1887

Abstract

The aim of this study was to identify an epidemiological association between Shiga toxin-producing O157 : H7 strains associated with human infection and with food sources. Frequency distributions of different genetic markers of O157 : H7 strains recovered from human and food sources were compared using molecular assays to identify O157 : H7 genotypes associated with variation in pathogenic potential and host specificity. Genotypic characterization included: lineage-specific polymorphism assay (LSPA-6), clade typing, () polymorphism, Shiga toxin-encoding bacteriophage insertion site analysis and variant analysis of Shiga toxin 2 gene ( and ) and antiterminator genes ( and ). The intermediate lineage (LI/II) dominated among both food and human strains. Compared to other clades, clades 7 and 8 were more frequent among food and human strains, respectively. The () polymorphism occurred more frequently among human strains than food strains. and were found at significantly higher frequencies among food and human strains, respectively. Moreover, and were detected at significantly higher frequencies among human strains compared to food strains. Bivariate analysis revealed significant concordance (<0.05) between the LSPA-6 assay and the other typing methods. Multivariable regression analysis suggested that () was the most distinctive genotype that can be used to detect bacterial clones with potential risk for human illness from food sources. This study supported previous reports of the existence of diversity in genetic markers among different isolation sources by including O157 : H7 strains from both food and human sources. This might enable tracking genotypes with potential risk for human illness from food sources.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.083063-0
2015-01-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/1/112.html?itemId=/content/journal/micro/10.1099/mic.0.083063-0&mimeType=html&fmt=ahah

References

  1. Ahmad A., Zurek L.. ( 2006;). Evaluation of the anti-terminator Q933 gene as a marker for Escherichia coli O157:H7 with high Shiga toxin production. . Curr Microbiol 53:, 324–328. [CrossRef][PubMed]
    [Google Scholar]
  2. Andersson T., Nilsson C., Kjellin E., Toljander J., Welinder-Olsson C., Lindmark H.. ( 2011;). Modeling gene associations for virulence classification of verocytotoxin-producing E. coli (VTEC) from patients and beef. . Virulence 2:, 41–53. [CrossRef][PubMed]
    [Google Scholar]
  3. Arthur T. M., Ahmed R., Chase-Topping M., Kalchayanand N., Schmidt J. W., Bono J. L.. ( 2013;). Characterization of Escherichia coli O157:H7 strains isolated from supershedding cattle. . Appl Environ Microbiol 79:, 4294–4303. [CrossRef][PubMed]
    [Google Scholar]
  4. Besser T. E., Shaikh N., Holt N. J., Tarr P. I., Konkel M. E., Malik-Kate P., Walsh C. W., Whittam T. S., Bono J. L.. ( 2007;). Greater diversity of Shiga toxin-encoding bacteriophage insertion sites among Escherichia coli O157: H7 isolates from cattle than in those from humans. . Appl Environ Microbiol 73:, 671–679. [CrossRef][PubMed]
    [Google Scholar]
  5. Beutin L., Miko A., Krause G., Pries K., Haby S., Steege K., Albrecht N.. ( 2007;). Identification of human-pathogenic strains of Shiga toxin-producing Escherichia coli from food by a combination of serotyping and molecular typing of Shiga toxin genes. . Appl Environ Microbiol 73:, 4769–4775. [CrossRef][PubMed]
    [Google Scholar]
  6. Bono J. L., Keen J. E., Clawson M. L., Durso L. M., Heaton M. P., Laegreid W. W.. ( 2007;). Association of Escherichia coli O157:H7 tir polymorphisms with human infection. . BMC Infect Dis 7:, 98. [CrossRef][PubMed]
    [Google Scholar]
  7. Botteldoorn N., Heyndrickx M., Rijpens N., Herman L.. ( 2003;). Detection and characterization of verotoxigenic Escherichia coli by a VTEC/EHEC multiplex PCR in porcine faeces and pig carcass swabs. . Res Microbiol 154:, 97–104. [CrossRef][PubMed]
    [Google Scholar]
  8. Eklund M., Scheutz F., Siitonen A.. ( 2001;). Clinical isolates of non-O157 Shiga toxin-producing Escherichia coli: serotypes, virulence characteristics, and molecular profiles of strains of the same serotype. . J Clin Microbiol 39:, 2829–2834. [CrossRef][PubMed]
    [Google Scholar]
  9. Flamm R. K., Hinrichs D. J., Thomashow M. F.. ( 1984;). Introduction of pAM beta 1 into Listeria monocytogenes by conjugation and homology between native L. monocytogenes plasmids. . Infect Immun 44:, 157–161.[PubMed]
    [Google Scholar]
  10. Franz E., van Hoek A. H., van der Wal F. J., de Boer A., Zwartkruis-Nahuis A., van der Zwaluw K., Aarts H. J., Heuvelink A. E.. ( 2012;). Genetic features differentiating bovine, food, and human isolates of shiga toxin-producing Escherichia coli O157 in The Netherlands. . J Clin Microbiol 50:, 772–780. [CrossRef][PubMed]
    [Google Scholar]
  11. Friedrich A. W., Bielaszewska M., Zhang W. L., Pulz M., Kuczius T., Ammon A., Karch H.. ( 2002;). Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. . J Infect Dis 185:, 74–84. [CrossRef][PubMed]
    [Google Scholar]
  12. Grant J., Wendelboe A. M., Wendel A., Jepson B., Torres P., Smelser C., Rolfs R. T.. ( 2008;). Spinach-associated Escherichia coli O157:H7 outbreak, Utah and New Mexico, 2006. . Emerg Infect Dis 14:, 1633–1636. [CrossRef][PubMed]
    [Google Scholar]
  13. Hartzell A., Chen C., Lewis C., Liu K. Q., Reynolds S., Dudley E. G.. ( 2011;). Escherichia coli O157:H7 of genotype lineage-specific polymorphism assay 211111 and clade 8 are common clinical isolates within Pennsylvania. . Foodborne Pathog Dis 8:, 763–768. [CrossRef][PubMed]
    [Google Scholar]
  14. Kaper J. B., Nataro J. P., Mobley H. L. T.. ( 2004;). Pathogenic Escherichia coli.. Nat Rev Microbiol 2:, 123–140. [CrossRef][PubMed]
    [Google Scholar]
  15. Laing C., Pegg C., Yawney D., Ziebell K., Steele M., Johnson R., Thomas J. E., Taboada E. N., Zhang Y. X., Gannon V. P. J.. ( 2008;). Rapid determination of Escherichia coli O157:H7 lineage types and molecular subtypes by using comparative genomic fingerprinting. . Appl Environ Microbiol 74:, 6606–6615. [CrossRef][PubMed]
    [Google Scholar]
  16. Lee K., French N. P., Hara-Kudo Y., Iyoda S., Kobayashi H., Sugita-Konishi Y., Tsubone H., Kumagai S.. ( 2011;). Multivariate analyses revealed distinctive features differentiating human and cattle isolates of Shiga toxin-producing Escherichia coli O157 in Japan. . J Clin Microbiol 49:, 1495–1500. [CrossRef][PubMed]
    [Google Scholar]
  17. LeJeune J. T., Abedon S. T., Takemura K., Christie N. P., Sreevatsan S.. ( 2004;). Human Escherichia coli O157:H7 genetic marker in isolates of bovine origin. . Emerg Infect Dis 10:, 1482–1485. [CrossRef][PubMed]
    [Google Scholar]
  18. Liu K., Knabel S. J., Dudley E. G.. ( 2009;). rhs genes are potential markers for multilocus sequence typing of Escherichia coli O157:H7 strains. . Appl Environ Microbiol 75:, 5853–5862. [CrossRef][PubMed]
    [Google Scholar]
  19. Lowe R. M., Baines D., Selinger L. B., Thomas J. E., McAllister T. A., Sharma R.. ( 2009;). Escherichia coli O157:H7 strain origin, lineage, and Shiga toxin 2 expression affect colonization of cattle. . Appl Environ Microbiol 75:, 5074–5081. [CrossRef][PubMed]
    [Google Scholar]
  20. Mainil J. G., Daube G.. ( 2005;). Verotoxigenic Escherichia coli from animals, humans and foods: who’s who. ? J Appl Microbiol 98:, 1332–1344. [CrossRef][PubMed]
    [Google Scholar]
  21. Manning S. D., Motiwala A. S., Springman A. C., Qi W., Lacher D. W., Ouellette L. M., Mladonicky J. M., Somsel P., Rudrik J. T.. & other authors ( 2008;). Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. . Proc Natl Acad Sci U S A 105:, 4868–4873. [CrossRef][PubMed]
    [Google Scholar]
  22. Mellor G. E., Sim E. M., Barlow R. S., D’Astek B. A., Galli L., Chinen I., Rivas M., Gobius K. S.. ( 2012;). Phylogenetically related Argentinean and Australian Escherichia coli O157 isolates are distinguished by virulence clades and alternative Shiga toxin 1 and 2 prophages. . Appl Environ Microbiol 78:, 4724–4731. [CrossRef][PubMed]
    [Google Scholar]
  23. Mellor G. E., Besser T. E., Davis M. A., Beavis B., Jung W., Smith H. V., Jennison A. V., Doyle C. J., Chandry P. S.. & other authors ( 2013;). Multilocus genotype analysis of Escherichia coli O157 isolates from Australia and the United States provides evidence of geographic divergence. . Appl Environ Microbiol 79:, 5050–5058. [CrossRef][PubMed]
    [Google Scholar]
  24. Nataro J. P., Kaper J. B.. ( 1998;). Diarrheagenic Escherichia coli.. Clin Microbiol Rev 11:, 142–201.[PubMed]
    [Google Scholar]
  25. Persson S., Olsen K. E., Ethelberg S., Scheutz F.. ( 2007;). Subtyping method for Escherichia coli shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. . J Clin Microbiol 45:, 2020–2024. [CrossRef][PubMed]
    [Google Scholar]
  26. Rangel J. M., Sparling P. H., Crowe C., Griffin P. M., Swerdlow D. L.. ( 2005;). Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. . Emerg Infect Dis 11:, 603–609. [CrossRef][PubMed]
    [Google Scholar]
  27. Ribot E. M., Fair M. A., Gautom R., Cameron D. N., Hunter S. B., Swaminathan B., Barrett T. J.. ( 2006;). Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. . Foodborne Pathog Dis 3:, 59–67. [CrossRef][PubMed]
    [Google Scholar]
  28. Riordan J. T., Viswanath S. B., Manning S. D., Whittam T. S.. ( 2008;). Genetic differentiation of Escherichia coli O157:H7 clades associated with human disease by real-time PCR. . J Clin Microbiol 46:, 2070–2073. [CrossRef][PubMed]
    [Google Scholar]
  29. Shaikh N., Tarr P. I.. ( 2003;). Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. . J Bacteriol 185:, 3596–3605. [CrossRef][PubMed]
    [Google Scholar]
  30. Stanton E., Park D., Döpfer D., Ivanek R., Kaspar C. W.. ( 2014;). Phylogenetic characterization of Escherichia coli O157 : H7 based on IS629 distribution and Shiga toxin genotype. . Microbiology 160:, 502–513. [CrossRef][PubMed]
    [Google Scholar]
  31. Vanaja S. K., Springman A. C., Besser T. E., Whittam T. S., Manning S. D.. ( 2010;). Differential expression of virulence and stress fitness genes between Escherichia coli O157:H7 strains with clinical or bovine-biased genotypes. . Appl Environ Microbiol 76:, 60–68. [CrossRef][PubMed]
    [Google Scholar]
  32. Wagner P. L., Neely M. N., Zhang X., Acheson D. W., Waldor M. K., Friedman D. I.. ( 2001;). Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. . J Bacteriol 183:, 2081–2085. [CrossRef][PubMed]
    [Google Scholar]
  33. Wang G., Clark C. G., Rodgers F. G.. ( 2002;). Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. . J Clin Microbiol 40:, 3613–3619. [CrossRef][PubMed]
    [Google Scholar]
  34. Whitworth J. H., Fegan N., Keller J., Gobius K. S., Bono J. L., Call D. R., Hancock D. D., Besser T. E.. ( 2008;). International comparison of clinical, bovine, and environmental Escherichia coli O157 isolates on the basis of Shiga toxin-encoding bacteriophage insertion site genotypes. . Appl Environ Microbiol 74:, 7447–7450. [CrossRef][PubMed]
    [Google Scholar]
  35. Whitworth J., Zhang Y., Bono J., Pleydell E., French N., Besser T.. ( 2010;). Diverse genetic markers concordantly identify bovine origin Escherichia coli O157 genotypes underrepresented in human disease. . Appl Environ Microbiol 76:, 361–365. [CrossRef][PubMed]
    [Google Scholar]
  36. Yang Z., Kovar J., Kim J., Nietfeldt J., Smith D. R., Moxley R. A., Olson M. E., Fey P. D., Benson A. K.. ( 2004;). Identification of common subpopulations of non-sorbitol-fermenting, beta-glucuronidase-negative Escherichia coli O157:H7 from bovine production environments and human clinical samples. . Appl Environ Microbiol 70:, 6846–6854. [CrossRef][PubMed]
    [Google Scholar]
  37. Yokoyama E., Hashimoto R., Etoh Y., Ichihara S., Horikawa K., Uchimura M.. ( 2011;). Biased distribution of IS629 among strains in different lineages of enterohemorrhagic Escherichia coli serovar O157. . Infect Genet Evol 11:, 78–82. [CrossRef][PubMed]
    [Google Scholar]
  38. Zhang Y. X., Laing C., Zhang Z. Z., Hallewell J., You C. P., Ziebell K., Johnson R. P., Kropinski A. M., Thomas J. E.. & other authors ( 2010;). Lineage and host source are both correlated with levels of Shiga toxin 2 production by Escherichia coli O157:H7 strains. . Appl Environ Microbiol 76:, 474–482. [CrossRef][PubMed]
    [Google Scholar]
  39. Ziebell K., Steele M., Zhang Y., Benson A., Taboada E. N., Laing C., McEwen S., Ciebin B., Johnson R., Gannon V.. ( 2008;). Genotypic characterization and prevalence of virulence factors among Canadian Escherichia coli O157:H7 strains. . Appl Environ Microbiol 74:, 4314–4323. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.083063-0
Loading
/content/journal/micro/10.1099/mic.0.083063-0
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