Behavior of Listeria innocua during the manufacturing and pit-ripening of Formaggio di Fossa di Sogliano PDO cheese

Submitted: 10 September 2019
Accepted: 10 February 2020
Published: 19 August 2020
Abstract Views: 657
PDF: 396
HTML: 44
Publisher's note
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.

Authors

Formaggio di Fossa di Sogliano is a traditional Italian Protected Designation of Origin (PDO) cheese ripened for a minimum of 5 months, with the feature of a ripening of at least 80 to at most 100 days in pits, digged into tuffaceous rocks according to medieval tradition of Italy. In this study, a challenge test using Listeria innocua as a surrogate of Listeria monocytogenes was performed, with the aim of increasing knowledge concerning the impact of the Fossa cheese process, and especially of the traditional ripening process of this PDO, on the behaviour of L. monocytogenes. Pasteurized milk was experimentally inoculated with 4.5 log CFU/mL cocktail by three L. innocua strains, and L. innocua and Mesophilic Lactic Acid Bacteria (LAB) counts as well as the evolution of temperatures, pH and aw values were monitored throughout the manufacturing and ripening processes. Throughout the ripening in maturation room a constant temperature of 8°C was observed reaching a temperature between 10 and 15.5°C during ripening into pit. In the final products data for LAB concentration, pH and aw values were roughly in accordance with literature, even if some differences were, probably due to variability of artisanal cheese productions. The numbers of L. innocua showed a slight decrease but remained stable until the end of ripening in maturation room, whereas a significant reduction of the microorganism was observed in the final product, at the end of the ripening into the pit. The findings give scientific evidence that the process of this PDO prevented the L. innocua growth, allowing us to speculate a similar behaviour of L. monocytogenes. Based on this study, the recommendation to extend as much as possible the ripening into pit (from 80 to 100 days) was provided to food business operators as a risk mitigation strategy to be implemented.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Aspridou Z, Moschakis T, Biliaderis CG, Koutsoumanis KP, 2014. Effect of the substrate’s microstructure on the growth of Listeria monocytogenes. Food Res Int 64: 683-691. https://doi.org/10.1016/j.foodres.2014.07.031. DOI: https://doi.org/10.1016/j.foodres.2014.07.031
Avellini P, Clementi F, Trabalza Marinucci M, Cenci Goga B, Rea S, Branciari R, Cavallucci C, Reali C, Di Antonio E, 1999). Pit cheese: compositional, microbiological and sensory characteristics. Ital J Food Sci 11: 317e333
Barbieri E, Schiavano GF, De Santi M, Vallorani L, Casadei L, Guescini M, Gioacchini AM, Rinaldi L, Stocchi V, Brandi G, 2012. Bacterial diversity of traditional Fossa (pit) cheese and its ripening environment. Int Dairy J 23:62-67. https://doi.org/10.1016/j.idairyj.2011.09.009. DOI: https://doi.org/10.1016/j.idairyj.2011.09.009
Commission Regulation (EC) No. 1183/2009 of 30 November 2009 entering a name in the register of protected designations of origin and protected geographical indications (Formaggio di Fossa di Sogliano (PDO). Official J European Union L 317, 3.12.2009, 34-35. In E. Union (Ed.), 853/2004. http://data.europa.eu/eli/reg/2009/1183/oj. Brussels, Belgium: The European parliament and the council of the European Union.
Commission Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs. In European Union (Ed.), 2073/2005. Brussels, Belgium: The European parliament and the council of the European Union
CLAL S.r.l. 2019. Available at: https://www.clal.it/en/ Accessed 05 September 2019.
Dalzini E, Cosciani-Cunico E, Bernini V, Bertasi B, Losio MN, Daminelli P, Varisco G, 2015. Behaviour of Escherichia coli O157 (VTEC), Salmonella Typhimurium and Listeria monocytogenes during the manufacture, ripening and shelf life of low fat salami. Food Control 47:306-311. https://doi.org/10.1016/j.idairyj.2010.02.004.
De Santi M, Sisti M, Barbieri E, Piccoli G, Brandi G, Stocchi V, 2010. A combined morphologic and molecular approach for characterizing fungal microflora from a traditional Italian cheese (Fossa cheese). Int Dairy J 20:465-471. doi: 10.1016/j.idairyj.2010.02.004. DOI: https://doi.org/10.1016/j.idairyj.2010.02.004
EFSA, 2018. Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA Journal, 16(1), 5134. European Food Safety Authority. https://doi.org/10.2903/j.efsa.2018.5134. DOI: https://doi.org/10.2903/j.efsa.2018.5134
Fontana C, Cappa F, Rebecchi A, Cocconcelli PS, 2010. Surface microbiota analysis of Taleggio, Gorgonzola, Casera, Scimudin and Formaggio di Fossa Italian cheeses. Int J Food Microbiol 138:205-211. https://doi.org/10.1016/j.ijfoodmicro.2010.01.017. DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.01.017
Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, Berche P, Bloecker H, Brandt P, Chakraborty T, Charbit A, Chetouani F, Couve E, de Daruvar A, Dehoux P, Domann E, Dominguez-Bernal G, Duchaud E, Durant L, Dussurget O, Entian KD, Fsihi H, Garcia-Del Portillo F, Garrido P, Gautier L, Goebel W, Gomez-Lopez N, Hain T, Hauf J, Jackson D, Jones LM, Kaerst U, Kreft J, Kuhn M, Kunst F, Kurapkat G, Madueno E, Maitournam A, Vicente JM, Ng E, Nedjari H, Nordsiek G, Novella S, de Pablos B, Perez-Diaz JC, Purcell R. Remmel B, Rose M, Schlueter T, Simoes N, Tierrez A, Vazquez-Boland JA, Voss H, Wehland J, Cossart P, 2001. Comparative genomics of Listeria species. Science 294:849-852. https://doi.org/ 10.1126/science.1063447.
Gobbetti M, Folkertsma B, Fox PF, Corsetti A, Smacchi E, De Angelis V, Rossi J, Kilcawley J, Cortini M, 1999. Microbiology and biochemistry of Fossa (pit) cheese. Int Dairy J 9:763-773. https://doi.org/10.1016/S0958-6946(99)00147-8. DOI: https://doi.org/10.1016/S0958-6946(99)00147-8
ISO, 1998. International Organizational for Standardization. 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 15214:1998. International Organization for Standardization, Geneva.
ISO, 1999. Microbiology of food and animal feeding stuffs - 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 6887-1:1999. International Organization for Standardization, Geneva.
ISO, 2004. Microbiology of food and animal feeding stuffs - Horizontal method for the detection and enumeration of Listeria monocytogenes - Part 1: Detection method. ISO 11290-1:1996/Amd 1:2004. International Organization for Standardization, Geneva.
ISO, 2007. Microbiology of food and animal feeding stuffs - General requirements and guidance for microbiological examinations. ISO 7218:2007. International Organization for Standardization, Geneva.
ISO, 2010. Microbiology of food and animal feeding stuffs - Preparation of test samples, initial suspension and decimal dilutions for microbiological examination - Part 5: Specific rules for the preparation of milk and milk products. ISO 6887-5:2010. International Organization for Standardization, Geneva.
ISO, 2004. Microbiology of food and animal feeding stuffs. Determination of Water Activity. ISO/FDIS 21807:2004. International Organization for Standardization, Geneva.
ISO, 2009. Microbiology of food and animal feeding stuffs - Guidelines on preparation and production of culture media - Part 1: General guidelines on quality assurance for the preparation of culture media in the laboratory. ISO/TS 11133-1: 2009. International Organization for Standardization, Geneva.
ISO, 2011. Microbiology of food and animal feeding stuffs – Guidelines on preparation and production of culture media – Part 2: Practical guidelines on performance testing of culture media. ISO/TS 11133-2: (2011). International Organization for Standardization, Geneva.
Izquierdo E, Marchioni E, Aoude-Werner D, Hasselmann C, Ennahar S, 2009. Smearing of soft cheese with Enterococcus faecium WHE 81, a multi-bacteriocin producer, against Listeria monocytogenes. Food Microbiol. 26:16-20 DOI: https://doi.org/10.1016/j.fm.2008.08.002
Lahou E, Uyttendaele M, 2017. Growth potential of Listeria monocytogenes in soft, semi-soft and semi-hard artisanal cheeses after post-processing contamination in deli retail establishments. Food Control 76:13-23. https://doi.org/10.1016/j.foodcont.2016.12.033. DOI: https://doi.org/10.1016/j.foodcont.2016.12.033
Lardeux AL, Guillier L, Brasseur E, Doux C, Gautier J, Gnanou-Besse N, 2015. Impact of the contamination level and the background flora on the growth of Listeria monocytogenes in ready-to-eat diced poultry. Lett. Appl. Microbiol. 60:481-490. https://doi.org/10.1111/lam.12395. DOI: https://doi.org/10.1111/lam.12395
Lomonaco S, Decastelli L, Nucera D, Gallina S, Manila Bianchi D, Civera T, 2009. Listeria monocytogenes in Gorgonzola: subtypes, diversity and persistence over time. Int J Food Microbiol 15:516-520. https://doi.org/10.1016/j.ijfoodmicro.2008.
Mascaro N, Stocchi R, Ricciutelli M, Cammertoni N, Renzi F, Cecchini S, Loschi AR, Rea S, 2010. Biogenic amine content and chemical and physical features of italian Formaggio di Fossa. Rivista dell’Associazione Italiana Veterinari Igienisti, 8, 49-52. https://doi.org/10.4081/ijfs.2010.1037.
Mellefont L, McMeekin T, Ross T, 2008. Effect of relative inoculum concentration on Listeria monocytogenes growth in co-culture. Int. J. Food Microbiol. 121:157-168. https://doi.org/10.1016/j.ijfoodmicro.2007.10.010 DOI: https://doi.org/10.1016/j.ijfoodmicro.2007.10.010
MIPAAF, 2019. Specification of Formaggio di Fossa di Sogliano. Ministero delle Politiche Agricole e forestali. https://www.politicheagricole.it/flex/cm/pages/ServeBLOB.php/L/IT/IDPagina/3340. Accessed 05 September 2019.
NACMCF, 2010. Parameters for determining inoculated pack/challenge study protocols. J Food Protect 73(1):140-202. https://doi.org/10.4315/0362-028X-73.1.140. DOI: https://doi.org/10.4315/0362-028X-73.1.140
O’Bryan CA, Crandall PG, Martin EM, Griffis CL, Johnson MG, 2006. Heat resistance of Salmonella spp., Listeria monocytogenes, Escherichia coli O157:H7, and Listeria innocua M1, a potential surrogate for Listeria monocytogenes, in meat and poultry: A review. J Food Science 71:R23-R30. https://doi.org/10.1111/j.1365-2621.2006.tb15639.x. DOI: https://doi.org/10.1111/j.1365-2621.2006.tb15639.x
Pirisi A, Comuniana R, Urgegheb PP, Scintua MF, 2011. Sheep’s and goat’s dairy products in Italy: Technological, chemical, microbiological, and sensory aspects. Small Ruminan Res 101:102-112. https://doi.org/10.1016/j.smallrumres.2011.09.030. DOI: https://doi.org/10.1016/j.smallrumres.2011.09.030
Schvartzman MS, Maffre A, Tenenhaus-Aziza F, Sanaa M, Butler F, Jordan K, 2011. Modelling the fate of Listeria monocytogenes during manufacture and ripening of smeared cheese made with pasteurised or raw milk. Int J Food Microbiol 145:31-38. https://doi.org/10.1016/j.ijfoodmicro.2010.11.032 DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.11.032
Toppino PM, Drava G, Contarini G, Manfredini M, Emandi GC, 1992. Caratteristiche di tipicità del “formaggio di fossa”. Rivista della Società Italiana di Scienza dell’Alimentazione 4:389-414. http://hdl.handle.net/11567/286659.
Valero A, Hernandez M, De Cesare A, Manfreda G, González-García P, Rodríguez-Lázaro D, 2014. Survival kinetics of Listeria monocytogenes on raw sheep milk cured cheese under different storage temperatures. Int J Food Microbiol 184:39-44. https://doi.org/10.1016/j.ijfoodmicro.2014.02.017. DOI: https://doi.org/10.1016/j.ijfoodmicro.2014.02.017
van Asselt ED, van der Fels-Klerx HJ, Marvin HJP, van Bokhorst-van de Veen H, Nierop Groot M, 2017. Overview of food safety hazards in the european dairy supply chain. Compr Rev Food Sci Food Saf 16: 59-75 https://doi.org/10.1111/1541-4337.12245. DOI: https://doi.org/10.1111/1541-4337.12245

How to Cite

1.
Giacometti F, Daminelli P, Fiorentini L, Cosciani-Cunico E, Monastero P, Dalzini E, Losio MN, Dell’Orfano G, Rossini R, Piva S, Serraino A. Behavior of <em>Listeria innocua</em> during the manufacturing and pit-ripening of Formaggio di Fossa di Sogliano PDO cheese. Ital J Food Safety [Internet]. 2020 Aug. 19 [cited 2024 Nov. 23];9(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/8552