Inhibitory effect of nisin-producing Lactococcus lactis on survival of Listeria monocytogenes strains in ultra-filtered white cheese
Subject Areas : Food Science and Technology
S. R. Hamidi
1
,
S. Hanifian
2
1 - MSc Graduate in Food Science and Technology, Tabriz Branch, Islamic Azad University, Tabriz, Iran
2 - Associate Professor of Department of Food Science and Technology, Tabriz Branch, Islamic Azad University, Tabriz, Iran
Keywords: Nisin, Lactic acid bacteria, hlyA, Inoculation study,
Abstract :
Listeria monocytogenes (Lm) is an important foodborne pathogen that is of great importance in milk and its products. Despite the measures taken to eliminate and control Lm contamination in pasteurized milk products, but due to its high spread in the environment, there is a possibility of secondary contamination in products such as Ultra-filtered (UF) white cheese. This study aimed to investigate the inhibitory effect of nisin-producing Lactococcus lactis on Lm in Ultra-filtered white cheese. Ultra-filtrated and pasteurized cow's milk was inoculated with 3 Log CFU/g of standard or native strains of Lm and control and treatment (containing nisin-producing L. lactis) cheese samples were manufactured. Changes in the population of Lm and nisin concentration were estimated throughout the storage period. According to the results, in all groups, the population of Lm began to decrease from day five onwards. Nonetheless, the decreasing trend in the treatment samples and in parallel with the production of nisin was significant (p < 0.01). The native strain of Lm was significantly (p < 0.01) more resistant than the standard one. Since the nisin-producing L. lactis, despite inhibiting Lm, did not negatively affect the growth of starter bacteria and the resulting pH decline of the cheese samples. Consequently, nisin-producing L. lactis can be used to control some bacterial contamination of the UF white cheese. It is also necessary to study the behavior of native strains isolated from food samples along with laboratory strains in inoculation studies.
References:
· Abdollahi, E. and Hanifian, S. (2016). Behavior of Yersinia enterocolitica in UF White Cheese: Impact of different storage temperatures on various strains. Journal of Food Safety, 36: 247–253.
· Adams, M., Ray, B. and Miller, K.W. (2003). Nisin in multifactorial food preservation, bacteriocin other than nisin: the pediocin-like cystibiotics of lactic acid bacteria, In: Roller, S. (Ed.). Natural Antimicrobials for the Minimal Processing of Foods. Woodhead Publishing Limited & CRC Press LLC, pp. 11, 64–77.
· Ahmadzadeh Nia, S. and Hanifian, S. (2017). Survival of Listeria monocytogenes strains in ultra‐filtered white cheese: Effect of Lactobacillus plantarum and incubation period. Journal of Food Processing and Preservation, 41(6): e13283.
· Benech, R.O., Kheadr, E.E., Laridi, R., Lacroix, C. and Fliss, I. (2002). Inhibition of Listeria innocua in cheddar cheese by addition of nisin Z in liposomes or by in situ production in mixed culture. Applied and Environmental Microbiology, 68(8): 3683-3690.
· Bergholz, T.M., Bowen, B., Wiedmann, M. and Boor, K.J. (2012). Listeria monocytogenes shows temperature-dependent and -independent responses to salt stress, including responses that induce cross-protection against other stresses. Applied and Environmental Microbiology, 78(8): 2602–2612.
· Cammi, G., Ricchi, M., Galiero, A., Daminelli, P., Cosciani-Cunico, E., Dalzini, E., et al. (2019). Evaluation of Mycobacterium avium subsp. paratuberculosis survival during the manufacturing process of Italian raw milk hard cheeses (Parmigiano Reggiano and Grana Padano). International Journal of Food Microbiology, 305: 108247.
· Castro, H., Ruusunen, M. and Lindström, M. (2017). Occurrence and growth of Listeria monocytogenes in packaged raw milk, International Journal of Food Microbiology, 261: 1–10.
· Chen, Y., Chen, M., Wang, J., Wu, Q., Cheng, J., Zhang, J. et al. (2020). Heterogeneity, characteristics, and public health implications of Listeria monocytogenes in ready-to-eat foods and pasteurized milk in China. Frontiers in Microbiology, 11: 642.
· Churchill, K.J., Sargeant, J.M., Farber, J.M. and O'Connor, A.M. (2019). Prevalence of Listeria monocytogenes in select ready-to-eat foods–deli meat, soft cheese, and packaged salad: a systematic review and meta-analysis. Journal of Food Protection, 82(2): 344–357.
· Cui, H.Y., Wu, J., Li, C.Z. and Lin, L. (2016). Anti-listeria effects of chitosan-coated nisin-silica liposome on Cheddar cheese. Journal of Dairy Science, 99(11): 8598–8606.
· Dal Bello, B., Cocolin, L., Zeppa, G., Field, D., Cotter, P.D. and Hill, C. (2012). Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in Cottage cheese. International Journal of Food Microbiology, 153(1-2): 58–65.
· Donaghy, J.A., Totton, N.L. and Rowe, M.T. (2004). Persistence of Mycobacterium paratuberculosis during manufacture and ripening of Cheddar cheese. Applied and Environmental Microbiology, 70: 4899–4905.
· Hanifian, S. (2014). Survival of Mycobacterium avium subsp. paratuberculosis in ultra-filtered white cheese. Letters in Applied Microbiology, 58(5): 466–471.
· Hanifian, S. (2020). Behavior of Mycobacterium avium paratuberculosis in Lighvan cheese tracked by propidium monoazide qPCR and culture. LWT, 133: 109886.
· Hanifian, S. and Jodeiri, H. (2013). Impact of salt concentration on persistence of Mycobacterium avium subsp. paratuberculosis in Iranian UF white cheese. Food Hygiene, 2(8): 1–14. [In Persian]
· Hanson, H., Whitfield, Y., Lee, C., Badiani, T., Minielly, C., Fenik, J. et al., (2019). Listeria monocytogenes associated with pasteurized chocolate milk, Ontario, Canada. Emerging Infectious Diseases. 25(3): 581–584.
· Institute of Standards and Industrial Research of Iran. (ISIRI), (1993). Cheese in brine: Specifications & test methods. 1st edition, ISIRI No. 2344-1. [In Persian]
· Kalantaripour, A. and Hanifian, S. (2017). Listeria isolated from traditional cheeses of Tabriz area: Occurrence, diversity and phenotypic characteristics. Journal of Food Microbiology, 4(6): 83–96. [In Persian]
· Karami, M., Ehsani, M.R., Mousavi, S.M., Rezaie K. and Safari, M. (2009). Changes in the rheological properties of Iranian UF-Feta cheese during ripening. Food Chemistry, 112: 539–544.
· Koch, J., Dworak, R., Prager, R., Becker, B., Brockmann, S., Wicke, A. et al. (2010). Large listeriosis outbreak linked to cheese made from pasteurized milk, Germany, 2006-2007. Foodborne Pathogens and Disease, 7 (12): 1581–1584.
· Liu, D., Lawrence, M.L., Ainsworth, A.J. and Austin, F.W. (2005). Comparative assessment of acid, alkali and salt tolerance in Listeria monocytogenes virulent and avirulent strains. FEMS Microbiology Letters, 243(2): 373–378.
· Malheiros, P.D.S., Daroit, D.J. and Brandelli, A. (2012). Inhibition of Listeria monocytogenes in minas frescal cheese by free and nanovesicle-encapsulated nisin. Brazilian Journal of Microbiology, 43(4): 1414–1418.
· Matereke, L.T. and Okoh, A.I. (2020). Listeria monocytogenes virulence, antimicrobial resistance and environmental persistence: A Review. Pathogens, 9(7): 528.
· Mirzaei, H., Khosroshahi, A.G. and Karim, G. (2008). The microbiological and chemical quality of traditional Lighvan cheese (white cheese in brine) produced in Tabriz, Iran. Journal of Animal and Veterinary Advances, 7(12): 1594–1599.
· Mohammadi, K. and Hanifian, S. (2014). Growth and enterotoxin production of Staphylococcus aureus in Iranian ultra-filtered white cheese. International Journal of Dairy Technology, 68(1): 111–117.
· Mohammadi, K., Karim, G., Razavilar, V. and Hanifian, S. (2009). Study on the growth and survival of Escherichia coli O157:H7 during the manufacture and storage of Iranian white cheese in brine. Iranian Journal of Veterinary Research, 4(29): 346–351.
· Mohammadi, Kh. and Jodeiri, H. (2013). Effect of different concentrations of nisin on starter culture of model cheeses manufactured from ultrafiltrated milk. Food Hygiene, 3(1): 33–43. [In Persian]
· Penna, T.C.V., Jozala, A.F., Novaes, L.C.D.L., Pessoa, A. and Cholewa, O. (2005). Production of nisin by Lactococcus lactis in media with skimmed milk. Applied Biochemistry and Biotechnology, 122(1-3): 619–637.
· Pietrysiak, E., Smith, S. and Ganjyal, G.M. (2019). Food safety interventions to control Listeria monocytogenes in the fresh apple packing industry: a review. Comprehensive Reviews in Food Science and Food Safety, 18(6): 1705–1726.
· Stecchini, M.L., Aquili, V. and Sarais, I. (1995). Behavior of Listeria monocytogenes in Mozzarella cheese in presence of Lactococcus lactis. International Journal of Food Microbiology, 25(3): 301–310.
· Swetha, C.S., Madhava Rao, T., Krishnaiah, N. and Vijaya Kumar, A. (2012). Detection of Listeria monocytogenes in fish samples by PCR assay. Annals of Biological Research, 3: 1880–1884.
· Thomas, L.V. and Wimpenny, J.W. (1996). Investigation of the effect of combined variations in temperature, pH, and NaCl concentration on nisin inhibition of Listeria monocytogenes and Staphylococcus aureus. Applied and Environmental Microbiology, 62: 2006–2012.
· Tirloni, E., Bernardi, C., Pomilio, F., Torresi, M., De Santis, E.P., Scarano, C. et al. (2020). Occurrence of Listeria spp. and Listeria monocytogenes isolated from PDO Taleggio production plants. Foods, 9(11): 1636.
· Vaseghi Bakhshayesh, V. and Hanifian, S. (2015). Behavior of various strains of Yersinia enterocolitica in Ultra-filtered cheese and inhibitory effect of lactic starter bacteria. Food Hygiene, 5(17): 13–26. [In Persian]
· Zaerzadeh, E., Mortazavi, S.A., Jafari, M.R., Afsharnejad, S. Tabatabaii, F. and Nassiri Mahallati, M. (2011). Antibacterial effect of nano-encapsulated nisin in liposoms in contrast to free nisin in control of Listeria monocytogenes in Iranian feta cheese (uf). Iranian Food Science and Technology Research Journal, 7(3): 191–199. [In Persian]
· Zafar, N., Nawaz, Z., Anam, S., Kanwar, R., Ali, A., Mudassar, M. et al. (2020). 31. Prevalence, molecular characterization and antibiogram study of Listeria monocytogenes isolated from raw milk and milk products. Pure and Applied Biology (PAB), 9(3): 1982–1987.
· Zhao, X., Chen, L., Wu, J.E., He, Y. and Yang, H. (2020). Elucidating antimicrobial mechanism of nisin and grape seed extract against Listeria monocytogenes in broth and on shrimp through NMR-based metabolomics approach. International Journal of Food Microbiology, 319: 108494.
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· Abdollahi, E. and Hanifian, S. (2016). Behavior of Yersinia enterocolitica in UF White Cheese: Impact of different storage temperatures on various strains. Journal of Food Safety, 36: 247–253.
· Adams, M., Ray, B. and Miller, K.W. (2003). Nisin in multifactorial food preservation, bacteriocin other than nisin: the pediocin-like cystibiotics of lactic acid bacteria, In: Roller, S. (Ed.). Natural Antimicrobials for the Minimal Processing of Foods. Woodhead Publishing Limited & CRC Press LLC, pp. 11, 64–77.
· Ahmadzadeh Nia, S. and Hanifian, S. (2017). Survival of Listeria monocytogenes strains in ultra‐filtered white cheese: Effect of Lactobacillus plantarum and incubation period. Journal of Food Processing and Preservation, 41(6): e13283.
· Benech, R.O., Kheadr, E.E., Laridi, R., Lacroix, C. and Fliss, I. (2002). Inhibition of Listeria innocua in cheddar cheese by addition of nisin Z in liposomes or by in situ production in mixed culture. Applied and Environmental Microbiology, 68(8): 3683-3690.
· Bergholz, T.M., Bowen, B., Wiedmann, M. and Boor, K.J. (2012). Listeria monocytogenes shows temperature-dependent and -independent responses to salt stress, including responses that induce cross-protection against other stresses. Applied and Environmental Microbiology, 78(8): 2602–2612.
· Cammi, G., Ricchi, M., Galiero, A., Daminelli, P., Cosciani-Cunico, E., Dalzini, E., et al. (2019). Evaluation of Mycobacterium avium subsp. paratuberculosis survival during the manufacturing process of Italian raw milk hard cheeses (Parmigiano Reggiano and Grana Padano). International Journal of Food Microbiology, 305: 108247.
· Castro, H., Ruusunen, M. and Lindström, M. (2017). Occurrence and growth of Listeria monocytogenes in packaged raw milk, International Journal of Food Microbiology, 261: 1–10.
· Chen, Y., Chen, M., Wang, J., Wu, Q., Cheng, J., Zhang, J. et al. (2020). Heterogeneity, characteristics, and public health implications of Listeria monocytogenes in ready-to-eat foods and pasteurized milk in China. Frontiers in Microbiology, 11: 642.
· Churchill, K.J., Sargeant, J.M., Farber, J.M. and O'Connor, A.M. (2019). Prevalence of Listeria monocytogenes in select ready-to-eat foods–deli meat, soft cheese, and packaged salad: a systematic review and meta-analysis. Journal of Food Protection, 82(2): 344–357.
· Cui, H.Y., Wu, J., Li, C.Z. and Lin, L. (2016). Anti-listeria effects of chitosan-coated nisin-silica liposome on Cheddar cheese. Journal of Dairy Science, 99(11): 8598–8606.
· Dal Bello, B., Cocolin, L., Zeppa, G., Field, D., Cotter, P.D. and Hill, C. (2012). Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in Cottage cheese. International Journal of Food Microbiology, 153(1-2): 58–65.
· Donaghy, J.A., Totton, N.L. and Rowe, M.T. (2004). Persistence of Mycobacterium paratuberculosis during manufacture and ripening of Cheddar cheese. Applied and Environmental Microbiology, 70: 4899–4905.
· Hanifian, S. (2014). Survival of Mycobacterium avium subsp. paratuberculosis in ultra-filtered white cheese. Letters in Applied Microbiology, 58(5): 466–471.
· Hanifian, S. (2020). Behavior of Mycobacterium avium paratuberculosis in Lighvan cheese tracked by propidium monoazide qPCR and culture. LWT, 133: 109886.
· Hanifian, S. and Jodeiri, H. (2013). Impact of salt concentration on persistence of Mycobacterium avium subsp. paratuberculosis in Iranian UF white cheese. Food Hygiene, 2(8): 1–14. [In Persian]
· Hanson, H., Whitfield, Y., Lee, C., Badiani, T., Minielly, C., Fenik, J. et al., (2019). Listeria monocytogenes associated with pasteurized chocolate milk, Ontario, Canada. Emerging Infectious Diseases. 25(3): 581–584.
· Institute of Standards and Industrial Research of Iran. (ISIRI), (1993). Cheese in brine: Specifications & test methods. 1st edition, ISIRI No. 2344-1. [In Persian]
· Kalantaripour, A. and Hanifian, S. (2017). Listeria isolated from traditional cheeses of Tabriz area: Occurrence, diversity and phenotypic characteristics. Journal of Food Microbiology, 4(6): 83–96. [In Persian]
· Karami, M., Ehsani, M.R., Mousavi, S.M., Rezaie K. and Safari, M. (2009). Changes in the rheological properties of Iranian UF-Feta cheese during ripening. Food Chemistry, 112: 539–544.
· Koch, J., Dworak, R., Prager, R., Becker, B., Brockmann, S., Wicke, A. et al. (2010). Large listeriosis outbreak linked to cheese made from pasteurized milk, Germany, 2006-2007. Foodborne Pathogens and Disease, 7 (12): 1581–1584.
· Liu, D., Lawrence, M.L., Ainsworth, A.J. and Austin, F.W. (2005). Comparative assessment of acid, alkali and salt tolerance in Listeria monocytogenes virulent and avirulent strains. FEMS Microbiology Letters, 243(2): 373–378.
· Malheiros, P.D.S., Daroit, D.J. and Brandelli, A. (2012). Inhibition of Listeria monocytogenes in minas frescal cheese by free and nanovesicle-encapsulated nisin. Brazilian Journal of Microbiology, 43(4): 1414–1418.
· Matereke, L.T. and Okoh, A.I. (2020). Listeria monocytogenes virulence, antimicrobial resistance and environmental persistence: A Review. Pathogens, 9(7): 528.
· Mirzaei, H., Khosroshahi, A.G. and Karim, G. (2008). The microbiological and chemical quality of traditional Lighvan cheese (white cheese in brine) produced in Tabriz, Iran. Journal of Animal and Veterinary Advances, 7(12): 1594–1599.
· Mohammadi, K. and Hanifian, S. (2014). Growth and enterotoxin production of Staphylococcus aureus in Iranian ultra-filtered white cheese. International Journal of Dairy Technology, 68(1): 111–117.
· Mohammadi, K., Karim, G., Razavilar, V. and Hanifian, S. (2009). Study on the growth and survival of Escherichia coli O157:H7 during the manufacture and storage of Iranian white cheese in brine. Iranian Journal of Veterinary Research, 4(29): 346–351.
· Mohammadi, Kh. and Jodeiri, H. (2013). Effect of different concentrations of nisin on starter culture of model cheeses manufactured from ultrafiltrated milk. Food Hygiene, 3(1): 33–43. [In Persian]
· Penna, T.C.V., Jozala, A.F., Novaes, L.C.D.L., Pessoa, A. and Cholewa, O. (2005). Production of nisin by Lactococcus lactis in media with skimmed milk. Applied Biochemistry and Biotechnology, 122(1-3): 619–637.
· Pietrysiak, E., Smith, S. and Ganjyal, G.M. (2019). Food safety interventions to control Listeria monocytogenes in the fresh apple packing industry: a review. Comprehensive Reviews in Food Science and Food Safety, 18(6): 1705–1726.
· Stecchini, M.L., Aquili, V. and Sarais, I. (1995). Behavior of Listeria monocytogenes in Mozzarella cheese in presence of Lactococcus lactis. International Journal of Food Microbiology, 25(3): 301–310.
· Swetha, C.S., Madhava Rao, T., Krishnaiah, N. and Vijaya Kumar, A. (2012). Detection of Listeria monocytogenes in fish samples by PCR assay. Annals of Biological Research, 3: 1880–1884.
· Thomas, L.V. and Wimpenny, J.W. (1996). Investigation of the effect of combined variations in temperature, pH, and NaCl concentration on nisin inhibition of Listeria monocytogenes and Staphylococcus aureus. Applied and Environmental Microbiology, 62: 2006–2012.
· Tirloni, E., Bernardi, C., Pomilio, F., Torresi, M., De Santis, E.P., Scarano, C. et al. (2020). Occurrence of Listeria spp. and Listeria monocytogenes isolated from PDO Taleggio production plants. Foods, 9(11): 1636.
· Vaseghi Bakhshayesh, V. and Hanifian, S. (2015). Behavior of various strains of Yersinia enterocolitica in Ultra-filtered cheese and inhibitory effect of lactic starter bacteria. Food Hygiene, 5(17): 13–26. [In Persian]
· Zaerzadeh, E., Mortazavi, S.A., Jafari, M.R., Afsharnejad, S. Tabatabaii, F. and Nassiri Mahallati, M. (2011). Antibacterial effect of nano-encapsulated nisin in liposoms in contrast to free nisin in control of Listeria monocytogenes in Iranian feta cheese (uf). Iranian Food Science and Technology Research Journal, 7(3): 191–199. [In Persian]
· Zafar, N., Nawaz, Z., Anam, S., Kanwar, R., Ali, A., Mudassar, M. et al. (2020). 31. Prevalence, molecular characterization and antibiogram study of Listeria monocytogenes isolated from raw milk and milk products. Pure and Applied Biology (PAB), 9(3): 1982–1987.
· Zhao, X., Chen, L., Wu, J.E., He, Y. and Yang, H. (2020). Elucidating antimicrobial mechanism of nisin and grape seed extract against Listeria monocytogenes in broth and on shrimp through NMR-based metabolomics approach. International Journal of Food Microbiology, 319: 108494.
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