english Antimicrobial properties of lysozyme in meat and meat products: possibilities and challenges
Resumo
Meat and meat products are highly perishable as they can provide an appropriate environment for microbial growth due to their high water activity and proper pH level. Quality, safety, sensory and nutritional properties of meat products are highly influenced by pathogenic and spoilage microorganisms. To prevent microbial growth, artificial antimicrobials have been used in food matrices, however safety concerns regarding the use of synthetic preservatives is a challenging issue. Additionally, consumer’s trend towards natural mildly processed products with extended shelf life necessitates the identification of alternative additives originating from natural sources of new acceptable and effective antimicrobials. Although the effectiveness of some natural antimicrobial agents has already been reported, still, there is lack of information regarding the possibility of using lysozyme as a preservative in meat and meat products either alone or in combination with other hurdles. In the present review the applications and beneficial effects of applying lysozyme in meat products, considering its limitations such as allergic problems, interactions with food constituents, reducing sensory changes and toxicity due to high required concentrations to prevent spoilage and oxidation in foods will be discussed
Downloads
Referências
Abdollahzadeh, E., Rezaei, M., & Hosseini, H. (2014). Antibacterial activity of plant essential oils and extracts: the role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control, 35, 177-183. DOI: http://doi.org/10.1016/j.foodcont.2013.07.004
Abdou, A. M., Higashiguchi, S., Aboueleinin, A., Kim, M., & Ibrahim, H. R. (2007). Antimicrobial peptides derived from hen egg lysozyme with inhibitory effect against Bacillus species. Food Control, 18(2), 173-178. DOI: http://doi.org/10.1016/j.foodcont.2005.09.010
Akashi, A. (1969). Preservative effect of egg-white lysozyme added to cooked sausage. Japanese Journal of Zootechnical Science, 40, 243-248.
Akashi, A. (1970). Preservative effect of egg-white lysozyme on salami sausage. Japanese Journal of Zootechnical Science, 41, 143-150.
Akashi, A. (1971). Preservative effect of egg white lysozyme on Vienna sausage. Japanese Journal of Zootechnical Science, 42(6), 289-295.
Amara, C. B., Eghbal, N., Degraeve, P., & Gharsallaoui, A. (2016). Using complex coacervation for lysozyme encapsulation by spray-drying. Journal of Food Engineering, 183, 50-57. DOI: http://doi.org/10.1016/j.foodeng.2016.03.016
Anand, S. P, & Sati, N. (2013). Artificial preservatives and their harmful effects: looking toward nature for safer alternatives. International Journal of Pharmaceutical Sciences and Research, 4, 2496-2501.
Avramescu, M.-E., Borneman, Z., & Wessling, M. (2008). Particle-loaded hollow-fiber membrane adsorbers for lysozyme separation. Journal of Membrane Science, 322(2), 306-313. DOI: http://doi.org/10.1016/j.memsci.2008.06.013
Barbiroli, A., Bonomi, F., Capretti, G., Iametti, S., Manzoni, M., Piergiovanni, L., & Rollini, M. (2012). Antimicrobial activity of lysozyme and lactoferrin incorporated in cellulose-based food packaging. Food Control, 26(2), 387-392. DOI: http://doi.org/10.1016/j.foodcont.2012.01.046
Benelhadj, S., Fejji, N., Degraeve, P., Attia, H., Ghorbel, D., & Gharsallaoui, A. (2016). Properties of lysozyme/Arthrospira platensis (Spirulina) protein complexes for antimicrobial edible food packaging. Algal Research, 15, 43-49. DOI: http://doi.org/10.1016/j.algal.2016.02.003
Bevilacqua, A., Sinigaglia, M., & Corbo, M. R. (2010). Use of lysozyme and na2‐ethylenediaminetetraacetic acid for the inhibition of hafnia alvei of dairy origin: individuation of the minimal inhibitory concentrations. Journal of Food Processing and Preservation, 34(5), 904-914. DOI: http://doi.org/10.1111/j.1745-4549.2009.00406.x
Branen, J. K., & Davidson, P. M. (2004). Enhancement of nisin, lysozyme, and monolaurin antimicrobial activities by ethylenediaminetetraacetic acid and lactoferrin. International Journal of Food Microbiology, 90, 63-74. DOI: http://doi.org/10.1016/s0168-1605(03)00172-7
Cannarsi, M., Baiano, A., Sinigaglia, M., Ferrara, L., Baculo, R., & Del Nobile, M. A. (2008). Use of nisin, lysozyme and EDTA for inhibiting microbial growth in chilled buffalo meat. International Journal of Food Science & Technology, 43(4), 573-578. DOI: http://doi.org/10.1111/j.1365-2621.2006.01438.x
Carrillo, W., García-Ruiz, A., Recio, I., & Moreno-Arribas, M. V. (2014). Antibacterial activity of hen egg white lysozyme modified by heat and enzymatic treatments against oenological lactic acid bacteria and acetic acid bacteria. Journal of food protection, 77(10), 1732-1739. DOI: http://doi.org/10.4315/0362-028X.JPF-14-009
Cegielska-Radziejewska, R., & Szablewski, T. (2013). Effect of modified lysozyme on the microflora and sensory attributes of ground pork. Journal of Food Protection, 76(2), 338-342. DOI: http://doi.org/10.4315/0362-028X.JFP-12-075
Chen, K., Han, S.-Y., Li, M., & Sheng, W.-J. (2017). Use of lysozyme and oligomeric proanthocyanidin to reduce sulfur dioxide and the evolution of volatile compounds in italian riesling ice wine during aging process. Journal of Food Processing and Preservation, 41, e12755. DOI: http://doi.org/10.1111/jfpp.12755
Cho, M. H., Bae, E. K., Ha, S. D., & Park, J. Y. (2005). Application of natural antimicrobials to food industry. Food science and Industry, 38, 36-45.
Chouliara, E., Karatapanis, A., Savvaidis, I. N., & Kontominas, M. G. (2007). Combined effect of oregano essential oil and modified atmosphere packaging on shelf-life extension of fresh chicken breast meat, stored at 4ºC. Food Microbiology, 24(6), 607-617. DOI: http://doi.org/10.1016/j.fm.2006.12.005
Chung, W., & Hancock, R. E. (2000). Action of lysozyme and nisin mixtures against lactic acid bacteria. International Journal of Food Microbiology, 60, 25-32. DOI: http://doi.org/10.1016/s0168-1605(00)00330-5
Cunningham, F. E., Proctor, V. A., & Goetsch, S. J. (1991). Egg-white lysozyme as a food preservative: an overview. World's Poultry Science Journal, 47(2), 141-163. DOI: http://doi.org/10.1079/WPS19910015
Dave, D., & Ghaly, A. E. (2011). Meat spoilage mechanisms and preservation techniques: a critical review. American Journal of Agricultural and Biological Science, 6(4), 486-510. DOI: http://doi.org/10.3844/ajabssp.2011.486.510
Düring, K., Porsch, P., Mahn, A., Brinkmann, O., & Gieffers, W. (1999). The non‐enzymatic microbicidal activity of lysozymes. FEBS letters, 449(2-3), 93-100. DOI: http://doi.org/10.1016/s0014-5793(99)00405-6
Fleming, A., & Allison, V. D. (1922). Observations on a bacteriolytic substance (“lysozyme”) found in secretions and tissues. The British Journal of Experimental Pathology, 3(5), 252-260.
Gill, A. O., & Holley, R. A. (2000). Surface application of lysozyme, nisin, and EDTA to inhibit spoilage and pathogenic bacteria on ham and bologna. Journal of Food Protection, 63(10), 1338-1346. DOI: http://doi.org/10.4315/0362-028x-63.10.1338
Gill, A. O., & Holley, R. A. (2003). Interactive inhibition of meat spoilage and pathogenic bacteria by lysozyme, nisin and EDTA in the presence of nitrite and sodium chloride at 24ºC. International journal of food microbiology, 80(3), 251-259. DOI: http://doi.org/10.1016/s0168-1605(02)00171-x
Goodarzi, A., Hovhannisyan, H., & Barseghyan, A. (2016). Elimination of pathogen Escherichia coli O157: H7 in ground beef by a newly isolated strain of lactobacillus acidophilus during storage at 5°C. Applied Food Biotechnology, 3, 170-176. DOI: http://doi.org/10.22037/afb.v3i3.11799
Herath, I. A. H. M. E., Priyanath, J. J. M., Ahn, D. U., & Abeyrathne, E. D. N. S. (2015). Use of lysozyme from chicken egg white as a nitrite replacer in an Italian-type chicken sausage. Functional Foods in Health and Disease, 5(9), 319-329. DOI: http://doi.org/10.31989/ffhd.v5i9.217
Hildebrandt, S., Schütte, L., Stoyanov, S., Hammer, G., Steinhart, H., & Paschke, A. (2010). In vitro determination of the allergenic potential of egg white in processed meat. Journal of allergy, 2010, 238573. DOI: http://doi.org/10.1155/2010/238573
Huang, W., Xu, H., Xue, Y., Huang, R., Deng, H., & Pan, S. (2012). Layer-by-layer immobilization of lysozyme–chitosan–organic rectorite composites on electrospun nanofibrous mats for pork preservation. Food Research International, 48(2), 784-791. DOI: http://doi.org/10.1016/j.foodres.2012.06.026
Hussain, A., Zia, K. M., Tabasum, S., Noreen, A., Ali, M., Iqbal, R., & Zuber, M. (2017). Blends and composites of exopolysaccharides; properties and applications: a review. International Journal of Biological Macromolecules, 94(A), 10-27. DOI: http://doi.org/10.1016/j.ijbiomac.2016.09.104
Ibrahim, H. R., Higashiguchi, S., Juneja, L. R., Kim, M., & Yamamoto, T. (1996). A structural phase of heat-denatured lysozyme with novel antimicrobial action. Journal of Agricultural and Food Chemistry, 44(6), 1416-1423. DOI: http://doi.org/10.1021/jf9507147
Johnson, L. N., Phillips, D. C., & Rupley, J. A. (1968). The activity of lysozyme: an interim review of crystallographic and chemical evidence. Brookhaven Symposia in Biology, 21(1), 120-138.
Kanatt, S. R., Chander, R., & Sharma, A. (2008). Chitosan and mint mixture: a new preservative for meat and meat products. Food Chemistry, 107(2), 845-852. DOI: http://doi.org/10.1016/j.foodchem.2007.08.088
Kasra-Kermanshahi, R., & Mobarak-Qamsari, E. (2015). Inhibition effect of lactic acid bacteria against food born pathogen, Listeria monocytogenes. Applied Food Biotechnology, 2(4), 11-19. DOI: http://doi.org/10.22037/afb.v2i4.8894
Kijowski, J., Marciszewska, C., Cegielska-Radziejewska, R., & Popiół, A. (2013). Effect of lysozyme treatment on quality and bacterial contamination of chilled chicken legs. Bulletin of the Veterinary Institute in Pulawy, 57, 79-84. DOI: http://doi.org/10.2478/bvip-2013-0015
Kim, S.-J., Cho, A. R., & Han, J. (2013). Antioxidant and antimicrobial activities of leafy green vegetable extracts and their applications to meat product preservation. Food Control, 29, 112-120. DOI: http://doi.org/10.1016/j.foodcont.2012.05.060
Kozuka, M., Murao, S., Yamane, T., Inoue, T., Ohkubo, I., & Ariga, H. (2015). Rapid and simple purification of lysozyme from the egg shell membrane. Journal of Nutritional Science and Vitaminology, 61, 101-103. DOI: http://doi.org/10.3177/jnsv.61.101
Leduc, V., Demeulemester, C., Guizard, C., Le Guern, L., Polack, B., & Peltre, G. (1999). Immunochemical detection of egg‐white antigens and allergens in meat products. Allergy, 54(5), 464-472. DOI: http://doi.org/10.1034/j.1398-9995.1999.00928.x
Lesnierowski, G., & Kijowski, J. (2007). Lysozyme. In R. Huopalahti, R. López-Fandiño, M. Anton & R Schade (Eds.), Bioactive Egg Compounds (p. 33-42). Berlin, GE: Springer.
Li, W., Li, X., Wang, Q., Pan, Y., Wang, T., Wang, H., ... Deng, H. (2014). Antibacterial activity of nanofibrous mats coated with lysozyme-layered silicate composites via electrospraying. Carbohydrate Polymers, 99, 218-225. DOI: http://doi.org/10.1016/j.carbpol.2013.07.055
Liberti, R., Franciosa, G., Gianfranceschi, M., & Aureli, P. (1996). Effect of combined lysozyme and lipase treatment on the survival of Listeria monocytogenes. International Journal of Food Microbiology, 32(1-2), 235-242. DOI: http://doi.org/10.1016/0168-1605(96)01121-X
Lodi, R., & Stadhouders, J. (1990). The use of lysozyme to control butyric acid fermentation. Bulletin of the International Dairy Federation, 251, 51-54.
Maehashi, K., Matano, M., Irisawa, T., Uchino, M., Kashiwagi, Y., & Watanabe, T. (2012). Molecular characterization of goose-and chicken-type lysozymes in emu (Dromaius novaehollandiae): evidence for extremely low lysozyme levels in emu egg white. Gene, 492, 244-249. DOI: http://doi.org/10.1016/j.gene.2011.10.021
Malicki, A., Jarmoluk, A., & Bruzewicz, S. (2004). Effect of sodium lactate used alone or in combination with lysozyme on the physico-chemical and microbiological properties of steamed sausage stored under the refrigeration. Journal of Veterinary Research (Poland), 48, 47-51.
Mascheroni, E., Capretti, G., Marengo, M., Iametti, S., Mora, L., Piergiovanni, L., & Bonomi, F. (2010). Modification of cellulose‐based packaging materials for enzyme immobilization. Packaging Technology and Science, 23, 47-57. DOI: http://doi.org/10.1002/pts.878
Mine, Y., Ma, F., & Lauriau, S. (2004). Antimicrobial peptides released by enzymatic hydrolysis of hen egg white lysozyme. Journal of Agricultural and Food Chemistry, 52(5), 1088-1094. DOI: http://doi.org/10.1021/jf0345752
Nagai, T., Inoue, R., Kanamori, N., Suzuki, N., & Nagashima, T. (2006). Characterization of honey from different floral sources. Its functional properties and effects of honey species on storage of meat. Food Chemistry, 97(2), 256-262. DOI: http://doi.org/10.1016/j.foodchem.2005.03.045
Naknukool, S., Hayakawa, S., Uno, T., & Ogawa, M. (2009). Antimicrobial activity of duck egg lysozyme against salmonella enteritidis. In G. Barbosa-Cánovas & P. Colonna (Eds.), Global Issues in Food Science and Technology (p. 293-307). Amsterdam, NL: Elsevier.
Nattress, F. M., Yost, C. K., & Baker, L. P. (2001). Evaluation of the ability of lysozyme and nisin to control meat spoilage bacteria. International Journal of Food Microbiology, 70(1-2), 111-119. DOI: http://doi.org/10.1016/s0168-1605(01)00531-1
Negi, P. S. (2012). Plant extracts for the control of bacterial growth: efficacy, stability and safety issues for food application. International Journal of Food Microbiology, 156, 7-17. DOI: http://doi.org/10.1016/j.ijfoodmicro.2012.03.006
Ntzimani, A. G., Giatrakou, V. I., & Savvaidis, I. N. (2010). Combined natural antimicrobial treatments (EDTA, lysozyme, rosemary and oregano oil) on semi cooked coated chicken meat stored in vacuum packages at 4ºC: microbiological and sensory evaluation. Innovative Food Science & Emerging Technologies, 11, 187-196. DOI: http://doi.org/10.1016/j.ifset.2009.09.004
Oh, M., Lee, J., Jeong, Y., & Kim, M. (2016). Synergistic antilisterial effects of mixtures of lysozyme and organic acids. Journal of Food Protection, 79(12), 2184-2189. DOI: http://doi.org/10.4315/0362-028X.JFP-16-156
Olaoye, O. A., Onilude, A. A., & Ubbor, S. C. (2015). Control of Brochothrix thermosphacta in pork meat using lactococcus lactis subsp. lactis i23 isolated from beef. Applied Food Biotechnology, 2(3), 49-55. DOI: http://doi.org/10.22037/afb.v2i3.7993
Oliveira, T. L. C. d., Ramos, A. L. S., Ramos, E. M, Piccoli, R. H., & Cristianini, M. (2015). Natural antimicrobials as additional hurdles to preservation of foods by high pressure processing. Trends in Food Science & Technology, 45, 60-85. DOI: http://doi.org/10.1016/j.tifs.2015.05.007.
Pilevar, Z., Hosseini, H., Beikzadeh, S., Khanniri, E., & Alizadeh, A. M. (2020). Application of bacteriocins in meat and meat products: An update. Current Nutrition & Food Science, 16(2), 120-133.
Pilevar, Z., & Hosseini, H. (2017). Effects of starter cultures on the properties of meat products: A review. Annual Research & Review in Biology, 1-17.
Pilevar, Z., & Hosseini, H. (2013). Chemical composition, antimicrobial and antioxidant activity of Echinophora platyloba DC. Journal of Pharmacy and Nutrition Sciences, 3, 270-283. DOI: http:doi.org/10.6000/1927-5951.2013.03.04.10
Pilevar, Z., Hosseini, H., Hajimehdipoor, H., Shahraz, F., Alizadeh, L., Mousavi Khaneghah, A., & Mahmoudzadeh, M. (2017). The Anti-Staphylococcus aureus effect of combined echinophora platyloba essential oil and liquid smoke in beef. Food Technology and Biotechnology, 55, 117-124. DOI: http://doi.org/10.17113/ftb.55.01.17.4633
Proctor, V. A., Cunningham, F. E., & Fung, D. Y. C. (1988). The chemistry of lysozyme and its use as a food preservative and a pharmaceutical. Critical Reviews in Food Science and Nutrition, 26(4), 359-395. DOI: http://doi.org/10.1080/10408398809527473
Prosapio, V., Reverchon, E., & De Marco, I. (2016). Production of lysozyme microparticles to be used in functional foods, using an expanded liquid antisolvent process. The Journal of Supercritical Fluids, 107, 106-113. DOI: http://doi.org/10.1016/j.supflu.2015.09.001
Quintavalla, S., & Vicini, L. (2002). Antimicrobial food packaging in meat industry. Meat science, 62(3), 373-380. DOI: http://doi.org/10.1016/s0309-1740(02)00121-3
Ranaii, V., Pilevar, Z., Mousavi Khaneghah, A., & Hosseini, H. (2020). Propionic acid: method of production, current state and perspectives. Food Technology and Biotechnology, 58(2), 115-127. DOI: http://dx.doi.org/10.17113/ftb.58.02.20.6356
Rao, M. S., Chander, R., & Sharma, A. (2008). Synergistic effect of chitooligosaccharides and lysozyme for meat preservation. LWT-Food Science and Technology, 41(10), 1995-2001. DOI: http://doi.org/10.1016/j.lwt.2008.01.013
Seetaramaiah, K., Smith, A. A., Murali, R., & Manavalan, R. (2011). Preservatives in food products-review. International Journal of Pharmaceutical & Biological Archives, 2(2), 583-599.
Strominger, J. L., & Tipper, D. J. (1974). Structure of bacterial cell walls: the lysozyme substrate. In E. Osserman, R. E. Canfield & S. Beychok (Eds.), Lysozyme (p. 169-85). New York, NY: Academic Press.
Sung, S.-Y., Sin, L. T., Tee, T.-T., Bee, S.-T., Rahmat, A. R., Rahman, W. A. W. A., ... Vikhraman, M. (2013). Antimicrobial agents for food packaging applications. Trends in Food Science & Technology, 33(2), 110-123. DOI: http://doi.org/10.1016/j.tifs.2013.08.001
Tribst, A. A. L., Franchi, M. A., & Cristianini, M. (2008). Ultra-high pressure homogenization treatment combined with lysozyme for controlling Lactobacillus brevis contamination in model system. Innovative Food Science & Emerging Technologies, 9(3), 265-271. DOI: http://doi.org/10.1016/j.ifset.2007.07.012
Weert, M. V. d., Hoechstetter, J., Hennink, W. E., & Crommelin, D. J. A. (2000). The effect of a water/organic solvent interface on the structural stability of lysozyme. Journal of Controlled Release, 68(3), 351-359. DOI: http://doi.org/10.1016/s0168-3659(00)00277-7
Whitaker, J. R., Wong, D. W. S., & Voragen, A. G. J. (2003). Handbook of Food Enzymology. New York, NY: Marcel Dekker.
Wu, T., Wu, C., Fu, S., Wang, L., Yuan, C., Chen, S., & Hu, Y. (2017). Integration of lysozyme into chitosan nanoparticles for improving antibacterial activity. Carbohydrate Polymers, 155, 192-200. DOI: http://doi.org/10.1016/j.carbpol.2016.08.076
You, S.-J., Udenigwe, C. C., Aluko, R. E., & Wu, J. (2010). Multifunctional peptides from egg white lysozyme. Food Research International, 43, 848-855. DOI: http://doi.org/10.1016/j.foodres.2009.12.004
Zhang, H., Kong, B., Xiong, Y. L., & Sun, X. (2009). Antimicrobial activities of spice extracts against pathogenic and spoilage bacteria in modified atmosphere packaged fresh pork and vacuum packaged ham slices stored at 4ºC. Meat science, 81(4), 686-692. DOI: http://doi.org/10.1016/j.meatsci.2008.11.011
Zhang, T., Zhou, P., Zhan, Y., Shi, X., Lin, J., Du, Y., ... Deng, H. (2015). Pectin/lysozyme bilayers layer-by-layer deposited cellulose nanofibrous mats for antibacterial application. Carbohydrate Polymers, 117, 687-693. DOI: http://doi.org/10.1016/j.carbpol.2014.10.064
Zimoch-Korzycka, A., & Jarmoluk, A. (2015). The use of chitosan, lysozyme, and the nano-silver as antimicrobial ingredients of edible protective hydrosols applied into the surface of meat. Journal of Food Science and Technology, 52, 5996-6002. DOI: http://doi.org/10.1007/s13197-014-1645-7
DECLARAÇÃO DE ORIGINALIDADE E DIREITOS AUTORAIS
Declaro que o presente artigo é original, não tendo sido submetido à publicação em qualquer outro periódico nacional ou internacional, quer seja em parte ou em sua totalidade.
Os direitos autorais pertencem exclusivamente aos autores. Os direitos de licenciamento utilizados pelo periódico é a licença Creative Commons Attribution 4.0 (CC BY 4.0): são permitidos o compartilhamento (cópia e distribuição do material em qualqer meio ou formato) e adaptação (remix, transformação e criação de material a partir do conteúdo assim licenciado para quaisquer fins, inclusive comerciais.
Recomenda-se a leitura desse link para maiores informações sobre o tema: fornecimento de créditos e referências de forma correta, entre outros detalhes cruciais para uso adequado do material licenciado.