Dietary supplementation of Yucca schidigera extract enhances productive and reproductive performances, blood profile, immune function, and antioxidant status in laying Japanese quails exposed to lead in the diet

Dietary supplementation of Yucca schidigera extract enhances productive and reproductive... ABSTRACT The present study investigated the toxic impacts of lead (LD) on the productive and reproductive performances of Japanese quails and the role of Yucca schidigera extract (YSE) in reducing these impacts. A total of 360 mature Japanese quails (at 2 months of age) were used and the experiment was lasted for 8 wk. The birds were divided into 6 equal groups as follows: control (basal diet), basal diet + 100 mg LD/kg diet, basal diet + YSE (100 mg/kg diet), basal diet + YSE (200 mg/kg diet), basal diet + LD (100 mg/kg diet) + YSE (100 mg/kg diet), and basal diet + LD (100 mg/kg diet) + YSE (200 mg/kg diet). LD resulted in a significant decrease in feed intake (FI), feed conversion ratio (FCR), and egg production of birds compared with the control group. Supplementation of YSE (100 or 200) to LD containing diet could significantly improve the quail performance parameters to be comparable with the control values. Fertility and hatchability % were decreased by LD, whereas YSE at both levels (100 or 200) separately or in combination with LD showed fertility and hatchability percentages comparable to that of control. Triglycerides, cholesterol, and LDL contents in LD plus YSE100 or LD plus YSE200 groups were significantly decreased than LD alone group. LD significantly decreased superoxide dismutase and catalase activities in the serum with no effect on reduced glutathione content. Co-exposure to YSE100 or YSE200 with LD significantly increased the catalase activity and numerically increased the superoxide dismutase activity than LD alone. YSE100 or YSE200 decreased malondialdehyde contents than LD alone group. LD plus YSE100 or YSE200 groups exhibited significant improvements in the level of immunoglobulins. Co-exposure to YSE with LD significantly decreased the LD residues in egg than the LD group. The obtained results showed that YSE exhibited a potential modulatory role against the LD-induced inhibitory effects on the productive and reproductive performances of Japanese quails and YSE at 200 mg/kg diet was more effective than 100 mg/kg diet in reversing the LD-induced alterations. INTRODUCTION The environmental contamination has been increased during the last decades resulting in potential hazards on all biological systems including birds which experienced a great reduction in their population (Gaston et al., 2003). Lead (LD) is one of the most widespread environmental pollutants particularly in industrial areas (Klaminder et al., 2006). Birds are exposed to LD from various sources such as the general environment, industrial pollution and contamination of water, soil and food by agricultural processing (Berglund et al., 2010). Oral administration of LD results in its absorption at a small extent but its elimination rate is slow; as a result, exposure to small quantities for long periods could lead to accumulation of harmful levels (Madhavi et al., 2007). When LD enters in to the blood stream, it is absorbed and some of it is bound to erythrocytes and some is conjugated in the liver then pass to kidney. After that, a small amount is excreted in urine and the remaining stay in plasma to be distributed in the body and accumulates in various organs and impaired their function. Ingestion of LD has been reported to induce poor performance, weight loss, decreased production, and even death of animals (Hoshiari and Pourkhabbaz, 2012). Lead has been reported to induce some clinical manifestations in birds such as atrophy of breast muscle and loss of visceral and subcutaneous fat (Beyer et al., 1998). It also resulted in weight loss, poor body conditions, and even starvation of birds as subsequent conditions following muscular paralysis of digestive system including esophagus, proventriculus, gizzard, and the intestines (Pattee and Pain, 2003). Lead has been accounted for mortality and morbidity in birds from different species in some previous reports (Mateo et al., 2003; Pain et al., 2015). Lead also exhibited some immunotoxic effects as described by Ohsawa (2009). Additionally, birds can maintain metals in high levels in different tissues like kidney, liver, meat, and eggs (Farahani, et al., 2015; Humayun et al., 2015). Such residues can be transmitted to human and other organisms through food chain resulting in a wide range of biochemical and physiological abnormalities in cardiovascular system, nervous system, reproductive organs, kidneys, and red blood cells (Elayat and Bakheetf, 2010). Lead poisoning has been also reported to induce oxidative stress and enhance the production of reactive oxygen species (ROS) as major mechanisms of its toxic action and thereby can cause cell structure damage, lipid peroxidation, and DNA and protein oxidation (Kasperczyk et al., 2012). The potential effect of LD in induction of oxidative stress suggests that some medicinal plants and herbs with antioxidant and possible chelating activities may be helpful in modulating the LD-induced toxicity (Patrick, 2006). Yucca schidigera is a plant belongs to the family “Agavaceae,” native to Mexico and the South-Western United States. Yucca is a widespread medicinal plant and is considered as natural (100%) additive (Balazi et al., 2013). It has many beneficial effects like growth promoter, hypocholesterolemic, hypoglycemic, anti-inflammatory, antioxidant, anticarcinogenic, and immunostimulatory (Alagawany et al., 2016a). Yucca is a commercial source of saponins, resveratrol, various enzymes, and antioxidants (Chrenková et al., 2012; Alagawany et al., 2016b; Farag et al., 2016). Steroid saponins of yucca products are approved by GRAS (Generally Recognized as Safe) given by FDA (Food and drug administration) that allows their human dietary use (Tenon et al., 2017). It is also used in the manufacture of cosmetics, beverages, and as dietary supplement for poultry and animal. In addition, yucca can conserve ammonia and decrease its content in the poultry houses and air and decrease blood urea concentration (Piacente et al., 2005) and has a great absorption capacity for harmful volatile compounds, such as ammonia and hydrogen sulfide (Vlckova et al., 2017). Therefore, the main objective of the present study was to investigate the toxic effects of LD on productive and reproductive performances, blood biochemical parameters, and the oxidative status of laying Japanese quails and to determine the egg quality criteria and residual concentrations of LD in the produced eggs. Additionally, this study would clarify the potential modulatory role of Yucca schidigera extract (YSE) against these effects. MATERIALS AND METHODS Birds and Diets The present study was carried out at Poultry Research Farm, Faculty of Agriculture, Zagazig University, Egypt. All experimental procedures were carried out according to the Local Experimental Animal Care Committee and approved by the ethics of the institutional committee of Zagazig University, Zagazig, Egypt. A total number of 360 mature Japanese quails (Coturnix coturnix japonica) at 2 mo of age with initial body weight 240.50 ± 2.00 g were used in a complete randomized design experiment with 6 treatments of 60 birds each. Each group was subdivided into 4 replicates with 15 birds. The experiment lasted for 8 wk. Birds were fed the basal diet with or without supplemental LD or YSE that formulated to meet laying quail requirements according to NRC (1994). The treatments were as follows: 1) control basal diet, 2) basal diet + 100 mg LD/kg diet, 3) basal diet + YSE (100 mg/kg diet), 4) basal diet + YSE (200 mg/kg diet), 5) basal diet + LD (100 mg/kg diet) + YSE (100 mg/kg diet), and 6) basal diet + LD (100 mg/kg diet) + YSE (200 mg/kg diet). The ingredients and chemical composition of the basal diet are presented in Table 1. Birds were housed in conventional type cage (50 × 30 × 50 cm3; 1,500 cm2 of floor space) with feed and fresh water provided ad libitum. Birds also were maintained on a 17 h light: 7 h dark cycle throughout the trial. All birds were kept under the same managerial, hygienic, and environmental conditions. Table 1. Composition and calculated analysis of the basal diets. Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 1Layer Vit. & Min. premix: Each 2.5 kg of vitamins and minerals premix (commercial source pfiezer Co.): consist of Vit. A 12 MIU, VIT E 15 KIU, Vit. D3 4 MIU, Vit. B1 1 g, Vit B2 8 g, Vit B6 2 g, Vit B12 10 mg, pantothenic acid 10.87 g, niacin30 g, folic acid 1 g, biotin 150 mg, copper 5 g, iron 15 g, manganese 70 g, iodine 0.5 g, selenium 0.15 g, zinc 60 g, and antioxidant 10 g. 2Calculated according to NRC (1994). View Large Table 1. Composition and calculated analysis of the basal diets. Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 1Layer Vit. & Min. premix: Each 2.5 kg of vitamins and minerals premix (commercial source pfiezer Co.): consist of Vit. A 12 MIU, VIT E 15 KIU, Vit. D3 4 MIU, Vit. B1 1 g, Vit B2 8 g, Vit B6 2 g, Vit B12 10 mg, pantothenic acid 10.87 g, niacin30 g, folic acid 1 g, biotin 150 mg, copper 5 g, iron 15 g, manganese 70 g, iodine 0.5 g, selenium 0.15 g, zinc 60 g, and antioxidant 10 g. 2Calculated according to NRC (1994). View Large Tested Chemicals Lead in the form of LD acetate (99.6% purity) was purchased from El-Gomhoria Chemical Co., Egypt. Yucca schidigera extract was purchased from Free Trade Egypt Company (El-Behera, Egypt). All other chemicals were purchased from Sigma (St. Louis, MO). All other reagents used were of analytical grade. Data Collection and Calculation Feed intake (FI) (g) was recorded daily, whereas feed conversion ratio (FCR) was calculated as the egg mass value divided by the amount of consumed feed. Egg numbers and weights were recorded daily to compute the egg mass. Fertility and Hatchability Percentages Twenty eggs from each replicate were collected and incubated at the end of each month. After hatching, chicks were counted and non-hatched eggs were examined to calculate the fertility and hatchability percentages. Fertility and hatchability percentages were calculated as follows: fertility percentage = (number of fertile eggs/total eggs set) × 100; hatchability percentage from fertile eggs = (number of hatched chicks/total number of fertile eggs) × 100; hatchability percentage from the total egg set = (number of hatched chicks/total eggs set) × 100. Egg Quality Criteria Egg quality criteria were measured monthly using 3 eggs from each replicate. Interior and exterior parameters of egg quality (percentages of yolk, albumen, shell, and egg shape index, yolk index Haugh units, and shell thickness) were determined according to Romanoff and Romanoff (1949). Blood Sampling and Laboratory Analyses Blood samples were randomly collected from 6 birds per treatment from the wing vein into sterilized tubes. The samples were allowed to coagulate for 30 min at room temperature and then centrifuged for 15 min at 3,500 rpm for serum separation; the serum samples were stored at –20°C until analysis. Total protein, albumin, globulin, total cholesterol, triglycerides, low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, alanine amino transferase (ALT), and aspartate aminotransferase (AST) were determined spectrophotometrically using commercial diagnostic kits provided from Biodiagnostic Co. (Giza, Egypt). Immunoglobulins (IgG and IgM) were determined according to Akiba et al. (1982). Antioxidant Assays Superoxide dismutase (SOD) and catalase (CAT) activities as well as reduced glutathione (GSH) and malondialdehyde (MDA) concentrations were determined in serum by spectrophotometric methods (Hitachi spectrophotometer, Japan) using commercial biodiagnostic kits provided from BioMérieux (Marcy l’etoile, France) according to the manufacturer's instructions. Determination of LD Residues Eggs were transferred to the laboratory in plastic bags and stored at cool and dark place. Then, each egg was washed by distilled water and soap and cut at the air cell end by dissecting scissors and pointed forceps. The content of each sample was placed in a clean glass jar. The samples then were dried at 75°C to get constant weight (Zaki, 1998). Then, the egg samples were digested by acid digestion method of Mahaffey et al. (1981),where 1 g of each sample was putted into a clean screw capped glass bottle and digested with a 4 mL of (nitric/perchloric acid, 1:1) as a digestion solution. Initial digestion was performed at room temperature for 24 h, and then heated for 2 h at110°C. Then the samples were left to cool and then followed by addition of deionized water and the solution was left for 1 h in water bath to expel nitrous gases. The digests were filtered and diluted to 25 mL deionized water (Julshman, 1983). The obtained solution was then analyzed using flame atomic absorption spectrophotometer. Statistical Analysis The data were statistically analyzed using general linear models procedure adapted by SPSS for user's guide with one-way ANOVA. The differences among treatments were determined using the post hoc Newman–Keuls test (P < 0.05). RESULTS Productive Performance of Japanese Quails Table 2 depicts the effects of LD along with the role of YSE on productive performance of quails during the experimental period. Supplementation of LD to quails diet showed a significant decrease in the FI, FCR, and egg production of birds compared with the control group. On the other hand, there were no significant changes in the egg weight or egg mass among the different experimental groups. Supplementation of YSE (100 or 200) to LD containing diet could significantly improve the quail performance parameters (FI, FCR, and egg production) and restored them to the control values. YSE200 groups showed the highest FI level and egg production percentage compared to all other groups. Table 2. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on productive parameters of Japanese quail. Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Table 2. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on productive parameters of Japanese quail. Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Reproductive Performance of Japanese Quails Results in Table 3 indicate that supplementation of diets with LD resulted in a significant decrease in the fertility percentage compared to the control group. On the other hand, YSE at both levels (100 or 200) separately or in combination with LD showed fertility percentages comparable to that of control. Table 3. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on reproductive parameters of Japanese quail. Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Table 3. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on reproductive parameters of Japanese quail. Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Results of hatchability (%) from the total set of eggs revealed no significant changes between control, YSE 100, or YSE200 groups. Whereas, this percentage was significantly decreased in the LD group compared to the control group. On the other hand, supplementation of YSE (100 mg/kg diet) to LD containing diet could not improve the reduced hatchability of quails, whereas addition of YSE (200 mg) to LD diet could restore the hatchability percentage of birds to control values. Hatchability (%) from the fertile eggs was found to be significantly decreased in the LD group compared to control, whereas the YSE100 group showed the highest percentage among all other experimental groups. On the other hand, supplementation of YSE (100 or 200 mg/kg diet) to LD diet could restore the hatchability (%) from the fertile eggs to that of control. Egg Quality Criteria Supplementation of quail's diet by LD, YSE (100 or 200) separately or in combination did not alter the egg composition (shell, yolk, and albumen), exterior or interior egg quality parameters than the control group as shown in Table 4. Table 4. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on egg quality criteria in Japanese quail. Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 1Overall treatment P-value. View Large Table 4. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on egg quality criteria in Japanese quail. Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 1Overall treatment P-value. View Large Liver Function Markers Liver function markers are given in Table 5. Total protein, albumin, and globulin levels were found to be decreased in serum of LD-exposed group only compared to control. The higher levels of total protein and albumin were obtained for birds of YSE200 group followed by the YSE100 group compared to the control group. Co-exposure to YSE 100 or 200 with LD was found to significantly increase the levels of total protein, albumin, and globulin. Table 5. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on liver functions in serum of Japanese quail. Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1AST: aspartate aminotransferase, ALT: alanine aminotransferase 2Overall treatment P-value. View Large Table 5. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on liver functions in serum of Japanese quail. Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1AST: aspartate aminotransferase, ALT: alanine aminotransferase 2Overall treatment P-value. View Large In response to LD exposure, the values of AST and ALT were increased significantly compared to the control group. On the other hand, lower levels of AST and ALT were observed for YSE100 and YSE200. AST and ALT levels in LD plus YSE100 or LD plus YSE200 groups were significantly decreased than LD alone group and a better reduction was observed in LD plus YSE 200 group; however, both the levels did not return the AST and ALT levels to the control values. Effects on Lipid Profile Exposure of quails to LD in their diet significantly increased the triglycerides, cholesterol, and LDL whereas significantly decreased HDL values compared to control and other treatment groups. On the other hand, contradicting results were obtained for the YSE200 group. Triglycerides, cholesterol, and LDL contents in LD plus YSE100 or LD plus YSE200 groups were significantly decreased than LD alone group and a better effect was observed in LD plus YSE 200 group where it could restore the triglyceride level to normal and decreased the cholesterol level than the LD+YSE100 group however still higher than control. Co-exposure to YSE 100 or 200 with LD was found to significantly increase the levels of HDL than control and YSE200 was more effective than YSE100. On the other hand, YSE100 alone did not alter the HDL value compared to control (Table 6). Table 6. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on lipid profile in serum of Japanese quail. Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Table 6. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on lipid profile in serum of Japanese quail. Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Effects on Antioxidant Status Table 7 shows the effects of LD and YSE on antioxidant system of quails. The LD treatment significantly decreased both the SOD and CAT enzyme activities in the serum of treated quails compared to the control group. YSE100 did not significantly change the antioxidant activities than those of control, whereas YSE200 significantly enhanced the SOD and CAT activities to be better than the control itself. Table 7. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on antioxidant and immunity in serum of Japanese quail. Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1SOD: superoxide dismutase, CAT: catalase, GSH: reduced glutathione, MDA: malondialdehyde, IgG: immunoglobulin G, IgM: immunoglobulin M. 2Overall treatment P-value. View Large Table 7. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on antioxidant and immunity in serum of Japanese quail. Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1SOD: superoxide dismutase, CAT: catalase, GSH: reduced glutathione, MDA: malondialdehyde, IgG: immunoglobulin G, IgM: immunoglobulin M. 2Overall treatment P-value. View Large GSH content was not significantly changed in all groups compared to control except YSE200 that was higher than control. Co-exposure to YSE100 or YSE200 with LD was found to significantly increase the CAT activity than LD alone to be comparable with control and numerically increase the SOD activity however still under control values. The lipid peroxidation, as evidenced by the formation of MDA, was significantly increased in LD-treated group compared to the control group. MDA contents in LD plus YSE100 or YSE200 groups were significantly decreased than LD alone group, and a better effect was observed in LD plus YSE 200 group. Meanwhile, MDA level in the YSE200 group was significantly lower than control however YES100 was comparable to both control and YSE200 groups. Effects on Immunoglobulins Results in Table 7 showed that the highest values of immunoglobulins (IgG and IgM) were obtained by birds fed diet supplemented with 200 mg YSE/kg followed by those received 100 mg YSE/kg diet, whereas the lowest values of IgG and IgM were obtained in response to LD exposure. On the other hand, LD plus YSE100 or LD plusYSE200 groups exhibited significant improvements in the level of immunoglobulins compared to the LD group and YSE200 showed better effects. LD Residues Analysis of eggs for detection of LD residues at the end of the experiment is represented in Figure 1, which revealed that the highest concentrations of accumulated LD were detected in eggs of LD-exposed group (0.932 ± 0.04). On the other hand, there were no significant changes in the residue level of LD among control, YSE100, and YSE200 groups (0.13 ± 0.04, 0.09 ± 0.03, 0.04 ± 0.02), respectively. Co-exposure to YSE100 or YSE200 with LD was found to significantly decrease the LD residues in egg 0.797 ± 0.04, 0.700 ± 0.02 respectively than the LD group. The YSE200 was better than YSE100 however still higher than control level. Figure 1. View largeDownload slide Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca schidigera extract (YSE, 100 or 200 mg/kg diet) on accumulation of lead residues (μg/g wet weight) in eggs of treated Japanese quails compared to the control group. Figure 1. View largeDownload slide Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca schidigera extract (YSE, 100 or 200 mg/kg diet) on accumulation of lead residues (μg/g wet weight) in eggs of treated Japanese quails compared to the control group. DISCUSSION The aim of the current poultry production is to achieve the highest growth rates, FCRs, and production percentages to cover the widely increasing demand of animal proteins particularly in developing countries. The intensive breeding and farming increased the sensitivity of birds to external stressors from their surrounding environment resulting in acute stress responses, reduced productive and reproductive performances, health problems, increased susceptibility to infectious diseases, and low-quality poultry products (Shahid ul Islam et al., 2014). Therefore, it is of importance to explore the stress responses to environmental contaminants on the productive and reproductive performance of birds and try to find effective methods to decrease these responses. Japanese quail could be used as a model to study the effects of environmental contamination as they are similar to wild birds, ready available, and information concerning their normal physiology is solid (Franson and Pain, 2011). The present study indicated that LD supplementation to diets of quails showed a significant decrease in FI, FCR, and egg production; however, it did not influence the other performance parameters including egg weight and egg mass compared to control. Exposure of quails to LD in their diet decreased the hatchability of total eggs set, hatchability of fertile eggs set, and the percentage of fertile eggs compared to control. On the other hand, LD did not alter the egg quality criteria of exposed quails. High dietary LD has been reported to inhibit the growth performance parameters in quails (Humayun et al., 2015; Farag et al., 2018). Similarly, LD decreased the body weight and egg production in adult quail hens (Stone and Soares, 1976). On the same context, Butkauskas and Sruoga (2004) stated that LD could increase the number of unfertile eggs of quail up to 30% relative to control. Salisbury, et al. (1958) reported a cessation of egg production in adult chicken hens intoxicated with LD. The inhibitory effect of dietary LD exposure on reproductive performance of female quails was reported by Edens and Garlich (1983), who demonstrated that dietary LD significantly depressed the total plasma calcium reflecting the inability of intoxicated quails to mobilize adequate amount of plasma calcium. Moreover, LD exposure decreased the weight and function of ovary in exposed quails. Therefore, it was suggested that ovary could be involved in the regulation of egg production than calcium. Additionally, LD has been reported to induce neurotoxicity in quails inducing impairment of the neurochemical control on reproductive hormones regulation (Edens, 1985). In our study, supplementation of YSE to bird's diet concurrently with LD resulted in significant improvements in the altered productive performance parameters of quails including FI, FCR, egg production, fertility, and hatchability to levels that are comparable to those of control. Dietary supplementation of Y. schidigera has been reported to induce significant impacts on layer performance by increasing the egg production and final body weight (Gurbuz et al., 2016). Similarly, Cheek (1998) reported that feeding poultry on yucca could improve their growth and productivity. These positive effects of yucca could be returned to the presence of steroidal saponins as a main component and other surface active components that could promote the utilization and absorption of nutrients from gastrointestinal tract by improving its epithelial lining of the cell membrane and decreasing the surface tension (Goetsch and Owens, 1985). Fertility and hatchability are important parameters in studying the reproductive performance; they are affected by environment, insufficient nutrients, and genetic involvement (Ayasan, 2013). Therefore, to obtain the highest fertility and hatchability percentages of quails, optimum conditions should be provided before and after hatching (Ggüçlü, 2011). In the present study, yucca at high level (200 mg/kg body weight) was found to improve fertility and hatchability percentages in the presence of LD. This improvement could be explained by the suggestions of El Anwer et al. (2009), who returned the increased hatchability and fertility to 2 main assumptions; the first assumption is the ability of yucca to reduce ammonia concentration in the surrounding atmosphere of eggs that could help in adjusting the egg pH. The reducing effect of yucca on blood urea has been previously reported in broilers (Balog et al., 1994) that could be mainly due to saponin, stilbenes, and carbohydrates in yucca. These components have been reported to have modulatory effects on renal functions and could increase the clearance of urea and lower blood concentrations of ammonia and urea (Duffy et al., 2001). YES has could inhibit urease enzyme in vivo and in vitro (Asplund 1991; Balog et al., 1994). Biochemical findings of the present study revealed that total protein level was found to be decreased in serum of LD-exposed group compared to control. These results are in accordance with those of Humayun et al. (2015) who studied hematobiochemical changes induced by LD poisoning in quails. The decreased protein level could be returned to increasing protein utilization to obtain the energy required by quails exposed to toxic stresses. Furthermore, Hamidipoor et al. (2016a) related the decrease in total protein of quails exposed to LD acetate and deltamethrin to the reduced utilization of dietary protein, malnutrition, or decreased protein synthesis in liver. Globulin and albumin are the major components of total protein and the changes in their levels can be used to monitor the health status of liver, kidney, and the immune system (Patra et al., 2011). When protein synthesis in the liver is reduced, it directly affects the globulin level. In agreement with this, the results of the present study showed that LD significantly decreased the albumin and globulin level than control a long with decreasing total protein level in LD-exposed quails. In the present study, the extent of LD-induced cellular injury was assessed by monitoring the serum level of ALT and AST. These enzymes were released into serum or plasma in case of liver damage, necrosis, or inflammation. In addition, ALT enzyme has been reported to increase in muscular dystrophy heart failure, anemia, and obstruction of bile duct (Philip et al., 1995). Herein, LD significantly elevated ALT and AST activities in the serum of LD-treated quails. These results agreed with previous works reported an elevation in ALT and AST activities in serum after exposure to LD in quails (Humayun et al., 2015; Hamidipoor et al., 2016a). Lead significantly reduced the total protein, albumin, and globulin levels and significantly increased the AST and ALT activities in quails (Hamidipoor et al., 2016b). This elevation may be attributed to increasing the permeability of cellular membrane, fluidity of the microsomal membrane, or the damage of hypatocytes cell membranes (Abdou et al., 2007). Production of free radicals increased cellular basal metabolic rate, irritability, and destructive alteration of liver under the influence of LD (Ibrahim et al., 2012). Considering the effect of LD on lipid profile, the present study showed that exposure of quails to LD in their diet significantly increased triglycerides, cholesterol, and LDL while significantly decreased HDL values compared to control and other treatment groups. Contradicting results were obtained by Hamidipoor et al. (2016b), where LD exposure had no significant changes in cholesterol, whereas it significantly reduced the concentration of triglycerides. The disturbances in lipid profile could be possibly returned to enhanced biosynthesis of cholesterol and its accumulation in liver and/or impairment of biliary functions (Ashour et al., 2014) and this came on line with the obtained results of liver functions. From the present study, it was obvious that dietary supplementation of YSE improved the blood biochemical parameters (total protein, albumin, globulin) and the activities of liver function enzymes (ALT and AST) and showed positive effects on the lipid profile of quails in the co-exposed groups (LD+YSE) especially at high level. This indicates the potential modulatory role of YSE on liver function mainly due to yucca saponins and phenolics that showed hypocholesterolemic, antioxidant, hypoglycemic, anti-inflammatory, immunostimulatory, antiviral, anticarcinogenic, and anti-mutagenic activities (Gupta, 2014; Alagawany et al., 2016a). It is well known that powder and extracts of plants rich in saponins can alter the lipid metabolism of birds and different animal as reported by Rao and Kendall (1986). Saponins reduced the serum cholesterol level in laying hens (Aslan et al., 2004) and rabbits (Morehouse et al., 1999). Saponins can form complexes with cholesterol leading to its precipitation and can reduce hypercholesterolemia by altering the stability and size of cholesterol micelle and decreasing its penetration into mucous membrane cells (Milgate and Roberts, 1995). Additionally, saponins can reduce the absorption of cholesterol and facilitate the discharge of neutral sterols including plant sterols, cholesterol, coprostanol, and bile acids in fecal matter (Jenkins and Atwal, 1994). Saponins can also destruct the cell membrane and cause loss of cholesterol (Morehouse, Bangerter, DeNinno, Inskeep, McCarthy, Pettini, Savoy, Sugarman, Wilkins, Wilson, Woody, Zaccaro and Chandler, 1999). Moreover, the presence of saponins can enhance bile acid absorption and form high molecular weight micelles (cellulose saponin–bile acid complexes) thus prevent bile acids reabsorption and lead to the increase in the cholesterol conversion into bile acids in the hepatic tissue (Sidhu and Oakenfull, 1986). The decrease in cholesterol absorption decreased its hepatic content and this enhanced the activity of HMG-CoA reductase and increased the LDL receptors in the liver (Harwood et al., 1993). Exposure to LD can impair the antioxidant defense system and increase the cell vulnerability to the free radicles attack leading to oxidative damage (Liu et al., 2010). This could explain the observed decrease in SOD and CAT activities of LD-exposed quails in the present study. However, LD did not significantly alter the GSH content in serum of quails. The altered antioxidant status after LD exposure has been reported in some previous works on animals and workers (Baranowska-Bosiacka et al., 2012; Dai et al., 2013). Oxidative stress of LD exposure was also evidenced by increased MDA (lipid peroxidation marker) compared to control. The elevated MDA indicated the inability of antioxidant defense system to counteract the ROS-induced damage. These results agreed with some earlier reports in which LD induced oxidative damage in birds and significantly enhanced lipid peroxidation in liver of chick embryos (Somashekaraiah et al., 1992), in brain, and liver of mallards exposed to LD in the diet and in geese and mallards exposed to sediments contaminated by LD (Mateo et al., 2003). MDA levels increased in liver following LD exposure (Sandhir and Gill, 1995). These results could be returned to the destructive effects of LD on cell membrane components including proteins and lipids resulting in altered membrane function and structure (Donaldson and Knowles, 1993). In the present study, supplementation of YSE to bird's diet contained LD significantly improved the antioxidant enzymes activities, whereas it significantly decreased the serum level of MDA in birds compared to the LD group. These results indicate that YSE could counteract the undesirable impact of oxidation reaction and could decrease the lipid peroxidation in birds exposed to environmental contamination. Gümüş and İmik (2016) demonstrated that yucca can act as a good antioxidant for poultry and its supplementation to broiler diets increased the total antioxidant capacity by improving the antioxidants activities. These positive impacts could be attributed to the phytochemicals of yucca such as polyphenolic compounds (resveratrol (RES) and yuccaols A, B, C, D, and E) and steroidal saponins (Alagawany et al., 2015). RES exhibited a powerful scavenging activity against free radicals generated by heavy metals as hydroxyl and superoxide radicals and could make activation of the major transcription factors that regulate the response to antioxidants (erythroid-derived nuclear factor) (Rubiolo and Vega, 2008) and could improve the activities of CAT, GSH-Px, SOD, glutathione S-transferase (GST), and nicotinamide adenine dinucleotide phosphate (NADPH) quinoneoxidoreductase (Young et al., 2000). It could also maintain the reduced state of glutathione by inhibiting the formation of glutathione disulfide; thereby it can protect cells from the attack of free radicales (FR), prevent the oxidative damage of macromolecules, and inhibit apolipoprotein B protein peroxidation (Yan et al., 2012). Similarly, RES as a dietary supplement has been reported to diminish oxidative stress and improve the antioxidant status in birds (Liu et al., 2014). Moreover, RES and other phenolic compounds from yucca could inhibit the generation of FR and reduced lipid peroxidation (LPO) in blood platelets (Olas et al., 2003). The impact of environmental pollutants on the bird's immune system is of great importance as birds are highly required to compensate the shortage in animal protein sources and the presence of these pollutants could increase the susceptibility of birds to parasites and infectious diseases (Galloway and Depledge, 2001). The present study showed that LD significantly decreased the levels of immunoglobulin (IgG and IgM) in exposed birds. These findings came on line with the observed decrease in the levels of plasma globulin of the same group that indicated a reduced immunity as the liver cannot synthesis enough globulin for immunologic actions. On the same context, exposure to LD significantly reduced IgG, IgA, and IgM in serum accompanied with increased MDA as a marker of oxidative damage in some organs of rats (Gurer and Ercal, 2000). The significant decrease in IgG and IgM can indicate the deleterious effect of LD on the functions of B cells that could be resulted from oxidative damage (decreased antioxidant activities and increased MDA) of LD on these cells and this is totally agreed with Nuran Ercal et al. (2001). Lead has been reported to decrease the activation of lymphocytes and inhibit their proliferation, decrease the migration and motility of macrophage (Kiremidjian-Schumacher et al., 1981), and reduce the cytotoxicity and natural killer (Talcott et al., 1985). From the present study, it was obvious that dietary supplementation of YSE improved the immune response, which was evidenced by the significant improvements in immunoglobulins. This could be probably due to the modulating effect of yucca in liver functions including the level of globulin and the antioxidant power of YSE observed in the present study. These effects are consistent with some previous reports on the positive effects of YSE on immune functions, where yucca saponins could enhance cellular and antibody humoral immune responses, stimulate the cytokines secretions, and activate the innate immunity (Palatnik de Sousa et al., 2004). Saponins in chicken diets increased the level of IgA (Zhai et al., 2011). Supplementation of yucca powder to broiler chicks stimulated the immune responses (cellular and humoral) (Su et al., 2016). Similarly, yucca powder improved IgG content in layer chicken (Alagawany et al., 2016a). Fresh egg and egg products are among the most important nutritional sources in the daily diet so investigating the residual level of heavy metals is important as they could induce negative impacts on bird performance, productivity, and the consumers as well (Li et al., 2005). The present study revealed that eggs from LD-exposed quails showed the highest residual level than other experimental groups. Birds can reduce the deposition of metals into their eggs through decreasing the deposition of minerals. This type of protection could be sufficient to prevent deposition of some metals like Cr and Mn but insufficient for LD (Hui, 2002). This is in consistence with our results and may explain the obtained decreased hatchability percentage that could be returned to the ability of LD to induce some embryo toxic impacts. On the other hand, YSE supplementation significantly reduced the LD residues suggesting that in addition to its antioxidant activity, it could also act as chelator and this makes YSE a powerful candidate for treating LD toxicity. CONCLUSIONS From the obtained results, we concluded that exposure of quails to LD in their diets resulted in apparent adverse effects on the performance parameters (productive and reproductive) and altered the biochemical parameters of liver function and lipid profile in addition to its inhibitory effect on immune response of birds. These adverse effects were accompanied with oxidative damage evidenced by decreased antioxidant enzymes and increased lipid peroxidation. On the other hand, using of YSE as a natural feed additive in quail diets could alleviate the deleterious effects of LD and enhanced the immune function via improving levels of immunoglobulin. However, YSE at high level (200 mg/kg diet) was more effective than low one (100 mg/kg diet). 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Dietary supplementation of Yucca schidigera extract enhances productive and reproductive performances, blood profile, immune function, and antioxidant status in laying Japanese quails exposed to lead in the diet

Poultry Science , Volume 97 (9) – Sep 1, 2018

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Oxford University Press
Copyright
© 2018 Poultry Science Association Inc.
ISSN
0032-5791
eISSN
1525-3171
D.O.I.
10.3382/ps/pey186
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Abstract

ABSTRACT The present study investigated the toxic impacts of lead (LD) on the productive and reproductive performances of Japanese quails and the role of Yucca schidigera extract (YSE) in reducing these impacts. A total of 360 mature Japanese quails (at 2 months of age) were used and the experiment was lasted for 8 wk. The birds were divided into 6 equal groups as follows: control (basal diet), basal diet + 100 mg LD/kg diet, basal diet + YSE (100 mg/kg diet), basal diet + YSE (200 mg/kg diet), basal diet + LD (100 mg/kg diet) + YSE (100 mg/kg diet), and basal diet + LD (100 mg/kg diet) + YSE (200 mg/kg diet). LD resulted in a significant decrease in feed intake (FI), feed conversion ratio (FCR), and egg production of birds compared with the control group. Supplementation of YSE (100 or 200) to LD containing diet could significantly improve the quail performance parameters to be comparable with the control values. Fertility and hatchability % were decreased by LD, whereas YSE at both levels (100 or 200) separately or in combination with LD showed fertility and hatchability percentages comparable to that of control. Triglycerides, cholesterol, and LDL contents in LD plus YSE100 or LD plus YSE200 groups were significantly decreased than LD alone group. LD significantly decreased superoxide dismutase and catalase activities in the serum with no effect on reduced glutathione content. Co-exposure to YSE100 or YSE200 with LD significantly increased the catalase activity and numerically increased the superoxide dismutase activity than LD alone. YSE100 or YSE200 decreased malondialdehyde contents than LD alone group. LD plus YSE100 or YSE200 groups exhibited significant improvements in the level of immunoglobulins. Co-exposure to YSE with LD significantly decreased the LD residues in egg than the LD group. The obtained results showed that YSE exhibited a potential modulatory role against the LD-induced inhibitory effects on the productive and reproductive performances of Japanese quails and YSE at 200 mg/kg diet was more effective than 100 mg/kg diet in reversing the LD-induced alterations. INTRODUCTION The environmental contamination has been increased during the last decades resulting in potential hazards on all biological systems including birds which experienced a great reduction in their population (Gaston et al., 2003). Lead (LD) is one of the most widespread environmental pollutants particularly in industrial areas (Klaminder et al., 2006). Birds are exposed to LD from various sources such as the general environment, industrial pollution and contamination of water, soil and food by agricultural processing (Berglund et al., 2010). Oral administration of LD results in its absorption at a small extent but its elimination rate is slow; as a result, exposure to small quantities for long periods could lead to accumulation of harmful levels (Madhavi et al., 2007). When LD enters in to the blood stream, it is absorbed and some of it is bound to erythrocytes and some is conjugated in the liver then pass to kidney. After that, a small amount is excreted in urine and the remaining stay in plasma to be distributed in the body and accumulates in various organs and impaired their function. Ingestion of LD has been reported to induce poor performance, weight loss, decreased production, and even death of animals (Hoshiari and Pourkhabbaz, 2012). Lead has been reported to induce some clinical manifestations in birds such as atrophy of breast muscle and loss of visceral and subcutaneous fat (Beyer et al., 1998). It also resulted in weight loss, poor body conditions, and even starvation of birds as subsequent conditions following muscular paralysis of digestive system including esophagus, proventriculus, gizzard, and the intestines (Pattee and Pain, 2003). Lead has been accounted for mortality and morbidity in birds from different species in some previous reports (Mateo et al., 2003; Pain et al., 2015). Lead also exhibited some immunotoxic effects as described by Ohsawa (2009). Additionally, birds can maintain metals in high levels in different tissues like kidney, liver, meat, and eggs (Farahani, et al., 2015; Humayun et al., 2015). Such residues can be transmitted to human and other organisms through food chain resulting in a wide range of biochemical and physiological abnormalities in cardiovascular system, nervous system, reproductive organs, kidneys, and red blood cells (Elayat and Bakheetf, 2010). Lead poisoning has been also reported to induce oxidative stress and enhance the production of reactive oxygen species (ROS) as major mechanisms of its toxic action and thereby can cause cell structure damage, lipid peroxidation, and DNA and protein oxidation (Kasperczyk et al., 2012). The potential effect of LD in induction of oxidative stress suggests that some medicinal plants and herbs with antioxidant and possible chelating activities may be helpful in modulating the LD-induced toxicity (Patrick, 2006). Yucca schidigera is a plant belongs to the family “Agavaceae,” native to Mexico and the South-Western United States. Yucca is a widespread medicinal plant and is considered as natural (100%) additive (Balazi et al., 2013). It has many beneficial effects like growth promoter, hypocholesterolemic, hypoglycemic, anti-inflammatory, antioxidant, anticarcinogenic, and immunostimulatory (Alagawany et al., 2016a). Yucca is a commercial source of saponins, resveratrol, various enzymes, and antioxidants (Chrenková et al., 2012; Alagawany et al., 2016b; Farag et al., 2016). Steroid saponins of yucca products are approved by GRAS (Generally Recognized as Safe) given by FDA (Food and drug administration) that allows their human dietary use (Tenon et al., 2017). It is also used in the manufacture of cosmetics, beverages, and as dietary supplement for poultry and animal. In addition, yucca can conserve ammonia and decrease its content in the poultry houses and air and decrease blood urea concentration (Piacente et al., 2005) and has a great absorption capacity for harmful volatile compounds, such as ammonia and hydrogen sulfide (Vlckova et al., 2017). Therefore, the main objective of the present study was to investigate the toxic effects of LD on productive and reproductive performances, blood biochemical parameters, and the oxidative status of laying Japanese quails and to determine the egg quality criteria and residual concentrations of LD in the produced eggs. Additionally, this study would clarify the potential modulatory role of Yucca schidigera extract (YSE) against these effects. MATERIALS AND METHODS Birds and Diets The present study was carried out at Poultry Research Farm, Faculty of Agriculture, Zagazig University, Egypt. All experimental procedures were carried out according to the Local Experimental Animal Care Committee and approved by the ethics of the institutional committee of Zagazig University, Zagazig, Egypt. A total number of 360 mature Japanese quails (Coturnix coturnix japonica) at 2 mo of age with initial body weight 240.50 ± 2.00 g were used in a complete randomized design experiment with 6 treatments of 60 birds each. Each group was subdivided into 4 replicates with 15 birds. The experiment lasted for 8 wk. Birds were fed the basal diet with or without supplemental LD or YSE that formulated to meet laying quail requirements according to NRC (1994). The treatments were as follows: 1) control basal diet, 2) basal diet + 100 mg LD/kg diet, 3) basal diet + YSE (100 mg/kg diet), 4) basal diet + YSE (200 mg/kg diet), 5) basal diet + LD (100 mg/kg diet) + YSE (100 mg/kg diet), and 6) basal diet + LD (100 mg/kg diet) + YSE (200 mg/kg diet). The ingredients and chemical composition of the basal diet are presented in Table 1. Birds were housed in conventional type cage (50 × 30 × 50 cm3; 1,500 cm2 of floor space) with feed and fresh water provided ad libitum. Birds also were maintained on a 17 h light: 7 h dark cycle throughout the trial. All birds were kept under the same managerial, hygienic, and environmental conditions. Table 1. Composition and calculated analysis of the basal diets. Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 1Layer Vit. & Min. premix: Each 2.5 kg of vitamins and minerals premix (commercial source pfiezer Co.): consist of Vit. A 12 MIU, VIT E 15 KIU, Vit. D3 4 MIU, Vit. B1 1 g, Vit B2 8 g, Vit B6 2 g, Vit B12 10 mg, pantothenic acid 10.87 g, niacin30 g, folic acid 1 g, biotin 150 mg, copper 5 g, iron 15 g, manganese 70 g, iodine 0.5 g, selenium 0.15 g, zinc 60 g, and antioxidant 10 g. 2Calculated according to NRC (1994). View Large Table 1. Composition and calculated analysis of the basal diets. Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 Item Basal diet (%) Ingredients Corn 60.05 Soybean meal (44%) 25.00 Corn gluten meal (60%) 5.70 Di-calcium phosphate 3.30 Limestone 3.80 Vit. & Min. premix1 0.25 NaCl 0.20 Dl- Methionine 0.05 L-Lysine Hcl 0.15 Cotton seed oil 1.50 Total 100 Calculated analysis (%)2 Crude protein 20.03 ME (kcal/kg) 2922 Calcium 2.51 Non-phytate phosphorus 0.55 Lysine 1.08 Methionine + Cystine 0.77 1Layer Vit. & Min. premix: Each 2.5 kg of vitamins and minerals premix (commercial source pfiezer Co.): consist of Vit. A 12 MIU, VIT E 15 KIU, Vit. D3 4 MIU, Vit. B1 1 g, Vit B2 8 g, Vit B6 2 g, Vit B12 10 mg, pantothenic acid 10.87 g, niacin30 g, folic acid 1 g, biotin 150 mg, copper 5 g, iron 15 g, manganese 70 g, iodine 0.5 g, selenium 0.15 g, zinc 60 g, and antioxidant 10 g. 2Calculated according to NRC (1994). View Large Tested Chemicals Lead in the form of LD acetate (99.6% purity) was purchased from El-Gomhoria Chemical Co., Egypt. Yucca schidigera extract was purchased from Free Trade Egypt Company (El-Behera, Egypt). All other chemicals were purchased from Sigma (St. Louis, MO). All other reagents used were of analytical grade. Data Collection and Calculation Feed intake (FI) (g) was recorded daily, whereas feed conversion ratio (FCR) was calculated as the egg mass value divided by the amount of consumed feed. Egg numbers and weights were recorded daily to compute the egg mass. Fertility and Hatchability Percentages Twenty eggs from each replicate were collected and incubated at the end of each month. After hatching, chicks were counted and non-hatched eggs were examined to calculate the fertility and hatchability percentages. Fertility and hatchability percentages were calculated as follows: fertility percentage = (number of fertile eggs/total eggs set) × 100; hatchability percentage from fertile eggs = (number of hatched chicks/total number of fertile eggs) × 100; hatchability percentage from the total egg set = (number of hatched chicks/total eggs set) × 100. Egg Quality Criteria Egg quality criteria were measured monthly using 3 eggs from each replicate. Interior and exterior parameters of egg quality (percentages of yolk, albumen, shell, and egg shape index, yolk index Haugh units, and shell thickness) were determined according to Romanoff and Romanoff (1949). Blood Sampling and Laboratory Analyses Blood samples were randomly collected from 6 birds per treatment from the wing vein into sterilized tubes. The samples were allowed to coagulate for 30 min at room temperature and then centrifuged for 15 min at 3,500 rpm for serum separation; the serum samples were stored at –20°C until analysis. Total protein, albumin, globulin, total cholesterol, triglycerides, low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, alanine amino transferase (ALT), and aspartate aminotransferase (AST) were determined spectrophotometrically using commercial diagnostic kits provided from Biodiagnostic Co. (Giza, Egypt). Immunoglobulins (IgG and IgM) were determined according to Akiba et al. (1982). Antioxidant Assays Superoxide dismutase (SOD) and catalase (CAT) activities as well as reduced glutathione (GSH) and malondialdehyde (MDA) concentrations were determined in serum by spectrophotometric methods (Hitachi spectrophotometer, Japan) using commercial biodiagnostic kits provided from BioMérieux (Marcy l’etoile, France) according to the manufacturer's instructions. Determination of LD Residues Eggs were transferred to the laboratory in plastic bags and stored at cool and dark place. Then, each egg was washed by distilled water and soap and cut at the air cell end by dissecting scissors and pointed forceps. The content of each sample was placed in a clean glass jar. The samples then were dried at 75°C to get constant weight (Zaki, 1998). Then, the egg samples were digested by acid digestion method of Mahaffey et al. (1981),where 1 g of each sample was putted into a clean screw capped glass bottle and digested with a 4 mL of (nitric/perchloric acid, 1:1) as a digestion solution. Initial digestion was performed at room temperature for 24 h, and then heated for 2 h at110°C. Then the samples were left to cool and then followed by addition of deionized water and the solution was left for 1 h in water bath to expel nitrous gases. The digests were filtered and diluted to 25 mL deionized water (Julshman, 1983). The obtained solution was then analyzed using flame atomic absorption spectrophotometer. Statistical Analysis The data were statistically analyzed using general linear models procedure adapted by SPSS for user's guide with one-way ANOVA. The differences among treatments were determined using the post hoc Newman–Keuls test (P < 0.05). RESULTS Productive Performance of Japanese Quails Table 2 depicts the effects of LD along with the role of YSE on productive performance of quails during the experimental period. Supplementation of LD to quails diet showed a significant decrease in the FI, FCR, and egg production of birds compared with the control group. On the other hand, there were no significant changes in the egg weight or egg mass among the different experimental groups. Supplementation of YSE (100 or 200) to LD containing diet could significantly improve the quail performance parameters (FI, FCR, and egg production) and restored them to the control values. YSE200 groups showed the highest FI level and egg production percentage compared to all other groups. Table 2. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on productive parameters of Japanese quail. Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Table 2. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on productive parameters of Japanese quail. Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Productive parameters Items Egg weight (g) Egg production (%) Egg mass (g) Feed intake (g/d) Feed conversion (g feed/g egg) Control 13.78 ± 0.79 83.52a,b ± 8.49 692.09 ± 102.17 31.54a,b ± 1.30 2.98b ± 0.31 Lead (LD) 13.66 ± 0.85 64.52c ± 0.67 530.66 ± 43.34 26.31b ± 0.52 2.66c ± 0.11 YSE 100 13.45 ± 0.63 73.01b,c ± 2.47 715.20 ± 34.38 32.61a,b ± 0.36 3.20a ± 0.30 YSE 200 14.31 ± 0.39 88.61a ± 0.69 618.52 ± 21.67 33.76a,b ± 2.38 3.40a ± 0.39 LD+YSE 100 14.44 ± 0.98 70.23b,c ± 3.91 640.28 ± 57.42 30.73a,b ± 1.17 2.79b,c ± 0.25 LD+YSE 200 16.90 ± 0.66 72.09b,c ± 0.82 713.14 ± 53.39 31.18a,b ± 1.34 2.74b,c ± 0.15 P-value1 0.060 0.010 0.200 0.031 0.057 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Reproductive Performance of Japanese Quails Results in Table 3 indicate that supplementation of diets with LD resulted in a significant decrease in the fertility percentage compared to the control group. On the other hand, YSE at both levels (100 or 200) separately or in combination with LD showed fertility percentages comparable to that of control. Table 3. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on reproductive parameters of Japanese quail. Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Table 3. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on reproductive parameters of Japanese quail. Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Reproductive parameters Items Fertility (%) Hatchability (%) (from the total set of eggs) Hatchability (%) (from the fertile eggs) Control 92.53a ± 0.75 74.58a ± 5.15 85.80a,b ± 3.93 Lead (LD) 78.85b ± 4.85 39.58b ± 10.48 47.36c ± 13.92 YSE 100 90.88a ± 3.83 71.77a ± 4.39 84.84a,b ± 4.86 YSE 200 91.31a ± 1.80 76.82a ± 3.90 91.47a ± 5.89 LD+YSE 100 83.39a,b ± 2.66 46.41b ± 7.81 62.84a,b,c ± 5.74 LD+YSE 200 84.83a,b ± 2.45 57.29a,b ± 5.13 55.56b,c ± 10.38 P-value1 0.030 0.003 0.005 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Results of hatchability (%) from the total set of eggs revealed no significant changes between control, YSE 100, or YSE200 groups. Whereas, this percentage was significantly decreased in the LD group compared to the control group. On the other hand, supplementation of YSE (100 mg/kg diet) to LD containing diet could not improve the reduced hatchability of quails, whereas addition of YSE (200 mg) to LD diet could restore the hatchability percentage of birds to control values. Hatchability (%) from the fertile eggs was found to be significantly decreased in the LD group compared to control, whereas the YSE100 group showed the highest percentage among all other experimental groups. On the other hand, supplementation of YSE (100 or 200 mg/kg diet) to LD diet could restore the hatchability (%) from the fertile eggs to that of control. Egg Quality Criteria Supplementation of quail's diet by LD, YSE (100 or 200) separately or in combination did not alter the egg composition (shell, yolk, and albumen), exterior or interior egg quality parameters than the control group as shown in Table 4. Table 4. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on egg quality criteria in Japanese quail. Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 1Overall treatment P-value. View Large Table 4. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on egg quality criteria in Japanese quail. Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 Egg quality criteria Items Shell % Shell thickness Egg shape index Yolk % Yolk index Albumen % Haugh unit score Control 18.32 ± 1.52 0.240 ± 0.01 83.83 ± 1.64 32.60 ± 2.23 48.83 ± 2.86 49.06 ± 2.66 92.36 ± 2.10 Lead (LD) 15.58 ± 1.29 0.246 ± 0.01 82.05 ± 3.07 32.88 ± 0.78 49.54 ± 2.73 51.53 ± 1.68 95.04 ± 1.97 YSE 100 18.29 ± 1.47 0.253 ± 0.01 81.35 ± 3.09 26.06 ± 1.72 46.80 ± 1.62 55.63 ± 3.01 95.45 ± 3.14 YSE 200 18.10 ± 0.48 0.246 ± 0.01 81.18 ± 0.38 36.70 ± 2.07 46.91 ± 1.24 45.19 ± 2.35 96.34 ± 0.46 LD+YSE 100 21.40 ± 1.60 0.246 ± 0.01 79.74 ± 2.08 33.56 ± 4.34 53.57 ± 3.93 45.03 ± 4.70 98.25 ± 0.88 LD+YSE 200 16.13 ± 0.98 0.253 ± 0.01 80.80 ± 3.35 34.65 ± 2.71 45.60 ± 0.95 49.21 ± 3.01 95.59 ± 0.30 P-value1 0.086 0.952 0.902 0.154 0.310 0.213 0.392 1Overall treatment P-value. View Large Liver Function Markers Liver function markers are given in Table 5. Total protein, albumin, and globulin levels were found to be decreased in serum of LD-exposed group only compared to control. The higher levels of total protein and albumin were obtained for birds of YSE200 group followed by the YSE100 group compared to the control group. Co-exposure to YSE 100 or 200 with LD was found to significantly increase the levels of total protein, albumin, and globulin. Table 5. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on liver functions in serum of Japanese quail. Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1AST: aspartate aminotransferase, ALT: alanine aminotransferase 2Overall treatment P-value. View Large Table 5. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on liver functions in serum of Japanese quail. Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Liver functions1 Items Total protein (g/dL) Albumin (g/dL) Globulin (g/dL) AST (IU/mL) ALT (IU/mL) Control 4.75b,c ± 0.05 1.81c ± 0.01 2.94b ± 0.05 56.31d ± 1.26 26.59d ± 0.40 Lead (LD) 3.48d ± 0.20 1.47e ± 0.01 2.01c ± 0.20 115.55a ± 1.47 39.44a ± 0.37 YSE 100 5.08b ± 0.05 1.96b ± 0.05 3.12b ± 0.01 46.22e ± 1.48 20.05e ± 0.03 YSE 200 5.87a ± 0.32 2.14a ± 0.04 3.73a ± 0.27 40.10e ± 2.02 16.64f ± 0.76 LD+YSE 100 4.28c ± 0.02 1.63d ± 0.01 2.65b ± 0.02 105.50b ± 2.59 33.75b ± 1.01 LD+YSE 200 4.43c ± 0.04 1.70d ± 0.02 2.73b ± 0.07 69.10c ± 4.61 29.86c ± 0.26 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1AST: aspartate aminotransferase, ALT: alanine aminotransferase 2Overall treatment P-value. View Large In response to LD exposure, the values of AST and ALT were increased significantly compared to the control group. On the other hand, lower levels of AST and ALT were observed for YSE100 and YSE200. AST and ALT levels in LD plus YSE100 or LD plus YSE200 groups were significantly decreased than LD alone group and a better reduction was observed in LD plus YSE 200 group; however, both the levels did not return the AST and ALT levels to the control values. Effects on Lipid Profile Exposure of quails to LD in their diet significantly increased the triglycerides, cholesterol, and LDL whereas significantly decreased HDL values compared to control and other treatment groups. On the other hand, contradicting results were obtained for the YSE200 group. Triglycerides, cholesterol, and LDL contents in LD plus YSE100 or LD plus YSE200 groups were significantly decreased than LD alone group and a better effect was observed in LD plus YSE 200 group where it could restore the triglyceride level to normal and decreased the cholesterol level than the LD+YSE100 group however still higher than control. Co-exposure to YSE 100 or 200 with LD was found to significantly increase the levels of HDL than control and YSE200 was more effective than YSE100. On the other hand, YSE100 alone did not alter the HDL value compared to control (Table 6). Table 6. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on lipid profile in serum of Japanese quail. Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Table 6. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on lipid profile in serum of Japanese quail. Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Lipid profile (mg/dL) Items Triglyceride(mg/dL) Cholesterol(mg/dL) LDL(mg/dL) HDL(mg/dL) Control 61.65c ± 0.89 118.25d ± 4.87 62.42c ± 1.45 32.14b ± 0.04 Lead (LD) 86.01a ± 3.86 188.50a ± 7.21 148.94a ± 9.08 21.15e ± 0.56 YSE 100 54.75d ± 0.85 101.07e ± 0.61 54.12c ± 0.15 33.37b ± 0.07 YSE 200 49.45e ± 0.49 76.25f ± 2.74 32.90d ± 2.67 40.52a ± 0.40 LD+YSE 100 68.54b ± 0.54 169.27b ± 3.96 111.58b ± 1.73 26.88d ± 0.36 LD+YSE 200 65.55b,c ± 0.25 151.72c ± 1.37 98.61b ± 4.24 30.46c ± 0.68 P-value1 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1Overall treatment P-value. View Large Effects on Antioxidant Status Table 7 shows the effects of LD and YSE on antioxidant system of quails. The LD treatment significantly decreased both the SOD and CAT enzyme activities in the serum of treated quails compared to the control group. YSE100 did not significantly change the antioxidant activities than those of control, whereas YSE200 significantly enhanced the SOD and CAT activities to be better than the control itself. Table 7. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on antioxidant and immunity in serum of Japanese quail. Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1SOD: superoxide dismutase, CAT: catalase, GSH: reduced glutathione, MDA: malondialdehyde, IgG: immunoglobulin G, IgM: immunoglobulin M. 2Overall treatment P-value. View Large Table 7. Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca Schidigera extract (YSE, 100 or 200 mg/kg diet) on antioxidant and immunity in serum of Japanese quail. Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Antioxidant and immunity1 Items SOD(U/mL) CAT(U/mL) GSH(ng/mL) MDA(μmol/mL) IgG(mg/dL) IgM(mg/dL) Control 0.215b ± 0.01 0.221b ± 0.01 0.230b ± 0.01 0.167d ± 0.01 576b,c ± 7.50 48.65c ± 0.43 Lead (LD) 0.162c ± 0.01 0.116d ± 0.01 0.209b ± 0.01 0.355a ± 0.02 406e ± 4.33 30.74f ± 0.43 YSE 100 0.222b ± 0.01 0.224b ± 0.01 0.247b ± 0.01 0.141d,e ± 0.01 609b ± 4.04 51.20b ± 0.52 YSE 200 0.276a ± 0.01 0.252a ± 0.01 0.291a ± 0.01 0.111e ± 0.01 667a ± 19.34 58.45a ± 0.25 LD+YSE 100 0.182b,c ± 0.01 0.191c ± 0.01 0.212b ± 0.01 0.303b ± 0.01 490d ± 5.19 34.34e ± 0.72 LD+YSE 200 0.210b,c ± 0.01 0.195c ± 0.01 0.225b ± 0.01 0.243c ± 0.01 554c ± 23.62 43.90d ± 0.40 P-value2 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Different superscripts within 1 column are significantly different (P < 0.05). 1SOD: superoxide dismutase, CAT: catalase, GSH: reduced glutathione, MDA: malondialdehyde, IgG: immunoglobulin G, IgM: immunoglobulin M. 2Overall treatment P-value. View Large GSH content was not significantly changed in all groups compared to control except YSE200 that was higher than control. Co-exposure to YSE100 or YSE200 with LD was found to significantly increase the CAT activity than LD alone to be comparable with control and numerically increase the SOD activity however still under control values. The lipid peroxidation, as evidenced by the formation of MDA, was significantly increased in LD-treated group compared to the control group. MDA contents in LD plus YSE100 or YSE200 groups were significantly decreased than LD alone group, and a better effect was observed in LD plus YSE 200 group. Meanwhile, MDA level in the YSE200 group was significantly lower than control however YES100 was comparable to both control and YSE200 groups. Effects on Immunoglobulins Results in Table 7 showed that the highest values of immunoglobulins (IgG and IgM) were obtained by birds fed diet supplemented with 200 mg YSE/kg followed by those received 100 mg YSE/kg diet, whereas the lowest values of IgG and IgM were obtained in response to LD exposure. On the other hand, LD plus YSE100 or LD plusYSE200 groups exhibited significant improvements in the level of immunoglobulins compared to the LD group and YSE200 showed better effects. LD Residues Analysis of eggs for detection of LD residues at the end of the experiment is represented in Figure 1, which revealed that the highest concentrations of accumulated LD were detected in eggs of LD-exposed group (0.932 ± 0.04). On the other hand, there were no significant changes in the residue level of LD among control, YSE100, and YSE200 groups (0.13 ± 0.04, 0.09 ± 0.03, 0.04 ± 0.02), respectively. Co-exposure to YSE100 or YSE200 with LD was found to significantly decrease the LD residues in egg 0.797 ± 0.04, 0.700 ± 0.02 respectively than the LD group. The YSE200 was better than YSE100 however still higher than control level. Figure 1. View largeDownload slide Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca schidigera extract (YSE, 100 or 200 mg/kg diet) on accumulation of lead residues (μg/g wet weight) in eggs of treated Japanese quails compared to the control group. Figure 1. View largeDownload slide Effects of separate and concurrent exposure to lead (LD, 100 mg/kg diet) and Yucca schidigera extract (YSE, 100 or 200 mg/kg diet) on accumulation of lead residues (μg/g wet weight) in eggs of treated Japanese quails compared to the control group. DISCUSSION The aim of the current poultry production is to achieve the highest growth rates, FCRs, and production percentages to cover the widely increasing demand of animal proteins particularly in developing countries. The intensive breeding and farming increased the sensitivity of birds to external stressors from their surrounding environment resulting in acute stress responses, reduced productive and reproductive performances, health problems, increased susceptibility to infectious diseases, and low-quality poultry products (Shahid ul Islam et al., 2014). Therefore, it is of importance to explore the stress responses to environmental contaminants on the productive and reproductive performance of birds and try to find effective methods to decrease these responses. Japanese quail could be used as a model to study the effects of environmental contamination as they are similar to wild birds, ready available, and information concerning their normal physiology is solid (Franson and Pain, 2011). The present study indicated that LD supplementation to diets of quails showed a significant decrease in FI, FCR, and egg production; however, it did not influence the other performance parameters including egg weight and egg mass compared to control. Exposure of quails to LD in their diet decreased the hatchability of total eggs set, hatchability of fertile eggs set, and the percentage of fertile eggs compared to control. On the other hand, LD did not alter the egg quality criteria of exposed quails. High dietary LD has been reported to inhibit the growth performance parameters in quails (Humayun et al., 2015; Farag et al., 2018). Similarly, LD decreased the body weight and egg production in adult quail hens (Stone and Soares, 1976). On the same context, Butkauskas and Sruoga (2004) stated that LD could increase the number of unfertile eggs of quail up to 30% relative to control. Salisbury, et al. (1958) reported a cessation of egg production in adult chicken hens intoxicated with LD. The inhibitory effect of dietary LD exposure on reproductive performance of female quails was reported by Edens and Garlich (1983), who demonstrated that dietary LD significantly depressed the total plasma calcium reflecting the inability of intoxicated quails to mobilize adequate amount of plasma calcium. Moreover, LD exposure decreased the weight and function of ovary in exposed quails. Therefore, it was suggested that ovary could be involved in the regulation of egg production than calcium. Additionally, LD has been reported to induce neurotoxicity in quails inducing impairment of the neurochemical control on reproductive hormones regulation (Edens, 1985). In our study, supplementation of YSE to bird's diet concurrently with LD resulted in significant improvements in the altered productive performance parameters of quails including FI, FCR, egg production, fertility, and hatchability to levels that are comparable to those of control. Dietary supplementation of Y. schidigera has been reported to induce significant impacts on layer performance by increasing the egg production and final body weight (Gurbuz et al., 2016). Similarly, Cheek (1998) reported that feeding poultry on yucca could improve their growth and productivity. These positive effects of yucca could be returned to the presence of steroidal saponins as a main component and other surface active components that could promote the utilization and absorption of nutrients from gastrointestinal tract by improving its epithelial lining of the cell membrane and decreasing the surface tension (Goetsch and Owens, 1985). Fertility and hatchability are important parameters in studying the reproductive performance; they are affected by environment, insufficient nutrients, and genetic involvement (Ayasan, 2013). Therefore, to obtain the highest fertility and hatchability percentages of quails, optimum conditions should be provided before and after hatching (Ggüçlü, 2011). In the present study, yucca at high level (200 mg/kg body weight) was found to improve fertility and hatchability percentages in the presence of LD. This improvement could be explained by the suggestions of El Anwer et al. (2009), who returned the increased hatchability and fertility to 2 main assumptions; the first assumption is the ability of yucca to reduce ammonia concentration in the surrounding atmosphere of eggs that could help in adjusting the egg pH. The reducing effect of yucca on blood urea has been previously reported in broilers (Balog et al., 1994) that could be mainly due to saponin, stilbenes, and carbohydrates in yucca. These components have been reported to have modulatory effects on renal functions and could increase the clearance of urea and lower blood concentrations of ammonia and urea (Duffy et al., 2001). YES has could inhibit urease enzyme in vivo and in vitro (Asplund 1991; Balog et al., 1994). Biochemical findings of the present study revealed that total protein level was found to be decreased in serum of LD-exposed group compared to control. These results are in accordance with those of Humayun et al. (2015) who studied hematobiochemical changes induced by LD poisoning in quails. The decreased protein level could be returned to increasing protein utilization to obtain the energy required by quails exposed to toxic stresses. Furthermore, Hamidipoor et al. (2016a) related the decrease in total protein of quails exposed to LD acetate and deltamethrin to the reduced utilization of dietary protein, malnutrition, or decreased protein synthesis in liver. Globulin and albumin are the major components of total protein and the changes in their levels can be used to monitor the health status of liver, kidney, and the immune system (Patra et al., 2011). When protein synthesis in the liver is reduced, it directly affects the globulin level. In agreement with this, the results of the present study showed that LD significantly decreased the albumin and globulin level than control a long with decreasing total protein level in LD-exposed quails. In the present study, the extent of LD-induced cellular injury was assessed by monitoring the serum level of ALT and AST. These enzymes were released into serum or plasma in case of liver damage, necrosis, or inflammation. In addition, ALT enzyme has been reported to increase in muscular dystrophy heart failure, anemia, and obstruction of bile duct (Philip et al., 1995). Herein, LD significantly elevated ALT and AST activities in the serum of LD-treated quails. These results agreed with previous works reported an elevation in ALT and AST activities in serum after exposure to LD in quails (Humayun et al., 2015; Hamidipoor et al., 2016a). Lead significantly reduced the total protein, albumin, and globulin levels and significantly increased the AST and ALT activities in quails (Hamidipoor et al., 2016b). This elevation may be attributed to increasing the permeability of cellular membrane, fluidity of the microsomal membrane, or the damage of hypatocytes cell membranes (Abdou et al., 2007). Production of free radicals increased cellular basal metabolic rate, irritability, and destructive alteration of liver under the influence of LD (Ibrahim et al., 2012). Considering the effect of LD on lipid profile, the present study showed that exposure of quails to LD in their diet significantly increased triglycerides, cholesterol, and LDL while significantly decreased HDL values compared to control and other treatment groups. Contradicting results were obtained by Hamidipoor et al. (2016b), where LD exposure had no significant changes in cholesterol, whereas it significantly reduced the concentration of triglycerides. The disturbances in lipid profile could be possibly returned to enhanced biosynthesis of cholesterol and its accumulation in liver and/or impairment of biliary functions (Ashour et al., 2014) and this came on line with the obtained results of liver functions. From the present study, it was obvious that dietary supplementation of YSE improved the blood biochemical parameters (total protein, albumin, globulin) and the activities of liver function enzymes (ALT and AST) and showed positive effects on the lipid profile of quails in the co-exposed groups (LD+YSE) especially at high level. This indicates the potential modulatory role of YSE on liver function mainly due to yucca saponins and phenolics that showed hypocholesterolemic, antioxidant, hypoglycemic, anti-inflammatory, immunostimulatory, antiviral, anticarcinogenic, and anti-mutagenic activities (Gupta, 2014; Alagawany et al., 2016a). It is well known that powder and extracts of plants rich in saponins can alter the lipid metabolism of birds and different animal as reported by Rao and Kendall (1986). Saponins reduced the serum cholesterol level in laying hens (Aslan et al., 2004) and rabbits (Morehouse et al., 1999). Saponins can form complexes with cholesterol leading to its precipitation and can reduce hypercholesterolemia by altering the stability and size of cholesterol micelle and decreasing its penetration into mucous membrane cells (Milgate and Roberts, 1995). Additionally, saponins can reduce the absorption of cholesterol and facilitate the discharge of neutral sterols including plant sterols, cholesterol, coprostanol, and bile acids in fecal matter (Jenkins and Atwal, 1994). Saponins can also destruct the cell membrane and cause loss of cholesterol (Morehouse, Bangerter, DeNinno, Inskeep, McCarthy, Pettini, Savoy, Sugarman, Wilkins, Wilson, Woody, Zaccaro and Chandler, 1999). Moreover, the presence of saponins can enhance bile acid absorption and form high molecular weight micelles (cellulose saponin–bile acid complexes) thus prevent bile acids reabsorption and lead to the increase in the cholesterol conversion into bile acids in the hepatic tissue (Sidhu and Oakenfull, 1986). The decrease in cholesterol absorption decreased its hepatic content and this enhanced the activity of HMG-CoA reductase and increased the LDL receptors in the liver (Harwood et al., 1993). Exposure to LD can impair the antioxidant defense system and increase the cell vulnerability to the free radicles attack leading to oxidative damage (Liu et al., 2010). This could explain the observed decrease in SOD and CAT activities of LD-exposed quails in the present study. However, LD did not significantly alter the GSH content in serum of quails. The altered antioxidant status after LD exposure has been reported in some previous works on animals and workers (Baranowska-Bosiacka et al., 2012; Dai et al., 2013). Oxidative stress of LD exposure was also evidenced by increased MDA (lipid peroxidation marker) compared to control. The elevated MDA indicated the inability of antioxidant defense system to counteract the ROS-induced damage. These results agreed with some earlier reports in which LD induced oxidative damage in birds and significantly enhanced lipid peroxidation in liver of chick embryos (Somashekaraiah et al., 1992), in brain, and liver of mallards exposed to LD in the diet and in geese and mallards exposed to sediments contaminated by LD (Mateo et al., 2003). MDA levels increased in liver following LD exposure (Sandhir and Gill, 1995). These results could be returned to the destructive effects of LD on cell membrane components including proteins and lipids resulting in altered membrane function and structure (Donaldson and Knowles, 1993). In the present study, supplementation of YSE to bird's diet contained LD significantly improved the antioxidant enzymes activities, whereas it significantly decreased the serum level of MDA in birds compared to the LD group. These results indicate that YSE could counteract the undesirable impact of oxidation reaction and could decrease the lipid peroxidation in birds exposed to environmental contamination. Gümüş and İmik (2016) demonstrated that yucca can act as a good antioxidant for poultry and its supplementation to broiler diets increased the total antioxidant capacity by improving the antioxidants activities. These positive impacts could be attributed to the phytochemicals of yucca such as polyphenolic compounds (resveratrol (RES) and yuccaols A, B, C, D, and E) and steroidal saponins (Alagawany et al., 2015). RES exhibited a powerful scavenging activity against free radicals generated by heavy metals as hydroxyl and superoxide radicals and could make activation of the major transcription factors that regulate the response to antioxidants (erythroid-derived nuclear factor) (Rubiolo and Vega, 2008) and could improve the activities of CAT, GSH-Px, SOD, glutathione S-transferase (GST), and nicotinamide adenine dinucleotide phosphate (NADPH) quinoneoxidoreductase (Young et al., 2000). It could also maintain the reduced state of glutathione by inhibiting the formation of glutathione disulfide; thereby it can protect cells from the attack of free radicales (FR), prevent the oxidative damage of macromolecules, and inhibit apolipoprotein B protein peroxidation (Yan et al., 2012). Similarly, RES as a dietary supplement has been reported to diminish oxidative stress and improve the antioxidant status in birds (Liu et al., 2014). Moreover, RES and other phenolic compounds from yucca could inhibit the generation of FR and reduced lipid peroxidation (LPO) in blood platelets (Olas et al., 2003). The impact of environmental pollutants on the bird's immune system is of great importance as birds are highly required to compensate the shortage in animal protein sources and the presence of these pollutants could increase the susceptibility of birds to parasites and infectious diseases (Galloway and Depledge, 2001). The present study showed that LD significantly decreased the levels of immunoglobulin (IgG and IgM) in exposed birds. These findings came on line with the observed decrease in the levels of plasma globulin of the same group that indicated a reduced immunity as the liver cannot synthesis enough globulin for immunologic actions. On the same context, exposure to LD significantly reduced IgG, IgA, and IgM in serum accompanied with increased MDA as a marker of oxidative damage in some organs of rats (Gurer and Ercal, 2000). The significant decrease in IgG and IgM can indicate the deleterious effect of LD on the functions of B cells that could be resulted from oxidative damage (decreased antioxidant activities and increased MDA) of LD on these cells and this is totally agreed with Nuran Ercal et al. (2001). Lead has been reported to decrease the activation of lymphocytes and inhibit their proliferation, decrease the migration and motility of macrophage (Kiremidjian-Schumacher et al., 1981), and reduce the cytotoxicity and natural killer (Talcott et al., 1985). From the present study, it was obvious that dietary supplementation of YSE improved the immune response, which was evidenced by the significant improvements in immunoglobulins. This could be probably due to the modulating effect of yucca in liver functions including the level of globulin and the antioxidant power of YSE observed in the present study. These effects are consistent with some previous reports on the positive effects of YSE on immune functions, where yucca saponins could enhance cellular and antibody humoral immune responses, stimulate the cytokines secretions, and activate the innate immunity (Palatnik de Sousa et al., 2004). Saponins in chicken diets increased the level of IgA (Zhai et al., 2011). Supplementation of yucca powder to broiler chicks stimulated the immune responses (cellular and humoral) (Su et al., 2016). Similarly, yucca powder improved IgG content in layer chicken (Alagawany et al., 2016a). Fresh egg and egg products are among the most important nutritional sources in the daily diet so investigating the residual level of heavy metals is important as they could induce negative impacts on bird performance, productivity, and the consumers as well (Li et al., 2005). The present study revealed that eggs from LD-exposed quails showed the highest residual level than other experimental groups. Birds can reduce the deposition of metals into their eggs through decreasing the deposition of minerals. This type of protection could be sufficient to prevent deposition of some metals like Cr and Mn but insufficient for LD (Hui, 2002). This is in consistence with our results and may explain the obtained decreased hatchability percentage that could be returned to the ability of LD to induce some embryo toxic impacts. On the other hand, YSE supplementation significantly reduced the LD residues suggesting that in addition to its antioxidant activity, it could also act as chelator and this makes YSE a powerful candidate for treating LD toxicity. CONCLUSIONS From the obtained results, we concluded that exposure of quails to LD in their diets resulted in apparent adverse effects on the performance parameters (productive and reproductive) and altered the biochemical parameters of liver function and lipid profile in addition to its inhibitory effect on immune response of birds. These adverse effects were accompanied with oxidative damage evidenced by decreased antioxidant enzymes and increased lipid peroxidation. On the other hand, using of YSE as a natural feed additive in quail diets could alleviate the deleterious effects of LD and enhanced the immune function via improving levels of immunoglobulin. However, YSE at high level (200 mg/kg diet) was more effective than low one (100 mg/kg diet). 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