1887

Abstract

strains of serotype O113 : H21 are commonly described as belonging to a Shiga toxin (Stx)-producing (STEC) pathotype worldwide. Albeit this STEC serotype is frequently identified among cattle and other domestic animals, to the best of our knowledge no human infections associated with STEC O113 : H21 have been registered in Brazil to date. Here, we report the virulence profile and genetic relatedness of a collection of O113 : H21 strains mainly isolated from the animal reservoir aimed at determining their potential as human pathogens. The strains from the animal reservoir (=34) were all classified as STEC, whereas the few isolates recovered so far from human diarrhoea (=3) lacked genes. Among the STEC, the gene was identified in 85 % of the strains that also carried , , , , , , -, , and ; the human strains harboured only , and . All the strains except one, isolated from cattle, were genetically classified as phylogenetic group B1. High mass plasmids were observed in 25 isolates, but only in the STEC group were these plasmids confirmed as the STEC O113 megaplasmid (pO113). Many closely related subgroups (more than 80 % similarity) were identified by PFGE, with human isolates clustering in a subgroup separate from most of the animal isolates. In conclusion, potentially pathogenic O113 : H21 STEC isolates carrying virulence markers in common with O113 : H21 clones associated with haemolytic uraemic syndrome cases in other regions were demonstrated to occur in the natural reservoir in our settings, and therefore the risk represented by them to public health should be carefully monitored.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.015263-0
2010-06-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/jmm/59/6/634.html?itemId=/content/journal/jmm/10.1099/jmm.0.015263-0&mimeType=html&fmt=ahah

References

  1. Abe, C. M., Salvador, F. A., Falsetti, I. N., Vieira, M. A. M., Blanco, J., Blanco, J. E., Blanco, M., Machado, A. M. O., Elias, W. P. & other authors ( 2008; ). Uropathogenic Escherichia coli (UPEC) strains may carry virulence properties of diarrheogenic E. coli. FEMS Immunol Med Microbiol 52, 397–406.[CrossRef]
    [Google Scholar]
  2. Beutin, L., Kaulfuss, S., Herold, S., Oswald, E. & Schmidt, H. ( 2005; ). Genetic analysis of enteropathogenic and enterohemorrhagic Escherichia coli serogroup O103 strains by molecular typing of virulence and housekeeping genes and pulsed-field gel electrophoresis. J Clin Microbiol 43, 1552–1563.[CrossRef]
    [Google Scholar]
  3. Bielaszewska, M., Fell, M., Greune, L., Prager, R., Fruth, A., Tschäpe, H., Schmidt, M. A. & Karch, H. ( 2004; ). Characterization of cytolethal distending toxin genes and expression in shiga toxin-producing Escherichia coli strains of non-O157 serogroups. Infect Immun 72, 1812–1816.[CrossRef]
    [Google Scholar]
  4. Bielaszewska, M., Friedrich, A. W., Aldick, T., Schurk-Bulgrin, R. & Karch, H. ( 2006; ). Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin Infect Dis 43, 1160–1167.[CrossRef]
    [Google Scholar]
  5. Birnboim, H. C. & Doly, J. ( 1979; ). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7, 1513–1523.[CrossRef]
    [Google Scholar]
  6. Blanco, M., Blanco, J. E., Blanco, J., Alonso, M. P., Balsalobre, C., Mourino, M., Madrid, C. & Juarez, A. ( 1996; ). Polymerase chain reaction for detection of Escherichia coli strains producing cytotoxic necrotizing factor type 1 and type 2 (CNF1 and CNF2). J Microbiol Methods 26, 95–101.[CrossRef]
    [Google Scholar]
  7. Blanco, J., Blanco, M., Blanco, J. E., Mora, A., Gonzáles, E. A., Bernárdez, M. E., Alonso, M. P., Coira, A., Rodriguez, A. & other authors ( 2003; ). Verotoxin-producing Escherichia coli in Spain: prevalence, serotypes, and virulence genes of O157 : H7 and non-O157 VTEC in ruminants, raw beef products, and humans. Exp Biol Med (Maywood) 228, 345–351.
    [Google Scholar]
  8. Brunder, W., Schmidt, H., Frosch, M. & Karch, H. ( 1999; ). The large plasmids of Shiga-toxin-producing Escherichia coli (STEC) are highly variable genetic elements. Microbiology 145, 1005–1014.[CrossRef]
    [Google Scholar]
  9. Caprioli, A., Morabito, S., Brugere, H. & Oswald, E. ( 2005; ). Enterohemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 36, 289–311.[CrossRef]
    [Google Scholar]
  10. Cergole-Novella, M. C., Nishimura, L. S., dos Santos, L. F., Irino, K., Vaz, T. M. I., Bergamini, A. M. & Guth, B. E. C. ( 2007; ). Distribution of virulence profiles related to new toxins and putative adhesins in Shiga toxin-producing Escherichia coli isolated from diverse sources in Brazil. FEMS Microbiol Lett 274, 329–334.[CrossRef]
    [Google Scholar]
  11. Cerqueira, A. M. F. ( 2000; ). Shiga toxin-producing Escherichia coli (STEC): prevalence in animal reservoir, virulence markers and analysis of clonal structure. PhD thesis, Universidade Federal de São Paulo, Escola Paulista de Medicina, São Paulo, Brazil.
  12. Cerqueira, A. M. F., Tibana, A. & Guth, B. E. C. ( 1997; ). High occurrence of Shiga-like toxin-producing strains among diarrheagenic Escherichia coli isolated from raw beef products in Rio de Janeiro City, Brazil. J Food Prot 60, 177–180.
    [Google Scholar]
  13. Chapman, P. A. C. A., Cerdan Malon, A. T. M. S. & Harkin, M. A. ( 2000; ). A one year study of Escherichia coli O157 in raw beef and lamb products. Epidemiol Infect 124, 207–213.[CrossRef]
    [Google Scholar]
  14. Clermont, O., Bonacorsi, S. & Bingen, E. ( 2000; ). Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66, 4555–4558.[CrossRef]
    [Google Scholar]
  15. Dos Santos, L. F., Gonçalves, E. M., Vaz, T. M. I., Irino, K. & Guth, B. E. C. ( 2007; ). Distinct pathotypes of O113 Escherichia coli strains isolated from humans and animals in Brazil. J Clin Microbiol 45, 2028–2030.[CrossRef]
    [Google Scholar]
  16. Gautom, R. K. ( 1997; ). Rapid pulsed-field gel electrophoresis protocol for typing of Escherichia coli O157 : H7 and other gram-negative organisms in one day. J Clin Microbiol 35, 2977–2980.
    [Google Scholar]
  17. Gonzales, A. G. M. ( 2003; ). Phenotypic and genotypic characteristics of Shiga toxin-producing Escherichia coli (STEC) isolated from cattle in Rio de Janeiro State. PhD thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
  18. Griffin, P. M. & Tauxe, R. V. ( 1991; ). The epidemiology of infections caused by Escherichia coli O157 : H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev 13, 60–98.
    [Google Scholar]
  19. Hogan, M. C., Gloor, J. M., Uhl, J. R., Cockerill, F. R. & Milliner, D. S. ( 2001; ). Two cases of non-O157 Escherichia coli hemolytic uremic syndrome caused by urinary tract infection. Am J Kidney Dis 38, E22 [CrossRef]
    [Google Scholar]
  20. Irino, K., Kato, M. A., Vaz, T. M. I., Ramos, I. I., Souza, M. A., Cruz, A. S., Gomes, T. A. T., Vieira, M. A. M. & Guth, B. E. C. ( 2005; ). Serotypes and virulence markers of Shiga toxin-producing Escherichia coli (STEC) isolated from dairy cattle in São Paulo State, Brazil. Vet Microbiol 105, 29–36.[CrossRef]
    [Google Scholar]
  21. Irino, K., Vaz, T. M. I., Medeiros, M. I., Kato, M. A. M. F., Gomes, T. A. T., Vieira, M. A. M. & Guth, B. E. C. ( 2007; ). Serotype diversity as a drawback in the surveillance of Shiga toxin-producing Escherichia coli infections in Brazil. J Med Microbiol 56, 565–567.[CrossRef]
    [Google Scholar]
  22. Johnson, K. E., Thorpe, C. M. & Sears, C. L. ( 2006; ). The emerging clinical importance of non-O157 Shiga toxin-producing Escherichia coli. Clin Infect Dis 43, 1587–1595.[CrossRef]
    [Google Scholar]
  23. Karch, H., Meyer, T., Russmann, H. & Heesemann, J. ( 1992; ). Frequent loss of Shiga-like toxin genes in clinical isolates of Escherichia coli upon subcultivation. Infect Immun 60, 3464–3467.
    [Google Scholar]
  24. Karmali, M. A., Petric, M., Lim, C., Fleming, P. C., Arbus, G. S. & Lior, H. ( 1985; ). The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis 151, 775–782.[CrossRef]
    [Google Scholar]
  25. Khaitan, A., Jandhyala, D. M., Thorpe, C. M., Ritchie, J. M. & Paton, A. W. ( 2007; ). The operon encoding SubAB, a novel cytotoxin, is present in Shiga toxin-producing Escherichia coli isolates from the United States. J Clin Microbiol 45, 1374–1375.[CrossRef]
    [Google Scholar]
  26. Leomil, L., Aidar-Ugrinovich, L., Guth, B. E. C., Irino, K., Vettorato, M. P., Onuma, D. L. & Castro, A. F. P. ( 2003; ). Frequency of Shiga toxin-producing Escherichia coli (STEC) isolates among diarrheic and non-diarrheic calves in Brazil. Vet Microbiol 97, 103–109.[CrossRef]
    [Google Scholar]
  27. Leyton, D. L., Sloan, J., Hill, R. E., Doughty, S. & Hartland, E. L. ( 2003; ). Transfer region of pO113 from enterohemorrhagic Escherichia coli: similarity with R64 and identification of a novel plasmid-encoded autotransporter, EpeA. Infect Immun 71, 6307–6319.[CrossRef]
    [Google Scholar]
  28. Lindgren, S. W., Melton, A. R. & O'Brien, A. D. ( 1993; ). Virulence of enterohemorrhagic Escherichia coli O91 : H21 clinical isolates in an orally infected mouse model. Infect Immun 61, 3832–3842.
    [Google Scholar]
  29. Mellmann, A., Bielaszewska, M., Köck, R., Friedrich, A. W., Fruth, A., Middendorf, B., Harmsen, D., Schmidt, M. A. & Karch, H. ( 2008; ). Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg Infect Dis 14, 1287–1290.[CrossRef]
    [Google Scholar]
  30. Melton-Celsa, A. R., Darnell, S. C. & O'Brien, A. D. ( 1996; ). Activation of Shiga-like toxins by mouse and human intestinal mucus correlates with virulence of enterohemorrhagic Escherichia coli O91 : H21 isolates in orally infected, streptomycin-treated mice. Infect Immun 64, 1569–1576.
    [Google Scholar]
  31. Newton, H. J., Sloan, J., Bulach, D. M., Seemann, T., Allison, C. C., Tauschek, M., Robins-Browne, R. M., Paton, J. C., Whittam, T. S. & other authors ( 2009; ). Shiga toxin-producing Escherichia coli strains negative for locus of enterocyte effacement. Emerg Infect Dis 15, 372–380.[CrossRef]
    [Google Scholar]
  32. Oliveira, M. G., Brito, J. R., Carvalho, R. R., Guth, B. E. C., Gomes, T. A. T., Vieira, M. A. M., Kato, M. A., Ramos, I. I., Vaz, T. M. I. & Irino, K. ( 2007; ). Water buffaloes (Bubalus bubalis) identified as an important reservoir of Shiga toxin-producing Escherichia coli in Brazil. Appl Environ Microbiol 73, 5945–5948.[CrossRef]
    [Google Scholar]
  33. Oliveira, M. G., Brito, J. R., Gomes, T. A. T., Guth, B. E. C., Vieira, M. A. M., Naves, Z. V., Vaz, T. M. I. & Irino, K. ( 2008; ). Diversity of virulence profiles of Shiga toxin-producing Escherichia coli serotypes in food-producing animals in Brazil. Int J Food Microbiol 127, 139–146.[CrossRef]
    [Google Scholar]
  34. Paton, J. C. & Paton, A. W. ( 1998; ). Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11, 450–479.
    [Google Scholar]
  35. Paton, A. W., Woodrow, M. C., Doyle, R. M., Lanser, J. A. & Paton, J. C. ( 1999; ). Molecular characterization of a Shiga toxigenic Escherichia coli O113 : H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. J Clin Microbiol 37, 3357–3361.
    [Google Scholar]
  36. Paton, A. W., Srimanote, P., Woodrow, M. C. & Paton, J. C. ( 2001; ). Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect Immun 69, 6999–7009.[CrossRef]
    [Google Scholar]
  37. Paton, A. W., Srimanote, P., Talbot, U. M., Wang, H. & Paton, J. C. ( 2004; ). A new family of potent AB5 cytotoxins produced by Shiga toxigenic Escherichia coli. J Exp Med 200, 35–46.[CrossRef]
    [Google Scholar]
  38. Piérard, D., Muyldermans, G., Moriau, L., Stevens, D. & Lawers, S. ( 1998; ). Identification of new verocytotoxin type 2 variant B-subunit genes in human and animal Escherichia coli isolates. J Clin Microbiol 36, 3317–3322.
    [Google Scholar]
  39. Pigatto, C. P., Schocken-Iturrino, R. P., Souza, E. M., Pedrosa, F. O., Comarella, L., Irino, K., Kato, M. A., Farah, S. M., Warth, J. F. & Fadel-Picheth, C. M. ( 2008; ). Virulence properties and antimicrobial susceptibility of Shiga toxin-producing Escherichia coli strains isolated from healthy cattle from Paraná State, Brazil. Can J Microbiol 54, 588–593.[CrossRef]
    [Google Scholar]
  40. Schmidt, H., Zhang, W. L., Hemmrich, U., Jelacic, S., Brunder, W., Tarr, P. I., Dobrindt, U., Hacker, J. & Karch, H. ( 2001; ). Identification and characterization of a novel genomic island integrated at selC in locus of enterocyte effacement-negative, Shiga toxin-producing Escherichia coli. Infect Immun 69, 6863–6873.[CrossRef]
    [Google Scholar]
  41. Souza, R. L., Nishimura, L. S. & Guth, B. E. C. ( 2007; ). Uncommon Shiga toxin-producing Escherichia coli serotype O165 : HNM as cause of hemolytic uremic syndrome in São Paulo, Brazil. Diagn Microbiol Infect Dis 59, 223–225.[CrossRef]
    [Google Scholar]
  42. Tarr, P. I. & Neill, M. A. ( 1996; ). The problem of non-O157 : H7 Shiga toxin (verocytotoxin) producing Escherichia coli. J Infect Dis 174, 1136–1139.[CrossRef]
    [Google Scholar]
  43. Tatarczak, M., Wieczorek, K., Posse, B. & Osek, J. ( 2005; ). Identification of putative adhesin genes in shigatoxigenic Escherichia coli isolated from different sources. Vet Microbiol 110, 77–85.[CrossRef]
    [Google Scholar]
  44. Toma, C., Martinez-Espinosa, E., Song, T., Miliwebsky, E., Chinen, I., Iyoda, S., Iwanaga, M. & Rivas, M. ( 2004; ). Distribution of putative adhesins in different seropathotypes of Shiga toxin-producing Escherichia coli. J Clin Microbiol 42, 4937–4946.[CrossRef]
    [Google Scholar]
  45. Vaz, T. M. I., Irino, K., Kato, M. A. M. F., Dias, A. M. G., Gomes, T. A. T., Medeiros, M. I. C., Rocha, M. M. M. & Guth, B. E. C. ( 2004; ). Virulence properties and characteristics of Shiga toxin-producing Escherichia coli strains in São Paulo, Brazil, from 1976 through 1999. J Clin Microbiol 42, 903–905.[CrossRef]
    [Google Scholar]
  46. Zheng, J., Cui, S., Teel, L. D., Zhao, S., Singh, R., O'Brien, A. D. & Meng, J. ( 2008; ). Identification and characterization of Shiga toxin type 2 variants in Escherichia coli isolates from animals, food, and humans. Appl Environ Microbiol 74, 5645–5652.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.015263-0
Loading
/content/journal/jmm/10.1099/jmm.0.015263-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error