A study of Salmonella in pigs from birth to carcass: Serotypes, genotypes, antibioticresistance and virulence profile

D J Bolton, C Ivory, D A McDowell

    Research output: Contribution to journalArticle

    27 Citations (Scopus)

    Abstract

    A study was undertaken to investigate Salmonella in pigs at each step from birth to carcass. Environmental and/or pig samples were taken at birth, farrowing, 1st weaning, 2nd weaning, finishing, transport, lairage, bleeding and chilling of carcasses and tested for Salmonella. All isolates were characterised in terms of sero- type, phage type (where relevant) and subtyping with pulsed field gel electrophosesis (PFGE). Isolates weretested for antibiotic resistance, resistance (intI1, blaCIT, blaTem, blaPSE-1, blaOXA-1, floR, catA1, aadA1, aadA2, tetA, tetB, tetG, sul1and aphA1) and virulence (invA, rck, spvC and pefA) genes. PCR was also performed to test for the presence of the left junction, thdF-S001 and the right junction, S004-int2 or S004-yidY of Salmonella genomic island 1 (SGI1). Overall 4.3%, 27.5% and 5% of environmental, throat/rectal and carcass sampleswere Salmonella positive, respectively. S. Typhimurium DT193 was detected during production, while S. Typhimurium DT17 and U311 were present in lairage at the abattoir, where strain characterisation suggested cross contamination of the live animals occurred. The carcasses were also cross contaminated with S. Brandenburg during processing. PFGE grouped the isolates by serotype and/or phage type. The DT193 isolates displayed the ACSSuTTmMn/Gm resistance phenotype and carried the invA, spvC, rck, bla-tem, aadA2, tetA, strA virulence/antibiotic resistance markers; U311 showed an ASSuTMn resistance pattern and carried invA and tetB; DT17 was sensitive to all antibiotics tested but invA, spv and rck positive while S. Brandenburg displayed neither resistance nor virulence gene carriage. None of the isolates possessed class 1 integrons and all isolates were negative for the left and right junctions of SGI1.It was concluded that control activities should target improved biosecurity at farm level and better sanitation in lairage. This study also provides further evidence that multiple drug resistance may be associated with non-SGI1 Salmonella strains. The continued emergence of non-DT104 S. Typhimurium isolates exhibiting multidrug resistance is a cause for concern as is the persistence of highly virulent Salmonella strains in the abattoir environment.
    LanguageEnglish
    Pages298-303
    JournalInternational Journal of Food Microbiology
    Volume160
    Issue number3
    DOIs
    Publication statusPublished - 2013

    Fingerprint

    Salmonella
    Virulence
    serotypes
    virulence
    Swine
    Genotype
    Parturition
    swine
    genomic islands
    genotype
    lairage
    Genomic Islands
    Salmonella Typhimurium
    Abattoirs
    multiple drug resistance
    Multiple Drug Resistance
    Microbial Drug Resistance
    Weaning
    antibiotic resistance
    bacteriophages

    Cite this

    @article{21a9217b52e74ddf902a8dd1475628e1,
    title = "A study of Salmonella in pigs from birth to carcass: Serotypes, genotypes, antibioticresistance and virulence profile",
    abstract = "A study was undertaken to investigate Salmonella in pigs at each step from birth to carcass. Environmental and/or pig samples were taken at birth, farrowing, 1st weaning, 2nd weaning, finishing, transport, lairage, bleeding and chilling of carcasses and tested for Salmonella. All isolates were characterised in terms of sero- type, phage type (where relevant) and subtyping with pulsed field gel electrophosesis (PFGE). Isolates weretested for antibiotic resistance, resistance (intI1, blaCIT, blaTem, blaPSE-1, blaOXA-1, floR, catA1, aadA1, aadA2, tetA, tetB, tetG, sul1and aphA1) and virulence (invA, rck, spvC and pefA) genes. PCR was also performed to test for the presence of the left junction, thdF-S001 and the right junction, S004-int2 or S004-yidY of Salmonella genomic island 1 (SGI1). Overall 4.3{\%}, 27.5{\%} and 5{\%} of environmental, throat/rectal and carcass sampleswere Salmonella positive, respectively. S. Typhimurium DT193 was detected during production, while S. Typhimurium DT17 and U311 were present in lairage at the abattoir, where strain characterisation suggested cross contamination of the live animals occurred. The carcasses were also cross contaminated with S. Brandenburg during processing. PFGE grouped the isolates by serotype and/or phage type. The DT193 isolates displayed the ACSSuTTmMn/Gm resistance phenotype and carried the invA, spvC, rck, bla-tem, aadA2, tetA, strA virulence/antibiotic resistance markers; U311 showed an ASSuTMn resistance pattern and carried invA and tetB; DT17 was sensitive to all antibiotics tested but invA, spv and rck positive while S. Brandenburg displayed neither resistance nor virulence gene carriage. None of the isolates possessed class 1 integrons and all isolates were negative for the left and right junctions of SGI1.It was concluded that control activities should target improved biosecurity at farm level and better sanitation in lairage. This study also provides further evidence that multiple drug resistance may be associated with non-SGI1 Salmonella strains. The continued emergence of non-DT104 S. Typhimurium isolates exhibiting multidrug resistance is a cause for concern as is the persistence of highly virulent Salmonella strains in the abattoir environment.",
    author = "Bolton, {D J} and C Ivory and McDowell, {D A}",
    note = "Reference text: Alban, L., Stege, H., Dahl, J., 2002. The new classification system for slaughter-pig herds in the Danish Salmonella surveillance-and-control program. Preventive Veterinary Medicine 53, 133–146. Alban, L., Baptista, F.M., Mogelmose, V., Sorensen, L.L., Christensen, H., Aabo, S., Dahl, J., 2012. Salmonella surveillance and control for finisher pigs and pork in Denmark — a case study. Food Research International 45, 656–665. Alcaine, S.D., Warnick, L.D., Wiedmann, M., 2007. Antimicrobial resistance in nontyphoidal Salmonella. Journal of Food Protection 70 (3), 780–790. Anderson, E.S., Ward, L.R., de Saxe, M.J., de Sa, J.D.H., 1977. Bacteriophage-typing designations of Salmonella Typhimurium. Journal of Hygiene Cambridge 78, 297. Anon., 1990. Microbiology of Food and Animal Feeding stuffs- Horizontal method for the detection of Salmonella spp. ISO 6579: 1990 (E). Anon, 2008a. Report of the Task Force on Zoonoses Data Collection on the analysis of the baseline survey on the prevalence of Salmonella in slaughter pigs, part B. The EFSA Journal 206, 1–111. Anon, 2008b. Annual Report for 2008 from the Health Protection Surveillance Centre, Ireland. 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 (3), 2597. http://dx.doi.org/10.2903/j.efsa.2012.2597 ([442pp.]. Available online: www.efsa.europa.eu/efsajournal). Aragaw, K., Molla, B., Muckle, A., Cole, L., Wilkie, E., Poppe, C., Kleer, J., Hildebrandt, G., 2007. The characterization of Salmonella serovars isolated from apparently healthy slaughtered pigs at Addis Ababa abattoir, Ethiopia. Preventive Veterinary Medicine 82 (3–4), 252–261. Bolton, L.F., Kelley, L.C., Lee, M.D., Fedora-Cray, P.J., Mauer, J.J., 1999. Detection of multidrug resistant Salmonella enterica serotype Typhimurium DT104 based on a gene which confers cross-resistance to florfenicol and chloramphenicol. Journal of Clinical Microbiology 37, 1348–1351. Boughton, C., Leonard, F.C., Egan, J., Kelly, G., O'Mahony, P., Markey, B.K., Griffin, M., 2004. Prevalence and number of Salmonella in Irish retail pork sausages. Journal of Food Protection 67, 1834–1839. Boyd, D.A., Peters, G.A., Lai-King, N., Mulvey, M.R., 2000. Partial characterization of a genomic island associated with the multidrug resistance region of Salmonella enterica Typhimurium DT104. FEMS Microbiology Letters 189, 285–291. Callow, B.R., 1959. A new phage-typing scheme for Salmonella Typhimurium. Journal of Hygiene Cambridge 57, 3. Carattoli, A., Filetici, E., Villa, L., Dionisi, A.M., Ricci, A., Luzzi, I., 2002. Antibiotic resistance genes and Salmonella genomic island 1 in Salmonella enterica serovar Typhimurium isolated in Italy. Antimicrobial Agents and Chemotherapy 46 (9), 2821–2828. Carlson, F.A., Bolton, L.F., Briggs, C.E., Hurd, H.S., Sharma, V.K., Fedora-Kray, P.J., Jones, B.D., 1999. Detection of multiresistant Salmonella Typhimurium DT 104 using multiplex and fluorogenic PCR. Molecular and Cellular Probes 13, 213–222. Chen, S., Zhao, S., White, D.G., Schroeder, C.M., Lu, R., Yang, H., McDermott, P.F., Ayers, S., Meng, J., 2004. Characterization of multiple antimicrobial resistant Salmonella serovars isolated from retail meats. Applied and Environmental Microbiology 70, 1–7. Chu, C., Chiu, C.H., Wu, W.Y., Chu, C.H., Liu, T.P., Ou, J.T., 2001. Large drug resistance virulence plasmids of clinical isolates of Salmonella enterica serovar Choleraesuis. Antimicrobial Agents and Chemotherapy 45, 2299–2303. Dahshan, H., Shahada, F., Chuma, T., Moriki, H., Okamoto, K., 2010. Genetic analysis of multidrug-resistant Salmonella enterica serovars Stanley and Typhimurium from cattle. Veterinary Microbiology 145, 76–83. Daly, M., Fanning, S., 2000. Characterization and chromosomal mapping of antimicrobial resistance genes in Salmonella enterica serotype Typhimurium. Applied and Environmental Microbiology 66, 842–4848. De Busser, E.V., Maes, D., Houf, K., Dewulf, J., Imberechts, H., Bertrand, S., De Zutter, L., 2011. Detection and characterization of Salmonella in lairage, on pig carcasses and intestines in five slaughterhouses. International Journal of Food Microbiology 145, 279–286. Gallardo, F., Ruiz, J.,Marco, F., Towner, K.J., Vila, J., 1999. Increase in incidence of resistance to ampicillin, chloramphenicol and trimethoprimin clinical isolates of Salmonella serotype Typhimuriumwith investigation of molecular epidemiology and mechanisms of resistance. Journal of MedicalMicrobiology 48, 367–374. Gebreyes, W.A., Altier, C., 2002. Molecular characterization of multi-drug resistance determinants among Salmonella enterica serovar Typhimurium isolates collected from swine. Journal of Clinical Microbiology 40, 2813–2822. Gebreyes, W.A., Thakur, S., Davies, P.R., Funk, J.A., Altier, C., 2004. Trends in antimicrobial resistance, phage types and integrons among Salmonella serotypes from pigs, 1997–2000. Journal of Antimicrobial Chemotherapy 53, 997–1003. Guerra, B., Soto, S.M., Arguelles, J.M.,Mendoza,M.C., 2001.Multidrug resistance is mediated by large plasmids carrying a class 1 integron in the emergent Salmonella enterica serotype [4,5,12:i:-]. Antimicrobial Agents and Chemotherapy 45, 1305–1308. Guerra, B., Junker, E., Miko, A., Helmuth, R., Mendoza, M.C., 2004. Characterization and localization of drug resistance determinants in multidrug-resistant, integron-carrying Salmonella enterica serotype Typhimurium strains. Microbial Drug Resistance 10 (2), 82–91. Haneda, T., Okada, N., Nakazawa, N., Kawakami, T., Danbar, H., 2001. Complete DNA sequence and comparative analysis of the 50-kilobase virulence plasmid of Salmonella enterica serovar Choleraesuis. Infection and Immunity 69 (4), 2612–2620. Hauser, E., Tietze, E., Helmuth, R., Junker, E., Blank, K., Prager, R., Rabsch, W., Appel, B., Fruth, A., Malorny, B., 2010. Pork contaminated with Salmonella enterica serovar 4, [5],12:i:−, an emerging health risk for humans. Applied and Environmental Microbiology 76 (14), 4601–4610. Hur, J., Jawale, C., Lee, J.H., 2011. Antimicrobial resistance of Salmonella isolated from food animals: a review. Food Research International http://dx.doi.org/10.1016/j.foodres.2011.05.014. Hurd, H.S., McKean, J.D., Wesley, I.V., Karriker, L.A., 2001. The effect of lairage on Salmonella isolation from market swine. Journal of Food Protection 64 (7), 939–944. ISO, 1981. International organisation for Standardisation 6579. Microbiology. Jordan, E., Egan, J., Dullea, C., Ward, J., McGillicuddy, K., Murray, G., Murphy, A., Bradshaw, B., Leonard, N., Rafter, P., McDowell, S., 2006. Salmonella surveillance in raw and cooked meat and meat products in the Republic of Ireland from 2002 to 2004. International Journal of Food Microbiology 112, 66–70. Karczmarczyk, M., Martins, M., McCusker, M., Mattar, S., Amaral, L., Leonard, N., Aarestrup, F.M., Fanning, S., 2010. Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: identification of a qnrB19-mediated quinolone resistance marker in two novel serovars. FEMS Microbiology Letters 313, 10–19. Knodler, L.A., Winfree, S., Drecktrah, D., Ireland, R., Steele-Mortimer, O., 2009. Ubiquitination of the bacterial inositol phosphatase, SopB, regulates its biological activity at the plasma membrane. Cellular Microbiology 11 (11), 1652–1670. Majtanova, L., Majtan, T., Majtan, V., 2010. Detection of the class 1 integrons and SGI1 among Salmonella enterica serovar Typhimurium DT104, U302, DT120, DT193, and non-typable human isolates. Japanese Journal of Infectious Diseases 63 (4), 292–295. Michael, G.B., Butaye, P., Cloeckaert, A., Schwarz, S., 2006. Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microbes and Infection 8, 1898–1914. Mulvey, M.R., Boyd, D.A., Olson, A.B., Doublet, B., Cloeckaet, A., 2006. The genetics of Salmonella genomic island 1. Microbes and Infection 8, 1915–1922. Ng, L.K.,Mulvey,M.R.,Martin, I., Peters,G.A., Johnson,W.,1999.Genetic characterization of antimicrobial resistance in Canadian isolates of Salmonella serovar Typhimurium DT104. Antimicrobial Agents and Chemotherapy 43 (12), 3018–3021. Perez-Perez, F.J., Hanson, N.D., 2002. Detection of plasmid-mediated AmpC beta- lactamase genes in clinical isolates by using multiplex PCR. Journal of Clinical Microbiology 40, 2153–2162. Piras, F.,Brown,D.J.,Meloni,D.,Mureddu, A.,Mazzette,R.,2011. Investigationof Salmonella enterica in Sardinian slaughter pigs: prevalence, serotype and genotype characterization. International Journal of Food Microbiology 151, 201–209. Poppe, C., Ziebell, K., Martin, L., Allen, K., 2002. Diversity in antimicrobial resistance and other characteristics among Salmonella Typhimurium DT104 isolates. Microbial Drug Resistance 8, 107–122. Prendergast, D.M., Duggan, S.J., Fanning, S., Cormican, M., Gonzales-Barron, U., Butler, F., Duffy, G., 2008. Prevalence and numbers of Salmonella spp. and Enterobacteriaceae on pork cuts in abattoirs in the Republic of Ireland. Journal of Applied Microbiology 105, 1209–1219. Prendergast, D.M., Duggan, S.J., Gonzales-Barron, U., Butler, F., Fanning, S., Cormican, M., Duffy, G., 2009. Prevalence, numbers and characteristics of Salmonella on Irish retail pork. International Journal of Food Microbiology 131, 233–239. 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 391, 59–67. Romero, E.V., Padilla, T.P., Garcia, M.I.G., 2005. Salmonella enterica serovar infantis producing a CTX-M-9 beta-lactamase. Antimicrobial Agents and Chemotherapy 49 (5), 2142–2143. Rossel, R., Jouffe, L., Beloeil, P.A., 2009. Analyse des facteurs associ{\'e}s {\`a} la contamination des carcasses de porcs par Salmonella {\`a} l'aide des r{\'e}seaux bay{\'e}siens. Journ{\'e}es de la Recherche Porcine 41, 43–48. Sandvang, D., Aarestrup, F.M., Jensen, L.B., 1998. Characterisation of integrons and antibiotic resistance genes in Danish multi-resistant Salmonella enterica Typhimurium DT104. FEMS Microbiology Letters 160, 37–41. Shahada, F.T., Chuma, T., Tobata, K., Okamoto, M., Takase, K., 2006. Molecular epidemiology of antimicrobial resistance among Salmonella enterica serovar Infantis from poultry in Kagoshima, Japan. International Journal of Antimicrobial Agents 28 (4), 302–307. Shahada, F., Amamoto, A., Chuma, T., Shirai, A., Okamoto, K., 2007. Antimicrobial suscepti bility phenotypes, resistance determinants and DNA fingerprints of Salmonella enterica serotype Typhimuriumisolated frombovine in Southern Japan. International Journal of Antimicrobial Agents 30, 150–156. Small, A., James, C., james, S., Davies, R., Liebana, E., Howell,M., Hutchinson,M., Buncic, S., 2006. Presence of Salmonella in the red meat abattoir lairage after routine cleaning and disinfection and on carcasses. Journal of Food Protection 69 (10), 2342–2351. Small, A.m., James, C., Purnell, G., Losito, P., James, S., Buncic, S., 2007. An evaluation of simple cleaning methods that may be used in red meat abattoir lairages. Meat Science 75, 220–228. van Asten, A.J.A.M., van Dijk, J.E., 2005. Distribution of ‘classic’ virulence factors among Salmonella spp. FEMS Immunology and Medical Microbiology 44, 251–259. Van Pelt, W., Valkenburg, S.M., 2001. Zoonoses and zoonottic agents in humans, food, animals and feed in the Netherlands. Available at www.keuringsdienstvanwaren.nl. Vieira-Pinto, M., Tenreiro, R., Martins, C., 2006. Unveiling contamination sources and dissemination routes of Salmonella sp. in pigs at a Portuguese slaughterhouse through macrorestriction profiling by pulsed-field gel electrophoresis. International Journal of FoodMicrobiology 110 (1), 77–84. Zhao, S., White, D.G., Friedman, S.L., Glenn, A., Blickenstaff, K., Ayers, S.L., Abbott, J.W., Hall-Robinson, E., McDermott, P.F., 2008. Antimicrobial resistance in Salmonella enterica Serovar Heidelberg isolates from retail meats, including poultry, from 2002 to 2006. Applied and Environmental Microbiology 74 (21), 6656–6662.",
    year = "2013",
    doi = "10.1016/j.ijfoodmicro.2012.11.001",
    language = "English",
    volume = "160",
    pages = "298--303",
    journal = "International Journal of Food Microbiology",
    issn = "0168-1605",
    publisher = "Elsevier",
    number = "3",

    }

    A study of Salmonella in pigs from birth to carcass: Serotypes, genotypes, antibioticresistance and virulence profile. / Bolton, D J; Ivory, C; McDowell, D A.

    In: International Journal of Food Microbiology, Vol. 160, No. 3, 2013, p. 298-303.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - A study of Salmonella in pigs from birth to carcass: Serotypes, genotypes, antibioticresistance and virulence profile

    AU - Bolton, D J

    AU - Ivory, C

    AU - McDowell, D A

    N1 - Reference text: Alban, L., Stege, H., Dahl, J., 2002. The new classification system for slaughter-pig herds in the Danish Salmonella surveillance-and-control program. Preventive Veterinary Medicine 53, 133–146. Alban, L., Baptista, F.M., Mogelmose, V., Sorensen, L.L., Christensen, H., Aabo, S., Dahl, J., 2012. Salmonella surveillance and control for finisher pigs and pork in Denmark — a case study. Food Research International 45, 656–665. Alcaine, S.D., Warnick, L.D., Wiedmann, M., 2007. Antimicrobial resistance in nontyphoidal Salmonella. Journal of Food Protection 70 (3), 780–790. Anderson, E.S., Ward, L.R., de Saxe, M.J., de Sa, J.D.H., 1977. Bacteriophage-typing designations of Salmonella Typhimurium. Journal of Hygiene Cambridge 78, 297. Anon., 1990. Microbiology of Food and Animal Feeding stuffs- Horizontal method for the detection of Salmonella spp. ISO 6579: 1990 (E). Anon, 2008a. Report of the Task Force on Zoonoses Data Collection on the analysis of the baseline survey on the prevalence of Salmonella in slaughter pigs, part B. The EFSA Journal 206, 1–111. Anon, 2008b. Annual Report for 2008 from the Health Protection Surveillance Centre, Ireland. 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 (3), 2597. http://dx.doi.org/10.2903/j.efsa.2012.2597 ([442pp.]. Available online: www.efsa.europa.eu/efsajournal). Aragaw, K., Molla, B., Muckle, A., Cole, L., Wilkie, E., Poppe, C., Kleer, J., Hildebrandt, G., 2007. The characterization of Salmonella serovars isolated from apparently healthy slaughtered pigs at Addis Ababa abattoir, Ethiopia. Preventive Veterinary Medicine 82 (3–4), 252–261. Bolton, L.F., Kelley, L.C., Lee, M.D., Fedora-Cray, P.J., Mauer, J.J., 1999. Detection of multidrug resistant Salmonella enterica serotype Typhimurium DT104 based on a gene which confers cross-resistance to florfenicol and chloramphenicol. Journal of Clinical Microbiology 37, 1348–1351. Boughton, C., Leonard, F.C., Egan, J., Kelly, G., O'Mahony, P., Markey, B.K., Griffin, M., 2004. Prevalence and number of Salmonella in Irish retail pork sausages. Journal of Food Protection 67, 1834–1839. Boyd, D.A., Peters, G.A., Lai-King, N., Mulvey, M.R., 2000. Partial characterization of a genomic island associated with the multidrug resistance region of Salmonella enterica Typhimurium DT104. FEMS Microbiology Letters 189, 285–291. Callow, B.R., 1959. A new phage-typing scheme for Salmonella Typhimurium. Journal of Hygiene Cambridge 57, 3. Carattoli, A., Filetici, E., Villa, L., Dionisi, A.M., Ricci, A., Luzzi, I., 2002. Antibiotic resistance genes and Salmonella genomic island 1 in Salmonella enterica serovar Typhimurium isolated in Italy. Antimicrobial Agents and Chemotherapy 46 (9), 2821–2828. Carlson, F.A., Bolton, L.F., Briggs, C.E., Hurd, H.S., Sharma, V.K., Fedora-Kray, P.J., Jones, B.D., 1999. Detection of multiresistant Salmonella Typhimurium DT 104 using multiplex and fluorogenic PCR. Molecular and Cellular Probes 13, 213–222. Chen, S., Zhao, S., White, D.G., Schroeder, C.M., Lu, R., Yang, H., McDermott, P.F., Ayers, S., Meng, J., 2004. Characterization of multiple antimicrobial resistant Salmonella serovars isolated from retail meats. Applied and Environmental Microbiology 70, 1–7. Chu, C., Chiu, C.H., Wu, W.Y., Chu, C.H., Liu, T.P., Ou, J.T., 2001. Large drug resistance virulence plasmids of clinical isolates of Salmonella enterica serovar Choleraesuis. Antimicrobial Agents and Chemotherapy 45, 2299–2303. Dahshan, H., Shahada, F., Chuma, T., Moriki, H., Okamoto, K., 2010. Genetic analysis of multidrug-resistant Salmonella enterica serovars Stanley and Typhimurium from cattle. Veterinary Microbiology 145, 76–83. Daly, M., Fanning, S., 2000. Characterization and chromosomal mapping of antimicrobial resistance genes in Salmonella enterica serotype Typhimurium. Applied and Environmental Microbiology 66, 842–4848. De Busser, E.V., Maes, D., Houf, K., Dewulf, J., Imberechts, H., Bertrand, S., De Zutter, L., 2011. Detection and characterization of Salmonella in lairage, on pig carcasses and intestines in five slaughterhouses. International Journal of Food Microbiology 145, 279–286. Gallardo, F., Ruiz, J.,Marco, F., Towner, K.J., Vila, J., 1999. Increase in incidence of resistance to ampicillin, chloramphenicol and trimethoprimin clinical isolates of Salmonella serotype Typhimuriumwith investigation of molecular epidemiology and mechanisms of resistance. Journal of MedicalMicrobiology 48, 367–374. Gebreyes, W.A., Altier, C., 2002. Molecular characterization of multi-drug resistance determinants among Salmonella enterica serovar Typhimurium isolates collected from swine. Journal of Clinical Microbiology 40, 2813–2822. Gebreyes, W.A., Thakur, S., Davies, P.R., Funk, J.A., Altier, C., 2004. Trends in antimicrobial resistance, phage types and integrons among Salmonella serotypes from pigs, 1997–2000. Journal of Antimicrobial Chemotherapy 53, 997–1003. Guerra, B., Soto, S.M., Arguelles, J.M.,Mendoza,M.C., 2001.Multidrug resistance is mediated by large plasmids carrying a class 1 integron in the emergent Salmonella enterica serotype [4,5,12:i:-]. Antimicrobial Agents and Chemotherapy 45, 1305–1308. Guerra, B., Junker, E., Miko, A., Helmuth, R., Mendoza, M.C., 2004. Characterization and localization of drug resistance determinants in multidrug-resistant, integron-carrying Salmonella enterica serotype Typhimurium strains. Microbial Drug Resistance 10 (2), 82–91. Haneda, T., Okada, N., Nakazawa, N., Kawakami, T., Danbar, H., 2001. Complete DNA sequence and comparative analysis of the 50-kilobase virulence plasmid of Salmonella enterica serovar Choleraesuis. Infection and Immunity 69 (4), 2612–2620. Hauser, E., Tietze, E., Helmuth, R., Junker, E., Blank, K., Prager, R., Rabsch, W., Appel, B., Fruth, A., Malorny, B., 2010. Pork contaminated with Salmonella enterica serovar 4, [5],12:i:−, an emerging health risk for humans. Applied and Environmental Microbiology 76 (14), 4601–4610. Hur, J., Jawale, C., Lee, J.H., 2011. Antimicrobial resistance of Salmonella isolated from food animals: a review. Food Research International http://dx.doi.org/10.1016/j.foodres.2011.05.014. Hurd, H.S., McKean, J.D., Wesley, I.V., Karriker, L.A., 2001. The effect of lairage on Salmonella isolation from market swine. Journal of Food Protection 64 (7), 939–944. ISO, 1981. International organisation for Standardisation 6579. Microbiology. Jordan, E., Egan, J., Dullea, C., Ward, J., McGillicuddy, K., Murray, G., Murphy, A., Bradshaw, B., Leonard, N., Rafter, P., McDowell, S., 2006. Salmonella surveillance in raw and cooked meat and meat products in the Republic of Ireland from 2002 to 2004. International Journal of Food Microbiology 112, 66–70. Karczmarczyk, M., Martins, M., McCusker, M., Mattar, S., Amaral, L., Leonard, N., Aarestrup, F.M., Fanning, S., 2010. Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: identification of a qnrB19-mediated quinolone resistance marker in two novel serovars. FEMS Microbiology Letters 313, 10–19. Knodler, L.A., Winfree, S., Drecktrah, D., Ireland, R., Steele-Mortimer, O., 2009. Ubiquitination of the bacterial inositol phosphatase, SopB, regulates its biological activity at the plasma membrane. Cellular Microbiology 11 (11), 1652–1670. Majtanova, L., Majtan, T., Majtan, V., 2010. Detection of the class 1 integrons and SGI1 among Salmonella enterica serovar Typhimurium DT104, U302, DT120, DT193, and non-typable human isolates. Japanese Journal of Infectious Diseases 63 (4), 292–295. Michael, G.B., Butaye, P., Cloeckaert, A., Schwarz, S., 2006. Genes and mutations conferring antimicrobial resistance in Salmonella: an update. Microbes and Infection 8, 1898–1914. Mulvey, M.R., Boyd, D.A., Olson, A.B., Doublet, B., Cloeckaet, A., 2006. The genetics of Salmonella genomic island 1. Microbes and Infection 8, 1915–1922. Ng, L.K.,Mulvey,M.R.,Martin, I., Peters,G.A., Johnson,W.,1999.Genetic characterization of antimicrobial resistance in Canadian isolates of Salmonella serovar Typhimurium DT104. Antimicrobial Agents and Chemotherapy 43 (12), 3018–3021. Perez-Perez, F.J., Hanson, N.D., 2002. Detection of plasmid-mediated AmpC beta- lactamase genes in clinical isolates by using multiplex PCR. Journal of Clinical Microbiology 40, 2153–2162. 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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 391, 59–67. Romero, E.V., Padilla, T.P., Garcia, M.I.G., 2005. Salmonella enterica serovar infantis producing a CTX-M-9 beta-lactamase. Antimicrobial Agents and Chemotherapy 49 (5), 2142–2143. Rossel, R., Jouffe, L., Beloeil, P.A., 2009. Analyse des facteurs associés à la contamination des carcasses de porcs par Salmonella à l'aide des réseaux bayésiens. Journées de la Recherche Porcine 41, 43–48. Sandvang, D., Aarestrup, F.M., Jensen, L.B., 1998. Characterisation of integrons and antibiotic resistance genes in Danish multi-resistant Salmonella enterica Typhimurium DT104. FEMS Microbiology Letters 160, 37–41. Shahada, F.T., Chuma, T., Tobata, K., Okamoto, M., Takase, K., 2006. 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    PY - 2013

    Y1 - 2013

    N2 - A study was undertaken to investigate Salmonella in pigs at each step from birth to carcass. Environmental and/or pig samples were taken at birth, farrowing, 1st weaning, 2nd weaning, finishing, transport, lairage, bleeding and chilling of carcasses and tested for Salmonella. All isolates were characterised in terms of sero- type, phage type (where relevant) and subtyping with pulsed field gel electrophosesis (PFGE). Isolates weretested for antibiotic resistance, resistance (intI1, blaCIT, blaTem, blaPSE-1, blaOXA-1, floR, catA1, aadA1, aadA2, tetA, tetB, tetG, sul1and aphA1) and virulence (invA, rck, spvC and pefA) genes. PCR was also performed to test for the presence of the left junction, thdF-S001 and the right junction, S004-int2 or S004-yidY of Salmonella genomic island 1 (SGI1). Overall 4.3%, 27.5% and 5% of environmental, throat/rectal and carcass sampleswere Salmonella positive, respectively. S. Typhimurium DT193 was detected during production, while S. Typhimurium DT17 and U311 were present in lairage at the abattoir, where strain characterisation suggested cross contamination of the live animals occurred. The carcasses were also cross contaminated with S. Brandenburg during processing. PFGE grouped the isolates by serotype and/or phage type. The DT193 isolates displayed the ACSSuTTmMn/Gm resistance phenotype and carried the invA, spvC, rck, bla-tem, aadA2, tetA, strA virulence/antibiotic resistance markers; U311 showed an ASSuTMn resistance pattern and carried invA and tetB; DT17 was sensitive to all antibiotics tested but invA, spv and rck positive while S. Brandenburg displayed neither resistance nor virulence gene carriage. None of the isolates possessed class 1 integrons and all isolates were negative for the left and right junctions of SGI1.It was concluded that control activities should target improved biosecurity at farm level and better sanitation in lairage. This study also provides further evidence that multiple drug resistance may be associated with non-SGI1 Salmonella strains. The continued emergence of non-DT104 S. Typhimurium isolates exhibiting multidrug resistance is a cause for concern as is the persistence of highly virulent Salmonella strains in the abattoir environment.

    AB - A study was undertaken to investigate Salmonella in pigs at each step from birth to carcass. Environmental and/or pig samples were taken at birth, farrowing, 1st weaning, 2nd weaning, finishing, transport, lairage, bleeding and chilling of carcasses and tested for Salmonella. All isolates were characterised in terms of sero- type, phage type (where relevant) and subtyping with pulsed field gel electrophosesis (PFGE). Isolates weretested for antibiotic resistance, resistance (intI1, blaCIT, blaTem, blaPSE-1, blaOXA-1, floR, catA1, aadA1, aadA2, tetA, tetB, tetG, sul1and aphA1) and virulence (invA, rck, spvC and pefA) genes. PCR was also performed to test for the presence of the left junction, thdF-S001 and the right junction, S004-int2 or S004-yidY of Salmonella genomic island 1 (SGI1). Overall 4.3%, 27.5% and 5% of environmental, throat/rectal and carcass sampleswere Salmonella positive, respectively. S. Typhimurium DT193 was detected during production, while S. Typhimurium DT17 and U311 were present in lairage at the abattoir, where strain characterisation suggested cross contamination of the live animals occurred. The carcasses were also cross contaminated with S. Brandenburg during processing. PFGE grouped the isolates by serotype and/or phage type. The DT193 isolates displayed the ACSSuTTmMn/Gm resistance phenotype and carried the invA, spvC, rck, bla-tem, aadA2, tetA, strA virulence/antibiotic resistance markers; U311 showed an ASSuTMn resistance pattern and carried invA and tetB; DT17 was sensitive to all antibiotics tested but invA, spv and rck positive while S. Brandenburg displayed neither resistance nor virulence gene carriage. None of the isolates possessed class 1 integrons and all isolates were negative for the left and right junctions of SGI1.It was concluded that control activities should target improved biosecurity at farm level and better sanitation in lairage. This study also provides further evidence that multiple drug resistance may be associated with non-SGI1 Salmonella strains. The continued emergence of non-DT104 S. Typhimurium isolates exhibiting multidrug resistance is a cause for concern as is the persistence of highly virulent Salmonella strains in the abattoir environment.

    U2 - 10.1016/j.ijfoodmicro.2012.11.001

    DO - 10.1016/j.ijfoodmicro.2012.11.001

    M3 - Article

    VL - 160

    SP - 298

    EP - 303

    JO - International Journal of Food Microbiology

    T2 - International Journal of Food Microbiology

    JF - International Journal of Food Microbiology

    SN - 0168-1605

    IS - 3

    ER -