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

Experimental Biology and Medicine

Volumn 228, Issue 4, 2003, Pages 345-351

  Blanco, Jorge ^a   Blanco, Miguel ^a   Blanco, Jesus E ^a   Mora, Azucena ^a   Gonzalez, Enrique A ^a   Bernardez, Maria I ^a   Alonso, Maria P ^a,b   Coira, Amparo ^b   Rodriguez, Asuncion ^b   Rey, Joaquin ^c   Alonso, Juan M ^c   Usera, Miguel A ^d  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b HOSPITAL XERAL CALDE   (Spain)

^c UNIVERSITY OF EXTREMADURA   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Cytotoxicity; Escherichia coli; Food safety; Food borne pathogens; Verotoxins

Indexed keywords

INTIMIN; VIRULENCE FACTOR; SHIGA TOXIN;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BEEF CATTLE; BOVIDS; CATTLE; DISEASE ASSOCIATION; DISEASE CARRIER; EAE GENE; ESCHERICHIA COLI; ESCHERICHIA COLI O105; ESCHERICHIA COLI O111; ESCHERICHIA COLI O113; ESCHERICHIA COLI O157; ESCHERICHIA COLI O171; ESCHERICHIA COLI O20; ESCHERICHIA COLI O22; ESCHERICHIA COLI O26; ESCHERICHIA COLI O77; FOOD CONTAMINATION; FOOD POISONING; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; HUMAN; INTESTINE MUCOSA; MEAT INDUSTRY; NON O157 VEROTOXIN PRODUCING ESCHERICHIA COLI; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PREVALENCE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEROTYPE; SEROTYPING; SHEEP; SPAIN; STRAIN IDENTIFICATION; TOXIN ANALYSIS; ANIMAL; BIOSYNTHESIS; ENTEROBACTER INFECTION; EPIDEMIC; GENETICS; GOAT; ISOLATION AND PURIFICATION; MEAT; METABOLISM; MICROBIOLOGY; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); BOS TAURUS; BOVIDAE; BOVINAE; ESCHERICHIA COLI; NEGIBACTERIA; OVIS; OVIS ARIES;

ANIMALS; CATTLE; DISEASE OUTBREAKS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FOOD POISONING; GENES, BACTERIAL; GOATS; HUMANS; MEAT; PREVALENCE; SHEEP; SHIGA TOXINS; SPAIN; VIRULENCE;

EID: 0037762687     PISSN: 15353702     EISSN: None     Source Type: Journal    
DOI: 10.1177/153537020322800403     Document Type: Article

References (67)

1. Doyle MP, Zhao T, Meng J, Zhao S. Escherichia coli O157:H7. In: Doyle MD, Beuchat LR, Montville TJ, Eds. Food Microbiology, Fundamentals and Frontiers. Washington, DC: ASM Press, pp171-191, 1997.
2. Johnson RP, Wilson JB, Michel P, Rahn K, Renwick SA, Gyles CL, Spika JS. Human infection with verocytotoxigenic Escherichia coli associated with exposure to farms and rural environments. In: Stewart CS, Flint HJ, Eds. Escherichia coli O157 in Farm Animals. Wallingford, UK: CABI Publishing, pp147-168, 1999.
3. Konowalchuk J, Speirs JL, Stavric S. Vero response to a cytotoxin of Escherichia coli. Infect Immun 18:775-779, 1977.
4. ÓBrien AD, LaVeck GD, Thompson MR, Formal SB. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli. J Infect Dis 146:763-769, 1982.
5. Schmidt H, Beutin L, Karch H. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect Immun 66:1055-1061, 1995.
6. Oswald E, Schmidt H, Morabito S, Karch H, Marchès O, Caprioli A. Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect Immun 68:64-71, 2000.
7. World Health Organization. Zoonotic non-O157 shiga toxin-producing Escherichia coli (STEC). Report of a WHO Scientific Working Group Meeting, Berlin, Germany. http://www.who.int/emc-documents/zoonoses/whocsraph988c.htm, 1998.
8. Bettelheim KA. Serotypes of verotoxin-producing Escherichia coli reported in the literature apart from those belonging to serogroup O157. http://www.sciencenet.com.au/bacteriologyhome.htm, 2000.
9. Blanco J, Blanco M, Blanco JE, Mora A, Alonso MP, González EA, Bernárdez MI. O:H serotypes of human verocytotoxigenic E. coli. http://www.lugo.usc.es/ecoli/SEROTIPOSHUM.htm, 2001.
10. Blanco J, Blanco M, Blanco JE, Mora A, Alonso MP, González EA, Bernárdez MI. Epidemiology of verocytotoxigenic Escherichia coli (VTEC) in ruminants. In: Duffy G, Garvey P, McDowell DA, Eds. Verocytotoxigenic E. coli. Trumbull, CT: Food and Nutrition Press, pp113-148, 2001.
11. Beutin L. Escherichia coli O157 and other types of verocytotoxigenic E. coli (VTEC) isolated from humans, animals and food in Germany. In: Stewart CS, Flint HJ, Eds. Escherichia coli O157 in Farm Animals. Wallingford, UK: CABI Publishing, pp121-145, 1999.
12. Boerlin P, McEwen SA, Boerlin-Petzold F, Wilson JB, Johnson RP, Gyles CL. Associations between virulence factors of shiga toxin-producing Escherichia coli and disease in humans. J Clin Microbiol 37:497-503, 1999.
13. Paton AW, Woodrow MC, Doyle RM, Lanser JA, Paton JC. 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, 1999.
14. Blanco M, Blanco JE, Blanco J, González EA, Alonso MP, Mass H, Jansen WH. Prevalence and characteristics of human and bovine vero-toxigenic Escherichia coli strains isolated in Galicia (north-western Spain). Eur J Epidemiol 12:13-19, 1996.
15. Blanco M, Blanco JE, Blanco J, González EA, Mora A, Prado C, Fernández L, Rio M, Ramos J, Alonso MP. Prevalence and characteristics of Escherichia coli serotype O157:H7 and other verotoxin-producing E. coli in healthy cattle. Epidemiol Infect 117:251-257, 1996.
16. Blanco M, Blanco JE, Blanco J, Mora A, Prado C, Alonso MP, Mouriño M, Madrid C, Balsalobre C, Juárez A. Distribution and characterization of faecal verotoxin-producing Escherichia coli (VTEC) isolated from healthy cattle. Vet Microbiol 54:309-319, 1997.
17. Blanco M, Blanco JE, Mora A, González EA, Blanco J. Serotypes and virulence genes of verocytotoxigenic E. coli (VTEC) isolated from cattle in Spain. In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 3: Pathogenicity and Virulence of Verocytotoxigenic E. coli, Concerted Action CT98-3935. Dublin, UK: The National Food Centre, p183, 2000.
18. Heuvelink AE, Van Den Biggelaar FLAM, Zwartkruis-Nahuis JTM, Herbes RG, Huyben R, Nagelkerke N, Melchers WJG, Monnens LAH, De Boer E. Occurrence of verocytotoxin-producing Escherichia coli O157 on Dutch dairy farms. J Clin Microbiol 36:3480-3487, 1998.
19. Bonardi S, Maggi E, Bottarelli A, Pacciarin ML, Ansuini A, Vellini G, Morabito S, Caprioli A. Isolation of verocytotoxin-producing Escherichia coli O157:H7 from cattle at slaughter in Italy. Vet Microbiol 67:203-211, 1999.
20. De Zutter L, Uradzinski J, Pierard D. Prevalence of enterohemorrhagic E. coli O157 in Belgian slaughter cattle. Abstracts of the Second International Symposium of the European Study Group on Enterohemorrhagic Escherichia coli. Acta Clin Bel 54:48, 1999.
21. Eriksson E, Engvall A, Gunnarsson A. Effects of pooling of samples and cold storage of pre-enrichment broth on sensitivity for detecting E. coli O157 in cattle faeces. In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 1: Methods for Verocytotoxigenic E. coli, Concerted Action CT98-3935. Dublin, UK: The National Food Centre, pp36-40, 1999.
22. Cizek A, Alexa P, Smola J. Shiga toxin-producing Escherichia coli O157 in feedlot cattle and rats from a large-scale farm. Abstracts of the Second International Symposium of the European Study Group on Enterohemorrhagic Escherichia coli. Acta Clin Bel 54:47, 1999.
23. Synge BA, Hopkins GF. Studies of verocytotoxigenic E. coli O157 in cattle in Scotland and association with human cases. In: Karmali MA, Goglio AG, Eds. Recent Advances in Verocytotoxin-Producing Escherichia coli Infections. New York: Elsevier Science, pp65-68, 1994.
24. Chapman PA, Siddons CA, Cerdan Malo AT, Harkin MA. A 1-year study of Escherichia coli O157 in cattle, sheep, pigs and poultry. Epidemiol Infect 119:245-250, 1997.
25. Sanderson MW, Gay JM, Hancock DD, Gay CC, Fox LK, Besser TE. Sensitivity of bacteriologic culture for detection of Escherichia coli O157:H7 in bovine feces. J Clin Microbiol 33:2616-2619, 1995.
26. Laegreid WW, Elder RO, Keen JE. Prevalence of Escherichia coli O157:H7 in range beef calves at weaning. Epidemiol Infect 123:291-298, 1999.
27. Van Donkersgoed J, Graham T, Gannon V. The prevalence of verotoxins, Escherichia coli O157, and Salmonella in the feces and rumen of cattle at processing. Can Vet J 40:332-338, 1999.
28. Hoyle B. Renewed concerns over E. coli O157:H7 in ground beef. ASM News 66:331-332, 2000.
29. Mainil J. Shiga/verocytotoxins and Shiga/verotoxigenic Escherichia coli in animals. Vet Res 30:235-257, 1999.
30. Rey J, Alonso JM, Blanco JE, Blanco M, Mora A, González EA, Blanco J. Serotypes and virulence genes of verocytotoxigenic E. coli (VTEC) isolated from sheep in Spain. In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 3: Pathogenicity and Virulence of Verocytotoxigenic E. coli, Concerted Action CT98-3935. Dublin, UK: The National Food Centre, p 185, 2000.
31. Beutin L, Geier D, Steinrück H, Zimmermann S, Scheutz F. Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals. J Clin Microbiol 31:2483-2488, 1993.
32. Bastian S, Carle I, Grimont F, Grimont PAD. Diversity of shiga toxin producing E. coli in herds of dairy cows and goats. Abstracts of the Second International Symposium of the European Study Group on Enterohemorrhagic Escherichia coli. Acta Clin Bel 54:49, 1999.
33. Sidjabat-Tambunan H, Bensink JC. Verotoxin-producing Escherichia coli from the faeces of sheep, calves and pigs. Aust Vet J 75:292-293, 1997.
34. Fagan PK, Hornitzky MA, Bettelheim KA, Djordjevic SP. Detection of shiga-like toxin (stx1 and stx2), intimin (eaeA), and enterohemorrhagic Escherichia coli (EHEC) hemolysin (EHEC hlyA) genes in animal feces by multiplex PCR. Appl Environ Microbiol 65:868-872, 1999.
35. Djordjevic SP, Hornitzky MA, Bailey G, Gill P, Vanselow B, Walker K, Bettelheim KA. Virulence properties and serotypes of Shiga toxin-producing Escherichia coli from healthy Australian slaughter-age sheep. J Clin Microbiol 39:2017-2021, 2001.
36. Kudva IT, Hatfield PG, Hovde CJ. Escherichia coli O157:H7 in microbial flora of sheep. J Clin Microbiol 34:431-433, 1996.
37. Kudva IT, Hatfield PG, Hovde CJ. Characterization of Escherichia coli O157:H7 and other shiga toxin-producing E. coli serotypes isolated from sheep. J Clin Microbiol 35:892-899, 1997.
38. Heuvelink AE, Van Den Biggelaar FLAM, De Boer E, Herbes RG, Melchers WJG, Huis 'T Veld JHJ, Monnens LAH. Isolation and characterization of verocytotoxin-producing Escherichia coli O157 strains from Dutch cattle and Sheep. J Clin Microbiol 36:878-882, 1998.
39. Johnsen G, Berget OI, Wasteson Y, Herikstad H. E. coli O157:H7 in faeces from cattle, sheep and pigs in the south west part of Norway during 1998. In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 3: Pathogenicity and virulence of Verocytotoxigenic E. coli, Concerted Action CT98-3935. Dublin, UK: The National Food Centre, p186, 2000.
40. Chapman PA, Siddons CA, Cerdan Malo AT, Harkin MA. A one year study of Escherichia coli O157 in raw beef and lamb products. Epidemiol Infect 124:207-213, 2000.
41. Heuvelink AE, Zwartkruis-Nahuis JTM, Beumer RR, De Boer E. Occurrence and survival of verocytotoxin-producing Escherichia coli O157 in meats obtained from retail outlets in The Netherlands. J Food Prot 62:1115-1122, 1999.
42. Tarr PI, Tran TN, Wilson RA. Escherichia coli O157:H7 in retail ground beef in Seattle: results of a one-year prospective study. J Food Prot 62:133-139, 1999.
43. Doyle MP, Schoeni JL. Isolation of Escherichia coli O157:H7 from retail fresh meats and poultry. Appl Environ Microbiol 53:2394-2396, 1987.
44. Read SC, Gyles CL, Clarke RC, Lior H, McEwen S. Prevalence of verocytotoxigenic Escherichia coli in ground beef, pork, and chicken in southwestern Ontario. Epidemiol Infect 105:11-20, 1990.
45. Suthienkul O, Brown E, Seriwatana J, Tienthongdee S, Sastravaha S, Echeverria P. Shiga-like-toxin-producing Escherichia coli in retail meats and cattle in Thailand. Appl Environ Microbiol 56:1135-1139, 1990.
46. Willshaw GA, Smith HR, Roberts D, Thirlwell J, Cheasly T, Rowe B. Examination of raw beef products for the presence of vero cytotoxin producing Escherichia coli, particularly those of serogroup O157. J Appl Bacteriol 75:420-426, 1993.
47. Lindqvist R, Antonsson AK, Norling B, Persson L, Ekström ACL, Fäger U, Eriksson E, Löfdahl S, Norberg P. The prevalence of verocytotoxin-producing Escherichia coli (VTEC) and E. coli O157:H7 in beef in Sweden determined by PCR assays and an immuno-magnetic serparation (IMS) method. Food Microbiol 15:591-601, 1998.
48. Blanco JE, Blanco M, Mora A, Alonso MP, Coira A, Rodríguez A, Blanco J. Serotypes and virulence genes of verocytotoxigenic E. coli (VTEC) isolated from human patients in Spain. In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 3: Pathogenicity and Virulence of Verocytotoxigenic E. coli, Concerted Action CT98-3935. Dublin, UK: The National Food Centre, p191, 2000.
49. Caprioli A, Tozzi AE. Epidemiology of Shiga toxin-producing, Escherichia coli infections in continental Europe. In: Kaper JB, ÓBrien AD, Eds. Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli strains. Washington, DC: American Society for Microbiology, pp38-48, 1998.
50. Gunzer F, Böhm H, Rüssmann H, Bitzan M, Aleksic S, Karch H. Molecular detection of sorbitol-fermenting Escherichia coli O157 in patients with hemolytic-uremic syndrome. J Clin Microbiol 30:1807-1810, 1992.
51. Karch H, Huppertz HI, Bockemühl J, Schmidt H, Schwarzkopf A, Lissner R. Shiga toxin-producing Escherichia coli infections in Germany. J Food Prot 60:1454-1457, 1997.
52. Pulz M. Epidemiology and current importance of enterohaemorrhagic Escherichia coli (EHEC) in North Bavaria (1996). Gesundheitswesen 59:656-660, 1997.
53. Pradel N, Livrelli V, De Champs C, Palcoux JB, Reynaud A, Scheutz F, Sirot J, Joly B, Forestier C. 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, 2000.
54. Burnens AP, Boss P, Orskov F, Orskow I, Schaad UB, Müller F, Heinzle R, Nicolet J. Occurrence and phenotypic properties of verotoxin producing Escherichia coli in sporadic cases of gastroenteritis. Eur J Clin Microbiol Infect Dis 11:631-634, 1992.
55. Piérard D, Stevens D, Moriau L, Lior H, Lauwers S. Isolation and virulence factors of verocytotoxin-producing Escherichia coli in human stool samples. Clin Microbiol Infect 3:531-540, 1997.
56. Scheutz F, Olesen B, Gerner-Smidt P. Verocytotoxigenic E. coli (VTEC) from Danish patients 1997-1999. Part 1: Characterised by serotypes and virulence factors (abstract). Proceedings of the 4th International Symposium and Workshop on Shiga Toxin (Verocytotoxin)-Producing Escherichia coli Infections; 2000; Kyoto, Japan. p98. Abstract nr 207.
57. Beutin L, Zimmermann S, Gleier K. Association between serotypes, virulence markers and disease in a group of 679 verocytotoxin-producing Escherichia coli (VTEC) strains isolated from human patients in Germany (1997-1999). In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 5: Epidemiology of Verocytotoxigenic E. coli, Concerted Action CT983-935. Dublin, UK: The National Food Centre, pp5-11, 2001.
58. Keskimäki M, Saari M, Heiskanen T, Siitonen A. Shiga toxin-producing Escherichia coli in Filand from 1990 through 1997: Prevalence and characteristics of isolates. J Clin Microbiol 36:3641-3646, 1998.
59. Mora A, Usera MA, Blanco M, Blanco JE, Alonso MP, Prats G, Stirrat A, Carter FM, Blanco J. Bacteriophage typing and virulence genes of verocytotoxigenic E. coli (VTEC) O157:H7 strains isolated in Spain. In: Duffy G, Garvey P, Coia J, Wasteson Y, McDowell DA, Eds. Verocytotoxigenic E. coli in Europe, 3: Pathogenicity and Virulence of Verocytotoxigenic E. coli, Concerted Action CT98-3935. Dublin, UK: The National Food Centre, p189, 2000.
60. Cheasty T, Allerberger F, Beutin L, Caprioli A, Heuvelink A, Karch H, Lofdahl S, Pièrard D, Scheutz F, Siitonen A, Smith H. VTEC O157 phage types isolated from 15 European countries: 1997-1999 (abstract). Proceedings of the 4th International Symposium and Workshop on Shiga Toxin (Verocytotoxin)-Producing Escherichia coli Infections; 2000; Kyoto, Japan. p126. Abstract nr 263.
61. Saari M, Cheasty T, Leino K, Siitonen A. Phage types and genotypes of shiga toxin-producing Escherichia coli O157 in Finland. J Clin Microbiol 39:1140-1143, 2001.
62. Ahmed R, Ali A, Demezuk W, Woodward D, Clark C, Khakhria R, Rodgers F. Emergence of new molecular and phage typing variants of E. coli O157:H7 in Canada. Proceedings of the 4th International Symposium and Workshop on Shiga Toxin (Verocytotoxin)-Producing Escherichia coli Infections; 2000; Kyoto, Japan. Abstract nr 224, p106.
63. Willshaw GA, Cheasty T, Frost JA, Threlfall EJ, Rowe B. Antimicrobial resistance of O157 VTEC in England and Wales. EVC news 5, Notiziario dell Istituto Superiore di Sanità 9(11 Suppl 3):3-4, 1996.
64. Smith HR, Rowe B, Gross RJ, Fry NK, Scotland SM. Haemorrhagic colitis and vero-cytotoxin-producing Escherichia coli in England and Wales. Lancet. 1:1062-1064, 1987.
65. Pebody RG, Furtado C, Rojas A, McCarthy N, Nylen G, Ruutu P, Leino T, Chalmers R, de Jong B, Donnelly M, Fisher I, Gilham C, Graverson L, Cheasty T, Willshaw G, Navarro M, Salmon R, Leinikki P, Wall P, Bartlett C. An international outbreak of vero cytotoxin-producing Escherichia coli O157 infection amongst tourists: a challenge for the European infectious disease surveillance network. Epidemiol Infect 123:217-223, 1999.
66. +. Alimentaria 275:109-113, 1996.
67. Gomariz M, Robertson MT, Serrano E, Iglesias L, Pérez-Trallero E. Estudio de dos brotes de E. coli O157:H7 en Gipuzkoa. Enferm. Infecc Microbiol Clín 18(S1):84, 2000.