Increasing the shelf life of minced chicken using two Lactobacillus species and EDTA
Subject Areas : Food Science and Technologyfariba zeynali 1 , ندا علی عباسی 2 , جواد علی اکبرلو 3
1 - Associate Professor, Department of Food Science and Technology, Faculty of Agriculture, Urmia University-Iran
2 - دانشجوی دانشگاه ارومیه
3 - دانشیار دانشکده دامپزشکی دانشگاه ارومیه
Keywords: EDTA, Chicken Meat, Lactobacillus,
Abstract :
Lactobacilli are known to have an inhibitory effect on the growth of a wide range of food spoilage and foodborne pathogens. The present study was conducted to evaluate the combined effect of Lactobacillus acidophilus + Lactobacillus plantarum (5 logs cfu/g) and also the combined effect of Lactobacillus plus EDTA (50 mM) on the shelf life of chicken breast meat. Treatments were grouped into the following: 1. without Lactobacillus and EDTA (C); 2. with Lactobacillus without EDTA (AP); 3. with Lactobacillus and EDTA (APE). Samples were stored at 4 ± 1°C and evaluated periodically for microbial counts (aerobic mesophilic count, coliform count and psychrotrophic count). Microbial analysis indicated that using of Lactobacillus species and Lactobacillus + EDTA had significant effects (p<0.05) in reducing the mesophilic, coliform and psychrotrophic counts, with the at least 1day extension of shelf life. Treatments with Lactobacillus species and Lactobacillus + EDTA showed lower pH values than the control sample. The results showed that application of Lactobacillus + EDTA in compared with the combined Lactobacillus species had more effect in reducing the growth of spoilage bacteria during refrigerated storage.
References:
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· Anang, D., Rusul, G., Bakar, J. and Ling, F. (2007). Effects of lactic acid and lauricidin on the survival of Listeria monocytogenes, Salmonella enteritidis and Escherichia coli O157: H7 in chicken breast stored at 4±1 °C. Food Control, 18: 961-969.
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· Atefyekta, M., Verdonck, F., Van Den Broeck, W., Goddeeris, B.M., Cox, E. and Vanrompay, D. (2010). Lactoferrin inhibits E. coli O157:H7 growth and attachment to intestinal epithelial cells. Veterinární Medicína, 55: 359–368.
· Belfiore, C., Castellano, P. and Vignolo, G. (2007). Reduction of Escherichia coli population following treatment with bacteriocins from lactic acid bacteria and chelators. Food Microbiology, 24: 223–229.
· Biscola, V., Abriouel, H., Todorov, S.D., Capuano, V.S.C., Gálvez, A. and de Melo Franco, B.D.G. (2014). Effect of autochthonous bacteriocin-producing Lactococcus lactis on bacterial population dynamics and growth of halotolerant bacteria in Brazilian charqui. Food Microbiology, 44: 296–301.
· Bomdespacho, L.Q., Cavallini, D.C.U., Zavarizi, A.C.M., Pinto, R.A. and Rossi, E.A. (2014). Evaluation of the use of probiotic acid lactic bacteria in the development of chicken hamburger. International Food Research Journal, 21(3): 965–972.
· Brashears, M.M., Reilly, S.S. and Gilliland, S.E. (1998) Antagonistic action of cells of Lactobacillus lactis toward Escherichia coli O157:H7 on refrigerated raw chicken meat. Journal of Food Protection, 61: 166–170.
· Buncic, S., Nychas, G.J., Lee, M.R.F., Koutsoumanis, K., Hébraud, M., Desvaux, M. and Antic D. (2014). Microbial pathogen control in the beef chain: recent research advances. Meat Science, 97(3): 288–297.
· Caplice, E. and Fizgernald, G.F. (1999). Food fermentation: role of microorganisms in food production and preservation. International Journal of Food Microbiology, 50: 131–194.
· Casaburi, A., Piombino, P., Nychas, G.J., Villani, F. and Ercolini, D. (2015). Bacterial population and the voatilome associated to meat spoilage. Food Microbiology, 45, 85–103.
· Casaburi, A., Di Martino, V., Ferranti, P., Picariello, L. and Villani, F. (2016). Technologic properties and bacteriocins production by Lactobacillus curvatus 54M16 and its use as starter culture for fermented sausage manufacture. Food Control, 59: 31–45.
· Castellano, P., Belfiore, C., Fadda, S. and Vignolo, G. (2008). A review of bacteriocinogenic lactic acid bacteria used as bioprotective cultures in fresh meat produced in Argentina. Meat Science, 79: 483–499.
· Castro, M.P., Palavecino, N.Z., Herman, C., Garro, O.A. and Campo, C.A. (2011). Lactic acid bacteria isolated from artisanal dry sausages: Characterization of antibacterial compounds and study of the factors affecting bacteriocin production. Meat Science, 87: 321–329.
· Deegan, L.H., Cotter, P.D., Hill, C. and Ross, P. (2006). Bacteriocin: biological tools for biopreservation and shelf-life extension. International Dairy Journal, 16: 1058–1071.
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· Etemadian, Y., Shabanpour, B., Mahonak, A. and Yahyai, A. (2011). Effect of vacuum packaging on chemical, microbial and sensorial properties of white fish lion. Iranian Journal of Food Science and Technology, 7(4): 298–304.
· Fadda, S., Chambon, M.C., Champomier-Verge`s, R., Talon, C. and Vignolo, G. (2008). Lactobacillus role during conditioning of refrigerated and vacuum-packaged Argentinean meat. Meat Science, 79: 603–610.
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· Gonzalez-Fandos, E. and Dominguez, J.L. (2006). Efficacy of lactic acid against Listeria monocytogenes attached to poultry skin during refrigerated storage. Journal of Applied Microbiology, 101: 1331–1339.
· Hancock, R. and Rozek, A. (2002). Role of membranes in the activities of antibacterial cationic peptides. FEMS Microbiology Letters, 206: 143–149.
· Hasapidou, A. and Savvaidis, I.N. (2011). The effects of modified atmosphere packaging, EDTA and oregano oil on the quality of chicken liver meat. Food Research International, 44: 2751–2756.
· ICMFS (International Commission on Microbiological Specifications for Foods), (1986). 2nd ed., Sampling for Microbiological Analysis: Principles and Scientific Applications, Vol. 2, University of Toronto Press.
· Ismail, S.A.S., Deak, T., Abd El-Rahman, H.A., Yassien, M.A.M. and Beuchat, L.R. (2000). Presence and changes in populations of yeasts on raw and processed poultry products stored at refrigeration temperature. International Journal of Food Microbiology, 62(12): 113–121.
· ISO (International Organization for Standardization), (2004). No. 11291-1. Microbiology of Food and Animal Feeding Stuffs-Horizontal Methods for Detection and Enumeration of Enterobacteriaceae part (2): colony count method.
· Ivanović S., Baltić M., Sinovec Z. and Stojanović, Z. (2005). Probiotic influence on acid number, acid degree and fatty acid content in chicken abdominal fatty tissue. Biotechnology and Animal Husbandry, 21(5-6): 129-133.
· Jeevaratnam, K., Jamuna, M. and Bawa, A.S. (2005). Biological preservation of foods-bacteriocins of lactic acid bacteria. Indian Journal of Biotechnology, 4: 446–454.
· Keokamnerd, T., Acton, J. C., Han, I. Y., & Dawson, P. L. (2008). Effect of commercial rosemary oleoresin preparations on ground chicken thigh meat quality packaged in a high-oxygen atmosphere. Poultry Science, 87, 170–179.
· Kilinc, B., Cakli, S., Dincer, T. and Cadun, A. (2007). Effects of phosphates treatment on the quality of frozen-thawed fish species. Journal of Muscle Foods, 20, 377–391.
· Koch, A.G. (2004). Biopreservation, In: Jensen W.K., editor. Encyclopedia of Meat Sciences. Elsevier Ltd.; 2004. p. 68–74.
· Lambert, A.D., Smith, J.P., and Dodds, K.L. (1991). Shelf life extension and microbiological safety of fresh meat. A review. Food Microbiology, 9: 267-297.
· Latou, E., Mexis, S.F., Badeka, A.V., Kontakos, S. and Kontominas, M.G. (2014). Combined effect of chitosan and modified atmosphere packaging for shelf life extension of chicken breast fillets, LWT - Food Science and Technology, 55(1): 263-268.
· Leroi, F., (2010). Occurrence and role of lactic acid bacteria in seafood products. Food Microbiology, 27: 698-709.
· Makras, L., Triantafyllou, V., Fayol-Messaoudi, D., Adriany, T., Zoumpopoulou, G., Tsakalidou, E. et al. (2006). Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Research in Microbiology, 157: 241-247.
· Maragkoudakis, P.E., Mountzouris, K.C., Psyrras, D., Cremonese, S., Fischer, J., Cantor, MD, et al. (2009). Functional properties of novel protective lactic acid bacteria and application in raw chicken meat against Listeria monocytogenes and Salmonella enteritidis. International Journal of Food Microbiology, 130: 219-226.
· Martinez, F.A.C., Balciunas, E.M., Converti, A., Cotter, P.D. and Oliveira, R.P.S. (2013). Bacteriocin production by Bifidobacterium spp.: A review. Biotechnology Advances, 31: 482–488.
· Masniyom, P., Soottawat, B. and Visessanguan, W. (2005). Combination effect of phosphate and modified atmosphere on quality and shelf-life extension of refrigerated seabass slices. Journal of Food Science and Technology, 38: 745-756.
· Mead, P.S. and Griffin, P.G. (1998). Escherichia coli O: H. The Lancet, pp: 352.
· Mexis, S. F; Chouliara, E., Kontominas, M.G. (2012). Shelf life extension of ground chicken meat using an oxygen absorber and a citrus extract. Food Science and Technology, 49(2012): 21-27.
· Murthy, T.R.K., Rao, V.K. and Natarajan, C. (1997). Effect of Lactococcus lactis var lactis bivar, diacetylactis on bacterial counts, pH and total acidity of minced goat meat during refrigerated storage. Meat Science, 47: 231-236.
· Muthukumarasamy, P., Han, J.H. and Holley, R.A. (2003). Bactericidal effects of Lactobacillus reuteri and allyl isothiocyanate on Escherichia coli O157:H7 in refrigerated ground beef. Journal of Food Protection, 66(11): 2038-2044.
· Naidu, A.S. (2002). Activated lactoferrin-a new approach to meat safety. Food Technology, 56: 40–45.
· Neetoo, H., Ye, M., Chen, H., Joerger, R.D., Hicksand D.T. and Hoover, D.G. (2007). Use of nisin-coated plasticfilms to control Listeria monocytogenes on vacuum-packaged cold-smoked salmon. International Journal Food Microbiology, 29(122): 8-15.
· Patricia, C., Belfiore, C. and Vignolo, G. (2011).Combination of bioprotective cultures with EDTA to reduce Escherichia coli O157:H7 in frozen ground-beef patties. Food Control, 22: 1461-1465.
· Yethon, J. and Whitfield, C. (2001). Lipopolysaccharide as a target for the development of novel therapeutics in Gram-negative bacteria. Current Drug Targets. Infections. Disorders, 1: 91–106.
· Zendo, T. (2013). Screening and characterization of novel bacteriocins from lactic acid bacteria. Bioscience, Biotechnology, and Biochemistry, 77: 893-899.
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· Alakomi, H., Saarela, M. and Helander, J. (2003). Effect of EDTA on Salmonella enterica serovar Typhimurium involves a component not assignable to lipopolysaccharide release. Microbiology 149: 2015–2021.
· Amani, M.S. (2012). Bio-Preservation challenge for shelf-life and safety improvement of minced beef .Global Journal of Biotechnology and Biochemistry 7 (2): 50-60.
· Anang, D., Rusul, G., Bakar, J. and Ling, F. (2007). Effects of lactic acid and lauricidin on the survival of Listeria monocytogenes, Salmonella enteritidis and Escherichia coli O157: H7 in chicken breast stored at 4±1 °C. Food Control, 18: 961-969.
· Arashisar, S., Hisar, O., Kaya, M. and Yanik, T. (2004). Effects of modified atmosphere and vacuum packaging on microbiological and chemical properties of rainbow trout (Oncorhynchus mykiss) fillets. Journal of Food Microbiology, 97: 209-214.
· Atefyekta, M., Verdonck, F., Van Den Broeck, W., Goddeeris, B.M., Cox, E. and Vanrompay, D. (2010). Lactoferrin inhibits E. coli O157:H7 growth and attachment to intestinal epithelial cells. Veterinární Medicína, 55: 359–368.
· Belfiore, C., Castellano, P. and Vignolo, G. (2007). Reduction of Escherichia coli population following treatment with bacteriocins from lactic acid bacteria and chelators. Food Microbiology, 24: 223–229.
· Biscola, V., Abriouel, H., Todorov, S.D., Capuano, V.S.C., Gálvez, A. and de Melo Franco, B.D.G. (2014). Effect of autochthonous bacteriocin-producing Lactococcus lactis on bacterial population dynamics and growth of halotolerant bacteria in Brazilian charqui. Food Microbiology, 44: 296–301.
· Bomdespacho, L.Q., Cavallini, D.C.U., Zavarizi, A.C.M., Pinto, R.A. and Rossi, E.A. (2014). Evaluation of the use of probiotic acid lactic bacteria in the development of chicken hamburger. International Food Research Journal, 21(3): 965–972.
· Brashears, M.M., Reilly, S.S. and Gilliland, S.E. (1998) Antagonistic action of cells of Lactobacillus lactis toward Escherichia coli O157:H7 on refrigerated raw chicken meat. Journal of Food Protection, 61: 166–170.
· Buncic, S., Nychas, G.J., Lee, M.R.F., Koutsoumanis, K., Hébraud, M., Desvaux, M. and Antic D. (2014). Microbial pathogen control in the beef chain: recent research advances. Meat Science, 97(3): 288–297.
· Caplice, E. and Fizgernald, G.F. (1999). Food fermentation: role of microorganisms in food production and preservation. International Journal of Food Microbiology, 50: 131–194.
· Casaburi, A., Piombino, P., Nychas, G.J., Villani, F. and Ercolini, D. (2015). Bacterial population and the voatilome associated to meat spoilage. Food Microbiology, 45, 85–103.
· Casaburi, A., Di Martino, V., Ferranti, P., Picariello, L. and Villani, F. (2016). Technologic properties and bacteriocins production by Lactobacillus curvatus 54M16 and its use as starter culture for fermented sausage manufacture. Food Control, 59: 31–45.
· Castellano, P., Belfiore, C., Fadda, S. and Vignolo, G. (2008). A review of bacteriocinogenic lactic acid bacteria used as bioprotective cultures in fresh meat produced in Argentina. Meat Science, 79: 483–499.
· Castro, M.P., Palavecino, N.Z., Herman, C., Garro, O.A. and Campo, C.A. (2011). Lactic acid bacteria isolated from artisanal dry sausages: Characterization of antibacterial compounds and study of the factors affecting bacteriocin production. Meat Science, 87: 321–329.
· Deegan, L.H., Cotter, P.D., Hill, C. and Ross, P. (2006). Bacteriocin: biological tools for biopreservation and shelf-life extension. International Dairy Journal, 16: 1058–1071.
· Dorn, P., Krabisch, P. and Gehra, H. (1989). Investigations on Salmonella decontamination of broiler carcasses. Archiv fur Geflugelkunde, 53: 123–134.
· Economou, T.N., Pournis, A. and Ntzimani, I.N.S. (2009). Nisin–EDTA treatments and modified atmosphere packaging to increase fresh chicken meat shelf-life. Food Chemistry, 114: 1470–1476.
· Etemadian, Y., Shabanpour, B., Mahonak, A. and Yahyai, A. (2011). Effect of vacuum packaging on chemical, microbial and sensorial properties of white fish lion. Iranian Journal of Food Science and Technology, 7(4): 298–304.
· Fadda, S., Chambon, M.C., Champomier-Verge`s, R., Talon, C. and Vignolo, G. (2008). Lactobacillus role during conditioning of refrigerated and vacuum-packaged Argentinean meat. Meat Science, 79: 603–610.
· FDA (Food and Drug Administration), (2001). Bacteriological Analytical Manual. Online.
· Givens, D.I. (2005). The role of animal nutrition in improving the nutritive value of animal-derived foods value of animal-derived foods in relation to chronic disease. Proceedings of the Nutrition Society, 64: 395–402.
· Gonzalez-Fandos, E. and Dominguez, J.L. (2006). Efficacy of lactic acid against Listeria monocytogenes attached to poultry skin during refrigerated storage. Journal of Applied Microbiology, 101: 1331–1339.
· Hancock, R. and Rozek, A. (2002). Role of membranes in the activities of antibacterial cationic peptides. FEMS Microbiology Letters, 206: 143–149.
· Hasapidou, A. and Savvaidis, I.N. (2011). The effects of modified atmosphere packaging, EDTA and oregano oil on the quality of chicken liver meat. Food Research International, 44: 2751–2756.
· ICMFS (International Commission on Microbiological Specifications for Foods), (1986). 2nd ed., Sampling for Microbiological Analysis: Principles and Scientific Applications, Vol. 2, University of Toronto Press.
· Ismail, S.A.S., Deak, T., Abd El-Rahman, H.A., Yassien, M.A.M. and Beuchat, L.R. (2000). Presence and changes in populations of yeasts on raw and processed poultry products stored at refrigeration temperature. International Journal of Food Microbiology, 62(12): 113–121.
· ISO (International Organization for Standardization), (2004). No. 11291-1. Microbiology of Food and Animal Feeding Stuffs-Horizontal Methods for Detection and Enumeration of Enterobacteriaceae part (2): colony count method.
· Ivanović S., Baltić M., Sinovec Z. and Stojanović, Z. (2005). Probiotic influence on acid number, acid degree and fatty acid content in chicken abdominal fatty tissue. Biotechnology and Animal Husbandry, 21(5-6): 129-133.
· Jeevaratnam, K., Jamuna, M. and Bawa, A.S. (2005). Biological preservation of foods-bacteriocins of lactic acid bacteria. Indian Journal of Biotechnology, 4: 446–454.
· Keokamnerd, T., Acton, J. C., Han, I. Y., & Dawson, P. L. (2008). Effect of commercial rosemary oleoresin preparations on ground chicken thigh meat quality packaged in a high-oxygen atmosphere. Poultry Science, 87, 170–179.
· Kilinc, B., Cakli, S., Dincer, T. and Cadun, A. (2007). Effects of phosphates treatment on the quality of frozen-thawed fish species. Journal of Muscle Foods, 20, 377–391.
· Koch, A.G. (2004). Biopreservation, In: Jensen W.K., editor. Encyclopedia of Meat Sciences. Elsevier Ltd.; 2004. p. 68–74.
· Lambert, A.D., Smith, J.P., and Dodds, K.L. (1991). Shelf life extension and microbiological safety of fresh meat. A review. Food Microbiology, 9: 267-297.
· Latou, E., Mexis, S.F., Badeka, A.V., Kontakos, S. and Kontominas, M.G. (2014). Combined effect of chitosan and modified atmosphere packaging for shelf life extension of chicken breast fillets, LWT - Food Science and Technology, 55(1): 263-268.
· Leroi, F., (2010). Occurrence and role of lactic acid bacteria in seafood products. Food Microbiology, 27: 698-709.
· Makras, L., Triantafyllou, V., Fayol-Messaoudi, D., Adriany, T., Zoumpopoulou, G., Tsakalidou, E. et al. (2006). Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Research in Microbiology, 157: 241-247.
· Maragkoudakis, P.E., Mountzouris, K.C., Psyrras, D., Cremonese, S., Fischer, J., Cantor, MD, et al. (2009). Functional properties of novel protective lactic acid bacteria and application in raw chicken meat against Listeria monocytogenes and Salmonella enteritidis. International Journal of Food Microbiology, 130: 219-226.
· Martinez, F.A.C., Balciunas, E.M., Converti, A., Cotter, P.D. and Oliveira, R.P.S. (2013). Bacteriocin production by Bifidobacterium spp.: A review. Biotechnology Advances, 31: 482–488.
· Masniyom, P., Soottawat, B. and Visessanguan, W. (2005). Combination effect of phosphate and modified atmosphere on quality and shelf-life extension of refrigerated seabass slices. Journal of Food Science and Technology, 38: 745-756.
· Mead, P.S. and Griffin, P.G. (1998). Escherichia coli O: H. The Lancet, pp: 352.
· Mexis, S. F; Chouliara, E., Kontominas, M.G. (2012). Shelf life extension of ground chicken meat using an oxygen absorber and a citrus extract. Food Science and Technology, 49(2012): 21-27.
· Murthy, T.R.K., Rao, V.K. and Natarajan, C. (1997). Effect of Lactococcus lactis var lactis bivar, diacetylactis on bacterial counts, pH and total acidity of minced goat meat during refrigerated storage. Meat Science, 47: 231-236.
· Muthukumarasamy, P., Han, J.H. and Holley, R.A. (2003). Bactericidal effects of Lactobacillus reuteri and allyl isothiocyanate on Escherichia coli O157:H7 in refrigerated ground beef. Journal of Food Protection, 66(11): 2038-2044.
· Naidu, A.S. (2002). Activated lactoferrin-a new approach to meat safety. Food Technology, 56: 40–45.
· Neetoo, H., Ye, M., Chen, H., Joerger, R.D., Hicksand D.T. and Hoover, D.G. (2007). Use of nisin-coated plasticfilms to control Listeria monocytogenes on vacuum-packaged cold-smoked salmon. International Journal Food Microbiology, 29(122): 8-15.
· Patricia, C., Belfiore, C. and Vignolo, G. (2011).Combination of bioprotective cultures with EDTA to reduce Escherichia coli O157:H7 in frozen ground-beef patties. Food Control, 22: 1461-1465.
· Yethon, J. and Whitfield, C. (2001). Lipopolysaccharide as a target for the development of novel therapeutics in Gram-negative bacteria. Current Drug Targets. Infections. Disorders, 1: 91–106.
· Zendo, T. (2013). Screening and characterization of novel bacteriocins from lactic acid bacteria. Bioscience, Biotechnology, and Biochemistry, 77: 893-899.
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