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Prevalence of Salmonella spp. and Yersinia enterocolitica in/on tonsils and mandibular lymph nodes of slaughtered pigs

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Abstract

A total of 156 tonsils and 156 mandibular lymph nodes from fattening pigs originating from 13 farms were sampled in Croatian slaughterhouses and examined for Salmonella spp. (n = 78 per organ) and Yersinia enterocolitica (n = 78 per organ) by cultural methods. Salmonella was isolated from two tonsils only, both originated from animals from the same farm (5.12 %), while Y. enterocolitica were recovered from 26 tonsils (33.33 %) which could be traced back to 10 farms. Salmonella was absent in mandibular lymph nodes, and Y. enterocolitica was isolated from eight lymph nodes (10.25 %) which originated from six farms. Y. enterocolitica was present inside the lymph nodes of two pigs. The high prevalence of Y. enterocolitica in/on pig tonsils could be the result of cross-contamination during splitting the carcasses with head. This procedure may result in higher prevalence of Y. enterocolitica on surface of mandibular lymph nodes than in their depth. Traditional veterinary postmortem examination of pig halves will not necessarily contribute to cross-contamination with Salmonella or Yersinia under conditions of present slaughter practice.

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References

  • Bonardi S, Brindani F, Pizzin G, Lucidi L, D’Incau M, Liebana E, Morabito S (2003) Detection of Salmonella spp., Yersinia enterocolitica and verocytotoxin-producing Escherichia coli O157 in pigs at slaughter in Italy. Int J Food Microbiol 85:101–110

    Article  CAS  PubMed  Google Scholar 

  • Bonardi S, Bassi L, Brindani F, D’Incau M, Barco L, Carra E, Pongolini S (2013) Prevalence, characterization and antimicrobial susceptibility of Salmonella enterica and Yersinia enterocolitica in pigs at slaughter in Italy. Int J Food Microbiol 163:248–257

    Article  CAS  PubMed  Google Scholar 

  • Commission Regulation (EU) No 219/2014 of 7 March 2014 amending Annex I to Regulation (EC) No 854/2004 of the European Parliament and of the Council as regards the specific requirements for post-mortem inspection of domestic swine. Off J Eur Union 69: 99–100

  • De Boer E, Nouws JF (1991) Slaughter pigs and pork as a source of human pathogenic Yersinia enterocolitica. Int J Food Microbiol 12:375–378

    Article  PubMed  Google Scholar 

  • EFSA (2011) Scientific opinion on the public health hazards to be covered by inspection of meat (swine). EFSA J 9(2351):198

    Google Scholar 

  • Fondrevez M, Labbé A, Houard E, Fravalo P, Madec F, Denis M (2010) A simplified method for detecting pathogenic Yersinia enterocolitica in slaughtered pig tonsils. J Microbiol Meth 83:244–249

    Article  Google Scholar 

  • Fredriksson-Ahomaa M, Björkroth J, Hielmand S, Korkeala H (2000) Prevalence and characterization of pathogenic Yersinia enterocolitica in pig tonsils from different slaughterhouses. Food Microbiol 17:93–101

    Article  CAS  Google Scholar 

  • Fredriksson-Ahomaa M, Bucher M, Hank C, Stolle A, Korkeala H (2001) High prevalence of Yersinia enterocolitica 4:O3 on pig offal in Southern Germany: a slaughtering technique problem. Syst Appl Microbiol 24:457–463

    Article  CAS  PubMed  Google Scholar 

  • Fredriksson-Ahomaa M, Stolle A, Stephan R (2007) Prevalence of pathogenic Yersinia enterocolitica in pigs slaughtered at a Swiss abattoir. Int J Food Microbiol 119:207–212

    Article  CAS  PubMed  Google Scholar 

  • Fredriksson-Ahomaa M, Gerhardt M, Stolle A (2009) High bacterial contamination of pig tonsils at slaughter. Meat Sci 83:334–336

    Article  PubMed  Google Scholar 

  • Gürtler M, Alter T, Kasimir S, Linnebur M, Fehlhaber K (2005) Prevalence of Yersinia enterocolitica in fattening pigs. J Food Prot 68:850–854

    PubMed  Google Scholar 

  • Kot B, Trafny EA, Jakubczak A (2007) Application of multiplex PCR for monitoring colonization of pig tonsils by Yersinia enterocolitica, including biotype 1A, and Yersinia pseudotuberculosis. J Food Prot 70:1110–1115

    CAS  PubMed  Google Scholar 

  • Kot B, Jakubczak A, Piechota M (2008) Isolation and characterization of Yersinia enterocolitica rods from pig tonsils. Med Wet 64:283–287

    Google Scholar 

  • Lowe BA, Marsh TL, Isaacs-Cosgrove N, Kirkwood RN, Kiupel M, Mulks MH (2011) Microbial communities in the tonsils of healthy pigs. Vet Microbiol 147:346–357

    Article  CAS  PubMed  Google Scholar 

  • Methner U, Rammler N, Fehlhaber K, Rösler U (2011) Salmonella status of pigs at slaughter—bacteriological and serological analysis. Int J Food Microbiol 151:15–20

    Article  PubMed  Google Scholar 

  • Nesbakken T, Eckner K, Hoidal HK, Rotterud OJ (2003) Occurrence of Yersinia enterocolitica and Campylobacter spp. in slaughter pigs and consequences for meat inspection, slaughtering, and dressing procedures. Int J Food Microbiol 80:231–240

    Article  PubMed  Google Scholar 

  • Nowak B, von Müffling T, Chaunchom S, Hartung J (2007) Salmonella contamination in pigs at slaughter and on the farm: a field study using an antibody ELISA test and a PCR technique. Int J Food Microbiol 115:259–267

    Article  CAS  PubMed  Google Scholar 

  • Oliveira M, Vieira-Pinto M, Martins da Costa P, Vilela CL, Martins C, Bernardo F (2012) Occurrence of Salmonella spp. in samples from pigs slaughtered for consumption: a comparison between ISO 6579:2002 and 23S rRNA fluorescent in situ hybridization method. Food Res Int 45:984–988

    Article  CAS  Google Scholar 

  • Ortiz Martínez P, Fredriksson-Ahomaa M, Sokolova Y, Roasto M, Berzins A, Korkeala H (2009) Prevalence of enteropathogenic Yersinia in Estonian, Latvian and Russian (Leningrad Region) pigs. Foodborne Pathog Dis 6:719–724

    Article  Google Scholar 

  • Ortiz Martínez P, Mylona S, Drake I, Fredriksson-Ahomaa M, Korkeala H, Corry JEL (2010) Wide variety of bioserotypes of enteropathogenic Yersinia enterocolitica in tonsils of English pigs at slaughter. Int J Food Microbiol 139:64–69

    Article  PubMed  Google Scholar 

  • Ortiz Martinez P, Fredriksson-Ahomaa M, Pallotti A, Rosmini R, Houf K, Korkeala H (2011) Variation in the prevalence of enteropathogenic Yersinia in slaughter pigs from Belgium, Italy, and Spain. Foodborne Pathog Dis 8:445–450

    Article  Google Scholar 

  • O’Sullivan T, Friendship R, Blackwell T, Pearl D, McEwen B, Carman S, Slavic D, Dewey C (2011) Microbiological identification and analysis of swine tonsils collected from carcasses at slaughter. Can J Vet Res 75:106–111

    PubMed Central  PubMed  Google Scholar 

  • Regulation (EC) No 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. Off J Eur Union L 155:206

  • Sarno E, Stephan R, Zweifel C (2012) Occurrence of Erysipelothrix spp., Salmonella spp., and Listeria spp. in tonsils of healthy Swiss pigs at slaughter. Arch Leb 63:11–15

    Google Scholar 

  • Simonova J, Borilova G, Steinhauserova I (2008) Occurrence of pathogenic strains of Yersinia enterocolitica in pigs and their antimicrobial resistance. Bull Vet Inst Pulawy 52:39–43

    Google Scholar 

  • Swanenburg M, van der Wolf PJ, Urlings HAP, Snijders JMA, van Knapen F (2001) Salmonella in slaughter pigs: the effect of logistic slaughter procedures of pigs on the prevalence of Salmonella in pork. Int J Food Microbiol 70:231–242

    Article  CAS  PubMed  Google Scholar 

  • Terentjeva M, Berzinš A (2010) Prevalence and antimicrobial resistance of Yersinia enterocolitica and Yersinia pseudotuberculosis in slaughter pigs in Latvia. J Food Prot 73:1335–1338

    PubMed  Google Scholar 

  • Uliczka F, Pisano F, Schaake J, Stolz T, Rohde M, Fruth A, Strauch E, Sturnik M, Batzilla J, Rakin A, Heesemann J, Dersch P (2011) Unique cell adhesion and invasion properties of Yersinia enterocolitica O:3, the most frequent cause of human yersiniosis. PLoS Pathog 7(7):e1002117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 Microbiol 27:158–161

    Article  PubMed  Google Scholar 

  • 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. Int J Food Microbiol 110:77–84

    Article  CAS  PubMed  Google Scholar 

  • Vieira-Pinto M, Tenreiro R, Aranha J, Martins C (2012) Relationship between tonsils and mandibular lymph nodes concerning Salmonella sp. Infection. Food Res Int 45:863–866

    Article  Google Scholar 

  • Zdolec N, Dobranić V, Božović B, Perić I, Juras M, Ovničević D, Dolar V, Kugelman LJ, Ljubičić S, Plazonić S, Doboš Z, Penić I, Pašalić T (2014) Results of veterinary post mortem meat inspection in Croatian pig slaughterhouses. Vet Stn 45:221–228

    Google Scholar 

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Acknowledgments

This research was supported by University of Zagreb (Programme Contract 2013/2014), project “Antimicrobial resistance of pathogenic bacteria from food of animal origin.” The authors gratefully acknowledge the assistance of Ana Konjević for technical support during laboratory analyses and Dr Borka Šimpraga and Fani Krstulović from Croatian Veterinary Institute for serotyping of Salmonella isolates.

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  1. Department of Hygiene, Technology and Food Safety, Faculty of Veterinary Medicine, University of Zagreb, Heinzelova 55, HR-10000, Zagreb, Croatia

    Nevijo Zdolec, Vesna Dobranić & Ivana Filipović

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  1. Nevijo Zdolec
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  2. Vesna Dobranić
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  3. Ivana Filipović
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Correspondence to Nevijo Zdolec.

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Zdolec, N., Dobranić, V. & Filipović, I. Prevalence of Salmonella spp. and Yersinia enterocolitica in/on tonsils and mandibular lymph nodes of slaughtered pigs. Folia Microbiol 60, 131–135 (2015). https://doi.org/10.1007/s12223-014-0356-9

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  • DOI: https://doi.org/10.1007/s12223-014-0356-9

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