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Salmonella prevalence and serovar distribution in healthy slaughter sheep and cattle determined by ISO 6579 and VIDAS UP Salmonella methods

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Abstract

Prevalence of Salmonella in slaughter sheep and cattle was determined by International Organization for Standardization Method 6579 (ISO) and Vitek Immunodiagnostic Assay System UP Salmonella Phage Technology (VIDAS UP Salmonella SPT—VIDAS UP). A total of 400 healthy slaughter sheep (n = 200) and cattle (n = 200) carcass (C), fecal content (FC), mesenteric lymph node (MLN), liver (L), kidney (K), spleen (S) and gall bladder (GB) were randomly sampled and analysed. ISO and VIDAS UP results indicated 13 (3.25%) and 17 (4.25%) of 400 animals carried Salmonella, respectively, regardless of sample type. There was no isolation from L, S, GB, while 2 C (0.5%), 6 FC (1.5%), 7 MLN (1.75%), 3 K (0.75%) were contaminated with Salmonella. S. Typhimurium (27.8%), S. Enteritidis (22.2%), S. Newport (22.2%) were the three dominant serovars, followed by S. Kentucky (11.1%), S. Umbilo (5.6%), S. Corvallis (5.6%), and S. Albany (5.6%). Overall prevalence in 2800 samples was 0.46% by ISO and 0.61% by VIDAS UP. High relative trueness (RT: 99.79%) of VIDAS UP with a substantial agreement to ISO (κ value: 0.80) indicated its efficiency to accompany ISO to monitor Salmonella in slaughter animals. As the first report to evaluate ISO and VIDAS UP in detecting Salmonella from slaughter sheep and cattle, this current prevalence signifies a risk for public health in red-meat and related products in Turkey.

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References

  • Akoachere JTK, Tanih NF, Ndip LM, Ndip RN (2009) Phenotypic characterization of Salmonella Typhimurium isolates from food-animals and abattoir drains in Buea, Cameroon. J Health Popul Nutr 27:612–618

    PubMed  PubMed Central  Google Scholar 

  • Alemu S, Zewde BM (2012) Prevalence and antimicrobial resistance profiles of Salmonella enterica serovars isolated from slaughtered cattle in Bahir Dar, Ethiopia. Trop Anim Health Prod 44:595–600. https://doi.org/10.1007/s11250-011-9941-y

    Article  PubMed  Google Scholar 

  • Benetti TM, Monteiro CLB, Beux MR, Abrahão WM (2013) Enzyme-linked imunoassays for the detection of Listeria sp. and Salmonella sp. in sausage: a comparison with conventional methods. Braz J Microbiol 44(3):791–794

    Article  CAS  Google Scholar 

  • Bonardi S, Bruini I, Magnani R, Cannistrà N, Brindani F (2017) Low prevalence of Salmonella enterica in cull dairy cattle at slaughter in Northern Italy. Ital J Food Sci 6:1–4. https://doi.org/10.4081/ijfs.2017.6172

    Article  Google Scholar 

  • Bradbery AN, Coverdale JA, Lucia LM, Acuff GR, Hartz CJ (2015) Detection of Salmonella in equine facility environmental samples by 2 methods. J Equine Vet Sci 35:418–436. https://doi.org/10.1016/j.jevs.2015.03.125

    Article  Google Scholar 

  • Chajecka-Wierzchowska W, Zadernowska A, Kłebukowska L, Łaniewska-Trokenheim Ł (2012) Salmonella detectıon in poultry meat—validation of Vidas xpress automatic enzyme-linked fluorescent immunoassay-based method. J Food Saf 32:407–414. https://doi.org/10.1111/j.1745-4565.2012.00394.x

    Article  CAS  Google Scholar 

  • Chatzopoulos DC, Sarrou S, Vasileiou NGC, Ioannidi KS, Peteinaki E, Valiakos G, Tsokana CN, Papadopoulos E, Spyrou V, Mavrogianni VS, Giannakopoulos A, Sbiraki A, Lacasta D, Bueso JP, Athanasiou LV, Billinis C, Fthenakis GC (2016) Dissemination of intestinal pathogens between lambs and puppies in sheep farms. Small Rumin Res 141:5–10. https://doi.org/10.1016/j.smallrumres.2016.06.006

    Article  Google Scholar 

  • EFSA, Ecdc (2016) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA J 14(4634):231

    Google Scholar 

  • FAO (2018a) Food and Agricultural Organisation. Retrieved from: http://www.fao.org/faostat/en/#data/QL

  • FAO (2018b) Food and Agricultural Organisation. Retrieved from: http://www.fao.org/faostat/en/#data/CL

  • Gava F, Wildemanna P, Gavab D, Ferraza SM, Degenhardtc R, Vaza EK (2015) Comparative analysis between ELFA ELISA using a recombinant bacteriophage protein and other diagnostic methods for Salmonella spp. detection in products of animal origin. Arch Vet Sci 20(4):54–61. https://doi.org/10.5380/avs.v20i4

    Article  Google Scholar 

  • Grimont PAD, Weill F (2007) Antigenic formulae of the Salmonella serovars: White Kauffmann Le Minor scheme, 9th edn. WHO Collaborating Centre for Reference and Research on Salmonella, Institute Pasteur, Paris, France

  • Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J, Grimont PA, Weill FX (2010) Supplement 2003–2007 (No. 47) to the White Kauffmann Le Minor scheme. Res Microbiol 161:26–29. https://doi.org/10.1016/j.resmic.2009.10.002

    Article  Google Scholar 

  • Hanlon KE, Miller MF, Guillen LM, Echeverry A, Dormedy E, Cemo B, Branham LA, Sanders S, Brashears MM (2018) Presence of Salmonella and Escherichia coli O157 on the hide, and presence of Salmonella, Escherichia coli O157 and Campylobacter in feces from small-ruminant (goat and lamb) samples collected in the United States, Bahamas and Mexico. Meat Sci 135:1–5. https://doi.org/10.1016/j.meatsci.2017.08.003

    Article  PubMed  Google Scholar 

  • Hurtado A, Ocejo M, Oporto B (2017) Salmonella spp. and Listeria monocytogenes shedding in domestic ruminants and characterization of potentially pathogenic strains. Vet Microbiol 210:71–76. https://doi.org/10.1016/j.vetmic.2017.09.003

    Article  PubMed  Google Scholar 

  • ISO (2002) International Standard Organization, 6579:2002 Microbiology of food and animal feeding stuffs-horizontal method for the detection of Salmonella spp

  • ISO (2003) Microbiology of food and animal feedingstuffs—carcass sampling for microbiological analysis. ISO 17604:2003, Geneva

    Google Scholar 

  • ISO (2007) International Standard Organization, 6579:2002/A1:2007 Microbiology of food and animal feedingstuffs-horizontal method for the detection of Salmonella spp. Amendment 1: Annex D: Detection of Salmonella spp. in animal faeces and in environmental samples from the primary production stage

  • ISO (2016) International Standard Organization, 16140:2016 Microbiology of food and animal feedingstuffs protocol for the alternative validation methods

  • Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, De Pinna E, Nair S, Fields PI, Weill FX (2014) Supplement 2008–2010 (No. 48) to the White Kauffmann Le Minor scheme. Res Microbiol 165:526–530. https://doi.org/10.1016/j.resmic.2014.07.004

    Article  PubMed  Google Scholar 

  • Jeuge S, Vignaud ML, Lailler R, Dufour C, Schmitt A, Le Hello S, Gregori T, Ellouze M, the Salmonovar consortium (2016) Evaluation of different analytical methods for detection of monophasic variants of S. Typhimurium during process and shelf-life of dried sausages. In International symposium Salmonella and Salmonellosis (I3S). June 6–8, 2016, Saint-Malo, France

  • Junillon T, Mosticon D, Mallen B, Baril F, Morand L, Michel D, Flandrois JP (2014) Optimization of the reactional medium and a food impact study for a colorimetric in situ Salmonella spp. detection method. Int J Food Microbiol 181:48–52. https://doi.org/10.1016/j.ijfoodmicro.2014.04.022

    Article  PubMed  Google Scholar 

  • Kuma F, Lakew M, Koran T, Olani A, Tamiru M, Yimesgen L, Zenebe T, Gerbi F (2017) A cross sectional study on Salmonella in apparently healthy sheep and goats slaughtered at Elfora and Luna export abattoirs, Ethiopia. Afr J Microbiol Res 11(13):530–536. https://doi.org/10.5897/AJMR2017.8449

    Article  CAS  Google Scholar 

  • Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  Google Scholar 

  • Lee KM, Runyon M, Herrman TJ, Phillips R, Hsieh J (2015) Review of Salmonella detection and identification methods: aspects of rapid emergency response and food safety. Food Control 47:264–276. https://doi.org/10.1016/j.foodcont.2014.07.011

    Article  Google Scholar 

  • Little CL, Richardson JF, Owen RJ, de Pinna E, Threlfall EJ (2008) Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003–2005. Food Microbiol 25:538–543. https://doi.org/10.1016/j.fm.2008.01.001

    Article  CAS  PubMed  Google Scholar 

  • Loiko MR, De Paula CMD, Langone ACJ, Rodrigues RQ, Cibulski S, Rodrigues RDO, Camargo AC, Nero LA, Mayer FQ, Tondo EC (2016) Genotypic and antimicrobial characterization of pathogenic bacteria at different stages of cattle slaughtering in southern Brazil. Meat Sci 116:193–200. https://doi.org/10.1016/j.meatsci.2016.01.010

    Article  PubMed  Google Scholar 

  • Milnes AS, Stewart I, Clifton-Hadley FA, Davies RH, Newell DG, Sayers AR, Cheasty T, Cassar C, Ridley A, Cook AJ, Evans SJ, Teale CJ, Smith RP, McNally A, Toszeghy M, Futter R, Kay A (2008) Paiba GA (2008) Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol Infect 136:739–751. https://doi.org/10.1017/S0950268807009223

    Article  CAS  PubMed  Google Scholar 

  • Moawad AA, Hotzel H, Awad O, Tomaso H, Neubauer H, Hafez HM, El-Adawy H (2017) Occurrence of Salmonella enterica and Escherichia coli in raw chicken and beef meat in northern Egypt and dissemination of their antibiotic resistance markers. Gut Pathog 9:1–13. https://doi.org/10.1186/s13099-017-0206-9

    Article  CAS  Google Scholar 

  • Pacheco da Silva FF, Horvath MB, Silveira JG (2014) Occurrence of Salmonella spp. and genetic Escherichia coli on beef carcasses sampled at a Brazillan slaughterhouse. Braz J Microbiol 45(1):17–23. https://doi.org/10.1590/s1517-83822014005000037

    Article  Google Scholar 

  • Raman R (2017) Evaluation of rapid Salmonella immunoassays and characterization of bacterial isolates that cause false-negative and false-positive results in the tests. Master of Science in Food Science Thesis, Department of Food Science, Faculty of Agriculture and Environmental Sciences, McGill University, Sainte-Anne-de-Bellevue, Québec, Canada

  • Ransom JR, Belk KE, Bacon RT, Sofos JN, Scanga JA, Smith GC (2002) Comparison of sampling methods for microbiological testing of beef animal rectal/colonal feces, hides, and carcasses. J Food Prot 65:621–626

    Article  CAS  Google Scholar 

  • TFC (2011) Turkish Food codex regulation on microbiological criteria. Turkish Food Codex, Official Gazette: 28157. 29 Dec 2011

  • Wieczorek K, Osek J (2013) Prevalence and characterisation of Salmonella in slaughtered cattle and beef in Poland. Bull Vet Inst Pulawy 57(4):607–611. https://doi.org/10.2478/bvip-2013-0103

    Article  CAS  Google Scholar 

  • Zadernowska A, Chajecka-Wierzchowska W, Kłebukowska L (2014) Vidas UP–enzyme-linked fluorescent immunoassay based on recombinant phage protein and fluorescence in situ hybridization as alternative methods for detection of Salmonella enterica serovars in meat. Foodborne Pathog Dis 11(9):747–752. https://doi.org/10.1089/fpd.2014.1738

    Article  CAS  PubMed  Google Scholar 

  • Zubair AI, Ibrahim KS (2012) Isolation of Salmonella from slaughtered animals and sewage at Zakho abattoir, Kurdistan Region, Iraq. Res Opin Anim Vet Sci 3(1):20–24

    Google Scholar 

Download references

Acknowledgements

This project was funded in part by the Bursa Uludag University Scientific Research Unit Grant, Project No: OUAP(V)-2013/29.

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Authors and Affiliations

  1. Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Tekirdag Namık Kemal University, 59030, Tekirdağ, Turkey

    Ece Cetin

  2. Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Bursa Uludag University, 16059, Bursa, Turkey

    Seran Temelli & Aysegul Eyigor

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Correspondence to Aysegul Eyigor.

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Cetin, E., Temelli, S. & Eyigor, A. Salmonella prevalence and serovar distribution in healthy slaughter sheep and cattle determined by ISO 6579 and VIDAS UP Salmonella methods. J Food Sci Technol 56, 5317–5325 (2019). https://doi.org/10.1007/s13197-019-04002-2

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