Nutritional modulation of the antioxidant capacities in poultry: the case of selenium

INTRODUCTION

Natural antioxidants play important roles in maintaining chicken health, productive and reproductive performance of breeders, layers, rearing birds, and growing broilers. There is a wide range of antioxidant molecules in the body. Some of them are supplied with feed (vitamin E, carotenoids, selenium), others are synthesized in tissues (ascorbic acid, coenzyme Q [CoQ], carnitine, taurine, antioxidant enzymes, etc.). In the body all antioxidants work together to create the antioxidant network called “antioxidant systems” (Surai, 2002, 2006, 2017). In this network, all antioxidants are closely connected to each other via various mechanisms, including stress-response elements, transcription factors (Nrf2, NF-kB, etc.), vitagenes, and other important elements (Surai and Fisinin, 2016d). In recent years, redox balance of the cell and reactive oxygen species (ROS) signaling have received tremendous attention and understanding of the antioxidant defense strategy in the cell/body is among important priorities in biochemistry and cell biology. Taking into account stressful conditions of commercial poultry production, regulation of the antioxidant defense systems of poultry by nutritional means becomes a topic of great interest. Optimal levels of vitamin E, selenium, and carotenoids in combination with other antioxidant compounds in the feed provide a maximum protection in stress condition and maintain productive and reproductive performance of poultry. In this review, an analysis of data on the effect of Se on the antioxidant defense network in poultry is presented.

STRESSES IN POULTRY PRODUCTION: DO NOT FREE RADICALS

Commercial poultry production is associated with a range of stresses (environmental, technological, nutritional, and biological/internal; Surai and Fisinin, 2016a, 2016b). For the last 4 decades information has been actively accumulated to suggest that most stresses at the molecular level are associated with overproduction of free radicals and oxidative stress (Surai, 2002, 2006, 2016; Surai and Fisinin, 2016c). Electron transport chain of mitochondria is the main source of free radicals in biological systems. Up to 3% of oxygen can escape from the energy production process and become free radicals which can damage all types of biological molecules including lipids, proteins, and DNA (Surai, 2018). Phagocyte cells are considered to be the second most important source of free radicals in the body. In this case, free radical production is absolutely an essential process and these damaging molecules are used as a weapon to kill pathogens. However, once these radicals escaped phagosome they can damage healthy tissues (Surai, 2006, 2018). Free radicals are produced due to other processes in the body, including xenobiotic metabolism and detoxification, prostanoid synthesis, inflammatory responses, etc. There is a range of internal and external factors increasing free radical production, including presence of transition metals (Fe²⁺ and Cu⁺), high levels of polyunsaturated fatty acids (PUFAs), high oxygen concentration, etc. (Surai, 2002, 2006, 2018).

To deal with various types of free radicals during evolution, protective defense mechanisms called antioxidant systems have been developed, shaped, and they are responsible for survival higher eukaryotes in oxygenated atmosphere. They include fat-soluble (vitamin E, carotenoids, and CoQ), water-soluble (ascorbic acid, glutathione, thioredoxin, carnitine, taurine, etc.) antioxidants, and antioxidant enzymes (superoxide dismutase [SOD], glutathione peroxidase [GSH-Px], and other selenoproteins, catalase, glutathione reductase, glutathione transferase, etc.). In many cases, synthesis of internal antioxidants including SOD, selenoproteins, and CoQ in response to stress conditions is an adaptive mechanism to prevent negative consequences of stresses. A redox balance of the cell/tissue/body is responsible for adaptive regulation of the antioxidant defenses and transcription factors such as Nrf2 and NFkB are involved in this process. In general, the antioxidant network includes 3 major lines of antioxidant defense (Surai, 2006, 2016). The first line of the defense starts from SOD which is responsible for detoxification of superoxide radical (Surai, 2016). The product of this reaction called hydroperoxide (H₂O₂) is still toxic and must be removed from the cell. Therefore, GSH-Px and catalase responsible for detoxification of H₂O₂ by converting it to water also belong to the first level of antioxidant defense. Since transition metals in free forms are involved in free radical formation (Surai, 2006), it is important to keep them bound to proteins and therefore metal-binding proteins are also important part of the first line of the antioxidant defense network. Such antioxidants as carnitine, taurine, and CoQ which are involved in maintenance of mitochondria integrity are also important elements of the first level of antioxidant defense. A range of selenoproteins (TR, SeW, SeR, etc.) regulating redox balance of the cell can also be a part of the first level of antioxidant defense (Surai, 2016, 2017). Recently, free radicals have been considered to be signaling molecules regulating adaptation to stress (Reczek and Chandel, 2015).

Because of a great number and variety of free radical produced in biological systems, the first line of the antioxidant defense network is not powerful enough to stop the process of free radical production. Therefore, the second level of defense includes chain breaking antioxidants such as vitamins E and C, carotenoids, GSH system (GSH, GSH-Px, GR, GSR), thioredoxin system (thioredoxins, TR, peroxiredoxins), some selenoproteins, carnitine, betaine, taurine, and others. This level of defense also includes various mechanisms of antioxidant recycling. For instance, it is proven that vitamin E after reacting with a free radical is oxidized and loses its antioxidant protective activity. However, due to presence of ascorbic acid it can be converted back to a reduced active form, but ascorbic acid is oxidized. Further ascorbic acid is reduced by TR and the system of recycling taking reducing equivalents from NADPH synthesized in the pentose phosphate cycle. This process connects antioxidant defenses to carbohydrate metabolism (Surai, 2002, 2006, 2016).

However, even the second level of the antioxidant defense system cannot prevent all damages to biological molecules and some molecules, including lipids, proteins, and DNA, could be damaged and they need to be repaired or removed from the cell. Thus, there is a third level of antioxidant defense which includes heat shock proteins (HSP), methionine sulfoxide reductase, DNA repair enzymes, phospholipases, etc.

Recently, a vitagene concept has been developed and successfully applied to poultry production (Surai and Fisinin, 2016c, 2016d). In accordance with this concept, there is a range of genes encoding for protective molecules such as SOD, thioredoxin system, HSP, sirtuins, etc. which regulate adaptive ability of the cell/tissue/body to various stress conditions.

CHOICE OF A MODEL SYSTEM TO ADDRESS ANTIOXIDANT SYSTEM MODULATION

To address the nutritional modulation of antioxidant defenses in poultry, a chain including breeder egg-newly hatched chick-post-hatch chick was chosen as a model system. First of all, there is an opportunity to observe antioxidant effects at all the stages of this model. Secondly, egg yolk (Speake et al., 1998) and chick embryonic tissues (Surai et al., 1996) are rich in polyunsaturated fatty acids making them to be very sensitive to oxidative stress and need for effective antioxidant protection. Thirdly, transfer of antioxidants to the newly hatched chick and their protection from various stresses in early postnatal life is key for the development of vital functions in poultry including immune and digestive system (Surai and Fisinin, 2015). Finally, effect of antioxidants in the maternal diet on the antioxidant defenses in growing chicks could show possible epigenetic effects (Surai, 2002).

The antioxidant system of the chicken embryo and newly hatched chick includes the fat-soluble antioxidants vitamin E (Surai et al., 1996; Surai, 1999a), carotenoids (Surai et al., 2001a, b; Surai, 2012a, b), and CoQ (Karadas et al., 2011), water-soluble antioxidants ascorbic acid (Surai et al., 1996), glutathione (Surai et al., 1999; Surai, 1999b), carnitine (Surai, 2015a, b), taurine (Surai, 2017), as well as antioxidant enzymes SOD, GSH-Px, catalase (Surai, 1999b, 2016), TR (Xiao et al., 2016), and selenium as a part of various selenoproteins (Surai, 2006; Pappas et al., 2008; Surai and Fisinin, 2016b). Vitamin E (Surai and Speake, 1998a; Surai, 1999a) and carotenoids (Surai and Speake, 1998b; Surai et al., 2001a,b; Surai, 2012a,b) are transferred from feed into egg yolk and to embryonic tissues. Selenium is shown to be transferred from the feed to the egg yolk, albumin (Surai and Fisinin, 2014), and to the developing embryo (Surai, 2006; Surai and Fisinin, 2016e).

From a range of antioxidants provided by the feed ingredients and feed supplements, only selenium (as a precursor of selenoprotein synthesis), vitamin E, and carotenoids can be used in this model. Dietary manipulation of the aforementioned nutrients is used for many years to improve antioxidant defenses in commercially relevant stress conditions of the industrial poultry production.

ROLES OF SE IN ANTIOXIDANT DEFENSE NETWORK MODULATION

Trace element selenium (Se) was discovered 200 yr ago, its essentiality in animal and human nutrition was proven in 1957, and first selenoprotein called GSH-Px was described in 1973 (Surai, 2006). Recently, a family of chicken selenoproteins has been updated to include 25 genes responsible for selenoprotein synthesis (Lei, 2017; Zhao et al., 2017; Li et al., 2018). It is proven that selenium in the form of SeCys performs its functions as an essential part of various selenoproteins which are important elements/modulators of the antioxidant network in poultry/animal body.

SELENIUM ABSORPTION AND METABOLISM

In feed ingredients including wheat, barley, corn, and soya, Se is found mainly in organic form, with SeMet representing more than 50% of total Se. However, Se concentration in feed is very variable and in most parts of the world is quite low. Therefore, to deal with a global Se deficiency, animal diets started to be supplemented with Se in 1970s (Surai, 2006). The Se requirements of poultry have been shown to be quite low, ranging from 0.06 mg/kg diet for laying hens up to 0.2 mg/kg diet for turkeys and ducks (Surai and Fisinin, 2014). How ever, in stress conditions Se requirement could be substantially increased and nowadays Se is incorporated in major premixes for all categories of poultry at 0.1 to 0.3 ppm in various forms including sodium selenite, selenite, and organic forms of selenium namely Se-Yeast, SeMet, OH-SeMet, and Zn-SeMet (Surai, 2006; Surai and Fisinin, 2014, 2016e).

The small intestine (duodenum and jejunum) is shown to be the primary site for absorption of dietary Se which is quite high comprising about 80%. The absorption efficacy decreases in order SeMet>Selenate>Selenite. Selenite is believed to be passively absorbed while selenate can use a Na⁺- mediated absorption mechanisms and SeMet absorption takes place in the same way as pure methionine (Surai, 2006). Absorbed Se binds to blood proteins, including plasma albumin, and is delivered to the liver where all Se forms are converted to hydrogen selenide (H₂Se). On one hand, H₂Se is used for selenoprotein synthesis, and on the other hand it can be methylated with formation of excretion products. Production of excretory Se metabolites is an important metabolic regulatory mechanism responsible for maintaining Se status of the body (Surai, 2006).

Selenoproteins are synthesized as needed for their functions. There are 2 fundamental factors regulating selenoprotein expression and syntheses namely Se status and level of stress reflected by the redox balance of the cell (Gladyshev, 2016). There are housekeeping selenoproteins which are responsible for maintenance of important cellular functions and they are the last ones to be affected by Se status or stress. Other selenoproteins are stress responsive, and their expression and synthesis are modulated by environment and dietary Se provision. The selenoproteins retained in tissues for longer periods during progressive Se deficiency are considered to have higher physiological significance in comparison to those whose activities rapidly decline. In this respect, the main GSH-Px forms rank as follows: GI-GSH-Px > PH-GSH-Px > Plasma GSH-Px = Cytosolic GSH-Px (Flohe and Brigelius-Flohe, 2016). Recently, it has been suggested that GPXs, TrxR1, SELP, and SPS2 play a more important role than the other selenoproteins in poultry (Luan et al., 2016).

Based on physiological features of chicken embryonic development, it could be concluded that albumin supplies the developing embryo with Se during the first 2 wk of the development, while egg yolk Se is transferred to the embryo during the last week of incubation (Surai, 2002, 2006). Expression of selenoproteins in chicken embryo is not well studied. The specific activity of Se-GSH-Px in the embryonic liver was characterized by continuous increase during the second half of the embryonic development reaching its maximum at hatching which was shown to be 3.0 times greater than that at day 10 of incubation (Surai, 1999b). GSH-Px activity in the embryonic liver follows the same patterns as it was shown for vitamin E and carotenoids (Surai et al., 1996) being an adaptive mechanism to be prepared for hatching stress. Furthermore, GSH-Px activity in the prenatal normoxic lung was shown to demonstrate a sharp increase between day 16 and day 18 and remained constant until hatch (Starrs et al., 2001). It is interesting to note that GSH-Px was shown to be 2.5-fold higher in duck embryo liver in comparison to chicken embryo (Jin et al., 2001) or 15-fold higher in the postnatal duck muscle in comparison to chicken muscle (Hoac et al., 2006). According to GSHPx activity, tissues of 35-d chickens can be placed in the following descending order: liver>>kidney>plasma = erythrocytes>>femoral muscle>>pectoral muscle (Arai et al., 1994).

MODULATING EFFECTS OF DIETARY Se

Main advantage of Se for breeders is related to building Se reserves in the body which can be used in stress conditions (Surai, 2006). This reserve can be built in muscles only with dietary SeMet which is nonspecifically incorporated into proteins in place of methionine. In stress conditions, protein catabolism and activation of proteasome will release Se providing it for additional synthesis of selenoproteins and improved antioxidant defenses (Surai and Fisinin, 2016a). It was shown that the intracellular redox status is an important element activating or downregulating the 20S proteasome chymotrypsin-like activity in living cells (Kretz-Remy and Arrigo, 2003). This is a very important finding, which explains how Se reserves in the body can be used to improve antioxidant defenses in stress conditions. The inclusion of organic Se into the diet is associated with a significant increase of Se level in breeder muscles (almost 3-fold increase vs selenite, Invernizzi et al., 2013; Jing et al., 2015). In the later study, Jing et al. (2015) also showed a significant increase in GSH-Px and SOD activity in their plasma. In addition, there was an increased expression of GSH-Px4 in testis and ovary due to Se supplementation in Se-supplemented pigeons (Wang et al., 2017). When gene expression was studied in the oviduct of Sesupplemented (0.3 ppm) breeders, Se-yeast, but not SS, increased transcripts of GPX4 and SEPP1. They were significantly upregulated (1.78- and 1.81-fold, respectively) in Se-yeast-fed hens but remained unaffected in SS birds (Wang et al., 2017).

Se-Yeast was shown to upregulate multiple genes involved in oxidative phosphorylation, mitochondrial function, and ubiquinone biosynthesis (Brennan et al., 2011). At the same time SS was shown to downregulate genes involved in oxidative phosphorylation and did not affect genes involved in ubiquinone synthesis. It directly involves in protection of lipids, proteins, and DNA from oxidative damage by quenching free radicals, regenerating other antioxidants (vitamins E and C), and regulating mitochondrial integrity (Varela-López et al., 2016). It was suggested that Se inadequacy could compromise the cells ability to obtain the optimal concentrations of coenzyme Q10, while optimal function of Se depends on the levels of coenzyme Q10 (Alehagen and Aaseth, 2015). It seems likely that additional synthesis of CoQ in stress conditions is an adaptive mechanism to deal with overproduction of free radicals. In an experiment conducted in China (Yuan et al., 2012) in broiler breeders, Se-Yeast or SeMet significantly increased the activity of TrxR1 in the liver and kidney and expression of GSH-Px in the liver of broiler breeder birds compared to SS. TrxR enzymes are essential components of the thioredoxin system consisting of thioredoxin, thioredoxin peroxidases (peroxiredoxins), and thioredoxin reductase, playing a vital role in regulating multiple cellular redox signaling pathways (Lu and Holmgren, 2014). Gowdy et al. (2015) recently proved that chicken TrxR is selenium dependent. Selenium dietary supplementation (0.4 mg/kg diet) increased TrxR activity in duodenal mucosa, liver, and in the kidney in chickens (Placha et al., 2014). Se deficiency was associated with a decreased expression of TrxR2 in chicken thyroids (Lin et al., 2014). Se deficiency in chickens was associated with a significant decrease in activity of TrxR1 (by 50%), TrxR2 (by 83%), and TrxR3 (by 36%) in the pancreas (Zhao et al., 2014).

Organic Se (Se-Yeast or SeMet) supplementation of the breeder diet (0.15 mg/kg) was associated with increased concentration of SepP1 in the serum and liver and enhanced SepP1 expression in the liver in comparison to birds receiving sodium selenite (Yuan et al., 2013). SepP is the major plasma selenoprotein, which is synthesized primarily in the liver and delivers Se to certain other organs and tissues (Gladyshev, 2016; Schweizer et al., 2016), and might have an important role as an antioxidant in plasma (Steinbrenner et al., 2006) acting as an extracellular PH-GSHPx (Saito et al., 1999). Importantly, selenoprotein (e.g., GSH-Px) response to dietary Se depends on many factors and in the case of adequate Se in the diet additional Se supplementation would not increase activity of the enzyme. In a recent study of Delezie et al. (2014), background Se level was 0.25 mg/kg and adding additional Se at 0.1, 0.3, or 0.5 mg/kg in different forms did not affect GSH-Px activity in serum of experimental birds.

The second part of the evidence proving antioxidant modulating properties of Se is related to the effect of maternal Se on the egg, developing embryo, newly hatched chick, and chicken in early postnatal life. The supplementation of the diet with Se is an effective way to increase Se concentrations in whole egg (for review, see Surai and Fisinin, 2014). Recently, it has been determined that SeMet comprised 53 to 71% of total Se in the egg albumen and 12 to 19% in the egg yolk (Lipiec et al., 2010). It was calculated that in the basic starter chicken diet the ratio of SeMet: Met is about 1:60,000; in the growing diet it is 1:50,000 and this ratio is almost the same for breeder birds (Schrauzer and Surai, 2009; Surai and Fisinin, 2014). This ratio can be changed to 1: 12 to 15,000 after dietary Se supplementation in the form of SeMet at 0.3 mg/kg. The calculation also showed that the ratio of SeMet/Met in the egg yolk is about 1:160,000 and in egg white it is approximately 1:87,000 (Surai and Fisinin, 2014). Enrichment of eggs with SeMet due to organic Se dietary supplementation could change those ratios substantially. Since SeMet is not synthesized by animals/poultry, it should be provided with the diet. In the egg obtained from the breeders fed on the commercial diet containing about 0.08 mg feed-derived Se/kg, 58 to 62% Se was found in the egg yolk and 38 to 42% in the albumin. After supplementing the diet with organic Se at 0.5 mg/kg, the Se distribution between egg yolk and albumin was shown to be more equal with 47 to 48% Se to be found in egg albumin (Pappas et al., 2005a). The efficiency of Se transfer from the diet (at 0.2 ppm supplementation) to the egg was quite high for organic Se sources comprising 56% for Se-Yeast and 76.3% for OH-SeMet (Jlali et al., 2013). It seems likely that efficiency of Se transfer to the egg also depends on the Se form, dose, as well as many other factors including chicken genetics, age, etc. In another study, at a dosage of 0.1, 0.3, and 0.5 mg/kg Se transfer from feed to the egg was shown to be 43.3, 42.3, and 34.1% for L-SeMet; 36.6, 33.3, and 23.6% for Se-Yeast; and 24.0, 23.6, and 16.0% for SS, respectively (Delezie et al., 2014).

Organic Se (0.3 mg/kg) in the maternal diet can increase GSH-Px activity in the egg yolk and egg albumen (Wang et al., 2010; Rajashree et al., 2014). A sparing effect of dietary Se on vitamin E was observed as evidenced by a significant increase in α-tocopherol concentration in the egg yolk (Surai, 2000). Taking into account a comparatively low vitamin E level in the diet of the control group (10.1 mg/kg), it could be suggested that the sparing effect of Se is mediated by a range of selenoproteins taking part in antioxidant defenses and preventing extensive usage of vitamin E. Similar positive effect of dietary Se on vitamin E concentration in the egg was reported later by Skrivan et al. (2008) and Tufarelli et al. (2016).

During incubation Se was transferred from the egg to the embryonic tissues and in the liver of the newly hatched chicks Se concentration increased from 0.38 mg/kg in the control group fed on commercial diet up to 0.73 and 1.4 mg/kg in Se-supplemented groups. Improved Se status of newly hatched chicks was associated with significantly increased GSH-Px activity in the liver of the newly hatched chicks and this difference remained significant at 5 d post-hatch (Surai, 2000).

Additional benefit in terms of improvement of antioxidant system of the newly hatched chick comes from significantly increased GSH concentration in the liver due to Se supplementation (Surai, 2000). It was shown that during chicken embryonic development GSH concentration in the liver and brain gradually decreases throughout development, but in the heart and kidney there is a substantial increase in GSH concentration at hatching time (Surai, 1999b).

As a result of the aforementioned improvements in antioxidant defense mechanisms, lipid peroxidation in the liver of experimental birds at day 1 and day 5 post-hatch significantly decreased ultimately reflecting improved resistance to stress (Surai, 2000). However, for the first 10 d post-hatch vitamin E in the chicken liver dramatically decreased and this could compromise antioxidant defenses at this critical period of chicken ontogenesis when digestive and immune systems are actively developing and desperately need an optimal antioxidant defenses/redox balance (Surai, 2000). Therefore, significant increase in vitamin E in the chicken liver together with increased GSH concentration and GSH-Px activity due to dietary supplementation of the maternal diet could be of great importance for the growing chicken. Similarly, in comparison to dietary SS supplementation, maternal SeMet supplementation significantly increased the antioxidant status of 1-d-old chicks exhibited by improvement of a range of oxidative stress markers, including increased GSH-Px and SOD activities in breast muscle, enhanced kidney GSH concentration, increased T-AOC in breast muscle and liver, and inhibited liver and pancreas lipid peroxidation (Wang et al., 2011). It was shown that in comparison to sodium selenite, organic Se sources (Se-Yeast or SeMet) significantly increased the activity of TrxR1 in the liver and kidney, GSH-Px activity and expression of TrxR1 in the liver of progeny chicks (Yuan et al., 2012). Compared with SS, both Se-Yeast and SeMet significantly increased the concentration and mRNA level of selenoprotein P1 (SelP1) in day-old chicks (Yuan et al., 2013).

Xiao et al. (2016) showed that Se supplementation (0.15 ppm Se for 8 wk) of the diet of breeders decreased reactive oxygen species (ROS), HSP70, malondialdehyde (MDA), carbonyl, and 8-hydroxydeoxyguanosine (8-OHdG) concentrations and increased GSH-Px, total SOD, and catalase activities in heat-stressed chick embryo. It was also shown that ROS, MDA, and carbonyl, 8-OHdG concentrations in SeMet treatment group were lower than those in SS treatment. Furthermore, Se supplementation elevated cellular GSH-Px1 mRNA level and activity, cytoplasmic TrxR1 activity, and SelP mRNA and protein level. Again, maternal organic selenium showed a higher efficacy than maternal SS in upregulating GSH-Px1, TrxR1, and SelP mRNA levels as well as GSH-Px1 and TrxR1 activities or SelP protein level (Xiao et al., 2016).

Protective effect of Se on breeders is related to building Se reserves in the muscles and making birds more resistant to stress conditions. Secondly, improved expression and activities of selenoproteins including GSH-Px, TrxR, and SepP substantially contributes to the antioxidant network. Thirdly, increased activities of SOD in breeder’s tissues due to Se supplementation could be an important adaptive mechanism in stress conditions to overcome the excess of free radical production and to re-establish an important equilibrium in the redox status of the cell/tissue/body. Finally, increased expression and possibly concentration of CoQ and other elements of the electron transport chain in the mitochondria could improve the efficiency of the antioxidant defense system. Regulation of antioxidant systems of the egg is related to increased vitamin E concentration and enhanced GSH-Px activity. Protective effect of dietary Se on the newly hatched chick is associated with increased concentrations of vitamin E and GSH, and enhanced activities of GSH-Px, TrxR, SepP, and SOD in the liver and/or muscles. Such an improvement of the antioxidant defense network is shown to decrease lipid peroxidation, protein oxidation, and DNA oxidation in the liver of the 19-day-old embryo exposed to heat stress. Lipid peroxidation also decreased in the newly hatched chicks. Providing Se in optimal form and in optimal concentration is a key to build the effective antioxidant network in the chicken body responsible for their adaptation to hatching stress and stressful postnatal development.

LONG-TERM MATERNAL EFFECT OF SELENIUM

For the last few years, information has been actively accumulated to indicate that Se in maternal diet could have a long-lasting effect on the antioxidant system of the progeny chicks. There was a significantly elevated Se level in the liver and breast muscles of the progeny chicks at 3 and 4 wk post-hatch, respectively (Pappas et al., 2005b). Organic selenium (0.3 mg/kg) in the maternal diet for 4 wk was responsible for increased Se concentration, decreased lipid (MDA), and protein (carbonyls) oxidation in muscles of 21-day-old progeny chicks and improved a water holding capacity of the meat (Wang et al., 2009). In comparison to SS dietary supplementation, maternal Se-Met supplementation (0.3 mg/kg) was shown to significantly improve the FCR of the offspring during 56-d growth and significantly decreased the mortality of the chicks during the first week post-hatch and 8-wk growing period (Wang et al., 2011). Interestingly, SeMet breeder supplementation improved hatchability (90.8 vs 85.1) as well. In continuation of this study it was shown that in comparison to SS supplemented breeder diet, SeMet in maternal diet (0.3 mg/kg) for 8 wk was responsible for significantly increased Se concentrations in serum, liver, kidney, and breast muscle of the 56-day-old offspring chickens. In contrast with maternal SS supplementation, several indexes of antioxidant defense in a progeny chicks obtained from breeders supplemented with SeMet were also improved including increased GSH-Px activity in serum and breast muscle, GSH concentration in serum, and total antioxidant capability in pancreas, as well as cytosolic GSH-Px mRNA abundance in breast muscle, liver, and pancreas (Zhang et al., 2014a). The maternal Se-Met treatment was shown to be associated with a significant reduction of the 48-h drip loss of 56-day-old progeny chickens in comparison with maternal SS treatment.

COMMERCIAL APPLICATIONS OF DIETARY Se

Generally speaking, beneficial effect of dietary Se on breeder’s performance would depend on the level of stress where additional antioxidant protection is required. For example, inclusion of omega-3 PUFAs into the breeder diet could be an important nutritional stress for the breeders and developing embryos. In particular, some aspects of egg quality such as Haugh Units are adversely affected by egg storage and dietary fish oil. In fact, maternal Se supplementation (0.5 mg/kg) was shown to slow down Haugh Units deterioration after 14 d of storage of eggs enriched with omega-3 fatty acids (Pappas et al., 2005a). A protective effect of dietary Se was shown when fish oil (a dietary stress factor) was included in the breeder diet and increased embryonic mortality in wk 3 of incubation and reduced hatchability and weight of 1-day-old chick observed. The addition of Se to the FO-enriched diets was found to ameliorate some of the aforementioned adverse effects (Pappas et al., 2006a).

There is a range of publications showing beneficial effects of Se on breeder and layer performance. Protective effects of selenium on production and reproduction performance of heat-stressed poultry have been recently summarized (Habibian et al., 2015). An experiment conducted with broiler breeder chickens in cages to evaluate the influence of organic and inorganic sources of supplementation showed a reduction in mortality in breeders fed on organic selenium, an increase in egg production, percentage of settable eggs and hatchability (Rajashree et al., 2014), as well as increased number of settable eggs, improved fertility, hatch of fertile eggs, A-grade chicks, and reduced embryonic mortality in comparison to breeders fed inorganic selenium or non-supplemented diet (Khan et al., 2017).

However, when balanced diet and well-controlled conditions are used in most cases the form and concentration of dietary Se do not affect breeder performance (Surai, 2000; Paton et al., 2002; Jing et al., 2015; Urso et al., 2015) or layer performance (Jiakui and Xialong 2004; Payne et al., 2005; Chantiratikul et al. 2008; Bennett and Cheng, 2010; Mohiti-Asli et al. 2010; Pavlovic et al., 2010; Scheideler et al., 2010; Pan et al., 2011; Jlali et al., 2013; Tufarelli et al., 2016).

CONCLUSIONS

Selenium is shown to be an effective modulator of the antioxidant systems in poultry (Figure 1). On the one hand, Se is involved in expression and synthesis of 25 selenoproteins, including GSH-Px, TrxR, and SepP. More than half of known selenoproteins are directly or indirectly involved in antioxidant defenses and redox status maintenance. Se affects non-enzymatic (vitamin E, CoQ, and GSH) and enzymatic (SOD) antioxidant defense mechanisms helping build a strong antioxidant defenses in breeders, developing embryos, and newly

Nutritional modulation of the antioxidant capacities in poultry: the case of selenium - Image 1

hatched chicks. Long-term maternal effects of dietary Se need additional investigation. It is clear that Se efficiency depends on the level of supplementation and form of dietary Se. Sodium selenite, a common Se dietary supplement, is not effective in increasing Se concentration in the egg and embryo and therefore has a limited ability to modulate antioxidant system of the developing embryo and newly hatched chicks. Organic Se sources are proven to be more effective modulators of the antioxidant systems in poultry. Our previous analysis (Surai and Fisinin, 2014) has shown that among organic Se sources, OH-SeMet has the greatest potential/ability to enrich the egg with Se (Jlali et al., 2013) and therefore to affect antioxidant defenses of the developing chicken embryo. Our analysis of composition of eggs collected from various avian species in wild (UK and New Zealand) showed that Se levels in those eggs are close to the levels found in commercial chicken eggs after 0.3 ppm organic Se supplementation (Pappas et al., 2006b). However, a recently introduced restriction in EU related to maximum organic Se supplementation of poultry/animal diets at 0.2 mg/kg makes OH-SeMet a supplemental Se form of choice to meet Se requirement of commercial poultry. Antioxidant/prooxidant (redox) balance of the gut (Surai and Fisinin, 2015) and the role/interactions of Se and microbiota in maintaining gut health (Surai et al., 2017) would be a priority for future research. In the second part of the review, nutritional modulation of the antioxidant defense system with vitamin E and carotenoids will be considered.

This article was originally published in 2019 Poultry Science 98:4231–4239. http://dx.doi.org/10.3382/ps/pey406. This is an Open Access article is licensed under a Creative Commons Attribution License.