Prevalence, serotypes and virulence genes of Shiga toxin-producing Escherichia coli isolated from ovine and caprine milk and other dairy products in Spain

International Journal of Food Microbiology

Volumn 107, Issue 2, 2006, Pages 212-217

  Rey, J ^a   Sanchez S ^a   Blanco, J E ^b   Hermoso De Mendoza, J ^a   Hermoso De Mendoza, M ^a   Garcia A ^a   Gil, C ^a   Tejero, N ^a   Rubio, R ^a   Alonso, J M ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

Dairy products; Escherichia coli O157:H7; Milk; Serotypes; Shiga toxin producing E. coli (STEC); Virulence factors

Indexed keywords

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE TYPING; CHEESE; CONTROLLED STUDY; DAIRY PRODUCT; GENOTYPE; GOAT; MILK; NONHUMAN; PASTEURIZATION; PATHOGENIC ESCHERICHIA COLI; POLYMERASE CHAIN REACTION; PREVALENCE; SEROTYPE; SHEEP; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; SPAIN;

BACTERIA (MICROORGANISMS); CAPRA; CAPRA HIRCUS; ESCHERICHIA COLI; ESCHERICHIA COLI O157:H7; OVIS; OVIS ARIES;

EID: 33644757771     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2005.08.025     Document Type: Article

References (56)

1. R. Ahmed, C. Bopp, A. Borczyk, and S. Kasatiya Phage-typing scheme for Escherichia coli O157:H7 J. Infect. Dis. 155 1987 806 809
2. F. Allerberger, A.W. Friedrich, K. Grif, M.P. Dierich, H.-R. Dornbusch, C.J. Mache, E. Nachbaur, M. Freilinger, P. Rieck, and M. Wagner Hemolytic-uremic syndrome associated with enterohemorrhagic Escherichia coli O26:H infection and consumption of unpasteurized cow's milk Int. J. Infect. Dis. 7 2003 42 45
3. N. Banatvala, P.M. Griffin, K.D. Greene, T.J. Barrett, W.F. Bibb, J.H. Green, and J.G. Wells The United States National prospective hemolytic uremic syndrome study: microbiologic, serologic, clinical, and epidemiologic findings J. Infect. Dis. 183 2001 1063 1070
4. L. Beutin, D. Geier, H. Steinruck, S. Zimmermann, and F. Scheutz Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals J. Clin. Microbiol. 31 1993 2483 2488
5. L. Beutin, G. Krause, S. Zimmermann, S. Kaulfuss, and K. Gleier Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period J. Clin. Microbiol. 42 2004 1099 1108
6. M. Bielaszewska, J. Janda, K. Blahova, H. Minarikova, E. Jikova, M.A. Karmali, J. Laubova, J. Sikulova, M.A. Preston, R. Khakhria, H. Karch, H. Klazarova, and O. Nyc Human Escherichia coli O157:H7 infection associated with the consumption of unpasteurized goat's milk Epidemiol. Infect. 119 1997 299 305
7. C.d.W. Blackburn, L.M. Curtis, L. Humpheson, C. Billon, and P.J. McClure Development of thermal inactivation models for Salmonella enteritidis and Escherichia coli O157:H7 with temperature, pH and NaCl as controlling factors Int. J. Food Microbiol. 38 1997 31 44
8. J. Blanco, M. Blanco, J.E. Blanco, A. Mora, M.P. Alonso, E.A. González, and M.I. Bernárdez Epidemiology of verocytotoxigenic Escherichia coli (VTEC) in ruminants G. Duffy P. Garvey D. McDowell Verocytotoxigenic Escherichia coli 2001 Food and Nutrition Press Inc Trumbull, USA 113 148
9. M. Blanco, J.E. Blanco, A. Mora, J. Rey, J.M. Alonso, M. Hermoso, J. Hermoso, M.P. Alonso, G. Dahbi, E.A. Gonzalez, M.I. Bernardez, and J. Blanco Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain J. Clin. Microbiol. 41 2003 1351 1356
10. J. Blanco, M. Blanco, J.E. Blanco, A. Mora, E.A. González, M.I. Bernárdez, M.P. Alonso, A. Coira, A. Rodríguez, J. Rey, J.M. Alonso, and M.A. Usera Verotoxin producing Escherichia coli (VTEC) in Spain: prevalence, serotypes and virulence genes of O157:H7 and non-O157 VTEC in ruminants, raw beef products, and human infections Exp. Biol. Med. 228 2003 345 351
11. M. Blanco, J.E. Blanco, A. Mora, G. Dahbi, M.P. Alonso, E.A. González, M.I. Bernárdez, and J. Blanco 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-ξ) J. Clin. Microbiol. 42 2004 645 651
12. J.E. Blanco, M. Blanco, M.P. Alonso, A. Mora, G. Dahbi, M.A. Coira, and J. Blanco Serotypes, virulence genes and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from human patients: prevalence in Lugo (Spain) from 1992 through 1999 J. Clin. Microbiol. 42 2004 311 319
13. K.N. Brett, V. Ramachandran, M.A. Hornitzky, K.A. Bettelheim, M.J. Walker, and S.P. Djordjevic stx1c is the most common Shiga toxin 1 subtype among Shiga toxin-producing Escherichia coli isolates from sheep but not among isolates from cattle J. Clin. Microbiol. 41 2003 926 936
14. Centers for Disease Control Outbreak of Escherichia coli O157:H7 infection associated with eating fresh cheese curds-Wisconsin, June 1998 Jama 284 2000 2991 2992
15. P.A. Chapman, and C.A. Siddons A comparison of immunomagnetic separation and direct culture for the isolation of verocytotoxin-producing Escherichia coli O157 from cases of bloody diarrhoea, non-bloody diarrhoea and asymptomatic contacts J. Med. Microbiol. 44 1996 267 271
16. R.C. Clarke, S.A. McEwen, V.P. Gannon, H. Lior, and C.L. Gyles Isolation of verocytotoxin-producing Escherichia coli from milk filters in south-western Ontario Epidemiol. Infect. 102 1989 253 260
17. A.N. De Araujo, and L.G. Giugliano Lactoferrin and free secretory component of human milk inhibit the adhesion of enteropathogenic Escherichia coli to HeLa cells BMC Microbiol. 1 2001 25
18. M.-L. De Buyser, B. Dufour, M. Maire, and V. Lafarge Implication of milk and milk products in food-borne diseases in France and in different industrialised countries Int. J. Food Microbiol. 67 2001 1 17
19. S.P. Djordjevic, M.A. Hornitzky, G. Bailey, P. Gill, B. Vanselow, K. Walker, and K.A. Bettelheim Virulence properties and serotypes of Shiga toxin-producing Escherichia coli from healthy Australian slaughter-age sheep J. Clin. Microbiol. 39 5 2001 2017 2021
20. S.P. Djordjevic, V. Ramachandran, K.A. Bettelheim, B.A. Vanselow, P. Holst, G. Bailey, and M.A. Hornitzky Serotypes and virulence gene profiles of Shiga toxin-producing Escherichia coli strains isolated from feces of pasture-fed and lot-fed sheep Appl. Environ. Microbiol. 70 2004 3910 3917
21. T. Djuretic, P.G. Wall, and G. Nichols General outbreaks of infectious intestinal disease associated with milk and dairy products in England and Wales: 1992 to 1996 Commun. Dis. Rep. CDR Rev. 7 1997 R41 R45
22. M.S. Donnenberg, J.B. Kaper, and B.B. Finlay Interactions between enteropathogenic Escherichia coli and host epithelial cells Trends Microbiol. 5 1997 109 114
23. C.R. Dorn Hemorrhagic colitis and hemolytic uremic syndrome caused by Escherichia coli in people consuming undercooked beef and unpasteurized milk J. Am. Vet. Med. Assoc. 193 1988 1360 1361
24. M. Eklund, K. Leino, and A. Siitonen Clinical Escherichia coli strains carrying stx genes: stx variants and stx-positive virulence profiles J. Clin. Microbiol. 40 2002 4585 4593
25. E.J. Elliott, R.M. Robins-Browne, E.V. O'Loughlin, V. Bennett-Wood, J. Bourke, P. Henning, G.G. Hogg, J. Knight, H. Powell, and D. Redmond Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features Arch. Dis. Child. 85 2001 125 131
26. S. Goh, C. Newman, M. Knowles, F.J. Bolton, V. Hollyoak, S. Richards, P. Daley, D. Counter, H.R. Smith, and N. Keppie E. coli O157 phage type 21/28 outbreak in North Cumbria associated with pasteurized milk Epidemiol. Infect. 129 2002 451 457
27. P.A. Guinee, C.M. Agterberg, and W.H. Jansen Escherichia coli O antigen typing by means of a mechanized microtechnique Appl. Microbiol. 24 1972 127 131
28. I. Herrera-Insua, H.F. Gomez, V.A. Diaz-Gonzalez, P. Chaturvedi, D.S. Newburg, and T.G. Cleary Human milk lipids bind Shiga toxin Adv. Exp. Med. Biol. 501 2001 333 339
29. A.E. Heuvelink, B. Bleumink, F.L. van den Biggelaar, M.C. Te Giffel, R.R. Beumer, and E. de Boer Occurrence and survival of verocytotoxin-producing Escherichia coli O157 in raw cow's milk in The Netherlands J. Food Prot. 61 1998 1597 1601
30. S.C. Ingham, Y.C. Su, and D.S. Spangenberg Survival of Salmonella typhimurium and Escherichia coli O157:H7 in cheese brines Int. J. Food Microbiol. 61 2000 73 79
31. A.E. Jerse, J. Yu, B.D. Tall, and J.B. Kaper A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells Proc. Natl. Acad. Sci. U. S. A. 87 1990 7839 7843
32. M.A. Karmali Infection by verocytotoxin-producing Escherichia coli Clin. Microbiol. Rev. 2 1989 15 38
33. W.E. Keene, K. Hedberg, D.E. Herriott, D.D. Hancock, R.W. McKay, T.J. Barrett, and D.W. Fleming A prolonged outbreak of Escherichia coli O157:H7 infections caused by commercially distributed raw milk J. Infect. Dis. 176 1997 815 818
34. R. Khakhria, D. Duck, and H. Lior Extended phage-typing scheme for Escherichia coli O157:H7 Epidemiol. Infect. 105 1990 511 520
35. H. Klie, M. Timm, H. Richter, P. Gallien, K.W. Perlberg, and H. Steinruck [Detection and occurrence of verotoxin-forming and/or shigatoxin producing Escherichia coli (VTEC and/or STEC) in milk] Berl Munch Tierarztl Wochenschr 110 1997 337 341
36. R.G. Leuschner, and M.P. Boughtflower Laboratory-scale preparation of soft cheese artificially contaminated with low levels of Escherichia coli O157, Listeria monocytogenes, and Salmonella enterica serovars Typhimurium, Enteritidis, and Dublin J. Food Prot. 65 2002 508 514
37. J. Lin, M.P. Smith, K.C. Chapin, H.S. Baik, G.N. Bennett, and J.W. Foster Mechanisms of acid resistance in enterohemorrhagic Escherichia coli Appl. Environ. Microbiol. 62 1996 3094 3100
38. M.M. Maher, K.N. Jordan, M.E. Upton, and A. Coffey Growth and survival of E. coli O157:H7 during the manufacture and ripening of a smear-ripened cheese produced from raw milk J. Appl. Microbiol. 90 2001 201 207
39. S. Massa, E. Goffredo, C. Altieri, and K. Natola Fate of Escherichia coli O157:H7 in unpasteurized milk stored at 8 degrees C Lett. Appl. Microbiol. 28 1999 89 92
40. L. McIntyre, J. Fung, A. Paccagnella, J. Isaac-Renton, F. Rockwell, B. Emerson, and T. Preston Escherichia coli O157 outbreak associated with the ingestion of unpasteurized goat's milk in British Columbia, 2001 Can. Commun. Dis. Rep. 28 2002 6 8
41. D. Morgan, C.P. Newman, D.N. Hutchinson, A.M. Walker, B. Rowe, and F. Majid Verotoxin producing Escherichia coli O 157 infections associated with the consumption of yoghurt Epidemiol. Infect. 111 1993 181 187
42. D.S. Newburg, S. Ashkenazi, and T.G. Cleary Human milk contains the Shiga toxin and Shiga-like toxin receptor glycolipid Gb3 J. Infect. Dis. 166 1992 832 836
43. J.C. Paton, and A.W. Paton Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections Clin. Microbiol. Rev. 11 1998 450 479
44. R.G. Pebody, C. Furtado, A. Rojas, N. McCarthy, G. Nylen, P. Ruutu, T. Leino, R. Chalmers, B. de Jong, M. Donnelly, I. Fisher, C. Gilham, L. Graverson, T. Cheasty, G. Willshaw, M. Navarro, R. Salmon, P. Leinikki, P. Wall, and C. Bartlett An international outbreak of Vero cytotoxin-producing Escherichia coli O157 infection amongst tourists; a challenge for the European infectious disease surveillance network Epidemiol. Infect. 123 1999 217 223
45. D. Pierard, L. Van Damme, L. Moriau, D. Stevens, and S. Lauwers Virulence factors of verocytotoxin-producing Escherichia coli isolated from raw meats Appl. Environ. Microbiol. 63 1997 4585 4587
46. F. Pirro, L.H. Wieler, K. Failing, R. Bauerfeind, and G. Baljer Neutralizing antibodies against Shiga-like toxins from Escherichia coli in colostra and sera of cattle Vet. Microbiol. 43 1995 131 141
47. G. Prats, C. Frías, N. Margall, T. Llovet, L. Gaztelurrutia, R. Elcuaz, A. Canut, R.M. Bartolomé, L. Torroba, Y. Dorronsoro, J. Blanco, M. Blanco, N. Rabella, P. Coll, and B. Mirellis Colitis hemorrágica por Escherichia coli verotoxigénica. Presentación de 9 casos Enferm. Infecc. Microbiol. Clin. 14 1996 7 15
48. J. Rey, J.E. Blanco, M. Blanco, A. Mora, G. Dahbi, J.M. Alonso, M. Hermoso, J. Hermoso, M.P. Alonso, M.A. Usera, E.A. Gonzalez, M.I. Bernardez, and J. Blanco Serotypes, phage types and virulence genes of shiga-producing Escherichia coli isolated from sheep in Spain Vet. Microbiol. 94 2003 47 56
49. S. Rubini, G. Cardeti, S. Amiti, G. Manna, R. Onorati, A. Caprioli, and S. Morabito Verocytotoxin-producing Escherichia coli O157 in sheep milk Vet. Rec. 144 1999 56
50. H. Russmann, E. Kothe, H. Schmidt, S. Franke, D. Harmsen, A. Caprioli, and H. Karch Genotyping of Shiga-like toxin genes in non-O157 Escherichia coli strains associated with haemolytic uraemic syndrome J. Med. Microbiol. 42 1995 404 410
51. H. Schmidt, L. Beutin, and H. Karch Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933 Infect. Immun. 63 1995 1055 1061
52. L. Slutsker, A.A. Ries, K.D. Greene, J.G. Wells, L. Hutwagner, and P.M. Griffin Escherichia coli O157:H7 diarrhea in the United States: clinical and epidemiologic features Ann. Intern. Med. 126 1997 505 513
53. R.C. Sprong, M.F.E. Hulstein, and R. van der Meer Bovine milk fat components inhibit food-borne pathogens Int. Dairy J. 12 2002 209 215
54. M.P. Vettorato, L. Leomil, B.E. Guth, K. Irino, and A.F. Pestana de Castro Properties of Shiga toxin-producing Escherichia coli (STEC) isolates from sheep in the State of Sao Paulo, Brazil Vet. Microbiol. 95 2003 103 109
55. S. Watarai, K. Inoue, Y. Kushi, E. Isogai, K. Yokota, K. Naka, K. Oguma, and H. Kodama Inhibition of Vero cell cytotoxic activity in Escherichia coli O157:H7 lysates by globotriaosylceramide, Gb3, from bovine milk Biosci. Biotechnol. Biochem. 65 2001 414 419
56. C. Zweifel, J.E. Blanco, M. Blanco, J. Blanco, and R. Stephan Serotypes and virulence genes of ovine non-O157 Shiga toxin-producing Escherichia coli in Switzerland Int. J. Food Microbiol. 95 2004 19 27