Abstract
We investigated the effects of selenium-enriched probiotics (SP) on broiler meat quality under high ambient temperature and explore their underlying mechanisms. A total of 200 1-day-old male broiler chicks (Ross 308) were randomly allotted to four treatment groups, each with five replicates, in groups of ten birds. These birds were fed a corn-soybean basal diet (C), a basal diet plus probiotics supplementation (P), a basal diet plus Se supplementation in the form of sodium selenite (SS, 0.30 mg Se/kg), and a basal diet with the addition of selenium-enriched probiotics (SP, 0.30 mg Se/kg). The experiment lasted for 42 days. The birds were sacrificed by cervical dislocation, and the breast muscles were removed for further process. Our results showed that SP diet significantly increased (p < 0.05) the physical (pH, colors, water holding capacity, drip loss, shear force) and sensory characteristics of breast meat. All P, SS, and SP supplementation enhanced the antioxidant system by increasing (p < 0.05) the Se concentrations, glutathione (GSH) levels, activities of glutathione peroxidase (GSH-Px), and superoxide dismutase (SOD) whereas decreasing (p < 0.05) malondialdehyde (MDA) levels, with SP being higher than P and SS. Moreover, SP diet significantly upregulated (p < 0.05) the mRNA levels of glutathione peroxidase genes (GPx1, GPx4) while it downregulated heat stress biomarkers such as heat shock protein (HSP) 70 as compared to C, P, and SS diets. In conclusion, our findings suggest that SP may function as beneficial nutritive supplement that is capable of improving meat quality during the summer season.
Similar content being viewed by others
References
Biesalski H-K (2005) Meat as a component of a healthy diet—are there any risks or benefits if meat is avoided in the diet? Meat Sci 70(3):5047
Skrivan M, Dlouha G, Mašata O, Ševčíková S (2008) Effect of dietary selenium on lipid oxidation, selenium and vitamin E content in the meat of broiler chickens. Czech J Anim Sci. 53:306–311
Khan AZ, Kumbhar S, Hamid M, Afzal S, Parveen F, Liu Y, Shu H, Mengistu BM, Huang K (2016) Effects of selenium-enriched probiotics on heart lesions by influencing the mRNA expressions of selenoproteins and heat shock proteins in heat stressed broiler chickens. PVJ 36(4):460–464
Akşit M, Yalcin S, Özkan S, Metin K, Özdemir D (2006) Effects of temperature during rearing and crating on stress parameters and meat quality of broilers. Poult Sci 85(11):1867–1874
Wang R, Pan X, Peng Z (2009) Effects of heat exposure on muscle oxidation and protein functionalities of pectoralis majors in broilers. Poult Sci 88(5):1078–1084
Chan JT, Omana DA, Betti M (2011) Effect of ultimate pH and freezing on the biochemical properties of proteins in turkey breast meat. Food Chem 127(1):109–117
St-Pierre N, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. J Dairy Sci. 86:E52-E779-524
Venojärvi M, Oksala N, Kinnunen S, Atalay M (2013) Chapter 23—stress proteins and heat shock proteins: role in muscle building and sports nutrition. In: Bagchi D, Nair S, Sen CK (eds) Nutrition and enhanced sports performance. Academic Press, San Diego, pp 229-235. doi:http://dx.doi.org/10.1016/B978-0-12-396454-0.00023-0
Gan F, Ren F, Chen X, Lv C, Pan C, Ye G, Shi J, Shi X, Zhou H, Shituleni SA (2013) Effects of selenium-enriched probiotics on heat shock protein mRNA levels in piglet under heat stress conditions. J Agric Food Chem 61(10):2385–2391
Gan F, Chen X, Liao SF, Lv C, Ren F, Ye G, Pan C, Huang D, Shi J, Shi X (2014) Selenium-enriched probiotics improve antioxidant status, immune function, and selenoprotein gene expression of piglets raised under high ambient temperature. J Agric Food Chem 62(20):4502–4508
Tinggi U (2003) Essentiality and toxicity of selenium and its status in Australia: a review. Toxicol Lett 137:103–110
Ahmad H, Tian J, Wang J, Khan MA, Wang Y, Zhang L, Wang T (2012) Effects of dietary sodium selenite and selenium yeast on antioxidant enzyme activities and oxidative stability of chicken breast meat. J Agric Food Chem 60(29):7111–7120
Joksimović-Todorović M, Davidović V, Sretenović L (2012) The effect of diet selenium supplement on meat quality. Biotechnol Animal Husbandry 28(3):553–561
Porto BA, Mangiapane E, Pessione A, Neves MJ, Pessione E, Martins FS (2015) Evaluation of sodium selenite effects on the potential probiotic Saccharomyces cerevisiae UFMG A-905: a physiological and proteomic analysis. J Funct Foods 17:828–836
Liu Y, Liu Q, Ye G, Khan A, Liu J, Gan F, Zhang X, Kumbhar S, Huang K (2014) Protective effects of selenium-enriched probiotics on carbon tetrachloride-induced liver fibrosis in rats. J Agric Food Chem 63(1):242–249
Fisinin VI, Papazyan TT, Surai PF (2009) Producing selenium-enriched eggs and meat to improve the selenium status of the general population. Crit Rev Biotechnol 29(1):18–28
Nido SA, Shituleni SA, Mengistu BM, Liu Y, Khan AZ, Gan F, Kumbhar S, Huang K (2016) Effects of selenium-enriched probiotics on lipid metabolism, antioxidative status, histopathological lesions, and related gene expression in mice fed a high-fat diet. Biol Trace Elem Res 171(2):399–409
Zoidis E, Pappas A, Georgiou C, Komaitis Ε, Feggeros K (2010) Selenium affects the expression of GPx4 and catalase in the liver of chicken. Comp Biochem Physiol B Biochem 155(3):294–300
Ran L, Wu X, Shen X, Zhang K, Ren F, Huang K (2010) Effects of selenium form on blood and milk selenium concentrations, milk component and milk fatty acid composition in dairy cows. J Sci Food Agr 90(13):2214–2219
NRC (1994) Nutrient requirements of poultry. National Academy Press, Washington, DC
Gamiz-Gracia L, De Castro ML (1999) Determination of selenium in nutritional supplements and shampoos by flow injection-hydride generation-atomic fluorescence spectrometry. Talanta 50(4):875–880
Pelicano ERL, De Souza P, De Souza H, Oba A, Norkus E, Kodawara L, De Lima T (2003) Effect of different probiotics on broiler carcass and meat quality. Rev Bras Cienc Avic 5(3):207–214
Hamid M, Liu D, Abdulrahim Y, Khan A, Qian G, Huang K (2017) Inactivation of Kupffer cells by selenizing astragalus polysaccharides prevents CCl4-induced hepatocellular necrosis in the male Wistar rat. Biol Trace Elem Res:1–11
Jahromi MF, Altaher YW, Shokryazdan P, Ebrahimi R, Ebrahimi M, Idrus Z, Tufarelli V, Liang JB (2016) Dietary supplementation of a mixture of Lactobacillus. IJB 60(7):1099–1110
Pan C, Zhao Y, Liao SF, Chen F, Qin S, Wu X, Zhou H, Huang K (2011) Effect of selenium-enriched probiotics on laying performance, egg quality, egg selenium content, and egg glutathione peroxidase activity. J Agric Food Chem 59(21):11424–11431
Le Bihan-Duval E, Debut M, Berri CM, Sellier N, Santé-Lhoutellier V, Jégo Y, Beaumont C (2008) Chicken meat quality: genetic variability and relationship with growth and muscle characteristics. BMC Genet 9(1):53
Zhang Z, Jia G, Zuo J, Zhang Y, Lei J, Ren L, Feng D (2012) Effects of constant and cyclic heat stress on muscle metabolism and meat quality of broiler breast fillet and thigh meat. Poult Sci 91(11):2931–2937
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
Yang Y, Meng F, Wang P, Jiang Y, Yin Q, Chang J, Zuo R, Zheng Q, Liu J (2012) Effect of organic and inorganic selenium supplementation on growth performance, meat quality and antioxidant property of broilers. AJB 11(12):3031–3036
Wang Y, Zhan X, Yuan D, Zhang X, Wu R (2011) Effects of selenomethionine and sodium selenite supplementation on meat quality, selenium distribution and antioxidant status in broilers. Czech J Anim Sci 56(7):305–313
Wang Z, Pan X, Peng Z, Zhao R, Zhou G (2009) Methionine and selenium yeast supplementation of the maternal diets affects color, water-holding capacity, and oxidative stability of their male offspring meat at the early stage. Poult Sci 88(5):1096–1101
Yao H-D, Wu Q, Zhang Z-W, Zhang J-L, Li S, Huang J-Q, Ren F-Z, Xu S-W, Wang X-L, Lei XG (2013) Gene expression of endoplasmic reticulum resident selenoproteins correlates with apoptosis in various muscles of se-deficient chicks. JN 143(5):613–619
Skomorucha I, Muchacka R, Sosnówka-Czajka E (2010) Effect of elevated air temperature on some quality parameters of broiler chicken meat. Ann Anim Sci10 (2):187-196
H-m N, Y-m G, J-x L, Zhao K, Z-x A, Zhong H (2011) Effects of methionine-Se, glycine-Zn and glycine-Cu on carcass characteristics and meat quality of broilers [J]. Hubei Agricultural Sciences 18:040
Fellenberg M, Speisky H (2006) Antioxidants: their effects on broiler oxidative stress and its meat oxidative stability. Worlds Poult Sci J 62(01):53–70
Miezeliene A, Alencikiene G, Gruzauskas R, Barstys T (2011) The effect of dietary selenium supplementation on meat quality of broiler chickens. Biotechnol Agron Soc 15:61
Briens M, Mercier Y, Rouffineau F, Vacchina V, Geraert P-A (2013) Comparative study of a new organic selenium source v. seleno-yeast and mineral selenium sources on muscle selenium enrichment and selenium digestibility in broiler chickens. BJN110 (04):617-624
Rayman MP (2004) The use of high-selenium yeast to raise selenium status: how does it measure up? BJN 92(04):557–573
Pophaly SD, Singh P, Kumar H, Tomar SK, Singh R (2014) Selenium enrichment of lactic acid bacteria and bifidobacteria: a functional food perspective. Trends Food Sci Technol 39(2):135–145
Zhan X, Wang M, Zhao R, Li W, Xu Z (2007) Effects of different selenium source on selenium distribution, loin quality and antioxidant status in finishing pigs. Anim Feed Sci Technol 132(3):202–211
Bellinger FP, Raman AV, Reeves MA, Berry MJ (2009) Regulation and function of selenoproteins in human disease. BCJ 422(1):11–22
Huang J-Q, Li D-L, Zhao H, Sun L-H, Xia X-J, Wang K-N, Luo X, Lei XG (2011) The selenium deficiency disease exudative diathesis in chicks is associated with downregulation of seven common selenoprotein genes in liver and muscle. NJ 141(9):1605–1610
Mahmoud KZ, Edens F (2005) Influence of organic selenium on HSP70 response of heat-stressed and enteropathogenic Escherichia coli-challenged broiler chickens (Gallus gallus). Comp Biochem Physiol C: Pharmacol Toxicol 141(1):69–75
Sunde RA, Hadley KB (2010) Phospholipid hydroperoxide glutathione peroxidase (Gpx4) is highly regulated in male turkey poults and can be used to determine dietary selenium requirements. EBM 235(1):23–31
Liao X, Lu L, Li S, Liu S, Zhang L, Wang G, Li A, Luo X (2012) Effects of selenium source and level on growth performance, tissue selenium concentrations, antioxidation, and immune functions of heat-stressed broilers. Biol Trace Elem Res 150(1–3):158–165
Hao Y, Gu X (2014) Effects of heat shock protein 90 expression on pectoralis major oxidation in broilers exposed to acute heat stress. Poult. Sci:PS3993
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31272627,31472253), the Research Fund for Doctoral Program of Higher Education in China (20110097110014, 20120097130002), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
Authorship
K.H. formulated the research question and designed the research; A.Z.K., S.K., Y.L., M.H., C.P., S.A.N., and F.P. conducted the research. A.Z.K., S.K., Y.L., and K.H. analyzed the data; A.Z.K and K.H. wrote the paper; and K.H. is responsible for the final content. All authors read and approved the final manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All protocols for conducting the experimental animals were approved by the “Committee for Care and Use of Experimental Animals” of Nanjing Agriculture University (animal ethical number: SYXK (Su) 2011-0036).
Conflict of Interest
The authors declare that they have no conflicts of interest.
Rights and permissions
About this article
Cite this article
Khan, A.Z., Kumbhar, S., Liu, Y. et al. Dietary Supplementation of Selenium-Enriched Probiotics Enhances Meat Quality of Broiler Chickens (Gallus gallus domesticus) Raised Under High Ambient Temperature. Biol Trace Elem Res 182, 328–338 (2018). https://doi.org/10.1007/s12011-017-1094-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12011-017-1094-z