholar]
  51. Stock, I. & Wiedemann, B. ( 2003; ). Natural antimicrobial susceptibilities and biochemical profiles of Yersinia enterocolitica-like strains: Y. frederiksenii, Y. intermedia, Y. kristensenii and Y. rohdei. FEMS Immunol Med Microbiol 38, 139–152.[CrossRef]
    [Google Scholar]
  52. Stock, I., Heisig, P. & Wiedemann, B. ( 1999; ). Expression of beta-lactamases in Yersinia enterocolitica strains of biovars 2, 4 and 5. J Med Microbiol 48, 1023–1027.[CrossRef]
    [Google Scholar]
  53. Sulakvelidze, A. ( 2000; ). Yersiniae other than Y.enterocolitica, Y. pseudotuberculosis and Y. pestis: the ignored species. Microb Infect 2, 497–513.[CrossRef]
    [Google Scholar]
  54. Tennant, S. M., Grant, T. H. A. & Robins-Browne, R. M. ( 2003; ). Pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunol Med Microbiol 38, 127–137.[CrossRef]
    [Google Scholar]
  55. Thoerner, P., Bin Kingombe, C. I., Bogli-Stuber, K., Bissig-Choisat, B., Wassenaar, T. M., Frey, J. & Jemmi, T. ( 2003; ). PCR detection of virulence genes in Yersinia enterocolitica and Yersinia pseudotuberculosis and investigation of virulence gene distribution. Appl Environ Microbiol 69, 1810–1816.[CrossRef]
    [Google Scholar]
  56. Tibana, A., Warnken, M. B., Nunes, M. P., Ricciardi, I. D. & Noleto, A. L. S. ( 1987; ). Occurrence of Yersinia species in raw and pasteurized milk in Rio de Janeiro, Brazil. J Food Prot 50, 580–583.
    [Google Scholar]
  57. Tzelepi, E., Arvanitidou, M., Mavroidi, A. & Tsakris, A. ( 1999; ). Antibiotic susceptibilities of Yersinia enterocolitica and Y. intermedia isolates from aquatic environments. J Med Microbiol 48, 157–160.[CrossRef]
    [Google Scholar]
  58. Versalovic, J., Koeuth, T. & Lupski, J. R. ( 1991; ). Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19, 6823–6831.[CrossRef]
    [Google Scholar]
  59. Warnken, M. B., Nunes, M. P. & Noleto, A. L. S. ( 1987; ). Incidence of Yersinia species in meat samples purchased in Rio de Janeiro, Brazil. J Food Prot 50, 578–579.
    [Google Scholar]
  60. Wauters, G., Aleksic, S., Charlier, J. & Schulze, G. ( 1991; ). Somatic and flagellar antigens of Yersinia enterocolitica and related species. Contrib Microbiol Immunol 12, 239–243.
    [Google Scholar]
  61. White, D. G., Zhao, S., Simjee, S., Wagner, D. D. & McDermott, P. F. ( 2002; ). Antimicrobial resistance of foodborne pathogens. Microb Infect 4, 405–412.[CrossRef]
    [Google Scholar]
  62. Wojciech, L., Staroniewicz, Z., Jakubczak, A. & Ugorski, M. ( 2004; ). Typing of Yersinia enterocolitica isolates by ITS profiling, REP- and ERIC-PCR. J Vet Med 51, 238–244.[CrossRef]
    [Google Scholar]
  63. Wren, B. W. & Tabaqchali, S. ( 1990; ). Detection of pathogenic Yersinia enterocolitica by the polymerase chain reaction. Lancet 336, 693.
    [Google Scholar]
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