Addition of carbon dioxide to dairy products to improve quality: A comprehensive review

Comprehensive Reviews in Food Science and Food Safety

Volumn 5, Issue 4, 2006, Pages 158-168

  Hotchkiss, Joseph H ^a   Werner, Brenda G ^a   Lee, Edmund Y C ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 33750432132     PISSN: 15414337     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1541-4337.2006.00008.x     Document Type: Review

References (130)

1. Alves RMV, Sarantopoulos CIGD, Van Dender AGF, Faria JDF. 1996. Stability of sliced mozzarella cheese in modified-atmosphere packaging. J Food Protect 59:838-44.
2. Amigo L, Olano A, Calvo MM. 1995. Preservation of raw milk with carbon dioxide. Z Lebensm Unters Forsch 200:293-6.
3. Barnett HJ, Nelson RW, Hunter PJ, Groninger H. 1971. Studies on the use of carbon dioxide in refrigerated brine for preservation of whole fish. Fish Bull 69:433-7.
4. Beaulieu M, Pouliot Y, Pouliot M. 1999. Thermal aggregation of whey proteins in model solutions as affected by casein/whey protein ratios. J Food Sci 64: 776-80.
5. Bennik MHL, Smid EJ, Rombouts FM, Gorris LGM. 1995. Growth of psychrotrophic foodborne pathogens in a solid surface model system under the influence of carbon dioxide and oxygen. Food Microbiol 12:509-19.
6. Boor KJ, Murphy SC. 2002. Microbiology of market milks. In: Robinson RK, editor. Dairy microbiology handbook: the microbiology of milk and milk products. 3rd ed. New York: Wiley-Interscience. p 91-122. p 13-36.
7. Brody AL. 1995. A perspective on MAP products in North America and Western Europe. In: Faber JM, Dodds KL, editors. Principles of modified atmosphere and sous vide product packaging. Lancaster, Pa: Technomic Publishing.
8. Butler JN. 1982. carbon dioxide equilibria and their applications. Reading, Mass: Addison-Wesley Publishing. p 259.
9. 2 acidified milk. J Dairy Res 62:641-4.
10. Calvo MM, Montilla MA, Olano A. 1993. Rennet-clotting properties and starter activity on milk acidified with carbon dioxide. J Food Protect 56:1073-6.
11. Calvo MM, Montilla MA, Cobbs A. 1999. Lactic acid production and rheological properties of yogurt made from milk acidified with carbon dioxide. J Sci Food Agric 79:1208-12.
12. Chambers JV. 2002. The microbiology of raw milk. In: RK Robinson RK, editor. Dairy microbiology handbook: the microbiology of milk and milk products, 3rd ed. New York: Wiley Interscience. p 39-90.
13. Chen JH, Hotckiss JH. 1991a. Effect of dissolved carbon dioxide on the growth of psychrotrophic organisms in cottage cheese. J Dairy Sci 74:2941-5.
14. Chen JH, Hotchkiss JH. 1991b. Long shelf-life cottage cheese through dissolved carbon dioxide and high-barrier packaging (abstr). J Dairy Sci 74 (Suppl 1):125.
15. Chen HH, Hotchkiss JH. 1993. Growth of Listeria monocytogenes and Clostridium sporogenes in cottage cheese in modified atmosphere packaging. J Dairy Sci 76:972-7.
16. Chen JH, Hotchkiss JH, Lawless HT. 1992. Sensory and microbiological quality of cottage cheese packaged in high-barrier film with added carbon dioxide (abstr). J Dairy Sci 75 (Suppl 1):95.
17. Cousin MA. 1982. Presence and activity of psychrotrophic microorganisms in milk and dairy products: a review. J Food Protect 45:172-207.
18. Daniels JA, Krishnamurthi R, Rizvi SSH. 1985. A review of the effects of carbon dioxide on microbial growth and food quality. J Food Protect 48:532-7.
19. Devlieghere F, Debevere J. 2000. Influence of carbon dioxide on the growth of spoilage bacteria. Food Sci Technol 33:531-7.
20. Devlieghere F, Debevere J, Van Impe J. 1998. Concentration of carbon dioxide in the water-phase as a parameter to model the effect of modified atmosphere on microorganisms. Int J Food Microbiol 43:105-13.
21. Dixon NM, Kell DB. 1989. The inhibition by carbon dioxide of the growth and metabolism of microorganisms. J Appl Bacteriol 67:109-36.
22. 2. J Appl Bacteriol 65:119-33.
23. Donald JR, Jones CL, Maclean ARM. 1924. The effect of carbonation on bacteria in beverages. J Am Pub Health 14:122-4.
24. Driscoll NR, Brennand CP, Hendricks DG. 1985. Sensory quality of nonfat dry milk after long-term storage. J Dairy Sci 68:1931-5.
25. Duthie CM. 1985. Effect of low-level carbonation on the keeping quality of processed milk. [MS thesis]. Ithaca, N.Y.: Cornell Univ. p 60.
26. Duthie CM, Shipe WF, Hotchkiss JH. 1985. Effect of low level carbonation on the keeping quality of processed milk (abstr). J Dairy Sci 68 (Supp 1):69.
27. Eliot SC, Vuillemard JC, Emond JP. 1998. Stability of shredded mozzarella cheese under modified atmospheres. J Food Sci 63:1075-80.
28. Espie WE, Madden RH. 1997. The carbonation of chilled bulk milk. Milchwissenschaft 52:249-53.
29. Farber JM. 1991. Microbiological aspects of modified atmosphere packaging technology review. J Food Protect 54:58-70.
30. Farber JM, Dodds KL.1995. Principles of modified atmosphere and sous vide product packaging. Lancaster, Pa: Technomic Publishing. p 464.
31. Fedio WM, Macleod A, Ozimek L. 1994. The effect of modified atmosphere packaging on the growth of microorganisms in cottage cheese. Milchwissenschaft 49:622-9.
32. Fierheller MG. 1991. MAP of miscellaneous products. In: Ooraiku B, Stiles ME, editors. Modified atmosphere packaging of food. New York: E. Horwood. p 246-60.
33. Frayer JM. 1941. The dissolved gases in milk and dye reduction. Vermont Agric Exp Sta Bull 461.
34. Fromm HI, Boor KJ. 2004. Characterization of pasteurized fluid milk shelf-life attributes. J Food Sci 69:M207-M214.
35. Gebre-Egziabher A, Humbert ES, Blankenagel G. 1980. Hydrolysis of milk proteins by microbial enzymes. J Food Protect 43:709-12.
36. Gevaudan S, Laguade A, Tarodo de la Fuente B, Cuq JL. 1996. Effect of treatment by gaseous carbon dioxide on the colloidal phase of skim milk. J Dairy Sci 79:1713-21.
37. Glass KA, Kaufman KM, Smith AL, Johnson EA, Chen JH, Hotchkiss JH. 1999. Toxin production by Clostridium botulinum in pasteurized milk treated with carbon dioxide. J Food Protect 62:872-6.
38. Gonzalez-Fandos E, Sanz S, Olarte C. 2000. Microbiological, physicochemical and sensory characteristics of Cameros cheese packaged under modified atmospheres. Food Microbiol 17:407-14.
39. Gorski D. 1996. Commitment to cottage cheese. Dairy Foods 97(4):20-3.
40. Gueimonde M, de los Reyes-Gavilan CG. 2004. Reduction of incubation time in carbonated Streptococcus thermophilus/Lactobacillus acidophilus fermented milks as affected by the growth and acidification capacity of the starter strains. Milchwissenschaft-Milk Sci Int 59:280-3.
41. 2-treated milk. Food Res Int 36:43-8.
42. Hanlin JH, Evancho GM, Slade PJ. 1995. Microbiological concerns associated with MAP and sous vide products. In: Faber JM, Dodds KL, editors. Principles of modified atmosphere and sous vide product packaging. Lancaster, Pa: Technomic Publishing. p 69-104.
43. Hendricks MT, Hotchkiss JH. 1997. Effect of carbon dioxide on Pseudomonas fluorescens and Listeria monocytogenes growth in aerobic atmospheres. J Food Protect 60:1548-52.
44. Hocking AD, Faedo M. 1992. Fungi causing thread mold spoilage of vacuum packaged cheddar cheese during maturation. Int J Food Microbiol 16:123-30.
45. Hoffman W. 1906. Ueber den Einfluss hohen hohlensauredrucks auf Bakterien im Wasser und in der milch. Arch Fur Hygiene 57:379-83.
46. Holm GE, Wright PE, Greenbank GR. 1927. Variations in the susceptibility of the fat in dry whole milks to oxidation when stored at various temperatures and at various atmospheres. J Dairy Sci 10:33-5.
47. Honer C. 1987. Protecting cottage cheese with carbon dioxide. Dairy Foods 88(5):40-5.
48. 2 treatment. Int J Microbiol 63:19-28.
49. Hotchkiss JH, Lee E. 1996. Extending shelf-life of dairy products with dissolved carbon dioxide. Eur Dairy Mag 3:16-9.
50. Hotchkiss JH, Chen JH, Lawless HT. 1998. Effect of direct addition of carbon dioxide on microbial and sensory changes in pasteurized milk. J Dairy Sci 82:690-5.
51. Hunziker OF. 1924. Facts about carbonated butter. J Dairy Sci 7:484-8.
52. Jackson CJ. 1936. Technique for obtaining anaerobic milk with some observations on its carbon dioxide content. J Dairy Res 7:25-8.
53. Jay JM. 2000. Modern food microbiology 6th ed. Gaithersburg, Md.: Aspen Publishing. p 679.
54. Juric M, Bertelson G, Mortenson G, Petersen MA. 2003. Light-induced colour and aroma changes in sliced, modified atmosphere packaged semi-hard cheeses. Int Dairy J 13:239-49.
55. Karagul-Yuceer Y, Coggins PC, Wilson JC, White CH. 1999. Carbonated yogurt: sensory properties and consumer acceptance. J Dairy Sci 82:1394-8.
56. Karagul-Yuceer Y, Wilson JC, White CH. 2001. Formulations and processing of yogurt affect the microbial quality of carbonated yogurt. J Dairy Sci 84:543-50.
57. King AD, Nagel CW. 1967. Growth inhibition of a Pseudomonas by carbon dioxide. J Food Sci 32:575-9.
58. King AD, Nagel CW. 1975. Influence of carbon dioxide upon the metabolism of Pseudomonas aeruginosa. J Food Sci 40:362-6.
59. King JS, Mabbitt LA. 1982. Preservation of raw milk by the addition of carbon dioxide. J Dairy Res 49:439-47.
60. Kosikowski FV, Brown DP. 1973. Influence of carbon dioxide and nitrogen on microbial population and shelf-life of cottage cheese and sour cream. J Dairy Sci 56:12-8.
61. Labuza TP. 1982. Shelf life dating of foods. Westport Ct.: Food and Nutrition Press. p 500.
62. Law BA, Mabbitt LA. 1983. New methods for controlling the spoilage of milk and milk products. In: Roberts TA, Skinner FA, editors. Food microbiology: advances and prospects. London: Academic Press. p 131-50.
63. Lee EYC. 1996. Carbon dioxide gas analysis and application in the determination of the shelf-life of modified atmosphere packaged dairy products. [MS thesis]. Ithaca, N.Y.: Cornell Univ. p 77.
64. Lee EYC, Hotchkiss JH. 1997. Microbial changes in cottage cheese packaged in 2.27 kg flexible film pouches and stored at 4 and 7°C (abstr). J Dairy Sci 80 (Suppl 1):129.
65. Lloyd MA, Zou J, Farnsworth H, Ogden LV, Pike OA. 2004. Quality at time of purchase of dried milk products commercially packaged in reduced oxygen atmosphere. J Dairy Sci 87:2337-43.
66. Loss CR. 2001. Effect of dissolved carbon dioxide on the thermal resistance of microorganisms in milk. [MS thesis]. Ithaca, N.Y.: Cornell Univ. p 92.
67. Loss CR, Hotchkiss JH. 2003. The use of dissolved carbon dioxide to extend the shelf-life of dairy products. In: Smit G, editor. Dairy processing: improving quality. Boca Raton, Fla.: CRC Press. p 391-416.
68. 2 injection on the pH and freezing point of milk and creams. J Dairy Sci 86:1578-89.
69. 2. J Dairy Sci 86:1590-1600.
70. 2 concentration, temperature, and pressure in a heat exchanger. J Dairy Sci 86:3822-3830.
71. Ma Y, Ryan C, Barbano DM, Galton DM, Rudan MA, Boor KJ. 2000. Effects of somatic cell count on quality and shelf-life of pasteurized fluid milk. J Dairy Sci 83:264-74.
72. 2 addition to milk on selected analytical testing methods. J Dairy Sci 84:1959-68.
73. 2 addition to raw milk on proteolysis and lipolysis at 4 degrees C. J Dairy Sci 86:1616-31.
74. Mabbitt LA. 1982. Preservation of refrigerated milk. Kieler Milchwirtschaftliche Forschungsberichte 34:28-31.
75. Maniar AB, Marcy JE, Bishop JR., Duncan SE. 1994. Modified atmosphere packaging to maintain direct-set cottage cheese quality. J Food Sci 59:1305-8.
76. Mannheim CH, Soffer T. 1996. Shelf-life extension of cottage cheese by modified atmosphere packaging. Food Sci Technol 29:767-71.
77. Marshall CE. 1902. The aeration of milk. Mich Agric Exp Sta Special Bull 16:25-30.
78. Martin JD. 2002. Effects of carbon dioxide on common raw milk bacteria using predictive modeling measured by conductivity. [MS thesis]. Ithaca, N.Y.: Cornell Univ. p 145.
79. Martin JD, Werner BG, Hotchkiss JH. 2003. Effects of carbon dioxide on bacterial growth parameters in milk as measured by conductivity. J Dairy Sci 86:1932-40.
80. McCarney T, Mullan WMA, Rowe MT. 1995. Effect of carbonation of milk on cheddar cheese yield and quality. Milchwissenschaft 50:670-4.
81. Moir CJ, Eyles MJ, Davey JA. 1993. Inhibition of Pseudomonads in cottage cheese by packaging in atmospheres containing carbon dioxide. Food Microbiol 10:345-51.
82. Molin G. 1983. The resistance to carbon dioxide of some food related bacteria. Euro J Appl Microbiol Biotechnol 8:214-7.
83. 2-treated milk. Eur Food Res Technol 200:289-92.
84. Moore JM, Smith AC, Gosslee DG. 1961. Effect of carbon dioxide upon freezing point of vacuum treated milk. J Milk Food Technol 24:176-80.
85. Muir DD. 1996a. The shelf-life of dairy products. 1. Factors influencing raw milk and fresh products. J Soc Dairy Technol 49:24-32.
86. Muir DD. 1996b. The shelf-life of dairy products. 2. Raw milk and fresh products. J Soc Dairy Technol 49: 44-8.
87. Muir DD. 1996c. The shelf-life of dairy products. 3. Factors influencing intermediate and long life dairy products. J Soc Dairy Technol 49: 67-72.
88. 2 on cheddar cheese composition and yield. J Dairy Sci 87: 3581-9.
89. 2 on the aging and proteolysis of cheddar cheese. J Dairy Sci 87:3590-600.
90. Noll CI, Supplee GC. 1941. Factors affecting the gas content of milk. J Dairy Sci 24:993-8.
91. Noriega L, Gueimonde M, Alonso L, de los Reyes-Gavilan CG. 2003. Inhibition of Bacillus cereus growth in carbonated fermented bifidus milk. Food Microbiol 20:519-26.
92. Parry RT. 1993. Principles and applications of modified atmosphere packaging of foods. New York: Blackie Academic & Professional Publishers. p 305.
93. Prucha MJ, Brannon JM, Ambrose AS. 1922. Does carbon dioxide in carbonated milk and milk products destroy bacteria. Univ Ill Agric Coll Exp Sta Circr 256:1-8.
94. Prucha MJ, Brannon JM, Ruehe HA. 1925. Carbonation of butter. J Dairy Sci 8:318-21.
95. 2 storage of raw milk: microbiological effects. J Dairy Sci 88:3130-8.
96. Rashed MA, Mehanna NM, Mehanna AS. 1986. Effect of carbon dioxide on improving the keeping quality of raw milk. J Soc Dairy Technol 39:62-4.
97. Roberts RF, Torrey GS. 1988. Inhibition of psychrotrophic bacterial growth in refrigerated milk by addition of carbon dioxide. J Dairy Sci 71:52-60.
98. Robinson RK, Tamime AY, Wszolek M. 2002. Microbiology of fermented milks. In: Robinson RK. editor. Dairy microbiology handbook: the microbiology of milk and milk products, 3rd ed. New York: Wiley-Interscience. p 367-430.
99. 2-enriched atmosphere. Milchwissenschaft 46:706-8.
100. Ruas-Madiedo P, Bada-Gancedo JC, Fernandez-Garcia E, Gonzalez de Llano D, de los Reyes-Gavilan CG. 1996. Preservation of the microbiological and biochemical quality of raw milk by carbon dioxide addition: a pilot-scale study. J Food Protect 59:502-8.
101. 2-acidified and non-acidified refrigerated milk. Eur Food Res Technol 206:179-83.
102. Ruas-Madiedo P, Bada-Gancedo JC, Alonso L, de los Reyes-Gavilan CG. 1998. Afuega'l Pitu cheese quality: carbon dioxide addition to refrigerated milk in acid-coagulated cheesemaking. Int Dairy J 8:951-8.
103. Ruas-Madiedo P, Bascaran V, Brana AF, Bada-Gancedo JC, de los Reyes-Gavilan CG. 1998a. Influence of carbon dioxide addition to raw milk on microbial levels and some fat-soluble vitamin contents of raw and pasteurized milk. J Agric Food Chem 46:1552-5.
104. Ruas-Madiedo P, Bascaran V, Brana AF, Bada-Gancedo JC, de los Reyes-Gavilan CG. 1998b. Influence of carbon dioxide addition to raw milk on microbial levels and some fat-soluble vitamin contents of raw and pasteurized milk (correction). J Agric Food Chem 46:2894-4.
105. Ruas-Madiedo P, de los Reyes-Gavilan CG, Olano A, Villamiel M. 2000. Influence of refrigeration and carbon dioxide addition to raw milk on microbial levels, free monosaccharides and myo-inositol content of raw and pasteurized milk. Eur Food Res Technol 212:44-7.
106. 2 treated milk. Food Res Int 35:681-90.
107. Ruas-Madiedo P, Bada-Gancedo JC, Delgado T, Gueimonde M, de los Reyes-Gavilan CG. 2003. Proteolysis in rennet-coagulated Spanish hard cheeses made from milk preserved by refrigeration and addition of carbon dioxide. J Dairy Res 70:115-22.
108. Salvador A, Fiszman SM. 2004. Textural and sensory characteristics of whole and skimmed flavored set-type yogurt during long storage. J Dairy Sci 87:4033-41.
109. Santos MV, Ma Y, Caplan Z, Barbano DM. 2003. Sensory threshold of off-flavors caused by proteolysis and lipolysis in milk. J Dairy Sci 86:1601-7.
110. Schroder MJA, Cousins CM, McKinnon CH. 1982. Effect of psychrotrophic post-pasteurization contamination on the keeping quality at 11°C and 5°C of HTST-pasteurized milk in the U.K. J Dairy Res 49:619-30.
111. Sears DF, Eisenberg RM. 1961. A model representing a physiological role of carbon dioxide at the cell membrane. J Gen Physiol 44:869-75.
112. Shipe WF, Senyk GF, Adler EJ, Ledford RA. 1982. Effect of infusion of carbon dioxide on the bacterial growth in fluid milk (abstr). J Dairy Sci 65 (Suppl 1):77.
113. Skudra LA. 1983. Effect of carbon dioxide on the microflora of milk. Dairy Sci Abstr 45:268.
114. Smith AC. 1964. The carbon dioxide content of milk during handling, processing and storage and its effect upon the freezing point. J Milk Food Technol 27:38-45.
115. Sorhaug T, Stepaniak L. 1997. Psychrotrophs and their enzymes in milk and dairy products: quality aspects. Trends Food Sci Technol 8:35-40.
116. Stretton S, Goodman AE. 1998. Carbon dioxide as a regulator of gene expression in microorganisms. Antonie van Leeuwenhoek 73:79-85.
117. Stretton S, Marshall KC, Dawes IW, Goodman AE. 1996. Characterization of carbon dioxide-inducible genes of the marine bacterium Pseudomonas sp. S91. FEMS Microbiol Lett 140:37-42.
118. Taylor DP, Ogden LV. 2002. Carbonation of viscous fluids: carbon dioxide holding capacity and rate to saturation of simulated yogurt. J Food Sci 67:1032-5.
119. Ternstrom A, Lindberg AM, Molin G. 1993. Classification of the spoilage flora of raw and pasteruized bovine-milk, with special reference to Pseudomonas and Bacillus. J Appl Bacteriol 75:25-34.
120. 2 addition and to raw milk on pasteurized milk quality. [MS thesis]. Ithaca, N.Y.: Cornell Univ. p 55.
121. U.S. Department of Health and Human Services. 1999. Grade "A" Pasteurized Milk Ordinance. Vol. Publication No. 229. 1999 Revision. Washington, D.C.: U.S. Department of Health and Human Services, Public Health Service, Food and Drug Administration. p 292.
122. Valley G, Rettger LF. 1927. The influence of carbon dioxide on bacteria. J Bacteriol 14:101-8.
123. Van Slyke LL, Baker JC. 1919. Carbonic acid and carbonate in cow's milk. NY Agric Exp Sta Bull 69:10-25.
124. Van Slyke LL, Bosworth AW. 1907. Effect of treating milk with carbon dioxide gas under gas pressure. NY Agric Exp Sta Bull 292:371-84.
125. Van Slyke LL, Keeler RF. 1920. The carbon dioxide content as a basis for distinguishing heated from unheated milk. NY Agric Exp Sta Bull 78:111-9.
126. Viljoen BC, Lourens-Hattingh A, Ikalafeng B, Peter G. 2003. Temperature abuse initiating yeast growth in yoghurt. Food Res Int 36:193-7.
127. Vinderola CG, Gueimonde M, Delgado T, Reinheimer JA, de los Reyes-Gavilan CG. 2000. Characteristics of carbonated fermented milk and survival of probiotic bacteria. Int Dairy J 10:213-20.
128. Werner BG, Hotchkiss JH. 2002. Effect of carbon dioxide on the growth of Bacillus cereus spores in milk during storage. J Dairy Sci 85:15-8.
129. Wright AO, Ogden LV, Eggett DL. 2003. Determination of carbonation threshold in yogurt. J Food Sci 68:378-81.
130. Woodroof JG, Phillips GF. 1981. Beverages - carbonated and noncarbonated. Westport, Conn.: AVI Publishing Company. p 592.