Collapse of the endogenous antioxidant enzymes in post-mortem broiler thigh muscles triggers oxidative stress and impairs water-holding capacity

  • Rafael H. Carvalho
  • Elza I. Ida
  • Marta S. Madruga
  • Massami Shimokomaki
  • Mario EstévezEmail author
Original Article


This study was conducted to investigate the effect of the collapse of the endogenous antioxidant enzymes, namely, catalase (CAT), glutathione peroxidase (GSH-Px) and superoxide dismutase (SOD) in post-mortem (PM) chicken thigh muscles on the extent of lipid and protein oxidation and the functionality of the muscle in terms of water-holding. To fulfil this objective, the samples were divided into two treatments: one group of muscles (n = 8) was subjected to delay cooling (DC) (at ~ 37 °C for 200 min PM) and then stored at 4 °C for 24 h. The second group (n = 8) was subjected to a normal cooling (NC): samples were immediately chilled at 4 °C for 24 h. DC samples presented a decrease in 16% of CAT, 25% GSH-Px and 20% SOD activity in relation to NC. Consistently, an increase of 36% of total carbonyl, 15% of Schiff bases and 27% of TBA-RS and 14% of tryptophan depletion was observed in DC samples, as compared to NC. The results suggested that DC challenged muscles to struggle against oxidative reactions, consuming endogenous antioxidant defenses and causing protein and lipid oxidation which in turn affect the quality and safety of chicken meat. These results emphasize the role of PM oxidative stress on chicken quality and safety. Antioxidant strategies like fast cooling may be combined with others (dietary antioxidants) to preserve chicken quality against oxidative stress.


M. peroneus longus Antioxidant enzymes Protein oxidation Carcass cooling Lipid oxidation Chicken quality 



Funding was provided by Secretaría de Estado de Investigación, Desarrollo e Innovación (Grant No. AGL2017-84586-R).


  1. Aebi H (1974) Catalase. In: Methods of enzymatic analysis, pp 673–684.
  2. Bai WK, Zhang FJ, He TJ, Su PW, Ying XZ, Zhang LL, Wang T (2016) Dietary probiotic Bacillus subtilis strain fmbj increases antioxidant capacity and oxidative stability of chicken breast meat during storage. PLoS ONE 11(12):1–17. Google Scholar
  3. Carvalho RH, Soares AL, Honorato DCB, Guarnieri PD, Pedrão MR, Paião FG, Oba A, Ida EI, Shimokomaki M (2014) The incidence of pale, soft, and exudative (PSE) turkey meat at a Brazilian commercial plant and the functional properties in its meat product. LWT Food Sci Technol 59(2):883–888. CrossRefGoogle Scholar
  4. Carvalho RH, Ida EI, Madruga MS, Martínez SL, Shimokomaki M, Estévez M (2017) Underlying connections between the redox system imbalance, protein oxidation and impaired quality traits in pale, soft and exudative (PSE) poultry meat. Food Chem 215:129–137. CrossRefGoogle Scholar
  5. Chen T, Zhou GH, Xu XL, Zhao GM, Li CB (2010) Phospholipase A2 and antioxidant enzyme activities in normal and PSE pork. Meat Sci 84(1):143–146. CrossRefGoogle Scholar
  6. Delles RM, Xiong YL, True AD, Ao T, Dawson KA (2014) Dietary antioxidant supplementation enhances lipid and protein oxidative stability of chicken broiler meat through promotion of antioxidant enzyme activity. Poult Sci 93(6):1561–1570. CrossRefGoogle Scholar
  7. Estévez M (2011) Protein carbonyls in meat systems: a review. Meat Sci 89(3):259–279. CrossRefGoogle Scholar
  8. Estévez M (2015) Oxidative damage to poultry: from farm to fork. Poult Sci 94(6):1368–1378. CrossRefGoogle Scholar
  9. Estévez M, Luna C (2017) Dietary protein oxidation: a silent threat to human health? Crit Rev Food Sci Nutr 57:3781–3793. CrossRefGoogle Scholar
  10. 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 Sci 80(4):1290–1296. CrossRefGoogle Scholar
  11. 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(3):402–409. CrossRefGoogle Scholar
  12. Ganhão R, Esévez M, Morcuende D (2011) Suitability of the TBA method for assessing lipid oxidation in a meat system with added phenolic-rich materials. Food Chem 126(2):772–778. CrossRefGoogle Scholar
  13. Hamm R (1961) Biochemistry of meat hydration. Adv Food Res 10:355–463. CrossRefGoogle Scholar
  14. 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(1–2):88–93. CrossRefGoogle Scholar
  15. Honikel KO (1987) How to measure the water-holding capacity of meat? Recommendation of standardized methods. In: Tarrant PV, Eikelenboom G, Monin G (eds) Evaluation and control of meat quality in pigs. Current topics in veterinary medicine and animal science, vol 38. Springer, Dordrecht, pp 129–142. Google Scholar
  16. Jiang Z, Lin Y, Zhou G, Luo L, Jiang S, Chen F (2009) Effects of dietary selenomethionine supplementation on growth performance, meat quality and antioxidant property in yellow broilers. J Agric Food Chem 57(20):9769–9772. CrossRefGoogle Scholar
  17. Lesiów T, Xiong YL (2013) A simple, reliable and reproductive method to obtain experimental pale, soft and exudative (PSE) pork. Meat Sci 93(3):489–494. CrossRefGoogle Scholar
  18. Liu LL, He JH, Xie HB, Yang YS, Li JC, Zou Y (2014) Resveratrol induces antioxidant and heat shock protein mRNA expression in response to heat stress in black-boned chickens. Poult Sci 93(1):54–62. CrossRefGoogle Scholar
  19. Mahecha L, Nuernberg K, Nuernberg G, Martin J, Hubbermann EM, Knoeller S, Claeyse E, De Smet S, Dannenberger D (2011) Antioxidant enzyme activities and antioxidant capacity in longissimus muscle from bulls fed diets rich in polyunsaturated fatty acids. Food Chem 127(2):379–386. CrossRefGoogle Scholar
  20. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem FEBS 47(3):469–474. CrossRefGoogle Scholar
  21. McKee SR, Sams AR (1998) Rigor mortis development at elevated temperatures induces pale exudative turkey meat characteristics. Poultry Sci 77:169–174. CrossRefGoogle Scholar
  22. Niu ZY, Min YN, Liu FZ (2017) Dietary vitamin E improves meat quality and antioxidant capacity in broilers by upregulating the expression of antioxidant enzyme genes. J Appl Anim Res 2119:1–5. Google Scholar
  23. Rysman T, Utrera M, Morcuende D, Van Royen G, Van Weyenberg S, De Smet S, Estévez M (2016) Apple phenolics as inhibitors of the carbonylation pathway during in vitro metal-catalyzed oxidation of myofibrillar proteins. Food Chem 211:784–790. CrossRefGoogle Scholar
  24. Soladoye OP, Juárez ML, Aalhus JL, Shand P, Estévez M (2015) Protein oxidation in processed meat: mechanisms and potential implications on human health. Compr Rev Food Sci Food Saf 14(2):106–122. CrossRefGoogle Scholar
  25. Utrera M, Estévez M (2012) Oxidation of myofibrillar proteins and impaired functionality: underlying mechanisms of the carbonylation pathway. J Agricutural Food Chem 60:8002−8011. CrossRefGoogle Scholar
  26. Utrera M, Morcuende D, Estévez M (2014a) Temperature of frozen storage affects the nature and consequences of protein oxidation in beef patties. Meat Sci 96(3):1250–1257. CrossRefGoogle Scholar
  27. Utrera M, Parra V, Estévez M (2014b) Protein oxidation during frozen storage and subsequent processing of different beef muscles. Meat Sci 96(1):812–820. CrossRefGoogle Scholar
  28. Wilhelm AE, Maganhini MB, Hernández-Blazquez FJ, Ida EI, Shimokomaki M (2010) Protease activity and the ultrastructure of broiler chicken PSE (pale, soft, exudative) meat. Food Chem 119(3):1201–1204. CrossRefGoogle Scholar

Copyright information

© Association of Food Scientists & Technologists (India) 2019

Authors and Affiliations

  1. 1.Graduate Program in Animal Science, Department of Veterinary Preventive MedicineLondrina State UniversityLondrinaBrazil
  2. 2.Graduate Program in Food Science, Department of Food Science and TechnologyLondrina State UniversityLondrinaBrazil
  3. 3.Post-Graduate Program in Food Science and TechnologyFederal University of ParaibaJoão PessoaBrazil
  4. 4.TECAL Research Group, IPROCAR Research InstituteUniversity of ExtremaduraCáceresSpain

Personalised recommendations