Tracking verocytotoxigenic Escherichia coli O157, O26, O111, O103 and O145 in Irish cattle

K M Thomas, M S McCann, M M Collery, P Whyte, D.A. McDowell, G Duffy

    Research output: Contribution to journalArticlepeer-review

    60 Citations (Scopus)


    The purpose of this study was to investigate carriage and transfer of verocytotoxigenic Escherichia coli (VTEC) O157, O26, O111, O103 and O145 from faeces and hide to dressed carcasses of Irish cattle as well as establishing the virulence potential of VTEC carried by these cattle. Individual cattle was tracked and faecal samples,hide and carcass (pre-evisceration and post-wash) swabs were analysed for verotoxin (vt1 and vt2) genes using a duplex real-time PCR assay. Positive samples were screened for the five serogroups of interest by real-time PCR. Isolates were recovered from PCR positive samples using immunomagnetic separation and confirmed by latex agglutination and PCR. Isolates were subject to a virulence screen (vt1, vt2, eaeA and hlyA) by PCR. Isolates carrying vt genes were examined by Pulsed-Field Gel Electrophoresis (PFGE). Of theVTEC isolated, E. coli O157 was the most frequently recovered from hide (17.6%), faeces (2.3%) and pre-evisceration/post-wash carcass (0.7%) samples. VTEC O26 was isolated from 0.2% of hide swabs and 1.5% of faeces samples. VTEC O145 was isolated from 0.7% of faeces samples. VTEC O26 and VTEC O145 were not recovered from carcass swabs. Non-VTEC O103 was recovered from all sample types (27.1% hide, 8.5% faeces, 5.5% pre-evisceration carcass, 2.2% post-wash carcass), with 0.2% of hide swabs and 1.0% of faeces samples found to be positive for VTEC O103 isolates. E. coli O111 was not detected in any samples. For the four serogroups recovered, the direct transfer from hide to carcass was not observed. This study shows that while VTEC O157 are being carried by cattle presented for slaughter in Ireland, a number of other verotoxin producing strains are beginning to emerge.
    Original languageEnglish
    Pages (from-to)288-296
    JournalInternational Journal of Food Microbiology
    Issue number3
    Publication statusPublished (in print/issue) - 3 Feb 2012

    Bibliographical note

    Reference text: Acheson, D.W., Reidl, J., Zhang, X., Keusch, G.T., Mekalanos, J.J., Waldor, M.K., 1998. In
    vivo transduction with shiga toxin 1-encoding phage. Infection and Immunity 66, 4496–4498.
    Anon, 1997. Clean Cattle Policy. Department of Agriculture, Food and Forestry, Dublin.
    Arthur, T.M., Bosilevac, J.M., Nou, X., Shackelford, S.D., Wheeler, T.L., Kent, M.P., Jaroni, D., Pauling, B., Allen, D.M., Koohmaraie, M., 2004. Escherichia coli O157 prevalence and enumeration of aerobic bacteria, Enterobacteriaceae, and Escherichia coli O157 at various steps in commercial beef processing plants. Journal of Food Protection 67, 658–665.
    Baird, B.E., Lucia, L.M., Acuff, G.R., Harris, K.B., Savell, J.W., 2006. Beef hide antimicrobial
    interventions as a means of reducing bacterial contamination. Meat Science 73, 245–248.
    Barkocy-Gallagher, G.A., Arthur, T.M., Rivera-Betancourt, M., Nou, X., Shackelford, S.D.,
    Wheeler, T.L., Koohmaraie, M., 2003. Seasonal prevalence of Shiga toxin-producing Escherichia coli, including O157:H7 and non-O157 serotypes, and Salmonella in commercial beef processing plants. Journal of Food Protection 66, 1978–1986.

    Beutin, L., Geier, D., Zimmermann, S., Karch, H., 1995. Virulence markers of Shiga-like toxin-producing Escherichia coli strains originating from healthy domestic animals of different species. Journal of Clinical Microbiology 33, 631–635.
    Biosearch Technologies, I., 2004. LightCycler 2.0 Color Compensation File [Online] Available at
    04.pdf2004(Accessed: 4 January 2007).
    Boerlin, P., McEwen, S.A., Boerlin-Petzold, F., Wilson, J.B., Johnson, R.P., Gyles, C.L., 1999.
    Associations between virulence factors of Shiga toxin-producing Escherichia coli and disease in humans. Journal of Clinical Microbiology 37, 497–503.
    Brichta-Harhay, D.M., Guerini, M.N., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., Wheeler, T.L., Koohmaraie, M., 2008. Salmonella and Escherichia coli O157:H7 contamination on hides and carcasses of cull cattle presented for slaughter in the United States: an evaluation of prevalence and bacterial loads by immunomagnetic separation and direct plating methods. Applied and Environmental Microbiology 74, 6289–6297.
    Carney, E., O'Brien, S.B., Sheridan, J.J., McDowell, D.A., Blair, I.S., Duffy, G., 2006. Prevalence and level of Escherichia coli O157 on beef trimmings, carcasses and boned
    head meat at a beef slaughter plant. Food Microbiology 23, 52–59.
    Coia, J.E., 1998. Clinical, microbiological and epidemiological aspects of Escherichia coli
    O157 infection. FEMS Immunology and Medical Microbiology 20, 1–9.
    Denny, J., Bhat, M., Eckmann, K., 2008. Outbreak of Escherichia coli O157:H7 associated
    with raw milk consumption in the Pacific Northwest. Foodborne Pathogens and Disease 5, 321–328.
    Donnenberg, M.S., Whittam, T.S., 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. The Journal of Clinical Investigation 107, 539–548.
    EFSA, 2011. European Food Safety Authority; the European Union summary report on
    trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA Journal 9 (3), 2090 378 pp..
    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 of the United States of America 97, 2999–3003.
    Etcheverría, A.I., Padola, N.L., Sanz, M.E., Polifroni, R., Krüger, A., Passucci, J., Rodríguez,
    E.M., Taraborelli, A.L., Ballerio, M., Parma, A.E., 2010. Occurrence of Shiga toxin- producing E. coli (STEC) on carcasses and retail beef cuts in the marketing chain of beef in Argentina. Meat Science 86, 418–421.
    Fox, J.T., Renter, D.G., Sanderson, M.W., Nutsch, A.L., Shi, X., Nagaraja, T.G., 2008. Associations between the presence and magnitude of Escherichia coli O157 in feces at
    harvest and contamination of preintervention beef carcasses. Journal of Food Protection 71, 1761–1767.
    Gill, C.O., Jones, T., 2000. Microbiological sampling of carcasses by excision or swabbing. Journal of Food Protection 63, 167–173.
    Gill, C.O., Landers, C., 2004. Microbiological conditions of detained beef carcasses before
    and after removal of visible contamination. Meat Science 66, 335–342.
    Gun, H., Yilmaz, A., Turker, S., Tanlasi, A., Yilmaz, H., 2003. Contamination of bovine carcasses and abattoir environment by Escherichia coli O157:H7 in Istanbul. International Journal of Food Microbiology 84, 339–344.
    Guyon, R., Dorey, F., Malas, J.P., Grimont, F., Foret, J., Rouvière, B., Collobert, J.F., 2001.
    Superficial contamination of bovine carcasses by Escherichia coli O157:H7 in a slaughterhouse in Normandy (France). Meat Science 58, 329–331.
    HSPC, 2010. Health Protection Surveillance Centre. Annual Report 2009. ISSN 1649-
    Hussein, H.S., 2007. Prevalence and pathogenicity of Shiga toxin-producing Escherichia
    coli in beef cattle and their products. Journal of Animal Science 85, E63–E72.
    Jacob, M.E., Renter, D.G., Nagaraja, T.G., 2010. Animal- and truckload-level associations
    between Escherichia coli O157:H7 in feces and on hides at harvest and contamination of preevisceration beef carcasses. Journal of Food Protection 73, 1030–1037.
    Jeon, B.-W., Jeong, J.-M., Won, G.-Y., Park, H., Eo, S.-K., Kang, H.-Y., Hur, J., Lee, J.H., 2006.
    Prevalence and characteristics of Escherichia coli O26 and O111 from cattle in Korea. International Journal of Food Microbiology 110, 123–126.
    Karmali, M.A., Petric, M., Corazon, L., Fleming, P.C., Arbus, G.S., Lior, H., 1985. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. The Journal of Infectious Diseases 151, 775–782.
    Lim, J.Y., Li, J., Sheng, H., Besser, T.E., Potter, K., Hovde, C.J., 2007. Escherichia coli O157:
    H7 colonization at the rectoanal junction of long-duration culture-positive cattle. Applied and Environmental Microbiology 73, 1380–1382.
    McEvoy, J.M., Doherty, A.M., Finnerty, M., Sheridan, J.J., McGuire, L., Blair, I.S., McDowell, D.A., Harrington, D., 2000. The relationship between hide cleanliness and bacterial numbers on beef carcasses at a commercial abattoir. Letters in Applied Microbiology 30, 390–395.
    McEvoy, J.M., Doherty, A.M., Sheridan, J.J., Thomson-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.
    Miyao, Y., Kataoka, T., Nomoto, T., Kai, A., Itoh, T., Itoh, K., 1998. Prevalence of verotoxin-producing Escherichia coli habored in the intestine of cattle in Japan. Veterinary Microbiology 61, 137–143.
    Nastasijevic, I., Mitrovic, R., Buncic, S., 2008. Occurrence of Escherichia coli O157 on hides of slaughtered cattle. Letters in Applied Microbiology 46, 126–131.
    Naylor, S.W., Low, J.C., Besser, T.E., Mahajan, A., Gunn, G.J., Pearce, M.C., McKendrick, I.J.,
    Smith, D.G., Gally, D.L., 2003. Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infection and Immunity 71, 1505–1512.
    Naylor, S.W., Gally, D.L., Low, J.C., 2005. Enterohaemorrhagic E. coli in veterinary medicine. International Journal of Medical Microbiology 295, 419–441.
    O'Brien, S.B., Duffy, G., Carney, E., Sheridan, J.J., McDowell, D.A., Blair, I.S., 2005. Prevalence and numbers of Escherichia coli O157 on bovine hides at a beef slaughter
    plant. Journal of Food Protection 68, 660–665.
    O'Hanlon, K.A., Catarame, T.M.G., Duffy, G., Blair, I.S., McDowell, D.A., 2004. RAPID de-
    tection and quantification of E. coli O157/O26/O111 in minced beef by real-time PCR. Journal of Applied Microbiology 96, 1013–1023.
    Orden, J.A., Cid, D., Ruiz-Santa-Quiteria, J.A., Garcia, S., Martinez, S., de la Fuente, R.,
    2002. Verotoxin-producing Escherichia coli (VTEC), enteropathogenic E. coli (EPEC) and necrotoxigenic E. coli (NTEC) isolated from healthy cattle in Spain. Journal of Applied Microbiology 93, 29–35.
    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.
    Pearce, M.C., Jenkins, C., Vali, L., Smith, A.W., Knight, H.I., Cheasty, T., Smith, H.R., Gunn,
    G.J., Woolhouse, M.E., Amyes, S.G., Frankel, G., 2004. Temporal shedding patterns and virulence factors of Escherichia coli serogroups O26, O103, O111, O145, and O157 in a cohort of beef calves and their dams. Applied and Environmental Microbiology 70, 1708–1716.
    Pearce, M.C., Evans, J., McKendrick, I.J., Smith, A.W., Knight, H.I., Mellor, D.J., Woolhouse,
    M.E., 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.
    Perelle, S., Dilasser, F., Grout, J., Fach, P., 2004. Detection by 5′-nuclease PCR of Shiga-
    toxin producing Escherichia coli O26, O55, O91, O103, O111, O113, O145 and O157:H7, associated with the world's most frequent clinical cases. Molecular and Cellular Probes 18, 185–192.
    Perelle, S., Dilasser, F., Grout, J., Fach, P., 2005. Detection of Escherichia coli serogroup
    O103 by real-time polymerase chain reaction. Journal of Applied Microbiology 98, 1162–1168.
    Prendergast, D.M., Lendrum, L., Pearce, R., Ball, C., McLernon, J., O'Grady, D., Scott, L.,
    Fanning, S., Egan, J., Gutierrez, M., 2011. Verocytotoxigenic Escherichia coli O157 in beef and sheep abattoirs in Ireland and characterisation of isolates by pulsed-field gel electrophoresis and multi-locus variable number of tandem repeat analysis. International Journal of Food Microbiology 144, 519–527.
    Reid, C.A., Small, A., Avery, S.M., Buncic, S., 2002. Presence of food-borne pathogens on
    cattle hides. Food Control 13, 411–415.
    Renter, D.G., Bohaychuk, V., Van Donkersgoed, J., King, R., 2007. Presence of non-O157
    Shiga toxin-producing Escherichia coli in feces from feedlot cattle in Alberta and absence on corresponding beef carcasses. Canadian Journal of Veterinary Research 71, 230–235.
    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 Pathogens and Disease 3, 59–67.
    Rice, D.H., Sheng, H.Q., Wynia, S.A., Hovde, C.J., 2003. Rectoanal mucosal swab culture is
    more sensitive than fecal culture and distinguishes Escherichia coli O157:H7-colonized cattle and those transiently shedding the same organism. Journal of Clinical Microbiology 41, 4924–4929.
    Sakai, T., Tanabe, S., Hashida, M., Ohmae, H., Kitahori, Y., 2010. Multiple-locus variable-
    number tandem repeat analysis of enterohemorrhagic Escherichia coli O157 in outbreak of food poisoning caused by formed beef chunk steaks. Japanese Journal of Infectious Diseases 63, 152–153.
    Sandhu, K.S., Clarke, R.C., McFadden, K., Brouwer, A., Louie, M., Wilson, J., Lior, H., Gyles,
    C.L., 1996. Prevalence of the eaeA gene in verotoxigenic Escherichia coli strains from dairy cattle in Southwest Ontario. Epidemiology and Infection 116, 1–7.
    Schmidt, H., Bielaszewska, M., Karch, H., 1999. Transduction of enteric Escherichia coli isolates with a derivative of Shiga toxin 2-encoding bacteriophage phi3538 isolated from Escherichia coli O157:H7. Applied and Environmental Microbiology 65, 3855–3861.
    Tutenel, A.V., Pierard, D., Van Hoof, J., Cornelis, M., De Zutter, L., 2003. Isolation and molecular characterization of Escherichia coli O157 isolated from cattle, pigs and chickens at slaughter. International Journal of Food Microbiology 84, 63–69.
    Van Donkersgoed, J., Graham, T., Gannon, V., 1999. The prevalence of verotoxins, Escherichia coli O157:H7, and Salmonella in the feces and rumen of cattle at processing. The Canadian Veterinary Journal 40, 332–338.
    Wieler, L.H., Vieler, E., Erpenstein, C., Schlapp, T., Steinruck, H., Bauerfeind, R., Byomi, A.,
    Baljer, G., 1996. Shiga toxin-producing Escherichia coli strains from bovines: association of adhesion with carriage of eae and other genes. Journal of Clinical Microbiology 34, 2980–2984.
    Willshaw, G.A., Thirlwell, J., Jones, A.P., Parry, S., Salmon, R.L., Hickey, M., 1994. Vero
    cytotoxin-producing Escherichia coli O157 in beefburgers linked to an outbreak of diarrhoea, haemorrhagic colitis and haemolytic uraemic syndrome in Britain. Letters in Applied Microbiology 19, 304–307.


    • Verocytotoxigenic
    • E. coli
    • Cattle
    • Abattoir
    • Hide
    • Carcass


    Dive into the research topics of 'Tracking verocytotoxigenic Escherichia coli O157, O26, O111, O103 and O145 in Irish cattle'. Together they form a unique fingerprint.

    Cite this