Unraveling the Chemical Identity of Meat Pigments

Critical Reviews in Food Science and Nutrition

Volumn 37, Issue 6, 1997, Pages 561-589

  Pegg, Ronald B ^a,b   Shahidi, Fereidoon ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Antimicrobial; Antioxidant; Color; Cooked cured meat pigment; Flavor; Meat curing; N nitrosamines; Natural; Nitrite; Nitrite free; Processed meats

Indexed keywords

PIGMENT;

ANIMAL; CATTLE; CHEMISTRY; COOKING; HUMAN; MEAT; METHODOLOGY; REVIEW; STANDARD;

ANIMALS; CATTLE; COOKERY; HUMANS; MEAT; MEAT PRODUCTS; PIGMENTS, BIOLOGICAL;

EID: 0031241386     PISSN: 10408398     EISSN: None     Source Type: Journal    
DOI: 10.1080/10408399709527789     Document Type: Article

References (111)

1. Binkerd, E. F. and Kolari, O. E., The history and use of nitrate and nitrite in the curing of meat, Food Cosmet. Toxicol., 13, 655, 1975.
2. Fox, J. B., Jr., Role of cure accelerators, in Proceedings of the Meat Industry Research Conference, American Institute Foundation, Chicago, IL, 1974, 17.
3. Polenske, E., Über den Verlust, welchen das Rindfleisch an Nährwerth durch das Pökeln erleidet, sowie über die Veränderungen Salpeter-haltiger Pökellaken. Mittheilungen aus dem chemischen Laboratorium des Kaiserlichen Gesundheitsamtes, 13, Arb. K. GesundhAmt., 7, 471, 1891.
4. Kisskalt, K., Beiträge zur Kenntnis der Ursachen des Rothwerdens des Fleisches beim Kochen, nebst einigen Versuchen über die Wirkung der schwefligen Säure auf die Fleischfarbe, Arch. Hyg., 35, 11, 1899.
5. Lehmann, K. B., Über das Hämorrhodin, ein neues weitverbreitetes Blutfarbstoffderivat, Sitzung. phys.-med. Ges. in Würzb., 48, 57, 1899.
6. Fox, J. B., Jr., The chemistry of meat pigments, J. Agric. Food Chem., 14, 207, 1966.
7. MacDougall, D. B., Mottram, D. S., and Rhodes, D. N., Contribution of nitrite and nitrate to the colour and flavour of cured meats, J. Sci. Food Agric., 26, 1743, 1975.
8. Bailey, M. E. and Swain, J. W., Influence of nitrite on meat flavor, in Proceedings of the Meat Industry Research Conference, American Meat Institute Foundation, Chicago, IL, 1973, 29.
9. Fooladi, M. H., Pearson, A. M. Coleman, T. H., and Merkel, R. A., The role of nitrite in preventing development of warmed-over flavour, Food Chem., 4, 283, 1979.
10. Igene, J. O., Yamauchi, K., Pearson, A. M., and Gray, J. I., Mechanisms by which nitrite inhibits the development of warmed-over flavour (WOF) in cured meat, Food Chem., 18, 1, 1985.
11. Morrissey, P. A. and Tichivangana, J. Z., The antioxidant activities of nitrite and nitrosylmyoglobin in cooked meats, Meat Sci., 14, 175, 1985.
12. Freybler, L. A., Gray, J. I., Asghar, A., Booren, A. M., Pearson, A. M., and Buckley, D. J., Nitrite stabilization of lipids in cured pork, Meat Sci., 33, 85, 1993.
13. Sofos, J. N., Busta, F. F., and Allen, C. E., Sodium nitrite and sorbic acid effects on Clostridium botulinum spore germination and total microbial growth in chicken frankfurter emulsions during temperature abuse, Appl. Environ. Microbiol., 37, 1103, 1979.
14. Benedict, R. C., Biochemical basis for nitrite-inhibition of Clostridium botulinum in cured meat, J. Food Prot., 43, 877, 1980.
15. Pierson, M. D. and Smoot, L. A., Nitrite, nitrite alternatives, and the control of Clostridium botulinum in cured meats, CRC Crit. Rev. Food Sci. Nutr., 17, 141, 1982.
16. Sen, N. P., Seaman, S., and Miles, W. F., Volatile nitrosamines in various cured meat products: Effect of cooking and recent trends, J. Agric. Food Chem., 27, 1354, 1979.
17. Sen, N. P., Tessier, L., Seaman, S. W., and Baddoo, P. A., Volatile and nonvolatile nitrosamines in fish and the effect of deliberate nitrosation under simulated gastric conditions, J. Agric. Food Chem., 33, 264, 1985.
18. Gough, T. A., Goodhead, K., and Walters, C. L., Distribution of some volatile nitrosamines in cooked bacon, J. Sci. Food Agric., 27, 181, 1976.
19. Massey, R. C., McWeeny, D. J., and Knowles, M. E., Interactions of nitrites in foodstuffs, in Interactions of Food Components, Birch, G. G. and Lindley, M. G., Eds., Elsevier Applied Science Publishers, London, UK, 1986, 117.
20. Preussmann, R. and Stewart, B. W., N-Nitroso carcinogens, in Chemical Carcinogens, 2nd ed., Searle, C. E., Ed., ACS Monograph 182, American Chemical Society, Washington, DC, 1984, 643.
21. O'Neill, I. K., von Borstel, R. C., Miller, C. T., Long, J., and Bartsch, H., N-Nitroso Compounds: Occurrence, Biological Effects and Relevance to Human Cancer, International Agency for Research on Cancer, Lyon, France, 1984.
22. Sen, N. P., Formation and occurrence of nitrosamines in foods, in Diet, Nutrition, and Cancer: A Critical Evaluation, Volume II, Reddy, B. S. and Cohen, L., Eds., CRC Press, Boca Raton, FL, 1986, 135.
23. Doll, R. and Peto, R., The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today, J. Natl. Cancer Inst., 66, 1191, 1981.
24. Peters, J. M., Preston-Martin, S., London, S. J., Bowman, J. D., Buckley, J. D., and Thomas, D. C., Processed meats and risk of childhood leukemia (California, USA), Can. Causes Contr., 5, 195, 1994.
25. Pim, L. R., Canadian government position in nitrite in cured meats, in Additive Alert: A Guide to Food Additives for the Canadian Consumer, Doubleday Canada Limited, Toronto, ON, 1979, 87.
26. Williams, D. L. H., Nitrosation mechanisms, Adv. Phys. Org. Chem., 19, 1983.
27. Anon., Nitrate, nitrite, and nitroso compounds in foods, Food Technol., 41(4), 127, 1987.
28. Sebranek, J. G., Advances in the technology of nitrite use and consideration of alternatives, Food Technol., 33(7), 58, 1979.
29. Sen, N. P., Donaldson, B., Seaman, S., Iyengar, J. R., and Miles, W. F., Inhibition of nitrosamine formation in fried bacon by propyl gallate and L-ascorbyl palmitate, J. Agric. Food Chem., 24, 397, 1976.
30. Bharucha, K. R., Cross, C. K., and Rubin, L. J., Long-chain acetals of ascorbic and erythorbic acids as antinitrosamine agents for bacon, J. Agric. Food Chem., 28, 1274, 1980.
31. Fiddler, W., Pensabene, J. W., Piotrowski, E. G., Phillips, J. G., Keating, J., Mergens, W. J., and Newmark, H. L., Inhibition of formation of volatile nitrosamines in fried bacon by the use of cure-solubilized α-tocopherol, J. Agric. Food Chem., 26, 653, 1978.
32. Gray, J. I., Reddy, S. K., Price, J. F., Mandagere, A., and Wilkens, W. F., Inhibition of N-nitrosamines in bacon, Food Technol., 36(6), 39, 1982.
33. Thompson, K., USDA proposes to lower bacon nitrite level to 100 ppm or 40 ppm with starter cultures, Meat Industry, June issue, 107, 1985.
34. Sweet, C. W., Additive Composition for Reduced Particle Size Meats in the Curing Thereof, U. S. Patent 3,899,600.
35. Shahidi, F., Rubin, L. J., Diosady, L. L, Chew, V., and Wood, D. F., Preparation of dinitrosyl ferrohemochrome from hemin and sodium nitrite. Can. Inst. Food Sci. Technol. J., 17, 33, 1984.
36. Shahidi, F., Rubin, L. J., Diosday, L. L., and Wood, D. F., Preparation of the cooked cured-meat pigment, dinitrosyl ferrohemochrome, from hemin and nitric oxide, J. Food Sci., 50, 272, 1985.
37. Shahidi, F. and Pegg, R. B., Novel synthesis of cooked cured-meat pigment, J. Food Sci., 56, 1205, 1991.
38. Shahidi, F. and Pegg, R. B., Powdered Cooked Cured-Meat Pigment Which is a Non-Nitrite Meat Preservative, U. S. Patent 5,230,915.
39. Shahidi, F. and Pegg, R. B., Stabilized Cooked Cured-Meat Pigment, U. S. Patent 5,425,956.
40. Shahidi, F. and Pegg, R. B., Proteinaceous Food Product Containing Containing Stabilized Cooked Cured-Meat Pigment, U. S. Patent 5,443,852.
41. Shahidi, F., Pegg, R. B., and Sen, N. P., Absence of volatile N-nitrosamines in cooked nitrite-free cured muscle foods, Meat Sci., 37, 327, 1994.
42. Schalfejeff, N., Isolation of hemin, Chem. Ber., 18, 232, 1885.
43. Labbe, R. F. and Nishida, G., A new method of hemin isolation, Biochim. Biophys. Acta, 26, 437, 1957.
44. Shahidi, F. and Pegg, R. B., Colour characteristics of cooked cured-meat pigment and its application to meat, Food Chem., 38, 61, 1990.
45. Pegg, R. B., Development of Nitrite-Free Meat Curing Systems, Ph.D. thesis, Memorial University of Newfoundland, Canada, 1993.
46. Shahidi, F. and Pegg, R. B., Effect of the preformed cooked cured-meat pigment (CCMP) on color parameters of muscle foods, J. Muscle Foods, 2, 297, 1991.
47. Shahidi, F., Pegg, R. B., and Sen, N. P., Novel nitrite-free processed meats, in Proceedings of the First International Conference on The Impact of Food Research on New Product Development, University of Karachi, Pakistan, January 24-26, 1993, Ali, R. and Barlow, P. J., Eds., University of Humberside, UK, 1993, 221.
48. Rickansrud, D. A. and Henrickson, R. L., Total pigments and myoglobin concentration in four bovine muscles, J. Food Sci., 32, 57, 1967.
49. Shahidi, F. and Pegg, R. B., Encapsulation of the pre-formed cooked cured-meat pigment, J. Food Sci., 56, 1500, 1991.
50. Hood, D. E. and Riordan, E. B., Discolouration in pre-packaged beef: measurement by reflectance spectrophotometry and shopper discrimination, J. Food Technol., 8, 333, 1973.
51. Cassens, R. G., Faustman, C., and Jiménez-Colmenero, F., Modern developments in research on color of meat, in Trends in Modern Meat Technology 2, Proceedings of the International Symposium, Den Dolder, The Netherlands, November 23-25, 1987, Krol, B., van Roon, P. S., and Houben, J. H., Eds., Wageningen Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 1988, 5.
52. Pate, T. D., Shuler, R. O., and Mandigo, R. W., The influence of glucono delta lactone on cured ham color and color stability, J. Food Sci., 36, 48, 1971.
53. Lawrie, R. A., Chemical and biochemical constitution of muscle, in Meat Science, 3rd ed., Pergamon Press, Oxford, UK, 1979, 75.
54. Ledward, D. A., Colour of raw and cooked meat, in The Chemistry of Muscle-Based Foods, Ledward, D. A., Johnston, D. E., and Knight, M. K., Eds., Special Publication No. 106, The Royal Society of Chemistry, Cambridge, UK, 1992, 128.
55. Synowiecki, J., Heeley, D. H., and Shahidi, F., Purification and characterization of myoglobin from harp seal (Phoca groenlandica), J. Agric. Food Chem., 40, 714, 1992.
56. Francis, F. J., Pigments and other colorants, in Food Chemistry, 2nd ed., Revised and Expanded, Fennema, O. R., Ed., Marcel Dekker, New York, USA, 1985, 545.
57. Stryer, L., Oxygen transporters: myoglobin and hemoglobin, in Biochemistry, W. H. Freeman and Company, New York, 1981, 43.
58. Livingston, D. J. and Brown, W. D., The chemistry of myoglobin and its reactions, Food Technol., 35(5), 244, 1981.
59. Giddings, G. G., The basis of color in muscle foods, CRC Crit Rev. Food Sci. Nutr., 9, 81, 1977.
60. Cotton, F. A., Wilkinson, G., and Gaus, P. L., Introduction to the transition elements: ligand field theory, in Basic Inorganic Chemistry, 3rd ed., John Wiley & Sons, Inc., New York, 1995, 503.
61. Kendrew, J. C., Myoglobin and the structure of proteins, Science, 139, 1259, 1963.
62. Thompson, R. M., Nitrosylmetalloporphyrin Complexes as Models for Cured Meat Pigments, Ph.D. thesis, University of Surrey, UK, 1988.
63. O'Keeffe, M. and Hood, D. E., Biochemical factors influencing metmyoglobin formation on beef from muscles of differing colour stability, Meat Sci., 7, 209, 1982.
64. Bard, J. and Townsend, W. E., Cured meats: meat curing, in The Science of Meat and Meat Products, 2nd ed., Price, J. F. and Schweigert, B. S., Eds., W. H. Freeman and Company, San Francisco, 1971, 452.
65. Sebranek, J. G. and Fox, J. B., Jr., A review of nitrite and chloride chemistry: interactions and implications for cured meats, J. Sci. Food Agric., 36, 1169, 1985.
66. Skibsted, L. H., Cured meat products and their oxidative stability, in The Chemistry of Muscle-Based Foods, Ledward, D. A., Johnston, D. E., and Knight, M. K., Eds., Special Publication No. 106, The Royal Society of Chemistry, Cambridge, UK, 1992, 266.
67. Izumi, K., Cassens, R. G., and Greaser, M. L., Reaction of nitrite with ascorbic acid and its significant role in nitrite-cured food, Meat Sci., 26, 141, 1989.
68. Yonetani, T., Yamamoto, H., Erman, J. E., Leigh, J. S., Jr., and Reed, G. H., Electromagnetic properties of hemoproteins. V. Optical and electron paramagnetic resonance characteristics of nitric oxide derivatives of metalloporphyrin-apohemoprotein complexes, J. Biol. Chem., 247, 2447, 1972.
69. Killday, K. B., Tempesta, M. S., Bailey, M. E., and Metral, C. J., Structural characterization of nitrosylhemochromogen of cooked cured meat: Implications in the meat-curing reaction, J. Agric. Food Chem., 36, 909, 1988.
70. Loew, G. H., Axe, F. U., Collins, J. R., and Du, P., Quantum-mechanical studies of model peroxidase compound I complexes, Inorg. Chem., 30, 2291, 1991.
71. Haldane, J., The red colour of salted meat, J. Hyg., 1, 115, 1901.
72. Tarladgis, B. G., Interpretation of the spectra of meat pigments. II. Cured meats. The mechanism of colour fading, J. Sci. Food Agric., 13, 485, 1962.
73. Lee, S. H. and Cassens, R. G., Nitrite binding sites on myoglobin, J. Food Sci., 41, 969, 1976.
74. Renerre, M. and Rougie, P., Influence du chauffage sur la fixation du nitrite à la myoglobine, Ann. Technol. Agric., 28, 423, 1979.
75. Walters, C. L. and Taylor, A. McM., The reduction of nitrite by skeletal-muscle mitochondria, Biochim. Biophys. Acta, 96, 522, 1965.
76. Walters, C. L., Casselden, R. J., and Taylor, A. McM., Nitrite metabolism by skeletal muscle mitochondria in relation to haem pigments, Biochim. Biophys. Acta, 143, 310, 1967.
77. Möhler, K., Formation of curing pigments by chemical, biochemical or enzymatic reactions, in Proceedings of the International Symposium on Nitrite in Meat Products, Zeist, The Netherlands, September 10-14, 1973, Krol, B. and Tinbergen, B. J., Eds., Wageningen Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 1974, 13.
78. Walters, C. L., Burger, I. H., Jewell, G. G., Lewis, D. F., and Parke, D. V., Mitochondrial enzyme pathways and their possible role during curing, Z. Lebensm. Unters. Forsch., 158, 193, 1975.
79. Fox, J. B., Jr., The pigments of meat, in The Science of Meat and Meal Products, 3rd ed., Price, J. F. and Schweigert, B. S., Eds., Food & Nutrition Press, Inc., Westport, CT, 1987, 193.
80. Tinbergen, B. J., Low-molecular meat fractions active in nitrite reduction, in Proceedings of the International Symposium on Nitrite in Meat Products, Zeist, The Netherlands, September 10-14, 1973, Krol, B. and Tinbergen, B. J., Eds., Wageningen Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 1974, 29.
81. Ando, N., Some compounds influencing colour formation, in Proceedings of the International Symposium on Nitrite in Meat Products, Zeist, The Netherlands, September 10-14, 1973, Krol, B. and Tinbergen, B. J., Eds., Wageningen Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, 1974, 149.
82. Alley, G., Cours, D., and Demeyer, D., Effect of nitrate, nitrite and ascorbate on colour and colour stability of dry, fermented sausage prepared using 'back slopping', Meat Sci., 32, 279, 1992.
83. Anderton, J. I. and Locke, D. J., Extraction of pigment from cooked cured-meat products, Nature, 175, 818, 1955.
84. Hornsey, H. C., The colour of cooked cured pork. I.-Estimation of the nitric oxide-haem pigments, J. Sci. Food Agric., 7, 534, 1956.
85. Sakata, R. and Nagata, Y., A method for measuring the color forming ability of processed meat products: extractability of the native nitroso heme pigments, Jpn. J. Zootech. Sci., 54, 667, 1983.
86. Bonnett, R., Chandra, S., Charalambides, A. A., Sales, K. D., and Scourides, P. A., Nitrosation and nitrosylation of haemoproteins and related compounds. IV. Pentaco-ordinate nitrosylprotohaem as the pigment of cooked cured meat. Direct evidence from E.S.R. spectroscopy, J.C.S. Perkin I, 1706, 1980.
87. Bonnett, R., Charalambides, A. A., and Martin, R. A., Nitrosation and nitrosylation of haemoproteins and related compounds. I. Porphyrins and metalloporphyrins, J.C.S. Perkin I, 974, 1978.
88. Bonnett, R., Hursthouse, M. B., Scourides, P. A., and Trotter, J., Nitrosation and nitrosylation of haemoproteins and related compounds. III. Attack at the vinyl groups of protoporphyrin dimethyl ester. X-ray analysis of 8(E)-8-nitroprotoporphyrin dimethyl ester, J.C.S. Perkin 1, 490, 1980.
89. Bonnett, R. and Nicolaidou, P., Nitrosation and nitrosylation of haemoproteins and related compounds. II. The reaction of nitrous acid with the side chains of α-acylamino-acidesters, J. C. S. Perkin I, 1969, 1979.
90. Wayland, B. B. and Olson, L. W., Nitric oxide complexes of iron(II) and iron(III) porphyrins, J.C.S. Chem. Comm., 897, 1973.
91. Wayland, B. B. and Olson, L. W., Spectroscopic studies and bonding model for nitric oxide complexes of iron porphyrins, J. Am. Chem. Soc., 96, 6037, 1974.
92. 15N Fourier transform nuclear magnetic resonance spectroscopy, J. Muscle Foods, 3, 123, 1992.
93. 15N NMR studies of nitrosyl (bent and linear), nitro, and nitrito ligands in 4-, 5-, and 6-coordinate complexes of the platinum metals, Inorg. Chem., 22, 3497, 1983.
94. Scheidt, W. R. and Frisse, M. E., Nitrosylmetalloporphyrins. II. Synthesis and molecular stereochemistry of nitrosyl-α,β,γ,δ-tetraphenylporphinatoiron(II), J. Am. Chem. Soc., 97, 17, 1975.
95. Andersen, H. J., Johansen, H. S., Shek, C. K., and Skibsted, L. H., Nitric oxide exchange in nitrosylmyoglobin, Z. Lebensm. Unters. Forsch., 191, 293, 1990.
96. Jankiewicz, L., Kwaśny, M., Wasylki, K., and Graczyk, A., Structure studies on the nitrosyl derivative of heme, J. Food Sci., 59, 57, 1994.
97. Maxwell, J. C. and Caughey, W. S., An infrared study of NO bonding to heme B and hemoglobin A. Evidence for inositol hexaphosphate induced cleavage of proximal histidine to iron bonds, Biochemistry, 15, 388, 1976.
98. Kamarei, A. R. and Karel, M., Effects of ionizing radiation on nitric oxide myoglobin. I. Effects on the NO-haem moiety, Int. J. Radiat. Biol., 44, 123, 1983.
99. Dickinson, L. C. and Chien, J. C. W., An electron paramagnetic resonance study of nitrosylmyoglobin, J. Am. Chem. Soc., 93, 5036, 1971.
100. Trittelvitz, E., Sick, H., and Gersonde, K., Conformational isomers of nitrosyl-haemoglobin. An electron-spin-resonance study, Eur. J. Biochem., 31, 578, 1972.
101. Lang, G. and Marshall, W., Mössbauer effect in some haemoglobin compounds, J. Mol. Biol., 18, 385, 1966.
102. Pegg, R. B. and Shahidi, F., A novel titration methodology for elucidation of the structure of preformed cooked cured-meat pigment by visible spectroscopy, Food Chem., 56, 105, 1996.
103. Pegg, R. B., Shahidi, F., Gogan, N. J., and DeSilva, S. I., Elucidation of the chemical structure of the preformed cooked cured-meat pigment by electron paramagnetic resonance spectroscopy, J. Agric. Food Chem., 44, 416, 1996.
104. Young, C. L., Nitric oxide, in Solubility Data Series. Volume 8. Oxides of Nitrogen, International Union of Pure and Applied Chemistry, Pergamon Press, Oxford, UK, 1981, 260.
105. Skoog, D. A. and Leary, J. J., Application of molecular ultraviolet/visible absorption spectroscopy, in Principles of Instrumental Analysis, 4th ed., Saunders College Publishing, Fort Worth, Texas, 1992, 150.
106. Neto, L. M., Nascimento, O. R., Tabak, M., and Caracelli, I., The mechanism of reaction of nitrosyl with met- and oxymyoglobin: an ESR study, Biochim. Biophys. Acta, 956, 189, 1988.
107. Morse, R. H. and Chan, S. I., Electron paramagnetic resonance studies of nitrosyl ferrous heme complexes, J. Biol. Chem., 255, 7876, 1980.
108. Olson, L. W., Schaeper, D., Lançon, D., and Kadish, K. M., Characterization of several novel iron nitrosyl porphyrins, J. Am. Chem. Soc., 104, 2042, 1982.
109. Lançon, D. and Kadish, K. M., Electrochemical and spectral characterization of iron mono- and dinitrosyl porphyrins, J. Am. Chem. Soc., 105, 5610, 1983.
110. Alves, O. C. and Wajnberg, E., Heat denaturation of metHb and HbNO: e.p.r. evidence for the existence of a new hemichrome, Int. J. Biol. Macromol., 15, 273, 1993.
111. Bersohn, M. and Baird, J. C., Hyperfine splitting, in An Introduction to Electron Paramagnetic Resonance, Chap. 3, W. A. Benjamin, Inc., New York, 1966, 27.