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Phenolic-rich extracts from Willowherb (Epilobium hirsutum L.) inhibit lipid oxidation but accelerate protein carbonylation and discoloration of beef patties

Abstract

An extraction procedure of phenolics from Willowherb (Epilobium hirsutum L.) was optimized; extracts were characterized in terms of phenolic content, composition, and in vitro antioxidant activity. Additionally, the effect of 50, 200, and 800 ppm Willowherb extracts on the oxidative stability (formation of thiobarbituric acid-reactive substances, α-aminoadipic, and γ-glutamic semialdehydes) of beef patties was studied. Acetone (50 %) extract, rich in ellagic acid, myricetin, hydroxybenzoic, and hydroxycinnamic acids, had the highest phenolic content compared to methanol (25, 50, 75, and 100 %), acetone (100 %), or water extracts and displayed intense in vitro antioxidant properties. Lipid oxidation levels in processed beef patties with added Willowherb extract remained as similar to that of 100 ppm gallic acid. A dose-dependent effect of Willowherb extract was observed on protein carbonylation and myoglobin oxidation. The lack of correlation between lipid and myoglobin oxidation and the underlying mechanisms involved in the pro-oxidant action of phenolics on meat proteins are thoroughly discussed.

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References

  1. Frankel E (1996) Antioxidants in lipid foods and their impact on food quality. Food Chem 57:51–55

    CAS  Article  Google Scholar 

  2. Faustman C, Sun Q, Mancini R, Suman SP (2010) Myoglobin and lipid oxidation interactions: mechanistic bases and control. Meat Sci 86:86–94

    CAS  Article  Google Scholar 

  3. Lund MN, Heinonen M, Baron CP, Estévez M (2011) Protein oxidation in muscle foods: a review. Mol Nutr Food Res 55:83–95

    CAS  Article  Google Scholar 

  4. 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 Sci 85:402–409

    Article  Google Scholar 

  5. 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 by products. J Agric Food Chem 60:3917–3926

    CAS  Article  Google Scholar 

  6. Estévez M (2011) Protein carbonyls in meat systems: a review. Meat Sci 89:259–279

    Article  Google Scholar 

  7. Estévez M, Ollilainen V, Heinonen M (2009) Analysis of protein oxidation markers α-aminoadipic and γ-glutamic semialdehydes in food proteins by using LC–ESI–multi-stage tandem MS. J Agric Food Chem 57:3901–3910

    Article  Google Scholar 

  8. Utrera M, Morcuende D, Rodríguez-Carpena JG, Estévez M (2011) Fluorescent HPLC for the detection of specific protein oxidation carbonyls—α-aminoadipic and γ-glutamic semialdehydes—in meat systems. Meat Sci 89:500–506

    CAS  Article  Google Scholar 

  9. Utrera M, Armenteros M, Ventanas S, Solano F, Estévez M (2012) Pre-freezing raw hams affects quality traits in cooked hams: potential influence of protein oxidation. Meat Sci 92:596–603

    CAS  Article  Google Scholar 

  10. Utrera M, Estévez M (2012) Oxidation of myofibrillar proteins and impaired functionality: underlying mechanisms of the carbonylation pathway. J Agric Food Chem 60:8002–8011

    CAS  Article  Google Scholar 

  11. Jia N, Kong B, Liu Q, Diao X, Xia X (2012) Antioxidant activity of black currant (Ribes nigrum L.) extract and its inhibitory effect on lipid and protein oxidation of pork patties during chilled storage. Meat Sci 91:533–539

    CAS  Article  Google Scholar 

  12. 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 Sci 92:451–457

    CAS  Article  Google Scholar 

  13. Tomás-Barberán FA, Andrés-Lacueva C (2012) Polyphenols and health: current state and progress. J Agric Food Chem 60:8773–8775

    Article  Google Scholar 

  14. 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 72:348–355

    Article  Google Scholar 

  15. Utrera M, Estévez M (2012) Analysis of tryptophan oxidation by fluorescence spectroscopy: effect of metal-catalyzed oxidation and selected phenolic compounds. Food Chem 135:88–93

    CAS  Article  Google Scholar 

  16. 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 223:461–468

    CAS  Article  Google Scholar 

  17. 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 58:4448–4455

    Article  Google Scholar 

  18. 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 128:276–283

    CAS  Article  Google Scholar 

  19. Kiss A, Kowalski J, Melzig MF (2004) Compounds from Epilobium angustifolium inhibit the specific metallopeptidases ACE, NEP and APN. Planta Med 70:919–923

    CAS  Article  Google Scholar 

  20. Barakat HH, Hussein SAM, Marzouk MS, Merfort I, Linscheid M, Nawwar MAM (1997) Polyphenolic metabolites of Epilobium hirsutum. Phytochemistry 46:935–941

    CAS  Article  Google Scholar 

  21. Wojdyło A, Oszmiański J, Czemerys R (2007) Antioxidant activity and phenolic compounds in 32 selected herbs. Food Chem 105:940–949

    Article  Google Scholar 

  22. Rey AI, Hopia A, Kivikari R, Kahkonen M (2005) Use of natural food/plant extracts: cloudberry (Rubus Chamaemorus), beetroot (Beta Vulgaris ‘‘Vulgaris’’) or Willow herb (Epilobium angustifolium) to reduce lipid oxidation of cooked pork patties. Lebensm Wiss Technol 38:363–370

    CAS  Article  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. Ross KA, Beta T, Arntfield SD (2009) A comparative study on the phenolic acids identified and quantified in dry beans using HPLC as affected by different extraction and hydrolysis methods. Food Chem 113:336–344

    CAS  Article  Google Scholar 

  25. Apak R, Güçlü K, Ozyürek M, Karademir SE (2004) Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. J Agric Food Chem 29:7970–7981

    Article  Google Scholar 

  26. AOAC (2000) Official methods of analysis. Association of Official Analytical Chemists, Gaithersburgh, p 2000

    Google Scholar 

  27. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  28. MacDougall DB (1994) Colour of meat. In: Pearson AM, Dutson TR (eds) Quality attributes and their measurement in meat, poultry and their products, vol. 9. Advances in Meat Research Series, pp 79–94

  29. Kähkönen MP, Hopia AI, Vuorela HJ, Rauha JP, Pihlaja K, Kujala TS, Heinonen M (1999) Antioxidant activity of plant extracts containing phenolic compounds. J Agric Food Chem 47:3954–3962

    Article  Google Scholar 

  30. Turkmen N, Velioglu YS (2007) Determination of alkaloids and phenolic compounds in black tea processed by two different methods in different plucking seasons. J Agric Food Chem 87:1408–1416

    CAS  Article  Google Scholar 

  31. Rodríguez-Carpena JG, Morcuende D, Andrade MJ, Kylli P, Estévez M (2011) Avocado (Persea americana Mill.) phenolics, in vitro antioxidant and antimicrobial activities, and inhibition of lipid and protein oxidation in porcine patties. J Agric Food Chem 59:5625–5635

    Article  Google Scholar 

  32. Chavan UD, Shahidi F, Naczk M (2001) Extraction of condensed tannins from beach pea (Lathyrus maritimus L.) as affected by different solvents. Food Chem 75:509–512

    CAS  Article  Google Scholar 

  33. Zhou K, Su L, Yu LL (2004) Phytochemicals and antioxidant properties in wheat bran. J Agric Food Chem 52:6108–6114

    CAS  Article  Google Scholar 

  34. Shikov AN, Poltanov EA, Dorman HJ, Makarov VG, Tikhonov VP, Hiltunen R (2006) Chemical composition and in vitro antioxidant evaluation of commercial water-soluble willow herb (Epilobium angustifolium L.) extracts. J Agric Food Chem 54:3617–3624

    CAS  Article  Google Scholar 

  35. Tóth BH, Blazics B, Kery A (2009) Polyphenol composition and antioxidant capacity of Epilobium species. J Pharm Biomed Anal 49:26–31

    Article  Google Scholar 

  36. Remmel I, Vares L, Toom L, Matto V, Raal A (2012) Phenolic compounds in five Epilobium species collected from Estonia. Nat Prod Commun 7:1323–1324

    CAS  Google Scholar 

  37. Bajer M, Kosakowska O, Pelc M, Bączek K (2008) Właściwości przeciwutleniające organów wegetatywnych Wiesiołka (Oenothera sp.) I Wierzbownicy (Epilobium sp). Zeszyty Problemowe Postępów Nauk Rolniczych 527:67–72

    Google Scholar 

  38. Meier B, Sticher O, Julkunen-Tiitto R (1988) Pharmaceutical aspects of the use of willows in herbal remedies. Planta Med 54:559–560

    CAS  Article  Google Scholar 

  39. Chobot V, Hadacek F (2011) Exploration of pro-oxidant and antioxidant activities of the flavonoid myricetin. Redox Rep 16:242–247

    CAS  Article  Google Scholar 

  40. Sun WQ, Zhang YJ, Zhou GH, Xu XL, Peng ZQ (2010) Effect of apple polyphenol on oxidative stability of sliced cooked cured beef and pork hams during chilled storage. J Muscle Foods 21:722–737

    CAS  Article  Google Scholar 

  41. Rietjens IMCM, Boersma MG, de Haan L, Spenkelink B, Awad HM, Cnubben NHP, van Zanden JJ, van der Woude H, Alink GM, Koeman JH (2002) The pro-oxidant chemistry of the natural antioxidants vitamin C, vitamin E, carotenoids and flavonoids. Environ Toxicol Pharmacol 11:321–333

    CAS  Article  Google Scholar 

  42. Akagawa M, Ishii Y, Ishii T, Shibata T, Yotsu-Yamashita M, Suyama K, Uchida K (2006) Metal-catalyzed oxidation of protein-bound dopamine. Biochem 45:15120–15128

    CAS  Article  Google Scholar 

  43. McBride NTM, Hogan SA, Kerry JP (2007) Comparative addition of rosemary extract and additives on sensory and antioxidant properties of retail packaged beef. Int J Food Sci Technol 42:1201–1207

    CAS  Article  Google Scholar 

  44. Hayes JE, Stepanyan V, Allen P, O’Grady MN, O’Brien NM, Kerry JP (2009) The effect of lutein, sesamol, ellagic acid and olive leaf extract on lipid oxidation and oxymyoglobin oxidation in bovine and porcine muscle model systems. Meat Sci 83:201–208

    CAS  Article  Google Scholar 

  45. Castro CE, Hathaway GM, Havlin R (1977) Oxidation and reduction of iron porphyrins and hemoproteins by quinones and hydroquinones. J Am Chem Soc 99:8032–8039

    CAS  Article  Google Scholar 

  46. Li H, Guo A, Wang H (2008) Mechanisms of oxidative browning of wine. Food Chem 108:1–13

    CAS  Article  Google Scholar 

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Acknowledgments

This paper belongs to a Master Thesis from the Official Master in Meat Science and Technology (University of Extremadura) funded by CONSOLIDER-CARNISENUSA project (Ref. CSD2007-00016). The Spanish Ministry of Economy and Competitiveness is acknowledged 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.” The European Community (Research Executive Agency) is acknowledged for the Marie Curie Reintegration Fellowship (PERG05-GA-2009-248959; Pox-MEAT).

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This article does not contain any studies with human or animal subjects.

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Correspondence to Mario Estévez.

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Cando, D., Morcuende, D., Utrera, M. et al. Phenolic-rich extracts from Willowherb (Epilobium hirsutum L.) inhibit lipid oxidation but accelerate protein carbonylation and discoloration of beef patties. Eur Food Res Technol 238, 741–751 (2014). https://doi.org/10.1007/s00217-014-2152-9

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  • DOI: https://doi.org/10.1007/s00217-014-2152-9

Keywords

  • Phenolic compounds
  • Willowherb
  • TBARS
  • Protein carbonylation
  • Discoloration