Food and Bioprocess Technology

, Volume 9, Issue 3, pp 532–542 | Cite as

Effect of Skin Wine Pomace and Sulfite on Protein Oxidation in Beef Patties During High Oxygen Atmosphere Storage

  • Javier Garcia-Lomillo
  • María Luisa González-SanJosé
  • Leif H. Skibsted
  • Sisse JongbergEmail author
Original Paper


Meat storage in high oxygen atmosphere has been reported to induce protein oxidation reactions decreasing meat quality. The incorporation of antioxidants has been proposed to reduce the extent of these reactions. In this study, the ability of red and white skin wine pomaces as well as sulfites to inhibit protein oxidation were tested in beef patties stored for up to 15 days at 4 °C in a high oxygen atmosphere (70 % O2 and 30 % CO2). SO2 (300 ppm) effectively protected against protein oxidation measured as radical formation by electron spin resonance (ESR) spectroscopy, as thiol loss by the DTNB assay and as myosin heavy chain (MHC) disulfide cross-linking by SDS-PAGE. Pomace from red wine production with a total phenol of 9.9 mg gallic acid equivalent/g protected against protein radical formation and against MHC cross-linking, but not against thiol loss by addition of 2.0 % (w/w) to the beef patties. Pomace from white wine production with a total phenol of 4.0 mg gallic acid equivalent/g only protected against MHC cross-linking. For both types of wine pomace, protein modifications not seen for sulfite addition were observed and were proposed to involve covalent phenol addition to proteins. Red wine pomace may be an alternative to sulfite as a meat additive for protection of beef patties against protein oxidation.


Beef patties Protein oxidation Protein radicals Sulfite Wine pomace Protein cross-linking 



Authors thank the financial support of the Autonomous Government of Castilla y León through the research projects (BU268A11-2 and BU282U13) and the Danish Council for Independent Research |Technology and Production within the Danish Agency for Science Technology and Innovation for granting the project entitled: “Antioxidant mechanisms of natural phenolic compounds against protein cross-link formation in meat and meat systems” (11-117033). The PhD grant of J. García-Lomillo (FPU grant) is funded by the “Ministerio de Educación, Cultura y Deporte” of the Spanish Government.


  1. Abrahamsson, V., Hoff, S., Nielsen, N. J., Lund, M. N., & Andersen, M. L. (2012). Determination of sulfite in beer based on fluorescent derivatives and liquid chromatographic separation. Journal of the American Society of Brewing Chemists, 70(4), 296–302.Google Scholar
  2. Andersen, M. L., Outtrup, H., & Skibsted, L. H. (2000). Potential antioxidants in beer assessed by ESR spin trapping. Journal of Agricultural and Food Chemistry, 48(8), 3106–3111.CrossRefGoogle Scholar
  3. Barceló, J. G. (1990). 8. Compuestos fenólicos. In Técnicas analíticas para vinos (1st ed., pp. 8.3–8.33). Barcelona: GAB.Google Scholar
  4. Benjakul, S., Sungsri-in, R., & Kijroongrojana, K. (2012). Effect of treating of squid with sodium chloride in combination with oxidising agent on bleaching, physical and chemical changes during frozen storage. Food and Bioprocess Technology, 5(6), 2077–2084.CrossRefGoogle Scholar
  5. Brewer, M. S. (2011). Natural antioxidants: sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety, 10(4), 221–247.CrossRefGoogle Scholar
  6. Cecil, R., & McPhee, J. R. (1955). A kinetic study of the reactions on some disulphides with sodium sulphite. The Biochemical Journal, 60(3), 496–506.CrossRefGoogle Scholar
  7. Council Directive 95/2/EC of 20 February 1995 on food additives other than colours and sweeteners. (1995). Official Journal of the European Union, L 61, 1–53.Google Scholar
  8. Davies, M. J. (1990). Detection of myoglobin-derived radicals on reaction of metmyoglobin with hydrogen peroxide and other peroxidic compounds. Free Radical Research Communications, 10(6), 361–370.CrossRefGoogle Scholar
  9. Fu, Q.-q., Liu, R., Zhang, W.-g., Li, Y.-p., Wang, J., & Zhou, G.-h. (2015). Effects of different packaging systems on beef tenderness through protein modifications. Food and Bioprocess Technology, 8(3), 580–588.CrossRefGoogle Scholar
  10. Ganhão, R., Morcuende, D., & Estévez, M. (2010). Protein oxidation in emulsified cooked burger patties with added fruit extracts: influence on colour and texture deterioration during chill storage. Meat Science, 85(3), 402–409.CrossRefGoogle Scholar
  11. García-Lomillo, J., González-SanJosé, M. L., Del Pino-García, R., Rivero-Pérez, M. D., & Muñiz-Rodríguez, P. (2014). Antioxidant and antimicrobial properties of wine byproducts and their potential uses in the food industry. Journal of Agricultural and Food Chemistry, 62(52), 12595–12602.CrossRefGoogle Scholar
  12. Hagerman, A. E., Rice, M. E., & Ritchard, N. T. (1998). Mechanisms of protein precipitation for two tannins, pentagalloyl glucose and Epicatechin16 (4 → 8) catechin (procyanidin). Journal of Agricultural and Food Chemistry, 46(7), 2590–2595.CrossRefGoogle Scholar
  13. Hayon, E., Treinin, A., & Wilf, J. (1972). Electronic spectra, photochemistry, and autoxidation mechanism of the sulfite-bisulfite-pyrosulfite systems. The SO2 -, SO3 -, SO4 -, and SO5 - radicals. Journal of the American Chemical Society, 94(1), 47–57.CrossRefGoogle Scholar
  14. Jiménez-Colmenero, F., Carballo, J., & Cofrades, S. (2001). Healthier meat and meat products: their role as functional foods. Meat Science, 59(1), 5–13.CrossRefGoogle Scholar
  15. Jongberg, S., Gislason, N. E., Lund, M. N., Skibsted, L. H., & Waterhouse, A. L. (2011a). Thiol–quinone adduct formation in myofibrillar proteins detected by LC-MS. Journal of Agricultural and Food Chemistry, 59(13), 6900–6905.CrossRefGoogle Scholar
  16. Jongberg, S., Skov, S. H., Tørngren, M. A., Skibsted, L. H., & Lund, M. N. (2011b). Effect of white grape extract and modified atmosphere packaging on lipid and protein oxidation in chill stored beef patties. Food Chemistry, 128(2), 276–283.CrossRefGoogle Scholar
  17. Jongberg, S., Tørngren, M. A., Gunvig, A., Skibsted, L. H., & Lund, M. N. (2013). Effect of green tea or rosemary extract on protein oxidation in bologna type sausages prepared from oxidatively stressed pork. Meat Science, 93(3), 538–546.CrossRefGoogle Scholar
  18. Jongberg, S., Wen, J., Tørngren, M. A., & Lund, M. N. (2014). Effect of high-oxygen atmosphere packaging on oxidative stability and sensory quality of two chicken muscles during chill storage. Food Packaging and Shelf Life, 1(1), 38–48.CrossRefGoogle Scholar
  19. Kim, Y. H., Huff-Lonergan, E., Sebranek, J. G., & Lonergan, S. M. (2010). High-oxygen modified atmosphere packaging system induces lipid and myoglobin oxidation and protein polymerization. Meat Science, 85(4), 759–767.CrossRefGoogle Scholar
  20. Lund, M. N., Heinonen, M., Baron, C. P., & Estévez, M. (2011). Protein oxidation in muscle foods: a review. Molecular Nutrition and Food Research, 55(1), 83–95.CrossRefGoogle Scholar
  21. Martínez, B., Miranda, J., Vázquez, B., Fente, C., Franco, C., Rodríguez, J., et al. (2012). Development of a hamburger patty with healthier lipid formulation and study of its nutritional, sensory, and stability properties. Food and Bioprocess Technology, 5(1), 200–208.CrossRefGoogle Scholar
  22. Martínez, B., Miranda, J. M., Franco, C. M., Cepeda, A., & Vázquez, M. (2011). Evaluation of transglutaminase and caseinate for a novel formulation of beef patties enriched in healthier lipid and dietary fiber. LWT - Food Science and Technology, 44(4), 949–956.CrossRefGoogle Scholar
  23. McFeeters, R. F. (1998). Use and removal of sulfite by conversion to sulfate in the preservation of salt-free cucumbers. Journal of Food Protection, 61(7), 885–890.Google Scholar
  24. McManus, J. P., Davis, K. G., Beart, J. E., Gaffney, S. H., Lilley, T. H., & Haslam, E. (1985). Polyphenol interactions. Part 1. Introduction; some observations on the reversible complexation of polyphenols with proteins and polysaccharides. Journal of the Chemical Society, Perkin Transactions, 2(9), 1429–1438.CrossRefGoogle Scholar
  25. Mildner-Szkudlarz, S., Zawirska-Wojtasiak, R., Szwengiel, A., & Pacyński, M. (2011). Use of grape by-product as a source of dietary fibre and phenolic compounds in sourdough mixed rye bread. International Journal of Food Science and Technology, 46(7), 1485–1493.CrossRefGoogle Scholar
  26. Morel, M. H., Bonicel, J., Micard, V., & Guilbert, S. (2000). Protein insolubilization and thiol oxidation in sulfite-treated wheat gluten films during aging at various temperatures and relative humidities. Journal of Agricultural and Food Chemistry, 48(2), 186–192.CrossRefGoogle Scholar
  27. Neta, P., & Huie, R. E. (1985). Free-radical chemistry of sulfite. Environmental Health Perspectives, 64, 209–217.CrossRefGoogle Scholar
  28. Nieto, G., Jongberg, S., Andersen, M. L., & Skibsted, L. H. (2013). Thiol oxidation and protein cross-link formation during chill storage of pork patties added essential oil of oregano, rosemary, or garlic. Meat Science, 95(2), 177–184.CrossRefGoogle Scholar
  29. Nissen, L. R., Månsson, L., Bertelsen, G., Huynh-Ba, T., & Skibsted, L. H. (2000). Protection of dehydrated chicken meat by natural antioxidants as evaluated by electron spin resonance spectrometry. Journal of Agricultural and Food Chemistry, 48(11), 5548–5556.CrossRefGoogle Scholar
  30. Pérez-Magariño, S., & González-San José, M. L. (2001). Influence of commercial pectolytic preparations on the composition and storage evolution of albillo white wines. International Journal of Food Science and Technology, 36(7), 789–796.CrossRefGoogle Scholar
  31. Pinelo, M., Arnous, A., & Meyer, A. S. (2006). Upgrading of grape skins: significance of plant cell-wall structural components and extraction techniques for phenol release. Trends in Food Science & Technology, 17(11), 579–590.CrossRefGoogle Scholar
  32. Rivero-Pérez, M. D., Muñiz, P., & González-Sanjosé, M. L. (2008). Contribution of anthocyanin fraction to the antioxidant properties of wine. Food and Chemical Toxicology, 46(8), 2815–2822.CrossRefGoogle Scholar
  33. Sabeena Farvin, K. H., Grejsen, H. D., & Jacobsen, C. (2012). Potato peel extract as a natural antioxidant in chilled storage of minced horse mackerel (Trachurus trachurus): effect on lipid and protein oxidation. Food Chemistry, 131(3), 843–851.CrossRefGoogle Scholar
  34. Sartor, L., Pezzato, E., Dell’Aica, I., Caniato, R., Biggin, S., & Garbisa, S. (2002). Inhibition of matrix-proteases by polyphenols: chemical insights for anti-inflammatory and anti-invasion drug design. Biochemical Pharmacology, 64(2), 229–237.CrossRefGoogle Scholar
  35. Satué-Gracia, M. T., Heinonen, M., & Frankel, E. N. (1997). Anthocyanins as antioxidants on human low-density lipoprotein and lecithin–liposome systems. Journal of Agricultural and Food Chemistry, 45(9), 3362–3367.CrossRefGoogle Scholar
  36. Serrano, R., & Bañón, S. (2012). Reducing SO2 in fresh pork burgers by adding chitosan. Meat Science, 92(4), 651–658.CrossRefGoogle Scholar
  37. Stadtman, E. R. (1990). Metal ion-catalyzed oxidation of proteins: biochemical mechanism and biological consequences. Free Radical Biology and Medicine, 9(4), 315–325.CrossRefGoogle Scholar
  38. Sun, W., Cui, C., Zhao, M., Zhao, Q., & Yang, B. (2011). Effects of composition and oxidation of proteins on their solubility, aggregation and proteolytic susceptibility during processing of Cantonese sausage. Food Chemistry, 124(1), 336–341.CrossRefGoogle Scholar
  39. Tseng, A., & Zhao, Y. (2013). Wine grape pomace as antioxidant dietary fibre for enhancing nutritional value and improving storability of yogurt and salad dressing. Food Chemistry, 138(1), 356–365.CrossRefGoogle Scholar
  40. Vally, H., & Misso, N. L. A. (2012). Adverse reactions to the sulphite additives. Gastroenterology and Hepatology from Bed to Bench, 5(1), 16–23.Google Scholar
  41. Viljanen, K., Halmos, A. L., Sinclair, A., & Heinonen, M. (2005). Effect of blackberry and raspberry juice on whey protein emulsion stability. European Food Research and Technology, 221(5), 602–609.CrossRefGoogle Scholar
  42. Vuorela, S., Salminen, H., Mäkelä, M., Kivikari, R., Karonen, M., & Heinonen, M. (2005). Effect of plant phenolics on protein and lipid oxidation in cooked pork meat patties. Journal of Agricultural and Food Chemistry, 53(22), 8492–8497.CrossRefGoogle Scholar
  43. Xiong, Y. L. (2000). Antioxidants in muscle foods. In E. A. Decker, C. Faustman, & C. J. Lopez-Bote (Eds.), Protein oxidation and implications for muscle food quality (pp. 85–112). New York: John Wiley & Sons, Inc.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Javier Garcia-Lomillo
    • 1
  • María Luisa González-SanJosé
    • 1
  • Leif H. Skibsted
    • 2
  • Sisse Jongberg
    • 2
    Email author
  1. 1.Department of Biotechnology and Food ScienceUniversity of BurgosBurgosSpain
  2. 2.Department of Food ScienceUniversity of CopenhagenFrederiksbergDenmark

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