Occurrence of Listeria monocytogenes in Ready-to-Eat Meat Products and Meat Processing Plants in Spain
Abstract
:1. Introduction
2. Experimental Section
2.1. Sampling of RTE Meat Products
Meat Processing Plant | Province | Samples (n) of RTE Meat Products | Samples (n) of Work Surface Samples | ||||||
---|---|---|---|---|---|---|---|---|---|
Cooked | Raw-Cured | Dry-Cured, Salted | Stainless Steel | Conveyor Belt | Cutting Board | ||||
Dirty | Clean | Dirty | Clean | Dirty | |||||
1 | Zaragoza | 4 | 3 | 1 | 3 | ||||
2 | Zaragoza | 2 | 2 | 2 | |||||
3 | Zaragoza | 2 | 2 | 4 | 1 | ||||
4 | Zaragoza | 2 | 6 | 1 | |||||
5 | Zaragoza | 4 | 5 | 3 | |||||
6 | Teruel | 2 | 3 | 1 | 4 | 2 | |||
7 | Teruel | 2 | 1 | 2 | |||||
8 | Teruel | 1 | 1 | 1 | 2 | ||||
9 | Teruel | 5 | 4 | 1 | 4 | 2 | |||
10 | Teruel | 1 | 1 | 2 | |||||
11 | Teruel | 1 | 1 | 1 | 2 | 1 | |||
12 | Teruel | 2 | 3 | 4 | |||||
13 | Salamanca | 2 | 1 | 2 | |||||
14 * | Salamanca | 2 | |||||||
15 | Salamanca | 1 | 2 | 1 | 2 | ||||
16 | Salamanca | 2 | 2 | 1 | |||||
17 | Salamanca | 2 | 2 | 1 | |||||
18 | Salamanca | 2 | 1 | 1 | |||||
19 | Cáceres | 3 | 1 | 2 | 3 | ||||
20 | Cáceres | 1 | 2 | 1 | |||||
21 | Cáceres | 2 | 1 | 1 | |||||
22 | Cáceres | 1 | 1 | 1 | 1 | ||||
23 | Badajoz | 2 | 2 | ||||||
24 | Badajoz | 2 | 2 | 2 | |||||
25 * | Badajoz | 1 | |||||||
26 | Badajoz | 1 | 1 | 1 | 1 | ||||
27 | Badajoz | 3 | 1 | ||||||
28 | Huelva | 1 | 5 | 2 | 1 | ||||
29 | Huelva | 1 | 1 | 1 | 1 | ||||
30 | Huelva | 2 | 2 | ||||||
31 | Huelva | 1 | 2 | 2 | 1 | ||||
32 | Huelva | 1 | 1 | 1 | |||||
Total | -- | 15 | 49 | 23 | 50 | 29 | 23 | 5 | 3 |
2.2. Sampling of Work Surfaces
2.3. Microbiological Analysis
2.4. Statistical Study
3. Results
3.1. Listeria Monocytogenes in RTE Meat Products
3.2. Listeria Monocytogenes in Environmental Samples from Meat Processing Plants
4. Discussion
Country/Area | Sample Type | n | Prevalence | Reference |
---|---|---|---|---|
Cooked Meat Products | ||||
New Zealand | Prepackaged pâté | 300 | 0.33% | [16] |
Packaged cooked ham | 104 | 0% | [16] | |
New Zealand | Cooked ham | 301 | 3.3% | [17] |
European Union | Heat treated RTE meat products | 3530 | 2.07% | [18] |
Belgium | Cooked meat products | 3405 | 4.9% | [19] |
Belgium | Cooked meat products | 639 | 1.1% | [20] |
Sweden | Cooked meat products | 507 | 1.2% | [21] |
United Kingdom | Cooked and sliced cold meat | 2894 | 2.07% | [22] |
Cooked and sliced pâté | 1184 | 1.86% | [22] | |
Spain | Pâté | 182 | 5.4% | [23] |
Spain | Sliced cooked meat products | 68 | 7.3% | [24] |
Spain | Vacuum-packed deli meat products | 420 | 5.48% | [25] |
Vacuum-packed pâté | 120 | 0.8% | [25] | |
Spain | Sliced cooked meat products | 396 | 8.8% | [26] |
Spain | Cooked products | 35 | 5.71% | This study |
Raw-Cured Meat Products | ||||
Brazil | Salami | 81 | 7.41% | [27] |
Brazil | Sliced salami | 45 | 6.7% | [28] |
Turkey | Fermented sausages | 300 | 11.7% | [29] |
France | Dried sausages | 30 | 10% | [30] |
Italy | Fermented sausages | 237 | 15.2% | [31] |
Spain | Raw-cured sausages | 72 | 30.55% | [32] |
Spain | Raw-cured sausages | 102 | 10.78% | [33] |
Spain | Raw-cured sausages | 19 | 15.8% | [34] |
Spain | Cured meat products | 345 | 6.7% | [26] |
Spain | Raw-cured meat products | 57 | 5.26% | This study |
Dry-Cured Salted Meat Products | ||||
Italy | Dry-cured and salted ham | 490 | 4.1% | [35] |
Deboned ham | 708 | 2% | [35] | |
Spain | Dry-cured salted products | 37 | 2.70% | This study |
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Meloni, D. Presence of Listeria monocytogenes in Mediterranean-Style Dry Fermented Sausages. Foods 2015, 4, 34–50. [Google Scholar] [CrossRef]
- Codex Alimentarius. Guidelines on the Application of General Principles of Food Hygiene to the Control of Listeria monocytogenes in Foods; Codex Alimentarius: Rome, Italy, 2007. [Google Scholar]
- Pradhan, A.B.; Ivanek, R.; Gröhn, Y.T.; Geornaras, I.; Sofos, J.H.; Wiedmann, M. Quantitative risk assessment for Listeria monocytogenes in selected categories of deli meats: Impact of lactate and diacetate on listeriosis cases and deaths. J. Food Prot. 2009, 72, 978–989. [Google Scholar] [PubMed]
- Williams, S.K.; Roof, S.; Boyle, E.A.; Burson, D.; Thippareddi, H.; Geornaras; Sofos, J.N.; Wiedmann, M.; Nightingale, K. Molecular ecology of Listeria monocytogenes and other Listeria species in small and very small ready-to-eat meat processing plants. J. Food Prot. 2011, 74, 63–77. [Google Scholar] [CrossRef] [PubMed]
- Cogan, T.A.; Slader, J.; Bloomfield, S.F.; Humphrey, T.J. Achieving hygiene in the domestic kitchen: The effectiveness of commonly used cleaning procedures. J. Appl. Microbiol. 2002, 92, 885–892. [Google Scholar] [CrossRef] [PubMed]
- Domínguez, L.; Badiola, J.J.; Cepeda, A.; Más, A.; Rodríguez, E.; Zurera, G.; Téllez, S. Report of the Scientific Committee of the Spanish Agency for Food Safety and Nutrition (AESAN) in relation to biofilms and its impact on food safety. Rev. Com. Cient. 2010, 12, 37–61. [Google Scholar]
- Blackman, I.C.; Frank, J.F. Growth of Listeria monocytogenes as a biofilm on various food-processing surfaces. J. Food Prot. 1996, 59, 827–831. [Google Scholar]
- Di Bonaventura, G.; Piccolomini, R.; Paludi, D.; D’Orio, V.; Vergara, A.; Conter, M.; Ianieri, A. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: Relationship with motility and cell surface hydrophobicity. J. Appl. Microbiol. 2008, 104, 1552–1561. [Google Scholar] [CrossRef] [PubMed]
- Lahou, E.; Uyttendaele, M. Evaluation of Three Swabbing Devices for Detection of Listeria monocytogenes on Different Types of Food Contact Surfaces. Int. J. Environ. Res. Public Health 2014, 11, 804–814. [Google Scholar] [CrossRef] [PubMed]
- Gómez, D.; Ariño, A.; Carramiñana, J.J.; Rota, C.; Yangüela, J. Comparison of sampling procedures for recovery of Listeria monocytogenes from stainless Steel food contact surfaces. J. Food Prot. 2012, 75, 1077–1082. [Google Scholar] [CrossRef] [PubMed]
- Petrie, A.; Watson, P. Statistics for Veterinary and Animal Science; Blackwell Science: Oxford, UK, 1999; p. 243. [Google Scholar]
- Araújo, P.C.C.; Franco, R.M.; Oliveira, L.A.T.; Carvalho, J.C.A.P. Occurrence of Listeria monocytogenes in turkey’s meat products commercialized in Niterói country-RJ- Brazil. Acta Sci. Vet. 2002, 30, 19–25. [Google Scholar]
- Martins, E.A.; Leal, P.M. Listeria monocytogenes in ready-to-eat, sliced, cooked ham and salami products, marketed in the city of São Paulo, Brazil: Occurrence, quantification, and serotyping. Food Control 2011, 22, 297–302. [Google Scholar] [CrossRef]
- Ingham, S.C.; Buege, D.R.; Dropp, B.K.; Losinski, J.A. Survival of Listeria monocytogenes during Storage of Ready-to-Eat Meat Products Processed by Drying, Fermentation, and/or Smoking. J. Food Prot. 2004, 67, 2698–2702. [Google Scholar] [PubMed]
- Leistner, L. Basic aspects of food preservation by hurdle technology. Int. J. Food Microbiol. 2000, 55, 181–186. [Google Scholar] [CrossRef]
- Wong, T.L.; Carey-Smith, G.V.; Hollis, L.; Hudson, J.A. Microbiological survey of prepackaged pâté and ham in New Zealand. Lett. Appl. Microbiol. 2005, 41, 106–107. [Google Scholar] [CrossRef] [PubMed]
- Cornelius, A.J.; Hudson, J.A.; Wong, T.L. Enumeration and growth of naturally occurring Listeria spp. in unpackaged ham. Food Microbiol. 2008, 25, 407–412. [Google Scholar] [CrossRef] [PubMed]
- EFSA (European Food safety Authority). Analysis of the baseline survey on the prevalence of Listeria monocytogenes in certain ready-to-eat foods in the EU, 2010–2011 Part A: Listeria monocytogenes prevalence estimates. EFSA J. 2013, 11, 3241. [Google Scholar] [CrossRef]
- Uyttendaele, M.; De Troy, P.; Debevere, J. Incidence of Listeria monocytogenes in different types of meat products on the Belgian retail market. Int. J. Food Microbiol. 1999, 53, 75–80. [Google Scholar] [CrossRef]
- Uyttendaele, M.; Busschaert, P.; Valero, A.; Geeraerd, A.H.; Vermeulen, A.; Jacxsens, L.; Goh, K.K.; de Loy, A.; van Impe, J.F.; Devlieghere, F. Prevalence and challenge tests of Listeria monocytogenes in Belgian produced and retailed mayonnaise-based deli-salads, cooked meat products and smoked fish between 2005 and 2007. Int. J. Food Microbiol. 2009, 133, 94–104. [Google Scholar] [CrossRef] [PubMed]
- Lambertz, S.T.; Nilsson, C.; Brådenmark, A.; Sylvén, S.; Johansson, A.; Jansson, L.M.; Lindblad, M. Prevalence and level of Listeria monocytogenes in ready-to-eat foods in Sweden 2010. Int. J. Food Microbiol. 2012, 160, 24–31. [Google Scholar] [CrossRef] [PubMed]
- Elson, R.; Burgess, F.; Little, C.L.; Mitchell, R.T. Microbiological examination of ready-to-eat cold sliced meats and pâté from catering and retail premises in the UK. J. Appl. Microbiol. 2004, 96, 499–509. [Google Scholar] [CrossRef] [PubMed]
- Dominguez, C.; Gomez, I.; Zumalacarregui, J. Prevalence and contamination levels of Listeria monocytogenes in smoked fish and pate sold in Spain. J. Food Prot. 2001, 64, 2075–2077. [Google Scholar] [PubMed]
- Pérez-Rodríguez, F.; Castro, R.; Posada-Izquierdo, G.D.; Valero, A.; Carrasco, E.; García-Gimeno, R.M.; Zurera, G. Evaluation of hygiene practices and microbiological quality of cooked meat products during slicing and handling at retail. Meat Sci. 2010, 86, 479–485. [Google Scholar] [CrossRef] [PubMed]
- Garrido, V.; Vitas, A.I.; García-Jalón, I. Survey of Listeria monocytogenes in ready-to-eat products: Prevalence by brands and retail establishments for exposure assessment of listeriosis in Northern Spain. Food Control 2009, 20, 986–991. [Google Scholar] [CrossRef]
- Vitas, A.I.; Aguado, V.; García-Jalón, I. Occurrence of Listeria monocytogenes in fresh and processed foods in Navarra (Spain). Int. J. Food Microbiol. 2004, 90, 349–356. [Google Scholar] [CrossRef]
- Borges, M.F.; de Siqueira, R.S.; Bittencourt, A.M.; Vanetti, M.C.D.; Gomide, L.A.M. Occurrence of Listeria monocytogenes in salami. Rev. Microbiol. 1999, 30, 362–364. [Google Scholar] [CrossRef]
- Sakate, R.I.; Aragon, L.C.; Raghiante, F.; Landgraf, M.; Franco, B.D.G.M.; Destro, M.T. Occurrence of Listeria monocytogenes in pre-sliced vacuum-packaged salami in São Paulo-Brazil. Arch. Latinoam. Nutr. 2003, 53, 184–187. [Google Scholar] [PubMed]
- Colak, H.; Hampikyan, H.; Ulusoy, B.; Bingol, E.B. Presence of Listeria monocytogenes in Turkish style fermented sausage (sucuk). Food Control 2007, 18, 30–32. [Google Scholar] [CrossRef]
- Thévenot, D.; Delignette-Muller, M.L.; Christieans, S.; Vernozy-Rozand, C. Prevalence of Listeria monocytogenes in 13 dried sausage processing plants and their products. Int. J. Food Microbiol. 2005, 102, 85–94. [Google Scholar] [CrossRef] [PubMed]
- De Cesare, A.; Mioni, R.; Manfreda, G. Prevalence of Listeria monocytogenes in fresh and fermented Italian sausages and ribotyping of contaminating strains. Int. J. Food Microbiol. 2007, 120, 124–130. [Google Scholar] [CrossRef] [PubMed]
- Rota, C.; Yangüela, J.; Blanco, D.; Carramiñana, J.J.; Herrera, A. Presencia de Listeria monocytogenes y Listeria sp. en longanizas frescas y curadas. Utilización de distintas condiciones de tiempo y temperatura de incubación. J. Vet. Med. B 1997, 44, 617–624. [Google Scholar] [CrossRef]
- Yangüela, J.; Blanco, D.; Carramiñana, J.J.; Rota, C.; Roncalés, P.; Herrera, A. Ecología microbiana y calidad sanitaria de la longaniza de Aragón. Microbiol. Aliment. Nutr. 1996, 14, 133–146. [Google Scholar]
- Martín, B.; Garriga, M.; Aymerich, T. Prevalence of Salmonella spp. and Listeria monocytogenes at small-scale Spanish factories producing traditional factories producing traditional fermented sausages. J. Food Prot. 2011, 74, 812–815. [Google Scholar] [CrossRef] [PubMed]
- Giovannini, A.; Migliorati, G.; Prencipe, V.; Calderone, D.; Zuccolo, C.; Cozzolino, P. Risk assessment for listeriosis in consumers of Parma and San Daniele hams. Food Control 2007, 18, 789–799. [Google Scholar] [CrossRef]
- Carpentier, B.; Cerf, O. Review—Persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 2011, 145, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Mena, C.; Almeida, G.; Carneiro, L.; Teixeira, P.; Hogg, T.; Gibbs, P. Incidence of Listeria monocytogenes in different food products commercialized in Portugal. Food Microbiol. 2004, 21, 213–216. [Google Scholar] [CrossRef]
- D’Amico, D.J.; Donnelly, C.W. Enhanced detection of Listeria spp. in farmstead cheese processing environments through dual primary enrichment, PCR, and molecular subtyping. J. Food Prot. 2008, 71, 2239–2248. [Google Scholar] [PubMed]
- Lundén, J.M.; Autio, T.J.; Korkeala, H.J. Transfer of persistent Listeria monocytogenes contamination between food processing plants associated with a dicing machine. J. Food Prot. 2002, 65, 1129–1133. [Google Scholar] [PubMed]
- Gounadaki, A.S.; Skandamis, P.N.; Drosinos, E.H.; Nychas, G.-J.E. Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiol. 2008, 25, 313–323. [Google Scholar] [CrossRef] [PubMed]
- Chevallier, I.; Ammor, S.; Laguet, A.; Labayle, S.; Castanet, V.; Dufour, E.; Talon, R. Microbial ecology of a small-scale facility producing traditional dry sausage. Food Control 2006, 17, 446–453. [Google Scholar] [CrossRef]
- Salvat, G.; Toquin, M.T.; Michel, Y.; Colin, P. Control of Listeria monocytogenes in the delicatessen industries: The lessons of a listeriosis outbreak in France. Int. J. Food Microbiol. 1995, 25, 75–81. [Google Scholar] [CrossRef]
- Lundén, J.M.; Autio, T.J.; Sjöberg, A.M.; Korkeala, H.J. Persistent and nonpersistent Listeria monocytogenes contamination in meat and poultry processing plants. J. Food Prot. 2003, 66, 2062–2069. [Google Scholar] [PubMed]
- FSAI (Food Safety Authority of Ireland). Establishing Baseline Data on the Presence of Listeria monocytogenes on Cooked Meat Slicers in Retail and Catering Premises; Monitoring and Surveillance Series; Microbiology: Dublin, Ireland, 2011; pp. 1–23. [Google Scholar]
- Ikeh, M.A.C.; Obi, S.K.C.; Ezeasor, D.N.; Ezenou, I.M.; Moneke, A.N. Incidence and pathogenicity profile of Listeria sp. isolated from food and environmental samples in Nsukka, Nigeria. Afr. J. Biotechnol. 2010, 9, 4776–4782. [Google Scholar]
- Lakićević, B.; Stjepanović, A.; Milijašević, M.; Terzićvidojević, A.; Golić, N.; Topisirović, L. The presence of Listeria spp. and Listeria monocytogenes in a chosen food processing establishment in Serbia. Arch. Biol. Sci. Belgrad. 2010, 62, 881–887. [Google Scholar] [CrossRef]
- Frank, J.F. Microbial attachment to food and food contact surfaces. Adv. Food Nutr. Res. 2001, 43, 320–370. [Google Scholar]
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Gómez, D.; Iguácel, L.P.; Rota, M.C.; Carramiñana, J.J.; Ariño, A.; Yangüela, J. Occurrence of Listeria monocytogenes in Ready-to-Eat Meat Products and Meat Processing Plants in Spain. Foods 2015, 4, 271-282. https://doi.org/10.3390/foods4030271
Gómez D, Iguácel LP, Rota MC, Carramiñana JJ, Ariño A, Yangüela J. Occurrence of Listeria monocytogenes in Ready-to-Eat Meat Products and Meat Processing Plants in Spain. Foods. 2015; 4(3):271-282. https://doi.org/10.3390/foods4030271
Chicago/Turabian StyleGómez, Diego, Laura Pilar Iguácel, Mª Carmen Rota, Juan José Carramiñana, Agustín Ariño, and Javier Yangüela. 2015. "Occurrence of Listeria monocytogenes in Ready-to-Eat Meat Products and Meat Processing Plants in Spain" Foods 4, no. 3: 271-282. https://doi.org/10.3390/foods4030271