Use of commercial protective cultures in portioned sheep milk cheeses to control Listeria monocytogenes

Submitted: 28 March 2022
Accepted: 29 October 2022
Published: 8 March 2023
Abstract Views: 1566
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The main objective of this study was to innovate soft and semi-cooked sheep milk cheese production processes with the use of a commercial protective culture able to control Listeria monocytogenes growth. A freeze-dried commercial culture of Lactobacillus plantarum was tested in DS cheese and PS cheese, two types of pasteurized sheep milk, raw-paste cheeses aged for no less than 20 and 30 days respectively. In the first step, in vitro tests were conducted to identify the most suitable matrix for the growth of L. plantarum in order to create a subculture that could be used at industrial cheese-making plants. During the second phase of the study, L. plantarum culture was introduced in the manufacturing process of the cheeses in a production plant. Finally, a challenge test was conducted on portioned DS and PS cheeses in order to evaluate the activity of the protective culture against L. monocytogenes: the cheeses were portioned, experimentally contaminated with L. monocytogenes strains, vacuum packed and stored at +4°C (correct storage conditions) and at +10°C (thermal abuse). Cheeses were analysed at the end of the shelf-life to evaluate the presence and growth of L. monocytogenes, to enumerate lactic acid bacteria and determine chemical-physical features. The results confirmed that protective cultures are a useful technological innovation to control L. monocytogenes growth during cheese storage without altering composition, microflora and chemical-physical characteristics of the product. However, the use of protective cultures should be applied as an integration of risk control measures and not as a substitute for preventive actions.

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Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G., Fiocco D, 2016. Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front Microbiol 7:464. DOI: https://doi.org/10.3389/fmicb.2016.00464
Bahramia A, Baboli ZM, Schimmel K, Jafari SM, Williams L, 2020. Efficiency of novel processing technologies for the control of Listeria monocytogenes in food products. Trends Food Sci Tech 96:61-78. DOI: https://doi.org/10.1016/j.tifs.2019.12.009
Benkerroum N, Ghouati Y, Ghalfi H, Elmejdoub T, Roblain D, Jacques P, Thonart P, 2002. Biocontrol of Listeria monocytogenes in a model cultured milk (Iben) by in situ bacteriocin production from Lactococcus lactis ssp. lactis. Int J Dairy Technol 55:145-51. DOI: https://doi.org/10.1046/j.1471-0307.2002.00053.x
Campagnollo F, Margalho L, Kamimura B, Feliciano M, Freire L, Lopes L, Alvarenga V, Cadavez V, Gonzales-Barron U, Schaffner D, Sant’Ana AS, 2018. Selection of indigenous lactic acid bacteria presenting anti-listerial activity, and their role in reducing the maturation period and assuring the safety of traditional Brazilian cheeses. Food Microbiol 73:288–97. DOI: https://doi.org/10.1016/j.fm.2018.02.006
Castellano P, Pérez Ibarreche M, Blanco Massani M, Fontana C, Vignolo G, 2017. Strategies for pathogen biocontrol using lactic acid bacteria and their metabolites: a focus on meat ecosystems and industrial environments. Microorganisms 5:38. DOI: https://doi.org/10.3390/microorganisms5030038
Coelho MC, Silva CCG, Ribeiro SC, Dapkevicius MLNE, Rosa HJD, 2014. Control of Listeria monocytogenes in fresh cheese using protective lactic acid bacteria. Int J Food Microbiol 191:53–9. DOI: https://doi.org/10.1016/j.ijfoodmicro.2014.08.029
Colagiorgi A, Bruini I, Di Ciccio PA, Zanardi E, Ghidini S, Ianieri A, 2017. Listeria monocytogenes biofilms in the wonderland of food industry. Pathogens 6:41. DOI: https://doi.org/10.3390/pathogens6030041
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 2012:376428. 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
EFSA, 2007. Introduction of a Qualified Presumption of Safety (QPS) approach for assessment of selected microorganisms referred to EFSA. EFSA J 587:1–16. DOI: https://doi.org/10.2903/j.efsa.2007.587
Falardeau J, Trmčić A, Wang S, 2021. The occurrence, growth, and biocontrol of Listeria monocytogenes in fresh and surface-ripened soft and semisoft cheeses. Compr Rev Food Sci Food Saf 20:4019–48. DOI: https://doi.org/10.1111/1541-4337.12768
Field D, Ross RP, Hill C, 2018. Developing bacteriocins of lactic acid bacteria into next generation biopreservatives. Curr Opin Food Sci 20:1–6. DOI: https://doi.org/10.1016/j.cofs.2018.02.004
García MJ, Ruíz F, Asurmendi P, Pascual L, Barberis L, 2020. Searching potential candidates for development of protective cultures: evaluation of two lactobacillus strains to reduce Listeria monocytogenes in artificially contaminated milk. J Food Saf 40:e12723. DOI: https://doi.org/10.1111/jfs.12723
Gobbetti M, De Angelis M, Di Cagno R, Mancini L, Fox PF, 2015. Pros and cons for using non-starter lactic acid bacteria (NSLAB) as secondary/adjunct starters for cheese ripening. Trends Food Sci Technol 45:167–78. DOI: https://doi.org/10.1016/j.tifs.2015.07.016
Gonzales-Barron U, Gonçalves-Tenório A, Rodrigues V, Cadavez V, 2017. Foodborne pathogens in raw milk and cheese of sheep and goat origin: A meta-analysis approach. Curr Opin Food Sci 18:7–13. https://doi.org/10.1016/j.cofs.2017.10.002. DOI: https://doi.org/10.1016/j.cofs.2017.10.002
Kaya HI, Ozel B, Simsek O, 2019. A natural way of food preservation: bacteriocins and their applications. in health and safety aspects of food processing technologies. Malik A, Erginkaya Z, Erten H (Eds). Berlin/Heidelberg, Germany: Springer; 633–59. DOI: https://doi.org/10.1007/978-3-030-24903-8_23
Leroy F., de Vuyst L, 2004. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67–78. DOI: https://doi.org/10.1016/j.tifs.2003.09.004
Martín I, Rodríguez A, Alía A, Martínez-Blanco M, Lozano-Ojalvo D, Córdoba JJ, 2022. Control of Listeria monocytogenes growth and virulence in a traditional soft cheese model system based on lactic acid bacteria and a whey protein hydrolysate with antimicrobial activity. Int J Food Microbiol 361:109444. DOI: https://doi.org/10.1016/j.ijfoodmicro.2021.109444
Martínez RCR, Wachsman M, Torres NI, LeBlanc JG, Todorov SD, Franco BDGM, 2013. Biochemical, antimicrobial and molecular characterization of a noncytotoxic bacteriocin produced by Lactobacillus plantarum ST71KS. Food Microbiol 34:376–81. DOI: https://doi.org/10.1016/j.fm.2013.01.011
Melo J, Andrew PW, Faleiro ML, 2015. Listeria monocytogenes in cheese and the dairy environment remains a Food Safety Challenge: the role of stress responses. Int Food Res J 67:75–90. DOI: https://doi.org/10.1016/j.foodres.2014.10.031
Mills S, Serrano L, Griffin C, O’Connor PM, Schaad G, Bruining C, Hill C, Ross P, Meijer WC, 2011. Inhibitory activity of Lactobacillus plantarum LMG P-26358 against Listeria innocua when used as an adjunct starter in the manufacture of cheese. Microb Cell Fact 10:S7. DOI: https://doi.org/10.1186/1475-2859-10-S1-S7
Muñoz A, Ananou S, Gálvez A, Martínez-Bueno M, Rodríguez A, Maqueda M, 2007. Inhibition of Staphylococcus aureus in dairy products by enterocin AS-48 produced in situ and ex situ: bactericidal synergism with heat. Int Dairy J 17:760–9. DOI: https://doi.org/10.1016/j.idairyj.2006.09.006
Oneca M, Irigoyen A, Ortigosa, M, Torre P, 2003. PCR and RAPD identification of L. plantarum strains isolated from ovine milk and cheese. Geographical distribution of strains. FEMS Microbiol Lett 227:271-7. DOI: https://doi.org/10.1016/S0378-1097(03)00691-8
Pala C, Scarano C, Venusti M, Sardo D, Casti D, Cossu F, Lamon S, Spanu V, Ibba M, Marras M, Paba A, Spanu C, De Santis EPL, 2016. Shelf life evaluation of Ricotta Fresca sheep cheese in modified atmosphere packaging. Ital J Food Saf 5:5502. DOI: https://doi.org/10.4081/ijfs.2016.5502
Panebianco F, Giarratana F, Caridi A, Sidari R, De Bruno A, Giuffrida A, 2021. Lactic acid bacteria isolated from traditional Italian dairy products: activity against Listeria monocytogenes and modelling of microbial competition in soft cheese. LWT 137:110446. DOI: https://doi.org/10.1016/j.lwt.2020.110446
Rodríguez E, Calzada J, Arqués JL, Rodríguez JM, Nuñez M, Medina M, 2005. Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese. Int Dairy J 15:51–7. DOI: https://doi.org/10.1016/j.idairyj.2004.05.004
Scatassa ML, Gaglio R, Cardamone C, Macaluso G, Arcuri L, Todaro M, Mancuso I, 2017. Anti-Listeria activity of lactic acid bacteria in two traditional Sicilian cheeses. Ital J Food Saf 6:6191. DOI: https://doi.org/10.4081/ijfs.2017.6191
Silva CCG, Silva SPM, Ribeiro SC, 2018. Application of bacteriocins and protective cultures in dairy food preservation. Front Microbiol 9:594. DOI: https://doi.org/10.3389/fmicb.2018.00594
Sorrentino E, Reale A, Tremonte P, Maiuro L, Succi M, Tipaldi L, Di Renzo T, Pannella G, Coppola R, 2013. Lactobacillus plantarum inhibits Penicillium spp.. involved in the spoilage of black truffles (Tuber aestivum). J Food Sci 78:M1188-94. DOI: https://doi.org/10.1111/1750-3841.12171
Todd ECD, Notermans S, 2011. Surveillance of listeriosis and its causative pathogen, Listeria monocytogenes. Food Control 22:1484–90. DOI: https://doi.org/10.1016/j.foodcont.2010.07.021
Wiedmann M, Sauders B, 2007. Ecology of Listeria species and L. monocytogenes in the natural environment. In: Ryser ET, Marth EH (eds). Listeria, listeriosis, and food safety. 3rd ed. Boca Raton, FL: CRC Press. pp. 21–53. DOI: https://doi.org/10.1201/9781420015188.ch2
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. Sawston, UK: Woodhead Publishing. DOI: https://doi.org/10.1533/9780857092540.1.132

Supporting Agencies

FAR 2019 Scarano

How to Cite

1.
Sanna R, Piras F, Siddi G, Meloni MP, Demontis M, Spanu V, Nieddu G, Cuccu M, De Santis EPL, Scarano C. Use of commercial protective cultures in portioned sheep milk cheeses to control <em>Listeria monocytogenes</em>. Ital J Food Safety [Internet]. 2023 Mar. 8 [cited 2024 Nov. 21];12(1). Available from: https://www.pagepressjournals.org/ijfs/article/view/10484