Abstract
Four hundred and fifty beef animal hides and a similar number of carcasses were screened for STEC in 3 beef abattoirs over a 12 month period using PCR and culture based methods. 67% (301/450) of hides and 27% (122/450) of carcasses were STEC PCR positive. Forty isolates representing 12 STEC serotypes (O5:H-,O13:H2, O26:H11, O33:H11, O55:H11, O113:H4, O128:H8, O136:H12, O138:H48, O150:H2, O168:H8 and ONT:H11) and 15 serotype-virulotype combinations were identified.This study provides much needed non-O157 STEC surveillance data and also provides further evidence of bovines as a source of clinically significant STEC as well as identifying 3 emerging serotypes O5:H- (eae-b1), O13:H2 (eae-z), and O150:H2 (eae-z) that should be considered when developing beef testing procedures for non-O157 STEC.
| Original language | English |
|---|---|
| Pages (from-to) | 223-229 |
| Journal | Food Microbiology |
| Volume | 32 |
| Issue number | 2 |
| DOIs | |
| Publication status | Published (in print/issue) - Dec 2012 |
Bibliographical note
Reference text: Aidar-Ugrinovich, L., Blanco, J., Blanco, M., Blanco, J.E., Leomil, L., Dahbi, G., Mora, A., Onuma, D.L., Silveira, W.D., de Castro, A.F.P., 2007. Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in Sao Paulo, Brazil. International Journal of Food Microbiology 115, 297-306.Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller,W., Lipman, D.J.,
1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402.
Anon, 1999. Zoonotic non-O157 Shiga toxin-producing Escherichia coli (STEC). Report of a WHO Scientific Working Group meeting, 23e26 June 1998, Berlin, Germany, pp. 1-30.
Anon, 2007. Scientific opinion of the panel on biological hazards on a request from EFSA on monitoring of verotoxigenic Escherichia coli (VTEC) and identification of human pathogenic types. EFSA Journal 579, 1e61.
Anon, 2011a. Growing the Success of Irish Food and Horticulture, Meat and Livestock, Reviewing Outlook 2010e2011. Bord Bia e Irish Food Board 2011.
Anon, 2011b. 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 EuropeanFood SafetyAuthority, Stockholm,Sweden. ECDC, 2011.
Anon, 2011c. Federal Register Vol. 76, No. 182 Tuesday, September 20, 2011. Available on: http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/2010-0023.pdf.
Anon, 2012. European food Safety authority, European centre for disease prevention and control; the european union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA Journal 10, 2597.
Arthur, T.M., Barkocy-Gallagher, G.A., Rivera-Betancourt, M., Koohmarie, M., 2002. Prevalence and characterisation of non-O157 shiga toxin-producing Escherichia coli on carcasses in commercial beef cattle processing plants. Applied and Environmental Microbiology 68 (910), 4847-4852.
Barham, A.R., Barham, B.L., Johnson, A.K., Allen, D.M., Blanton, J.R., Miller, M.F., 2002.
Effects of the transportation of beef cattle from the feed-yard to the packing plant on prevalence levels of Escherichia coli O157 and Salmonella spp. Journal of Food Protection 65, 280-283.
Bettelheim, K.A., 2003. Non-O157 verotoxin-producing Escherichia coli: a problem, paradox, and paradigm. Experimental Biology and Medicine 228, 333-344.
Bettelheim, K.A., 2007. The non-O157 Shiga-toxigenic (Verocytotoxigenic) Escherichia coli; under-rated pathogens. Critical in Microbiology 33, 67-87.
Beutin, L., Miko, A., Krause, G., Pries, K., Haby, S., Steege, K., Albreacht, 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. Applied Environmental Microbiology 73, 4769-4775.
Blanco, M., Blanco, J.E., Mora, A., Dahbil, G., Alonsol, M.P., Gonzalez, E.A., Bernardez, M.I., Blanco, J., 2004. Serotypes, virulence genes, and intimin types of shiga toxin (verotoxin)-producing Escherichia coli isolates from cattle in Spain and identification of a new intimin variant gene (eae-). Journal of Clinical Microbiology 42, 645-651.
Bolton, D.J., 2010. Verocytotoxigenic (shiga toxin-producing) Escherichia coli: virulence factors and pathogenicity in the farm to fork paradigm. Foodborne Pathogens and Disease 8, 357-365.
Bosilevac, J.M., Koohmaraie, M., 2011. Prevalence and characterization of non-O157 shiga toxin producing Escherichia coli isolated from commercial ground beef in the United States. Applied Environmental Microbiology. 02833-10.
Breum, S.O., Boel, J., 2010. Prevalence of Escherichic coli O157 and verocytotoxin producing E. coli (VTEC) on Danish beef carcasses. International Journal of Food Microbiology 141, 90-96.
Brunder,W., Schmidt, H., Karch,W., 1996. KatP, a novel catalase peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 142, 3305-3315.
Burk, C., Dietrich, R., Acar, G., Moravek, M., Bulte, M., Martlbauer, E., 2003. Identification and characterization of a new variant of shiga toxin 1 in Escherichia coli ONT: H19 of bovine origin. Journal of Clinical Microbiology 41, 2106e2112.
Caprioli, A., Morabito, S., Brugreb, H., Oswald, E., 2005. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Veterinary Research 36, 289-311.
Castello, A., Eguiarte, L.E., Souza, V., 2005. A genomic population genetics analysis of the pathogenic enterocyte effacement island in Escherichia coli: the search for the unit of selection. Proceedings of the National Academy of Sciences of the United States of America 102, 1542-1547.
Cebula, T.A., Payne, W.L., Feng, P., 1995. Simultaneous identification of strains of Escherichia coli serotype O157:H7 and their Shiga-like toxin type by mismatch amplification mutation assay-multiplex PCR. Journal of Clinical Microbiology 33, 248-250.
Coombes, B.K., Wickham, M.E., Mascarenhas, M., Gruenheid, S., Brett Finlay, B., Karmali, M.A., 2008. Molecular analysis as an aid to assess the public health risk of non-O157 Shiga toxin-producing Escherichia coli strains. Applied Environmental Microbiology 74, 2153-2160.
Currie, A., MacDonald, J., Ellis, A., Siushansian, J., Chui, L., Charlebois, M., Peermohamed, M., Everett, D., Fehr, M., Ng, L.K., 2007. Outbreak of Escherichia coli O157:H7 infections associated with consumption of beef donair. Journal of Food Protection 70, 1483-1488.
Dopler, D., Geue, L., Schares, S., Mintel, B., Hoffmann, B., Fischer, E.A.J., 2011. Dynamics of shiga-toxin producing Escherichia coli (STEC) and their virulence factors in cattle. Preventive Veterinary Medicine, Published Online. http:// dx.doi.org/10.1016/j.prevetmed.2011.08.007.
Doughty, S., Sloan, J., Bennett-Wood, V., Robertson, M., Robins- Browne, R.M., Hartland, E.L., 2002. Identification of a novel fimbrial gene cluster related to long polar fimbriae in locus of enterocyte effacement-negative strains of enterohemorrhagic Escherichia coli. Infection and Immunity 70, 6761-6769.
Elder, R.O., Keen, J.E., Siragusa, G.R., Barkocy-Gallagher, G.A., Koohmaraie, M., Laegreid, W.W., 2000. Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proceedings of the National Academy of Sciences 97, 2999e3003.
Fitzhenry, R.J., Pickard, D.J., Hartland, E.L., Reece, S., Dougan, G., Phillips, A.D. Frankel, G., 2002. Intimin type influences the site of human intestinal mucosal colonization by enterohemorrhagic Escherichia coli O157:H7. Gut, 180-185.
Frankel, G., Phillips, A.D., Rosenshine, I., Dougan, G., Kaper, J.B., Knutton, S., 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Molecular Microbiology 30, 911-921.
Fuller, C.A., Pellino, C.A., Flagler, M.J., Strasser, J.E., Weiss, A.A., 2011. Shiga toxin subtypes display dramatic differences in potency. Infection and Immunity 79 1329e1337.
Galli, L., Miliwebsky, E.,Irino, K., Leotta, G., Rivas, M., 2010. Virulence profile comparison between LEE-negative shiga toxin-producing Escherichia coli (STEC) strains isolated fromcattle and humans. Veterinary Microbiology 143, 307-313.
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. Epidemiological Review 13, 60 - 98
Gunzer, F., Bohm, H., Russmann, H., Bitzan, M., Aleksic, S., Karch, H., 1992. Molecular
detection of sorbitol-fermenting Escherichia coli O157 in patients with hemolytic-uremic syndrome. Journal of Clinical Microbiology 30, 1807-1810.
Herold, S., Paton, J.C., Paton, A.W., 2009. Sab, a novel autotransporter of locus of enterocyte effacement-negative shiga toxigenic Escherichia coli O113:H21, contributes to adherence and biofilm formation. Infection and Immunity 77, 3234-3243.
Hii, J.H., Gyles, C., Morooka, T., Karmali, M.A., Clarke, R., De Grandis, S., Brunton, J.L., 1991. Development of verotoxin 2- and verotoxin 2 variant (VT2v)-specific oligonucleotide probes on the basis of the nucleotide sequence of the B cistron of VT2v from Escherichia coli E32511 and B2F1. Journal of Clinical Microbiology 29, 2704-2709.
Jelacic, J.K., Damrow, T., Chen, G.S., Jelacic, S., Bielaszewska, M., Ciol, M., Carvalho, H.M., Melton-Celsa, A.R., O’Biren, A.D., Tarr, P.I., 2003. Shiga toxin producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. The Journal of Infectious Diseases 188, 719-729.
Jenkins, C., Pearce, M.C., Chart, H., Cheasty, T., Wilshaw, G.A., Gunn, G.J., Dougan, G., Smith, H.R., Synge, B.A., Frankel, G., 2002. An eight-month study of a population of verocytotoxigenic Escherichia coli (VTEC) in a Scottish cattle herd. Journal of Applied Microbiology 93, 944-953.
Jenkins, C., Lawson, A.J., Cheasty, T., Willshaw, G.A., Wright, P., Dougan, G., Frankel, G., Smith, H.R., 2003. Subtyping intimin genes from enteropathogenic Escherichia coli associated with outbreaks and sporadic cases in the United Kingdom and Eire. Molecular and Cellular Probes 17, 149-156.
Johnson, R.P., Clarke, R.C., Wilson, J.B., Read, S.C., Rahn, K., Renwick, S.A., Sandhu, K.A.,
Alves, D., Karmali, M.A., Lior, H., Mcewen, S.A., Spika, J.S., Gyles, C.L., 1996.
Growing concerns and recent outbreaks involving non-O157:H7 serotypes of verotoxigenic Escherichia coli. Journal of Food Protection 59, 1112-1122.
Karmali, M.A., Mascarenhas, M., Shen, S., Ziebell, K., Johnson, S., Reid-Smith, R., Isaac
Renton, J., Clark, C., Rahn, K., Kaper, J.B., 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. Journal of Clinical. Microbiology 41, 4930-4940.
King, L.A., Mailles, A., Mariani-Kurkdji, P., Vernozy-Rozand, C., Montet, M.P., Grimont, F., Pihier, N., Devalk, H., Perret, F., Bingen, E., Espié, E., Vaillant, V., 2009. Community-wide outbreak of Escherichia coli O157:H7 associated with consumption of frozen beef burgers. Epidemiology and Infection 137, 889-896.
Kobayashi, H., Shimada, J., Nakazawa, M., Morozumi, T., Pohjanvirta, T., Pelkonen, S.,
Yamamoto, K., 2001. Prevalence and characteristics of shiga toxin-producing Escherichia coli from healthy cattle in Japan. Applied and Environmental Microbiology 67, 484-489.
Kuczius, T., Bielaszewska, M., Friedrich, A.W., WenLan, Z., 2004. A rapid method for
the discrimination of genes encoding classical Shiga toxin (Stx) 1 and its variants, Stx1c and Stx1d in Escherichia coli. Molecular Nutrition & Food Research 48, 515-521.
Kumar, H.S., Karunasagar, I., Karunasagar, I., Teizou, T., Shima, K., Yamasaki, S., 2004.
Characterisation of Shiga toxin-producing Escherichia coli (STEC) isolated from seafood and beef. FEMS Microbiology Letters 233, 173-178.
Lahti, E., Ruoho, O., Rantala, L., Hanninen, M.L., Honkanen-Buzalski, T., 2003. Longitudinal study of Escherichia coli O157 in a cattle finishing unit. Applied and Environmental Microbiology 69, 554-561.
Leung, P.H., Yam, W.C., Ng, W.W., Peiris, J.S., 2001. The prevalence and characterization
of verotoxin-producing Escherichia coli isolated from cattle and pigs in an abattoir in Hong Kong. Epidemiology and Infection 126, 173-179.
Leung, P.H.M., Peiris, J.S.M., Ng, W.W.S., Robins-Browne, R.M., Bettelheim, K.A., Yam, W.C., 2003. A newly discovered verotoxin variant, vt2g, produced by bovine verocytotoxigenic Escherichia coli. Applied and Environmental Microbiology 69, 7549-7553.
Lucchesi, P.M.A., Kruger, A., Parma, A.E., 2006. Distribution of saa gene variants in
verocytotoxigenic Escherichia coli isolated from cattle and food. Research Microbiology 157, 263-266.
Machado, J., Grimont, F., Grimont, P.A.D., 2000. Identification of Escherichia coli flagellar types by restriction of the amplified fliC gene. Research in Microbiology 151, 535-546.
McEvoy, J.M., Doherty, A.M., Sheridan, J.J., Thompson-Carter, F.M., Garvey, P., McGuire, L., Blair, I.S., McDowell, D.A., 2003. The prevalence and spread of Escherichia coli O157:H7 at a commercial beef abattoir. Journal of Applied Microbiology 95, 256-266.
McLean, C., Bettelheim, K.A., Kuzevski, A., Falconer, L., Djordjevic, S.P., 2005. Isolation of Escherichia coli O5:H-, possessing genes for shiga toxin 1, intimin-B and enterohaemolysin, from an intestinal biopsy from an adult case of bloody diarrhoea; evidence for two distinct O5:H- pathotypes. Journal of Medical Microbiology 54, 605-607.
McNally, A., Roe, A.J., Simpson, S., Thomas-Carter, F.M., Hoey, D.E., Currie, C.,
Chakraborty, T., Smith, D.G., Gally, D.L., 2001. Differences in levels of secreted locus of enterocyte effacement proteins between human disease-associated and bovine Escherichia coli O157. Infection and Immunity 69, 5107-5114.
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. Infection and Immunity 64, 1569-1576.
Minihan, D., O‘Mahony, M., Whyte, P., Collins, J.D., 2003. An investigation on the effect of transport and lairage on the faecal shedding prevalence of Escherichia coli O157 in cattle. Journal of Veterinary Medicine, Series B-Infectious Diseases and Veterinary Public Health 50, 378-382.
Monaghan, A., Byrne, B., Fanning, S., Sweeney, T., McDowell, D., Bolton, D.J., 2011. Serotypes and virulence profiles of non-O157 shiga-toxin producing Escherichia coli (STEC) from bovine farms. Applied Environmental Microbiology 77, 8662-8668.
Muniesa, M., Recktenwald, J., Bielaszewska, M., Karch, H., Schmidt, H., 2000. Characterization of a shiga toxin 2e-converting bacteriophage from an Escherichia coli strain of human origin. Infection and Immunity 68, 4850-4855.
Nastasijevic, I., Mitrovic, R., Buncic, S., 2009. The occurrence of Escherichia coli O157 in/on faeces, carcasses and fresh meats from cattle. Meat Science 82, 101-105.
Nicholls, L., Grant, T.H., Robins-Browne, R.M., 2000. Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Molecular Microbiology 35, 275-288.
Orskov, I., Orskov, F., Jann, B., Jann, K., 1977. Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Microbiological and Molecular Biology Reviews 41, 667-710.
Paton, A.W., 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, rfbO111, and rfbO157. Journal of Clinical Microbiology 36, 598-602.
Paton, A.W., Paton, J.C., 1999. Molecular characterization of the locus encoding biosynthesis of the lipopolysaccharide o antigen of Escherichia coli serotype O113. Infection and Immunity 67, 5930-5937.
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. Infection and Immunity 69, 6999-7009.
Paton, A.W., Paton, J.C., 2002. Direct detection and characterization of shiga toxigenic
Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa. Journal of Clinical Microbiology 40, 271-274.
Pearce, M.C., Evans, J., McKendrick, I.J., Smith, A.W., Knight, H.I., Mellor, D.J., Woolhouse, M.E.J., Gunn, G.J., Low, J.C., 2006. Prevalence and virulence factors of Escherichia coli serogroups O26, O103, O111, and O145 shed by cattle in scotland. Applied and Environmental Microbiology 72, 653-659.
Pierard, D., Muyldermans, G., Moriau, L., Stevens, D., Lauwers, S., 1998. Identification
of new verocytotoxin type 2 variant b-subunit genes in human and animal Escherichia coli isolates. Journal of Clinical Microbiology 36, 3317-3322.
Pradel, N., Livrelli, V., De Champs, C., Palcoux, J.B., Reynaud, A., Scheutz, F., Sirot, J., Joly, B., Forestier, C., 2000. Prevalence and characterization of shiga toxin producing Escherichia coli Isolated from cattle, food, and children during a one-year prospective study in France. Journal of Clinical Microbiology 38, 1023-1031.
Ramachandran, V., Brett, K., Hornitzky, M.A., Dowton, M., Bettelheim, K.A., Walker, M.J., Djordjevic, S.P., 2003. Distribution of intimin subtypes among Escherichia coli isolates from ruminant and human sources. Journal of Clinical Microbiology 41, 5022-5032.
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. Emerging Infectious Disease 11, 603-609.
Rey, J., Blanco, J.E., Blanco, M., Mora, A., Dahbi, G., Alonso, J.M., Hermoso, M., Hermoso, J., Alonso, M.P., Usera, M.A., Gonzalez, E.A., Bernardez, M.I., Blanco, J., 2003. Serotypes, phage types and virulence genes of shiga toxin-producing Escherichia coli isolated from sheep in Spain. Veterinary Microbiology 94, 47-56.
Rigobelo, E.C., Stella, A.E., Avila, F.A., macedo, C., Marin, J.M., 2006. Characterization of Escherichia coli isolated from carcasses of beef cattle during their processing at an abattoir in Brazil. International Journal of Food Microbiology 110, 194-198.
Riley, L.W., Remis, R.S., Helgerson, S.D., McGee, H.B., Wells, J.G., Davis, B.R., Herbert, R.J., Olcott, E.S., Johnson, L.M., Hargrett, N.T., Blake, P.A., Cohen, M.L., 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. New England Journal of Medicine 308, 681-685.
Rogerie, F., Marecat, A., gambade, S., Dupond, F., beaubois, P., Lange, M., 2001. Characterisation of shiga toxin producing E. coli and O157 serotype E. coli isolated in France from healthy domestic cattle. International Journal of Food Microbiology 63, 217e223.
Schmidt, H., Rüssmann, H., Schwarzkopf, A., Aleksic, S., Heesemann, J., Karch, H.,
1994. Prevalence of attaching and effacing Escherichia coli in stool samples from
patients and controls. Zentralbl Bakteriol 281, 201e213.
Schmidt, H., Henkel, B., 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 in Escherichia coli O157 strains. FEMS Microbiology
Letters 148, 265-272.
Schmidt, H., Scheef, J., Morabito, S., Caprioli, A., Wieler, L.H., Karch, H., 2000. A new shiga toxin 2 variant (stx2f) from Escherichia coli isolated from pigeons. Applied Environmental Microbiology 66, 1205-1208.
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. Infection and Immunity 69, 6863-6873.
Szalo, I.M., Goffaux, F., Pirson, V., Pierard, D., Ball, H., Mainil, J., 2002. Presence in bovine enteropathogenic (EPEC) and enterohaemorrhagic (EHEC) Escherichia coli of genes encoding for putative adhesins of human EHEC strains. Research in Microbiology 153, 653-658.
Tarr, P.I., Bilge, S.S., Vary Jr., J.C., Jelacic, S., Habeeb, R.L., Ward, T.R., Baylor, M.R., Besser, T.E., 2000. Iha a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infection and Immunity 68, 1400-1407.
Tarr, C.L., Large, T.M., Moeller, C.L., Lacher, D.W., Tarr, P.I., Acheson, D.W., Whittam, T.S., 2002. Molecular characterization of a serotype O121:H19 clone, a distinct shiga toxin-producing clone of pathogenic Escherichia coli. Infection and Immunity 70, 6853-6859.
Terrance, M.A., Barkocy-Gallagher, G.A., Rivera-Betancourt, M., Koomaraie, M., 2002.
Prevalence and characterization of non-O157 shiga toxin producing Escherichia coli on carcasses in commercial beef cattle processing plants. Applied and Environmental Microbiology 68, 4847-4852.
Toma, C., Martínez 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. Journal of Clinical Microbiology 42, 4937-4946.
Torres, A.G., Giron, J.A., Perna, N.T., Burland, V., Blattner, F.R., Avelino-Flores, F., Kaper, J.B., 2002. Identification and characterization of lpfabcc’de, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infection and Immunity 70, 5416-5427.
Torres, A.G., Zhou, X., Kaper, J.B., 2005. Adherence of diarrheagenic Escherichia coli
strains to epithelial cells. Infection and Immunity 73, 18-29.
Tutenel, A.V., Pierard, D., Van Hoof, J., De Zutter, L., 2003. Molecular characterization of Escherichia coli O157 contamination routes in a cattle slaughterhouse. Journal of Food Protection 66, 1564-1569.
Wells, J.G., Davis, B.R., Wachsmuth, I.K., Riley, L.W., Remis, R.S., Sokolow, R., Morris, G.K., 1983. Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. Journal of Clinical Microbiology 18, 512-520.
Zhang, W., Bielaszewska, M., Kuczius, T., Karch, H., 2002. Identification, characterization,
and distribution of a shiga toxin 1 gene variant (stx1c) in Escherichia coli strains isolated from humans. Journal of Clinical Microbiology 40, 1441-1446.
Zweifel, C., Schumacher, S., Blanco, M., Blanco, J.E., Tasara, T.S., Blanco, J., Stephan, R.,
2005. Phenotypic and genotypic characteristics of non-O157 Shiga toxin producing
Escherichia coli (STEC) from Swiss cattle. Veterinary Microbiology 105, 37-45.
