Abstract
Fungal contamination of food is responsible for health issues and food waste. In this work, the incorporation of a lactic acid bacteria (LAB) with antifungal properties (Lactobacillus buchneri UTAD104) into whey protein-based films and coatings was tested for the control of an ochratoxigenic fungi (Penicillium nordicum) in a cheese matrix. The incorporation of L. buchneri cells resulted in thicker films with less luminosity than control films and colour alteration. Nevertheless, cells inclusion did not alter moisture content, water vapour permeability, mechanical properties, hydrophobicity and chemical structure of the films. Whey protein films were able to maintain the viability of L. buchneri UTAD104 cells in 105 CFU/mL after 30 days of storage at 25 °C. When applied in cheese, films and coatings containing L. buchneri cells prevented fungal contamination for at least 30 days, while control cheeses with films and coatings either without LAB or with Lactobacillus casei UM3 (a strain without antifungal ability) showed fungal contamination during that period. Ochratoxin A was not found in cheeses treated with films and coatings containing L. buchneri UTAD104. Results showed that the inclusion of a LAB with antifungal properties in edible films and coatings can help to reduce or eliminate P. nordicum contamination in cheeses.
Similar content being viewed by others
References
Aloui, H., Licciardello, F., Khwaldia, K., Hamdi, M., & Restuccia, C. (2015). Physical properties and antifungal activity of bioactive films containing Wickerhamomyces anomalus killer yeast and their application for preservation of oranges and control of postharvest green mold caused by Penicillium digitatum. International Journal of Food Microbiology, 200, 22–30.
Aziz, S. G.-G., & Almasi, H. (2018). Physical characteristics, release properties, and antioxidant and antimicrobial activities of whey protein isolate films incorporated with thyme (Thymus vulgaris L.) extract-loaded nanoliposomes. Food and Bioprocess Technology, 11(8), 1552–1565.
Bahram, S., Rezaei, M., Soltani, M., Kamali, A., Ojagh, S. M., & Abdollahi, M. (2014). Whey protein concentrate edible film activated with cinnamon essential oil. Journal of Food Processing and Preservation, 38(3), 1251–1258.
Ballesteros, L. F., Cerqueira, M. A., Teixeira, J. A., & Mussatto, S. I. (2018). Production and physicochemical properties of carboxymethyl cellulose films enriched with spent coffee grounds polysaccharides. International Journal of Biological Macromolecules, 106, 647–655.
Bambace, M. F., Alvarez, M. V., & Moreira, M. D. R. (2019). Novel functional blueberries: fructo-oligosaccharides and probiotic lactobacilli incorporated into alginate edible coatings. Food Research International, 122, 653–660.
Bianchini, A., & Bullerman, L. B. (2009). Biological control of molds and mycotoxins in foods. In Appell, M., Kendra, D. F.& Trucksess, M. W. (Eds.), Mycotoxin Prevention and Control in Agriculture (Vol. 1031, pp. 1–16, ACS symposium series). Washington: ACS symposium series, American Chemical Society.
Burgain, J., Gaiani, C., Linder, M., & Scher, J. (2011). Encapsulation of probiotic living cells from laboratory scale to industrial applications. Journal of Food Engineering, 104(4), 467–483.
Campos, C. A., Gerschenson, L. N., & Flores, S. K. (2010). Development of edible films and coatings with antimicrobial activity. Food and Bioprocess Technology, 4(6), 849–875.
Cerqueira, M. A., Souza, B. W. S., Teixeira, J. A., & Vicente, A. A. (2012). Effect of glycerol and corn oil on physicochemical properties of polysaccharide films—a comparative study. Food Hydrocolloids, 27(1), 175–184.
Corsetti, A., Gobbetti, M., Rossi, J., & Damiani, P. (1998). Antimould activity of sourdough lactic acid bacteria: identification of a mixture of organic acids produced by Lactobacillus sanfrancisco CB1. Applied Microbiology and Biotechnology, 50(2), 253–256.
Dai, L., Yuan, Y., Song, Z., Qiu, Y., & Yue, T. (2018). Preparation and characterization of Lactobacilli-loaded composite films with sustaining antipathogenic activity and preservation effect. Journal of Food Science, 83(10), 2511–2519.
Falguera, V., Quintero, J. P., Jiménez, A., Muñoz, J. A., & Ibarz, A. (2011). Edible films and coatings: structures, active functions and trends in their use. Trends in Food Science & Technology, 22(6), 292–303.
Fan, Y., Xu, Y., Wang, D., Zhang, L., Sun, J., Sun, L., & Zhang, B. (2009). Effect of alginate coating combined with yeast antagonist on strawberry (Fragaria × ananassa) preservation quality. Postharvest Biology and Technology, 53(1–2), 84–90.
Fang, Y., Tung, M. A., Britt, I. J., Yada, S., & Dalgleish, D. G. (2002). Tensile and barrier properties of edible films made from whey proteins. Journal of Food Science, 67(1), 188–193.
Fernandes, R. V. B., Borges, S. V., Botrel, D. A., & Oliveira, C. R. (2014). Physical and chemical properties of encapsulated rosemary essential oil by spray drying using whey protein–inulin blends as carriers. International Journal of Food Science and Technology, 49(6), 1522–1529.
Gerez, C. L., Torres, M. J., Font de Valdez, G., & Rollán, G. (2013). Control of spoilage fungi by lactic acid bacteria. Biological Control, 64(3), 231–237.
Gialamas, H., Zinoviadou, K. G., Biliaderis, C. G., & Koutsoumanis, K. P. (2010). Development of a novel bioactive packaging based on the incorporation of Lactobacillus sakei into sodium-caseinate films for controlling Listeria monocytogenes. Food Research International, 43(10), 2402–2408.
Giraffa, G., Chanishvili, N., & Widyastuti, Y. (2010). Importance of lactobacilli in food and feed biotechnology. Research in Microbiology, 161(6), 480–487.
Guimarães, A., Abrunhosa, L., Pastrana, L. M., & Cerqueira, M. A. (2018a). Edible films and coatings as carriers of living microorganisms: a new strategy towards biopreservation and healthier foods. Comprehensive Reviews in Food Science and Food Safety, 17(3), 594–614.
Guimarães, A., Santiago, A., Teixeira, J. A., Venâncio, A., & Abrunhosa, L. (2018b). Anti-aflatoxigenic effect of organic acids produced by Lactobacillus plantarum. International Journal of Food Microbiology, 264, 31–38.
Guimarães, A., Venancio, A., & Abrunhosa, L. (2018c). Antifungal effect of organic acids from lactic acid bacteria on Penicillium nordicum. Food Additives & Contaminants: Part A, 35(9), 1803–1818.
Hymery, N., Vasseur, V., Coton, M., Mounier, J., Jany, J.-L., Barbier, G., & Coton, E. (2014). Filamentous fungi and mycotoxins in cheese: a review. Comprehensive Reviews in Food Science and Food Safety, 13(4), 437–456.
Kanmani, P., & Lim, S. T. (2013). Development and characterization of novel probiotic-residing pullulan/starch edible films. Food Chemistry, 141(2), 1041–1049.
Khwaldia, K., Perez, C., Banon, S., Desobry, S., & Hardy, J. (2004). Milk proteins for edible films and coatings. Critical Reviews in Food Science and Nutrition, 44(4), 239–251.
Kokoszka, S., Debeaufort, F., Lenart, A., & Voilley, A. (2010). Water vapour permeability, thermal and wetting properties of whey protein isolate based edible films. International Dairy Journal, 20(1), 53–60.
Lavermicocca, P., Valerio, F., Evidente, A., Lazzaroni, S., Corsetti, A., & Gobbetti, M. (2000). Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Applied and Environmental Microbiology, 66(9), 4084–4090.
Le Tien, C., Letendre, M., Ispas-Szabo, P., Mateescu, M. A., Delmas-Patterson, G., Yu, H. L., et al. (2000). Development of biodegradable films from whey proteins by cross-linking and entrapment in cellulose. Journal of Agricultural and Food Chemistry, 48(11), 5566–5575.
Li, Y., Jiang, Y., Liu, F., Ren, F., Zhao, G., & Leng, X. (2011). Fabrication and characterization of TiO2/whey protein isolate nanocomposite film. Food Hydrocolloids, 25(5), 1098–1104.
López-Rubio, A., & Lagaron, J. M. (2012). Whey protein capsules obtained through electrospraying for the encapsulation of bioactives. Innovative Food Science and Emerging Technologies, 13, 200–206.
Martins, J. T., Cerqueira, M. A., Bourbon, A. I., Pinheiro, A. C., Souza, B. W. S., & Vicente, A. A. (2012). Synergistic effects between κ-carrageenan and locust bean gum on physicochemical properties of edible films made thereof. Food Hydrocolloids, 29(2), 280–289.
Medeiros, B. G., dos Souza, M. P. S., Pinheiro, A. C., Bourbon, A. I., Cerqueira, M. A., Vicente, A. A., et al. (2014). Physical characterisation of an alginate/lysozyme nano-laminate coating and its evaluation on ‘Coalho’cheese shelf life. Food and Bioprocess Technology, 7(4), 1088–1098.
Mohammadi, R., Mortazavian, A. M., Khosrokhavar, R., & da Cruz, A. G. (2011). Probiotic ice cream: viability of probiotic bacteria and sensory properties. Annals of Microbiology, 61(3), 411–424.
Mokrzycki, W. S., & Tatol, M. (2011). Colour difference ∆E—a survey. Machine graphics and vision, 20(4), 383–411.
Niku-Paavola, M. L., Laitila, A., Mattila-Sandholm, T., & Haikara, A. (1999). New types of antimicrobial compounds produced by Lactobacillus plantarum. Journal of Applied Microbiology, 86(1), 29–35.
Özcelik, S., Kuley, E., & Özogul, F. (2016). Formation of lactic, acetic, succinic, propionic, formic and butyric acid by lactic acid bacteria. LWT - Food Science and Technology, 73, 536–542.
Ozdemir, M., & Floros, J. D. (2008). Optimization of edible whey protein films containing preservatives for water vapor permeability, water solubility and sensory characteristics. Journal of Food Engineering, 86(2), 215–224.
Pavli, F., Kovaiou, I., Apostolakopoulou, G., Kapetanakou, A., Skandamis, P., Nychas, G. E., et al. (2017). Alginate-based edible films delivering probiotic bacteria to sliced ham pretreated with high pressure processing. International Journal of Molecular Sciences, 18(9), 1867.
Perdones, A., Sánchez-González, L., Chiralt, A., & Vargas, M. (2012). Effect of chitosan–lemon essential oil coatings on storage-keeping quality of strawberry. Postharvest Biology and Technology, 70, 32–41.
Pereira, J. O., Soares, J., Sousa, S., Madureira, A. R., Gomes, A., & Pintado, M. (2016). Edible films as carrier for lactic acid bacteria. LWT - Food Science and Technology, 73, 543–550.
Pereira, O. J., Soares, J., Monteiro, M., Gomes, A., & Pintado, M. (2018). Impact of whey protein coating incorporated with Bifidobacterium and Lactobacillus on sliced ham properties. Meat Science, 139, 125–133.
Pérez, L. M., Piccirilli, G. N., Delorenzi, N. J., & Verdini, R. A. (2016). Effect of different combinations of glycerol and/or trehalose on physical and structural properties of whey protein concentrate-based edible films. Food Hydrocolloids, 56, 352–359.
Pérez-Gago, M. B., & Krochta, J. M. (2001). Denaturation time and temperature effects on solubility, tensile properties, and oxygen permeability of whey protein edible films. Journal of Food Science, 66(5), 705–710.
Pérez-Gago, M. B., Nadaud, P., & Krochta, J. M. (1999). Water vapor permeability, solubility, and tensile properties of heat-denatured versus native whey protein films. Journal of Food Science, 64(6), 1034–1037.
Phan, T. D., Debeaufort, F., Luu, D., & Voilley, A. (2005). Functional properties of edible agar-based and starch-based films for food quality preservation. Journal of Agricultural and Food Chemistry, 53(4), 973–981.
Piermaria, J., Diosma, G., Aquino, C., Garrote, G., & Abraham, A. (2015). Edible kefiran films as vehicle for probiotic microorganisms. Innovative Food Science and Emerging Technologies, 32, 193–199.
Prema, P., Smila, D., Palavesam, A., & Immanuel, G. (2010). Production and characterization of an antifungal compound (3-phenyllactic acid) produced by Lactobacillus plantarum strain. Food and Bioprocess Technology, 3(3), 379–386.
Ramos, Ó. L., Fernandes, J. C., Silva, S. I., Pintado, M. E., & Malcata, F. X. (2012a). Edible films and coatings from whey proteins: a review on formulation, and on mechanical and bioactive properties. Critical Reviews in Food Science and Nutrition, 52(6), 533–552.
Ramos, Ó. L., Pereira, J. O., Silva, S. I., Fernandes, J. C., Franco, M. I., Lopes-da-Silva, J. A., Pintado, M. E., & Malcata, F. X. (2012b). Evaluation of antimicrobial edible coatings from a whey protein isolate base to improve the shelf life of cheese. Journal of Dairy Science, 95(11), 6282–6292.
Ramos, Ó. L., Pereira, R. N., Rodrigues, R. M., Teixeira, J. A., Vicente, A. A., & Malcata, F. X. (2016). Whey and whey powders: production and uses. In B. Caballero, P. M. Finglas, & F. Toldrá (Eds.), Encyclopedia of food and health (pp. 498–505). Oxford: Academic Press.
Ramos, Ó. L., Reinas, I., Silva, S. I., Fernandes, J. C., Cerqueira, M. A., Pereira, R. N., Vicente, A. A., Poças, M. F., Pintado, M. E., & Malcata, F. X. (2013). Effect of whey protein purity and glycerol content upon physical properties of edible films manufactured therefrom. Food Hydrocolloids, 30(1), 110–122.
Ramos, Ó. L., Silva, S. I., Soares, J. C., Fernandes, J. C., Poças, M. F., Pintado, M. E., & Malcata, F. X. (2012c). Features and performance of edible films, obtained from whey protein isolate formulated with antimicrobial compounds. Food Research International, 45(1), 351–361.
Reinoso, E., Mittal, G. S., & Lim, L.-T. (2008). Influence of whey protein composite coatings on plum (Prunus domestica L.) fruit quality. Food and Bioprocess Technology, 1(4), 314–325.
Reis, J. A., Paula, A. T., Casarotti, S. N., & Penna, A. L. B. (2012). Lactic acid bacteria antimicrobial compounds: Characteristics and applications. Food Engineering Reviews, 4(2), 124–140.
Rhee, S. J., Lee, J.-E., & Lee, C.-H. (2011). Importance of lactic acid bacteria in Asian fermented foods. Microbial Cell Factories, 10(1), S5.
Rizzello, C. G., Cassone, A., Coda, R., & Gobbetti, M. (2011). Antifungal activity of sourdough fermented wheat germ used as an ingredient for bread making. Food Chemistry, 127(3), 952–959.
Sánchez-González, L., Saavedra, J. I. Q., & Chiralt, A. (2013). Physical properties and antilisterial activity of bioactive edible films containing Lactobacillus plantarum. Food Hydrocolloids, 33(1), 92–98.
Sánchez-González, L., Saavedra, J. I. Q., & Chiralt, A. (2014). Antilisterial and physical properties of biopolymer films containing lactic acid bacteria. Food Control, 35(1), 200–206.
Schnurer, J., & Magnusson, J. (2005). Antifungal lactic acid bacteria as biopreservatives. Trends in Food Science and Technology, 16(1–3), 70–78.
Settier-Ramírez, L., López-Carballo, G., Gavara, R., & Hernández-Muñoz, P. (2019). Antilisterial properties of PVOH-based films embedded with Lactococcus lactis subsp. lactis. Food Hydrocolloids, 87, 214–220.
Soukoulis, C., Behboudi-Jobbehdar, S., Yonekura, L., Parmenter, C., & Fisk, I. (2014a). Impact of milk protein type on the viability and storage stability of microencapsulated Lactobacillus acidophilus NCIMB 701748 using spray drying. Food and Bioprocess Technology, 7(5), 1255–1268.
Soukoulis, C., Behboudi-Jobbehdar, S., Yonekura, L., Parmenter, C., & Fisk, I. D. (2014b). Stability of Lactobacillus rhamnosus GG in prebiotic edible films. Food Chemistry, 159, 302–308.
Soukoulis, C., Singh, P., Macnaughtan, W., Parmenter, C., & Fisk, I. D. (2016). Compositional and physicochemical factors governing the viability of Lactobacillus rhamnosus GG embedded in starch-protein based edible films. Food Hydrocolloids, 52, 876–887.
Soukoulis, C., Yonekura, L., Gan, H.-H., Behboudi-Jobbehdar, S., Parmenter, C., & Fisk, I. (2014c). Probiotic edible films as a new strategy for developing functional bakery products: The case of pan bread. Food Hydrocolloids, 39(100), 231–242.
Ström, K., Sjögren, J., Broberg, A., & Schnürer, J. (2002). Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(l-Phe-l-pro) and cyclo(l-Phe-trans-4-OH-l-pro) and 3-phenyllactic acid. Applied and Environmental Microbiology, 68(9), 4322–4327.
Su, J.-F., Yuan, X.-Y., Huang, Z., Wang, X.-Y., Lu, X.-Z., Zhang, L.-D., & Wang, S. B. (2012). Physicochemical properties of soy protein isolate/carboxymethyl cellulose blend films crosslinked by Maillard reactions: Color, transparency and heat-sealing ability. Materials Science and Engineering: C, 32(1), 40–46.
Tapia, M. S., Rojas-Grau, M. A., Rodríguez, F. J., Ramírez, J., Carmona, A., & Martin-Belloso, O. (2007). Alginate- and gellan-based edible films for probiotic coatings on fresh-cut fruits. Journal of Food Science, 72(4), 190–196.
Tharanathan, R. N. (2003). Biodegradable films and composite coatings: past, present and future. Trends in Food Science & Technology, 14(3), 71–78.
Varsha, K. K., & Nampoothiri, K. M. (2016). Appraisal of lactic acid bacteria as protective cultures. Food Control, 69, 61–64.
Ye, J., Ma, D., Qin, W., & Liu, Y. (2018). Physical and antibacterial properties of sodium alginate - sodium carboxymethylcellulose films containing Lactococcus lactis. Molecules, 23(10), 2645.
Acknowledgements
This study was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UIDB/04469/2020 unit and BioTecNorte operation (NORTE-01-0145-FEDER-000004) funded by the European Regional Development Fund under the scope of Norte2020 - Programa Operacional Regional do Norte. Ana Guimarães received support through grant SFRH/BD/103245/2014 from the Portuguese FCT.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Guimarães, A., Ramos, Ó., Cerqueira, M. et al. Active Whey Protein Edible Films and Coatings Incorporating Lactobacillus buchneri for Penicillium nordicum Control in Cheese. Food Bioprocess Technol 13, 1074–1086 (2020). https://doi.org/10.1007/s11947-020-02465-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-020-02465-2