The effect of sodium reduction with and without potassium chloride on the survival of Listeria monocytogenes in Cheddar cheese

Journal of Dairy Science

Volumn 96, Issue 10, 2013, Pages 6172-6185

  Hystead, E ^a   Diez Gonzalez, F ^a   Schoenfuss, T C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cheddar cheese; KCl; Listeria monocytogenes; Sodium reduction

Indexed keywords

LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES;

FLAVORING AGENT; POTASSIUM CHLORIDE; SALT INTAKE;

ANALYSIS; CHEESE; DRUG EFFECTS; FOOD CONTROL; FOOD HANDLING; FOOD SAFETY; GROWTH, DEVELOPMENT AND AGING; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; MICROBIOLOGY; PH; PHARMACOLOGY; PHYSIOLOGY; PROCEDURES; SALT INTAKE; SODIUM RESTRICTION; STANDARDS; TEMPERATURE;

CHEESE; DIET, SODIUM-RESTRICTED; FLAVORING AGENTS; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD SAFETY; HYDROGEN-ION CONCENTRATION; LACTOCOCCUS LACTIS; LISTERIA MONOCYTOGENES; POTASSIUM CHLORIDE; SODIUM CHLORIDE, DIETARY; TEMPERATURE;

EID: 84884351449     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2013-6675     Document Type: Article

References (77)

1. Agarwal S., McCoy D., Graves W., Gerard P.D., Clark S. Sodium content in retail Cheddar, Mozzarella, and process cheeses varies considerably in the United States. J. Dairy Sci. 2011, 94:1605-1615.
2. Official Methods of Analysis. Method 993.13. Nitrogen (total) in fertilizers. Combustion method 2005, AOAC International, AOAC International, Arlington, VA.
3. Appel L.J., Angell S.Y., Cobb L.K., Limper H.M., Nelson D.E., Samet J.M., Brownson R.C. Population-wide sodium reduction: The bumpy road from evidence to policy. Ann. Epidemiol. 2012, 22:417-425.
4. Bautista-Gallego J., Arroyo-Lopez F.N., Duran-Quintana M.C., Garrido-Fernandez A. Individual effects of sodium, potassium, calcium, and magnesium chloride salts on Lactobacillus pentosus and Saccharomyces cerevisiae growth. J. Food Prot. 2008, 71:1412-1421.
5. Bergholz T.M., den Bakker H.C., Fortes E.D., Boor K.J., Wiedmann M. Salt stress phenotypes in Listeria monocytogenes vary by genetic lineage and temperature. Foodborne Pathog. Dis. 2010, 7:1537-1549.
6. Bouzas J., Kantt C.A., Bodyfelt F.W., Torres J.A. Time and temperature influence on chemical aging indicators for a commercial Cheddar cheese. J. Food Sci. 1993, 58:1307-1312.
7. Boziaris I.S., Skandamis P.N., Anastasiadi M., Nychas G.J. 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. 2007, 102:796-805.
8. Brandsma I. Reducing sodium: A European perspective. Food Technol. 2006, 60:24-29.
9. Buyong N., Kok J., Luchansky J.B. Use of a genetically enhanced, pediocin-producing starter culture, Lactococcus lactis subsp. lactis MM217, to control Listeria monocytogenes in Cheddar cheese. Appl. Environ. Microbiol. 1998, 64:4842-4845.
10. Carpenter C.E., Broadbent J.R. External concentration of organic acid anions and pH: Key independent variables for studying how organic acids inhibit growth of bacteria in mildly acidic foods. J. Food Sci. 2009, 74:R12-R15.
11. Cataldo G., Conte M.P., Chiarini F., Seganti L., Ammendolia M.G., Superti F., Longhi C. Acid adaptation and survival of Listeria monocytogenes in Italian-style soft cheeses. J. Appl. Microbiol. 2007, 103:185-193.
12. CDC (Centers for Disease Control and Prevention). 2013. Centers for Disease Control and Prevention Foodborne Outbreak Online Database (FOOD). Accessed Apr. 2, 2013. http://http://wwwn.cdc.gov/foodborneoutbreaks/.
13. Cohen H.W., Hailpern S.M., Alderman M.H. Sodium intake and mortality follow-up in the Third National Health and Nutrition Examination Survey (NHANES III). J. Gen. Intern. Med. 2008, 23:1297-1302.
14. Cole M.B., Jones M.V., Holyoak C. The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes. J. Appl. Bacteriol. 1990, 69:63-72.
15. Doyle M.E., Glass K.A. Sodium reduction and its effect on food safety, food quality and human health. Compr. Rev. Food Sci. Food Safety 2010, 9:44-55.
16. Dykes G.A., Moorhead S.M. Survival of osmotic and acid stress by Listeria monocytogenes strains of clinical or meat origin. Int. J. Food Microbiol. 2000, 56:161-166.
17. Ennahar S., Deschamps N., Richard J. Natural variation in susceptibility of Listeria strains to class IIa bacteriocins. Curr. Microbiol. 2000, 41:1-4.
18. FDA (Food and Drug Administration). 2013a. Recalls, market withdrawals, & safety alerts. Accessed Apr. 2, 2013. http://http://www.fda.gov/Safety/Recalls/default.htm.
19. FDA (Food and Drug Administration). 2013b. Recall-Firm press release for Alpine Slicing and Cheese Conversion Company. Accessed Apr. 2, 2013. http://http://www.fda.gov/Safety/Recalls/ucm285982.htm.
20. Fitzgerald E., Buckley J. Effect of total and partial substitution of sodium chloride on the quality of Cheddar cheese. J. Dairy Sci. 1985, 68:3127-3134.
21. Fox P.F., Guinee T.P., Cogan T.M., McSweeney P.L.H. Salting of cheese curd. Fundamentals of Cheese Science 2000, Aspen Publishers Inc., Gaithersburg, MD, Pages 153-168.
22. Fugett E., Fortes E., Nnoka C., Wiedmann M. International Life Sciences Institute North America Listeria monocytogenes strain collection: Development of standard Listeria monocytogenes strain sets for research and validation studies. J. Food Prot. 2006, 69:2929-2938.
23. Gahan C.G.M., O'Driscoll B., Hill C. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Appl. Environ. Microbiol. 1996, 62:3128-3132.
24. Galvez A., Lopez R.L., Abriouel H., Valdivia E., Omar N.B. Application of bacteriocins in the control of foodborne pathogenic and spoilage bacteria. Crit. Rev. Biotechnol. 2008, 28:125-152.
25. Genigeorgis C., Carniciu M., Dutulescu D., Farver T.B. Growth and survival of Listeria monocytogenes in market cheese stored at 4 to 30°C. J. Food Prot. 1991, 54:662-668.
26. Gianfranceschi M., D'Ottavio M.C., Gattuso A., Pourshaban M., Bertoletti I., Bignazzi R., Manzoni P., Marchetti M., Aureli P. Listeriosis associated with Gorgonzola (Italian blue-veined cheese). Foodborne Pathog. Dis. 2006, 3:190-195.
27. Goepfert J.M., Olson N.F., Marth E.H. Behavior of Salmonella typhimurium during manufacture and curing of Cheddar cheese. Appl. Microbiol. 1968, 16:862-866.
28. Grummer J., Bobowski N., Karalus M., Vickers Z., Schoenfuss T. Use of potassium chloride and flavor enhancers in low sodium Cheddar cheese. J. Dairy Sci. 2013, 96:1401-1418.
29. Grummer J., Karalus M., Zhang K., Vickers Z., Schoenfuss T.C. Manufacture of reduced-sodium Cheddar-style cheese with mineral salt replacers. J. Dairy Sci. 2012, 95:2830-2839.
30. Grummer J., Schoenfuss T.C. Determining salt concentrations for equivalent water activity in reduced sodium cheese by use of a model system. J. Dairy Sci. 2011, 94:4360-4365.
31. Guinee T.P. Salting and the role of salt in cheese. Int. J. Dairy Technol. 2004, 57:99-109.
32. Guinee T.P., Fox P.F. Salt in cheese: Physical, chemical and biological aspects. Cheese: Chemistry, Physics and Microbiology 2004, 1:207-260. Elsevier, London, UK. 3rd. P.F. Fox, P.L.H. McSweeney, T.M. Cogan, T.P. Guinee (Eds.).
33. Hickey D.K., Guinee T.P., Hou J., Wilkinson M.G. Effects of variation in cheese composition and maturation on water activity in Cheddar cheese during ripening. Int. Dairy J. 2013, 30:53-58.
34. Hill C., Cotter P.D., Sleator R.D., Gahan C.G.M. Bacterial stress response in Listeria monocytogenes: Jumping the hurdles imposed by minimal processing. Int. Dairy J. 2002, 12:273-283.
35. Hou J., Hannon J.A., McSweeney P.L.H., Beresford T., Guinee T. Effect of curd washing on composition, lactose metabolism, pH, and growth of non-starter lactic acid bacteria in full-fat Cheddar cheese. Int. Dairy J. 2012, 25:21-28.
36. ISO/IDF (International Organization for Standardization/International Dairy Federation). 2007. Milk and milk products-Determination of calcium, sodium, potassium and magnesium contents-Atomic absorption spectrometric method. ISO 8070:2007 (IDF 119:2007). ISO, Geneva, Switzerland; IDF, Brussels, Belgium.
37. Kim W.S., Ren J., Dunn N.W. Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses. FEMS Microbiol. Lett. 1999, 171:57-65.
38. Koenig S., Marth E.H. Behavior of Staphylococcus aureus in Cheddar cheese made with sodium chloride or a mixture of sodium chloride and potassium chloride. J. Food Prot. 1982, 45:996-1002.
39. Kosikowski F.V. Low sodium Cheddar cheeses through whole milk retentate supplementation. J. Dairy Sci. 1983, 66:2494-2500.
40. Lindsay R.C., Hargett S.M., Bush C.S. Effect of sodium/potassium (1:1) chloride and low sodium chloride concentrations on quality of Cheddar cheese. J. Dairy Sci. 1982, 65:360-370.
41. Linnan M.J., Mascola L., Lou X.D., Goulet V., May S., Salminen C., Hird D.W., Yonekura M.L., Hayes P., Weaver R., Audurier A., Plikaytis B.D., Fannin S.L., Kleks A., Broome C.V. Epidemic listeriosis associated with Mexican-style cheese. N. Engl. J. Med. 1988, 319:823-828.
42. Maisnier-Patin S., Deschamps N., Tatini S.R., Richard J. Inhibition of Listeria monocytogenes in Camembert cheese made with a nisin-producing starter. Lait 1992, 72:249-263.
43. Marshall R.T. Standard Methods for the Examination of Dairy Products 1992, American Public Health Association, Washington, DC. 16th.
44. Marsili R. Monitoring chemical changes in Cheddar cheese during aging by high performance liquid chromatography and gas chromatography techniques. J. Dairy Sci. 1985, 68:3155-3161.
45. McLauchlin J., Greenwood M.H., Pini P.N. The occurrence of Listeria monocytogenes in cheese from a manufacturer associated with a case of listeriosis. Int. J. Food Microbiol. 1990, 10:255-262.
46. McSweeney P.L.H. Biochemistry of cheese ripening: Introduction and overview. Cheese: Chemistry, Physics and Microbiology 2004, 1:347-360. Elsevier, London, UK. 3rd. P.F. Fox, P.L.H. McSweeney, T.M. Cogan, T.P. Guinee (Eds.).
47. Mehta A., Tatini S.R. An evaluation of the microbiological safety of reduced-fat Cheddar-like cheese. J. Food Prot. 1994, 57:776-779.
48. Milillo S.R., Story R.S., Pak D., O'Bryan C.A., Crandall P.G., Ricke S.C. Antimicrobial properties of three lactic acid bacterial cultures and their cell free supernatants against Listeria monocytogenes. J. Environ. Sci. Health B 2013, 48:63-68.
49. Murtaza M.A., Rehman S.U., Anjum F.M., Huma N., Tarar O.M., Mueen-Ud-Din G. Organic acid contents of buffalo milk Cheddar cheese as influenced by accelerated ripening and sodium salt. J. Food Biochem. 2012, 36:99-106.
50. Nair S.S., Mistry V.V., Nauth K.R. Reduction of salt (NaCl) losses during the manufacture of Cheddar cheese. J. Dairy Sci. 2004, 87:2831-2838.
51. O'Shea E.F., Cotter P.D., Ross R.P., Hill C. Strategies to improve the bacteriocin protection provided by lactic acid bacteria. Curr. Opin. Biotechnol. 2013, 24:130-134.
52. O'Sullivan L., Ross R.P., Hill C. Potential of bacteriocin-producing lactic acid bacteria for improvements in food safety and quality. Biochimie 2002, 84:593-604.
53. Pagotto F., Ng L.K., Clark C., Farber J. Canadian listeriosis reference service. Foodborne Pathog. Dis. 2006, 3:132-137. Canadian Public Health Laboratory Network.
54. Park S.-H., Choi M.-R., Park J.-W., Park K.-H., Chung M.-S., Ryu S., Kang D.-H. Use of organic acids to inactivate Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes on organic fresh apples and lettuce. J. Food Sci. 2011, 76:M293-M298.
55. Phan-Thanh L., Mahouin F., Aligé S. Acid responses of Listeria monocytogenes. Int. J. Food Microbiol. 2000, 55:121-126.
56. Pritchard T.J., Flanders K.J., Donnelly C.W. Comparison of the incidence of Listeria on equipment versus environmental sites within dairy processing plants. Int. J. Food Microbiol. 1995, 26:375-384.
57. Reddy K.A., Marth E.H. Composition of Cheddar cheese made with sodium chloride and potassium chloride either singly or as mixtures. J. Food Compost. Anal. 1993, 6:354-363.
58. Reddy K.A., Marth E.H. Microflora of Cheddar cheese made with sodium chloride, potassium chloride, or mixtures of sodium and potassium chloride. J. Food Prot. 1995, 58:54-61.
59. Richardson G.H. Standard Methods for the Examination of Dairy Products 1985, American Public Health Association, Washington, DC. 15th.
60. Ricke S.C. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult. Sci. 2003, 82:632-639.
61. Rudolf M., Scherer S. High incidence of Listeria monocytogenes in European red smear cheese. Int. J. Food Microbiol. 2001, 63:91-98.
62. Ryan S., Hill C., Gahan C.G.M. Chapter 3 Acid Stress Responses in Listeria monocytogenes. Advances in Applied Microbiology 2008, 65:67-91. Academic Press. London, UK. S.S. Allen, I. Laskin, S. Sariaslani, M.G. Geoffrey (Eds.).
63. Ryser E.T., Marth E.H. Behavior of Listeria monocytogenes during the manufacture and ripening of Cheddar cheese. J. Food Prot. 1987, 50:7-13.
64. Sanders J.W., Venema G., Kok J. Environmental stress responses in Lactococcus lactis. FEMS Microbiol. Rev. 1999, 23:483-501.
65. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.A., Roy S.L., Jones J.L., Griffin P.M. Foodborne illness acquired in the United States-Major pathogens. Emerg. Infect. Dis. 2011, 17:7-15.
66. Schroeder C.L., Bodyfelt F.W., Wyatt C.J., McDaniel M.R. Reduction of sodium chloride in Cheddar cheese: Effect on sensory, microbiological, and chemical properties. J. Dairy Sci. 1988, 71:2010-2020.
67. Shrestha S., Grieder J.A., McMahon D.J., Nummer B.A. Survival of Listeria monocytogenes introduced as a post-aging contaminant during storage of low-salt Cheddar cheese at 4, 10, and 21°C. J. Dairy Sci. 2011, 94:4329-4335. a.
68. Shrestha S., Grieder J.A., McMahon D.J., Nummer B.A. Survival of Salmonella serovars introduced as a post-aging contaminant during storage of low-salt Cheddar cheese at 4, 10, and 21 °C. J. Food Sci. 2011, 76:M616-M621. b.
69. Sutherland B.J. Control of salt absorption and whey drainage in Cheddar cheese manufacture. Aust. J. Dairy Technol. 1974, 29:86-93.
70. Taormina P.J. Implications of salt and sodium reduction on microbial food safety. Crit. Rev. Food Sci. Nutr. 2010, 50:209-227.
71. Tompkin R.B. Control of Listeria monocytogenes in the food-processing environment. J. Food Prot. 2002, 65:709-725.
72. Turner W.K., Thomas T.D. Lactose fermentation in Cheddar cheese and the effect of salt. N. Z. J. Dairy Sci. Technol. 1980, 15:265-276.
73. Upreti P., McKay L.L., Metzger L.E. Influence of calcium and phosphorus, lactose, and salt-to-moisture ratio on cheddar cheese quality: Changes in residual sugars and water-soluble organic acids during ripening. J. Dairy Sci. 2006, 89:429-443.
74. Verheul A., Rombouts F.M., Abee T. Utilization of oligopeptides by Listeria monocytogenes Scott A. Appl. Environ. Microbiol. 1998, 64:1059-1065.
75. Walker S.J., Archer P., Banks J.G. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Bacteriol. 1990, 68:157-162.
76. Wehr H.M., Frank J.F. Standard Methods for the Examination of Dairy Products 2004, American Public Health Association, Washington, DC. 17th.
77. Zacharof M.P., Lovitt R.W. Bacteriocins produced by lactic acid bacteria a review article. APCBEE Procedia 2012, 2:50-56.