Protein oxidation in processed meat: Mechanisms and potential implications on human health

Comprehensive Reviews in Food Science and Food Safety

Volumn 14, Issue 2, 2015, Pages 106-122

  Soladoye, O P ^a,b   Juarez M L ^b   Aalhus, J L ^b   Shand, P ^a   Estevez M ^c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b LACOMBE RESEARCH CENTRE   (Canada)

^c UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

Emerging technologies; Health; Muscle foods; Processing techniques; Protein oxidation

Indexed keywords

FOOD SAFETY; FREE RADICALS; HEALTH; MEATS; MUSCLE; NUTRITION; OXIDATION; PROTEINS;

ANTIOXIDANT PROTECTION; EMERGING TECHNOLOGIES; FREE RADICAL GENERATION; MICROBIAL DETERIORATION; MUSCLE FOODS; PHYSICOCHEMICAL PROPERTY; PROCESSING TECHNIQUE; PROTEIN OXIDATION;

THERMAL PROCESSING (FOODS);

EID: 84930786537     PISSN: None     EISSN: 15414337     Source Type: Journal    
DOI: 10.1111/1541-4337.12127     Document Type: Article

References (173)

1. Aalhus JL, Dugan MER. 2014. Spoilage, factors affecting (b) oxidative and enzymatic. In: Devine C, Dikeman M, editors. Encyclopedia of meat sciences. 2nd ed. London, UK: Academic Press. p 392-400.
2. Akagawa M, Sasaki D, Kurota Y, Suyama K. 2005. Formation of α-aminoadipic and γ-glutamic semialdehydes in proteins by the maillard reaction. Ann N Y Acad Sci 1043:129-34.
3. Akagawa M, Sasaki D, Ishii Y, Kurota Y, Yotsu-Yamashita M, Uchida K, Suyama K. 2006. New method for the quantitative determination of major protein carbonyls, α-aminoadipic and γ-glutamic semialdehydes: investigation of the formation mechanism and chemical nature in vitro and in vivo. Chem Res Tox 19:1059-65.
4. Anderson GH, Li GSK, Jones JD, Bender F. 1975. Effect of hydrogen peroxide treatment on the nutritional quality of rapeseed flour fed to weanling rats. J Nutr 105:317-25.
5. Anderson GH, Ashley DVM, Jones JD. 1976. Utilization of l-methionine sulfoxide, l-methionine sulfone and cysteic acid by the weanling rat. J Nutr 106:1108-14.
6. Armenteros M, Heinonen M, Ollilainen V, Toldrá F, Estévez M. 2009. Analysis of protein carbonyls in meat products by using the DNPH-method, fluorescence spectroscopy and liquid chromatography-electrospray ionisation-mass spectrometry (LC-ESI-MS). Meat Sci 83:104-12.
7. Astruc T, Marinova P, Labas R, Gatellier P, Santé-Lhoutellier V. 2007. Detection and localization of oxidized proteins in muscle cells by fluorescence microscopy. J Agric Food Chem 55:9554-8.
8. Badr HM, Mahmoud KA. 2011. Antioxidant activity of carrot juice in gamma irradiated beef sausage during refrigerated and frozen storage. Food Chem 127:1119-30.
9. Bax ML, Aubry L, Ferreira C, Daudin JD, Gatellier P, Rémond D, Santé-Lhoutellier V. 2012. Cooking temperature is a key determinant of in vitro meat protein digestion rate: investigation of underlying mechanisms. J Agric Food Chem 60:2569-76.
10. Bax M, Buffière C, Hafnaoui N, Gaudichon C, Savary-Auzeloux I, Dardevet D, Rémond D. 2013. Effects of meat cooking, and of ingested amount, on protein digestion speed and entry of residual proteins into the colon: a study in minipigs. PLoS One 8:1-7.
11. Berlett BS, Stadtman ER. 1997. Protein oxidation in aging, disease, and oxidative stress. J Bio Chem 272:20313-6.
12. Bess KN. 2011. Effects of various salt purity levels on lipid oxidation and sensory characteristics of ground turkey and pork. [M.S. thesis]. Urbana, Ill.: Univ. of Illinois at Urbana-Champaign. Available from: https://www.ideals.illinois.edu/bitstream/handle/2142/24260/Bess_Kelsey.pdf?sequence=1
13. Boye J, Wijesinha-Bettoni R, Burlingame B. 2012. Protein quality evaluation twenty years after the introduction of the protein digestibility corrected amino acid score method. Br J Nutr 108:S183-211.
14. Brault D, D'Aprano G, Lacroix M. 1997. Formation of free-standing sterilized edible films from irradiated caseinates. J Agric Food Chem 45:2964-9.
15. Cava R, Ladero L, González S, Carrasco A, Ramírez MR. 2009. Effect of pressure and holding time on colour, protein and lipid oxidation of sliced dry-cured Iberian ham and loin during refrigerated storage. Innov Food Sci Emerg Technol 10:76-81.
16. Cheah PB, Ledward DA. 1996. High pressure effects on lipid oxidation in minced pork. Meat Sci 43:123-34.
17. Cheah PB, Ledward DA. 1997. Catalytic mechanism of lipid oxidation following high pressure treatment in pork fat and meat. J Food Sci 62:1135-9.
18. Chelh I, Gatellier P, Santé-Lhoutellier V. 2006. Technical note: a simplified procedure for myofibril hydrophobicity determination. Meat Sci 74:681-3.
19. Chen N, Zhao M, Sun W. 2013. Effect of protein oxidation on the in vitro digestibility of soy protein isolate. Food Chem 141:3224-9.
20. Conchillo A, Ansorena D, Astiasarán I. 2005. Intensity of lipid oxidation and formation of cholesterol oxidation products during frozen storage of raw and cooked chicken. J Sci Food Agric 85:141-6.
21. Cuq JL, Besancon P, Chartier L, Cheftel C. 1978. Oxidation of methionine residues of food proteins and nutritional availability of protein-bound methionine sulphoxide. Food Chem 3:85-102.
22. Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. 2003. Protein carbonylation in human diseases. Trends Mol Med 9:169-76.
23. Daneshvar B, Frandsen H, Autrupand H, Dragsted LO. 1997. γ-Glutamyl semialdehyde and 2-amino-adipic semialdehyde: biomarkers of oxidative damage to proteins. Biomarkers 2:117-23.
24. Davies KJA. 2001. Degradation of oxidized proteins by the 20S proteasome. Biochimie 83:301-10.
25. De Palo P, Maggiolino A, Centoducati P, Tateo A. 2013. Effects of two different packaging materials on veal calf meat quality and shelf life. J Animal Sci 91:2920-30.
26. Decker EA, Xiong YL, Calvert JT, Crum AD, Blanchard SP. 1993. Chemical, physical, and functional properties of oxidized turkey white muscle myofibrillar proteins. J Agric Food Chem 41:186-9.
27. Dizdaroglu M, Gajewski E, Simic MG. 1984. Enzymatic digestibility of peptides cross-linked by ionizing radiation. Intl J Rad Biol 45:283-95.
28. EFSA. 2010. Guidance on human health risk-benefit assessment of foods. EFSA J 8:1673-1714. Available from: http://www.efsa.europa.eu/en/search/doc/1673.pdf (01/09/2015).
29. Engberg RM, Lauridsen C, Jensen SK, Jakobsen K. 1996. Inclusion of oxidized vegetable oil in broiler diets. Its influence on nutrient balance and on the antioxidative status of broilers. Poultry Sci 75:1003-11.
30. Esterbauer H, Muskiet F, Horrobin DF. 1993. Cytotoxicity and genotoxicity of lipid-oxidation products. Am J Clin Nutr 57:779S-86S.
31. Estévez M. 2011. Protein carbonyls in meat systems: a review. Meat Sci 89:259-79.
32. Estévez M, Cava R. 2006. Effectiveness of rosemary essential oil as an inhibitor of lipid and protein oxidation: contradictory effects in different types of frankfurters. Meat Sci 72:348-55.
33. Estévez M, Heinonen M. 2010. Effect of phenolic compounds on the formation of α-aminoadipic and γ-glutamic semialdehydes from myofibrillar proteins oxidized by copper, iron, and myoglobin. J Agric Food Chem 58:4448-55.
34. Estévez M, Ventanas S, Cava R. 2005. Protein oxidation in frankfurters with increasing levels of added rosemary essential oil: effect on color and texture deterioration. J Food Sci 70:C427-32.
35. Estévez M, Morcuende D, Ventanas S. 2008. Determination of oxidation. In: Nollet LM, Toldra F, editors. Handbook of processed meat and poultry analysis. Boca Raton, Fla.: CRC Press. p 141-62.
36. Estévez M, Ollilainen V, Heinonen M. 2009. Analysis of protein oxidation markers α-aminoadipic and γ-glutamic semialdehydes in food proteins using liquid chromatography (LC)-electrospray ionization (ESI)-multistage tandem mass spectrometry (MS). J Agric Food Chem 57:3901-10.
37. Estévez M, Ventanas S, Heinonen M. 2011a. Formation of Strecker aldehydes between protein carbonyls-α-aminoadipic and γ-glutamic semialdehydes-and leucine and isoleucine. Food Chem 128:1051-7.
38. Estévez M, Ventanas S, Heinonen M, Puolanne E. 2011b. Protein carbonylation and water-holding capacity of pork subjected to frozen storage: Effect of muscle type, premincing, and packaging. J Agric Food Chem 59:5435-43.
39. Evenepoel P, Claus D, Geypens B, Maes B, Hiele M, Rutgeerts P, Ghoos Y. 1998. Evidence for impaired assimilation and increased colonic fermentation of protein, related to gastric acid suppression therapy. Aliment Pharm Therap 12:1011-9.
40. FAO. 2013. Dietary protein quality evaluation in human nutrition. FAO food and nutrition paper. Vol. 92, p 66. Rome: Food and Agriculture Organization of the United Nations.
41. Filgueras RS, Gatellier P, Zambiazi RC, Santé-Lhoutellier V. 2011. Effect of frozen storage duration and cooking on physical and oxidative changes in M. Gastrocnemius pars interna and M. Iliofiburalis of rhea americana. Meat Sci 88:645-51.
42. FSIS, Food Safety and Inspection Service. 1999. Irradiation of meat food products. Federal Register 64. (264) 72150-72166. 9 CFR Parts 381 abd 424. Docket No. 97-076F.
43. Fuentes V, Ventanas J, Morcuende D, Estévez M, Ventanas S. 2010. Lipid and protein oxidation and sensory properties of vacuum-packaged dry-cured ham subjected to high hydrostatic pressure. Meat Sci 85:506-14.
44. Ganhão R, Morcuende D, Estévez M. 2010a. Protein oxidation in emulsified cooked burger patties with added fruit extracts: influence on colour and texture deterioration during chill storage. Meat Sci 85:402-9.
45. Ganhão R, Morcuende D, Estévez M. 2010b. Tryptophan depletion and formation of α-aminoadipic and γ-glutamic semialdehydes in porcine burger patties with added phenolic-rich fruit extracts. J Agric Food Chem 58:3541-48.
46. Garcia MN, Martinez-Torres C, Leets I, Tropper E, Ramirez J, Layrisse M. 1996. Heat treatment on heme iron and iron-containing proteins in meat: Iron absorption in humans from diets containing cooked meat fractions. J Nutr Biochem 7:49-54.
47. Garrison WM. 1987. Reaction mechanisms in the radiolysis of peptides, polypeptides, and proteins. Chem Rev 87:381-98.
48. Gatellier P, Santé-Lhoutellier V. 2009. Digestion study of proteins from cooked meat using an enzymatic microreactor. Meat Sci 81:405-9.
49. Gatellier P, Kondjoyan A, Portanguen S, Santé-Lhoutellier V. 2010. Effect of cooking on protein oxidation in n-3 polyunsaturated fatty acids enriched beef. Implication on nutritional quality. Meat Sci 85:645-50.
50. Genot C, Domguia-Kenmogne HB, Michalski MC, Awada M, Meynier A. 2011. Oxidative fate of lipid structures in food and during digestion-possible metabolic significance. Presented at 6. International CIGR Technical Symposium Towards a Sustainable Food Chain Food Process, Bioprocessing and Food Quality Management, Nantes, FRA (2011-04-18 - 2011-04-20). http://prodinra.inra.fr/record/192264
51. Gheisari HR, Møller JKS, Adamsen ChE, LHS. 2010. Sodium chloride or heme protein induced lipid oxidation in raw, minced chicken meat and beef. Czech J Food Sci 28:364-75.
52. Giroux M, Lacroix M. 1998. Nutritional adequacy of irradiated meat-a review. Food Res Intl 31:257-64.
53. Gravador RS, Jongberg S, Andersen M, Luciano G, Priolo A, Lund MN. 2014. Dietary citrus pulp improves protein stability in lamb meat stored under aerobic conditions. Meat Sci 97:231-6.
54. Grolichová M, Dvorák P, Musilová H. 2004. Employing ionizing radiation to enhance food safety-a review. Acta Cet BRNO 73:143-9.
55. Grune T, Jung T, Merker K, Davies KJA. 2004. Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease. Intl J Biochem Cell Bio 36:2519-30.
56. Haak L, Raes K, Smet K, Claeys E, Paelinck H, De Smet S. 2006. Effect of dietary antioxidant and fatty acid supply on the oxidative stability of fresh and cooked pork. Meat Sci 74:476-86.
57. Haak L, Raes K, Van Dyck S, De Smet S. 2008. Effect of dietary rosemary and α-tocopheryl acetate on the oxidative stability of raw and cooked pork following oxidized linseed oil administration. Meat Sci 78:239-47.
58. Halliwell B. 1994. Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344:721-4.
59. Hande G, Nuran E, Suneetha M, Subramaniam P, Hilmi O, Jay WH. 2006. Misincorporation of free m-tyrosine into cellular proteins: a potential cytotoxic mechanism for oxidized amino acids. Biochem J 395:277-84.
60. Hawkins CL, Morgan PE, Davies MJ. 2009. Quantification of protein modification by oxidants. Free Rad Bio Med 46:965-88.
61. Henry FC. 2009. Irradiation effects on meat: a review. Revista de ciências agrárias 32:255-62. Available from: http://www.scielo.oces.mctes.pt/pdf/rca/v32n2/v32n2a23.pdf.
62. Hernández P, Navarro JL, Toldrá F. 1999. Lipolytic and oxidative changes in two Spanish pork loin products: dry-cured loin and pickled-cured loin. Meat Sci 51:123-8.
63. Heś M, Waszkowiak K, Szymandera-Buszka K. 2012. The effect of iodine salts on lipid oxidation and changes in nutritive value of protein in stored processed meats. Meat Sci 92:139-43.
64. Hoac T, Daun C, Trafikowska U, Zackrisson J, Åkesson B. 2006. Influence of heat treatment on lipid oxidation and glutathione peroxidase activity in chicken and duck meat. Innov Food Sci Emerg Technol 7:88-93.
65. Honikel KO. 2008. The use and control of nitrate and nitrite for the processing of meat products. Meat Sci 78:68-76.
66. Jensen C, Engberg R, Jakobsen K, Skibsted LH, Bertelsen G. 1997. Influence of the oxidative quality of dietary oil on broiler meat storage stability. Meat Sci 47:211-22.
67. Jin G, Zhang J, Yu X, Lei Y, Wang J. 2011. Crude lipoxygenase from pig muscle: partial characterization and interactions of temperature, NaCl and pH on its activity. Meat Sci 87:257-63.
68. Jongberg S, Skov SH, Tørngren MA, Skibsted LH, Lund, MN. 2011. Effect of white grape extract and modified atmosphere packaging on lipid and protein oxidation in chill stored beef patties. Food Chem 128:276-83.
69. Juárez M. Failla S, Ficco A, Peña F, Avilés C, Polvillo O. 2010. Buffalo meat composition as affected by different cooking methods. Food Bioprod Proc 88:145-8.
70. Jung S, Nam KC, Ahn DU, Kim HJ, Jo C. 2013. Effect of phosvitin on lipid and protein oxidation in ground beef treated with high hydrostatic pressure. Meat Sci 95:8-13.
71. Juntachote T, Berghofer E, Siebenhandl S, Bauer F. 2007. The effect of dried galangal powder and its ethanolic extracts on oxidative stability in cooked ground pork. LWT - Food Sci Technol 40:324-30.
72. Kamin-Belsky N, Brillon AA, Arav R, Shaklai N. 1996. Degradation of myosin by enzymes of the digestive system: comparison between native and oxidatively cross-linked protein. J Agric Food Chem 44:1641-6.
73. Kenmogne-Domguia HB, Moisan S, Viau M, Genot C, Meynier A. 2014. The initial characteristics of marine oil emulsions and the composition of the media inflect lipid oxidation during in vitro gastrointestinal digestion. Food Chem 152:146-54.
74. Kim YH, Huff-Lonergan E, Sebranek JG, Lonergan SM. 2010. High-oxygen modified atmosphere packaging system induces lipid and myoglobin oxidation and protein polymerization. Meat Sci 85:759-67.
75. Lee Y, Song KB. 2002. Effect of γ-irradiation on the molecular properties of myoglobin. J Biochem Mol Bio 35:590-4.
76. Lee SK, Mei L, Decker, EA. 1997. Influence of sodium chloride on antioxidant enzyme activity and lipid oxidation in frozen ground pork. Meat Sci 46:349-55.
77. Leygonie C, Britz T, Hoffman LC. 2012. Impact of freezing and thawing on the quality of meat: review. Meat Sci 91:93-8.
78. Li C, Xiong YL, Chen J. 2013. Protein oxidation at different salt concentrations affects the cross-linking and gelation of pork myofibrillar protein catalyzed by microbial transglutaminase. J Food Sci 78:C823-31.
79. Li ZL, Mo L, Le G, Shi Y. 2014. Oxidized casein impairs antioxidant defense system and induces hepatic and renal injury in mice. Food Chem Toxicol 64:86-93.
80. Lin CF, Asghar A, Gray JI, Buckley DJ, Booren AM, Crackel RL, Flegal, CJ. 1989. Effects of oxidised dietary oil and antioxidant supplementation on broiler growth and meat stability. Br Poultry Sci 30:855-64.
81. Liu G, Xiong YL. 2000. Electrophoretic pattern, thermal denaturation, and in vitro digestibility of oxidized myosin. J Agric Food Chem 48:624-30.
82. Liu Z, Xiong YL, Chen J. 2011. Morphological examinations of oxidatively stressed pork muscle and myofibrils upon salt marination and cooking to elucidate the water-binding potential. J Agric Food Chem 59:13026-34.
83. Lund MN, Hviid MS, Skibsted LH. 2007a. The combined effect of antioxidants and modified atmosphere packaging on protein and lipid oxidation in beef patties during chill storage. Meat Sci 76:226-33.
84. Lund MN, Lametsch R, Hviid MS, Jensen ON, Skibsted LH. 2007b. High-oxygen packaging atmosphere influences protein oxidation and tenderness of porcine longissimus dorsi during chill storage. Meat Sci 77:295-303.
85. Lund MN, Hviid MS, Claudi-Magnussen C, Skibsted, LH. 2008a. Effects of dietary soybean oil on lipid and protein oxidation in pork patties during chill storage. Meat Sci 79:727-33.
86. Lund MN, Luxford C, Skibsted LH, Davies MJ. 2008b. Oxidation of myosin by haem proteins generates myosin radicals and protein cross-links. Biochem J 410:565-74.
87. Lund MN, Heinonen M, Baron CP, Estévez M. 2011. Protein oxidation in muscle foods: a review. Mol Nutr Food Res 55:83-95.
88. Ma HJ, Ledward DA, Zamri AI, Frazier RA, Zhou GH. 2007. Effects of high pressure/thermal treatment on lipid oxidation in beef and chicken muscle. Food Chem 104:1575-9.
89. Martinaud A, Mercier Y, Marinova P, Tassy C, Gatellier P, Renerre M. 1997. Comparison of oxidative processes on myofibrillar proteins from beef during maturation and by different model oxidation systems. J Agric Food Chem 45:2481-7.
90. Mei L., Crum AD, Decker EA. 1994. Development of lipid oxidation and inactivation of antioxidant enzymes in cooked pork and beef. J Food Lipids 1:273-83.
91. Mesquita CS, Oliveira R, Bento F, Geraldo D, Rodrigues J, Marcos JC. 2014. Simplified 2, 4 dinitrophenylhydrazine spectrophotometric assay for quantification of carbonyls in oxidized proteins. Anal Biochem 458:69-71.
92. Miller DK, Gomez-Basauri JV, Smith VL, Kanner J, Miller DD. 1994. Dietary iron in swine rations affects nonheme iron and tbars in pork skeletal muscles. J Food Sci 59:747-50.
93. Millward DJ, Layman DK, Tomé D, Schaafsma G. 2008. Protein quality assessment: impact of expanding understanding of protein and amino acid needs for optimal health. Am J Clin Nutr 87:1576S-81S.
94. Morzel M, Gatellier P, Sayd T, Renerre M, Laville E. 2006. Chemical oxidation decreases proteolytic susceptibility of skeletal muscle myofibrillar proteins. Meat Sci 73:536-43.
95. Nieto G, Jongberg S, Andersen ML, Skibsted LH. 2013. Thiol oxidation and protein cross-link formation during chill storage of pork patties added essential oil of oregano, rosemary, or garlic. Meat Sci 95:177-84.
96. Oliver CN, Ahn BW, Moerman EJ, Goldstein S, Stadtman ER. 1987. Age-related changes in oxidized proteins. J Biol Chem 262:5488-91.
97. Opstvedt J, Miller R, Hardy RW, Spinelli J. 1984. Heat-induced changes in sulfhydryl groups and disulfide bonds in fish protein and their effect on protein and amino acid digestibility in rainbow trout (Salmo gairdneri). J Agric Food Chem 32:929-35.
98. Orlien V, Hansen E, Skibsted, LH. 2000. Lipid oxidation in high-pressure processed chicken breast muscle during chill storage: critical working pressure in relation to oxidation mechanism. Eur Food Res Technol 211:99-104.
99. Ozdal T, Capanoglu E, Altay F. 2013. A review on protein-phenolic interactions and associated changes. Food Res Intl 51:954-70.
100. Park D, Xiong YL. 2007. Oxidative modification of amino acids in porcine myofibrillar protein isolates exposed to three oxidizing systems. Food Chem 103:607-16.
101. Popova T, Marinova P, Vasileva V, Gorinov Y, Lidji K. 2009. Oxidative changes in lipids and proteins in beef during storage. Archiva Zootechnica 12:30-8.
102. Promeyrat A, Le Louët L, Kondjoyan A, Astruc T, Santé-Lhoutellier V, Gatellier P, Daudin JD. 2011. Combined effect of meat composition and heating parameters on the physicochemical state of proteins. Procedia Food Sci 1:1118-25.
103. Puolanne E, Halonen M. 2010. Theoretical aspects of water-holding in meat. Meat Sci 86:151-65.
104. Purchas RW, Busboom JR, Wilkinson BHP. 2006. Changes in the forms of iron and in concentrations of taurine, carnosine, coenzyme Q10, and creatine in beef longissimus muscle with cooking and simulated stomach and duodenal digestion. Meat Sci 74:443-9.
105. Rababah T, Hettiarachchy N, Horax R, Eswaranandam S, Mauromoustakos A, Dickson J, Niebuhr S. 2004. Effect of electron beam irradiation and storage at 5 °C on thiobarbituric acid reactive substances and carbonyl contents in chicken breast meat infused with antioxidants and selected plant extracts. J Agric Food Chem 52:8236-41.
106. Renerre M, Poncet K, Mercier Y, Gatellier P, Métro B. 1998. Influence of dietary fat and vitamin E on antioxidant status of muscles of turkey. J Agric Food Chem 47:237-44.
107. Requena JR, Chao C, Levine RL, Stadtman ER. 2001. Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci 9:69-74.
108. Rhee KS, Ziprin YA. 2001. Pro-oxidative effects of NaCl in microbial growth-controlled and uncontrolled beef and chicken. Meat Sci 57:105-12.
109. Rodgers KJ, Wang H, Fu S, Dean RT. 2002. Biosynthetic incorporation of oxidized amino acids into proteins and their cellular proteolysis. Free Rad Bio Med 32:766-75.
110. Rodríguez-Carpena JG, Morcuende D, Estévez M. 2011. Avocado by-products as inhibitors of color deterioration and lipid and protein oxidation in raw porcine patties subjected to chilled storage. Meat Sci 89:166-173.
111. Rowe LJ, Maddock KR, Lonergan, SM, Huff-Lonergan E. 2004. Influence of early postmortem protein oxidation on beef quality. J Anim Sci 82:785-93.
112. Rutherfurd SM, Moughan PJ. 2012. Available versus digestible dietary amino acids. Br J Nutr 108:S298-S305.
113. Rutherfurd SM, Montoya CA, Moughan PJ. 2014. Effect of oxidation of dietary proteins with performic acid on true ileal amino acid digestibility as determined in the growing rat. J Agric Food Chem 62:699-707.
114. Sallam KI, Samejima K. 2004. Microbiological and chemical quality of ground beef treated with sodium lactate and sodium chloride during refrigerated storage. LWT - Food Sci Technol 37:865-71.
115. Salminen H, Estévez M, Kivikari R, Heinonen M. 2006. Inhibition of protein and lipid oxidation by rapeseed, camelina and soy meal in cooked pork meat patties. Eur Food Res Technol 223:461-8.
116. Santé-Lhoutellier V, Aubry L, Gatellier P. 2007. Effect of oxidation on in vitro digestibility of skeletal muscle myofibrillar proteins. J Agric Food Chem 55:5343-8.
117. Santé-Lhoutellier V, Astruc T, Marinova P, Greve E, Gatellier P. 2008a. Effect of meat cooking on physicochemical state and in vitro digestibility of myofibrillar proteins. J Agric Food Chem 56:1488-94.
118. Santé-Lhoutellier V, Engel E, Aubry L, Gatellier P. 2008b. Effect of animal (lamb) diet and meat storage on myofibrillar protein oxidation and in vitro digestibility. Meat Sci 79:777-83.
119. Santé-Lhoutellier VS, Théron L, Cepeda M, Grajales A, Gatellier P. 2008c. Comparison of proteolysis in native, heat-treated and aged proteins from turkey meat. Br Poultry Sci 49:308-14.
120. Sayre LM, Perry G, Smith MA. 2007. Oxidative stress and neurotoxicity. Chem Res Toxicol 21:172-88.
121. Scalbert A, Manach C, Morand C, Rémésy C, Jiménez L. 2005. Dietary polyphenols and the prevention of diseases. Crit Rev Food Sci Nutr 45:287-306.
122. Schönfeldt HC, Hall NG. 2012. Dietary protein quality and malnutrition in Africa. Br J Nutr 108:S69-76.
123. Sell DR, Strauch CM, Shen W, Monnier VM. 2007. 2-Aminoadipic acid is a marker of protein carbonyl oxidation in the aging human skin: effects of diabetes, renal failure and sepsis. Biochem J 404:269-77.
124. Shacter E. 2000. Quantification and significance of protein oxidation in biological samples. Drug Met Rev 32:307-26.
125. Skibsted LH. 2011. Nitric oxide and quality and safety of muscle based foods. Nitric Oxide - Bio Chem 24:176-83.
126. Soto-Vaca A, Gutierrez A, Losso JN, Xu Z, Finley JW. 2012. Evolution of phenolic compounds from color and flavor problems to health benefits. J Agric Food Chem 60:6658-77.
127. Souza CG, Moreira JD, Siqueira IR, Pereira AG, Rieger DK, Souza DO, Perry MLS. 2007. Highly palatable diet consumption increases protein oxidation in rat frontal cortex and anxiety-like behavior. Life Sci 81:198-203.
128. Souza MAA, Visentainer JV, Carvalho RH, Garcia F, Ida EI, Shimokomaki M. 2013. Lipid and protein oxidation in charqui meat and jerked beef. Brazilian Arch Bio Tech 56:107-12.
129. Soyer A, Özalp B, Dalmiş Ü, Bilgin V. 2010. Effects of freezing temperature and duration of frozen storage on lipid and protein oxidation in chicken meat. Food Chem 120:1025-30.
130. Srinivasan S, Xiong YL, Decker EA. 1996. Inhibition of protein and lipid oxidation in beef heart surimi-like material by antioxidants and combinations of pH, NaCl, and buffer type in the washing media. J Agric Food Chem 44:119-25.
131. Stadtman ER. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 62:797-821.
132. Stadtman ER, Levine RL. 2000. Protein oxidation. Annals New York Academy of Sciences 899:191-208.
133. Stadtman ER, Levine RL. 2003. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25:207-18.
134. Summo C, Caponio F, Paradiso VM, Pasqualone A, Gomes T. 2010. Vacuum-packed ripened sausages: evolution of oxidative and hydrolytic degradation of lipid fraction during long-term storage and influence on the sensory properties. Meat Sci 84:147-51.
135. Sun W, Cui C, Zhao M, Zhao Q, Yang B. 2011a. Effects of composition and oxidation of proteins on their solubility, aggregation and proteolytic susceptibility during processing of Cantonese sausage. Food Chem 124:336-341.
136. Sun W, Zhao M, Yang B, Zhao H, Cui C. 2011b. Oxidation of sarcoplasmic proteins during processing of Cantonese sausage in relation to their aggregation behaviour and in vitro digestibility. Meat Sci 88:462-7.
137. Taborsky G, McCollum K. 1973. Oxidative modification of proteins in the presence of ferrous ion and air. Effect of ionic constituents of the reaction medium on the nature of the oxidation products. Biochem 12:1341-8.
138. Taylor A, Davies KJA. 1987. Protein oxidation and loss of protease activity may lead to cataract formation in the aged lens. Free Rad Bio Med 3:371-7.
139. Timm-Heinrich M, Eymard S, Baron CP, Nielsen HH, Jacobsen C. 2013. Oxidative changes during ice storage of rainbow trout (Oncorhynchus mykiss) fed different ratios of marine and vegetable feed ingredients. Food Chem 136:1220-30.
140. Toldrá F. 1998. Proteolysis and lipolysis in flavour development of dry-cured meat products. Meat Sci 49:101-10.
141. Traore S, Aubry L, Gatellier P, Przybylski W, Jaworska D, Kajak-Siemaszko K, Santé-Lhoutellier V. 2012. Effect of heat treatment on protein oxidation in pig meat. Meat Sci 91:14-21.
142. Tuboly E, Lebovics VK, Gaál Ö, Mészáros L, Farkas J. 2003. Microbiological and lipid oxidation studies on mechanically deboned turkey meat treated by high hydrostatic pressure. J Food Engr 56:241-4.
143. Uchida K, Kato Y, Kawakishi S. 1990. A novel mechanism for oxidative cleavage of prolyl peptides induced by the hydroxyl radical. Biochem Biophys Res Com 169:265-71.
144. Utrera M, Estévez M. 2012. Oxidation of myofibrillar proteins and impaired functionality: underlying mechanisms of the carbonylation pathway. J Agric Food Chem 60:8002-11.
145. Utrera M, Estévez M. 2013a. Impact of trolox, quercetin, genistein and gallic acid on the oxidative damage to myofibrillar proteins: the carbonylation pathway. Food Chem 141:4000-9.
146. Utrera M, Estévez M. 2013b. Oxidative damage to poultry, pork, and beef during frozen storage through the analysis of novel protein oxidation markers. J Agric Food Chem 61:7987-93.
147. Utrera M, Rodríguez-Carpena JG, Morcuende D, Estévez M. 2012. Formation of lysine-derived oxidation products and loss of tryptophan during processing of porcine patties with added avocado byproducts. J Agric Food Chem 60:3917-26.
148. Utrera M, Parra V, Estévez M. 2014a. Protein oxidation during frozen storage and subsequent processing of different beef muscles. Meat Sci 96:812-20.
149. Utrera M, Morcuende D, Estévez M. 2014b. Temperature of frozen storage affects the nature and consequences of protein oxidation in beef patties. Meat Sci 96:1250-7.
150. Utrera M, Morcuende D, Estévez M. 2014c. Fat content has a significant impact on protein oxidation occurred during frozen storage of beef patties. LWT - Food Sci Technol 56:62-8.
151. Van Hecke T, Van den Bussche J, Vanhaecke L, Vossen E, Van Camp J, De Smet S. 2014a. Nitrite curing of chicken, pork, and beef inhibits oxidation but does not affect N-nitroso compound (NOC)-specific DNA adduct formation during in vitro digestion. J Agric Food Chem 62:1980-8.
152. Van Hecke T, Vossen E, Van den Bussche J, Raes K, Vanhaecke L, De Smet S. 2014b. Fat content and nitrite-curing influence the formation of oxidation products and NOC-specific DNA adducts during in vitro digestion of meat. PLoS ONE 9:e101122.
153. Ventanas S, Estévez M, Tejeda JF, Ruiz J. 2006. Protein and lipid oxidation in Longissimus dorsi and dry cured loin from Iberian pigs as affected by crossbreeding and diet. Meat Sci 72:647-55.
154. Ventanas S, Ventanas J, Tovar J, García C, Estévez M. 2007. Extensive feeding versus oleic acid and tocopherol-enriched mixed diets for the production of Iberian dry-cured hams: effect on chemical composition, oxidative status and sensory traits. Meat Sci 77:246-56.
155. Villaverde A, Estévez M. 2013. Carbonylation of myofibrillar proteins through the Maillard pathway: effect of reducing sugars and reaction temperature. J Agric Food Chem 61:3140-7.
156. Villaverde A, Morcuende D, Estévez M. 2014a. Effect of curing agents on the oxidative and nitrosative damage to meat proteins during processing of fermented sausages. J Food Sci 79:1331-42.
157. Villaverde A, Ventanas J, Estévez M. 2014b. Nitrite promotes protein carbonylation and Strecker aldehyde formation in experimental fermented sausages: are both events connected? Meat Sci 98:665-72.
158. Villaverde A, Parra V, Estévez M. 2014c. Oxidative and nitrosative stress induced in myofibrillar proteins by a hydroxyl-radical-generating system: impact of nitrite and ascorbate. J Agric Food Chem 62:2158-64.
159. Vossen E, Doolaege EHA, Moges HD, De Meulenaer B, Szczepaniak S, Raes K, De Smet S. 2012. Effect of sodium ascorbate dose on the shelf-life stability of reduced nitrite liver pâtés. Meat Sci 91:29-35.
160. Vuorela S, Salminen H, Makela M, Kivikari R, Karonen M, Heinonen M. 2005. Effect of plant phenolics on protein and lipid oxidation in cooked pork meat patties. J Agric Food Chem 53:8492-7.
161. Wada S. 1992. Quality and lipid change of sardine meat by high pressure treatment In: Balny C, Hayashi R, Heremans K, Masson P, editors. High-pressure and biotechnology. France: John Libbey Eurotext. p 235-238.
162. Wang TJ, Ngo D, Psychogios N, Dejam A, Larson, MG, Vasan RS, Ghorbani A, O'Sullivan J, Cheng S, Rhee EP, Sinha S, McCabe E, Fox CS, O'Donnell CJ, Ho JE, Florez JC, Magnusson M, Pierce KA, Souza AL, Yu Y, Carter C, Light PE, Melander O, Clish CB, Gerszten RE. 2013. 2-Aminoadipic acid is a biomarker for diabetes risk. J Clin Invest 123:4309-17.
163. Wei F, Jing S, Zhuqing L, Guowei L, Yonghui S. 2012. Effect of oxidated food protein on mice gut flora and redox state. Chin J Microecol 24:193-6.
164. Wójciak KM, Dolatowski ZJ. 2012. Oxidative stability of fermented meat products. Acta Sci Pol Technol Aliment 11:99-109.
165. Xiao S, Zhang WG, Lee EJ, Ma CW, Ahn DU. 2011. Effects of diet, packaging, and irradiation on protein oxidation, lipid oxidation, and color of raw broiler thigh meat during refrigerated storage. Poultry Sci 90:1348-57.
166. Xiao S, Zhang WG, Lee EJ, Ahn D. 2013. Effects of diet, packaging and irradiation on protein oxidation, lipid oxidation of raw broiler thigh meat. Iowa State Univ. Animal Industry Report 2013.
167. Xiong YL. 2000. Protein oxidation and implications for muscle food quality. In: Decker E, Faustman C, Clemente JLB, editors. Antioxidant in muscle foods. Chichester, UK: Wiley. p 85-111.
168. Xiong YL, Blanchard SP, Ooizumi T, Ma Y. 2010. Hydroxyl radical and ferryl-generating systems promote gel network formation of myofibrillar protein. J Food Sci 75:C215-21.
169. Youngman LD, Park JK, Ames BN. 1992. Protein oxidation associated with aging is reduced by dietary restriction of protein or calories. Proc Natl Acad Sci 89:9112-6.
170. Youssef EY, Garcia CER, Shimokomaki M. 2003. Effect of salt on color and warmed-over flavor in charqui meat processing. Braz Arch Bio Tech 46:595-600.
171. Zhang W, Xiao S, Lee EJ, Ahn DU. 2011. Effects of dietary oxidation on the quality of broiler breast meat. Iowa State Univ. Animal Industry Report 2011.
172. Zhang W, Xiao S, Ahn DU. 2013. Protein oxidation: basic principles and implications for meat quality. Crit Rev Food Sci Nutr 53:1191-201.
173. Zhuqing Leslie LI, Lingyan WU, Guowei LE, Yonghui SHI. 2013. Effect of oxidized casein on the oxidative damage of blood and digestive organs in mice. Acta Nutrimenta Sin 35:39-43.