[EN] Pork is considered a major source of Salmonella Typhimurium infection in humans in the EU, including monophasic strains (mST). Widespread distribution of virulent serotypes such as monophasic variants of S. Typhimurium have emerged as a public health threat. Despite the current situation, within the EU there is no mandatory programme for the control of Salmonella at pork production level. In this con- text, the aims of this study were: to examine the presence of Salmonella in the swine production system from arrival at the slaughterhouse until the end of processing, and investigate the genetic relationship among serovars. A total of 21 pig herds were intensively sampled during processing at the slaughter- house. ERIC-PCR followed by PFGE were performed among isolates recovered at the different steps in the slaughterhouse to assess their genetic relationship. The results showed a high level of Salmonella pork batch contamination upon arrival at the slaughterhouse (71.4%) and at the end of the slaughtering pro- cess (66.7%), with mST the main serovar isolated from both origins (53.1% and 38.2%, respectively). Similarly, this study shows that 14.3% of the strains isolated from carcasses have the same Xbal-PFGE pro- file as those previously recovered in the slaughterhouse environment, but not in the live animals from that same batch. In conclusion, there is a high level of Salmonella swine batch contamination upon arrival at the slaughterhouse and at the end of the slaughtering process, mST being the most frequently isolated serovar. Moreover, a strong genetic relationship has been observed between strains isolated from the batch on arrival at the slaughterhouse, the processing environment and pork carcass contamination. In this sense, it would be necessary to implement a control programme to reduce the bacterium from pork farms and raise the awareness of biosecurity measures. We wish to thank the slaughterhouse staff for their collaboration in the study and their technical support. In addition, we want to thank University CEU-UCH for the financial support (Consolidacion de Indicadores INDI 18/19 and IDOC 18/12). CERCA Programme from the Generalitat de Catalunya is also acknowledged. The English text version was revised by N. Macowan English Language Service. Marin, C.; Chinillac, MC.; Cerda-Cuellar, M.; Montoro-Dasí, L.; Sevilla-Navarro, S.; Marco-Jiménez, F.; Ayats, T.... (2020). Contamination of pig carcass with Salmonella enterica serovar Typhimurium monophasic variant 1,4 [5], 12: i:- originates mainly in live animals. Science of The Total Environment. 703:1-7. https://doi.org/10.1016/j.scitotenv.2019.134609 Amass, S.F, 2005a. Biosecurity: stopping the bugs from getting in. Pig J. 55, 104–114. Available online in: https://thepigsite.com/articles/biosecurity-stopping-the-bugs-from-getting-in-part-1-of-2 (accessed: 17th March, 2017). Andres, V. M., & Davies, R. H. (2015). Biosecurity Measures to Control Salmonella and Other Infectious Agents in Pig Farms: A Review. Comprehensive Reviews in Food Science and Food Safety, 14(4), 317-335. doi:10.1111/1541-4337.12137 ARGUELLO, H., ÁLVAREZ-ORDOÑEZ, A., CARVAJAL, A., RUBIO, P., & PRIETO, M. (2013). Role of Slaughtering in Salmonella Spreading and Control in Pork Production. Journal of Food Protection, 76(5), 899-911. doi:10.4315/0362-028x.jfp-12-404 Arguello, H., Carvajal, A., Collazos, J. A., García-Feliz, C., & Rubio, P. (2012). Prevalence and serovars of Salmonella enterica on pig carcasses, slaughtered pigs and the environment of four Spanish slaughterhouses. Food Research International, 45(2), 905-912. doi:10.1016/j.foodres.2011.04.017 Arguello, H., Carvajal, A., Naharro, G., Arcos, M., Rodicio, M. R., Martin, M. C., & Rubio, P. (2013). Sero- and genotyping of Salmonella in slaughter pigs, from farm to cutting plant, with a focus on the slaughter process. International Journal of Food Microbiology, 161(1), 44-52. doi:10.1016/j.ijfoodmicro.2012.11.013 Baptista, F. M., Alban, L., Nielsen, L. R., Domingos, I., Pomba, C., & Almeida, V. (2010). Use of Herd Information for Predicting Salmonella Status in Pig Herds. Zoonoses and Public Health, 57, 49-59. doi:10.1111/j.1863-2378.2010.01354.x Baptista, F. M., Dahl, J., & Nielsen, L. R. (2010). Factors influencing Salmonella carcass prevalence in Danish pig abattoirs. Preventive Veterinary Medicine, 95(3-4), 231-238. doi:10.1016/j.prevetmed.2010.04.007 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. International Journal of Food Microbiology, 163(2-3), 248-257. doi:10.1016/j.ijfoodmicro.2013.02.012 Botteldoorn, N., Heyndrickx, M., Rijpens, N., Grijspeerdt, K., & Herman, L. (2003). Salmonella on pig carcasses: positive pigs and cross contamination in the slaughterhouse. Journal of Applied Microbiology, 95(5), 891-903. doi:10.1046/j.1365-2672.2003.02042.x Campos, J., Mourão, J., Peixe, L., & Antunes, P. (2019). Non-typhoidal Salmonella in the Pig Production Chain: A Comprehensive Analysis of Its Impact on Human Health. Pathogens, 8(1), 19. doi:10.3390/pathogens8010019 Casanova-Higes, A., Marín-Alcalá, C. M., Andrés-Barranco, S., Cebollada-Solanas, A., Alvarez, J., & Mainar-Jaime, R. C. (2019). Weaned piglets: another factor to be considered for the control of Salmonella infection in breeding pig farms. Veterinary Research, 50(1). doi:10.1186/s13567-019-0666-7 Colello, R., Ruiz, M. J., Padín, V. M., Rogé, A. D., Leotta, G., Padola, N. L., & Etcheverría, A. I. (2018). Detection and Characterization of Salmonella Serotypes in the Production Chain of Two Pig Farms in Buenos Aires Province, Argentina. Frontiers in Microbiology, 9. doi:10.3389/fmicb.2018.01370 Dang-Xuan, S., Nguyen-Viet, H., Pham-Duc, P., Unger, F., Tran-Thi, N., Grace, D., & Makita, K. (2019). Risk factors associated with Salmonella spp. prevalence along smallholder pig value chains in Vietnam. International Journal of Food Microbiology, 290, 105-115. doi:10.1016/j.ijfoodmicro.2018.09.030 Davies, R., Gosling, R. ., Wales, A. D., & Smith, R. P. (2016). Use of an attenuated live Salmonella Typhimurium vaccine on three breeding pig units: A longitudinal observational field study. Comparative Immunology, Microbiology and Infectious Diseases, 46, 7-15. doi:10.1016/j.cimid.2016.03.005 De Busser, E. V., De Zutter, L., Dewulf, J., Houf, K., & Maes, D. (2013). Salmonella control in live pigs and at slaughter. The Veterinary Journal, 196(1), 20-27. doi:10.1016/j.tvjl.2013.01.002 Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010. Official Journal of European Union (DOI 20.10.2010). L276/33-79. Duggan, S.J., Mannion, C., Prendergast, D.M., Leonard, N., Fanning, S., Gonzales-Barron, U., Egan, J., Butler, F., Duffy, G., 2010. Tracking the Salmonella status of pigs and pork from lairage through the slaughter process in the Republic of Ireland. J. Food Prot. 73, 2148–2160. https://doi.org/10.4315/0362-028x-73.12.2148. Gomes-Neves, E., Antunes, P., Tavares, A., Themudo, P., Cardoso, M. F., Gärtner, F., … Peixe, L. (2012). Salmonella cross-contamination in swine abattoirs in Portugal: Carcasses, meat and meat handlers. International Journal of Food Microbiology, 157(1), 82-87. doi:10.1016/j.ijfoodmicro.2012.04.015 Grimont, P., Weill, F.X., 2007. Antigenic Formulae of the Salmonella servovars. 9th ed. WHO Collaborating Center for Reference and Research on Salmonella (WHOCC-Salm). Institut Pasteur, Paris. Hurd, H. S., McKean, J. D., Griffith, R. W., Wesley, I. V., & Rostagno, M. H. (2002). Salmonella enterica Infections in Market Swine with and without Transport and Holding. Applied and Environmental Microbiology, 68(5), 2376-2381. doi:10.1128/aem.68.5.2376-2381.2002 ISO 6579:2002 (Anexo D), 2002. Microbiology of Food and Animal Feeding Stuffs. Horizontal Method for the Detection of Salmonella spp. International Organization for Standardization, Geneve, Switzerland. Mannion, C., Fanning, J., McLernon, J., Lendrum, L., Gutierrez, M., Duggan, S., & Egan, J. (2012). The role of transport, lairage and slaughter processes in the dissemination of Salmonella spp. in pigs in Ireland. Food Research International, 45(2), 871-879. doi:10.1016/j.foodres.2011.02.001 Marin, C., & Lainez, M. (2009). Salmonella detection in feces during broiler rearing and after live transport to the slaughterhouse. Poultry Science, 88(9), 1999-2005. doi:10.3382/ps.2009-00040 Marquer, P., Rabade, T., Forti, R., 2014. Pig farming in the European Union, considerable variations from one Member State to another. Eurostat Stat. Focus 15, 1–12. http://ec.europa.eu/eurostat/statisticsexplained/index.php/Pig_farming_sector_-_statistical_portrait_2014 (accessed: 1st March, 2017). Moré, E., Ayats, T., Ryan, P. G., Naicker, P. R., Keddy, K. H., Gaglio, D., … Cerdà-Cuéllar, M. (2017). Seabirds (Laridae) as a source ofCampylobacter spp.,Salmonellaspp. and antimicrobial resistance in South Africa. Environmental Microbiology, 19(10), 4164-4176. doi:10.1111/1462-2920.13874 MULDER, R. W. A. W. (1995). IMPACT OF TRANSPORT AND RELATED STRESSES ON THE INCIDENCE AND EXTENT OF HUMAN PATHOGENS IN PIGMEAT AND POULTRY. Journal of Food Safety, 15(3), 239-246. doi:10.1111/j.1745-4565.1995.tb00136.x Pesciaroli, M., Cucco, L., De Luca, S., Massacci, F. R., Maresca, C., Medici, L., … Magistrali, C. F. (2017). Association between pigs with high caecal Salmonella loads and carcass contamination. International Journal of Food Microbiology, 242, 82-86. doi:10.1016/j.ijfoodmicro.2016.11.021 Schut, C. H., Farzan, A., Ainslie-Garcia, M. H., Friendship, R. M., & Lillie, B. N. (2019). Antibody Responses to Salmonella in Pigs from Weaning Up to Marketing and Presence of Salmonella at Slaughter. Foodborne Pathogens and Disease, 16(3), 187-194. doi:10.1089/fpd.2018.2454 Vidic, B., Savic, S., Prica, N., & Suvajdzic, L. (2015). Epizootiology and Control Measures for Salmonella in Pigs. Procedia Food Science, 5, 312-315. doi:10.1016/j.profoo.2015.09.067 Visscher, C. F., Klein, G., Verspohl, J., Beyerbach, M., Stratmann-Selke, J., & Kamphues, J. (2011). Serodiversity and serological as well as cultural distribution of Salmonella on farms and in abattoirs in Lower Saxony, Germany. International Journal of Food Microbiology, 146(1), 44-51. doi:10.1016/j.ijfoodmicro.2011.01.038

MAGRAMA (Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente), 2016. http://www.mapama.gob.es/es/ministerio/servicios/informacion/plataforma-de-conocimiento-para-el-medio-rural-y-pesquero/observatorio-de-tecnologias-probadas/sistemas-prodnut-animal/ganado-porcino.aspx (accessed: 28th December, 2016).

MAGRAMA (Ministry of Agriculture and Fisheries, Food and Environment), 2016. http://www.mapama.gob.es/es/ministerio/servicios/informacion/plataforma-de-conocimiento-para-el-medio-rural-y-pesquero/observatorio-de-tecnologias-probadas/sistemas-prodnut-animal/ganado-porcino.aspx (accessed: 28th decade, 2016).

Contamination of pig carcass with Salmonella enterica serovar Typhimurium monophasic variant 1,4 [5], 12: i:- originates mainly in live animals

Abstract