Food and Bioprocess Technology

, Volume 8, Issue 4, pp 854–864 | Cite as

Role of Phenolics Extracting from Rosa canina L. on Meat Protein Oxidation During Frozen Storage and Beef Patties Processing

  • Mariana Utrera
  • David Morcuende
  • Rui Ganhão
  • Mario Estévez
Original Paper


Recent findings suggested that using frozen material for meat processing leads to products with increased protein oxidation rates and impaired quality traits. Therefore, the effects of frozen storage and the addition of a phenolic-rich dog rose extract (Rosa canina L.; RC), on lipid and protein oxidation, moisture losses, color stability, and hardness of beef patties were investigated. Protein oxidation was assessed by means of tryptophan loss and the formation of specific lysine oxidation products: α-aminoadipic semialdehyde (AAS), α-aminoadipic acid (AAA), and Schiff bases. Frozen storage increased proteins susceptibility towards oxidation during successive technological processes. The addition of the RC extract inhibited the formation of AAS, AAA, and had an antioxidant effect towards tryptophan oxidation, but promoted the formation of Schiff bases and incremented the hardness of beef patties. The antioxidant effect may be attributed to the phenolic compounds, mainly procyanidins, found on the RC extract. Further knowledge on the interactions between phenolics and proteins is needed to optimize the application of these antioxidants against meat protein oxidation.


Frozen storage Beef patties Phenolic compounds Protein oxidation Lipid oxidation 



Mario Estévez thanks the Spanish Ministry of Science and Innovation for the contract through the “Ramón y Cajal (RYC-2009-03901)” program and the support through the project “Protein oxidation in frozen meat and dry-cured products: mechanisms, consequences and development of antioxidant strategies” (AGL2010-15134). Mario Estévez thanks the European Community for the economical support from the Marie Curie Reintegration (ERG) Fellowship (PERG-GA-2009-248959—Pox-MEAT). Mariana Utrera thanks the University of Extremadura (Uex) for the pre-doctoral grant (Human Resources Recruitment Program “C Action”).


  1. Akagawa, M., & Suyama, K. (2001). Amine oxidase-like activity of polyphenols: Mechanism and properties. European Journal of Biochemistry, 268, 1953–1963.CrossRefGoogle Scholar
  2. Bourne, M. C. (1978). Texture profile analysis. Food Technology, 33, 62–66.Google Scholar
  3. De Freitas, V., & Mateus, N. (2001). Structural features of procyanidin interactions with salivary proteins. Journal of Agriculture and Food Chemistry, 49, 940–945.CrossRefGoogle Scholar
  4. Deaville, E. R., Green, R. J., Mueller-Harvey, I., Willoughby, I., & Frazier, R. A. (2007). Hydrolyzable tannin structures influence relative globular and random coil protein binding strengths. Journal of Agriculture and Food Chemistry, 55, 4554–4561.CrossRefGoogle Scholar
  5. Estévez, M. (2011). Protein carbonyls in meat systems: A review. Meat Science, 89, 259–279.CrossRefGoogle Scholar
  6. Estévez, M., & Heinonen, M. (2010). Effect of phenolic compounds on the formation of a-aminoadipic and γ-glutamic semialdehydes from myofibrillar proteins oxidised by copper, iron, and myoglobin. Journal of Agricultural and Food Chemistry, 58, 4448–4455.CrossRefGoogle Scholar
  7. Estévez, M., Ventanas, S., & Cava, R. (2005). Protein oxidation in frankfurters with increasing levels of added rosemary essential oil: Effect on colour and texture deterioration. Journal of Food Science, 70, 427–432.CrossRefGoogle Scholar
  8. Estévez, M., Kylli, P., Puolanne, E., Kivikari, R., & Heinonen, M. (2008). Fluorescence spectroscopy as a novel approach for the assessment of myofibrillar protein oxidation in oil-in-water emulsions. Meat Science, 80, 1290–1296.CrossRefGoogle Scholar
  9. Estévez, M., Ventanas, S., Heinonen, M., & Puolanne, E. (2011). Protein carbonylation and water-holding capacity of pork subjected to frozen storage: Effect of muscle type, premincing, and packaging. Journal of Agricultural and Food Chemistry, 59, 5435–5443.CrossRefGoogle Scholar
  10. Filgueras, R. S., Gatellier, P., Ferreira, C., Zambiazi, R. C., & Santé-Lhoutellier, V. (2011). Nutritional value and digestion rate of rhea meat proteins in association with storage and cooking processes. Meat Science, 89, 6–12.CrossRefGoogle Scholar
  11. Ganhão, R., Estévez, M., Kylli, P., Heinonen, M., & Morcuende, D. (2010a). Characterization of selected wild Mediterranean fruits and comparative efficacy as inhibitors of oxidative reactions in emulsified raw pork burger patties. Journal of Agriculture and Food Chemistry, 58, 8854–8861.CrossRefGoogle Scholar
  12. Ganhão, R., Estévez, M., & Morcuende, D. (2010b). Protein oxidation in emulsified cooked burger patties with added fruit extracts: Influence on colour and texture deterioration during chill storage. Meat Science, 85, 402–409.CrossRefGoogle Scholar
  13. Halliwell, B. (2008). Are polyphenols antioxidants or pro-oxidants? What do we learn from cell culture and in vivo studies? Archives of Biochemistry and Biophysics, 476, 107–112.CrossRefGoogle Scholar
  14. Heim, K. E., Tagliaferro, A. R., & Bobilya, D. J. (2002). Flavonoid antioxidants: chemistry, metabolism and structure–activity relationships. The Journal of Nutritional Biochemistry, 13, 572–584.CrossRefGoogle Scholar
  15. Hidalgo, F. J., & Zamora, R. (2000). Modification of bovine serum albumin structure following reaction with 4,5(E)-Epoxy-2(E)-heptenal. Chemical Research in Toxicology, 13, 501–508.CrossRefGoogle Scholar
  16. Hidalgo, F. J., Alaiz, M., & Zamora, R. (1998). A spectrophotometric method for the determination of proteins damaged by oxidized lipids. Analitycal Biochemistry, 262, 129–136.CrossRefGoogle Scholar
  17. Huang, L., Xiong, Y. L., Kong, B., Huang, X., & Li, J. (2013). Influence of storage temperature and duration on lipid and protein oxidation and flavour changes in frozen pork dumpling filler. Meat Science, 95, 295–301.CrossRefGoogle Scholar
  18. Hui, Y. H., Cornillon, P., Guerrero-Legarreta, I., Lim Miang, H., Murell, K. D., & Wai-Kit, N. (2004). Handbook of frozen foods. New York: Marcel Dekker, Inc.Google Scholar
  19. Ladikos, D., & Lougovois, V. (1990). Lipid oxidation in muscle foods: A review. Food Chemistry, 35, 295–314.CrossRefGoogle Scholar
  20. Leygonie, C., Britz, T. J., & Hoffman, L. C. (2012). Impact of freezing and thawing on the quality of meat: Review. Meat Science, 91, 93–98.CrossRefGoogle Scholar
  21. Lund, M. N., Heinonen, M., Baron, C. P., & Estévez, M. (2011). Protein oxidation in muscle foods: A review. Molecular Nutrition and Food Research, 55, 83–95.CrossRefGoogle Scholar
  22. Mancini, R. A., & Hunt, M. C. (2005). Current research in meat color. Meat Science, 71, 100–121.CrossRefGoogle Scholar
  23. Min, B., & Ahn, D. U. (2005). Mechanism of lipid peroxidation in meat and meat products—A review. Food Science and Biotechnology, 14, 152–163.Google Scholar
  24. Ozdal, T., Capanoglu, E., & Altay, F. (2013). A review on protein–phenolic interactions and associated changes. Food Research International, 51, 954–970.CrossRefGoogle Scholar
  25. Petrović, L., Grujić, R., & Petrović, M. (1993). Definition of the optimal freezing rate-2. Investigation of the physico-chemical properties of beef M. longissimus dorsi frozen at different freezing rates. Meat Science, 33, 319–331.CrossRefGoogle Scholar
  26. Rawel, H. M., Kroll, J., & Rohn, S. (2001). Reactions of phenolic substances with lysozyme physicochemical characterization and proteolytic digestion of the derivatives. Food Chemistry, 72, 59–71.CrossRefGoogle Scholar
  27. Rohn, S., Rawel, H. M., & Kroll, J. (2004). Antioxidant activity of protein bound quercetin. Journal of Agriculture and Food Chemistry, 52, 4725–4729.CrossRefGoogle Scholar
  28. Scalbert, A., Johnson, I. T., & Saltmarsh, M. (2005). Polyphenols: Antioxidants and beyond. The American Journal of Clinical Nutrition, 81, 215S–217S.Google Scholar
  29. Soyer, A., Özalp, B., Dalmıs, U., & Bilgin, V. (2010). Effects of freezing temperature and duration of frozen storage on lipid and protein oxidation in chicken meat. Food Chemistry, 120, 1025–1030.CrossRefGoogle Scholar
  30. SPSS. (1999). SPSS for windows: Advanced statistic release. Chicago: SPSS.Google Scholar
  31. Stadtman, E. R. (2004). Role of oxidant species in aging. Current Medicinal Chemistry, 11, 1105–1112.CrossRefGoogle Scholar
  32. Timm-Heinrich, M., Eymard, S., Baron, C. P., Nielsen, H. H., & Jacobsen, C. (2013). Oxidative changes during ice storage of rainbow trout (Oncorhynchus mykiss) fed different ratios of marine and vegetable feed ingredients. Food Chemistry, 136, 1220–1230.CrossRefGoogle Scholar
  33. Utrera, M., & Estévez, M. (2012). Oxidation of myofibrillar proteins and impaired functionality: Underlying mechanisms of the carbonylation pathway. Journal of Agricultural and Food Chemistry, 60, 8002–8011.CrossRefGoogle Scholar
  34. Utrera, M., & Estévez, M. (2013). Impact of trolox, quercetin, genistein and gallic acid on the oxidative damage to myofibrillar proteins: The carbonylation pathway. Food Chemistry, 141, 4000–4009.CrossRefGoogle Scholar
  35. Utrera, M., Armenteros, M., Ventanas, S., Solano, F., & Estévez, M. (2012a). Pre-freezing raw hams affects quality traits in cooked hams: Potential influence of protein oxidation. Meat Science, 92, 596–603.CrossRefGoogle Scholar
  36. Utrera, M., Rodríguez-Carpena, J. G., Morcuende, D., & Estévez, M. (2012b). Formation of lysine-derived oxidation products and loss of tryptophan during processing of porcine patties with added avocado byproducts. Journal of Agricultural and Food Chemistry, 60, 3917–3926.CrossRefGoogle Scholar
  37. Utrera, M., Parra, V., & Estévez, M. (2014a). Protein oxidation during frozen storage and subsequent processing of different beef muscles. Meat Science, 96, 812–820.CrossRefGoogle Scholar
  38. Utrera, M., Morcuende, D., & Estévez, M. (2014b). Temperature of frozen storage affects the nature and consequences of protein oxidation and the interactions with lipids in beef patties. Meat Science, 96, 1250–1257.CrossRefGoogle Scholar
  39. 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 Science and Technology, 56, 62–68.CrossRefGoogle Scholar
  40. Vijayalakshmi, G., Adinarayana, M., & Rao, P. J. (2010). Kinetics and mechanisms of oxidation of some antioxidants with photochemically generated tert-butoxyl radicals. Indian Journal of Biochemistry & Biophysics, 47, 292–297.Google Scholar
  41. Vossen, E., Utrera, M., De Smet, S., Morcuende, D., & Estévez, M. (2012). Dog rose (Rosa canina L.) as a functional ingredient in porcine frankfurters without added sodium ascorbate and sodium nitrite. Meat Science, 92, 451–457.CrossRefGoogle Scholar
  42. Wang, H., Cao, G., & Prior, R. L. (1997). Oxygen radical absorbing capacity of anthocyanins. Journal of Agriculture and Food Chemistry, 45, 304–309.CrossRefGoogle Scholar
  43. Xia, X., Kong, B., Liu, Q., & Liu, J. (2009). Physicochemical change and protein oxidation in porcine longissimus dorsi as influenced by different freeze thaw cycles. Meat Science, 83, 239–245.CrossRefGoogle Scholar
  44. Zaritzky, N. (2012). Physical–chemical principles in freezing. In D. W. Sun (Ed.), Handbook of frozen food processing and packaging (pp. 3–38). Boca Raton: CRC Press.Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Mariana Utrera
    • 1
  • David Morcuende
    • 1
  • Rui Ganhão
    • 2
  • Mario Estévez
    • 1
  1. 1.IPROCAR Research Institute, Food TechnologyUniversity of ExtremaduraCáceresSpain
  2. 2.Food Science Department, School of Maritime TechnologyPolytechnic Institute of LeiriaPenichePortugal

Personalised recommendations