A small study of Yersinia enterocolitica in pigs from birth to carcass and characterisation of porcine and human strains

D J Bolton, C Ivory, D A McDowell

    Research output: Contribution to journalArticle

    14 Citations (Scopus)

    Abstract

    The objectives of this study were to investigate the present of Yersinia enterocolitica at the different stages of production from birth to chilled carcasses; to characterise the isolates in terms of bioserotype, virulence factors (ail, ystA, ystB, inv, yadA and virF) and antibiotic resistance profiles and to examine strains causing diarrheal illness in Ireland. Rectal, throat, floor, partition, wall and/or carcass swabs and water samples were testing for Y. enterocolitica using the bacteriological analytical method. Presumptive positive isolates were confirmed using API 20E strips. The isolates were then combined with 10 clinical strains, biotyped, serotyped, their antibiotic resistance phenotypes determined by disc diffusion and tested for the presence of ail, ystA, ystB, inv, yadA and virF genes using multiplex PCR assays. Y. enterocolitica had an overall prevalence rate of 0.55% (4/726). Y. enterocolitica 2/O:9 and 1A/O:9 were detected on the farm and/or in the abattoir. The clinical isolates were 1A/O:5, 1A/O:8, 1A/O:9, 2/O:9 or 4/O:9. All biotype 1A strains were ail, ystA, yadA and virF negative but carried the ystB gene. All biotype 2 and 4 strains were ail, ystA, yadA and virF positive. Resistant to cephalothin, ampicillin and amoxicillin/clavulanic acid was common and one 2/O:9 strain was resistant to compound sulphonamides and tetracycline. Intermediate resistance to neomycin and streptomycin was also observed. The data presented may explain the low incidence of yersiniosis in Ireland and suggests that biotype 1A may present a public health risk. Neomycin and tetracycline resistance have rarely been reported in Y. enterocolitica and should be monitored in future surveillance studies.
    LanguageEnglish
    Pages521-524
    JournalFood Control
    Volume33
    DOIs
    Publication statusPublished - 2013

    Fingerprint

    Yersinia enterocolitica
    Swine
    Parturition
    Neomycin
    Microbial Drug Resistance
    Ireland
    Cephalothin
    Tetracycline Resistance
    Amoxicillin-Potassium Clavulanate Combination
    Abattoirs
    Multiplex Polymerase Chain Reaction
    Sulfonamides
    Virulence Factors
    Streptomycin
    Ampicillin
    Pharynx
    Tetracycline
    Genes
    Public Health
    Phenotype

    Keywords

    • Yersinia enterocolitica
    • Pigs
    • Clinical strains
    • Bioserotype
    • Virulence factors
    • Antibiotic resistance

    Cite this

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    title = "A small study of Yersinia enterocolitica in pigs from birth to carcass and characterisation of porcine and human strains",
    abstract = "The objectives of this study were to investigate the present of Yersinia enterocolitica at the different stages of production from birth to chilled carcasses; to characterise the isolates in terms of bioserotype, virulence factors (ail, ystA, ystB, inv, yadA and virF) and antibiotic resistance profiles and to examine strains causing diarrheal illness in Ireland. Rectal, throat, floor, partition, wall and/or carcass swabs and water samples were testing for Y. enterocolitica using the bacteriological analytical method. Presumptive positive isolates were confirmed using API 20E strips. The isolates were then combined with 10 clinical strains, biotyped, serotyped, their antibiotic resistance phenotypes determined by disc diffusion and tested for the presence of ail, ystA, ystB, inv, yadA and virF genes using multiplex PCR assays. Y. enterocolitica had an overall prevalence rate of 0.55{\%} (4/726). Y. enterocolitica 2/O:9 and 1A/O:9 were detected on the farm and/or in the abattoir. The clinical isolates were 1A/O:5, 1A/O:8, 1A/O:9, 2/O:9 or 4/O:9. All biotype 1A strains were ail, ystA, yadA and virF negative but carried the ystB gene. All biotype 2 and 4 strains were ail, ystA, yadA and virF positive. Resistant to cephalothin, ampicillin and amoxicillin/clavulanic acid was common and one 2/O:9 strain was resistant to compound sulphonamides and tetracycline. Intermediate resistance to neomycin and streptomycin was also observed. The data presented may explain the low incidence of yersiniosis in Ireland and suggests that biotype 1A may present a public health risk. Neomycin and tetracycline resistance have rarely been reported in Y. enterocolitica and should be monitored in future surveillance studies.",
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    author = "Bolton, {D J} and C Ivory and McDowell, {D A}",
    note = "Reference text: Abdel-Haq, N. M., Papadopol, R., Asmar, B. I., & Brown, W. J. (2006). Antibiotic susceptibilities of Yersinia enterocolitica recovered from children over a 12-year period. International Journal of Antimicrobial Agents, 27, 449e452. Anon. (2012). The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2010. EFSA Journal, 10(3), 2597. Batzilla, J., Heeseman, J., & Rakin, A. (2011). The pathogenic potential of Yersinia enterocolitica 1A. International Journal of Medical Microbiology, 301, 556e561. Baumgartner, A., Kuffer, M., Suter, D., Jemmi, T., & Rohner, P. (2007). Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland. International Journal of Food Microbiology, 115, 110e114. Bhagat, N., & Virdi, J. S. (2007). Distribution of virulence-associated genes in Yersinia enterocolitica biovar 1A correlates with clonal groups and not the source of isolation. FEMS Microbiology Letters, 266, 177e183. Bhagat, N., & Virdi, J. S. (2011). The enigma of Yersinia enterocolitica biovar 1A. Critical Reviews in Microbiology, 37, 25e39. Bottone, E. J. (1997). Yersinia enterocolitica: the charisma continues. Clinical Microbiological Reviews, 10, 257e276. Bottone, E. J. (1999). Yersinia enterocolitica: overview and epidemiological correlates. Microbes and Infection, 1, 323e333. Cimolai, N., Trombley, C., & Blair, G. K. (1994). Implications of Yersinia enterocolitica biotyping. Archives of Disease in Childhood, 70, 19e21. Drummond, N., Murphy, B. P., Ringwood, T., Prentice, M. B., Buckley, J. F., & Fanning, S. (2012). Yersinia enterocolitica: a brief review of the issues relating to the zoonotic pathogen, public health challenges and the pork production chain. Foodborne Pathogens and Disease, 9(3), 179e189. Fabrega, A., & Vila, J. (2012). Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enfermedades Infecciosas Microbiologia Clinica, 30(1), 24e32. Fredriksson-Ahomaa, M., Stolle, A., Siitonen, A., & Koekeala, H. (2006). Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O:3 originate mainly from pigs. Journal of Medical Microbiology, 55, 747e749. Grant, T., Bennett-Wood, V., & Robins-Browne, R. M. (1998). Identification of virulence-associated characteristics in clinical isolates of Yersinia enterocolitica lacking classical virulence markers. Infection and Immunity, 66, 1113e1120. Huovinen, E., Sihvonen, L. M., Virtanen, M. J., Haukka, K., Siitonen, A., & Kuusi, M. (2010). Symptoms and sources of Yersinia enterocolitica-infection: a case control study. BMC Infection and Disease, 10, 122. Jimenez-Valera, M., Ruiz-Bravo, A., & Ramos-Cormenzana, A. (1985). Synergistic effects of dicloxacillin or clavulanic acid in combination with penicillin G or cephalothin against Yersinia enterocolitica. Antimicrobiol Agents and Chemotherapy, 29(1), 104e106. Kouwatli, K., Bejar, V., Ruiz-Bravo, A., & Ramos-Cormenzana, A. (1981). Effect of temperature on sensitivity of Yersinia enterocolitica to beta-lactam-type agents. Microbiological Letters, 16, 55e58. Morris, J. G., Jr., Prado, V., Ferreccio, C., Robins-Browne, R. M., Bordun, A. M., Cayazzo, M., et al. (1991). Yersinia enterocolitica isolated from two cohorts of young children in Santiago, Chile: incidence of and lack of correlation between illness and proposed virulence factors. Journal of Clinical Microbiology, 29, 2784e2788. Ortiz Martainez, P. (2012). Prevalence of enteropathogenic Yersinia in pigs from different European countries and contamination in the pork chain. Dissertation. Helsinki, Finland: University of Helsinki. Prats, G., Mirelis, B., Llovet, T., Munoz, C., Miro, E., & Navarro, F. (2000). Antibiotic resistance trends in enteropathogenic bacteria isolated in 1985e1987 and 1995e 1998 in Barcelona. Antimicrobial Agents and Chemotherapy, 44, 1140e1145. Ramamurthy, T., Yoshino, K., Huang, X., Balakrish Nair, G., Carniel, E., Maruyama, T., et al. (1997). The novel heat-stable enterotoxin subtype gene (ystB) of Yersinia enterocolitica: nucleotide sequence and distribution of the yst genes. Microbial Pathogens, 23, 189e200. Rastawicki,W., Gierczynski, R., Jagielski, M., Kaluzewski, S., & Jeljaszewicz, J. (2000). Susceptibility of polish clinical strains of Yersinia enterocolitica serotype O3 to antibiotics. Internatuional Journal of Antimicrobial Agents, 13, 297e300. Revell, P. A., & Miller, V. L. (2001). Yersinia virulence: more than a plasmid. FEMS Microbiology Letters, 205, 159e164. Ringwood, T., Murphy, B. P., Drummond, N., Buckley, J. F., Coveney, A. P., Redmond, H. P., et al. (2012). Current evidence for human yersinosis in Ireland. European Journal of Clinical Microbiology and Infectious Disease, 31(11), 2969e2981. Simmonds, S. D., Noble, M. A., & Freeman, H. J. (1987). Gastrointestinal features of culture-positive Yersinia enterocolitica infection. Gastroenterology, 92, 112e117. Tennant, S. M., Grant, T. H., & Robins-Browne, R. M. (2003). Mini-review: pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunology and Medical Microbiology, 38, 127e137. Thoerner, P., Bin Kingombe, C. I., Bogli-Stuber, K., Bissig-Choisat, B.,Wassenaar, T. M., Frey, J., et al. (2003). PCR detection of virulence genes in Yersinia enterocolitica and Yersinia pseudotuberculosis and investigation of virulence gene distribution. Applied and Environmental Microbiology, 69(3), 1810e1816. Van Damme, I., Habib, I., & De Zutter, L. (2010). Yersinia enterocolitica in slaughter pig tonsils: enumeration and detection by enrichment versus direct plating culture. Food Microbiology, 27(1), 158e161. Wauters, G., Kandolo, K., & Janssens, M. (1987). Revised biogrouping scheme of Yersinia enterocolitica. Contributions to Microbiology and Immunology, 9, 14e21. Weagant, S. D., Feng,W., & Stanfield, J. T. (2007). Bacteriological analytical manual. In Yersinia enterocolitica and Yersinia pseudotuberculosis: Available at http://www. fda.gov/Food/Science Research/LaboratoryMethods/Bacteriological Analytical. White, D. G., Zhao, S., Simjee, S., Wagner, D. D., & McDermott, P. F. (2002). Antimicrobial resistance of food-borne pathogens. Microbes and Infection, 4, 405e412.",
    year = "2013",
    doi = "10.1016/j.foodcont.2013.03.039",
    language = "English",
    volume = "33",
    pages = "521--524",
    journal = "Food Control",
    issn = "0956-7135",
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    }

    A small study of Yersinia enterocolitica in pigs from birth to carcass and characterisation of porcine and human strains. / Bolton, D J; Ivory, C; McDowell, D A.

    In: Food Control, Vol. 33, 2013, p. 521-524.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - A small study of Yersinia enterocolitica in pigs from birth to carcass and characterisation of porcine and human strains

    AU - Bolton, D J

    AU - Ivory, C

    AU - McDowell, D A

    N1 - Reference text: Abdel-Haq, N. M., Papadopol, R., Asmar, B. I., & Brown, W. J. (2006). Antibiotic susceptibilities of Yersinia enterocolitica recovered from children over a 12-year period. International Journal of Antimicrobial Agents, 27, 449e452. Anon. (2012). The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2010. EFSA Journal, 10(3), 2597. Batzilla, J., Heeseman, J., & Rakin, A. (2011). The pathogenic potential of Yersinia enterocolitica 1A. International Journal of Medical Microbiology, 301, 556e561. Baumgartner, A., Kuffer, M., Suter, D., Jemmi, T., & Rohner, P. (2007). Antimicrobial resistance of Yersinia enterocolitica strains from human patients, pigs and retail pork in Switzerland. International Journal of Food Microbiology, 115, 110e114. Bhagat, N., & Virdi, J. S. (2007). Distribution of virulence-associated genes in Yersinia enterocolitica biovar 1A correlates with clonal groups and not the source of isolation. FEMS Microbiology Letters, 266, 177e183. Bhagat, N., & Virdi, J. S. (2011). The enigma of Yersinia enterocolitica biovar 1A. Critical Reviews in Microbiology, 37, 25e39. Bottone, E. J. (1997). Yersinia enterocolitica: the charisma continues. Clinical Microbiological Reviews, 10, 257e276. Bottone, E. J. (1999). Yersinia enterocolitica: overview and epidemiological correlates. Microbes and Infection, 1, 323e333. Cimolai, N., Trombley, C., & Blair, G. K. (1994). Implications of Yersinia enterocolitica biotyping. Archives of Disease in Childhood, 70, 19e21. Drummond, N., Murphy, B. P., Ringwood, T., Prentice, M. B., Buckley, J. F., & Fanning, S. (2012). Yersinia enterocolitica: a brief review of the issues relating to the zoonotic pathogen, public health challenges and the pork production chain. Foodborne Pathogens and Disease, 9(3), 179e189. Fabrega, A., & Vila, J. (2012). Yersinia enterocolitica: pathogenesis, virulence and antimicrobial resistance. Enfermedades Infecciosas Microbiologia Clinica, 30(1), 24e32. Fredriksson-Ahomaa, M., Stolle, A., Siitonen, A., & Koekeala, H. (2006). Sporadic human Yersinia enterocolitica infections caused by bioserotype 4/O:3 originate mainly from pigs. Journal of Medical Microbiology, 55, 747e749. Grant, T., Bennett-Wood, V., & Robins-Browne, R. M. (1998). Identification of virulence-associated characteristics in clinical isolates of Yersinia enterocolitica lacking classical virulence markers. Infection and Immunity, 66, 1113e1120. Huovinen, E., Sihvonen, L. M., Virtanen, M. J., Haukka, K., Siitonen, A., & Kuusi, M. (2010). Symptoms and sources of Yersinia enterocolitica-infection: a case control study. BMC Infection and Disease, 10, 122. Jimenez-Valera, M., Ruiz-Bravo, A., & Ramos-Cormenzana, A. (1985). Synergistic effects of dicloxacillin or clavulanic acid in combination with penicillin G or cephalothin against Yersinia enterocolitica. Antimicrobiol Agents and Chemotherapy, 29(1), 104e106. Kouwatli, K., Bejar, V., Ruiz-Bravo, A., & Ramos-Cormenzana, A. (1981). Effect of temperature on sensitivity of Yersinia enterocolitica to beta-lactam-type agents. Microbiological Letters, 16, 55e58. Morris, J. G., Jr., Prado, V., Ferreccio, C., Robins-Browne, R. M., Bordun, A. M., Cayazzo, M., et al. (1991). Yersinia enterocolitica isolated from two cohorts of young children in Santiago, Chile: incidence of and lack of correlation between illness and proposed virulence factors. Journal of Clinical Microbiology, 29, 2784e2788. Ortiz Martainez, P. (2012). Prevalence of enteropathogenic Yersinia in pigs from different European countries and contamination in the pork chain. Dissertation. Helsinki, Finland: University of Helsinki. Prats, G., Mirelis, B., Llovet, T., Munoz, C., Miro, E., & Navarro, F. (2000). Antibiotic resistance trends in enteropathogenic bacteria isolated in 1985e1987 and 1995e 1998 in Barcelona. Antimicrobial Agents and Chemotherapy, 44, 1140e1145. Ramamurthy, T., Yoshino, K., Huang, X., Balakrish Nair, G., Carniel, E., Maruyama, T., et al. (1997). The novel heat-stable enterotoxin subtype gene (ystB) of Yersinia enterocolitica: nucleotide sequence and distribution of the yst genes. Microbial Pathogens, 23, 189e200. Rastawicki,W., Gierczynski, R., Jagielski, M., Kaluzewski, S., & Jeljaszewicz, J. (2000). Susceptibility of polish clinical strains of Yersinia enterocolitica serotype O3 to antibiotics. Internatuional Journal of Antimicrobial Agents, 13, 297e300. Revell, P. A., & Miller, V. L. (2001). Yersinia virulence: more than a plasmid. FEMS Microbiology Letters, 205, 159e164. Ringwood, T., Murphy, B. P., Drummond, N., Buckley, J. F., Coveney, A. P., Redmond, H. P., et al. (2012). Current evidence for human yersinosis in Ireland. European Journal of Clinical Microbiology and Infectious Disease, 31(11), 2969e2981. Simmonds, S. D., Noble, M. A., & Freeman, H. J. (1987). Gastrointestinal features of culture-positive Yersinia enterocolitica infection. Gastroenterology, 92, 112e117. Tennant, S. M., Grant, T. H., & Robins-Browne, R. M. (2003). Mini-review: pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunology and Medical Microbiology, 38, 127e137. Thoerner, P., Bin Kingombe, C. I., Bogli-Stuber, K., Bissig-Choisat, B.,Wassenaar, T. M., Frey, J., et al. (2003). PCR detection of virulence genes in Yersinia enterocolitica and Yersinia pseudotuberculosis and investigation of virulence gene distribution. Applied and Environmental Microbiology, 69(3), 1810e1816. Van Damme, I., Habib, I., & De Zutter, L. (2010). Yersinia enterocolitica in slaughter pig tonsils: enumeration and detection by enrichment versus direct plating culture. Food Microbiology, 27(1), 158e161. Wauters, G., Kandolo, K., & Janssens, M. (1987). Revised biogrouping scheme of Yersinia enterocolitica. Contributions to Microbiology and Immunology, 9, 14e21. Weagant, S. D., Feng,W., & Stanfield, J. T. (2007). Bacteriological analytical manual. In Yersinia enterocolitica and Yersinia pseudotuberculosis: Available at http://www. fda.gov/Food/Science Research/LaboratoryMethods/Bacteriological Analytical. White, D. G., Zhao, S., Simjee, S., Wagner, D. D., & McDermott, P. F. (2002). Antimicrobial resistance of food-borne pathogens. Microbes and Infection, 4, 405e412.

    PY - 2013

    Y1 - 2013

    N2 - The objectives of this study were to investigate the present of Yersinia enterocolitica at the different stages of production from birth to chilled carcasses; to characterise the isolates in terms of bioserotype, virulence factors (ail, ystA, ystB, inv, yadA and virF) and antibiotic resistance profiles and to examine strains causing diarrheal illness in Ireland. Rectal, throat, floor, partition, wall and/or carcass swabs and water samples were testing for Y. enterocolitica using the bacteriological analytical method. Presumptive positive isolates were confirmed using API 20E strips. The isolates were then combined with 10 clinical strains, biotyped, serotyped, their antibiotic resistance phenotypes determined by disc diffusion and tested for the presence of ail, ystA, ystB, inv, yadA and virF genes using multiplex PCR assays. Y. enterocolitica had an overall prevalence rate of 0.55% (4/726). Y. enterocolitica 2/O:9 and 1A/O:9 were detected on the farm and/or in the abattoir. The clinical isolates were 1A/O:5, 1A/O:8, 1A/O:9, 2/O:9 or 4/O:9. All biotype 1A strains were ail, ystA, yadA and virF negative but carried the ystB gene. All biotype 2 and 4 strains were ail, ystA, yadA and virF positive. Resistant to cephalothin, ampicillin and amoxicillin/clavulanic acid was common and one 2/O:9 strain was resistant to compound sulphonamides and tetracycline. Intermediate resistance to neomycin and streptomycin was also observed. The data presented may explain the low incidence of yersiniosis in Ireland and suggests that biotype 1A may present a public health risk. Neomycin and tetracycline resistance have rarely been reported in Y. enterocolitica and should be monitored in future surveillance studies.

    AB - The objectives of this study were to investigate the present of Yersinia enterocolitica at the different stages of production from birth to chilled carcasses; to characterise the isolates in terms of bioserotype, virulence factors (ail, ystA, ystB, inv, yadA and virF) and antibiotic resistance profiles and to examine strains causing diarrheal illness in Ireland. Rectal, throat, floor, partition, wall and/or carcass swabs and water samples were testing for Y. enterocolitica using the bacteriological analytical method. Presumptive positive isolates were confirmed using API 20E strips. The isolates were then combined with 10 clinical strains, biotyped, serotyped, their antibiotic resistance phenotypes determined by disc diffusion and tested for the presence of ail, ystA, ystB, inv, yadA and virF genes using multiplex PCR assays. Y. enterocolitica had an overall prevalence rate of 0.55% (4/726). Y. enterocolitica 2/O:9 and 1A/O:9 were detected on the farm and/or in the abattoir. The clinical isolates were 1A/O:5, 1A/O:8, 1A/O:9, 2/O:9 or 4/O:9. All biotype 1A strains were ail, ystA, yadA and virF negative but carried the ystB gene. All biotype 2 and 4 strains were ail, ystA, yadA and virF positive. Resistant to cephalothin, ampicillin and amoxicillin/clavulanic acid was common and one 2/O:9 strain was resistant to compound sulphonamides and tetracycline. Intermediate resistance to neomycin and streptomycin was also observed. The data presented may explain the low incidence of yersiniosis in Ireland and suggests that biotype 1A may present a public health risk. Neomycin and tetracycline resistance have rarely been reported in Y. enterocolitica and should be monitored in future surveillance studies.

    KW - Yersinia enterocolitica

    KW - Pigs

    KW - Clinical strains

    KW - Bioserotype

    KW - Virulence factors

    KW - Antibiotic resistance

    U2 - 10.1016/j.foodcont.2013.03.039

    DO - 10.1016/j.foodcont.2013.03.039

    M3 - Article

    VL - 33

    SP - 521

    EP - 524

    JO - Food Control

    T2 - Food Control

    JF - Food Control

    SN - 0956-7135

    ER -