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ready-to-eat meats, Listeria monocytogenes, nisin, sodium citrate, sodium diacetate, refrigerated storage


This study evaluated commercially available dip solutions of nisin alone, buffered sodium citrate combined with sodium diacetate (BSCSD), and combined solution of the three antimicrobials for potential to control growth of surface-inoculated Listeria monocytogenes during vacuum packaged refrigerated storage of model beef frankfurters. None of the treatments prevented growth of L. monocytogenes during Frankfurter storage. The combined treatments slowed growth of L. monocytogenes better than individual treatments. Failure to completely eliminate L. monocytogenes on frankfurters or inhibit outgrowth during storage might be attributed to high initial L. monocytogenes inoculum levels, insufficient quantities of antimicrobials to interact with all the target cells, low nisin activity at high pH, or presence of resistant subpopulations, such as nisin-resistant strains. The model conditions used in the experimental setup, such as elimination of natural microbiota from frankfurters and nutrient-rich diluent used for Listeria introduction on the surface, could also contributed to enhanced survival and growth of the pathogen.
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Abee, T., Rombouts, F., Hugenholtz, J., Guihard, G. and Le-Tellier, L. 1994. Mode of action of Nisin Z against Listeria monocytogenesScott A grown at high and low temperatures. Appl. Environ. Microbiol. 60:1962-1968.

Baranyi, J. and Roberts, T.A. 1994. A dynamic approach to predicting bacterial growth in food. Int. J. Food Microbiol. 23:277-294.

Baranyi, J. 2005. DMFit version 2.0: anExcel add-in fitting sigmoid curves. Available at: www.combase.cc/index.php/en/8-category-en-gb/21-tools

Barmpalia, I. M., Geornaras, I., Belk, K. E., Scanga, J. A., Kendall, P. A., Smith, G. C. and Sofos, J. N. 2004. Control of Listeria monocytogenes on frankfurters with antimicrobials in the formulation and by dipping in organic acid solutions. J. Food Protect. 67:2456-2464.

Barmpalia, I.M., Koutsoumanis, K.P., Geornaras, I., Belk, K.E., Scanga, J.A., Kendall, P.A., Smith, G.C. and Sofos, J.N. 2005. Effect of antimicrobials as ingredients of pork bologna for Listeria monocytogenes control during storage at 4°C or 10°C. Food Microbiol. 22:205-211.

Bedie, G.K., Samelis, J., Sofos, J., Belk, K.E., Scanga, J.A. and Smith, G.C. 2001. Antimicrobials in the formulation to control Listeria monocytogenes postprocessing contamination on frankfurters stored at 4°C in vacuum packages. J. Food Protect. 64:1949-1955.

Bouttefroy, A., Mansour, M., Linder, M. and Milliere, J.B. 2000. Inhibitory concentrations of nisin, sodium chloride, and pH on Listeria monocytogenes ATCC 15313 in broth by an experimental design approach. Int. J. Food Microbiol. 54:109-115.

Buckner, R. 2008. Re: Proposed draft microbiological criteria for Listeria Monocytogenesin ready-to-eat foods at step 3, (CX/FH 08/40/5 October 2008). Consumer Federation of America.

Ceylan, E., Hajmeer, M. and Marsden, J.L. 2003. Efficacy of buffered sodium citrate alone and in combination with sodium diacetate against Listeria monocytogenes on beef franks. Cattlemen's Day.

Cleveland, J., Montiville, T.J., Nes, I.F. and Chikindas, M.L. 2001. Bacteriocins: safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71:1-20.

Crandall, A.D. and Montville, T.J. 1998. Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl. Environ. Microbiol. 64:231-237.

Delves-Broughton, J. 2005. Nisin as a food preservative. Food Aust. 57:525-527.

Doores, S., Davidson, P.M., Sofos, J.N. and Brannen, J.L. 2005. Organic acids. In: "Antimicrobials in food".3rd ed. P.M. Davidson, J.N. Sofos and A.L. Branen (Ed.).p. 91-142. CRC Press, Taylor and Francis Group, Boca Raton, FL

Dorsa, W.J., Marshall, D.L., Moody, M.W. and Hackney, C.R. 1993. Low temperature growth and thermal inactivation of Listeria monocytogenes in precooked crawfish tail meat. J. Food Protect. 56:106-109.

El-Khateib, T., Yousef, A.E. and Ockerman, H.W. 1993. Inactivation and attachment of Listeria monocytogenes on beef muscle treated with lactic acid and selected bacteriocin. J. Food Protect. 56:29-33.

Fang, T.J. and Lin, L.1994. Growth of Listeria monocytogenes and Pseudomonas fragion cooked pork in a modified atmosphere packaging/ nisin combination system.J. Food Protect. 57:479-485.

Federal Register. 1988. Nisin preparation: Affirmation of GRAS status as a direct human food ingredient. Federal Register. 53:11247-11257.

Geornaras, I., Skandamis, P.N., Belk, K.E., Scanga, J.A., Kendall, P.A., Smith, G.C. and Sofos, J.N. 2005. Postprocessing antimicrobial treatments to control Listeria monocytogenes in commercial vacuum-packaged bologna and ham stored at 10°C. J. Food Protect. 68:991-998.

Geornaras, I., Skandamis, P.N., Belk, K.E., Scanga, J.A., Kendall, P.A., Smith, G.C. and Sofos, J.N. 2006a. Post-processing application of chemical solutions for control of Listeria monocytogenes, cultured under different conditions, on commercial smoked sausage formulated with and without potassium lactate-sodium diacetate. Food Microbiol. 23:762-771.

Geornaras, I., Skandamis, P.N., Belk, K.E., Scanga, J.A., Kendall, P.A., Smith, G.C. and Sofos, J.N. 2006b. Postprocess control of Listeria monocytogenes on commercial frankfurters formulated with and without antimicrobials and stored at 10°C. J. Food Protect. 69:53-61.

Henning, S., Metz, R. and Hammes, W.P. 1986. Studies on the mode of action of nisin. Int. J. Food Microbiol. 3:121-134.

Hull, R.S. 2007. Method of inhibiting the growth of Clostridium perfringens in meat products. U. S. patent 7,311,934. Available at: www.freepatentsonline.com/7311934.html.

Juneja, V.K. and Thippareddi, H. 2004. Inhibitory effects of organic acid salts on growth of Clostridium perfingens from spore inocula during chilling of marinated ground turkey breast. Int.J. Food Microbiol. 93:155-163.

Liu, S., Graham, J.E., Bigelow, L., Morse, P.D. and Wilkinson, B.J. 2002. Identification of Listeria monocytogenes genes expressed in response to growth at low temperature. Appl. Environ. Microbiol. 68:1697-1705.

Luchansky, J.B. and Call, J.E. 2004. Evaluation of nisin-coated cellulose casings for the control of Listeria monocytogenes inoculated onto the surface of commercially prepared frankfurters.J. Food Protect. 67:1017-1021.

Lunden, J.M., Autio, T.J., Sjoberg, A.M. and Koekeala, H.J. 2003. Persistent and nonpersistent Listeria monocytogenes contamination in meat and poultry processing plants. J. Food Protect. 66:2062-2069.

Martinis, E.C.P., Crandall, A.D., Mazzotta, A.S. and Montville, T.J. 1997. Influence of pH, salt and temperature on nisin resistance of Listeria monocytogenes.J. Food Protect. 60:420-423.

Mead, P.S., Slutsker, L., Dietz, V., Mccaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.

Montville, T. and Chen Y. 1998. Mechanistic action of pediocin and nisin: recent progress and unresolved questions.Appl. Microbiol. Biotechnol. 50:511-519.

Muriana, P.M. 1996. Bacteriocins for control of Listeriaspp. in food. J. Food Protect. 59:54-63.

Naidu, A.S. 2000. Nisin. In "Natural food antimicrobial systems". A.S. Naidu (Ed.), p.389-430. CRC Press, .Boca Raton, FL

Nilsson, L., Huss, H.H. and Gram, L. 1997. Inhibition of Listeria monocytogenes on cold-smoked salmon by nisin and carbon dioxide atmosphere. Int. J. Food Microbiol. 38:217-227.

Patel, J.R., Sanglay, G.C., Sharma, M. and Solomon, M.B. 2006. Combining antimicrobials and hydrodynamic pressure processing for control of Listeria monocytogenes in frankfurters. J. Muscle Foods. 18:1-18.

Rutherford, T. J. 2004. Combined effects of packaging atmosphere, storage temperature and antimicrobials on selected quality and safety attributes of ready-to-shrimp. Master’s thesis, Mississippi State University, MS.

Ryser, E.T. and Donnelly, C.W. 2001. Listeria. Ch. 36. In "Compendium of methods for the microbiological examination of foods".F.P. Downes and K. Ito (Ed.), p. 343-356. APHA, Washington, D.C.

Samelis, J., Sofos, J., Kain, M.L., Scanga, J.A., Belk, K.E. and Smith, G.C. 2001. Organic acids and their salts as dipping solutions to control Listeria monocytogenes inoculated following processing of sliced pork bolognastored at 4°C in vacuum packages. J. Food Protect. 64:1722-1729.

Samelis, J., Bedie, G.K., Sofos, J., Belk, K., Scanga, J.A. and Smith, G.C. 2002. Control of Listeria monocytogenes with combined antimicrobials after post-process contamination and extended storage of frankfurters at 4°C in vacuum packages. J. Food Protect. 65:299-307.

Samelis, J., Bedie, G.K., Sofos, J., Belk, K.E., Scanga, J.A. and Smith, G.C. 2005. Combinations of nisin with organic acids or salts to control Listeria monocytogenes on sliced pork bologna stored at 4°C in vacuum packages. Lebensmittel-Wissenschaft und -Technologie. 38:21-28.

SAS 2002. Statistical Analysis System for Windows, version 9.1.3. Statistical Analysis Systems Institute, Cary, NC.

Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones J.L. and Griffin, P.M. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis.17(1):7-15.

Schlyter, J.H., Glass, K.A., Leoffelholz, J., Degnan, A.J. and Luchansky, J.B. 1993. The effects of diacetate with nitrite, lactate or pediocin on the viability of Listeria monocytogenes in turkey slurries. Int. J. Food Microbiol.19:271-281.

Shelef, L.A. and Addala, L. 1994. Inhibition of Listeria monocytogenes and other bacteria by sodium diacetate. J. Food Saf. 14:103-115.

Sivarooban, T., Hettiarachchy, N.S. and Johnson, M.G. 2007. Inhibition of Listeria monocytogenes using nisin with grape seed extract on turkey frankfurters at 4 and 10°C. J. Food Protect. 70:1017-1020.

Stekelenberg, F.K. and Kant-Muermans, M.L.T. 2001. Effects of sodium lactate and other additives in a cooked ham product on sensory quality and development of a strain of Lactobacillus curvatus and Listeria monocytogenes. Int. J. Food Microbiol. 66:197-203.

Stopforth, J.D., Yoon, Y., Barmpalia, I.M., Samelis, J., Skandamis, P.N. and Sofos, J.N. 2005. Reduction of Listeria monocytogenes during exposure to a simulated gastric fluid following storage of inoculated frankfurters formulated and treated with preservatives. Int. J. Food Microbiol. 99:309-319.

Thippareddi, H., Juneja, V.K., Phebus, R.K., Marsden, J.L. and Kastner, C.L. 2003. Control of Clostridium perfringens germination and outgrowth by buffered sodium citrate during chilling of roast beef and injected pork. J. Food Protect. 66:376-381.

Tokarskyy, O. and Marshall, D.L. 2008. Mechanism of synergistic inhibition of Listeria monocytogenes growth by lactic acid, monolaurin, and nisin. Appl. Environ. Microbiol. 74:7126-7129.

Tokarskyy, O. and Marshall, D.L. 2010. Novel technologies for microbial spoilage prevention. In "Handbook of meat processing". F. Toldra (Ed.), p. 263-286. John Wiley and Sons, Ames, IA

Ukuku, D.O. and Shelef, L.A. 1997. Sensitivity of six strains of Listeria monocytogenes to nisin. J. Food Protect. 60:867-869.

U. S. Code of Federal Regulations. USDA-FSIS. Title 9. Part 430. Section 430.4. Control of Listeria monocytogenes in post-lethality exposed ready-to-eat products.

U. S. DEPARTMENT OF AGRICULTURE and AGRICULTURAL RESEARCH SERVICE. 2019. Pathogen Modeling Program (PMP) online. Available athttps://pmp.errc.ars.usda.gov/PMPOnline.aspx

U. S. DEPARTMENT OF AGRICULTURE and ECONOMIC RESEARCH SERVICE. 2014. Cost estimates of foodborne illnesses. Listeria monocytogenes. Available at www.ers.usda.gov/data-products/cost-estimates-of-foodborne-illnesses/cost-estimates-of-foodborne-illnesses/#Pathogen

U. S. DEPARTMENT OF AGRICULTURE and FOOD AND SAFETY INSPECTION SERVICE. 1996. Use of sodium citrate buffered with citric acid in certain cured and uncured processed meat and poultry products, Direct final rule.Federal Register. 61:18047-18050.

U. S. DEPARTMENT OF AGRICULTURE and FOOD SAFETY AND INSPECTION SERVICE 2000. Food additives for use in meat and poultry products: sodium diacetate, sodium acetate, sodium lactate and potassium lactate, Direct final rule.Federal Register. 65:3121-3123.

U. S. DEPARTMENT OF AGRICULTURE and FOOD AND SAFETY INSPECTION SERVICE. 2014. FSIS Compliance guideline: controlling Listeria monocytogenes in post-lethality exposed ready-to-eat meat and poultry product. Available at www.fsis.usda.gov/wps/wcm/connect/d3373299-50e6-47d6-a577-e74a1e549fde/Controlling-Lm-RTE-Guideline.pdf?MOD=AJPERES

U. S. FOOD AND DRUG ADMINISTRATION. 2018. Recalls, market withdrawals and safety alerts 2018. Available at: www.fda.gov/Safety/Recalls/ArchiveRecalls/2018/default.htm?Page=1

Wederquist, H. and Sofos, J.N. 1994. Listeria monocytogenes inhibition in refrigerated vacuum packaged turkey bologna by chemical additives. J. Food Sci. 59:498-500.

Zhu, M., Du, M., Cordray, J. and Ahn, D.U. 2005. Control of Listeria monocytogenes contamination in ready-to-eat meat products. Compr. Rev. Food Sci. F. 4:34-42.