selenium deficiency

In the 1980s it was proven that Se deficiency in chickens was associated with decreased GSH-Px in various tissues (Surai, Reference SURAI2006). For the next 30 years this question was studied in more detail. Se deficiency decreased GSH-Px activity and/or expression in liver (Liu et al., Reference LIU, FU, XU, WANG and LI2015), brain (Xu et al., Reference XU, YAO, ZHANG, ZHANG, WANG, ZHANG and JIANG2013), pancreas (Zhao et al., Reference ZHAO, YAO, FAN, ZHANG and XU2014a), muscles (Yao et al., Reference YAO, ZHAO, ZHAO, FAN, KHOSO, ZHANG, LIU and XU2014), thyroid (Lin et al., Reference LIN, WANG, TAN, LIANG, YAO, ZHANG and XU2014), duodenal mucosa (Liu et al., Reference LIU, QU, WANG and WU2016a), spleen and other immune organs (thymus and bursa of Fabricius; Zhang et al., Reference ZHANG, WANG, ZHANG, LI, WANG and XU2012). In Se-deficient chicks, activities of GSH-Px3, liver and gizzard GSH-Px1, liver and gizzard GSH-Px4 decreased dramatically to 3, 2, 5, 10 and 5%, respectively, of Se-adequate levels (Li and Sunde, Reference LI and SUNDE2016). Furthermore, Se deficiency in chickens decreased mRNA expression of GSH-Px and protein expression and activities in duodenum, jejunum and rectum (Yu et al., Reference YU, CHEN, ZHAI, ZHANG, XU, WANG and HU2015). Compared with the Se-supplemented chicks, the Se deficient chicks had lower muscle mRNA levels of GSH-Px1, GSH-Px3, GSH-Px4 and decreased protein expression of GSH-Px1 and GSH-Px4 (Huang et al., Reference HUANG, REN, JIANG, XIAO and LEI2015). Similarly, Se deficiency in turkey was associated with a decrease in GSH-Px4 mRNA levels in the liver (Sunde and Hadley, Reference SUNDE and HADLEY2010).

selenium supplementation

The addition of Se to various diets significantly elevated GSH-Px activity in chicken plasma (Rao et al., Reference RAO, PRAKASH, KUMARI, RAJU and PANDA2013), liver (Placha et al., Reference PLACHA, TAKACOVA, RYZNER, COBANOVA, LAUKOVA, STROMPFOVA, VENGLOVSKA and FAIX2014), seminal plasma, spermatozoa, testes (Surai et al., Reference SURAI, KOSTJUK, WISHART, MACPHERSON, SPEAKE, NOBLE, IONOV and KUTZ1998) and egg yolk (Wang et al., Reference WANG, PAN, ZHANG, PENG, ZHAO and ZHOU2010). Correlation analysis has shown that tissue Se concentration (pooled data) was correlated to Se added to feed (r=0.529, P<0.01, log values) and to GSH-Px activity (r=0.332, P<0.05), with the latter not being correlated with Se added to feed (Zoidis et al., Reference ZOIDIS, DEMIRIS, KOMINAKIS and PAPPAS2014). Information has been accumulated to show that, in comparison to traditional sodium selenite, organic Se in some cases is more effective in upregulation of GSH-Px activity (Surai, Reference SURAI2006). Organic Se in the form of selenised yeast (Se-Yeast) at 0.3 mg/kg was shown to increase GSH-Px activity in egg in comparison to sodium selenite (SS) supplemented breeders (Rajashree et al., Reference RAJASHREE, MUTHUKUMAR and KARTHIKEYAN2014). Similarly, Se-Yeast dietary supplementation increased GSH-Px activity in the liver and breast muscle of 42 day old chickens in comparison to SS-supplemented birds (Chen et al., Reference CHEN, WU and LI2014). Seleno-methionine (Se-Met) and Se-Yeast were more effective than SS in increasing GSH-Px in chicken plasma (Jing et al., Reference JING, DONG, WANG, LIU and TONG2015). Se-Yeast supplementation in broiler diets resulted in greater tissue Se concentrations than SS and pGSH-Px3 and tissue Se concentrations remained greater in birds previously fed a diet with Se-Yeast than in those fed SS after being fed a low-Se diet (Payne and Southern, Reference PAYNE and SOUTHERN2005). Recently a basic chicken diet (BD) containing 0.048 mg feed-derived Se/kg was supplemented with three different forms of Se namely sodium selenite (SS), Se-yeast and OH-SeMet at 0.2 mg/kg and fed from day one up to six weeks. It was shown that, in comparison to BD, all three forms of Se increased GSH-Px activities in the plasma and liver, while Se-Yeast and OH-SeMet were more effective (by 11-28%) in enhancing GSH-Px activity in the liver than SS (Zhao et al., Reference ZHAO, SUN, HUANG, BRIENS, QI, XU and LEI2017). In comparison with SS, organic Se sources significantly elevated mRNA abundance of GSH-Px1 and GSH-Px4 in chicken liver, while OH-SeMet increased expression of GSH-Px3 in comparison to SS or Se-Yeast at week six of age. Importantly, when the diet is adequate in Se usually there is no response to extra Se supplementation. No effect of Se source (Se-Met vs. Se-Yeast) or dosage (0.1; 0.3 or 0.5 mg/kg) was observed on serum GSH-Px activities in chickens (Delezie et al., Reference DELEZIE, ROVERS, VAN DER AA, RUTTENS, WITTOCX and SEGERS2014). Similarly, plasma GSH-Px activity was not affected by Se source or concentration (Payne and Southern, Reference PAYNE and SOUTHERN2005a).

selenium excess

It has been shown that Se excess in chicken diet imposes oxidative stress (Surai, Reference SURAI2002; Reference SURAI2002a; Reference SURAI2002b) which is associated with decreased GSH-Px activity. For example, in acute Se toxicosis GSH-Px activity in red blood cells (RBC) was significantly elevated at the first sampling (3 h after treatment) and decreased to the control level thereafter (Mézes and Sályi, Reference MÉZES and SÁLYI1994). In fact, GSH-Px activity declined in the blood plasma and in the red blood cell haemolysate (Balogh et al., Reference BALOGH, WEBER, ERDÉLYI and MÉZES2004), spleen (Peng et al., Reference PENG, CUI, HE, CUI, FANG, ZUO, DENG, PAN, ZHOU and LAI2012) and liver (Zoidis et al., Reference ZOIDIS, PAPPAS, GEORGIOU, KOMAITIS and FEGGEROS2010) as a result of Se excess in the diet. Indeed, sodium selenite-induced (10 and 15 mg/kg diet) oxidative stress in chicken spleen was associated with decreases in GSH-Px, SOD and catalase (CAT) activities and increases in lipid peroxidation (Peng et al., Reference PENG, CUI, HE, CUI, FANG, ZUO, DENG, PAN, ZHOU and LAI2012). Dietary Se (3 mg/kg) depressed growth performance of chicken and down-regulated nine and three selenoprotein genes in thymus and spleen, respectively, and only Sepp1 was up-regulated in the bursa of Fabricius (Tang et al., Reference TANG, HUANG, WANG, LI, XU, JIA, LIU, CHEN, SHANG and ZHAO2016).

heat stress

It seems likely that GSH-Px activation is an important adaptive mechanism to deal with oxidative stress imposed by heat. Indeed, heat stress increased GSH-Px activity in the chicken liver (Tan et al., Reference TAN, YANG, FU, FENG and ZHANG2010), serum (Yang et al., Reference YANG, TAN, FU, FENG and ZHANG2010), erythrocytes (Aengwanich and Suttajit, Reference AENGWANICH and SUTTAJIT2013) and thigh muscle (Huang et al., Reference HUANG, JIAO, SONG, ZHAO, WANG and LIN2015a), but was not affected in breast muscle. In contrast, Se and vitamin E supplementation increased GSH-Px activity in skeletal muscles of heat stressed chickens, while there was no effect of such supplementation in the control, unstressed chickens (Ghazi Harsini et al., Reference GHAZI HARSINI, HABIBIYAN, MOEINI and ABDOLMOHAMMADI2012). It should be mentioned that heart muscle is extremely sensitive to heat stress and various feed additives can help protect it. In the heart of heat-stressed chickens at day 31 of age, both Curcuma xanthorrhiza and Origanum compactum essential oils were shown to increase GSH-Px activity compared with an unsupplemented control (Akbarian et al., Reference AKBARIAN, MICHIELS, GOLIAN, BUYSE, WANG and DE SMET2014). However, when stress is too high to allow adaptation, activity decreases, and extreme heat stress decreased GSH-Px activity in serum, muscle (Sahin et al., Reference SAHIN, ORHAN, TUZCU, SAHIN, HAYIRLI, BILGILI and KUCUK2016), spleen (Xu et al., Reference XU, LI, HUANG, HE and TIAN2014) and bursa of Fabricius (Xu and Tian, Reference XU and TIAN2015).

cold stress

Data on the effect of cold stress on GSH-Px activity are not consistent. For example, when broilers were exposed to a cool environment for three weeks, plasma GSH-Px activity decreased compared with normal temperature chicks (Ramnath and Rekha, Reference RAMNATH and REKHA2009). In contrast, acute cold stress was associated with increased GSH-Px activity in spleen, thymus and bursa of Fabricius (Zhao et al., Reference ZHAO, ZHANG, QU, YAO, LI, LI and XU2014b). In fact, acute cold stress initially increased (1-3 hours) and then decreased (24h) GSH-Px activity in chicken heart tissue (Zhao et al., Reference ZHAO, ZHANG, WANG, ZHANG, YAO, LI and XU2013). In contrast, in chronic cold stress, GSH-Px activity in the heart initially decreased (five days) and later (10-20 days) recovered (Zhao et al., Reference ZHAO, ZHANG, WANG, ZHANG, YAO, LI and XU2013).

other stresses

Various other conditions can affect GSH-Px activity in chicken blood and tissues. Among the mycotoxins studied, aflatoxin B1 showed the most consistent negative effect on GSH-Px activity in various chicken tissues including liver and spleen (Liu et al., Reference LIU, MA, ZHAO, JIA, ZHANG, JI and WANG2016b). Depending on the experimental conditions, including doses used, T-2 toxin was shown to decrease hepatic activity of GSH-Px by 36.8% (Dvorska et al., Reference DVORSKA, PAPPAS, KARADAS, SPEAKE and SURAI2007) or 30% (Bócsai et al., Reference BÓCSAI, PELYHE, ZÁNDOKI, ANCSIN, SZABÓ-FODOR, ERDÉLYI, MÉZES and BALOGH2016) or increase hepatic GSH-Px activity three-fold (Leal et al., Reference LEAL, SHIMADA, RUÍZ and GONZÁLEZ DE MEJÍA1999). It is interesting to note that subtoxic dietary level of deoxynivalenol (DON) increased GSH-Px activity in chicken duodenal mucosa (Placha et al., Reference PLACHA, BORUTOVA, GRESAKOVA, PETROVIC, FAIX and LENG2009) and dietary zearalenone (ZEA) increased GSH-Px in the duodenal mucosa and kidney tissues (Grešáková et al., Reference GREŠÁKOVÁ, BOŘUTOVÁ, FAIX, PLACHÁ, COBANOVÁ, KOŠÍKOVÁ and LENG2012).

It has been shown that GSH-Px activity in liver and muscle was significantly higher during feed withdrawal in layers kept under dark conditions than in the control group (Naziroglu et al., Reference NAZIROGLU, SAHIN, SIMSEK, AYDILEK and ERTAS2000). Transporting chickens increased GSH-Px in muscles (Wang et al., Reference WANG, ZHU, LI, LIU, LI, GAO, ZHOU and ZHANG2015), while it did not affect erythrocyte GSH-Px activity (Perai et al., Reference PERAI, KERMANSHAHI, MOGHADDAM and ZARBAN2015). Increased humidity is shown to increase GSH-Px activity in chicken pectoral muscles (Wei et al., Reference WEI, HU, SA, LIU, LI and SUN2014). Exposure of broilers to blue light increased GSH-Px in their breast and leg muscles (Ke et al., Reference KE, LIU, WANG and CHEN2011). In contrast, in pullets, fasting resulted in a significant decrease of whole blood haemolysate GSH-Px activity (Milinković-Tur et al., Reference MILINKOVIĆ-TUR, STOJEVIĆ, PIRSLJIN, ZDELAR-TUK, POLJICAK-MILAS, LJUBIĆ and GRADINSKI-VRBANAC2007) and high nutrient density diet decreased GSH-Px in heart muscle (Peng et al., Reference PENG, WANG, NING and GUO2013).

diseases

Eimeria tenella challenge was associated with substantial (more than 2.5-fold) increase in GSH-Px activity in chicken plasma (Bun et al., Reference BUN, GUO, GUO, JI and CAO2011). Mitochondrial GSH-Px activity in lung was elevated in broilers with pulmonary hypertension syndrome (PHS) compared to controls (Iqbal et al., Reference IQBAL, CAWTHON, BEERS, WIDEMAN and BOTTJE2002). Similarly, GSH-Px was upregulated in the brain of cold-induced, pulmonary hypertensive chickens (Hassanpour et al., Reference HASSANPOUR, KHALAJI-PIRBALOUTY, NASIRI, MOHEBBI and BAHADORAN2015). However, in most cases, disease challenge was associated with decreased GSH-Px activity. In particular, decreased blood GSH-Px activity was shown in situations of necrotic enteritis (Zhou et al., Reference ZHOU, ZENG, NI, TU, YIN, PAN and JING2016), infection bronchitis (Lin et al., Reference LIN, HUANG, GUO, LIU, LIU, ZOU, ZHU, DENG, KUANG, ZHANG, CAO and HU2015) and Ascaridia infection (Gabrashanska et al., Reference GABRASHANSKA, GALVEZ-MORROS, TEODOROVA, ERMIDOU-POLLET and POLLET2007). Similarly, Newcastle disease infection decreased GSH-Px activity in chicken brain and liver (Subbaiah et al., Reference SUBBAIAH, RANIPRAMEELA, VISWESWARI, RAJENDRA and LOKANATHA2011).

antioxidant supplements

Dietary antioxidants can affect GSH-Px activity in chickens. However, data on the relationship between dietary vitamin E and GSH-Px are not consistent. In most cases, dietary vitamin E activated GSH-Px activity in liver (Hu et al., Reference HU, WANG, AHMAD, ZHANG, ZHANG and ZHONG2015) and erythrocytes (Cinar et al., Reference CINAR, YILDIRIM, YIGIT, YALCINKAYA, DURU, KISA and ATMACA2014). Although, under different experimental conditions, vitamin E supplementation decreased chicken plasma GSH-Px (Mahmoud and Hijazi, Reference MAHMOUD and HIJAZI2007) but did not affect activity in muscles (Voljc et al., Reference VOLJC, FRANKIC, LEVART, NEMEC and SALOBIR2011). Ascorbic acid, a water-soluble dietary antioxidant, was shown to increase activity of the GSH-Px activity in chicken plasma (Oztürk-Urek et al., Reference OZTÜRK-UREK, BOZKAYA and TARHAN2001) or erythrocytes (Cinar et al., Reference CINAR, YILDIRIM, YIGIT, YALCINKAYA, DURU, KISA and ATMACA2014). Similarly, GSH-Px activity in serum, liver and breast muscle significantly increased in chickens fed with lipoic acid (Chen et al., Reference CHEN, MA, JI, ZHANG, ZHAO, ZHANG and JIE2011).

plant extracts

Various plant materials or extracts have been shown to increase GSH-Px activity in chicken tissues. For example, dietary polysavone (1·5 g/kg), a natural extract from alfalfa, rich in carotenoids and flavonoids, increased GSH-Px in chicken serum and liver (Dong et al., Reference DONG, GAO, SU, TONG and ZHANG2011). Dietary lycopene (carotenoid) in the maternal hen's diet increased GSH-Px activity in the liver of the newly hatched chicks (Sun et al., Reference SUN, CHEN, WANG, MA, XIE, GAO, CHEN, ZHANG and BI2015). Similarly, tomato pomace, a rich source of lycopene, increases serum GSH-Px (Hosseini-Vashan et al., Reference HOSSEINI-VASHAN, GOLIAN and YAGHOBFAR2016). As mentioned above, Сurcuma xanthorrhiza and Origanum compactum, rich sources of flavonoids, increased GSH-Px in chicken heart (Akbarian et al., Reference AKBARIAN, MICHIELS, GOLIAN, BUYSE, WANG and DE SMET2014), while orange peel extract and Curcuma xanthorrhiza essential oil increased GSH-Px in chicken erythrocytes (Akbarian et al., Reference AKBARIAN, GOLIAN, KERMANSHAHI, DE SMET and MICHIELS2015). Supplementation of ginger increased GSH-Px activity in chicken serum (Zhang et al., Reference ZHANG, YANG, WANG, YANG, JIANG and GAI2009), while supplementation of Astragalus membranaceus root powder increased activity of GSH-Px in the serum of chickens at 21 and 42 days (Zhang et al., Reference ZHANG, YANG, WANG and YANG2013). Interestingly, garlic oil also increases GSH-Px activity in blood plasma, erythrocytes and liver of chicken (Ancsin et al., Reference ANCSIN, ERDELYI, BALOGH, SZABO-FODOR and MEZES2013).

However, plants and their extracts are not always effective in modulating GSH-Px activity. For example, xanthophyll supplementation enhanced antioxidant capacity and reduced lipid peroxidation in different tissues of hens and chicks, but did not affect serum or liver GSH-Px activity (Gao et al., Reference GAO, XIE, MA, ZHANG, ZHU, SHU, SUN, JIN and BI2013). Furthermore, dietary supplementation of clove and agrimony or clove and lemon balm did not affect blood GSH-Px activity in chickens (Petrovic et al., Reference PETROVIC, MARCINCAK, POPELKA, SIMKOVA, MARTONOVA, BULECA, MARCINCAKOVA, TUCKOVA, MOLNAR and KOVAC2012).

other supplements

There is a range of feed supplements that are associated with increasing GSH-Px activity in chicken tissues. For example, live yeast probiotics, containing Saccharomyces cerevisiae at 4.125×10⁶ CFU per 100 ml, increased serum GSH-Px activity in broiler chickens (Aluwong et al., Reference ALUWONG, KAWU, RAJI, DZENDA, GOVWANG, SINKALU and AYO2013). Similarly Lactobacillus plantarum (probiotic) dietary supplementation increases GSH-Px activities in chicken serum and liver at 21 days of age (Shen et al., Reference SHEN, YI, NI, ZENG, JING, LEI, BIAN, ZENG, LI and XIN2014). A stimulating effect of a probiotic on liver and serum GSH-Px was confirmed later by Bai et al. (Reference BAI, HUANG, ZHANG, HE, ZHANG and WANG2017). It has been shown that LPS can decrease GSH-Px activity in intestinal mucosa (Wu et al., Reference WU, WANG and QI2016) and downregulates GSH-Px mRNA expressions (Zheng et al., Reference ZHENG, WU, SONG, ZHANG, ZHANG, ZHANG, ZHANG, WANG and WANG2016). In chicken bursal lymphocytes, Sargassum polysaccharide increases GSH-Px activity (Zhang et al., Reference ZHANG, HU, LIU and SHUAI2011) and bursopentine, a novel pentapeptide isolated from chicken bursa of Fabricius, increases GSH-Px activity in dendritic cells (Qin et al., Reference QIN, YIN, YU and YANG2015). Furthermore, vitamin A in high doses decreased GSH-Px activity in the chicken liver and brain (Surai et al., Reference SURAI, KUKLENKO, IONOV, NOBLE and SPARKS2000), while menadione did not affect GSH-Px in chicken liver (Marchionatti et al., Reference MARCHIONATTI, PEREZ, DIAZ DE BARBOZA, PEREIRA and TOLOSA DE TALAMONI2008).

drugs

There are some common drugs used in poultry industry which affect GSH-Px. For example, it was shown that salinomycin (Kamashi et al., Reference KAMASHI, REDDY, REDDY and REDDY2004) and deltamethrin (Jayasree et al., Reference JAYASREE, REDDY, REDDY, ANJANEYULU and KALAKUMAR2003) increased GSH-Px in whole blood of chickens. However, in another paper it was shown that GSH-Px activity in the liver decreased rapidly as a result of salinomycin toxic effects (Mézes et al., Reference MÉZES, SÁLYI, BÁNHIDI and SZEBERÉNYI1992). In fact, in acute monensin poisoning GSH-Px activity in liver and breast muscle initially decreased, then tended to rise (Sályi et al., Reference SÁLYI, MÉZES and BÁNHIDI1990).