Browse > Article
http://dx.doi.org/10.5851/kosfa.2013.33.3.395

The Effects of Sodium Chloride on the Physiological Characteristics of Listeria monocytogenes  

Choi, Kyoung-Hee (Department of Oral Microbiology, College of Dentistry, Wonkwang University)
Yoon, Yohan (Department of Food and Nutrition, Sookmyung Women's University)
Publication Information
Food Science of Animal Resources / v.33, no.3, 2013 , pp. 395-402 More about this Journal
Abstract
Sodium chloride is used to improve various properties of processed meat products, e.g., taste, preservation, water binding capacity, texture, meat batter viscosity, safety, and flavor; however, many studies have shown that sodium chloride increases the resistance of many foodborne pathogens to heat and acid. Listeria monocytogenes has been isolated from various readyto- eat (RTE) meat and dairy products formulated with sodium chloride; therefore, the objective of this paper was to review the effects of sodium chloride on the physiological characteristics of L. monocytogenes. The exposure of L. monocytogenes to sodium chloride may increase biofilm formation on foods or food contact surfaces, virulence gene transcription, invasion of Caco-2 cells, and bacteriocin production, depending on L. monocytogenes strain and serotype as well as sodium chloride concentration. When L. monocytogenes cells were exposed to sodium chloride, their resistance to UV-C irradiation and freezing temperatures increased, but sodium chloride had no effect on their resistance to gamma irradiation. The morphological properties of L. monocytogenes, especially cell elongation and filament formation, also change in response to sodium chloride. These findings indicate that sodium chloride affects various physiological responses of L. monocytogenes and thus, the effect of sodium chloride on L. monocytogenes in RTE meat and dairy products needs to be considered with respect to food safety. Moreover, further studies of microbial risk assessment should be conducted to suggest an appropriate sodium chloride concentration in animal origin foods.
Keywords
sodium chloride; L. monocytogenes; biofilm; stress response; resistance;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Yousef, A. E. and Marth, E. H. (1988) Inactivation of Listeria monocytogenes by ultraviolet energy. J. Food Sci. 53, 571-573.   DOI
2 Zaika, L. L. and Fanelli, J. S. (2003) Growth kinetics and cell morphology of Listeria monocytogenes Scott A as affected by temperature, NaCl, and EDTA. J. Food Prot. 66, 1208-1215.
3 Zarei, M., Khezizadeh, M., Kazemipour, S., Hesami, G., and Bemani, E. (2012) Growth and cell morphology of Listeria monocytogenes as affected by various concentrations of NaCl and KCl. J. Appl. Biol. Sci. 6, 55-58.
4 Sammarco, M. L., Ripabelli, G., Ruberto, A., Iannitto, G., and Grasso, G. M. (1997) Prevalence of Salmonellae, Listeriae, and Yersiniae in the slaughterhouse environment and on work surfaces, equipment, and workers. J. Food Prot. 60, 367-371.
5 Shadbolt, C., Ross, T., and McMeekin, T. A. (2001) Differentiation of the effects of lethal pH and water activity: Food safety implications. Lett. Appl. Microbiol. 32, 99-102.   DOI   ScienceOn
6 Skandamis, P. N., Stopforth, J. D., Yoon, Y., Kendall, P. A., and Sofos, J. N. (2009) Heat and acid tolerance responses of Listeria monocytogenes as affected by sequential exposure to hurdles during growth. J. Food Prot. 72, 1412-1418.
7 Skandamis, P. N., Yoon, Y., Stopforth, J. D., Kendall, P. A., and Sofos, J. N. (2008) Heat and acid tolerance of Listeria monocytogenes after exposure to single and multiple sublethal stresses. Food Microbiol. 25, 294-303.   DOI   ScienceOn
8 Sofos, J. N. (1993) Current microbiological considerations in food preservation. Int. J. Food Microbiol. 19, 87-108.   DOI   ScienceOn
9 Tarver, T. (2009) Biofilms a threat to food safety. Food Technol. 63, 46-52.
10 Harris, L. J., Fleming, H. P., and Klaenhammer, T. R. (1991) Sensitivity and resistance of Listeria monocytogenes ATCC 19115, Scott A, and UAL500 to nisin. J. Food Prot. 54, 834-840.
11 Hazeleger, W. C., Dalvoorde, M., and Beumer, R. R. (2006) Fluorescence microscopy of NaCl-stressed, elongated Salmonella and Listeria cells reveals the presence of septa in filaments. Int. J. Food Microbiol. 112, 288-290.   DOI   ScienceOn
12 Hill, C., Cotter, P. D., Sleator, R. D., and Gahan, C. G. M. (2002) Bacterial stress response in Listeria monocytogenes: Jumping the hurdles imposed by minimal processing. Int. Dairy J. 12, 273-283.   DOI   ScienceOn
13 Bouttefroy, A., Mansour, M., Linder, M., and Milliere, J.-B. (2000) Inhibitory combinations of nisin, sodium chloride, and pH on Listeria monocytogenes ATCC15313 in broth by an experimental design approach. Int. J. Food Microbiol. 54, 109-115.   DOI   ScienceOn
14 Boziaris, I. S., Skandamis, P. N., Anastasiadi, M., and Nychas, G.-J. E. (2007) Effect of NaCl and KCl on fate and growth/no growth interfaces of Listeria monocytogenes Scott A at different pH and nisin concentrations. J. Appl. Microbiol. 102, 796-805.   DOI   ScienceOn
15 Breslin, P. A. and Beauchamp, G. K. (1997) Salt enhances flavour by suppressing bitterness. Nature 387, 563.
16 Breuer, B. and Radler, F. (1996) Inducible resistance against nisin in Lactobacillus casei. Arch. Microbiol. 165, 114-118.   DOI
17 Breukink, E., Wiedemann, I., van Kraaij, C., Kuipers, O. P., Sahl, H. G., and de Kruiff, B. B. (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286, 2361-2364.   DOI   ScienceOn
18 Briggs, A. and Yazdany, S. (1970) Effect of sodium chloride on the heat and radiation resistance and on the recovery of heated or irradiated spores of the genus Bacillus. J. Appl. Microbiol. 33, 621-632.   DOI
19 Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakaraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J., and Kreft, J. (2001) Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14, 584-640.   DOI   ScienceOn
20 Vasseur, C., Baverel, L., Herbraud, M., and Labadie, J. (1999) Effect of osmotic alkaline, acid or thermal stresses on the growth and inhibition of Listeria monocytogenes. J. Appl. Microbiol. 86, 469-476.   DOI   ScienceOn
21 Vogel, B. F., Hansen, L. T., Mordhorst, H., and Gram, L. (2010) The survival of Listeria monocytogenes during long term desiccation is facilitated by sodium chloride and organic material. Int. J. Food Microbiol. 140, 192-200.   DOI   ScienceOn
22 Weis, J. and Seeliger, H. P. R. (1975) Incidence of Listeria monocytogenes in nature. Appl. Microbiol. 30, 29-32.
23 Welshimer, H. J. and Donker-Voet, J. (1971) Listeria monocytogenes in nature. Appl. Microbiol. 21, 516-519.
24 Wong, E., Linton, R. H., and Gerrard, D. E. (1998) Reduction of Escherichia coli and Salmonella Senftenberg on pork skin and pork muscle using ultraviolet light. Food Microbiol. 15, 415-423.   DOI   ScienceOn
25 Wulff, G., Gram, L., Ahrens, P., and Vogel, B. F. (2006) One group of genetically similar Listeria monocytogenes strains frequently dominate and persist in several fish slaughter and smokehouses. Appl. Environ. Microb. 72, 4313-4322.   DOI   ScienceOn
26 Yoon, Y., Kim, G., Nam, M., Shim, W.-B., Seo, E., Kim, J.- H., Lee, J.-W., Byun, M.-W., and Chung, D.-H. (2009) Effect of glucose on Listeria monocytogenes survival under sequential sublethal stresses of gamma irradiation and NaCl. Food Sci. Biotechnol. 18, 162-166.
27 Yoon, Y. and Sofos, J. N. (2008) Autoinducer-2 activity of gramnegative foodborne pathogenic bacteria and its influence on biofilm formation. J. Food Sci. 73, M140-M147.   DOI   ScienceOn
28 Chae, M. S. and Schraft, H. (2000) Comparative evaluation of adhesion and biofilm formation of different Listeria monocytogenes strains. Int. J. Food Microbiol. 62, 103-111.   DOI   ScienceOn
29 Buncic, S., Avery, S. M., Rocourt, J., and Dimitrijevic. (2001) Can food-related environmental factors induce different behaviour in two key serovars, 4b and 1/2a, of Listeria monocytogenes? Int. J. Food Microbiol. 65, 201-212.   DOI   ScienceOn
30 Caly, D., Takilt, D., Lebert, V., and Tresse, O. (2009) Sodium chloride affects Listeria monocytogenes adhesion to polystyrene and stainless steel by regulating flagella expression. Lett. Appl. Microbiol. 49, 751-756.   DOI   ScienceOn
31 Chavant, P., Martinie, B., Meylheuc, T., Bellon-Fontaine, M. N., and Hebraud, M. (2002) Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl. Environ. Microb. 68, 728-737.   DOI   ScienceOn
32 Conlon, K. M., Humphreys, H., and O'Gara, J. P. (2002) icaR encodes a transcriptional repressor involved in environmental regulations of ica operon expression and biofilm formation in Staphylococcus epidermidis. J. Bacteriol. 184, 4400-4408.   DOI
33 Conte, M. P., Peptrone, G., Di Biase, A. M., Ammendolia, M. G., Superti, F., and Seganti, L. (2000) Acid tolerance in Listeria monocytogenes influences invasiveness of enterocyte-like cells and macrophage-like cells. Microb. Pathog. 29, 137-144.   DOI   ScienceOn
34 Conte, M. P., Peptrone, G., Di Biase, A. M., Longhi, C., Penta, M., Tinari, A., Superti, F., Fabozzi, G., Visca, P., and Seganti, L. (2002) Effect of acid adaptation on the fate of Listeria monocytogenes in THP-1 human macrophages activated by gamma interferon. Infet. Immun. 70, 4369-4378.   DOI
35 Corry, J. E. L. (1974) The effect of sugrs and polyols on the heat resistance of salmonellae. J. Appl. Bacteriol. 37, 31-43.   DOI
36 Norwood, D. E. and Gilmour, A. (2001) The differential adherence capabilities of two Listeria monocytogenes strains in monoculture and multispecies biofilms as a function of temperature. Lett. Appl. Micrbiol. 33, 320-324.   DOI   ScienceOn
37 Myers, E. R., Dallmier, A. W., and Martin, S. E. (1993) Sodium chloride, potassium chloride, and virulence in Listeria monocytogenes. Appl. Environ. Microb. 59, 2082-2086.
38 Nadon, C., Bowen, B. M., Wiedmann, M., and Boor, K. J. (2002) ${\sigma}^B$ contributes to Prf-mediated virulence in Listeria monocytogenes. Infect. Immun. 70, 3948-3952.   DOI   ScienceOn
39 Navarre, W. W. and Schneewind, O. (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 63, 174-229.
40 Notermans, S., Dufrenne, J., Teunis, P., and Chackraborty. (1998) Studies on the risk assessment of Listeria monocytogenes. J. Food Prot. 61, 244-248.
41 Olesen, I., Thorsen, L., and Jespersen, L. (2010) Relative transcription of Listeria monocytogenes virulence genes in liver pates with varying NaCl content. Int. J. Food Microbiol. 141, S60-S68.   DOI   ScienceOn
42 Olesen, I., Vogensen, F. K., and Jespersen, L. (2009) Gene transcription and virulence potential of Listeria monocytogenes strains after exposure to acidic and NaCl stress. Foodborne Path. Dis. 6, 669-680.   DOI   ScienceOn
43 Pan, Y., Breidt, Jr., F., and Gorski, L. (2010) Synergistic effects of sodium chloride, glucose, and temperature on biofilm formation by Listeria monocytogenes serotype 1/2a and 4b strains. Appl. Environ. Microb. 76, 1433-1441.   DOI   ScienceOn
44 Pawar, D. D., Malik, S. V. S., Bhilegaonkar, K. N., and Barbuddhe, S. B. (2000) Effect of nisin and its combination with sodium chloride on the survival of Listeria monocytogenes added to raw buffalo meat mince. Meat. Sci. 56, 215-219.   DOI   ScienceOn
45 Bereksi, N., Gavini, F., Benezech, T., and Faille, C. (2002) Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. J. Appl. Microbiol. 92, 556-565.   DOI   ScienceOn
46 Abee, T. and Wouters, J. A. (1999) Microbial stress responses in minimal processing. Int. J. Food Microbiol. 50, 65-91.   DOI   ScienceOn
47 Bae, D., Liu, C., Zhang, T., Jones, M., Peterson, S. N., and Wang, C. (2012) Global gene expression of Listeria monocytogenes to salt stress. J. Food Prot. 75, 906-912.   DOI   ScienceOn
48 Ben Hammou, F., Skali, S. N., Idaomar, M., and J. Abrini. (2010) Combination of nisin with salt (NaCl) to control Listeria monocytogenes on sheep natural sausage casing stored at $6^{\circ}C$. Afr. J. Biotechnol. 9, 1190-1195.
49 Bernbom, N., Vogel, B. F., and Gram, L. (2011) Listeria monocytogenes survival of UV-C radiation is enhanced by presence of sodium chloride, organic food material and by bacterial biofilm formation. Int. J. Food Micrbiol. 147, 69-73.   DOI   ScienceOn
50 PHAC (Public Health Agency of Canada) (2008) Listeria monocytogenes outbreak. Availale at: http://web.archive.org/ web/20090207083151/http://www.phac-aspc.gc.ca/alert-alerte/ listeria/listeria_2008-eng.php. Accessed on June 11, 2013.
51 Recourt, J., Jacquet, C., and Reilly, A. (2000) Epidemiology of human listeriosis and seafoods. Int. J. Food Microbiol. 62, 197-209.   DOI   ScienceOn
52 Ryan, S., Hill, C., and Gahan, C. G. M. (2008) Acid stress response in Listeria monocytogenes. Adv. Appl. Microbiol. 65, 67-91.   DOI   ScienceOn
53 Rychlik, I. and Barrow, P. A. (2005) Salmonella stress management and its relevance to behaviour during intestinal colonization and infection. FEMS Microbiol. Rev. 29, 1021-1040.   DOI   ScienceOn
54 Samelis, J., Ikeda, J. S., and Sofos, J. N. (2003) Evaluation of the pH-dependent, stationary phases acid resistance of Listeria monocytogenes and Salmonella Typhimurium DT104 induced by culturing in media with 1% glucose: A comparative study with Escherichia coli O157:H7. J. Appl. Microbiol. 95, 563-575.   DOI   ScienceOn
55 Lianou, A., Stopforth, J. D., Yoon, Y., Wiedmann, M., and Sofos, J. N. (2006) Growth and stress resistance variation in culture broth among Listeria monocytogenes strains of various serotypes and origins. J. Food Prot. 69, 2640-2647.
56 Mantovani, H. C. and Russell, J. B. (2001) Nisin resistance of Streptococcus bovis. Appl Environ Microb. 67, 808-813.   DOI   ScienceOn
57 Martinez, B., Bravo, D., and Rodriguez, A. (2005) Consequences of the development of nisin-resistant Listeria monocytogenes in fermented dairy products. J. Food Prot. 68, 2383-2388.
58 Mattick, K. L., Jorgensen, F., Legan, D., Cole, M., Porter, J., Lappin-Scott, H. M., and Humphrey, T. J. (2000) The filamentation and survival of Salmonella enterica serovar Enteritidis and Salmonella enterica serovar Typhimurium at low water activity. Appl. Environ. Microb. 66, 1274-1279.   DOI
59 Mbandi, E. and Shelef, L. A. (2002) Enhanced antimicrobial effects of combination of lactate and diacetate on Listeria monocytogenes and Salmonella spp. in beef bologna. Int. J. Food Microbiol. 76, 191-198.   DOI   ScienceOn
60 Mattick, K. L., Phillips, L. E., Jorgensen, F., Lappin-Scott, H. M., and Hymphrey, T. J. (2003) Filament formation by Salmonella spp. inoculated into liquid food matrices at refrigeration temperatures, and growth patterns when warmed. J. Food Prot. 66, 215-219.
61 McClure, P. J., Roberts, T. A., and Oguru, P. O. (1989) Comparison of the effects of sodium chloride, pH and temperature on the growth of Listeria monocytogenes on gradient plates and in liquid medium. Lett. Appl. Microbiol. 9, 95-99.   DOI
62 McKinney, J., Williams, R. C., Boadman, G. D., Eifert, J. D., and Summer, S. S. (2009) Dose of UV light required to inactivate Listeria monocytogenes in distilled water, fresh brine, and spent brine. J. Food Prot. 72, 2144-2150.
63 McLauchlin, J., Mitchell, R. T., Smerdon, W. J., and Jewell, K. (2004) Listeria monocytogenes and listeriosis: A review of hazard characterisation for use in microbiological risk assessment of foods. Int. J. Food Microbiol. 92, 15-33.   DOI   ScienceOn
64 Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., and Shapiro, C. (1999) Food-related illness and death in the United States. Emerg. Infect. Dis. 5, 607-625.   DOI   ScienceOn
65 Mendonca, A. F., Romero, M. G., Lihono, M. A., Nannapaneni, R., and Johnson, M. G. (2004) Radiation resistance and virulence of Listeria monocytogenes Scott A following starvation in physiological saline. J. Food Prot. 67, 470-474.
66 Mendum, M. L. and Smith, L. T. (2002) Characterization of glycine betaine porter I from Listeria monocytogenes and its roles in salt and chill tolerance. Appl. Environ. Microb. 68, 813-819.   DOI   ScienceOn
67 Isom, L. L., Khambatta, Z. S., Moluf, J. L., Akers, D. F., and Martin, S. E. (1995) Filament formation in Listeria monocytogenes. J. Food Prot. 58, 1031-1033.
68 Meng, J. and Doyle, M. P. (1998) Emerging and evolving microbial foodborne pathogens. Bull. Inst. Pasteur. 96, 15-33.   DOI   ScienceOn
69 Muriana, P. M. (1996) Bacteriocins for control of Listeria spp. in food. J. Food Prot. Supp, 54-63.
70 Hornbaek, T., Brockhoff, P. B., Siegumfeldt, H., and Budde, B. B. (2006) Two subpopulations of Listeria monocytogenes occur at subinhibitory concentrations of leucocin 4010 and nisin. Appl. Environ. Microb. 72, 1631-1638.   DOI   ScienceOn
71 Jensen, A., Larsen, M. H., Ingmer, H., Vogel, B. F., and Gram, L. (2007) Sodium chloride enhances adherence and aggregation and strain variation influences invasiveness of Listeria monocytogenes strains. J. Food Prot. 70, 592-599.
72 Jones, T., Gill, C. O., and McMullen, L. M. (2004) The behaviour of log phase Escherichia coli at temperatures that fluctuate about the minimum for growth. Lett. Appl. Microbiol. 39, 296-300.   DOI   ScienceOn
73 Juneja, V. K., Altuntas, E. G., Ayhan, K., Hwang, C-A., Sheen, S., and Friedman, M. (2013) Predictive model for the reduction of heat resistance of Listeria monocytogenes in ground beef by the combined effect of sodium chloride and apple polyphenols. Int. J. Food Microbiol. 164, 54-59.   DOI   ScienceOn
74 Kathariou, S. (2002) Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J. Food Prot. 65, 1811-1829.
75 Kazmierczak, M. J., Mithoe, S. C., Boor, K. J., and Wiedmann, M. (2003) Listeria monocytogenes ${\sigma}^B$ regulates stress response and virulence functions. J. Bacteriol. 185, 5722-5734.   DOI   ScienceOn
76 Kim, K. Y. and Frank, J. F. (1995) Effect of nutrients on biofilm formation by Listeria monocytogenes on stainless steel. J. Food Prot. 58, 24-28.
77 Lado, B. H. and Yousef, A. E. (2007) Characterization of Listeria monocytogenes important to food processors. In: Listeria, listeriosis, and food safety. Ryser, E. T. and Marth, H (ed) CRC Press, Boca Raton, FL. USA.
78 Knobloch, J. K. M., Bartscht, K., Sabottke, A., Rohde, H., Feucht, H. H., and Mack, D. (2001) Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, and activator of the sigB operon: Differential activation mechanisms due to ethanol and salt stress. J. Bacteriol. 183, 2624-2633.   DOI   ScienceOn
79 Kumar, C. G. and Anand, S. K. (1998) Significance of microbial biofilms in the food industry: A review. Int. J. Food Microbiol. 42, 9-27.   DOI   ScienceOn
80 Kuzhiyil, A., Lee, Y., Shim, A., and Xiong, A. (2012) Ostmotic stress induces kanamycin resistance in Escherichia coli B23 through increased capsule formation. J. Exp. Microbiol. Immun. 16, 5-10.
81 Lee, J. (2012) Effect of fat and sodium on resistance and invasion of Listeria monocytogenes. MS. Thesis, Sookmyung Women's Univ., Seoul, Korea.
82 Leistner, L. and Russell, N. J. (1991). Solutes and low water activity. In: Food preservatives. Russell, N. J. and Gould, G. W. (eds.) Avi Publishing Company, Inc., New York, NY, pp. 111-134.
83 Cramton, S. E., Ulrich, M., Gotz, F., and Doring, G. (2001) Anaerobic conditions induce expression of polysaccharide interceullular adhesion in Staphylococcus aureus and Staphylococcus epidermidis. Inf. Immun. 69, 4079-4985.   DOI   ScienceOn
84 Crandall, A. D. and Montville, T. J. (1998) Nisin resistance in Listeria monocytogenes ATCC700302 is a complex phenotype. Appl. Environ. Microb. 64, 231-237.
85 Delves-Broughton, J. (1990) Nisin and its uses as a food preservative. Food Technol. 44, 100-112.
86 Fretz, R., Sagel, U., Ruppitsch, W., Pietzka, A. T., Stoger, A., Huhulescu, S., Heuberger, S., Pichler, J., Much, P., Pfaff, G., Stark, K., Prager, R., Flieger, A., Feenstra, O., and Allerberger, F. (2010) Listeriosis outbreak caused by acid curd cheese 'Quargel', Austria and Germany 2009. Available at: http:// web.archive.org/web/20090207083151/http://www.phac-aspc. gc.ca/alert-alerte/listeria/listeria_2008-eng.php. Accessed on June 11, 2013.
87 Djordjevic, D., Wiedmann, M., and McLandsborough, L. A. (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl. Environ. Microb. 68, 2950-2958.   DOI   ScienceOn
88 Faleiro, M. L., Andrew, P. W., and Power, D. (2003) Stress response of Listeria monocytogenes isolated from cheese and other foods. Int. J. Food Microbiol. 84, 207-216.   DOI   ScienceOn
89 Foegeding, P. M., Thomas, A. B., Pilkington, D. H., and Klaenhanmmer, T. R. (1992) Enhanced control of Listeria monocytogenes by in situ-produced pediocin during dry fermented sausage production. Appl. Environ. Microb. 58, 884-890.
90 Garner, M. R., James, K. E., Callahan, M. C., Wiedmann, M., and Boor, K. J. (2006) Exposure to salt and organic acids increases the ability of Listeria monocytogenes to invade Caco-2 cells but decreases its ability to survive gastric stress. Appl. Environ. Microb. 72, 5384-5395.   DOI   ScienceOn
91 Gill, C. O., Badoni, M., and Jones, T. H. (2007) Behaviours of log phase cultures of eight strains of Escherichia coli incubated at temperatures of 2, 6, 8 and $10^{\circ}C$. Int. J. Food Microbiol. 119, 200-206.   DOI   ScienceOn
92 Glass, K. A. and Doyle, M. P. (1989) Fate of Listeria monocytogenes in processed meat products during refrigerated storage. Appl. Environ. Microb. 55, 1565-1569.
93 Grade, S. M., Avila, M., Medina, M., and Nunez, M. (2004) Fast induction of nisin resistance in Streptococcus thermophilus INIA 463 during growth in milk. Int. J. Food Microbiol. 96, 165-172.   DOI   ScienceOn