Salmonella spp. in Pigs Slaughtered in Small and Medium-Sized Abattoirs in Central Italy: Preliminary Results on Occurrence and Control Strategies
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. Isolation, Identification, and Serotyping
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- European Food Safety Authority & European Centre for Disease Prevention and Control. The European Union One Health 2019 Zoonoses Report. EFSA J. 2021, 19, 6406. [Google Scholar]
- ANVISA. Ministério da Saúde. Surtos de Doenças Transmitidas por Alimentos no Brasil. Available online: http://portalarquivos2.saude.gov.br/images/pdf/2019/fevereiro/15/Apresenta----o-Surtos-DTA---Fevereiro-2019.pdf (accessed on 24 June 2021).
- Centers for Disease Control and Prevention (CDC). Surveillance for Foodborne Disease Outbreaks, United States, 2017, Annual Report; Department of Health and Human Services: Atlanta, GA, USA, 2019.
- Gurman, P.M.; Ross, T.; Kiermeier, A. Quantitative Microbial Risk Assessment of Salmonellosis from the Consumption of Australian Pork: Minced Meat from Retail to Burgers Prepared and Consumed at Home. Risk Anal. 2016, 38, 2625–2645. [Google Scholar] [CrossRef]
- Sodagari, H.R.; Wang, P.; Robertson, I.; Habib, I.; Sahibzada, S. Non-Typhoidal Salmonella at the Human-Food-of-Animal-Origin Interface in Australia. Animals 2020, 10, 1192. [Google Scholar] [CrossRef]
- Wang, J.; Li, J.; Liu, F.; Cheng, Y.; Su, J. Characterization of Salmonella enterica Isolates from Diseased Poultry in Northern China between 2014 and 2018. Pathogens 2020, 9, 95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Graziani, C.; Mughini-Gras, L.; Owczarek, S.; Dionisi, A.M.; Luzzi, I.; Busani, L. Distribution of Salmonella Enterica Isolates from Human Cases in Italy, 1980 to 2011. Eurosurveillance 2013, 18, 20519. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piras, F.; Brown, D.; Meloni, D.; Mureddu, A.; Mazzette, R. Investigation of Salmonella Enterica in Sardinian Slaughter Pigs: Prevalence, Serotype and Genotype Characterization. Int. J. Food Microbiol. 2011, 151, 201–209. [Google Scholar] [CrossRef] [PubMed]
- Andres, V.M.; Davies, R.H. Biosecurity Measures to Control Salmonella and Other Infectious Agents in Pig Farms: A Review. Compr. Rev. Food Sci. Food Saf. 2015, 14, 317–335. [Google Scholar] [CrossRef]
- Campos, J.; Mourão, J.; Peixe, L.; Antunes, P. Non-Typhoidal Salmonella in the Pig Production Chain: A Comprehensive Analysis of Its Impact on Human Health. Pathogens 2019, 8, 19. [Google Scholar] [CrossRef] [Green Version]
- Massacci, F.R.; Morelli, A.; Cucco, L.; Castinel, A.; Ortenzi, R.; Tofani, S.; Pezzotti, G.; Estellé, J.; Paniccià, M.; Magistrali, C.F. Transport to the Slaughterhouse Affects the Salmonella Shedding and Modifies the Fecal Microbiota of Finishing Pigs. Animals 2020, 10, 676. [Google Scholar] [CrossRef]
- Bonardi, S.; Morganti, M.; Pupillo, G.; Brindani, F. Salmonella Brandenburg in the Pork Chain in Italy: Genetic Comparison with the Human Isolates. Ital. J. Food Saf. 2018, 7, 6938–6940. [Google Scholar] [CrossRef] [Green Version]
- Hill, A.A.; Simons, R.; Swart, A.N.; Kelly, L.; Hald, T.; Snary, E.L. Assessing the Effectiveness of On-Farm and Abattoir Interventions in Reducing Pig Meat-Borne Salmonellosis within E.U. Member States. Risk Anal. 2016, 36, 546–560. [Google Scholar] [CrossRef]
- Bonardi, S.; Alpigiani, I.; Bruini, I.; Barilli, E.; Brindani, F.; Morganti, M.; Cavallini, P.; Bolzoni, L.; Pongolini, S. Detection of Salmonella Enterica in Pigs at Slaughter and Comparison with Human Isolates in Italy. Int. J. Food Microbiol. 2016, 218, 44–50. [Google Scholar] [CrossRef]
- Botteldoorn, N.; Heyndrickx, M.; Rijpens, N.; Grijspeerdt, K.; Herman, L. Salmonella on Pig Carcasses: Positive Pigs and Cross Contamination in the Slaughterhouse. J. Appl. Microbiol. 2003, 95, 891–903. [Google Scholar] [CrossRef] [Green Version]
- Pesciaroli, M.; Cucco, L.; De Luca, S.; Massacci, F.; Maresca, C.; Medici, L.; Paniccià, M.; Scoccia, E.; Staffolani, M.; Pezzotti, G.; et al. Association between Pigs with High Caecal Salmonella Loads and Carcass Contamination. Int. J. Food Microbiol. 2017, 242, 82–86. [Google Scholar] [CrossRef] [PubMed]
- Swanenburg, M.; Urlings, H.A.P.; Keuzenkamp, D.A.; Snijders, J.M.A. Salmonella in the Lairage of Pig Slaughterhouses. J. Food Prot. 2001, 64, 12–16. [Google Scholar] [CrossRef] [PubMed]
- Marín, C.; Chinillac, M.C.; Cerdà-Cuéllar, M.; Dasí, L.M.; Navarro, S.S.; Ayats, T.; Marco-Jimenez, F.; Vega, S. Contamination of Pig Carcass with Salmonella Enterica Serovar Typhimurium Monophasic Variant 1,4[5],12:i:- originates mainly in live animals. Sci. Total. Environ. 2019, 703, 134609. [Google Scholar] [CrossRef] [PubMed]
- Correia-Gomes, C.; Leonard, F.; Graham, D. Description of Control Programmes for Salmonella in Pigs in Europe. Progress to Date? J. Food Saf. 2021, e12916. [Google Scholar] [CrossRef]
- Bersot, L.D.S.; Cavicchioli, V.Q.; Viana, C.; Burin, R.C.K.; Camargo, A.C.; de Almeida Nogueira Pinto, J.P.; Nero, L.A.; Destro, M.T. Prevalence, Antimicrobial Resistance, and Diversity of Salmonella along the Pig Production Chain in Southern Brazil. Pathogens 2019, 8, 204. [Google Scholar] [CrossRef] [Green Version]
- EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on the Public Health Hazards to be Covered by Inspection of Meat (Swine). EFSA J. 2011, 9, 2351. [Google Scholar] [CrossRef] [Green Version]
- Sánchez-Rodríguez, J.; Navas, L.; Vinuesa, F.; Castells, C.; Martínez, M.; López, A.; Lindez, B.; Cabrera-Vique, C. New insights on the risk factors associated with the presence of Salmonella on pig carcasses. Lessons from small slaughterhouses. Food Control. 2018, 87, 46–52. [Google Scholar] [CrossRef]
- Technical specifications on harmonised epidemiological indicators for public health hazards to be covered by meat inspection of swine. EFSA J. 2011, 9, 2371. [CrossRef]
- European Commission. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Off. J. Eur. Union 2005, 338, 1–26. [Google Scholar]
- European Commission. Commission Regulation (EU) No 218/2014 of 7 March 2014 amending Annexes to Regulations (EC) No 853/2004 and (EC) No 854/2004 of the European Parliament and of the Council and Commission Regulation (EC) No 2074/2005. Off. J. Eur. Union 2014, 69, 95–98. [Google Scholar]
- AFNOR (AFNOR BIO 12/10-09/02). Available online: https://nf-validation.afnor.org/wp-content/uploads/2014/03/Synt-BIO-12-10-09-02_en.pdf (accessed on 19 July 2021).
- International Organization for Standardization. EN ISO 6579-1:2017. Microbiology of the Food Chain—Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella—Part 1: Detection of Salmonella spp.; International Organization for Standardization: Geneve, Switzerland, 2017. [Google Scholar]
- Grimont, P.A.D.; Weill, F.-X. Antigenic Formulae of the Salmonella Serovars. In WHO Collaborating Center for Ref-erence and Research on Salmonella, 9th ed.; Institut Pasteur: Paris, France, 2007; Available online: http://www.scacm.org/free/Antigenic%20Formulae%20of%20the%20Salmonella%20Serovars%202007%209th%20edition.pdf (accessed on 17 July 2021).
- Epi Info 7.2, CDC Division of Health Informatics & Surveillance (DHIS), Center for Surveillance, Epidemiology & Laboratory Services (CSELS). Available online: https://www.cdc.gov/epiinfo/index.html (accessed on 14 August 2021).
- Ghafir, Y.; China, B.; Korsak, N.; Dierick, K.; Collard, J.-M.; Godard, C.; De Zutter, L.; Daube, G. Belgian Surveillance Plans To Assess Changes in Salmonella Prevalence in Meat at Different Production Stages. J. Food Prot. 2005, 68, 2269–2277. [Google Scholar] [CrossRef] [Green Version]
- Cilia, G.; Turchi, B.; Fratini, F.; Bilei, S.; Bossù, T.; De Marchis, M.L.; Cerri, D.; Pacini, M.I.; Bertelloni, F. Prevalence, Virulence and Antimicrobial Susceptibility of Salmonella spp., Yersinia enterocolitica and Listeria monocytogenes in European Wild Boar (Sus scrofa) Hunted in Tuscany (Central Italy). Pathogens 2021, 10, 93. [Google Scholar] [CrossRef]
- Zhou, Z.; Jin, X.; Zheng, H.; Li, J.; Meng, C.; Yin, K.; Xie, X.; Huang, C.; Lei, T.; Sun, X.; et al. The prevalence and load of Salmonella, and key risk points of Salmonella contamination in a swine slaughterhouse in Jiangsu province, China. Food Control. 2018, 87, 153–160. [Google Scholar] [CrossRef]
- Powell, L.F.; Cheney, T.E.A.; Williamson, S.; Guy, E.; Smith, R.P.; Davies, R.H. A Prevalence Study of Salmonella spp., Yersinia spp., Toxoplasma gondii and Porcine Reproductive and Respiratory Syndrome Virus in UK Pigs at Slaughter. Epidemiol. Infect. 2015, 144, 1538–1549. [Google Scholar] [CrossRef] [Green Version]
- Fois, F.; Piras, F.; Torpdahl, M.; Mazza, R.; Consolati, S.G.; Spanu, C.; Scarano, C.; De Santis, E.P.L. Occurrence, Characterization, and Antimicrobial Susceptibility of Salmonella Entericain Slaughtered Pigs in Sardinia. J. Food Sci. 2017, 82, 969–976. [Google Scholar] [CrossRef]
- Di Ciccio, P.; Ossiprandi, M.C.; Zanardi, E.; Ghidini, S.; Belluzzi, G.; Vergara, A.; Ianieri, A. Microbiological Contamination in Three Large-Scale Pig Slaughterhouses in Northern Italy. Ital. J. Food Saf. 2016, 5, 6151. [Google Scholar] [CrossRef]
- Arguello, H.; Carvajal, A.; Collazos, J.A.; García-Feliz, C.; Rubio, P. Prevalence and Serovars of Salmonella Enterica on Pig Carcasses, Slaughtered Pigs and the Environment of Four Spanish Slaughterhouses. Food Res. Int. 2012, 45, 905–912. [Google Scholar] [CrossRef]
- Ghougal, K.; Dib, A.L.; Lakhdara, N.; Lamri, M.; Baghezza, S.; Azizi, A.; Merrad, R.; Zouikri, A.; Cheraitia, D.; Trouni, M.; et al. Risk factors related to bacterial contamination by Enterobacteriaceae and fecal coliforms and the prevalence of Salmonella spp. in Algerian farms, slaughterhouses and butcheries: A two-year follow-up study. Math. Biosci. Eng. 2021, 6, 768–785. [Google Scholar] [CrossRef]
- Bonardi, S.; Bruini, I.; Magnani, R.; Cannistrà, N.; Brindani, F. Low Prevalence of Salmonella Enterica in Cull Dairy Cattle at Slaughter in Northern Italy. Ital. J. Food Saf. 2017, 6, 6172. [Google Scholar] [CrossRef] [Green Version]
- Wheatley, P.; Giotis, E.S.; McKevitt, A.I. Effects of Slaughtering Operations on Carcass Contamination in an Irish Pork Production Plant. Ir. Vet. J. 2014, 67, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baptista, F.; Dahl, J.; Nielsen, L. Factors influencing Salmonella carcass prevalence in Danish pig abattoirs. Prev. Veter. Med. 2010, 95, 231–238. [Google Scholar] [CrossRef]
- Magossi, G.; Bai, J.; Cernicchiaro, N.; Jones, C.; Porter, E.; Trinetta, V. Seasonal Presence of Salmonella spp., Salmonella Typhimurium and Its Monophasic Variant Serotype I 4,[5],12:i:-, in Selected United States Swine Feed Mills. Foodborne Pathog. Dis. 2019, 16, 276–281. [Google Scholar] [CrossRef] [PubMed]
- Arguello, H.; Alvarez-Ordóñez, A.; Carvajal, A.; Rubio, P.; Prieto, M. Role of Slaughtering in Salmonella Spreading and Control in Pork Production. J. Food Prot. 2013, 76, 899–911. [Google Scholar] [CrossRef] [PubMed]
- European Commission. Commission Regulation (EC) No 2160/2003 of the European Parliament and of the Council of 17 November 2003 on the Control of Salmonella and Other Specified Food-Borne Zoonotic Agents. Off. J. Eur. Union 2003, 325, 1–15. [Google Scholar]
- Martínez-Avilés, M.; Garrido-Estepa, M.; Álvarez, J.; De La Torre, A. Salmonella Surveillance Systems in Swine and Humans in Spain: A Review. Veter. Sci. 2019, 6, 20. [Google Scholar] [CrossRef] [Green Version]
- European Commission. Commission Regulation (EC) No. 852/2004 of the European Parliament and of the Council of 29 April 2004 on the Hygiene of Foodstuffs. Off. J. Eur. Union 2004, 139, 1–23. [Google Scholar]
- European Commission. Regulation (EU) of the Commission No 217/2014 of 7 March 2014 amending Regulation (EC) No 2073/2005 as Regards Salmonella in Pig Carcases. Off. J. Eur. Union 2014, 69, 93–94. [Google Scholar]
- Møgelmose, V.; Lindegaard, L.L.; Dahl, J. A Sudden Increase in Salmonella—How the Surveillance System Reacted: A Danish Experience. In Proceedings of the 12th International Symposium on the Epidemiology and Control of Biological, Chemical and Physical Hazards in Pigs and Pork, Foz doIguaçu, Brazil, 21–24 August 2017; pp. 116–120. [Google Scholar] [CrossRef]
- SANCO/2008/E2/036. Analysis of the Costs and Benefits of Setting a Target for the Reduction of Salmonella in Slaughter Pigs”, Report for EUROPEAN COMMISSION Health and Consumers Directorate-General, June 2010. Available online: https://ec.europa.eu/food/system/files/2016-10/biosafety_food-borne-disease_salmonella_fattening-pigs_slaughthouse-analysis-costs.pdf (accessed on 20 July 2021).
Salmonella Serovars | Overall (%) (n = 45) | Season | Slaughterhouse Capacity | ||
---|---|---|---|---|---|
Spring/Summer (%) (n = 25) | Autumn/Winter (%) (n = 20) | <5000 Animals/Year (%) (n = 8) | 5000–50,000 Animals/Year (%) (n = 37) | ||
4,[5],12:i:- | 33.33 | 36.00 | 30.00 | 50.00 | 29.73 |
Derby | 40.00 | 44.00 | 35.00 | 25.00 | 43.24 |
Infantis | 2.22 | 0.00 | 5.00 | 0.00 | 2.70 |
Bredeney | 4.44 | 4.00 | 5.00 | 0.00 | 5.41 |
Typhimurium | 2.22 | 4.00 | 0.00 | 12.50 | 0.00 |
Give | 2.22 | 0.00 | 5.00 | 12.50 | 0.00 |
London | 4.44 | 0.00 | 10.00 | 0.00 | 5.41 |
Rissen | 6.67 | 4.00 | 10.00 | 0.00 | 8.11 |
Brandeburg | 2.22 | 4.00 | 0.00 | 0.00 | 2.70 |
Goldcoast | 2.22 | 4.00 | 0.00 | 0.00 | 2.70 |
Salmonella Serovars | 2017 (%) (n = 8) | 2018 (%) (n = 21) | 2019 (%) (n = 16) |
---|---|---|---|
4,[5],12:i:- | 50.00 | 23.80 | 37.50 |
Derby | 37.50 | 57.10 | 18.80 |
Infantis | 12.50 | 0.00 | 0.00 |
Bredeney | 0.00 | 9.50 | 0.00 |
Typhimurium | 0.00 | 4.80 | 0.00 |
Give | 0.00 | 4.80 | 0.00 |
London | 0.00 | 0.00 | 12.50 |
Rissen | 0.00 | 0.00 | 18.80 |
Brandeburg | 0.00 | 0.00 | 6.30 |
Goldcoast | 0.00 | 0.00 | 6.30 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Primavilla, S.; Roila, R.; Zicavo, A.; Ortenzi, R.; Branciari, R.; Shtylla Kika, T.; Valiani, A.; Ranucci, D. Salmonella spp. in Pigs Slaughtered in Small and Medium-Sized Abattoirs in Central Italy: Preliminary Results on Occurrence and Control Strategies. Appl. Sci. 2021, 11, 7600. https://doi.org/10.3390/app11167600
Primavilla S, Roila R, Zicavo A, Ortenzi R, Branciari R, Shtylla Kika T, Valiani A, Ranucci D. Salmonella spp. in Pigs Slaughtered in Small and Medium-Sized Abattoirs in Central Italy: Preliminary Results on Occurrence and Control Strategies. Applied Sciences. 2021; 11(16):7600. https://doi.org/10.3390/app11167600
Chicago/Turabian StylePrimavilla, Sara, Rossana Roila, Alessia Zicavo, Roberta Ortenzi, Raffaella Branciari, Tana Shtylla Kika, Andrea Valiani, and David Ranucci. 2021. "Salmonella spp. in Pigs Slaughtered in Small and Medium-Sized Abattoirs in Central Italy: Preliminary Results on Occurrence and Control Strategies" Applied Sciences 11, no. 16: 7600. https://doi.org/10.3390/app11167600
APA StylePrimavilla, S., Roila, R., Zicavo, A., Ortenzi, R., Branciari, R., Shtylla Kika, T., Valiani, A., & Ranucci, D. (2021). Salmonella spp. in Pigs Slaughtered in Small and Medium-Sized Abattoirs in Central Italy: Preliminary Results on Occurrence and Control Strategies. Applied Sciences, 11(16), 7600. https://doi.org/10.3390/app11167600