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Effects of increasing dietary sodium selenite and selenium yeast levels on growth performance, meat quality and muscle anti-oxidative capacity of broilers

Abstract

The objective of this experiment was to assess the effects of dietary sodium selenite and selenium (Se) yeast levels on growth performance, meat quality and muscle anti-oxidative capacity of broilers. A total of 360 1-day-old Cobb broilers were randomly assigned to 5 dietary treatments for 6 weeks. Diets (corn-soybean meal based diets) were supplemented with 0 mg/kg, 0.3 mg/kg and 0.6 mg/kg sodium selenium, and 0.3 mg/kg and 0.6 mg/kg selenium yeast, respectively. The results showed that Feed/Gain was significantly decreased with the increase of Se supplemental level during day 1-21 (P < 0.05), and body weight gain and Feed/Gain of broilers were improved with the increase of Se supplemental level by day 22 to 42 (P < 0.05). The dietary Se levels significantly affected the a*, cohesion, adhesion, chewing and recovery values of meat as well (P < 0.05). Se supplementation in diets also increased DPPH, hydroxyl radical scavenging and SOD, but significantly decreased TBARS and POV values compared to control (P < 0.05). The biological utilization rates of organic Se against inorganic Se were 116.0%, 123.1%, 109.7%, 109.8%, and 135.2%, respectively. The present results supported that organic Se was more bio-available and more effective in terms of growth performance, meat quality, muscle antioxidant and organ deposition efficiency compared to inorganic selenium. Therefore, the addition of 0.6 mg/kg selenium yeast (SY) during broiler breeding was the most effective.

Keywords:
broilers; growth performance; anti-oxidative capacity; meat quality; selenium

1 Introduction

The color, texture, and flavor of meat influence consumer choice, while the richness of trace elements in meat stimulates consumer demand (Sottero et al., 2019Sottero, B., Leonarduzzi, G., Testa, G., Gargiulo, S., Poli, G., & Biasi, F. (2019). Lipid oxidation derived aldehydes and oxysterols between health and disease. European Journal of Lipid Science and Technology, 121(1), 1700047. http://dx.doi.org/10.1002/ejlt.201700047.
http://dx.doi.org/10.1002/ejlt.201700047...
). Selenium (Se), as a trace element, is essential for organisms to perform their vital functions. Se is one of the essential nutrients in the human body, which can regulate the synthesis of glutathione peroxidase in the body, and protect cells apart from damage and maintain the function of cell membranes. At the same time, Se is also irreplaceable in the body's immune function, and has the effects of enhancing human immunity, anti-aging, and anti-tumor (Nguyen et al., 2022Nguyen, M. H., Xiao, H., Tan, X., Chen, F., & Shi, X. (2022). Comparative growth, biochemical and sensory analyses reveal the feasibility of large-scale development of selenium-enriched Tartary buckwheat sprouts. Food Science and Technology, 42, e81722.; Zhang et al., 2022Zhang, H.-Y., Wang, Q., Shi, L.-Y., Zhang, X.-F., & Zhang, H.-L. (2022). Synthesis and antioxidant activity of selenium polysaccharide from Lotus root. Food Science and Technology, 42, e40522. http://dx.doi.org/10.1590/fst.40522.
http://dx.doi.org/10.1590/fst.40522...
). Related studies have found that Se supplementation is important for animal and human health as well as for ecological improvement (Liu et al., 2022Liu, M., Cao, W., Gao, P., Zhao, J., Muhammad, U., Ni, S., Zhou, Y., Wang, S., Pei, F., Zhang, Z., Yuan, L., Wang, Z., Cui, A., Chen, Z., Feng, Z., Hu, K., Chen, H., & Zuo, S. (2022). Effects of two different selenium fertilizers on accumulation of selenium and heavy metals in rice grains in field trials. Food Science and Technology, 42, e117521. http://dx.doi.org/10.1590/fst.117521.
http://dx.doi.org/10.1590/fst.117521...
). Adequate amounts of Se in the organism have an important role in maintaining normal muscle function (Pappas et al., 2012Pappas, A. C., Zoidis, E., Papadomichelakis, G., & Fegeros, K. (2012). Supranutritional selenium level affects fatty acid composition and oxidative stability of chicken breast muscle tissue. Journal of Animal Physiology and Animal Nutrition, 96(3), 385-394. http://dx.doi.org/10.1111/j.1439-0396.2011.01152.x. PMid:21535232.
http://dx.doi.org/10.1111/j.1439-0396.20...
; Chen et al., 2017Chen, F., Zhu, L., Qiu, H., & Qin, S. (2017). Selenium-enriched Saccharomyces cerevisiae improves growth, antioxidant status and selenoprotein gene expression in Arbor Acres broilers. Journal of Animal Physiology and Animal Nutrition, 101(2), 259-266. http://dx.doi.org/10.1111/jpn.12571. PMid:27868237.
http://dx.doi.org/10.1111/jpn.12571...
; Zoidis et al., 2018Zoidis, E., Seremelis, I., Kontopoulos, N., & Danezis, G. P. (2018). Selenium-dependent antioxidant enzymes: actions and properties of selenoproteins. Antioxidants, 7(5), 66. http://dx.doi.org/10.3390/antiox7050066. PMid:29758013.
http://dx.doi.org/10.3390/antiox7050066...
). Se deficiency leads to a decrease in the expression and activity of related selenoproteins, causing the development of muscle degenerative diseases such as Keshan's disease in humans, mulberry heart disease in pigs, and white muscle diseases in foals (Delesalle et al., 2017Delesalle, C., de Bruijn, M., Wilmink, S., Vandendriessche, H., Mol, G., Boshuizen, B., Plancke, L., & Grinwis, G. (2017). White muscle disease in foals: focus on selenium soil content. A case series. BMC Veterinary Research, 13(1), 121. http://dx.doi.org/10.1186/s12917-017-1040-5. PMid:28468621.
http://dx.doi.org/10.1186/s12917-017-104...
; Hosnedlova et al., 2017Hosnedlova, B., Kepinska, M., Skalickova, S., Fernandez, C., Ruttkay-Nedecky, B., Malevu, T. D., Sochor, J., Baron, M., Melcova, M., Zidkova, J., & Kizek, R. (2017). A summary of new findings on the biological effects of selenium in selected animal species: a critical review. International Journal of Molecular Sciences, 18(10), 2209. http://dx.doi.org/10.3390/ijms18102209. PMid:29065468.
http://dx.doi.org/10.3390/ijms18102209...
).

The bio-availability of Se in animals and its pharmacological and toxicological effects are related to its chemical form (Han et al., 2017Han, X. J., Qin, P., Li, W. X., Ma, Q. G., Ji, C., Zhang, J. Y., & Zhao, L. H. (2017). Effect of sodium selenite and selenium yeast on performance, egg quality, antioxidant capacity, and selenium deposition of laying hens. Poultry Science, 96(11), 3973-3980. http://dx.doi.org/10.3382/ps/pex216. PMid:29050423.
http://dx.doi.org/10.3382/ps/pex216...
). Adding a certain amount of organic Se to the diet has a certain degree of improvement on the growth performance, serum antioxidant index and meat quality of animals. It has also been reported that organic Se exhibits higher efficiency than inorganic Se in reducing the frequency of pectoralis PSE meat (Bakhshalinejad et al., 2019Bakhshalinejad, R., Hassanabadi, A., & Swick, R. A. (2019). Dietary sources and levels of selenium supplements affect growth performance, carcass yield, meat quality and tissue selenium deposition in broilers. Animal Nutrition, 5(3), 256-263. http://dx.doi.org/10.1016/j.aninu.2019.03.003. PMid:31528727.
http://dx.doi.org/10.1016/j.aninu.2019.0...
; Mariezcurrena-Berasain et al., 2022Mariezcurrena-Berasain, M. D., Mariezcurrena-Berasain, M. A., Lugo, J., Libien-Jimenez, Y., Pinzon-Martinez, D. L., Salem, A., & Garcia-Fabila, M. (2022). Effects of dietary supplementation with organic selenium-enriched yeast on growth performance, carcass characteristics, and meat quality of finishing lambs. Tropical Animal Health and Production, 54(1), 49. http://dx.doi.org/10.1007/s11250-021-02992-w. PMid:35020037.
http://dx.doi.org/10.1007/s11250-021-029...
). In poultry farming, there are two main sources of Se supplementation, namely inorganic Se (mainly sodium selenite, Na2SeO3) and organic Se (mainly Se-Yeast or Se-Met preparations). Sodium selenite plays an important role in improving growth and health of poultry as a conventional Se sources in poultry diets (Han et al., 2017Han, X. J., Qin, P., Li, W. X., Ma, Q. G., Ji, C., Zhang, J. Y., & Zhao, L. H. (2017). Effect of sodium selenite and selenium yeast on performance, egg quality, antioxidant capacity, and selenium deposition of laying hens. Poultry Science, 96(11), 3973-3980. http://dx.doi.org/10.3382/ps/pex216. PMid:29050423.
http://dx.doi.org/10.3382/ps/pex216...
). Related studies had shown that organic Se is more readily absorbed and utilized by the organism compared to inorganic Se (Attia et al., 2010Attia, A., Abdalah, A. A., Zeweil, H. S., Bovera, F., Tag El-Din, A. A., & Araft, M. A. (2010). Effect of inorganic or organic selenium supplementation on productive performance, egg quality and some physiological traits of dual-purpose breeding hens. Czech Journal of Animal Science, 55(11), 505-519. http://dx.doi.org/10.17221/1715-CJAS.
http://dx.doi.org/10.17221/1715-CJAS...
; Delezie et al., 2014Delezie, E., Rovers, M., Van der Aa, A., Ruttens, A., Wittocx, S., & Segers, L. (2014). Comparing responses to different selenium sources and dosages in laying hens. Poultry Science, 93(12), 3083-3090. http://dx.doi.org/10.3382/ps.2014-04301. PMid:25352676.
http://dx.doi.org/10.3382/ps.2014-04301...
) .

Although some previous studies have investigated the toxic levels of dietary Se in poultry production (Michalczuk et al., 2021Michalczuk, M., Batorska, M., Sikorska, U., Bien, D., Urban, J., Capecka, K., & Konieczka, P. (2021). Selenium and the health status, production results, and product quality in poultry. Animal Science Journal, 92(1), e13662. http://dx.doi.org/10.1111/asj.13662. PMid:34786781.
http://dx.doi.org/10.1111/asj.13662...
), there was a lack of data regarding comparison of the growth performance, meat quality, and organ Se enrichment and antioxidant capacity of broilers.

Therefore, the effects of the two kinds of Se sources on the growth performance, meat quality and muscle antioxidant indexes of broilers were compared by adding organic Se and inorganic Se to the diet in this study, and which provided reference materials for the application of organic Se in poultry production and new ideas for the development of Se-rich muscle products.

2 Materials and methods

2.1 Ethics statement

The protocol was reviewed and approved by the Animal Care and Use Committee of Gansu Agricultural University. All procedures were carried out in strict accordance with the recommendations in the Guide for Guidelines for Experimental Animals of the Ministry of Science and Technology (Beijing, China), and all efforts were made to minimize suffering (AEC-CAAS-20191003).

2.2 Broilers management and experimental design

A total of 360 Cobb broilers (one-day-old) were randomly allocated into five dietary treatments with six replicates and twelve broilers in each. The feeding period was 42 d, and which was divided into two stages: starter (0-21 d) and finisher (22-42 d). The basic experimental diets were formulated according to the nutritional requirements of China’s agricultural industry standard for raising chickens (NY/T33-2004). The Se content of basal diets was 0.138 mg/kg on a dry matter basis. The ingredient composition and estimated nutrient content of the experimental basal diets are given in Table 1. This diet was supplemented with sodium selenite or Se yeast at 0.3 and 0.6 mg/kg feed, respectively.

Table 1
Ingredient composition and Nutrient Content of the Basal Diets.

2.3 Growth performance and health status

All broilers were raised in three-tier battery cages with 12 broilers in one individual experimental unit (cages) (160 × 70 cm) with 20 h of light/day through-out the trial. The experiment was conducted with the temperature maintained at 34 °C at the arrival of the bird in an environmentally controlled room and gradually decreased. A total of 30 replicates of the 5 treatments were randomly distributed into 30 cages in the chicken house. Each cage is equipped with a feeding trough and 4 nipple drinkers. Chicks were provided with water and feed ad libitum. This experiment was conducted under strict bio-security measures. The broilers were vaccinated against Newcastle Disease (7 and 21 d post-hatch) and Infectious Bursal Disease (14 and 28 d post-hatch). At 0, 21 and 42 days of feeding for determination of growth performance, including body weight gain (BWG), feed intake (FI), and feed gain ratio (F/G). Mortalities and post-mortem weight were recorded daily for the calculation of mortality, body weight gain, and mortality-corrected F/G.

2.4 Meat quality

At the end of the experiment, one bird per replicate with body weight near the replicate average value (i.e., 6 broilers per treatment) was selected and weighed from each cage. The selected birds were euthanized by CO2 inhalation and then immediately dissected to collect a thigh muscle sample. The pH was measured by portable pH-meter (Testo 205 pH meter, Lenzkirch, Germany) and average values at three different points were obtained for each sample. CIE (International Commission on Lumination) lightness (L∗), redness (a∗), and yellowness (b∗) value measurements were analyzed using a colorimeter (Konica Minolta CR-300, Minolta Co., Ltd., Osaka, Japan) at 24 h after slaughter and were calculated for different points as the average of 5 repetitions; while flakes of fat and connective tissue were avoided. Quality and structural indices, such as hardness, elasticity, adhesion, mastication and recovery, were determined using the model in Texture meter (Universal TA, Henan, China). Cooking loss values of samples were determined according to outlined by Renaudeau & Mourot (2007)Renaudeau, D., & Mourot, J. (2007). A comparison of carcass and meat quality characteristics of Creole and Large White pigs slaughtered at 90 kg BW. Meat Science, 76(1), 165-171. http://dx.doi.org/10.1016/j.meatsci.2006.10.024. PMid:22064203.
http://dx.doi.org/10.1016/j.meatsci.2006...
. Before cooking, meat samples were dried to keep the surface moisture away and weighed accurately. Then the muscle samples were put in cooking bags and cooked in a water bath until a core temperature of reached to 70 °C was reached. Finally, the packaging was subsequently removed and the samples were dried and weighted again as the same process. The cooking loss rate of meat sample was calculated according to the following Formula 1:

Cooking loss % = M 1 M 2 M 1 × 100 % (1)

In the formula, M1 is the mass of meat samples before cooking (g), M2 is the mass of meat samples after cooking (g).

Same after cooking, each muscle strips were sampled along parallel with the muscle fibers orientation using an equipped sampler with a 30 kg tension/compression load cell, and the shear force values were determined with a Warner-Bratzler shear force (WBSF) (model TA-XT2i, Stable Micro Systems, UK). The average value of five replicates was used for statistical analysis.

2.5 Chemical analysis

One gram of frozen muscle samples was homogenized in 9 mL of ice-cold 0.9% saline solution, and the homogenate was centrifuged at 4000 rmp for 15 min at 4°C. The supernatant was then used for further analysis. Superoxide dismutase (SOD) activity was determined using an assay kit purchased from Nanjing Jiancheng Institute of Biological Engineering (Nanjing, China). The POV (Peroxide Value) was expressed as the unit of mmol O2/kg muscle. TBARS (Thiobarbituric acid-reactive substances) was calculated from a standard curve of MDA (Malonaldehyde) and was expressed as the unit of mg MDA/kg muscle (Borella et al., 2019Borella, T.G., Peccin, M. M., Mazon, J. M., Roman, S. S., Cansian, R. L., Soares, M. B. A., 2019. Effect of rosemary (Rosmarinus officinalis) antioxidant in industrial processing of frozen-mixed hamburger during shelf life. Journal of Food Processing and Preservation, 43(9), e14092. https://doi.org/10.1111/jfpp.14092.
https://doi.org/10.1111/jfpp.14092...
).

To determine Se, feeds and meat samples were digested using the MDS-2000 microwave oven in a mixture of nitric acid (HNO3) and hydrogen peroxide (H2O2) (LabX, Midland, ON, Canada). The Se content assay of meat and organ was performed following the method of Pan et al. (2007)Pan, C., Huang, K., Zhao, Y., Qin, S., Chen, F., & Hu, Q. (2007). Effect of selenium source and level in hen’s diet on tissue selenium deposition and egg selenium concentrations. Journal of Agricultural and Food Chemistry, 55(3), 1027-1032. http://dx.doi.org/10.1021/jf062010a. PMid:17263508.
http://dx.doi.org/10.1021/jf062010a...
using an AF-610A atomic fluorescence spectrometer (Beijing Beifen-Ruili Analytical Instrument Co., Ltd., Yangzhou, China). To determine the concentration of lactate (LA), muscle samples frozen in liquid nitrogen were homogenized in 4.5 mL of normal saline, and centrifuged at 2000 × g at 4 °C, and then 1 mL of the supernatant was diluted with 4 mL of distilled water, mix with 1 mL of enzyme reaction mixture and 0.2 mL of developer and add 2 mL of terminator. Lactate content was used to determine the concentration of spectrophotometrically (530 nm) using a commercial kit (Nanjing Jiancheng Bioengineering Institute, Nanjing, China).

2.6 Free radical scavenging activity of thigh muscles

2,2-Diphenyil-1-picrylhydrazyl (DPPH) radical scavenging activity of meat was determined using the conventional DPPH method as described by Goffman & Bergman (2004)Goffman, F. D., & Bergman, C. J. (2004). Rice kernel phenolic content and its relationship with antiradical efficiency. Journal of the Science of Food and Agriculture, 84(10), 1235-1240. http://dx.doi.org/10.1002/jsfa.1780.
http://dx.doi.org/10.1002/jsfa.1780...
. The amount of DPPH was determined at 515 nm, the amount of DPPH was determined at 520 nm, and an ethanolic stock solution (0.4 mL) at each sample of various concentration was added to 1.6 mL of the DPPH solution (80 mg DPPH per liter of 100% ethanol), which was placed at room temperature for 30 minutes. The calculation Formula 2 of DPPH free radical scavenging activity is as follows:

DPPH radical scavenging activity % = (1 - sample absorbance blank absorbance ) × 100 (2)

0.5 g of meat sample was added to 2 mL of extract. After homogenizing at 10000 r/min, centrifuge at 8500 r/min for 15 min, and then take the supernatant. The supernatant is a crude extract of •OH radicals. Scavenging activity of the •OH free radical were determined using corresponding diagnostic kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China) according to instructions.

2.7 Statistical analysis

The data were analyzed using the two-way analysis of variance with a model using SPSS Statistic software 21.0 (IBM Corporation, USA), and means were compared by Fisher's Protected Least Significant Difference (LSD) test in case of significative effect. For all parameters, a probability value of (P < 0.05) was considered statistically significant.

The least square multiple linear regression equation in the GLM program of SAS 9.2 was adopted and the biological utilization ratio of organic Se to inorganic Se was calculated with multiple linear regression slope.

3 Results and discussion

3.1 Growth performance of broilers

The effect of Se sources and supplemental levels on growth performance of broilers is presented in Table 2. During the starter (1-21 d), dietary Se sources had no significant effects on FI, BWG and F/G of broilers (P > 0.05). With the increase of Se supplemental level, F/G was significantly decreased (P < 0.05), and broilers has a significant trend of improvement for BWG (P = 0.06). During the finisher (22-42 d), BWG and F/G of broilers were improved with the increase of Se supplemental level (P < 0.05), and Se sources and Se levels has a trend of interactions for BWG (P = 0.07). During day 1 to day 42, there was a trend of improvement in BWG with different Se sources (P = 0.08), and BWG and F/G were significantly affected with increasing percentage of Se supplementation (P < 0.05).

Table 2
Effects of Dietary Sodium Selenite and Selenium Yeast Levels on Growth Performance of Broilers.

When Se was identified as one of the essential trace elements for humans and animals by the World Health Organization in 1973 (Schwarz & Fredga, 1969Schwarz, K., & Fredga, A. (1969). Biological potency of organic selenium compounds. I. Aliphatic monoseleno- and diseleno-dicarboxylic acids. The Journal of Biological Chemistry, 244(8), 2103-2110. http://dx.doi.org/10.1016/S0021-9258(18)94372-3. PMid:5782002.
http://dx.doi.org/10.1016/S0021-9258(18)...
), Se sources and Se levels have been a hot topic in livestock and poultry farming. Studies have shown that the addition of 0.2 mg/kg sodium selenite and yeast Se to the diet significantly increased BWG and FCR in ruminants (Juniper et al., 2008Juniper, D. T., Phipps, R. H., Ramos-Morales, E., & Bertin, G. (2008). Effect of dietary supplementation with selenium-enriched yeast or sodium selenite on selenium tissue distribution and meat quality in beef cattle. Journal of Animal Science, 86(11), 3100-3109. http://dx.doi.org/10.2527/jas.2007-0595. PMid:18567732.
http://dx.doi.org/10.2527/jas.2007-0595...
). Se supplementation also significantly improved feed conversion in poultry (Upton et al., 2009Upton, J. R., Edens, F. W., & Ferket, P. R. (2009). The effects of dietary oxidized fat and selenium source on performance, glutathione peroxidase, and glutathione reductase activity in broiler chickens. Journal of Applied Poultry Research, 18(2), 193-202. http://dx.doi.org/10.3382/japr.2008-00019.
http://dx.doi.org/10.3382/japr.2008-0001...
). The results of this experimental showed that the Se sources did not have a significant effect on the production performance of broiler chickens and which were different from previous studies, the reason why the Se sources and Se levels did not have a significant effect on early production performance may be that different forms of Se have different tolerance thresholds (Meng et al., 2019Meng, T., Liu, Y. L., Xie, C. Y., Zhang, B., Huang, Y. Q., Zhang, Y. W., Yao, Y., Huang, R., & Wu, X. (2019). Effects of different selenium sources on laying performance, egg selenium concentration, and antioxidant capacity in laying hens. Biological Trace Element Research, 189(2), 548-555. http://dx.doi.org/10.1007/s12011-018-1490-z. PMid:30232747.
http://dx.doi.org/10.1007/s12011-018-149...
), on the other hand, it may be that the digestive function of chickens is not fully developed and the absorption of trace elements is insufficient, resulting in the growth performance was not obvious, but with the increase of Se supplementation levels, the F/G of broilers was significantly improved at finisher and the BWG of broilers was significantly increased as well. In conclusion, Se levels improved the growth performance of broilers, with the best effect in the 0.6 mg/kg SY group.

3.2 Meat quality

Effect of different Se sources and supplementation levels on meat quality of broiler thigh muscle is shown in Table 3. Neither the Se sources nor the supplementation levels used in this experiment affected the CIE brightness, muscle maturation loss, elasticity, cohesion, adhesion, chewing and recovery of the meat (P > 0.05), but the increase in the supplementation levels significantly affected the a*, cohesion, adhesion, chewing and recovery values (P < 0.05). There were significant differences between Se sources and Se levels on muscle pH, lactate levels, shear force, and hardness, and the 0.6 mg/kg SY-fed group had higher pH value at 0, 24 h than that of the other groups (P < 0.05). Lactic acid (LA) content was influenced by Se sources and Se levels, and while 0.6 mg/kg SY-fed group had the lowest lactic acid content in current study (P < 0.05), and the same case for the meat tenderness (P < 0.05).

Table 3
Mean Scores for Color, Shear Force, pH, Cooking Loss, Texture, and Selenium Content of Chicken Meat Stored at 4 °C.

The freshness, texture, and nutritional content of meat are not only important indicators of meat quality, but also important factors that affect consumers' willingness to buy (Liu et al., 2011Liu, S. M., Sun, H. X., Jose, C., Murray, A., Sun, Z. H., Briegel, J. R., Jacob, R., & Tan, Z. L. (2011). Phenotypic blood glutathione concerntration and selenium supplementation interaction on meat colour stability and fatty acid concentrations in Merno lambs. Meat Science, 87(2), 130-139. http://dx.doi.org/10.1016/j.meatsci.2010.09.011. PMid:20951501.
http://dx.doi.org/10.1016/j.meatsci.2010...
). Among them, meat color is the most direct sensory evaluation of consumers. The change of meat color is caused by the oxidation of myoglobin in the muscle, therefore, it is important to prevent muscle oxidation to keep the meat color stable. The addition of yeast Se to the diet significantly improved the meat color by increasing the a* value and decreasing the b* value in the breast muscle of Wolf Mountain males (Wang et al., 2009Wang, Z. G., Pan, X. J., Peng, Z. Q., Zhao, R. Q., & Zhou, G. H. (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. Poultry Science, 88(5), 1096-1101. http://dx.doi.org/10.3382/ps.2008-00207. PMid:19359700.
http://dx.doi.org/10.3382/ps.2008-00207...
). In this study, there was no relationship between meat color and Se sources, but the increase of Se could significantly improve the a* value of meat. It is mainly because Se effectively reduces the content of oxygen radicals in tissues and which prevents the oxidation of Fe2+ to Fe3+ (Liang et al., 2019Liang, L., Vladimir, F., Ge, J., Liu, C., & Xing, W. (2019). Highly active PtAu alloy surface towards selective formic acid electrooxidation. Journal of Energy Chemistry., 37, 157-162. http://dx.doi.org/10.1016/j.jechem.2019.02.015.
http://dx.doi.org/10.1016/j.jechem.2019....
). The pH value of the muscle is also an important indicator of the reaction to the quality of the meat. Muscle undergoes anaerobic enzymatic production of lactic acid after slaughter (Oliveira et al., 2008Oliveira, R. B. P., Oliveira, A. L., & Glória, M. B. A. (2008). Screening of lactic acid bacteria from vacuum packaged beef for antimicrobial activity. Brazilian Journal of Microbiology, 39(2), 368-374. http://dx.doi.org/10.1590/S1517-83822008000200031. PMid:24031232.
http://dx.doi.org/10.1590/S1517-83822008...
), therefore, muscle pH was decreasing with time after slaughter and meat quality reduced as well, but Se supplementation in the diet could improve the ability of myocytes to scavenge metabolites lactic acid and prevent excessive oxidation of polyunsaturated fatty acids to improve meat quality (Jablonska et al., 2016Jablonska, E., Reszka, E., Gromadzinska, J., Wieczorek, E., Krol, M. B., Raimondi, S., Socha, K., Borawska, M. H., & Wasowicz, W. (2016). The effect of selenium supplementation on glucose homeostasis and the expression of genes related to glucose metabolism. Nutrients, 8(12), 772. http://dx.doi.org/10.3390/nu8120772. PMid:27983572.
http://dx.doi.org/10.3390/nu8120772...
), It was found that Se supplementation slowed the decrease in pH of pork (Calvo et al., 2016aCalvo, L., Toldra, F., Aristoy, M. C., Lopez-Bote, C. J., & Rey, A. I. (2016a). Effect of dietary organic selenium on muscle proteolytic activity and water-holding capacity in pork. Meat Science, 121, 1-11. http://dx.doi.org/10.1016/j.meatsci.2016.05.006. PMid:27232379.
http://dx.doi.org/10.1016/j.meatsci.2016...
, bCalvo, L., Toldra, F., Rodriguez, A. I., Lopez-Bote, C., & Rey, A. I. (2016b). Effect of dietary selenium source (organic vs. mineral) and muscle pH on meat quality characteristics of pigs. Food Science & Nutrition, 5(1), 94-102. http://dx.doi.org/10.1002/fsn3.368. PMid:28070320.
http://dx.doi.org/10.1002/fsn3.368...
; Liang et al., 2019Liang, L., Vladimir, F., Ge, J., Liu, C., & Xing, W. (2019). Highly active PtAu alloy surface towards selective formic acid electrooxidation. Journal of Energy Chemistry., 37, 157-162. http://dx.doi.org/10.1016/j.jechem.2019.02.015.
http://dx.doi.org/10.1016/j.jechem.2019....
). Moreover, the higher pH of Se-treated meat could be caused by the higher consumption of hydrogen peroxide (H2O2) catalyzed by antioxidant enzymes (Boiago et al., 2014Boiago, M. M., Borba, H., Leonel, F. R., Giampietro-Ganeco, A., Ferrari, F. B., Stefani, L. M., & Souza, P. A. (2014). Sources and levels of selenium on breast meat quality of broilers. Ciência Rural, 44(9), 1692-1698. http://dx.doi.org/10.1590/0103-8478cr20131256.
http://dx.doi.org/10.1590/0103-8478cr201...
), and on the other hand, it could be that Se regulates some of the glycolysis and slowing down the synthesis of lactic acid (Zeng & Combs, 2008Zeng, H., & Combs, G. J. Jr. (2008). Selenium as an anticancer nutrient: roles in cell proliferation and tumor cell invasion. The Journal of Nutritional Biochemistry, 19(1), 1-7. http://dx.doi.org/10.1016/j.jnutbio.2007.02.005. PMid:17588734.
http://dx.doi.org/10.1016/j.jnutbio.2007...
). It was found in current study that there was a significant interaction between Se sources and Se levels on pH and lactate content, where diet with 0.6 mg/kg of SY not only slowed down the decrease of pH but also regulated the synthesis of lactate, both of which are consistent with the above scholars' conclusions. With the improvement of living standard in recent years, the tenderness of meat has become a decisive factor when people choose meat, in the present experimental results, there was a significant interaction between Se sources and Se levels on meat shear. With the increase of Se levels, the cooking loss of meat was significantly reduced and there was no regular change in other textural indicators. The results of this study are consistent with most scholars' findings (Baowei et al., 2011Baowei, W., Guoqing, H., Qiaoli, W., & Bin, Y. (2011). Effects of yeast selenium supplementation on the growth performance, meat quality, immunity, and antioxidant capacity of goose. Journal of Animal Physiology and Animal Nutrition, 95(4), 440-448. http://dx.doi.org/10.1111/j.1439-0396.2010.01070.x. PMid:21050274.
http://dx.doi.org/10.1111/j.1439-0396.20...
; Calvo et al., 2017Calvo, L., Segura, J., Toldra, F., Flores, M., Rodriguez, A. I., Lopez-Bote, C. J., & Rey, A. I. (2017). Meat quality, free fatty acid concentration, and oxidative stability of pork from animals fed diets containing different sources of selenium. Food Science & Technology International, 23(8), 716-728. http://dx.doi.org/10.1177/1082013217718964. PMid:28675104.
http://dx.doi.org/10.1177/10820132177189...
; Khan et al., 2018Khan, A. Z., Kumbhar, S., Liu, Y., Hamid, M., Pan, C., Nido, S. A., Parveen, F., & Huang, K. (2018). Dietary supplementation of selenium-enriched probiotics enhances meat quality of broiler chickens (Gallus gallus domesticus) raised under high ambient temperature. Biological Trace Element Research, 182(2), 328-338. http://dx.doi.org/10.1007/s12011-017-1094-z. PMid:28702872.
http://dx.doi.org/10.1007/s12011-017-109...
; Li et al., 2018Li, J. L., Zhang, L., Yang, Z. Y., Zhang, Z. Y., Jiang, Y., Gao, F., & Zhou, G. H. (2018). Effects of different selenium sources on growth performance, antioxidant capacity and meat quality of local chinese subei chickens. Biological Trace Element Research, 181(2), 340-346. http://dx.doi.org/10.1007/s12011-017-1049-4. PMid:28516388.
http://dx.doi.org/10.1007/s12011-017-104...
), but some scholars also reported that different levels of Se fermentation products provided no changes in color, water-holding capacity, cooking loss, or shear force (Aristides et al., 2018Aristides, L. G. A., Venancio, E. J., Alfieri, A. A., Otonel, R. A. A., Frank, W. J., & Oba, A. (2018). Carcass characteristics and meat quality of broilers fed with different levels of Saccharomyces cerevisiae fermentation product. Poultry Science, 97(9), 3337-3342. http://dx.doi.org/10.3382/ps/pey174. PMid:29771392.
http://dx.doi.org/10.3382/ps/pey174...
). The different effects of Se on meat tenderness may be due to the different animal breeds, and no mechanism of Se affect physical properties of meat has been reported at this time.

3.3 Analysis of anti-oxidation ability and lipid oxidation

Effect of different Se sources and Se levels on muscle antioxidant capacity and degree of lipid oxidation is shown in Table 4. Se supplementation in diets increased DPPH (0-24 h), hydroxyl radical (0-24 h) scavenging and increased SOD (P < 0.05), and significantly decreased TBARS (0-24 h) and POV values (0-24 h) compared to CG group, except for hydroxyl radical (0 h) for which there was no significant interaction (P > 0.05), except for the hydroxyl radical (0 h), which had a significant interaction in all groups (P < 0.05). In the present study, it was concluded that the diet with 0.6 mg/kg had higher DPPH (0-24 h), hydroxyl radical (0-24 h) scavenging and SOD values and significantly reduced TBARS (0-24 h) and POV values (0-24 h) compared to all other groups.

Table 4
DPPH and •OH Radical Scavenging Activity, SOD Activities, TBARS and POV Values in Raw Meat Stored at 4 °C (%).

There are many antioxidant defense systems in the animal body, including enzymatic and non-enzymatic antioxidant systems, which can scavenge the reactive oxygen radicals (ROS) generated in the body in a timely manner and ensure that the collective free radicals always maintain a dynamic balance to maintain the healthy state of the body (Chung et al., 2006Chung, J. Y. K. J., Kim, J. H., Ko, Y. H., & Jang, I. S. (2006). Effects of dietary supplemented inorganic and organic selenium on antioxidant defense systems in the intestine, serum, liver and muscle of Korean native goats. Asian-Australasian Journal of Animal Sciences, 20(1), 759-765. http://dx.doi.org/10.5713/ajas.2007.52.
http://dx.doi.org/10.5713/ajas.2007.52...
; Chadio et al., 2015Chadio, S. E., Pappas, A. C., Papanastasatos, A., Pantelia, D., Dardamani, A., Fegeros, K., & Zervas, G. (2015). Effects of high selenium and fat supplementation on growth performance and thyroid hormones concentration of broilers. Journal of Trace Elements in Medicine and Biology, 29, 202-207. http://dx.doi.org/10.1016/j.jtemb.2014.09.010. PMid:25447588.
http://dx.doi.org/10.1016/j.jtemb.2014.0...
; Xu et al., 2018Xu, P., Zheng, Y. D., Zhu, X. X., Li, S. Y., & Zhou, C. L. (2018). L-lysine and L-arginine inhibit the oxidation of lipids and proteins of emulsion sausage by chelating iron ion and scavenging radical. Asian-Australasian journal of animal sciences, 31(6), 905-913. http://dx.doi.org/10.5713/ajas.17.0617. PMid:29268578.
http://dx.doi.org/10.5713/ajas.17.0617...
) . Se is widely used in livestock and poultry production as an antioxidant feed additive. Li et al. found that the addition of yeast Se and sodium selenite in broiler diets could improve the enzymatic activity of antioxidant enzymes in the organism compared with the control group (Li et al., 2018Li, J. L., Zhang, L., Yang, Z. Y., Zhang, Z. Y., Jiang, Y., Gao, F., & Zhou, G. H. (2018). Effects of different selenium sources on growth performance, antioxidant capacity and meat quality of local chinese subei chickens. Biological Trace Element Research, 181(2), 340-346. http://dx.doi.org/10.1007/s12011-017-1049-4. PMid:28516388.
http://dx.doi.org/10.1007/s12011-017-104...
), and Traş et al. (2000)Traş, B., Inal, F., Baş, A. L., Altunok, V., Elmas, M., & Yazar, E. (2000). Effects of continuous supplementations of ascorbic acid, aspirin, vitamin E and selenium on some haematological parameters and serum superoxide dismutase level in broiler chickens. British Poultry Science, 41(5), 664-666. http://dx.doi.org/10.5713/ajas.17.0617. PMid:11201449.
http://dx.doi.org/10.5713/ajas.17.0617...
found that the addition of Se in the diet could significantly increase the serum SOD activity of broiler chickens, and also prevent and slow down the damage of oxidative effects on the organism. In this experiment, three antioxidant indicators were selected, and the test results showed that the Se sources and Se levels significantly increased the scavenging rate of DPPH and OH radicals and SOD enzyme activity in muscle compared with the control group, with the best effect in the 0.6 mg/kg SY group, which was consistent with the above scholars' findings. The increase in antioxidant capacity of muscle slows down the process of lipid oxidation, thus allowing the meat to obtain a longer shelf life. Ebeid et al. (2013)Ebeid, T. A., Zeweil, H. S., Basyony, M. M., Dosoky, W. M., & Badry, H. (2013). Fortification of rabbit diets with vitamin E or selenium affects growth performance, lipid peroxidation, oxidative status and immune response in growing rabbits. Livestock Science, 155(2-3), 323-331. http://dx.doi.org/10.1016/j.livsci.2013.05.011.
http://dx.doi.org/10.1016/j.livsci.2013....
found that Se supplementation significantly reduced MDA content during 6 days of refrigerated storage. The MDA content of chicken meat was increased with the aging time (Ma et al., 2019Ma, G., Chen, H., Zhang, Q., Ma, J., Yu, Q., Han, L., Chen, C., & Song, R. (2019). Protective characterization of low dose sodium nitrite on yak meat myoglobin in a hydroxy radical oxidation environment: Fourier Transform Infrared spectroscopy and laser Micro-Raman spectroscopy. LWT, 116, 108556. http://dx.doi.org/10.1016/j.lwt.2019.108556.
http://dx.doi.org/10.1016/j.lwt.2019.108...
). To make the experimental data more convincing, TBARS values (0, 24 h) and POV values (0, 24 h) in muscle were measured in this experiment to assess the extent of muscle oxidation. The results showed that the TBARS (0, 24 h) and POV (0, 24 h) values in the SY group were significantly lower than those in the SS and CG groups, and the lowest levels was found in the SY-fed group at 0.6 mg/kg. By assessing the antioxidant capacity of muscle and the degree of lipid oxidation, we found that the effect of organic Se was significantly better than inorganic Se, and the reason for this result may be that the delivery mechanism of organic Se and inorganic Se differ significantly, and organic Se had higher absorption and utilization, bio-safety and enhancement of antioxidant capacity of organisms than inorganic Se. The rate of lipid oxidation in muscle depends on the antioxidant capacity of the animal organism. To make the experimental data more convincing, TBARS values (0, 24 h) and POV values (0, 24 h) in muscle were measured in this experiment to assess the extent of muscle oxidation. The results showed that the TBARS (0, 24 h) and POV (0, 24 h) values in the SY group were significantly lower than those in the SS and CG groups, and the lowest levels was found in the SY-fed group at 0.6 mg/kg, and the test results were consistent with the previous study. By assessing the antioxidant capacity of muscle and the degree of lipid oxidation, we found that the reason for organic Se was better than inorganic Se may be that the delivery mechanism of organic Se and inorganic Se differ significantly, and organic Se has higher absorption and utilization, biosafety and enhancement of antioxidant capacity of organisms than inorganic Se (Wang et al., 2020Wang, H., Gao, W., Huang, L., Shen, J. J., Liu, Y., Mo, C. H., Yang, L., & Zhu, Y. W. (2020). Mineral requirements in ducks: an update. Poultry Science, 99(12), 6764-6773. http://dx.doi.org/10.1016/j.psj.2020.09.041. PMid:33248592.
http://dx.doi.org/10.1016/j.psj.2020.09....
). The study by Ma et al. showed that organic Se was actively absorbed in the intestine, whereas inorganic Se requires passive absorption (Ma et al., 2014Ma, Y. L., Lindemann, M. D., Pierce, J. L., Unrine, J. M., & Cromwell, G. L. (2014). Effect of inorganic or organic selenium supplementation on reproductive performance and tissue trace mineral concentrations in gravid first-parity gilts, fetuses, and nursing piglets. Journal of Animal Science, 92(12), 5540-5550. http://dx.doi.org/10.2527/jas.2014-7590. PMid:25403188.
http://dx.doi.org/10.2527/jas.2014-7590...
). The analysis by Surai et al. showed that organic Se is more effective than inorganic Se in regulating the antioxidant system of poultry (Surai, 2014Surai, P. F. (2014). Polyphenol compounds in the chicken/animal diet: from the past to the future. Journal of Animal Physiology and Animal Nutrition, 98(1), 19-31. http://dx.doi.org/10.1111/jpn.12070. PMid:23527581.
http://dx.doi.org/10.1111/jpn.12070...
). In short, the SY-fed group had greater antioxidant capacity and was more environmentally friendly than the SS-fed group. Feeding 0.6 mg/kg of Se yeast could effectively improve the antioxidant capacity of meat, delaying lipid oxidation and extending its shelf life.

3.4 Selenium enrichment levels in muscle and organs

The result of accumulation of different Se sources and Se levels in muscle and organs is shown in Table 5. Different Se sources increased Se deposition in broiler heart (P < 0.05), and which increasing Se levels in the diet improved Se levels in broiler heart, liver, kidney and muscle as well (P < 0.05). There were significant differences between Se sources and Se levels on Se deposition on the kidney and heart of broilers (P < 0.05). The group with 0.6 mg/kg yeast Se had the highest Se content in muscle and organs. With Se content of heart, liver, kidney and muscle in broilers as indicators, the biological utilization rates of organic Se against inorganic Se were 116.0%, 123.1%, 109.7%, 109.8%, and 135.2%, respectively (Table 6).

Table 5
Selenium enrichment content in muscle and organs.
Table 6
Multivariate linear regression equation between inorganic and organic Se.

Our results showed that the proportion of Se deposition in muscle and liver tissue was increased as Se level in the diet, and the deposition of the two Se sources in the muscle tissue was not significantly different. The organic Se or inorganic Se supplementation in the diet could increase the content of Se in muscle (Marounek et al., 2009Marounek, M., Dokoupilova, A., Volek, Z., & Hoza, I. (2009). Quality of meat and selenium content in tissues of rabbits fed diets supplemented with sodium selenite, selenized yeast and selenized algae. World Rabbit Science, 17(4), 207-212. https://doi.org/10.4995/wrs.2009.645.
https://doi.org/10.4995/wrs.2009.645...
). Grossi et al.confirmed this finding, and the study found that muscle Se concentration was improved with the increase in Se concentration in the feed (Grossi et al.,, 2017Grossi, S., Rossi, L., De Marco, M., & Rossi, C. A. S. (2017). The effect of different sources of selenium supplementation on the meat quality traits of young charolaise bulls during the finishing phase. Antioxidants, 10(4), 596. https://doi.org/10.3390/antiox10040596.
https://doi.org/10.3390/antiox10040596...
), and the same results were obtained in studies on beef and lamb (Juniper et al., 2008Juniper, D. T., Phipps, R. H., Ramos-Morales, E., & Bertin, G. (2008). Effect of dietary supplementation with selenium-enriched yeast or sodium selenite on selenium tissue distribution and meat quality in beef cattle. Journal of Animal Science, 86(11), 3100-3109. http://dx.doi.org/10.2527/jas.2007-0595. PMid:18567732.
http://dx.doi.org/10.2527/jas.2007-0595...
; Bezerra et al., 2020Bezerra, H., Buarque, V., Silva, L., Leme, P., Vidal, A., Vaz, A., Gallo, S. B., Silva, S. L., & Leme, P. R. (2020). Effect of castor and cashew nut shell oils, selenium and vitamin e as antioxidants on the health and meat stability of lambs fed a high-concentrate diet. Antioxidants, 9(12), 1298. http://dx.doi.org/10.3390/antiox9121298. PMid:33353112.
http://dx.doi.org/10.3390/antiox9121298...
). In this experiment, there was a significant difference in organic Se and inorganic Se in the deposition of the heart of the chicken. This phenomenon may be caused by the accumulation of organic Se. These discoveries confirmed the high biological effects of organic Se used for chickens (Briens et al., 2014Briens, M., Mercier, Y., Rouffineau, F., Mercerand, F., & Geraert, P. A. (2014). 2-Hydroxy-4-methylselenobutanoic acid induces additional tissue selenium enrichment in broiler chickens compared with other selenium sources. Poultry Science, 93(1), 85-93. http://dx.doi.org/10.3382/ps.2013-03182. PMid:24570427.
http://dx.doi.org/10.3382/ps.2013-03182...
). The increase of Se levels in liver and kidney may be because the activation of Se is in the liver and excreted in the kidneys (Burk & Hill, 2015Burk, R. F., & Hill, K. E. (2015). Regulation of selenium metabolism and transport. Annual Review of Nutrition, 35(1), 109-134. http://dx.doi.org/10.1146/annurev-nutr-071714-034250. PMid:25974694.
http://dx.doi.org/10.1146/annurev-nutr-0...
), and the anti-oxidation constantly repeats this process leading to the deposition of Se in the organs. In word, the enrichment of Se in organs contributes to a timely response to oxidative damage in the organism, and organic Se is more bioavailable than inorganic Se.

4 Conclusions

In conclusion, in the entire breeding process of chickens, with 0.6 mg/kg SY can improve the tenderness and color of the meat, reduce lipid peroxidation, better free radical removal ability and improve Se content in muscle and organs deposition. These results also prove that SY is an effective strategy to improve the quality parameters and antioxidant capabilities of meat in a short period of time, and produce Se-rich meat.

  • Practical Application: Selenium is widely used as a feed additive in livestock and poultry production, but there are no reports on the growth performance, meat quality, organ selenium enrichment and antioxidant capacity of broiler chickens with different selenium sources and selenium levels. In this study, the effects of the two selenium sources on the growth performance, meat quality and muscle antioxidant indexes of broiler chickens were compared by adding organic selenium and inorganic selenium to the diet, which provided theoretical support for the application of selenium in poultry production.
  • Funding

    This work was supported by the National Natural Science Foundation of China under Grants 31660664 and 31702123, Fuxi Young Talent Cultivation Project of Gansu Agricultural University under Grant GAUFX-02Y07, Fuxi Foundation of Gansu Agricultural University under Grant GAUFX-04J03, and Discipline Team Project of Gansu Agricultural University under Grant GAU-XKTD-2022-24.

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Publication Dates

  • Publication in this collection
    13 Mar 2023
  • Date of issue
    2023

History

  • Received
    20 Oct 2022
  • Accepted
    07 Dec 2022
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