Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aebi H (1974) Catalase. In: Methods of enzymatic analysis, pp 673–684. https://doi.org/10.1016/B978-0-12-091302-2.50032-3
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. https://doi.org/10.1371/journal.pone.0167339
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. https://doi.org/10.1016/j.lwt.2014.07.019
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. https://doi.org/10.1016/j.foodchem.2016.07.182
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. https://doi.org/10.1016/j.meatsci.2009.08.039
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. https://doi.org/10.3382/ps.2013-03682
Estévez M (2011) Protein carbonyls in meat systems: a review. Meat Sci 89(3):259–279. https://doi.org/10.1016/j.meatsci.2011.04.025
Estévez M (2015) Oxidative damage to poultry: from farm to fork. Poult Sci 94(6):1368–1378. https://doi.org/10.3382/ps/pev094
Estévez M, Luna C (2017) Dietary protein oxidation: a silent threat to human health? Crit Rev Food Sci Nutr 57:3781–3793. https://doi.org/10.1080/10408398.2016.1165182
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. https://doi.org/10.1016/j.meatsci.2008.06.004
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. https://doi.org/10.1016/j.meatsci.2010.02.008
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. https://doi.org/10.1016/j.foodchem.2010.11.064
Hamm R (1961) Biochemistry of meat hydration. Adv Food Res 10:355–463. https://doi.org/10.1016/S0065-2628(08)60141-X
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. https://doi.org/10.1016/j.ifset.2005.10.001
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. https://doi.org/10.1007/978-94-009-3301-9_11
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. https://doi.org/10.1021/jf902411c
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. https://doi.org/10.1016/j.meatsci.2012.11.022
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. https://doi.org/10.3382/ps.2013-03423
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. https://doi.org/10.1016/j.foodchem.2010.12.117
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. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
McKee SR, Sams AR (1998) Rigor mortis development at elevated temperatures induces pale exudative turkey meat characteristics. Poultry Sci 77:169–174. https://doi.org/10.1093/ps/77.1.169
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. https://doi.org/10.1080/09712119.2017.1309321
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. https://doi.org/10.1016/j.foodchem.2016.05.126
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. https://doi.org/10.1111/1541-4337.12127
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. https://doi.org/10.1021/jf302111j
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. https://doi.org/10.1016/j.meatsci.2013.10.032
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. https://doi.org/10.1016/j.meatsci.2013.09.006
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. https://doi.org/10.1016/j.foodchem.2009.08.034
Funding
Funding was provided by Secretaría de Estado de Investigación, Desarrollo e Innovación (Grant No. AGL2017-84586-R).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Carvalho, R.H., Ida, E.I., Madruga, M.S. et al. Collapse of the endogenous antioxidant enzymes in post-mortem broiler thigh muscles triggers oxidative stress and impairs water-holding capacity. J Food Sci Technol 56, 1371–1379 (2019). https://doi.org/10.1007/s13197-019-03611-1
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-019-03611-1