[en] This study assessed the bioprotective effect of Carnobacterium maltaromaticum (CM) against Pseudomonas fluorescens (PF) and Brochothrix thermosphacta (BT) in ground beef and sliced cooked ham stored in high- and low-oxygen-modified atmospheres (66/4/30% O2/N2/CO2 and 70/30% N2/CO2, respectively). Both meat products were inoculated with CM, PF, and BT individually or in combination and stored for 7 days (3 days at 4 °C + 4 days at 8 °C) for ground beef and 28 days (10 days at 4 °C + 18 days at 8 °C) for sliced cooked ham. Each food matrix was assigned to 6 treatments: NC (no bacterial inoculation, representing the indigenous bacteria of meat), CM, BT, PF, CM + BT, and CM + PF. Bacterial growth, pH, instrumental color, and headspace gas composition were assessed during storage. CM counts remained stable from inoculation and throughout the shelf-life. CM reduced the population of inoculated and indigenous spoilage bacteria, including BT, PF, and enterobacteria, and showed a negligible impact on the physicochemical quality parameters of the products. Furthermore, upon simulating the shelf-life of ground beef and cooked ham, a remarkable extension could be observed with CM. Therefore, CM could be exploited as a biopreservative in meat products to enhance quality and shelf-life.
Research Center/Unit :
FARAH. Santé publique vétérinaire - ULiège
Disciplines :
Food science
Author, co-author :
de Andrade Cavalari, Caroline Maria; Laboratory of Agrifood Food Research and Inovation (LAPIAgro), Graduate Program in Animal Science, School of Life Sciences, Pontifícia Universidade Católica do Paraná, Imaculada Conceição, 1155, Curitiba 80215-901, Brazil, Laboratory of Food Technology, Faculty of Veterinary Medicine & Fundamental and Applied Research for Animal and Health (FARAH) Research Unit, Université de Liège, Avenue de Cureghem 10, Liège 4000, Belgium
Imazaki, Pedro Henrique; INTHERES, Université de Toulouse, INRAE, ENVT, 23 Chemin des Capelles, Toulouse 31300, France, Laboratory of Food Technology, Faculty of Veterinary Medicine & Fundamental and Applied Research for Animal and Health (FARAH) Research Unit, Université de Liège, Avenue de Cureghem 10, Liège 4000, Belgium
Pirard, Barbara ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH) > FARAH: Santé publique vétérinaire
Lebrun, Sarah ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA)
Gemmi, Céline ; Université de Liège - ULiège > GIGA > GIGA I3 - Cellular and Molecular Immunology
Antoine, Céline ; Université de Liège - ULiège > Fundamental and Applied Research for Animals and Health (FARAH)
Crevecoeur, Sébastien ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Clinquart, Antoine ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Technologie des denrées alimentaires
de Macedo, Renata Ernlund Freitas; Laboratory of Agrifood Food Research and Inovation (LAPIAgro), Graduate Program in Animal Science, School of Life Sciences, Pontifícia Universidade Católica do Paraná, Imaculada Conceição, 1155, Curitiba 80215-901, Brazil. Electronic address: renata.macedo@pucpr.br
Language :
English
Title :
Carnobacterium maltaromaticum as bioprotective culture against spoilage bacteria in ground meat and cooked ham.
AFNOR, Hygiène et sécurité des produits alimentaires—Lignes directrices pour l'élaboration d'un protocole de test de vieillissement pour la validation de la durée de vie microbiologique—Denrées périssables, réfrigérées. La Plaine Saint-Denis: Association Française de Normalisation., 01–003, 2004.
Arnau, J., Guerrero, L., Casademont, G., Gou, P., Physical and chemical changes in different zones of normal and PSE dry cured ham during processing. Food Chemistry 52:1 (1995), 63–69, 10.1016/0308-8146(94)P4182-F.
Barcenilla, C., Ducic, M., López, M., Prieto, M., Álvarez-Ordóñez, A., Application of lactic acid bacteria for the biopreservation of meat products: A systematic review. Meat Science, 183, 2022, 108661, 10.1016/J.MEATSCI.2021.108661.
Bredholt, S., Nesbakken, T., Holck, A., Industrial application of an antilisterial strain of lactobacillus sakei as a protective culture and its effect on the sensory acceptability of cooked, sliced, vacuum-packaged meats. International Journal of Food Microbiology 66:3 (2001), 191–196, 10.1016/S0168-1605(00)00519-5.
Brillet, A., Pilet, M.F., Prevost, H., Cardinal, M., Leroi, F., Effect of inoculation of Carnobacterium divergens V41, a biopreservative strain against listeria monocytogenes risk, on the microbiological, chemical and sensory quality of cold-smoked salmon. International Journal of Food Microbiology 104:3 (2005), 309–324, 10.1016/j.ijfoodmicro.2005.03.012.
Brillet-Viel, A., Pilet, M.-F., Courcoux, P., Prévost, H., Leroi, F., Optimization of growth and bacteriocin activity of the food bioprotective Carnobacterium divergens V41 in an animal origin protein free medium. Frontiers in Marine Science, 3(AUG), 2016, 128, 10.3389/fmars.2016.00128.
Casaburi, A., Nasi, A., Ferrocino, I., Di Monaco, R., Mauriello, G., Villani, F., Ercolini, D., Spoilage-related activity of Carnobacterium maltaromaticum strains in air-stored and vacuum-packed meat. Applied and Environmental Microbiology 77:20 (2011), 7382–7393, 10.1128/AEM.05304-11.
Casaburi, A., Piombino, P., Nychas, G.J., Villani, F., Ercolini, D., Bacterial populations and the volatilome associated to meat spoilage. Food Microbiology 45:PA (2015), 83–102, 10.1016/j.fm.2014.02.002.
Castellano, P., González, C., Carduza, F., Vignolo, G., Protective action of lactobacillus curvatus CRL705 on vacuum-packaged raw beef. Effect on sensory and structural characteristics. Meat Science 85:3 (2010), 394–401, 10.1016/j.meatsci.2010.02.007.
Chen, X., Zhu, L., Liang, R., Mao, Y., Hopkins, D.L., Li, K., Luo, X., Shelf-life and bacterial community dynamics of vacuum packaged beef during long-term super-chilled storage sourced from two Chinese abattoirs. Food Research International, 130, 2020, 108937, 10.1016/j.foodres.2019.108937.
Danielski, G.M., Imazaki, P.H., de Andrade Cavalari, C.M., Daube, G., Clinquart, A., de Macedo, R.E.F., Carnobacterium maltaromaticum as bioprotective culture in vitro and in cooked ham. Meat Science, 162, 2020, 10.1016/J.MEATSCI.2019.108035.
Devlieghere, F., Debevere, J., Influence of dissolved carbon dioxide on the growth of spoilage bacteria. LWT - Food Science and Technology 33:8 (2000), 531–537, 10.1006/fstl.2000.0705.
Djenane, D., Roncalés, P., Carbon monoxide in meat and fish packaging: Advantages and limits. Foods, 7(2), 2018, 10.3390/foods7020012.
Edima, H.C., Cailliez-Grimal, C., Revol-Junelles, A.-M., Rondags, E., Millière, J.-B., Short communication: Impact of pH and temperature on the acidifying activity of Carnobacterium maltaromaticum. Journal of Dairy Science 91 (2008), 3806–3813, 10.3168/jds.2007-0878.
Evangelista, A.G., Danielski, G.M., Corrêa, J.A.F., de Cavalari, C.M.A., Souza, I.R., Luciano, F.B., de Macedo, R.E.F., Carnobacterium as a bioprotective and potential probiotic culture to improve food quality, food safety, and human health - a scoping review. Critical Reviews in Food Science and Nutrition, 2022, 10.1080/10408398.2022.2038079.
FAO, Preservation and Processing Technologies to Improve Availability and Safety of Meat and Meat Products in Developing Countries. 1995.
FAO, Meat Market Review: Emerging Trends and Outlook. 2022, 2022.
Grispoldi, L., Karama, M., Sechi, P., Iulieto, M.F., Cenci-Goga, B.T., Effect of the addition of starter cultures to ground meat for hamburger preparation. Microbiology Research, 11(1), 2020, 10.4081/mr.2020.8623.
Héquet, A., Laffitte, V., Brocail, E., Aucher, W., Cenatiempo, Y., Frère, J., Berjeaud, J.M., Development of a new method for the detection of lactic acid bacteria capable of protecting ham against Enterobacteriaceae. Letters in Applied Microbiology 48:6 (2009), 668–674, 10.1111/J.1472-765X.2009.02590.X.
Holck, A.L., Pettersen, M.K., Moen, M.H., Sørheim, O., Prolonged shelf life and reduced drip loss of chicken filets by the use of carbon dioxide emitters and modified atmosphere packaging. Journal of Food Protection 77:7 (2014), 1133–1141, 10.4315/0362-028X.JFP-13-428.
Hunt, M.C., King, A., Barbut, S., Clause, J., Cornforth, D., Hanson, D., Mohan, A., AMSA meat color measurement guidelines. 2012, American Meat Science Association, Champaign, Illinois USA.
Imazaki, P.H., Taminiau, B., Fall, P.A., Elansary, M., Douny, C., Scippo, M.-L., Clinquart, A., Oxidative stability and microbial ecology of fresh beef with extremely long shelf-life. Journal of Food Processing and Preservation, 1(13), 2023, 10.1155/2023/5319266.
ISO, Viande et produits à base de viande, Dénombrement des Pseudomonas spp. présomptifs, ISO 13720. 1995, Genève: Organisation internationale de normalisation.
ISO, Viande et produits à base de viande—Dénombrement de Brochothrix thermosphacta— Technique par comptage des colonies obtenues, ISO 13722. 1996, Genève: Organisation internationale de normalisation.
ISO, Viande et produits à base de viande—Mesurage du pH—Méthode de référence, ISO 2917. 1999, Organisation internationale de normalisation, Genève, 1999.
Iulietto, M.F., Sechi, P., Borgogni, E., Cenci-Goga, B.T., Meat spoilage: A critical review of a neglected alteration due to ropy slime producing bacteria. Italian Journal of Animal Science, 14(3), 2015, 4011, 10.4081/ijas.2015.4011.
Jakobsen, M., Bertelsen, G., Colour stability and lipid oxidation of fresh beef. Development of a response surface model for predicting the effects of temperature, storage time, and modified atmosphere composition. Meat Science 54:1 (2000), 49–57, 10.1016/S0309-1740(99)00069-8.
Karwowska, M., Łaba, S., Szczepański, K., Food loss and waste in meat sector—Why the consumption stage generates the most losses?. Sustainability, 13(11), 2021, 6227, 10.3390/SU13116227.
Kasra-Kermanshahi, R., Mobarak-Qamsari, E., Inhibition effect of lactic acid bacteria against food born pathogen, Listeria monocytogenes. Applied Food Biotechnology 2:4 (2015), 11–19, 10.22037/afb.v2i4.8894.
Kolbeck, S., Kienberger, H., Kleigrewe, K., Hilgarth, M., Vogel, R.F., Effect of high levels of CO2 and O2 on membrane fatty acid profile and membrane physiology of meat spoilage bacteria. European Food Research and Technology 247:4 (2021), 999–1011, 10.1007/S00217-020-03681-Y/FIGURES/4.
Koné, A.P., Zea, J.M.V., Gagné, D., Cinq-Mars, D., Guay, F., Saucier, L., Application of Carnobacterium maltaromaticum as a feed additive for weaned rabbits to improve meat microbial quality and safety. Meat Science 135 (2018), 174–188, 10.1016/j.meatsci.2017.09.017.
Laursen, B.G., Bay, L., Cleenwerck, I., Vancanneyt, M., Swings, J., Dalgaard, P., Leisner, J.J., Carnobacterium divergens and Carnobacterium maltaromaticum as spoilers or protective cultures in meat and seafood: Phenotypic and genotypic characterization. Systematic and Applied Microbiology 28:2 (2005), 151–164, 10.1016/j.syapm.2004.12.001.
Laursen, B.G., Leisner, J.J., Dalgaard, P., Carnobacterium species: Effect of metabolic activity and interaction with Brochothrix thermosphacta on sensory characteristics of modified atmosphere packed shrimp. Journal of Agricultural and Food Chemistry 54:10 (2006), 3604–3611, 10.1021/jf053017f.
Leisner, J.J., Laursen, B.G., Prévost, H., Drider, D., Dalgaard, P., Carnobacterium: Positive and negative effects in the environment and in foods. FEMS Microbiology Reviews 31:5 (2007), 592–613, 10.1111/j.1574-6976.2007.00080.x.
Macdougall, D.B., Taylor, A.A., Colour retention in fresh meat stored in oxygen-a commercial scale trial. International Journal of Food Science & Technology 10:3 (2007), 339–347, 10.1111/J.1365-2621.1975.Tb00037.X.
Mills, J., Donnison, A., Brightwell, G., Factors affecting microbial spoilage and shelf-life of chilled vacuum-packed lamb transported to distant markets: A review. Meat Science 98:1 (2014), 71–80, 10.1016/j.meatsci.2014.05.002.
Nilsson, L., Hansen, T.B., Garrido, P., Buchrieser, C., Glaser, P., Knøchel, S., Gravesen, A., Growth inhibition of listeria monocytogenes by a nonbacteriocinogenic Carnobacterium piscicola. Journal of Applied Microbiology 98:1 (2005), 172–183, 10.1111/j.1365-2672.2004.02438.x.
Olivera, D.F., Bambicha, R., Laporte, G., Cárdenas, F.C., Mestorino, N., Kinetics of colour and texture changes of beef during storage. Journal of Food Science and Technology 50:4 (2013), 821–825, 10.1007/s13197-012-0885-7.
Said, L.B., Gaudreau, H., Dallaire, L., Tessier, M., Fliss, I., Bioprotective culture: A new generation of food additives for the preservation of food quality and safety. Industrial Biotechnology 15:3 (2019), 138–147, 10.1089/ind.2019.29175.lbs.
Saraoui, T., Cornet, J., Guillouet, E., Pilet, M.F., Chevalier, F., Joffraud, J.J., Leroi, F., Improving simultaneously the quality and safety of cooked and peeled shrimp using a cocktail of bioprotective lactic acid bacteria. International Journal of Food Microbiology 241 (2017), 69–77, 10.1016/J.IJFOODMICRO.2016.09.024.
Singh, V.P., Recent approaches in food bio-preservation-A review. Open Veterinary Journal 8:1 (2018), 104–111 Faculty of Veterinary Medicine, University of Tripoli https://doi.org/10.4314/ovj.v8i1.16.
Spanu, C., Piras, F., Mocci, A.M., Nieddu, G., De Santis, E.P.L., Scarano, C., Use of Carnobacterium spp protective culture in MAP packed ricotta fresca cheese to control Pseudomonas spp. Food Microbiology 74 (2018), 50–56, 10.1016/j.fm.2018.02.020.
Stoops, J., Maes, P., Claes, J., Van Campenhout, L., Growth of Pseudomonas fluorescens in modified atmosphere packaged tofu. Letters in Applied Microbiology 54:3 (2012), 195–202, 10.1111/j.1472-765X.2011.03196.x.
Tshabalala, P.A., de Kock, H.L., Buys, E.M., Survival of Escherichia coli O157:H7 co-cultured with different levels of Pseudomonas fluorescens and lactobacillus plantarum on fresh beef. Brazilian Journal of Microbiology 43:4 (2012), 1406–1413, 10.1590/S1517-83822012000400023.
Zagorec, M., Champomier-Vergès, M.C., Meat microbiology and spoilage. Lawrie's Meat Science, 8th ed., 2017, Elsevier, 187–203, 10.1016/B978-0-08-100694-8.00006-6.
Zhang, P., Badoni, M., Gänzle, M., Yang, X., Growth of Carnobacterium spp. isolated from chilled vacuum-packaged meat under relevant acidic conditions. International Journal of Food Microbiology 286 (2018), 120–127, 10.1016/j.ijfoodmicro.2018.07.032.
Zhang, P., Baranyi, J., Tamplin, M., Interstrain interactions between bacteria isolated from vacuum-packaged refrigerated beef. Applied and Environmental Microbiology 81:8 (2015), 2753–2761, 10.1128/AEM.03933-14.
Zhang, P., Gänzle, M., Yang, X., Complementary antibacterial effects of bacteriocins and organic acids as revealed by comparative analysis of Carnobacterium spp. from meat. Applied and Environmental Microbiology 85:20 (2019), 1–15, 10.1128/AEM.01227-19.
Zhang, W., Xiao, S., Ahn, D.U., Protein oxidation: Basic principles and implications for meat quality. In Critical Reviews in Food Science and Nutrition 53:11 (2013), 1191–1201, 10.1080/10408398.2011.577.
