Hostname: page-component-77f85d65b8-v2srd Total loading time: 0 Render date: 2026-04-17T19:00:57.451Z Has data issue: false hasContentIssue false
  • English
  • Français

Shiga toxin-producing Escherichia coli in swine: the public health perspective

Published online by Cambridge University Press:  09 January 2014

Marion Tseng ,
Pina M. Fratamico ,
Shannon D. Manning  and
Julie A. Funk
Marion Tseng*
Affiliation:
College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824, USA
Pina M. Fratamico
Affiliation:
Eastern Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, Wyndmoor, PA 19038, USA
Shannon D. Manning
Affiliation:
Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA
Julie A. Funk
Affiliation:
College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824, USA
*
*Corresponding author. E-mail: marionkttseng@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Shiga toxin-producing Escherichia coli (STEC) strains are food-borne pathogens that are an important public health concern. STEC infection is associated with severe clinical diseases in human beings, including hemorrhagic colitis (HC) and hemolytic uremic syndrome (HUS), which can lead to kidney failure and death. Cattle are the most important STEC reservoir. However, a number of STEC outbreaks and HUS cases have been attributed to pork products. In swine, STEC strains are known to be associated with edema disease. Nevertheless, the relationship between STEC of swine origin and human illness has yet to be determined. This review critically summarizes epidemiologic and biological studies of swine STEC. Several epidemiologic studies conducted in multiple regions of the world have demonstrated that domestic swine can carry and shed STEC. Moreover, animal studies have demonstrated that swine are susceptible to STEC O157:H7 infection and can shed the bacterium for 2 months. A limited number of molecular epidemiologic studies, however, have provided conflicting evidence regarding the relationship between swine STEC and human illness. The role that swine play in STEC transmission to people and the contribution to human disease frequency requires further evaluation.

Keywords

shiga toxin-producing Escherichia coli (STEC)swinefood safety

Information

Type
Review Article
Information
Animal Health Research Reviews , Volume 15 , Issue 1 , June 2014 , pp. 63 - 75
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Ateba, CN and Mbewe, M (2011). Detection of Escherichia coli O157:H7 virulence genes in isolates from beef, pork, water, human and animal species in the northwest province, South Africa: public health implications. Research in Microbiology 162: 240–248.Google Scholar
Baker, DR, Moxley, RA, Steele, MB, LeJeune, JT, Christopher-Hennings, J, Chen, DG, Hardwidge, PR and Francis, DH (2007). Differences in virulence among Escherichia coli O157:H7 strains isolated from humans during disease outbreaks and from healthy cattle. Applied and Environmental Microbiology 73: 7338–7346.Google Scholar
Barrett, TJ, Lior, H, Green, JH, Khakhria, R, Wells, JG, Bell, BP, Greene, KD, Lewis, J and Griffin, PM (1994). Laboratory investigation of a multistate food-borne outbreak of Escherichia coli O157:H7 by using pulsed-field gel electrophoresis and phage typing. Journal of Clinical Microbiology 32: 3013–3017.Google Scholar
Bertschinger, HU and Gyles, CL (1994). Oedema disease of pigs. In: Gyles, CL (ed) Escherichia coli in Doemstic Animals and Humans. Wallingford, UK: CAB International, pp. 193–219.Google Scholar
Bettelheim, KA (2007). The non-O157 Shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Critical Reviews in Microbiology 33: 67–87.CrossRefGoogle ScholarPubMed
Beutin, L, Krause, G, Zimmermann, S, Kaulfuss, S and Gleier, K (2004). Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. Journal of Clinical Microbiology 42: 1099–1108.Google Scholar
Beutin, L, Miko, A, Krause, G, Pries, K, Haby, S, Steege, K and Albrecht, 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 and Environmental Microbiology 73: 4769–4775.CrossRefGoogle ScholarPubMed
Beutin, L, Kruger, U, Krause, G, Miko, A, Martin, A and Strauch, E (2008). Evaluation of major types of Shiga toxin 2e-producing Escherichia coli bacteria present in food, pigs, and the environment as potential pathogens for humans. Applied and Environmental Microbiology 74: 4806–4816.Google Scholar
Bielaszewska, M, Mellmann, A, Zhang, W, Kock, R, Fruth, A, Bauwens, A, Peters, G and Karch, H (2011). Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infectious Diseases 11: 671–676.Google Scholar
Bonardi, S, Brindani, F, Pizzin, G, Lucidi, L, D'Incau, M, Liebana, E and Morabito, S (2003). Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin-producing Escherichia coli O157 in pigs at slaughter in Italy. International Journal of Food Microbiology 85: 101–110.Google Scholar
Booher, SL, Cornick, NA and Moon, HW (2002). Persistence of Escherichia coli O157: H7 in experimentally infected swine. Veterinary Microbiology 89: 69–81.Google Scholar
Borges, CA, Beraldo, LG, Maluta, RP, Cardozo, MV, Guth, BE, Rigobelo, EC and de Avila, FA (2012). Shiga toxigenic and atypical enteropathogenic Escherichia coli in the feces and carcasses of slaughtered pigs. Foodborne Pathogens and Disease 9: 1119–1125.Google Scholar
Borie, C, Monreal, Z, Guerrero, P, Sanchez, ML, Martinez, J, Arellano, TM and Prado, V (1997). Prevalence and characterization of enterohaemorrhagic Escherichia coli isoated from healthy cattle and pigs slaughtered in Santiago, Chile. Archivos De Medicina Veterinaria 29: 205–212.Google Scholar
Botteldoorn, N, Heyndrickx, M, Rijpens, N and Herman, L (2003). Detection and characterization of verotoxigenic Escherichia coli by a VTEC/EHEC multiplex PCR in porcine faeces and pig carcass swabs. Research in Microbiology 154: 97–104.CrossRefGoogle ScholarPubMed
Brooks, HJ, Mollison, BD, Bettelheim, KA, Matejka, K, Paterson, KA and Ward, VK (2001). Occurrence and virulence factors of non-O157 Shiga toxin-producing Escherichia coli in retail meat in Dunedin, New Zealand. Letters in Applied Microbiology 32: 118–122.Google Scholar
Bugarel, M, Martin, A, Fach, P and Beutin, L (2011). Virulence gene profiling of enterohemorrhagic (EHEC) and enteropathogenic (EPEC) Escherichia coli strains: a basis for molecular risk assessment of typical and atypical EPEC strains. BMC Microbiology 11: 142.Google Scholar
Bush, E (1997). U.S. swine herd appears free of Escherichia coli O157: H7. Food Safety Digest January/February: 4.Google Scholar
Carter, AO, Borczyk, AA, Carlson, JA, Harvey, B, Hockin, JC, Karmali, MA, Krishnan, C, Korn, DA and Lior, H (1987). A severe outbreak of Escherichia coli O157: H7 – associated hemorrhagic colitis in a nursing home. New England Journal of Medicine 317: 1496–1500.Google Scholar
CDC (1995a). Escherichia coli O157:H7 outbreak linked to commercially distributed dry-cured salami – Washington and California, 1994. Morbidity and Mortality Weekly Report 44: 157–160.Google Scholar
CDC (1995b). Community outbreak of hemolytic uremic syndrome attributable to Escherichia coli O111: NM-South Australia, 1995. Morbidity and Mortality Weekly Report 44: 550–558.Google Scholar
CDC (2012). National Shiga toxin-producing Escherichia coli (STEC) surveillance annual summary, 2009. [Available online at http://www.cdc.gov/ncezid/dfwed/PDFs/national-stec-surv-summ-2009-508c.pdf]. Last accessed January 31, 2013.Google Scholar
Chapman, TA, Wu, XY, Barchia, I, Bettelheim, KA, Driesen, S, Trott, D, Wilson, M and Chin, JJ (2006). Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Applied and Environmental Microbiology 72: 4782–4795.Google Scholar
Cobbold, R and Desmarchelier, P (2000). A longitudinal study of Shiga-toxigenic Escherichia coli (STEC) prevalence in three Australian diary herds. Veterinary Microbiology 71: 125–137.Google Scholar
Cobbold, R and Desmarchelier, P (2001). Characterisation and clonal relationships of Shiga-toxigenic Escherichia coli (STEC) isolated from Australian dairy cattle. Veterinary Microbiology 79: 323–335.CrossRefGoogle ScholarPubMed
Conedera, G, Mattiazzi, E, Russo, F, Chiesa, E, Scorzato, I, Grandesso, S, Bessegato, A, Fioravanti, A and Caprioli, A (2007). A family outbreak of Escherichia coli O157 haemorrhagic colitis caused by pork meat salami. Epidemiology and Infection 135: 311–314.Google Scholar
Cornick, NA (2010). Tylosin and chlorotetracycline decrease the duration of fecal shedding of E. coli O157: H7 by swine. Veterinary Microbiology 143: 417–419.Google Scholar
Cornick, NA and Helgerson, AF (2004). Transmission and infectious dose of Escherichia coli O157: H7 in swine. Applied and Environmental Microbiology 70: 5331–5335.Google Scholar
Cornick, NA and Vukhac, H (2008). Indirect transmission of Escherichia coli O157: H7 occurs readily among swine but not among sheep. Applied and Environmental Microbiology 74: 2488–2491.Google Scholar
Cornick, NA, Booher, SL and Moon, HW (2002). Intimin facilitates colonization by Escherichia coli O157: H7 in adult ruminants. Infection and Immunity 70: 2704–2707.CrossRefGoogle ScholarPubMed
Cray, WC Jr, and Moon, HW (1995). Experimental infection of calves and adult cattle with Escherichia coli O157: H7. Applied and Environmental Microbiology 61: 1586–1590.Google Scholar
Dean-Nystrom, EA, Bosworth, BT, Cray, WC Jr, and Moon, HW (1997). Pathogenicity of Escherichia coli O157: H7 in the intestines of neonatal calves. Infection and Immunity 65: 1842–1848.CrossRefGoogle ScholarPubMed
Dean-Nystrom, EA, Melton-Celsa, AR, Pohlenz, JF, Moon, HW and O'Brien, AD (2003). Comparative pathogenicity of Escherichia coli O157 and intimin-negative non-O157 Shiga toxin-producing E coli strains in neonatal pigs. Infection and Immunity 71: 6526–6533.CrossRefGoogle ScholarPubMed
DeGrandis, S, Law, H, Brunton, J, Gyles, C and Lingwood, CA (1989). Globotetraosylceramide is recognized by the pig edema disease toxin. Journal of Biological Chemistry 264: 12520–12525.Google Scholar
Diekema, DJ, Barr, J, Boyken, LD, Buschelman, BJ, Jones, RN, Pfaller, MA and Herwaldt, LA (1997). A cluster of serious Escherichia coli infections in a neonatal intensive-care unit. Infection Control and Hospital Epidemiology 18: 774–776.Google Scholar
Dohoo, I, Martin, W, and Stryhn, H (2010). Introduction to observational studies. In: Veterinary Epidemiologic Research, 2nd edn. Charlottetown, Prince Edward Island, Canada: VER Inc., pp. 151–162.Google Scholar
Doyle, MP, Archer, J, Kaspar, CW and Weiss, R (2006). Human illness casued by E. coli O157:H7 from food and non-food sources. [Available online at http://fri.wisc.edu/docs/pdf/FRIBrief_EcoliO157H7humanillness.pdf]. Last accessed February 10, 2013.Google Scholar
Durso, LM, Reynolds, K, Bauer, N Jr, and Keen, JE (2005). Shiga-toxigenic Escherichia coli O157: H7 infections among livestock exhibitors and visitors at a Texas County Fair. Vector Borne and Zoonotic Diseases 5: 193–201.Google Scholar
EFSA (2009). Technical specifications for the monitoring and reporting of verotoxigenic Escherichia coli (VTEC) on animals and food (VTEC surveys on animals and food). EFSA Journal 7: 1366.Google Scholar
Eriksson, E, Nerbrink, E, Borch, E, Aspan, A and Gunnarsson, A (2003). Verocytotoxin-producing Escherichia coli O157: H7 in the Swedish pig population. Veterinary Record 152: 712–717.CrossRefGoogle ScholarPubMed
Fairbrother, JM and Gyles, CL (2012). Colibacillosis. In: Zimmerman, JJ, Karriker, LA, Ramirez, A, Schwartz, KJ and Stevenson, GW (eds) Diseases of Swine, 10th edn. Hoboken, NJ: John Wiley & Sons, Inc., pp. 723–747.Google Scholar
Feder, I, Wallace, FM, Gray, JT, Fratamico, P, Fedorka-Cray, PJ, Pearce, RA, Call, JE, Perrine, R and Luchansky, JB (2003). Isolation of Escherichia coli O157: H7 from intact colon fecal samples of swine. Emerging Infectious Diseases 9: 380–383.Google Scholar
Feder, I, Gray, JT, Pearce, RA, Fratamico, PM, Bush, E, Porto-Fett, A, Wallace, FM, Fedorka-Cray, PJ and Luchansky, JB (2007). Testing of swine feces obtained through the National Animal Health Monitoring System's Swine 2000 study for the presence of Escherichia coli O157: H7. Journal of Food Protection 70: 1489–1492.Google Scholar
Feng, PC, Jinneman, K, Scheutz, F and Monday, SR (2011). Specificity of PCR and serological assays in the detection of Escherichia coli Shiga toxin subtypes. Applied and Environmental Microbiology 77: 6699–6702.Google Scholar
Franke, S, Harmsen, D, Caprioli, A, Pierard, D, Wieler, LH and Karch, H (1995). Clonal relatedness of Shiga-like toxin-producing Escherichia coli O101 strains of human and porcine origin. Journal of Clinical Microbiology 33: 3174–3178.Google Scholar
Fratamico, PM, Bagi, LK, Bush, EJ and Solow, BT (2004). Prevalence and characterization of Shiga toxin-producing Escherichia coli in swine feces recovered in the National Animal Health Monitoring System's Swine 2000 study. Applied and Environmental Microbiology 70: 7173–7178.Google Scholar
Fratamico, PM, Bhagwat, AA, Injaian, L and Fedorka-Cray, PJ (2008). Characterization of Shiga toxin-producing Escherichia coli strains isolated from swine feces. Foodborne Pathogen and Disease 5: 827–838.Google Scholar
Friedrich, AW, Bielaszewska, M, Zhang, WL, Pulz, M, Kuczius, T, Ammon, A and Karch, H (2002). Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. Journal of Infectious Diseases 185: 74–84.Google Scholar
FSIS (2011). USDA Food Safety and Inspection Service. Shiga toxin-producing Escherichia coli in certain raw beef products. Federal Register 76: 58157–58165.Google Scholar
Griffin, PM and Tauxe, RV (1991). The epidemiology of infections caused by Escherichia coli O157: H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiologic Reviews 13: 60–98.Google Scholar
Griffin, PM, Ostroff, SM, Tauxe, RV, Greene, KD, Wells, JG, Lewis, JH and Blake, PA (1988). Illnesses associated with Escherichia coli O157: H7 infections. A broad clinical spectrum. Annals of Internal Medicine 109: 705–712.Google Scholar
Gyles, CL (2007). Shiga toxin-producing Escherichia coli: an overview. Journal of Animal Science 85: E45–E62.Google Scholar
Henderson, H (2008). Direct and indirect zoonotic transmission of Shiga toxin-producing Escherichia coli. Journal of the American Veterinary Medical Association 232: 848–859.CrossRefGoogle ScholarPubMed
Heuvelink, AE, Zwartkruis-Nahuis, JT, van den Biggelaar, FL, van Leeuwen, WJ and de Boer, E (1999). Isolation and characterization of verocytotoxin-producing Escherichia coli O157 from slaughter pigs and poultry. International Journal of Food Microbiology 52: 67–75.Google Scholar
Hoffmann, S, Batz, MB and Morris, JG (2012). Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. Journal of Food Protection 75: 1292–1302.Google Scholar
Izumiya, H, Terajima, J, Wada, A, Inagaki, Y, Itoh, KI, Tamura, K and Watanabe, H (1997). Molecular typing of enterohemorrhagic Escherichia coli O157: H7 isolates in Japan by using pulsed-field gel electrophoresis. Journal of Clinical Microbiology 35: 1675–1680.Google Scholar
Jay, MT, Cooley, M, Carychao, D, Wiscomb, GW, Sweitzer, RA, Crawford-Miksza, L, Farrar, JA, Lau, DK, O'Connell, J, Millington, A, Asmundson, RV, Atwill, ER and Mandrell, RE (2007). Escherichia coli O157: H7 in feral swine near spinach fields and cattle, central California coast. Emerging Infectious Diseases 13: 1908–1911.CrossRefGoogle ScholarPubMed
Jo, MY, Kim, JH, Lim, JH, Kang, MY, Koh, HB, Park, YH, Yoon, DY, Chae, JS, Eo, SK and Lee, JH (2004). Prevalence and characteristics of Escherichia coli O157 from major food animals in Korea. International Journal of Food Microbiology 95: 41–49.Google Scholar
Johnsen, G, Wasteson, Y, Heir, E, Berget, OI and Herikstad, H (2001). Escherichia coli O157: H7 in faeces from cattle, sheep and pigs in the southwest part of Norway during 1998 and 1999. International Journal of Food Microbiology 65: 193–200.Google Scholar
Jordan, DM, Cornick, N, Torres, AG, Dean-Nystrom, EA, Kaper, JB and Moon, HW (2004). Long polar fimbriae contribute to colonization by Escherichia coli O157: H7 in vivo. Infection and Immunity 72: 6168–6171.Google Scholar
Jordan, DM, Booher, SL and Moon, HW (2005). Escherichia coli O157: H7 does not require intimin to persist in pigs. Infection and Immunity 73: 1865–1867.CrossRefGoogle ScholarPubMed
Karmali, MA (1989). Infection by verocytotoxin-producing Escherichia coli. Clinical Microbiology Reviews 2: 15–38.CrossRefGoogle ScholarPubMed
Karmali, MA, Petric, M, Lim, C, Fleming, PC, Arbus, GS and Lior, H (1985). The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. Journal of Infectious Diseases 151: 775–782.Google Scholar
Karmali, MA, Gannon, V and Sargeant, JM (2010). Verocytotoxin-producing Escherichia coli (VTEC). Veterinary Microbiology 140: 360–370.Google Scholar
Kaspar, C, Doyle, ME and Archer, J (2010). White paper on non-O157:H7 Shiga toxin-producing E. coli from meat and non-meat sources. [Available online at http://fri.wisc.edu/docs/pdf/FRI_Brief_NonO157STEC_4_10.pdf]. Last accessed February 10, 2013.Google Scholar
Kaufmann, M, Zweifel, C, Blanco, M, Blanco, JE, Blanco, J, Beutin, L and Stephan, R (2006). Escherichia coli O157 and non-O157 Shiga toxin-producing Escherichia coli in fecal samples of finished pigs at slaughter in Switzerland. Journal of Food Protection 69: 260–266.Google Scholar
Keen, JE, Wittum, TE, Dunn, JR, Bono, JL and Durso, LM (2006). Shiga-toxigenic Escherichia coli O157 in agricultural fair livestock, United States. Emerging Infectious Diseases 12: 780–786.Google Scholar
Keen, JE, Durso, LM and Meehan, TP (2007). Isolation of Salmonella enterica and Shiga-toxigenic Escherichia coli O157 from feces of animals in public contact areas of United States zoological parks. Applied and Environmental Microbiology 73: 362–365.Google Scholar
Kennedy, CA, Lenahan, M, Ryan, M, Fanning, S, Sheridan, J, McNamara, E, Carroll, A and Sweeney, T (2010). Shiga toxin-producing Escherichia coli isolated from human and pig origin induce different gene expression profiles in human Caco-2 epithelial cells. Livestock Science 133: 189–191.Google Scholar
Keum, HO, Kim, HK, Rho, SM, Moon, HJ, Park, SJ and Park, BK (2010). Comparative study of Clostridium perfringens, Salmonella spp. and E. coli focused on characteristics of E. coli O157 isolated from pigs of HACCP- and non-HACCP-accredited swine farms in Korea. Korean Journal of Veterinary Research 50: 113–116.Google Scholar
Kijima-Tanaka, M, Ishihara, K, Kojima, A, Morioka, A, Nagata, R, Kawanishi, M, Nakazawa, M, Tamura, Y and Takahashi, T (2005). A national surveillance of Shiga toxin-producing Escherichia coli in food-producing animals in Japan. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 52: 230–237.Google Scholar
Kim, J, Kim, S, Kwon, N, Bae, W, Lim, J, Koo, H, Kim, J, Noh, K, Jung, W, Park, K, Park, Y, Kim, JY, Kim, SH, Kwon, NH, Bae, WK, Lim, JY, Koo, HC, Kim, JM, Noh, KM, Jung, WK, Park, KT and Park, YH (2005). Isolation and identification of Escherichia coli O157: H7 using different detection methods and molecular determination by multiplex PCR and RAPD. Journal of Veterinary Science 6: 7–19.Google Scholar
Kobayashi, H, Ly Thi Lien, K, Tran Thi, P, Yamasaki, S and Taniguchi, T (2003). Prevalence of pathogenic Escherichia coli in a swine breeding environment in Can Tho Province, Vietnam. Japan Agricultural Research Quarterly 37: 59–63.CrossRefGoogle Scholar
Lanier, WA, Leeper, MM, Smith, KE, Tillman, GE, Holt, KG and Gerner-Smidt, P (2009). Pulsed-field gel electrophoresis subtypes of Shiga toxin-producing Escherichia coli O157 isolated from ground beef and humans, United States, 2001–2006. Foodborne Pathogens and Disease 6: 1075–1082.Google Scholar
Law, D (2000). Virulence factors of Escherichia coli O157 and other Shiga toxin-producing E. coli. Journal of Applied Microbiology 88: 729–745.Google Scholar
Lenahan, M, Crowley, H, O'Brien, SB, Byrne, C, Sweeney, T and Sheridan, JJ (2009a). The potential use of chilling to control the growth of Enterobacteriaceae on porcine carcasses and the incidence of E. coli O157: H7 in pigs. Journal of Applied Microbiology 106: 1512–1520.Google Scholar
Lenahan, M, O'Brien, SB, Byrne, C, Ryan, M, Kennedy, CA, McNamara, EB, Fanning, S, Sheridan, JJ and Sweeney, T (2009b). Molecular characterization of Irish E. coli O157: H7 isolates of human, bovine, ovine and porcine origin. Journal of Applied Microbiology 107: 1340–1349.Google Scholar
Leung, PH, Yam, WC, Ng, WW and Peiris, JS (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.Google Scholar
Li, MC, Wang, F and Li, F (2011). Identification and molecular characterization of antimicrobial-resistant Shiga toxin-producing Escherichia coli isolated from retail meat products. Foodborne Pathogens and Disease 8: 489–493.Google Scholar
MacDonald, DM, Fyfe, M, Paccagnella, A, Trinidad, A, Louie, K and Patrick, D (2004). Escherichia coli O157: H7 outbreak linked to salami, British Columbia, Canada, 1999. Epidemiology and Infection 132: 283–289.CrossRefGoogle ScholarPubMed
Martins, RP, Da Silva, MC, Dutra, V, Nakazato, L and Leite Dda, S (2011). Prevalence of enterotoxigenic and Shiga toxin-producing Escherichia coli in pigs slaughtered in Mato Grosso, Brazil. Journal of Infection in Developing Countries 5: 123–127.Google Scholar
Milnes, AS, Sayers, AR, Stewart, I, Clifton-Hadley, FA, Davies, RH, Newell, DG, Cook, AJ, Evans, SJ, Smith, RP and Paiba, GA (2009). Factors related to the carriage of Verocytotoxigenic E. coli, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica in cattle, sheep and pigs at slaughter. Epidemiology and Infection 137: 1135–1148.Google Scholar
Muniesa, M, Recktenwald, J, Bielaszewska, M, Karch, H and 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.Google Scholar
Nakazawa, M and Akiba, M (1999). Swine as a potential reservoir of Shiga toxin-producing Escherichia coli O157: H7 in Japan. Emerging Infectious Diseases 5: 833–834.Google Scholar
Nataro, JP and Kaper, JB (1998). Diarrheagenic Escherichia coli. Clinical Microbiology Reviews 11: 142–201.Google Scholar
Oporto, B, Esteban, JI, Aduriz, G, Juste, RA and Hurtado, A (2008). Escherichia coli O157: H7 and non-O157 Shiga toxin-producing E. coli in healthy cattle, sheep and swine herds in Northern Spain. Zoonoses Public Health 55: 73–81.Google Scholar
Osek, J and Gallien, P (2002). Molecular analysis of Escherichia coli O157 strains isolated from cattle and pigs by the use of PCR and pulsed-field gel electrophoresis methods. Veterinarni Medicina 47: 149–158.Google Scholar
Oteiza, JM, Chinen, I, Miliwebsky, E and Rivas, M (2006). Isolation and characterization of Shiga toxin-producing Escherichia coli from precooked sausages (morcillas). Food Microbiology 23: 283–288.Google Scholar
Paton, AW, Ratcliff, RM, Doyle, RM, Seymour-Murray, J, Davos, D, Lanser, JA and Paton, JC (1996). Molecular microbiological investigation of an outbreak of hemolytic-uremic syndrome caused by dry fermented sausage contaminated with Shiga-like toxin-producing Escherichia coli. Journal of Clinical Microbiology 34: 1622–1627.CrossRefGoogle ScholarPubMed
Pierard, D, Huyghens, L, Lauwers, S and Lior, H (1991). Diarrhoea associated with Escherichia coli producing porcine oedema disease verotoxin. Lancet 338: 762.Google Scholar
Pinaka, O, Pournaras, S, Mouchtouri, V, Plakokefalos, E, Katsiaflaka, A, Kolokythopoulou, F, Barboutsi, E, Bitsolas, N and Hadjichristodoulou, C (2013). Shiga toxin-producing Escherichia coli in Central Greece: prevalence and virulence genes of O157: H7 and non-O157 in animal feces, vegetables, and humans. European Journal of Clinical Microbiology and Infectious Diseases 32: 1401–1408.Google Scholar
Pritchard, GC, Smith, R, Ellis-Iversen, J, Cheasty, T and Willshaw, GA (2009). Verocytotoxigenic Escherichia coli O157 in animals on public amenity premises in England and Wales, 1997 to 2007. Veterinary Record 164: 545–549.Google Scholar
Rangel, JM, Sparling, PH, Crowe, C, Griffin, PM and Swerdlow, DL (2005). Epidemiology of Escherichia coli O157: H7 outbreaks, United States, 1982–2002. Emerging Infectious Diseases 11: 603–609.Google Scholar
Rios, M, Prado, V, Trucksis, M, Arellano, C, Borie, C, Alexandre, M, Fica, A and Levine, MM (1999). Clonal diversity of Chilean isolates of enterohemorrhagic Escherichia coli from patients with hemolytic-uremic syndrome, asymptomatic subjects, animal reservoirs, and food products. Journal of Clinical Microbiology 37: 778–781.Google Scholar
Rowe, PC, Orrbine, E, Lior, H, Wells, GA and McLaine, PN (1993). Diarrhoea in close contacts as a risk factor for childhood haemolytic uraemic syndrome. The CPKDRC co-investigators. Epidemiology and Infection 110: 9–16.Google Scholar
Samadpour, M (1995). Molecular epidemiology of Escherichia coli O157: H7 by restriction fragment length polymorphism using Shiga-like toxin genes. Journal of Clinical Microbiology 33: 2150–2154.Google Scholar
Samadpour, M, Ongerth, JE, Liston, J, Tran, N, Nguyen, D, Whittam, TS, Wilson, RA and Tarr, PI (1994) Occurrence of Shiga-like toxin-producing Escherichia coli in retail fresh seafood, beef, lamb, pork, and poultry from grocery stores in Seattle, Washington. Applied and Environmental Microbiology 60: 1038–1040.Google Scholar
Sánchez, S, Martínez, R, García, A, Vidal, D, Blanco, J, Blanco, M, Blanco, JE, Mora, A, Herrera-León, S and Echeita, A (2010). Detection and characterisation of O157: H7 and non-O157 Shiga toxin-producing Escherichia coli in wild boars. Veterinary Microbiology 143: 420–423.CrossRefGoogle ScholarPubMed
Scallan, E, Hoekstra, RM, Angulo, FJ, Tauxe, RV, Widdowson, MA, Roy, SL, Jones, JL and Griffin, PM (2011). Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases 17: 7–15.Google Scholar
Sheoran, AS, Chapman-Bonofiglio, S, Harvey, BR, Mukherjee, J, Georgiou, G, Donohue-Rolfe, A and Tzipori, S (2005). Human antibody against Shiga toxin 2 administered to piglets after the onset of diarrhea due to Escherichia coli O157: H7 prevents fatal systemic complications. Infection and Immunity 73: 4607–4613.Google Scholar
Shringi, S, Garcia, A, Lahmers, KK, Potter, KA, Muthupalani, S, Swennes, AG, Hovde, CJ, Call, DR, Fox, JG and Besser, TE (2012). Differential virulence of clinical and bovine-biased enterohemorrhagic Escherichia coli O157: H7 genotypes in piglet and Dutch belted rabbit models. Infection and Immunity 80: 369–380.Google Scholar
Singer, RS, Sischo, WM and Carpenter, TE (2004). Exploration of biases that affect the interpretation of restriction fragment patterns produced by pulsed-field gel electrophoresis. Journal of Clinical Microbiology 42: 5502–5511.Google Scholar
Slanec, T, Fruth, A, Creuzburg, K and Schmidt, H (2009). Molecular analysis of virulence profiles and Shiga toxin genes in food-borne Shiga toxin-producing Escherichia coli. Applied and Environmental Microbiology 75: 6187–6197.Google Scholar
Sonntag, AK, Bielaszewska, M, Mellmann, A, Dierksen, N, Schierack, P, Wieler, LH, Schmidt, MA and Karch, H (2005). Shiga toxin 2e-producing Escherichia coli isolates from humans and pigs differ in their virulence profiles and interactions with intestinal epithelial cells. Applied and Environmental Microbiology 71: 8855–8863.Google Scholar
Spika, JS, Parsons, JE, Nordenberg, D, Wells, JG, Gunn, RA and Blake, PA (1986). Hemolytic uremic syndrome and diarrhea associated with Escherichia coli O157: H7 in a day care center. Journal of Pediatrics 109: 287–291.Google Scholar
Tarr, PI, Gordon, CA and Chandler, WL (2005). Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. The Lancet 365: 1073–1086.Google Scholar
Thomas, A, Cheasty, T, Chart, H and Rowe, B (1994). Isolation of Vero cytotoxin-producing Escherichia coli serotypes O9ab:H- and O101: H-carrying VT2 variant gene sequences from a patient with haemolytic uraemic syndrome. European Journal of Clinical Microbiology and Infectious Diseases 13: 1074–1076.Google Scholar
Trotz-Williams, LA, Mercer, NJ, Walters, JM, Maki, AM and Johnson, RP (2012). Pork implicated in a Shiga toxin-producing Escherichia coli O157: H7 outbreak in Ontario, Canada. Canadian Journal of Public Health. Revue Canadienne de Sante Publique 103: e322–e326.Google Scholar
Varma, JK, Greene, KD, Reller, ME, DeLong, SM, Trottier, J, Nowicki, SF, DiOrio, M, Koch, EM, Bannerman, TL, York, ST, Lambert-Fair, MA, Wells, JG and Mead, PS (2003). An outbreak of Escherichia coli O157 infection following exposure to a contaminated building. The Journal of American Medical Association 290: 2709–2712.Google Scholar
Vernozy-Rozand, C, Montet, MP, Bertin, Y, Trably, F, Girardeau, JP, Martin, C, Livrelli, V and Beutin, L (2004). Serotyping, stx2 subtyping, and characterization of the locus of enterocyte effacement island of Shiga toxin-producing Escherichia coli and E. coli O157: H7 strains isolated from the environment in France. Applied and Environmental Microbiology 70: 2556–2559.Google Scholar
Wahlstrom, H, Tysen, E, Olsson Engvall, E, Brandstrom, B, Eriksson, E, Morner, T and Vagsholm, I (2003). Survey of Campylobacter species, VTEC O157 and Salmonella species in Swedish wildlife. Veterinary Record 153: 74–80.Google Scholar
Wells, JE, Kalchayanand, N, Berry, ED and Oliver, WT (2012). Effects of antimicrobials fed as dietary growth promoters on fecal shedding of Campylobacter, Salmonella, and Shiga-toxin producing Escherichia coli in swine. Journal of Applied Microbiology 114: 318–328.Google Scholar
Williams, DM, Sreedhar, SS, Mickell, JJ and Chan, JC (2002). Acute kidney failure: a pediatric experience over 20 years. Archives of Pediatrics and Adolescent Medicine 156: 893–900.Google Scholar
Williams, RC, Isaacs, S, Decou, ML, Richardson, EA, Buffett, MC, Slinger, RW, Brodsky, MH, Ciebin, BW, Ellis, A and Hockin, J (2000). Illness outbreak associated with Escherichia coli O157: H7 in Genoa salami. E. coli O157: H7 Working Group. Canadian Medical Association Journal 162: 1409–1413.Google Scholar
Xia, X, Meng, J, McDermott, PF, Ayers, S, Blickenstaff, K, Tran, TT, Abbott, J, Zheng, J and Zhao, S (2010). Presence and characterization of Shiga toxin-producing Escherichia coli and other potentially diarrheagenic E. coli strains in retail meats. Applied and Environmental Microbiology 76: 1709–1717.Google Scholar
Yan, Y, Shi, Y, Cao, D, Meng, X, Xia, L and Sun, J (2011). Prevalence of Stx phages in environments of a pig farm and lysogenic infection of the field E. coli O157 isolates with a recombinant converting phage. Current Microbiology 62: 458–464.Google Scholar
Zweifel, C, Schumacher, S, Beutin, L, Blanco, J and Stephan, R (2006). Virulence profiles of Shiga toxin 2e-producing Escherichia coli isolated from healthy pig at slaughter. Veterinary Microbiology 117: 328–332.Google Scholar