Selection of commercial protective cultures to be added in Sardinian fermented sausage to control Listeria monocytogenes
https://doi.org/10.4081/ijfs.2022.10368
Accepted: 2 March 2022
HTML: 10
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Sardinian fermented sausage “Salsiccia Sarda” is a Mediterranean-style, semi-dry, fermented, RTE product, representing the main pork meat product in Sardinia (Italy). The high variability that characterizes the technological processes applied in different production plants results in sausages with different chemico-physical features sometimes permissive for the growth of Listeria monocytogenes. In order to guarantee the hygienic-sanitary quality of the final product and to innovate the manufacturing process, the main objective of this study was to evaluate the use of different commercial protective cultures to control L. monocytogenes growth in the Sardinian fermented sausage. In the first step, in vitro tests were carried out to evaluate the effectiveness of five freeze-dried bioprotective cultures availabe on the market in limiting the growth of L. monocytogenes. The two protective cultures that showed the best in vitro results were selected for a challenge test on artificially contaminated Sardinian fermented sausages. Moreover, the protective culture that showed the best results in inhibiting the growth of L. monocytogenes according to in vitro and challenge test experiments, was included into real production settings and validated in three producing plants. As a result, it was observed that protective cultures represent an important technological innovation for the Sardinian fermented sausage processing plants as they allow to control L. monocytogenes growth without altering the composition, the microflora and the chemical-physical characteristics of the product, thus ensuring safety and quality. Protective cultures also showed to reduce Enterobacteriaceae mean levels at the end of ripening and not to affect the natural concentration of lactic acid bacteria and coagulase-negative staphylococci.
ANSES, 2021. EURL Lm Technical guidance document on challenge tests and durability studies for assessing shelf-life of ready-to-eat foods related to L. monocytogenes, version 4 of 1 July 2021.
Autio T, Sateri T, Fredriksson-Ahomaa M, Rahkio M, Lunden J, Korkeala H, 2000. Listeria monocytogenes contamination pattern in pig slaughterhouses. J Food Prot 63:1438-42. DOI: https://doi.org/10.4315/0362-028X-63.10.1438
Blanco-Lizarazao CM, Sotelo-Dìaz I, Llorente-Bosquetes A, 2016. In vitro modelling of simultaneous interactions of Listeria monocytogenes, Lactobacillus sakei, and Staphylococcus carnosus. Food Sci Biotechnol 25:341-8. DOI: https://doi.org/10.1007/s10068-016-0048-0
Boscher E, Houard E, Denis M, 2012. Prevalence and Distribution of Listeria monocytogenes Serotypes and Pulsotypes in Sows and Fattening Pigs in Farrow-to-Finish Farms. J Food Prot 75:889–95. DOI: https://doi.org/10.4315/0362-028X.JFP-11-340
Chasseignaux E, Gerault P, Toquin M, Salvat G, Colin P, Ermel G, 2002. Ecology of Listeria monocytogenes in the environment of raw poultry meat and raw pork meat processing plants. FEMS Microbiol Lett 210:271-5. DOI: https://doi.org/10.1111/j.1574-6968.2002.tb11192.x
Cosentino S, Fadda ME, Deplano M, Melis R, Pomata R, Pisano MB, 2012. Antilisterial activity of nisin-like bacteriocin-producing Lactococcus lactis subsp. lactis isolated from fermented Sardinian dairy products. J Biomed Biotechnol 2012, ID 376428 doi:10.1155/2012/376428 DOI: https://doi.org/10.1155/2012/376428
Davidson PM, Techathuvanan C, 2015. The use of natural antimicrobials in food, chapter in: Taylor TM, Handbook of natural antimicrobials for food safety and quality, Woodhead Publishing, 2015. DOI: https://doi.org/10.1016/B978-1-78242-034-7.00001-3
European Food Safety Authority and European Centre for Disease Prevention and Control, 2021. The European Union One Health 2020 Zoonoses Report. EFSA J 19:6971. DOI: https://doi.org/10.2903/j.efsa.2021.6971
European Food Safety Authority, 2018. Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J 16:5134
Esteban JI, Oporto B, Aduriz G, Juste RA, Hurtado A, 2009. Fecal shedding and strain diversity of Listeria monocytogenes in healthy ruminants and swine in northern Spain. BMC Vet Res 2009;5:2. DOI: https://doi.org/10.1186/1746-6148-5-2
European Commission (EC). Commission regulation (EC) no 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. In: Off. J. Eur. Union 2005, L 338/1, 22/12/2005.
European Commission, 2008. Regulation (EC) no 1333/2008 of the European Parliament and of the council of 16 December 2008 on food additives. In: Official Journal, L 354/16, 31/12/2008.
Fosse J, Seegers H, Magras C, 2009. Prevalence and Risk Factors for Bacterial Food‐Borne Zoonotic Hazards in Slaughter Pigs: A Review. Zoon Publ Health 56:429–54. DOI: https://doi.org/10.1111/j.1863-2378.2008.01185.x
Greco M, Mazzette R, De Santis EPL, Corona A, Cosseddu AM, 2005. Evolution and identification of lactic acid bacteria isolated during the ripening of Sardinian sausages. Meat Sci 69:733–9. DOI: https://doi.org/10.1016/j.meatsci.2004.11.004
Hugas M, Garriga M, Aymerich MT, Monfort JM, 1995, Inibition of Listeria in dry fermented sausages by the bacteriocinogenic Lactobacillus sakei CTC494. J Appl Microbiol 75:322-30. DOI: https://doi.org/10.1111/j.1365-2672.1995.tb03144.x
ISO, 1992. Microbiology of food and animal feeding stuffs — Horizontal method for the enumeration of mesophilic lactic acid bacteria — Colony-count technique at 30 degrees C. ISO Norm 15214:1998. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain - Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. - Part 1: Detection method. ISO Norm 11290-1:2017. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain - Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. - Enumeration method. ISO Norm 11290-2:2017. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain - Preparation of test samples, initial suspension and decimal dilutions for microbiological examination - Part 1: General rules for the preparation of the initial suspension and decimal dilutions. ISO Norm 6887:2017. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2017. Microbiology of the food chain - Horizontal method for the detection and enumeration of Enterobacteriaceae - Part 2: Colony-count technique. ISO Norm 21528:2017. International Standardization Organization ed., Geneva, Switzerland.
ISO, 2020. Microbiology of the food chain - Horizontal method for the detection, enumeration and serotyping of Salmonella - Part 1: Detection of Salmonella spp. ISO Norm 6579-1:2020. International Standardization Organization ed., Geneva, Switzerland.
Italian Republic, 2020. Aggiornamento dell’Elenco nazionale dei prodotti agroalimentari tradizionali ai sensi del Decreto Ministeriale 8 settembre 1999, n.350. Regolamento recante norme per l'individuazione dei prodotti tradizionali di cui all'articolo 8, comma 1, del decreto legislativo 30 aprile 1998, n. 173. Prot. Uscita N.0001375 del 10/02/2020
Janssens M, Myter N, De Vuyst L, Leroy F, 2013. Community dynamics of coagulase-negative staphylococci during spontaneous artisan-type meat fermentations differ between smoking and moulding treatments. Int J Food Microbiol 166:168-75. DOI: https://doi.org/10.1016/j.ijfoodmicro.2013.06.034
Kanuganti SR, Wesley IV, Reddy PG, McKean J, Hurd HS, 2002. Detection of Listeria monocytogenes in pigs and pork. J Food Prot 65:1470–4. DOI: https://doi.org/10.4315/0362-028X-65.9.1470
Leroy F, De Vuyst L, 2005. Simulation of the effect of sausage ingredients and technology on the functionality of the bacteriocin-producing Lactobacillus sakei CTC 494 strain. Int J Food Microbiol 100:141-52. DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.10.011
Ryu J, Park SH, Yeom YS, Shrivastav A, Lee SH, Kim YR, Kim HY, 2013. Simultaneous detection of Listeria species isolates from meat processed foods using multiplex PCR. Food Control 32:659-64. DOI: https://doi.org/10.1016/j.foodcont.2013.01.048
Mangia NP, Murgia MA, Garau G, Deiana P, 2007. Microbiologia e valutazione igienico-sanitaria della salsiccia sarda. Ind Aliment Italy 46:533-6.
Maragkoudakis PA, Mountzouris KC, Psyrras D, Cremonese S, Fischer J, Cantor MD, Tsakalidou E, 2009. Functional properties of novel protective lactic acid bacteria and application in raw chicken meat against Listeria monocytogenes and Salmonella enteritidis. Int J Food Microbiol 130:219-26. DOI: https://doi.org/10.1016/j.ijfoodmicro.2009.01.027
Martìn I, Rodrìgez A, Sànchez-Montero L, Padilla P, Còrdoba JJ, 2021. Effect of the Dry-Cured Fermented Sausage "Salchichón" Processing with a Selected Lactobacillus sakei in Listeria monocytogenes and Microbial Population. Foods 10:856. DOI: https://doi.org/10.3390/foods10040856
Mataragas M, Rantsioua K, Alessandria V, Cocolin L, 2015. Estimating the non-thermal inactivation of Listeria monocytogenes in fermented sausages relative to temperature, pH and water activity. Meat Sci 100:171-8. DOI: https://doi.org/10.1016/j.meatsci.2014.10.016
Meloni D, 2015. Presence of Listeria monocytogenes in Mediterranean-Style Dry Fermented Sausages. Foods 4:34-50. DOI: https://doi.org/10.3390/foods4010034
Meloni D, Consolati SG, Mazza R, Mureddu A, Fois F, Piras F, Mazzette R, 2014. Presence and molecular charachterization of the major serovars of Listeria monocytogenes in ten Sardinian fermented sausage processing plants. Meat Sci 97:443-50. DOI: https://doi.org/10.1016/j.meatsci.2014.02.012
Meloni D, Piras F, Mureddu A, Fois F, Consolati SG, Lamon S, Mazzette R, 2013. Listeria monocytogenes in five Sardinian swine slaughterhouses: Prevalence, Serotype and Genotype Characterization. J Food Prot 76:1863–7. DOI: https://doi.org/10.4315/0362-028X.JFP-12-505
Mureddu A, Mazza R, Fois F, Meloni D, Bacciu R, Piras F, Mazzette R, 2014. Listeria monocytogenes persistence in ready-to-eat sausages and in processing plants. Ital J Food Saf 3:12–5. DOI: https://doi.org/10.4081/ijfs.2014.1697
Neri D, Antoci S, Iannetti L, Ciorba AB, D'Aurelio R, Del Matto I, Di Leonardo M, Giovannini A, Prencipe VA, Pomilio F, Santarellia GA, Miglioratia G, 2019. EU and US control measures on Listeria monocytogenes and Salmonella spp. in certain ready-to-eat meat products: An equivalence study. Food Control 96:98-103. DOI: https://doi.org/10.1016/j.foodcont.2018.09.001
Nielsen JW, Dickson JS, Crouse JD, 1990. Use of a bacteriocin produced by Pediococcus acidilactici to inhibit Listeria monocytogenes associated with fresh meat. Appl Environ Microbiol 56:2142-5. DOI: https://doi.org/10.1128/aem.56.7.2142-2145.1990
Nieto-Lozano JC, Reguera JI, Peláez-Martínezb MC, Hardisson de la Torre A, 2006. Effect of a bacteriocin produced by Pediococcus acidilactici against Listeria monocytogenes and Clostridium perfringens on Spanish raw meat. Meat Sci 72:57-61. DOI: https://doi.org/10.1016/j.meatsci.2005.06.004
Peccio A, Auto T, Korkeala R, Rosmini R, Trevisani M, 2003. Listeria monocytogenes occurrence and characterization in meat-producing plants. Lett Appl Microbiol 37:234-8. DOI: https://doi.org/10.1046/j.1472-765X.2003.01384.x
Pedonese F, Torracca B, Mancini S, Pisano S, Turchi B, Cerri D, Nuvoloni R, 2020. Effect of a Lactobacillus sakei and Staphylococcus xylosus protective culture on Listeria monocytogenes growth and quality traits of Italian fresh sausage (salsiccia) stored at abusive temperature. Ital J Anim Sci 19:1363–74. DOI: https://doi.org/10.1080/1828051X.2020.1844084
Piras F, Spanu C, Mocci AM, Demontis M, De Santis EPL, Scarano C, 2019. Occurrence and traceability of Salmonella spp. in five Sardinian fermented sausage facilities. Ital J Food Saf 8:8011. DOI: https://doi.org/10.4081/ijfs.2019.8011
Thévenot D, Delignette-Muller ML, Christieans S, Vernozy-Rozand C, 2005. Fate of Listeria monocytogenes in experimentally contaminated French sausages. Int J Food Microbiol 101:189–200. DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.11.006
Thévenot D, Dernburg A, Vernozy-Rozand C, 2006. An updated review of Listeria monocytogenes in the pork meat industry and its products. J Appl Microbiol 101:7-17. DOI: https://doi.org/10.1111/j.1365-2672.2006.02962.x
Tjener K, Stahnke LH, Andersen L, Martinussen J, 2004. The pH-unrelated influence of salt, temperature and manganese on aroma formation by Staphylococcus xylosus and Staphylococcus carnosus in a fermented meat model system. Int J Food Microbiol 97:31-42. DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.04.007
Young NWG, O'Sullivan GR, 2011. The influence of ingredients on products stability and shelf life. In: Kilcast D, Subramaniam P. Food and Beverage Stability and Shelf Life, Woodhead Publishing, 2011. DOI: https://doi.org/10.1533/9780857092540.1.132
Zagorec M, Champomier-Vergès MC, 2017. Lactobacillus sakei: A Starter for sausage fermentation, a protective culture for meat products. Microorganisms 5:56. DOI: https://doi.org/10.3390/microorganisms5030056
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
Downloads
Citations
