Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113

A Monaghan, B Byrne, DA McDowell, A M Carroll, E B McNamara, D J Bolton

    Research output: Contribution to journalArticle

    12 Citations (Scopus)

    Abstract

    Thirty-nine Shiga toxin–producing Escherichia coli (STEC) O113 Irish farm, abattoir, and clinical isolates were analyzed in conjunction with eight Australian, New Zealand, and Norwegian strains for H (flagellar) antigens, virulence gene profile (eaeA, hlyA, tir, espA, espB katP, espP, etpD, saa, sab, toxB, iha, lpfAO157/OI-141, lpfAO113, and lpfAO157/OI-154), Shiga toxin gene variants (stx1c, stx1d, stx2, stx2c, stx2dact, stx2e, stx2f, and stx2g) and were genotyped using pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). All of the Irish strains were O113:H4, regardless of source, while all non-Irish isolates carried the H21 flagellar antigen. The stx1 gene was present in 30 O113:H4 strains only, whereas the stx2d gene was common to all isolates regardless ofsource. In contrast, eaeA was absent, while hlyA was found in the Australian, New Zealand, Norwegian, and two of the Irish human clinical isolates. saa was present in the O113:H21 but not in the O113:H4 serotype. To the best of the author’s knowledge, this is the first report of clinically significant STEC lacking both the eaeA and saa genes. PFGE analysis was inconclusive; however, MLST grouped the strains into three sequence types (ST): ST10, ST56, and ST223. Based on our findings, it was concluded that the stx2d gene is common in STEC O113, which are generally eaeA negative. Furthermore, STEC O113:H4 is a new, emerging bovine serotype of human clinical significance
    LanguageEnglish
    Pages1088-1096
    JournalFoodborne Pathogens and Disease
    Volume9
    Issue number12
    DOIs
    Publication statusPublished - 2012

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    Shiga-Toxigenic Escherichia coli
    Shiga toxin-producing Escherichia coli
    Food
    farms
    Genes
    Multilocus Sequence Typing
    genes
    Pulsed Field Gel Electrophoresis
    pulsed-field gel electrophoresis
    New Zealand
    serotypes
    Shiga Toxin
    antigens
    Shiga toxin
    Abattoirs
    slaughterhouses
    Virulence
    Farms
    virulence
    Antigens

    Cite this

    Monaghan, A., Byrne, B., McDowell, DA., Carroll, A. M., McNamara, E. B., & Bolton, D. J. (2012). Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113. Foodborne Pathogens and Disease, 9(12), 1088-1096. https://doi.org/10.1089/fpd.2012.1257
    Monaghan, A ; Byrne, B ; McDowell, DA ; Carroll, A M ; McNamara, E B ; Bolton, D J. / Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113. In: Foodborne Pathogens and Disease. 2012 ; Vol. 9, No. 12. pp. 1088-1096.
    @article{a06fb27566ab44978fda024f96965f0d,
    title = "Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113",
    abstract = "Thirty-nine Shiga toxin–producing Escherichia coli (STEC) O113 Irish farm, abattoir, and clinical isolates were analyzed in conjunction with eight Australian, New Zealand, and Norwegian strains for H (flagellar) antigens, virulence gene profile (eaeA, hlyA, tir, espA, espB katP, espP, etpD, saa, sab, toxB, iha, lpfAO157/OI-141, lpfAO113, and lpfAO157/OI-154), Shiga toxin gene variants (stx1c, stx1d, stx2, stx2c, stx2dact, stx2e, stx2f, and stx2g) and were genotyped using pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). All of the Irish strains were O113:H4, regardless of source, while all non-Irish isolates carried the H21 flagellar antigen. The stx1 gene was present in 30 O113:H4 strains only, whereas the stx2d gene was common to all isolates regardless ofsource. In contrast, eaeA was absent, while hlyA was found in the Australian, New Zealand, Norwegian, and two of the Irish human clinical isolates. saa was present in the O113:H21 but not in the O113:H4 serotype. To the best of the author’s knowledge, this is the first report of clinically significant STEC lacking both the eaeA and saa genes. PFGE analysis was inconclusive; however, MLST grouped the strains into three sequence types (ST): ST10, ST56, and ST223. Based on our findings, it was concluded that the stx2d gene is common in STEC O113, which are generally eaeA negative. Furthermore, STEC O113:H4 is a new, emerging bovine serotype of human clinical significance",
    author = "A Monaghan and B Byrne and DA McDowell and Carroll, {A M} and McNamara, {E B} and Bolton, {D J}",
    note = "Reference text: Aldick T, Bielaszewska M, Zhang W, Brockmeyer J, Schmidt H, Friedrich AW, Kim KS, Schmidt MA, Karch H. Hemolysin from Shiga toxin–negative Escherichia coli O26 strains injures microvascular endothelium. Microbes Infect 2007;9:282–290. Anonymous. The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-Borne Outbreaks in the European Union in 2009. EFSA J 2011;9:2090. Beutin L, Zimmermann S, Gleier K. Human infections with Shiga toxin–producing Escherichia coli other than serogroup O157 in Germany. Emerg Infect Dis 1998;4:635–639. Beutin L, Kaulfuss S, Cheasty T, Brandenburg B, Zimmermann S, Gleier K, Willshaw GA, Smith HR. Characteristics and association with disease of two major subclones of Shiga toxin (Verocytotoxin)–producing strains of Escherichia coli (STEC) O157 that are present among isolates from patients in Germany. Diagn Microbiol Infect Dis 2002;44:337–346. Beutin L, Kong Q, Feng L, Wang Q, Krause G, Leomil L, Jin Q, Wang L. Development of PCR assays targeting the genes involved in synthesis and assembly of the new Escherichia coli O174 and O177 O antigens. J Clin Microbiol 2005;43:5143– 5149. Blanco J, Blanco M, Blanco JE, Mora A, Gonza ´lez EA, Bernardez MI, Alonso MP, Coira A, Rodriguez A, Rey J, Alonso JM, Usera MA. 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. Exp Biol Med (Maywood) 2003;228:345–351. Blanco M, Blanco JE, Dahbi G, Mora A, Alonso MP, Varela G, Gadea MP, Schelotto F, Gonza ´lez EA, Blanco J. Typing of intimin (eae) genes from enteropathogenic Escherichia coli (EPEC) isolated from children with diarrhea in Montevideo, Uruguay Identification of two novel intimin variants (mB and xR/b2B). J Med Microbiol 2006;55:1165–1174. Bolton DJ. Verocytotoxigenic (Shiga toxin–producing) Escherichia coli: Virulence factors and pathogenicity in the farm to fork paradigm. Foodborne Pathog Dis 2011;8:357–365. Bosilevac JM, Koohmaraie M. Prevalence and characterization of non-O157 Shiga toxin–producing Escherichia coli isolated from commercial ground beef in the United States. Appl Environ Microbiol 2011;77:2103–2112. Brunder W, Schmidt H, Karch H. KatP, a novel catalase peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 1996;142:3305–3315. Brunder W, Schmidt H, Karch H. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol Microbiol 1997;24: 767–778. Burk C, Dietrich R, Acar G, Moravek M, Bulte M, Martlbauer E. Identification and characterization of a new variant of Shiga toxin 1 in Escherichia coli ONT:H19 of bovine origin. J Clin Microbiol 2003;41:2106–2112. Cebula TA, Payne WL, Feng P. Simultaneous identification of strains of Escherichia coli serotype O157:H7 and their Shiga-like toxin type by mismatch amplification mutation assay- multiplex PCR. J Clin Microbiol 1995;33:248–250. Decludt B, Bouvet P, Mariani-Kurkdjian P, Grimont F, Grimont PA, Hubert B, Loirat C. Haemolytic uraemic syndrome and Shiga toxin–producing Escherichia coli infection in children in France. The Societe de Nephorlogie Pediatrique Epidemiol Infect 2000; 124: 215–220. dos Santos LF, Irino K, Vaz TM, Guth BE. Set of virulence genes and genetic relatedness of O113:H21 Escherichia coli strains isolated from the animal reservoir and human infections in Brazil. J Med Microbiol 2010;59:634–640. Doughty S, Sloan J, Bennett-Wood V, Robertson M, Robins-Browne RM, Hartland EL. Identification of a novel fimbrial gene cluster related to long polar fimbriae in locus of entero- cyte effacement–negative strains of enterohemorrhagic Escherichia coli. Infect Immun 2002;70:6761–6769. Fernandez D, Irino K, Sanz ME, Padola NL, Parma AE. Characterization of Shiga toxin–producing Escherichia coli isolated from dairy cows in Argentina. Lett Appl Microbiol 2010;51: 377–382. Franke S, Gunzer F, Wieler LH, Baljer G, Karch H. Construction of recombinant Shiga-like toxin-IIv (SLT-IIv) and its use in monitoring the SLT-IIv antibody status of pigs. Vet Microbiol 1995;43:41–52. Friedrich AW, Borell J, Bielaszewska M, Fruth A, Tscha Fuller CA, Pellino CA, Flagler MJ, Strasser JE, Weiss AA. Shiga toxin subtypes display dramatic differences in potency. Infect Immun 2011;79:1329–1337. Garvey P, McKeown P, Carroll A, McNamara E. Epidemiology of verotoxigenic E. coli in Ireland, 2006. Epi-Insight 2008;9:2–3. Garvey P, McKeown P, Carroll A, McNamara E. Epidemiology of verotoxigenic E. coli in Ireland, 2007. Epi-Insight 2009a; 10(9). Garvey P, McKeown P, Carroll A, McNamara E. Epidemiology of verotoxigenic E. coli In Ireland, 2008. Epi-Insight 2009b; 10(9). Griffin PM, Tauxe RV. 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    year = "2012",
    doi = "10.1089/fpd.2012.1257",
    language = "English",
    volume = "9",
    pages = "1088--1096",
    journal = "Foodborne Pathogens and Disease",
    issn = "1535-3141",
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    Monaghan, A, Byrne, B, McDowell, DA, Carroll, AM, McNamara, EB & Bolton, DJ 2012, 'Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113', Foodborne Pathogens and Disease, vol. 9, no. 12, pp. 1088-1096. https://doi.org/10.1089/fpd.2012.1257

    Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113. / Monaghan, A; Byrne, B; McDowell, DA; Carroll, A M; McNamara, E B; Bolton, D J.

    In: Foodborne Pathogens and Disease, Vol. 9, No. 12, 2012, p. 1088-1096.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Characterization of Farm, Food, and Clinical Shiga Toxin–Producing Escherichia coli (STEC) O113

    AU - Monaghan, A

    AU - Byrne, B

    AU - McDowell, DA

    AU - Carroll, A M

    AU - McNamara, E B

    AU - Bolton, D J

    N1 - Reference text: Aldick T, Bielaszewska M, Zhang W, Brockmeyer J, Schmidt H, Friedrich AW, Kim KS, Schmidt MA, Karch H. Hemolysin from Shiga toxin–negative Escherichia coli O26 strains injures microvascular endothelium. Microbes Infect 2007;9:282–290. Anonymous. The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-Borne Outbreaks in the European Union in 2009. EFSA J 2011;9:2090. Beutin L, Zimmermann S, Gleier K. Human infections with Shiga toxin–producing Escherichia coli other than serogroup O157 in Germany. Emerg Infect Dis 1998;4:635–639. Beutin L, Kaulfuss S, Cheasty T, Brandenburg B, Zimmermann S, Gleier K, Willshaw GA, Smith HR. Characteristics and association with disease of two major subclones of Shiga toxin (Verocytotoxin)–producing strains of Escherichia coli (STEC) O157 that are present among isolates from patients in Germany. Diagn Microbiol Infect Dis 2002;44:337–346. Beutin L, Kong Q, Feng L, Wang Q, Krause G, Leomil L, Jin Q, Wang L. Development of PCR assays targeting the genes involved in synthesis and assembly of the new Escherichia coli O174 and O177 O antigens. J Clin Microbiol 2005;43:5143– 5149. Blanco J, Blanco M, Blanco JE, Mora A, Gonza ´lez EA, Bernardez MI, Alonso MP, Coira A, Rodriguez A, Rey J, Alonso JM, Usera MA. 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. Exp Biol Med (Maywood) 2003;228:345–351. Blanco M, Blanco JE, Dahbi G, Mora A, Alonso MP, Varela G, Gadea MP, Schelotto F, Gonza ´lez EA, Blanco J. Typing of intimin (eae) genes from enteropathogenic Escherichia coli (EPEC) isolated from children with diarrhea in Montevideo, Uruguay Identification of two novel intimin variants (mB and xR/b2B). J Med Microbiol 2006;55:1165–1174. Bolton DJ. Verocytotoxigenic (Shiga toxin–producing) Escherichia coli: Virulence factors and pathogenicity in the farm to fork paradigm. Foodborne Pathog Dis 2011;8:357–365. Bosilevac JM, Koohmaraie M. Prevalence and characterization of non-O157 Shiga toxin–producing Escherichia coli isolated from commercial ground beef in the United States. Appl Environ Microbiol 2011;77:2103–2112. Brunder W, Schmidt H, Karch H. KatP, a novel catalase peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 1996;142:3305–3315. Brunder W, Schmidt H, Karch H. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol Microbiol 1997;24: 767–778. Burk C, Dietrich R, Acar G, Moravek M, Bulte M, Martlbauer E. Identification and characterization of a new variant of Shiga toxin 1 in Escherichia coli ONT:H19 of bovine origin. J Clin Microbiol 2003;41:2106–2112. Cebula TA, Payne WL, Feng P. Simultaneous identification of strains of Escherichia coli serotype O157:H7 and their Shiga-like toxin type by mismatch amplification mutation assay- multiplex PCR. J Clin Microbiol 1995;33:248–250. Decludt B, Bouvet P, Mariani-Kurkdjian P, Grimont F, Grimont PA, Hubert B, Loirat C. Haemolytic uraemic syndrome and Shiga toxin–producing Escherichia coli infection in children in France. The Societe de Nephorlogie Pediatrique Epidemiol Infect 2000; 124: 215–220. dos Santos LF, Irino K, Vaz TM, Guth BE. Set of virulence genes and genetic relatedness of O113:H21 Escherichia coli strains isolated from the animal reservoir and human infections in Brazil. J Med Microbiol 2010;59:634–640. Doughty S, Sloan J, Bennett-Wood V, Robertson M, Robins-Browne RM, Hartland EL. Identification of a novel fimbrial gene cluster related to long polar fimbriae in locus of entero- cyte effacement–negative strains of enterohemorrhagic Escherichia coli. Infect Immun 2002;70:6761–6769. Fernandez D, Irino K, Sanz ME, Padola NL, Parma AE. Characterization of Shiga toxin–producing Escherichia coli isolated from dairy cows in Argentina. Lett Appl Microbiol 2010;51: 377–382. Franke S, Gunzer F, Wieler LH, Baljer G, Karch H. Construction of recombinant Shiga-like toxin-IIv (SLT-IIv) and its use in monitoring the SLT-IIv antibody status of pigs. Vet Microbiol 1995;43:41–52. Friedrich AW, Borell J, Bielaszewska M, Fruth A, Tscha Fuller CA, Pellino CA, Flagler MJ, Strasser JE, Weiss AA. Shiga toxin subtypes display dramatic differences in potency. Infect Immun 2011;79:1329–1337. Garvey P, McKeown P, Carroll A, McNamara E. Epidemiology of verotoxigenic E. coli in Ireland, 2006. Epi-Insight 2008;9:2–3. Garvey P, McKeown P, Carroll A, McNamara E. Epidemiology of verotoxigenic E. coli in Ireland, 2007. Epi-Insight 2009a; 10(9). Garvey P, McKeown P, Carroll A, McNamara E. Epidemiology of verotoxigenic E. coli In Ireland, 2008. Epi-Insight 2009b; 10(9). Griffin PM, Tauxe RV. The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev 1991;13:60–98. Gunzer F, Bohm H, Russmann H, Bitzan M, Aleksic S, Karch H. Molecular detection of sorbitol-fermenting Escherichia coli O157 in patients with hemolytic uremic syndrome. J Clin Microbiol 1992;30:1807–1810. Herold S, Paton JC, Paton AW. Sab, a novel autotransporter of locus of enterocyte effacement–negative Shiga-toxigenic Escherichia coli O113:H21, contributes to adherence and biofilm formation. Infect Immun 2009;489:3234–3243 Hii JH, Gyles C, Morooka T, Karmali MA, Clarke R, De Grandis S, Brunton JL. 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. J Clin Microbiol 1991;29: 2704–2709. Hogan MC, Gloor JM, Uhl JR, Cockerill FR, Milliner DS. 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    PY - 2012

    Y1 - 2012

    N2 - Thirty-nine Shiga toxin–producing Escherichia coli (STEC) O113 Irish farm, abattoir, and clinical isolates were analyzed in conjunction with eight Australian, New Zealand, and Norwegian strains for H (flagellar) antigens, virulence gene profile (eaeA, hlyA, tir, espA, espB katP, espP, etpD, saa, sab, toxB, iha, lpfAO157/OI-141, lpfAO113, and lpfAO157/OI-154), Shiga toxin gene variants (stx1c, stx1d, stx2, stx2c, stx2dact, stx2e, stx2f, and stx2g) and were genotyped using pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). All of the Irish strains were O113:H4, regardless of source, while all non-Irish isolates carried the H21 flagellar antigen. The stx1 gene was present in 30 O113:H4 strains only, whereas the stx2d gene was common to all isolates regardless ofsource. In contrast, eaeA was absent, while hlyA was found in the Australian, New Zealand, Norwegian, and two of the Irish human clinical isolates. saa was present in the O113:H21 but not in the O113:H4 serotype. To the best of the author’s knowledge, this is the first report of clinically significant STEC lacking both the eaeA and saa genes. PFGE analysis was inconclusive; however, MLST grouped the strains into three sequence types (ST): ST10, ST56, and ST223. Based on our findings, it was concluded that the stx2d gene is common in STEC O113, which are generally eaeA negative. Furthermore, STEC O113:H4 is a new, emerging bovine serotype of human clinical significance

    AB - Thirty-nine Shiga toxin–producing Escherichia coli (STEC) O113 Irish farm, abattoir, and clinical isolates were analyzed in conjunction with eight Australian, New Zealand, and Norwegian strains for H (flagellar) antigens, virulence gene profile (eaeA, hlyA, tir, espA, espB katP, espP, etpD, saa, sab, toxB, iha, lpfAO157/OI-141, lpfAO113, and lpfAO157/OI-154), Shiga toxin gene variants (stx1c, stx1d, stx2, stx2c, stx2dact, stx2e, stx2f, and stx2g) and were genotyped using pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). All of the Irish strains were O113:H4, regardless of source, while all non-Irish isolates carried the H21 flagellar antigen. The stx1 gene was present in 30 O113:H4 strains only, whereas the stx2d gene was common to all isolates regardless ofsource. In contrast, eaeA was absent, while hlyA was found in the Australian, New Zealand, Norwegian, and two of the Irish human clinical isolates. saa was present in the O113:H21 but not in the O113:H4 serotype. To the best of the author’s knowledge, this is the first report of clinically significant STEC lacking both the eaeA and saa genes. PFGE analysis was inconclusive; however, MLST grouped the strains into three sequence types (ST): ST10, ST56, and ST223. Based on our findings, it was concluded that the stx2d gene is common in STEC O113, which are generally eaeA negative. Furthermore, STEC O113:H4 is a new, emerging bovine serotype of human clinical significance

    U2 - 10.1089/fpd.2012.1257

    DO - 10.1089/fpd.2012.1257

    M3 - Article

    VL - 9

    SP - 1088

    EP - 1096

    JO - Foodborne Pathogens and Disease

    T2 - Foodborne Pathogens and Disease

    JF - Foodborne Pathogens and Disease

    SN - 1535-3141

    IS - 12

    ER -