Holding Pens as Sources of Contamination of Coagulase-Positive Staphylococcus to Pigs Waiting for Slaughter

Lauren Machado Moreira, Alana Borges Tavares, Celina Nunes Ebersol, Taís Gonçalves Gonçalves, Helenice Gonzalez de Lima, Natacha Debonim Cereser, Cláudio Dias Timm


Background: Coagulase-Positive Staphylococcus (SCP) are important pathogens related to foodborne illness associated with pork consumption. The isolation of SCP from pork products has been reported in several countries, including Brazil. Therefore, the identification of the sources of contamination of the pork products is fundamental to ensure the food safety. Although the animals remain in the holding pens during the pre-slaughter, these facilities have not been studied as a possible source of contamination for pigs. The aim of this study was to determine the importance of holding pens as sources of contamination of SCP to pigs and to identify other sources in the slaughter flowchart.

Materials, Methods & Results: It was followed four pigs from ten different lots sent to slaughter. Prior to slaughter, samples were collected from the floors of the holding pens in the slaughterhouse. During slaughter, samples from seven different points were collected: 1) stool from the rectum immediately after stunning; 2) external surface of the carcass after dehairing; 3) internal surface of the carcass after evisceration; 4) external surface of the half-carcass prior to entry into the cold chamber; 5) tongue surface; 6) jowls; and 7) mesenteric lymph nodes. The strains were obtained through microbiological analysis. To compare the similarity between the strains, rep-PCR was performed. Of the ten samples collected in the holding pens, four (40%) were contaminated with SCP. At slaughter, 280 samples were collected and 56 (20%) SCP isolates were obtained. The lymph nodes were the point of greatest isolation (19.6%), followed by the surface of the carcass at the entrance to the cold chamber (17.8%), the rectum after desensitization (16.1%), carcass surface after opening of the abdominal cavity (16.1%), jowls (12.5%), carcass surface after dehairing (8.9%) and tongue surface (8.9%). In the rep-PCR analysis, isolates with indistinguishable band pattern were observed involving both those obtained on the holding pens and at different points in the slaughtering flowchart.

Discussion: The holding pens contamination may have occurred due to hygiene failure after leaving lots with pigs harboring SCP. Considering that the recommendation, in view of animal welfare, is to use anti-slip material in the pens floor, it may be difficult to clean this area due to roughness in the concrete, which would allow the microorganisms remain in the place. Some studies have reported the presence of S. aureus in pigs from finishing farms, demonstrating that these animals may be harboring this bacterium in the gastrointestinal tract when sent to slaughter, excreting it in the pens during waiting in the slaughterhouse. Some strains isolated from tongue, rectum and lymph nodes were considered indistinguishable by rep-PCR from the strains isolated from the holding dump, what demonstrate that the holding pens act as an important source of SCP contamination for the pigs that will be slaughtered. The results show that the period in which the animals remain in the holding pens during pre-slaughter is sufficient for the pigs to be contaminated with SCP, the microorganisms to settle in the mesenteric lymph nodes and the animals excrete these bacteria in the feces. The persistence of the contamination to the end products is a possibility, since strains isolated from stool samples were also isolated from other points in the slaughter flowchart, including the carcass. It can be concluded that the holding pens are important sources of SCP contamination for the swine, which once contaminated, can disseminate the microorganism in the slaughter flowchart through the feces, mesenteric lymph nodes and oral cavity. This is the first study in Brazil that shows that the holding pens are important sources of SCP contamination for pigs sent to slaughter.

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Beneke B., Klees S., Stührenberg B. Fetsch A., Kraushaar B. & Tenhagen B.A. 2011. Prevalence of methicillin-resistant Staphylococcus aureus in a fresh meat pork production chain. Journal of Food Protection. 74(1): 126-129.

Brasil. 2003. Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa nº 62, de 26/08/2003. Métodos Analíticos Oficiais para Análises Microbiológicas para Controle de Produtos de Origem Animal e Água. Diário Oficial da União, Brasília, 18 set. 2003. Seção I, p. 14-51.

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(1): 279-286.

Gilbert P., McBain A.J. & Rickard A.H 2003. Formation of microbial biofilm in hygienic situations: a problem of control. International Biodeterioration & Biodegration. 51(4): 245-248.

Guerra Filho J.B.P., Veiga S.J., Possebon F.S., Sudano M.J., Galvão J.A., Yamatogi R.S. & Pinto J.P.A.N. 2014. Prevalência e sorotipagem de Salmonella em linfonodos e fezes de suínos. Blucher Food Science Proceedings. 1(1): 337-338.

Jay J.M. 2005. Microbiologia de Alimentos. 6th edn. Porto Alegre: Artmed, 712p.

Khanna T., Friendship R., Dewey C. & Weese J.S. 2008. Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Veterinary Microbiology. 128(3): 298-303.

Lassok B. & Tenhagen B.A. 2013. From pig to pork: methicillin-resistant Staphylococcus aureus in the pork production chain. Journal of Food Protection. 76(6): 1095-1108.

Laukkanen R., Ranta J., Dong X., Hakkinen M., Martínez P.O., Lundén J. & Korkeala H. 2010. Reduction of enteropathogenic Yersinia in the pig slaughterhouse by using bagging of the rectum. Journal of Food Protection. 73(12): 2161-2168.

Ludtke C.B., Ciocca J.R.P., Dandin T., Barbalho P.C., Vilela J.A. & Costa O.A.D. 2010. Abate humanitário de suínos. Rio de Janeiro: WSPA, 132p.

Lima E.D.S., Pinto P.S.A., Santos J.L.D., Vanetti M.C.D., Bevilacqua P.D., Almdeida L.P., Pinto M.S. & DIAS F.S 2004. Isolamento de Salmonella sp e Staphylococcus aureus no processo do abate suíno como subsídio ao sistema de Análise de Perigos e Pontos Críticos de Controle-APPCC1. Pesquisa Veterinária Brasileira. 24(4): 185-190.

Linhares L.L., Sreevatsan S., Munoz-Zanzi C.A., Torremorell M. & Davies P.R. 2015. The effect of anatomic site and age on detection of Staphylococcus aureus in pigs. Journal of Veterinary Diagnostic Investigation. 27(1): 55-60.

Masson G.C.I.H., Ferreira G.S., Oliveira L.F. & Carvalho S. 2012. Perfil de resistência a antimicrobianos de Staphylococcus aureus isolados de granjas e frigoríficos de suínos. Archives of Veterinary Science. 17(1): 1-14.

Molla B., Byrne M., Abley M., Mathews J., Jackson C.R., Fedorka-Cray P. & Gebreyes W.A. 2012. Epidemiology and genotypic characteristics of methicillin-resistant Staphylococcus aureus strains of porcine origin. Journal of Clinical Microbiology. 50(11): 3687-3693.

Moo D., O'Boyle D., Mathers W. & Frost A.J. 1980. The isolation of Salmonella from jejunal and caecal lymph nodes of slaughtered animals. Australian Veterinary Journal. 56(4): 181-183.

Nitzsche S., Zweifel C. & Stephan R. 2007. Phenotypic and genotypic traits of Staphylococcus aureus strains isolated from pig carcasses. Veterinary Microbiology. 120(3) 292-299.

Normanno G., Dambrosio A., Lorusso V., Samoilis G., Di Taranto P. & Parisi A. 2015. Methicillin-resistant Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir workers in Italy. Food Microbiology. 51: 51-56.

O'Brien A.M., Hanson B.M., Farina S.A., Wu J.Y., Simmering J.E., Wardyn S.E. & Smith T.C. 2012. MRSA in conventional and alternative retail pork products. PLoS One. 7(1): e30092.

Perlin G.O., Pereira L.F., Ferreira B.P.M. & Martins L.A. 2015. Pesquisa de Staphylococcus aureus e Salmonella spp. em embutidos cárneos registrados em serviço de inspeção municipal – sim em 2012 de três municípios do estado do Paraná. Acta Veterinaria Brasilica. 9(1): 43-49.

Sambrook J. & Russel D.W. 2001. Molecular Cloning: a laboratory manual. 3rd edn. New York: Cold Spring Harbor Laboratory Press, 999p.

Tanih N.F., Sekwadi E., Ndip R.N. & Bessong P.O. 2015. Detection of pathogenic Escherichia coli and Staphylococcus aureus from cattle and pigs slaughtered in abattoirs in Vhembe District, South Africa. The Scientific World Journal. 2015: 195972.

Versalovic J., Schneider M., De Bruijn F.J. & Lupski J.R. 1994. Genomic fingerprinting of bacteria with repetitive sequence based polymerase chain reaction. Methods in Molecular and Cellular Biology. 5: 25-40.

Welker C.A.D., Both J.M.C., Longaray S.M., Haas S., Soeiro M.L.T. & RAMOS, R.C. 2010. Análise microbiológica dos alimentos envolvidos em surtos de doenças transmitidas por alimentos (DTA) ocorridos no estado do Rio Grande do Sul, Brasil. Revista Brasileira de Biociências. 8(1): 44-48.

DOI: https://doi.org/10.22456/1679-9216.84208

Copyright (c) 2018 Lauren Machado Moreira, Alana Borges Tavares, Celina Nunes Ebersol, Taís Gonçalves Gonçalves, Helenice Gonzalez de Lima, Natacha Debonim Cereser, Cláudio Dias Timm

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