The prevalence, distribution and characterization of Shiga toxin-producing Escherichia coli (STEC) serotypes and virulotypes from a cluster of bovine farms

Journal of Applied Microbiology

Volumn 113, Issue 5, 2012, Pages 1238-1248

  Ennis, C ^a   McDowell, D ^b   Bolton, D J ^a  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Beef; Serotypes; Shiga toxin producing Escherichia coli; STEC; Virulence factors; Virulotypes

Indexed keywords

BEEF; ESCHERICHIA COLI; GENES; PUBLIC HEALTH;

ANTIBIOTICS RESISTANCE; ENRICHMENT CULTURE; ESCHERICHIA COLI O157; IMMUNOMAGNETIC SEPARATION; IRELAND; SEROTYPES; SHIGA TOXIN-PRODUCING ESCHERICHIA COLI; VIRULENCE FACTORS; VIRULOTYPE;

ANTIBIOTICS;

OLIGONUCLEOTIDE; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; CATTLE; COLIFORM BACTERIUM; DISEASE PREVALENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PUBLIC HEALTH; TOXIN; VIRULENCE;

ANIMAL EXPERIMENT; ANTIBIOTIC SENSITIVITY; ARTICLE; COW; IMMUNOMAGNETIC SEPARATION; INCIDENCE; IRELAND; MULTIDRUG RESISTANCE; NONHUMAN; PREVALENCE; SCREENING TEST; SEROTYPE; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; VIRULOTYPE;

IRELAND;

BOVINAE; ESCHERICHIA COLI;

EID: 84867733730     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2012.05421.x     Document Type: Article

References (73)

1. Aidar-Ugrinovich, L., Blanco, J., Blanco, M., Blanco, J.E., Leomil, L., Dahbi, G., Mora, A., Onuma, D.L. et al. (2007) Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in São Paulo, Brazil. Int J Food Microbiol 115, 297-306.
2. Anon (2011) Shiga toxin/verotoxin-producing Escherichia coli in humans, food and animals in the EU/EEA, with special reference to the German outbreak strain STEC O104. Technical Report by the European Centre for Disease Prevention and Control and the European Food Safety Authority, Stockholm, Sweden.
3. Ateba, C.N. and Bezuidenhout, C.C. (2008) Review: characterisation of Escherichia coli O157 strains from human, cattle and pigs in the North-West Province, South Africa. Int J Food Microbiol 128, 181-188.
4. Avery, L.M., Hill, P., Killham, K. and Jones, D.L. (2004) Escherichia coli O157 survival following the surface and sub-surface application of human pathogen contaminated organic waste to soil. Soil Biol Biochem 36, 2101-2103.
5. von Baum, H. and Marre, R. (2005) Review: antimicrobial resistance of Escherichia coli and therapeutic implications. Int J Med Microbiol 295, 503-511.
6. Bell, B.P., Goldoft, M., Griffin, P.M., Davis, M., Gordon, D.C., Tarr, P.L., Bartleson, C.A., Lewis, J.H. et al. (1994) A multistate outbreak of Escherichia coli O157:H7- associated bloody diarrhoea and haemolytic uraemic syndrome from hamburgers. The Washington experience. J Am Vet Med Assoc 272, 1349-1353.
7. Besser, T.E., Richards, B.L., Rice, D.H. and Hancock, D.D. (2001) Escherichia coli O157:H7 infection of calves: infectious dose and direct contact transmission. Epidemiol Infect 127, 555-560.
8. Bettelheim, K.A., Hornitzky, M.A., Djordjevic, S.T. and Kuzevski, A. (2003) Antibiotic resistance among verocytotoxigenic Escherichia coli (VTEC) and non-VTEC isolated from domestic animals and humans. J Med Microbiol 52, 155-162.
9. Beutin, L., Wang, Q., Naumann, D., Han, W., Krause, G., Leomil, L., Wang, L. and Feng, L. (2007) Relationship between O-antigen subtypes, bacterial surface structures and O-antigen gene clusters in Escherichia coli O123 strains carrying genes for shiga toxins and intimin. J Med Microbiol 56, 177-184.
10. Blanco, M., Blanco, J.E., Mora, A., Dahbi, G., Alonso, M.P., González, E.A., Bernárdez, M.I. and Blanco, J. (2004) Serotypes, virulence genes and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from cattle in Spain: identification of a new intimin variant gene (eae-ε). J Clin Microbiol 42, 645-651.
11. Boerlin, P., McEwen, S.A., Boerlin-Petzoid, F., Wilson, J.B., Johnson, R.P. and Gyles, C.L. (1999) Associations between virulence factors of shiga toxin-producing Escherichia coli and disease in humans. J Clin Microbiol 37, 497-503.
12. Bolton, D.J. (2011) Verocytotoxigenic (shiga toxin-producing) Escherichia coli: virulence factors and pathogenicity in the farm to fork paradigm. Foodborne Pathog Dis 8, 357-365.
13. Bosilevac, J.M. and Koohmaraie, M. (2011) Prevalence and characterisation of non-O157 shiga toxin-producing Escherichia coli isolated from commercial ground beef in the United States. Appl Environ Microbiol 77, 2103-2112.
14. Brunder, W., Schmidt, H. and Karch, H. (1996) KatP, a novel catalase-peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 142, 3305-3315.
15. Caprioli, A., Morabito, S., Brugreb, H. and Oswald, E. (2005) Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 36, 286-311.
16. CLSI (2008) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated form animals; Approved Standard- Third Edition. CLSI Document M31-A3.
17. Cobbold, R. and Desmarchelier, P. (2001) Characterisation and clonal relationships of Shiga-toxigenic Escherichia coli (STEC) isolated from Australian dairy cattle. Vet Microbiol 79, 323-335.
18. Cooley, M., Carychao, D., Crawford-Miksza, L., Jay, M.T., Myers, C., Rose, C., Keys, C., Farrar, J. et al. (2007) Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California. PLoS ONE 2, E1159.
19. Dundas, S., Andrew Todd, W.T., Stewart, A.I., Murdoch, P.S., Chaudhuri, A.K.R. and Hutchinson, S.J. (2001) The central Scotland Escherichia coli O157:H7 outbreak: risk factors for the haemolytic uremic syndrome and death among hospitalized patients. Clin Infect Dis 33, 923-931.
20. European Food Safety Authority (EFSA) (2012) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA Journal 2012; 10(3):2597. [442 pp.] doi:10.2903/j.efsa.2012.2597. Available online: www.efsa.europa.eu/efsajournal.
21. Farina, C., Goglio, A., Conedera, G., Minelli, F. and Caprioli, A. (1996) Antimicrobial susceptibility of Escherichia coli O157 and other enterohemorrhagic Escherichia coli isolated in Italy. Eur J Clin Microbiol Infect Dis 15, 351-353.
22. Feng, P., Weagant, S.D. and Monday, S.R. (2001) Genetic analysis for virulence factors in Escherichia coli O104:H21 that was implicated in an outbreak of hemorrhagic colitis. J Clin Microbiol 39, 24-28.
23. Fratamico, P.M., Yan, X., Caprioli, A., Esposito, G., Needleman, D.S., Pepe, T., Tozzoli, R., Cortesi, M.L. et al. (2011) The complete DNA sequence and analysis of the virulence plasmid and of five additional plasmids carried by Shiga toxin-producing Escherichia coli O26:H11 strain H30. Int J Med Microbiol 301, 192-203.
24. Friedrich, A.W., Bielaszewska, M., Zhang, W.L., Pulz, M., Kuczius, T., Ammon, A. and Karch, H. (2002) Escherichia coli harbouring shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis 185, 74-84.
25. Fukushima, H. and Seki, R. (2004) High numbers of Shiga toxin-producing Escherichia coli found in bovine faeces collected at slaughter in Japan. FEMS Microbiol Lett 238, 189-197.
26. Fukuyama, M., Furuhata, K., Oonaka, K., Yakiwara, R., Koizumi, T., Hara, M., Dogasaki, C., Shimada, T. et al. (2003) Isolation and serotyping of verotoxin-producing Escherichia coli (VTEC) from pig. Kansenshogaku Zasshi 77, 1032-1039.
27. Fukuyama, M., Oonaka, K., Furuhata, K., Hara, M. and Nakazawa, M. (2005) Drug sensitivity of verotoxin-producing Escherichia coli O157:H7. Kansenshogaku Zasshi 79, 451-456.
28. Giammanco, G.M., Pignato, S., Grimont, F.P.A.D., Caprioli, A., Morabito, S. and Giammanco, G. (2002) Characterization of shiga toxin-producing E. coli O157:H7 isolated in Italy and in France. J Clin Microbiol 40, 4619-4624.
29. Golding, S.S. and Matthews, K.R. (2004) Intrinsic mechanism decreases susceptibility of E. coli to multiple antibiotics. J Food Prot 67, 34-39.
30. Griffin, P.M. and Tauxe, R.V. (1991) The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated haemolytic uremic syndrome. Epidemiol Rev 13, 60-98.
31. Gyles, C.L. (2007) Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 85, E45-E62.
32. Hussein, H.S. (2007) Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J Anim Sci 85, E63-E72.
33. Jenkins, C., Pearce, M.C., Chart, H., Cheasty, T., Willshaw, G.A., Gunn, G.J., Dougan, G., Smith, H.R. et al. (2002) An eight-month study of a population of verocytotoxigenic Escherichia coli (VTEC) in a Scottish cattle herd. J Appl Microbiol 93, 944-953.
34. Jenkins, C., Perry, N.T., Cheasty, T., Shaw, D.J., Frankel, G., Dougan, G., Smith, H.R., Paton, A.W. et al. (2003) Distribution of the saa gene in strains of Shiga toxin-producing Escherichia coli of human and bovine origins. J Clin Microbiol 41, 1775-1778.
35. Karmali, M.A., Mascarenhas, M., Shen, S., Ziebel, K., Johnson, S., Reid-Smith, R., Isaac-Renton, J., Clark, C. et al. (2003) Association of genomic O island 122 of Escherichia coli EDL 933 with verocytotoxin-producing Escherichia coli seropathotypes that are linked to epidemic and/or serious disease. J Clin Microbiol 41, 4930-4940.
36. Kleanthous, H., Smith, H.R., Scotland, S.M., Gross, R.J., Rowe, B., Taylor, C.M. and Milford, D.V. (1990) Haemolytic uraemic syndromes in the British Isles, 1985-8: association with Verocytotoxin producing Escherichia coli. Part 2: microbiological aspects. Arch Dis Child 65, 722-727.
37. Klein, G. and Bülte, M. (2003) Antibiotic susceptibility pattern of Escherichia coli strains with verocytotoxigenic E. coli-associated virulence factors from food and animal faeces. Food Microbiol 20, 27-33.
38. Kobayashi, H., Shimada, J., Nakazawa, M., Morozumi, T., Pohjanvirta, T., Pelkonen, S. and Yamamoto, K. (2001) Prevalence and characteristics of shiga toxin-producing Escherichia coli from healthy cattle in Japan. Appl Environ Microbiol 67, 484-489.
39. Kumar, H.S., Karunasaga, I., Karunasaga, I., Teizou, T., Shima, K. and Yamasaki, S. (2004) Characterization of shiga toxin producing Escherichia coli (STEC) isolated from seafood and beef. FEMS Microbiol Lett 233, 173-178.
40. Machado, J., Grimont, F. and Grimont, P.A.D. (2000) Identification of Escherichia coli flagellar types by restriction of the amplified fliC gene. Res Microbiol 151, 535-546.
41. McNally, A., Roe, A.J., Simpson, S., Thomson-Carter, F.M., Hoey, D.E.E., Currie, C., Chakraborty, T., Smith, D.G.E. et al. (2001) Differences in levels of secreted locus of enterocyte effacement proteins between human disease-associated and bovine Escherichia coli O157. Infect Immun 69, 5107-5114.
42. Meng, J., Zhao, S., Doyle, M. and Joseph, S.W. (1998) Antibiotic resistance of Escherichia coli O157:H7 and O157:NM isolated from animals, food and humans. J Food Prot 61, 1511-1514.
43. Monaghan, Á., Byrne, B., Fanning, S., Sweeney, T., McDowell, D. and Bolton, D.J. (2011) Serotypes and virulence profiles of beef and dairy farm non-O157 verocytotoxigenic Escherichia coli (VTEC). Appl Environ Microbiol 77, 8662-8668.
44. Mora, A., Blanco, J.E., Blanco, M., Alonso, M.P., Dhabi, G., Echeita, A., Gonzalez, E.A., Bernardez, M.I. et al. (2005) Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain. Res Microbiol 156, 793-806.
45. Murakami, J., Kishi, K., Hirai, K., Hiramatsu, K., Yamasaki, T. and Nasu, M. (2000) Macrolides and clindamycin suppress the release of shiga-like toxins for Escherichia coli O157:H7 in vitro. Int J Antimicrob Agents 15, 103-109.
46. Nataro, J.P. and Kaper, J.B. (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142-201.
47. Nielsen, E.M., Skov, M.N., Madsen, J.J., Lodal, J., Jespersen, J.B. and Baggesen, D.L. (2004) Verocytotoxin-producing Escherichia coli in wild birds and rodents in close proximity to farms. Appl Environ Microbiol 70, 6944-6947.
48. Paton, A.W. and Paton, J.C. (1998) Detection and characterization of shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfb (O111), and rfb (O157). J Clin Microbiol 36, 598-602.
49. Paton, A.W. and Paton, J.C. (2002) Direct detection and characterization of shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA and saa. J Clin Microbiol 40, 271-274.
50. Paton, A.W., Woodrow, M.C., Doyle, R.M., Lanser, J.A. and Paton, J.C. (1999) Molecular characterization of a Shiga toxigenic Escherichia coli O113:H21 strain lacking eae responsible for a cluster of cases of haemolytic-uremic syndrome. J Clin Microbiol 37, 3357-3361.
51. Paton, A.W., Srimanote, P., Woodrow, M.C. and 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.
52. Pearce, M.C., Evans, J., McKendrick, I.J., Smith, A.W., Knight, H.I., Mellor, D.J., Woolhouse, M.E.J., Gunn, G.J. et al. (2006) Prevalence and virulence factors of Escherichia coli serogroups O26, O103, O111 and O145 shed by cattle in Scotland. Appl Environ Microbiol 72, 653-659.
53. Pennington, H. (2010) Review: Escherichia coli O157. Lancet, 365, 1073-1086.
54. Poole, K. (2004) Efflux-mediated multiresistance in Gram-negative bacteria. Clin Microbiol Infect 10, 12-26.
55. Pradel, N., Livrelli, V., De Champs, C., Palcoux, J.B., Reynaud, A., Scheutz, F., Sirot, J., Joly, B. et al. (2000) Prevalence and characterization of shiga toxin-producing Escherichia coli isolated from cattle, food and children during a one-year prospective study in France. J Clin Microbiol 38, 1023-1031.
56. Ramachandran, V., Brett, K., Hornizky, M.A., Dowton, M., Bettelheim, K.A., Walker, M.J. and Djorjevic, S.P. (2003) Distribution of intimin subtypes among Escherichia coli isolates from ruminant and human sources. J Clin Microbiol 41, 5022-5032.
57. Riley, L.W., Remis, R.S., Helgerson, S.D., McGee, H.B., Wells, J.G., Davis, B.R., Hebert, R.J., Olcott, E.S. et al. (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308, 681-685.
58. Sargeant, J.M., Sanderson, M.W., Griffin, D.D. and Smith, R.A. (2004) Factors associated with the presence of Escherichia coli O157 in feedlot-cattle water and feed in Midwestern USA. Prev Vet Med 66, 207-237.
59. Schmidt, H., Rüssmann, H., Schwarzkopf, A., Aleksic, S., Heesemann, J. and Karch, H. (1994) Prevalence of attaching and effacing Escherichia coli in stool samples from patients and controls. Zentralbl Bakteriol 281, 201-213.
60. Schmidt, H., Henkel, B. and Karch, H. (1997) A gene cluster closely related to type II secretion pathway operons of gram-negative bacteria is located on the large plasmid of enterohemorrhagic Escherichia coli O157 strains. FEMS Microbiol Lett 148, 265-272.
61. Schmidt, H., Zhang, W.L., Hemmrich, U., Jelacic, S., Brunder, W., Tarr, P.I., Dobrindt, U., Hacker, J. and 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.
62. Schroeder, C.M., Meng, J., Zhao, S., DebRoy, C., Torcolini, J., Zhao, C., McDermott, P.F., Wagner, D.D. et al. (2002) Antimicrobial resistance of Escherichia coli O26, O103, O111, O128 and O145 from animals and humans. Emerg Infect Dis 8, 1409-1414.
63. Scott, L., McGee, P., Walsh, C., Fanning, S., Sweeney, T., Blanco, J., Karczmarczyk, M., Earley, B. et al. (2009) Detection of numerous verocytotoxigenic E. coli serotypes, with multiple antibiotic resistance from cattle faeces and soil. Vet Microbiol 134, 288-293.
64. Shiomi, M., Togawa, M., Fujita, K. and Murata, R. (1999) Effect of early oral fluoroquinolones in hemorrhagic colitis due to E. coli O157:H7. Pediatr Int 41, 228-232.
65. Singh, R., Schroeder, C.M., Meng, J., White, D.G., McDermott, P.F., Wagner, D.D., Yang, H., Simjee, S. et al. (2005) Identification of antimicrobial resistance and class 1 integrons in Shiga toxin-producing Escherichia coli recovered from humans and food animals. J Antimicrob Chemother 56, 216-219.
66. Stephan, R. and Schumacher, S. (2001) Resistance patterns of non-O157 Shiga toxin-producing Escherichia coli (STEC) strains isolated from animals, food and asymptomatic human carriers in Switzerland. Lett Appl Microbiol 32, 114-117.
67. Szalo, I.M., Goffaux, F., Pirson, V., Pierard, D., Ball, H. and Mainil, J. (2002) Presence in bovine enteropathogenic (EPEC) and enterohaemorrhagic (EHEC) Escherichia coli of genes encoding for putative virulence adhesins of human EHEC strains. Res Microbiol 153, 653-658.
68. Tarr, C.L., Large, T.M., Moeller, C.L., Lacher, D.W., Tarr, P.I., Acheson, D.W. and Whittam, T.S. (2002) Molecular characterization of a serotype O121:H19, clone, a distinct shiga toxin-producing clone of pathogenic Escherichia coli. Infect Immun 70, 6853-6859.
69. Threlfall, E.J., Ward, L.R., Frost, J.A. and Willshaw, G.A. (2000) The emergence and spread of antibiotic resistance in food-borne bacteria. Int J Food Microbiol 62, 1-5.
70. Toma, C., Martinez, E.E., Song, T., Miliwebsky, E., Chinen, I., Iyoda, S., Iwanaga, M. and Rivas, M. (2004) Distribution of putative adhesins in different seropathotypes of Shiga toxin-producing Escherichia coli. J Clin Microbiol 42, 4937-4946.
71. Walsh, C., Duffy, G., O'Mahony, R., Fanning, S., Blair, I.S. and McDowell, D.A. (2006) Antimicrobial resistance in Irish isolates of verocytotoxigenic Escherichia coli (E. coli)-VTEC. Int J Food Microbiol 109, 173-178.
72. Zhao, T., Zhao, P., West, J.W., Bernard, J.K., Cross, H.G. and Doyle, M.P. (2006) Inactivation of enterhemorrhagic Escherichia coli in rumen content- or feces- contaminated drinking water for cattle. Appl Environ Microbiol 72, 3268-3273.
73. Zweifel, C., Schumacher, S., Blanco, M., Blanco, J.E., Tasara, T., Blanco, J. and Stephan, R. (2005) Phenotypic and genotypic characteristics of non-O157 Shiga toxin-producing Escherichia coli (STEC) from Swiss cattle. Vet Microbiol 105, 37-45.