Effects of maternal dietary canthaxanthin and 25-hydroxycholecalciferol supplementation on antioxidant status and calcium-phosphate metabolism of progeny ducks

Effects of maternal dietary canthaxanthin and 25-hydroxycholecalciferol supplementation on... Abstract Three experiments were conducted to investigate the effects of maternal dietary canthaxanthin (CX) and 25-hydroxycholecalciferol (25-OH-D3) supplementation on antioxidant status and calcium-phosphate metabolism of progeny ducks. Cherry Valley duck breeders (38 wk old) were fed either a control diet or the same diet plus CX (6 mg/kg) and 25-OH-D3 (0.069 mg/kg) for 32 weeks. Experiments 1, 2, and 3 were conducted with progeny ducks hatched from eggs laid by duck breeder hens at 54, 62, and 70 wk of age, respectively. Progeny ducks from both maternal treatments were fed with the same NRC (1994) vitamin regimen starter (1 to 14 d) and finisher (15 to 35 d) diets in experiments 1 and 2, and fed with the same high vitamin regimen starter (1 to 14 d) and finisher (15 to 35 d) diets in experiments 3. High vitamin regimen had higher levels of all vitamins, except biotin, than the NRC (1994) vitamin regimen. In experiment 1, maternal CX and 25-OH-D3 increased (P < 0.05) shank pigmentation and tibiotarsus ash and tended to decrease (P < 0.1) liver total superoxide dismutase activity (T-SOD) of one-day-old progeny ducks; and increased (P < 0.05) shank pigmentation, decreased (P = 0.05) liver protein carbonyl, and tended to increase (P < 0.1) liver total antioxidant capacity (T-AOC) of 14-day-old progeny ducks. In experiment 2, maternal CX and 25-OH-D3 increased (P < 0.05) shank pigmentation and liver T-AOC and decreased (P < 0.05) liver protein carbonyl of one-day-old progeny ducks, but increased (P < 0.05) the serum phosphate level of 14-day-old progeny ducks. In experiment 3, maternal CX and 25-OH-D3 increased (P < 0.05) shank pigmentation of one-, 14-, and 35-day-old progeny ducks and tended to increase (P < 0.1) liver T-SOD and tibiotarsus ash, but decrease (P < 0.1) liver malondialdehyde of one-day-old progeny ducks. It can be concluded that progeny dietary high vitamin regimen could partially prevent maternal CX-derived progeny shank pigmentation from bleaching. Maternal CX- and 25-OH-D3-derived effects are influenced by the hen's age and progeny's dietary vitamin regimen. INTRODUCTION The nutritional and physiological relationship between mother and progeny has been widely studied in oviparous, ovoviviparous, and viviparous species (Kidd, 2003; Uller and Olsson, 2006; Victora et al., 2008). In poultry, the nutritional status of breeder hens can affect the nutrient profile of breeder eggs and subsequently influence embryonic development and progeny performance (Wilson, 1997; Kidd, 2003). The possibility of using maternal dietary strategies to overcome problems (e.g., oxidant stress, skeletal disorder) that cause significant economic loss pre- and post hatch has been the subject of poultry science research for many years (Surai, 2000; Driver et al., 2006b). The presence of canthaxanthin (CX, a powerful carotenoid antioxidant) in chicken eggs was documented as early as the 1950s (Paust, 1991). Later, scientists realized that the dietary CX level of breeder hens is positively correlated to CX concentration and antioxidant status of egg yolk, embryo, and post-hatched chicks (Grashorn and Steinberg, 2002; Surai et al., 2003; Rosa et al., 2012; Surai, 2012; Bonilla et al., 2017). Recent studies show that the supplementation of 6 mg/kg CX in maternal diet (sufficient in antioxidants) can benefit the progeny broilers (increases antioxidant status and decreases mortality) in the first 21 d (Zhang et al., 2011; Rosa et al., 2017). Also interesting is the use of maternal dietary 25-hydroxycholecalciferol (25-OH-D3, biologically active metabolite of vitamin D3) to improve skeletal heath of progeny chicks. In the study of Zang et al. (2011), egg yolk 25-OH-D3 concentration was increased by 170% (12.82 vs. 34.63 μg/kg) when 0.035 mg/kg 25-OH-D3 was supplemented to a NRC (1994) based laying hen diet. In the broiler breeder experiment conducted by Atencio et al. (2005c), the relative biological value of 25-OH-D3 in comparison to vitamin D3, calculated using slope ratio, was 111% for progeny body ash content. It would be safe to conclude that, for poultry breeders, 25-OH-D3 is a good source of vitamin D3. We have previously demonstrated the application of the combination of CX and 25-OH-D3 in duck breeder diet (Ren et al., 2016a,b,c; Ren et al., 2017). Basically, the observations in these studies were in good agreement with either CX or 25-OH-D3 experiments mentioned in the last paragraph. However, a few questions still remain to be answered: 1) The effects of maternal CX and 25-OH-D3 may be different in duck breeders at different ages. 2) The effects of maternal CX and 25-OH-D3 may be different in progeny ducks under different vitamin regimens. Hence, 3 experiments were conducted here to investigate these issues using progeny ducks from duck breeders at the ages of 54, 62, and 70 wk, respectively. MATERIALS AND METHODS All animal procedures used in this study were approved by the Animal Nutrition Institute Animal Care and Use Committee at the Sichuan Agricultural University. The duck breeder trial was conducted at Jinyan breeding farm (6,000 egg-laying duck breeders in dimensions) located at Mianzhu City (Sichuan Province, China). Cherry Valley duck breeders (38 wk old) were fed either a control diet or the same diet plus CX (6 mg/kg) and 25-OH-D3 (0.069 mg/kg) for 32 wk (from June 2012 to January 2013). Each treatment had 390 females and 78 males (the hen: drake ratio was 5:1). Duck breeders were raised on semi-open sheds (straw litter floors, with no heating) with an outside area including a swimming pool, a drinker, and a feeder. Feed and water were provided ad libitum, and a 17L:7D photoperiod was used during the trial. According to lab analysis conducted by DSM Nutritional Products Ltd. (Wurmisweg, Switzerland), no CX or 25-OH-D3 were detected in the control diet, while 5.67 mg/kg CX and 0.070 mg/kg 25-OH-D3 were detected in the diet supplemented with CX and 25-OH-D3. Composition and nutrient levels of the control diet are the same as the regular vitamin regimen duck breeder diet listed in Ren et al. (2016a). Experiments 1, 2, and 3 were conducted with progeny ducks hatched from eggs laid by duck breeder hens at 54 (October 2012), 62 (December 2012), and 70 (January 2013) wk of age, respectively. Experiments 1, 2, and 3 Progeny trials were performed in an environmentally controlled room at the Poultry Nutrition Research Laboratory (Sichuan Agricultural University, Yaan, Sichuan, China). Feed and water were provided ad libitum, and a 24L:0D photoperiod was used during the trials. In experiment 1, progeny ducks from each maternal treatment were allotted to 8 cages (15 birds in each cage). Progeny ducks from both maternal treatments received the same starter (from 1 to 14 d) and grower (from 15 to 35 d) diets. Composition and nutrient levels of the starter diet are the same as the NRC (1994) vitamin regimen starter diet listed in Ren et al. (2017). Composition and nutrient levels of the grower diet, which is also under the NRC (1994) vitamin regimen, are listed in Table 1. Experiment 2 was conducted in the same manner as experiment 1 (the only difference between experiment 1 and 2 is that progeny ducks were from duck breeders at a different age). Experiment 3 was conducted in the same manner as experiments 1 and 2, except both starter and grower diets were under a high vitamin regimen, which had higher levels of all vitamins, except biotin, than the NRC (1994) vitamin regimen (see footnote of Table 1). Table 1. Composition and nutrient levels of the basal diet (as-fed basis). Item (%, unless noted)  Progeny diet (15 to 35 d)  Corn  46.5  Wheat bran  15  Rice bran  8  Soybean meal, 43%  8  Rapeseed meal  8  Cottonseed meal  6  Rapeseed oil  3.88  Calcium carbonate  0.96  Dicalcium phosphate, 2H2O  1.175  L-Lysine-HCl  0.27  D, L-Methionine  0.126  Threonine, 98.5%  0.044  Tryptophan, 98.5%  0.032  Sodium chloride  0.4  Choline chloride, 50%  0.1  Bentonite  0.913  Mineral premix1  0.5  Vitamin premix2  0.1  Analyzed nutrient content    ME (Kcal/kg, calculated)  2814  CP (analyzed)  18.12  Calcium (analyzed)  0.84  Total phosphorus (analyzed)  0.74  Nonphytate phosphorus (calculated)  0.378  Item (%, unless noted)  Progeny diet (15 to 35 d)  Corn  46.5  Wheat bran  15  Rice bran  8  Soybean meal, 43%  8  Rapeseed meal  8  Cottonseed meal  6  Rapeseed oil  3.88  Calcium carbonate  0.96  Dicalcium phosphate, 2H2O  1.175  L-Lysine-HCl  0.27  D, L-Methionine  0.126  Threonine, 98.5%  0.044  Tryptophan, 98.5%  0.032  Sodium chloride  0.4  Choline chloride, 50%  0.1  Bentonite  0.913  Mineral premix1  0.5  Vitamin premix2  0.1  Analyzed nutrient content    ME (Kcal/kg, calculated)  2814  CP (analyzed)  18.12  Calcium (analyzed)  0.84  Total phosphorus (analyzed)  0.74  Nonphytate phosphorus (calculated)  0.378  1Supplied per kilogram of diet: copper, 8 mg; iron, 80 mg; zinc, 90 mg; manganese, 70 mg; selenium, 0.3 mg; iodine, 0.4 mg. 2Supplied per kilogram of diet. NRC vitamin regimen: vitamin A, 2500 IU; vitamin D3, 400 IU; vitamin K3, 0.5 mg; vitamin E, 10 mg; vitamin B1, 1.8 mg; vitamin B2, 4 mg; vitamin B6, 2.5 mg; vitamin B12, 0.01 mg; nicotine acid, 55 mg; pantothenic acid, 11 mg; biotin, 0.15 mg; folic acid, 0.55 mg. HIGH vitamin regimen: vitamin A, 15,000 IU; vitamin D3, 5000 IU; vitamin K3, 5 mg; vitamin E, 80 mg; vitamin B1, 3 mg; vitamin B2, 9 mg; vitamin B6, 7 mg; vitamin B12, 0.04 mg; nicotine acid, 80 mg; pantothenic acid, 15 mg; biotin, 0.15 mg; folic acid, 2 mg; vitamin C, 200 mg; 25-hydroxycholecalciferol, 0.069 mg. View Large Sample Collection and Analysis On d 1 of each experiment, 12 newly hatched progeny ducks were randomly selected from each maternal treatment. Shank pigmentation of these progeny ducks was measured using a DSM Color Fan (DSM Nutritional Products Ltd.). Then, progeny ducks were euthanized for liver and tibiotarsus (both sides) sample collection. On d 14 and 35 of each experiment, one progeny duck was randomly selected from each cage, and livers and tibiotarsi (both sides) were sampled after shank pigmentation measurement and blood collection (bled via wing venipuncture at 10 am; blood samples were clotted at room temperature for 2 h, then centrifuged at 1,200 × g for 10 min at 4°C to obtain serum, and stored at −20°C). Liver samples were analyzed as previously described for the levels of malondialdehyde (MDA), total superoxide dismutase (T-SOD), total antioxidant capacity (T-AOC), and protein carbonyl (Ren et al., 2016c). Tibiotarsus ash content was determined according to method 942.05 in AOAC (2006). Tibiotarsus strength was determined as described in Ren et al. (2016c). Plasma levels of calcium and phosphate were quantified using colorimetric assay kits purchased from Nanjing Jiancheng Bioengineering Institute (Nanjing, Jiangsu Province, P. R. China). Statistical Analysis The differences between progeny ducks from maternal control group and maternal CX and 25-OH-D3 supplemented groups were demonstrated using 2-tailed independent Student t test (SPSS 23, IBM Corp., Chicago, IL). Data are shown as means and pooled standard error of the means (SEM). The results were considered significant at the P ≤ 0.05, and a trend at 0.05 < P ≤ 0.1. RESULTS Experiment 1 (Duck Breeders Aged 54 wk) As presented in Table 2, maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P < 0.001) and tibiotarsus ash content (P = 0.046) and tended to decrease liver T-SOD activity (P = 0.086) of one-day-old progeny ducks. Maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P = 0.005), tended to increase liver T-AOC (P = 0.071), and decreased liver protein carbonyl level (P = 0.050) of 14-day-old progeny ducks. Shank pigmentation of 35-day-old progeny ducks tended to be increased (P = 0.075) by maternal dietary supplementation of CX and 25-OH-D3. No difference (P > 0.1) was observed on liver MDA level, tibiotarsus strength, or serum calcium and phosphate levels. Table 2. Effects of maternal dietary CX and 25-OH-D3 supplementation on shank pigmentation, liver antioxidant status, tibia quality, and serum levels of calcium and phosphate in progeny ducks (experiment 1).1 Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.50  10.63***  0.85  <0.001   14 d  3.56  6.06***  0.48  0.005   35 d  5.00  6.50*  0.42  0.075  Liver MDA (nmol/mg protein)           1 d  5.41  4.62  0.47  0.416   14 d  2.95  2.68  0.12  0.286   35 d  2.86  2.79  0.11  0.762  Liver T-SOD (U/mg protein)           1 d  190  171*  5  0.086   14 d  122  128  4  0.472   35 d  106  113  5  0.514  Liver T-AOC (U/mg protein)           1 d  4.10  4.60  0.45  0.592   14 d  2.10  2.57*  0.13  0.071   35 d  2.57  2.66  0.13  0.731  Liver protein carbonyl (nmol/mg protein)           1 d  31.7  30.5  1.2  0.631   14 d  30.7  25.8**  1.3  0.050   35 d  25.4  23.3  1.1  0.343  Tibiotarsus strength (kg force)           1 d  1.25  1.37  0.04  0.132   14 d  8.0  8.2  0.3  0.663   35 d  19.4  19.7  0.6  0.809  Tibiotarsus ash (%)           1 d  36.7  37.7**  0.2  0.046   14 d  50.3  50.8  0.7  0.757   35 d  55.8  57.8  1.1  0.382  Serum calcium (mmol/L)           14 d  1.73  1.94  0.07  0.132   35 d  1.47  1.49  0.12  0.941  Serum phosphate (mmol/L)           14 d  4.81  4.66  0.10  0.470   35 d  4.45  4.66  0.10  0.308  Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.50  10.63***  0.85  <0.001   14 d  3.56  6.06***  0.48  0.005   35 d  5.00  6.50*  0.42  0.075  Liver MDA (nmol/mg protein)           1 d  5.41  4.62  0.47  0.416   14 d  2.95  2.68  0.12  0.286   35 d  2.86  2.79  0.11  0.762  Liver T-SOD (U/mg protein)           1 d  190  171*  5  0.086   14 d  122  128  4  0.472   35 d  106  113  5  0.514  Liver T-AOC (U/mg protein)           1 d  4.10  4.60  0.45  0.592   14 d  2.10  2.57*  0.13  0.071   35 d  2.57  2.66  0.13  0.731  Liver protein carbonyl (nmol/mg protein)           1 d  31.7  30.5  1.2  0.631   14 d  30.7  25.8**  1.3  0.050   35 d  25.4  23.3  1.1  0.343  Tibiotarsus strength (kg force)           1 d  1.25  1.37  0.04  0.132   14 d  8.0  8.2  0.3  0.663   35 d  19.4  19.7  0.6  0.809  Tibiotarsus ash (%)           1 d  36.7  37.7**  0.2  0.046   14 d  50.3  50.8  0.7  0.757   35 d  55.8  57.8  1.1  0.382  Serum calcium (mmol/L)           14 d  1.73  1.94  0.07  0.132   35 d  1.47  1.49  0.12  0.941  Serum phosphate (mmol/L)           14 d  4.81  4.66  0.10  0.470   35 d  4.45  4.66  0.10  0.308  ***P ≤ 0.01, **0.01 < P ≤ 0.05, *0.05 < P ≤ 0.1 when compared with control group. 1CX+25-OH-D3 = 6 mg/kg canthaxanthin + 0.069 mg/kg 25-hydroxycholecalciferol in maternal diet; MDA = malondialdehyde; T-SOD = total superoxide dismutase; T-AOC = total antioxidant capacity; SEM = standard error of the mean. 2Shank pigmentation of progeny ducks was measured using a DSM Color Fan. A higher number indicates a higher degree of pigmentation. View Large Experiment 2 (Duck Breeders Aged 62 wk) Maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P < 0.001, Table 3) and liver T-AOC (P < 0.001) and decreased liver protein carbonyl level (P = 0.029) of one-day-old progeny ducks. The serum phosphate level of 14-day-old progeny ducks was increased (P = 0.040) by maternal dietary supplementation of CX and 25-OH-D3. No difference (P > 0.1) was observed on liver MDA level, liver T-SOD activity, tibiotarsus strength, tibiotarsus ash content, or serum calcium level. No difference was observed in 35-day-old progeny ducks (P > 0.1). Table 3. Effects of maternal dietary CX and 25-OH-D3 supplementation on shank pigmentation, liver antioxidant status, tibia quality, and serum levels of calcium and phosphate in progeny ducks (experiment 2).1 Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  3.19  9.25***  0.85  <0.001   14 d  5.38  6.31  0.41  0.264   35 d  6.81  6.25  0.26  0.287  Liver MDA (nmol/mg protein)           1 d  2.53  2.21  0.17  0.352   14 d  2.79  2.95  0.13  0.544   35 d  2.95  2.86  0.13  0.731  Liver T-SOD (U/mg protein)           1 d  207  191  9  0.413   14 d  153  165  10  0.573   35 d  142  132  4  0.250  Liver T-AOC (U/mg protein)           1 d  2.84  6.87***  0.54  <0.001   14 d  2.51  2.76  0.11  0.264   35 d  2.19  2.26  0.08  0.695  Liver protein carbonyl (nmol/mg protein)           1 d  33.8  26.0**  1.8  0.029   14 d  22.0  22.5  0.8  0.793   35 d  19.2  19.3  0.3  0.923  Tibiotarsus strength (kg force)           1 d  1.19  1.24  0.04  0.510   14 d  6.7  6.5  0.3  0.804   35 d  15.7  15.3  0.3  0.558  Tibiotarsus ash (%)           1 d  33.5  33.7  0.7  0.880   14 d  50.8  50.7  0.5  0.923   35 d  55.9  57.7  0.9  0.323  Serum calcium (mmol/L)           14 d  2.12  2.19  0.09  0.733   35 d  2.31  2.44  0.06  0.300  Serum phosphate (mmol/L)           14 d  4.42  5.30**  0.22  0.040   35 d  4.93  5.05  0.27  0.833  Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  3.19  9.25***  0.85  <0.001   14 d  5.38  6.31  0.41  0.264   35 d  6.81  6.25  0.26  0.287  Liver MDA (nmol/mg protein)           1 d  2.53  2.21  0.17  0.352   14 d  2.79  2.95  0.13  0.544   35 d  2.95  2.86  0.13  0.731  Liver T-SOD (U/mg protein)           1 d  207  191  9  0.413   14 d  153  165  10  0.573   35 d  142  132  4  0.250  Liver T-AOC (U/mg protein)           1 d  2.84  6.87***  0.54  <0.001   14 d  2.51  2.76  0.11  0.264   35 d  2.19  2.26  0.08  0.695  Liver protein carbonyl (nmol/mg protein)           1 d  33.8  26.0**  1.8  0.029   14 d  22.0  22.5  0.8  0.793   35 d  19.2  19.3  0.3  0.923  Tibiotarsus strength (kg force)           1 d  1.19  1.24  0.04  0.510   14 d  6.7  6.5  0.3  0.804   35 d  15.7  15.3  0.3  0.558  Tibiotarsus ash (%)           1 d  33.5  33.7  0.7  0.880   14 d  50.8  50.7  0.5  0.923   35 d  55.9  57.7  0.9  0.323  Serum calcium (mmol/L)           14 d  2.12  2.19  0.09  0.733   35 d  2.31  2.44  0.06  0.300  Serum phosphate (mmol/L)           14 d  4.42  5.30**  0.22  0.040   35 d  4.93  5.05  0.27  0.833  ***P ≤ 0.01, **0.01 < P ≤ 0.05 when compared with control group. 1CX+25-OH-D3 = 6 mg/kg canthaxanthin + 0.069 mg/kg 25-hydroxycholecalciferol in maternal diet; MDA = malondialdehyde; T-SOD = total superoxide dismutase; T-AOC = total antioxidant capacity; SEM = standard error of the mean. 2Shank pigmentation of progeny ducks was measured using a DSM Color Fan. A higher number indicates a higher degree of pigmentation. View Large Experiment 3 (Duck Breeders Aged 70 wk) Maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P < 0.001, Table 4), tended to increase liver T-SOD activity (P = 0.059) and tibiotarsus ash content (P = 0.080), and tended to decrease liver MDA level (P = 0.092) of one-day-old progeny ducks. Shank pigmentation of 14- (P = 0.004) and 35-day-old (P = 0.010) progeny ducks was increased by maternal dietary supplementation of CX and 25-OH-D3. No difference (P > 0.1) was observed on liver T-AOC, liver protein carbonyl level, tibiotarsus strength, or serum calcium and phosphate levels. Table 4. Effects of maternal dietary CX and 25-OH-D3 supplementation on shank pigmentation, liver antioxidant status, tibia quality, and serum levels of calcium and phosphate in progeny ducks (experiment 3).1 Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.75  9.94***  0.74  <0.001   14 d  5.13  7.38***  0.43  0.004   35 d  6.38  7.50***  0.23  0.010  Liver MDA (nmol/mg protein)           1 d  4.40  3.40*  0.30  0.092   14 d  2.72  2.55  0.17  0.654   35 d  2.76  2.67  0.19  0.828  Liver T-SOD (U/mg protein)           1 d  145  167*  6  0.059   14 d  119  108  6  0.389   35 d  120  126  6  0.678  Liver T-AOC (U/mg protein)           1 d  7.75  8.45  0.64  0.595   14 d  2.53  2.61  0.11  0.753   35 d  2.41  2.44  0.06  0.834  Liver protein carbonyl (nmol/mg protein)           1 d  32.2  30.0  1.8  0.567   14 d  20.1  21.4  0.5  0.213   35 d  20.2  20.8  0.3  0.250  Tibiotarsus strength (kg force)           1 d  1.19  1.22  0.03  0.702   14 d  6.3  6.2  0.2  0.818   35 d  14.3  14.6  0.5  0.743  Tibiotarsus ash (%)           1 d  36.0  37.5*  0.4  0.080   14 d  45.9  47.4  1.4  0.614   35 d  57.8  58.2  0.9  0.803  Serum calcium (mmol/L)           14 d  2.37  2.41  0.07  0.788   35 d  2.46  2.29  0.05  0.708  Serum phosphate (mmol/L)           14 d  4.54  4.25  0.10  0.150   35 d  4.52  4.19  0.22  0.458  Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.75  9.94***  0.74  <0.001   14 d  5.13  7.38***  0.43  0.004   35 d  6.38  7.50***  0.23  0.010  Liver MDA (nmol/mg protein)           1 d  4.40  3.40*  0.30  0.092   14 d  2.72  2.55  0.17  0.654   35 d  2.76  2.67  0.19  0.828  Liver T-SOD (U/mg protein)           1 d  145  167*  6  0.059   14 d  119  108  6  0.389   35 d  120  126  6  0.678  Liver T-AOC (U/mg protein)           1 d  7.75  8.45  0.64  0.595   14 d  2.53  2.61  0.11  0.753   35 d  2.41  2.44  0.06  0.834  Liver protein carbonyl (nmol/mg protein)           1 d  32.2  30.0  1.8  0.567   14 d  20.1  21.4  0.5  0.213   35 d  20.2  20.8  0.3  0.250  Tibiotarsus strength (kg force)           1 d  1.19  1.22  0.03  0.702   14 d  6.3  6.2  0.2  0.818   35 d  14.3  14.6  0.5  0.743  Tibiotarsus ash (%)           1 d  36.0  37.5*  0.4  0.080   14 d  45.9  47.4  1.4  0.614   35 d  57.8  58.2  0.9  0.803  Serum calcium (mmol/L)           14 d  2.37  2.41  0.07  0.788   35 d  2.46  2.29  0.05  0.708  Serum phosphate (mmol/L)           14 d  4.54  4.25  0.10  0.150   35 d  4.52  4.19  0.22  0.458  ***P ≤ 0.01, *0.05 < P ≤ 0.1 when compared with control group. 1CX+25-OH-D3 = 6 mg/kg canthaxanthin + 0.069 mg/kg 25-hydroxycholecalciferol in maternal diet; MDA = malondialdehyde; T-SOD = total superoxide dismutase; T-AOC = total antioxidant capacity; SEM = standard error of the mean. 2Shank pigmentation of progeny ducks was measured using a DSM Color Fan. A higher number indicates a higher degree of pigmentation. View Large DISCUSSION Color is an important attribute for customer acceptance of poultry products (Yang and Jiang, 2005). In this study, maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation of newly hatched ducklings in all 3 experiments. These observations are consistent with our previous data (Zhang et al., 2011; Ren et al., 2016b,c; Ren et al., 2017). In China, while regional color preference exists, poultry producers define the quality of one-day-old ducklings/chicks using a variety of characteristics, including shank color (Yang and Jiang, 2005). Hence, maternal dietary carotenoid supplementation may benefit producers who want to enhance shank pigmentation of their newly hatched ducklings/chicks. In the study of Johnson-Dahl et al. (2017), dietary CX (6 mg/kg) supplementation increased egg yolk CX content from 0 to 300 μg/egg in 7 days. That means a quick shank pigmentation regulation could be conducted in one-day-old chicks/ducklings, according to market. Also important is the shank color of slaughter-age ducks/broilers. In general, it is well accepted that progeny dietary carotenoid is the dominant factor that regulates shank color of slaughter-age ducks/broilers, because maternal carotenoids-derived progeny skin pigmentation can fade a few d post hatch due to chemical or physical breakdown (Zhang et al., 2011; Ren et al., 2016c). Interestingly, here in experiment 3, maternal dietary CX and 25-OH-D3 supplemetation increased shank pigmentation of 35-day-old progeny ducks when progeny ducks were fed a high vitamin regimen diet, which is effective in improving body antioxidant status (Ren et al., 2016c; Ren et al., 2017). While a pigmentation increase from 6.38 to 7.5 does not necessarily mean an increase in customer acceptance, the current results do suggest that dietary antioxidant status should be considered in order to increase shank pigmentation of slaughter-age ducks/broilers (through either the maternal or progeny way). It is reported that antioxidant vitamins (e.g., vitamin A and E) can prevent carotenoids from bleaching (Hartley and Kennedy, 2004; Leclaire et al., 2011). In this study, hens and drakes were mixed, and under the same diet and management. Although breeding eggs came from hens, future studies should investigate the effects of drakes. Both CX and 25-OH-D3 have been shown as effective in improving body antioxidant status (Foote and Denny, 1968; Foote et al., 1970; Garcion et al., 1999). As expected, in this study, maternal dietary CX and 25-OH-D3 supplementation increased antioxidant status of newly hatched ducklings. The question is, how do CX and 25-OH-D3 enhance the antioxidant system? Basically, CX increases body antioxidant status by improving the non-enzymatic antioxidants system (Kennedy and Liebler, 1991; Kennedy and Liebler, 1992), while 25-OH-D3 has been reported to enhance the enzymatic antioxidants system (Sardar et al., 1995; Garcion et al., 1999). In our previous studies, either T-AOC (non-enzymatic antioxidants) or T-SOD (enzymatic antioxidants system) of one-day-old ducklings was increased by maternal supplementation of CX and 25-OH-D3 (Ren et al., 2016b,c). In this study, maternal dietary CX and 25-OH-D3 increased liver T-AOC, but not T-SOD, of one-day-old ducklings in experiment 2 (duck breeders aged 62 wk); however, they tended to increase T-SOD, but not T-AOC, of one-day-old ducklings in experiments 1 and 3 (duck breeders aged 54 and 70 wk). These results suggest that, other than CX and 25-OH-D3, factors such as hen age also may influence the development of the embryonic antioxidant system. Similarly, Johnson-Dahl et al. (2017) reported that both hen age and CX level could affect maternal CX-derived progeny non-enzymatic antioxidants system enhancement. The antioxidant status of 35-day-old progeny ducks was not expected to be affected by maternal CX and 25-OH-D3 supplementation because of depletion and dilution of maternal CX and 25-OH-D3 as the progeny ducks grew. Interestingly, antioxidant status of 14-day-old progeny ducks was increased by maternal dietary CX and 25-OH-D3 in experiment 1, but not in experiments 2 and 3. These results, along with the findings in Ren et al. (2016c) and Johnson-Dahl et al. (2017), suggest: 1) The positive effects of maternal CX and 25-OH-D3 on progeny antioxidant system wane faster in old duck breeders, and 2) a progeny dietary high vitamin regimen may cover up the positive effects of maternal CX and 25-OH-D3 on the progeny antioxidant system. The concept that vitamin D3 mobilizes calcium from the eggshell to the avian embryo was documented as early as the 1970s (Moriuchi and Deluca, 1974; Sunde et al., 1978). In recent literatures (Atencio et al., 2005a,b,c, 2006; Driver et al., 2006a), much work has been conducted to establish the optimal levels and forms of vitamin D3 that can benefit poultry embryonic skeletal development. In Atencio et al. (2005a), chicks from hens fed the highest levels of vitamin D3 (4,000 IU/kg) had the highest tibiotarsus ash content. Similarly, in this study, the supplementation of CX and 25-OH-D3 to a 3,000 IU/kg vitamin D3 basal diet increased tibiotarsus ash content of one-day-old ducklings in experiment 1 (duck breeders aged 54 wk), and tended to increase that in experiment 3 (duck breeders aged 70 wk). However, in experiment 2 (duck breeders aged 62 wk) and a previous study [duck breeders aged 46 wk (Ren et al., 2016c)], maternal dietary supplementation of CX and 25-OH-D3 had no effect on tibiotarsus ash of one-day-old ducklings. These different observations may be due to different egg yolk vitamin D3 deposition efficiency in duck breeders in different laying periods (Mattila et al., 2004). Progeny duck tibiotarsus ash content after d 1 was not affected by maternal dietary supplementation of CX and 25-OH-D3, suggesting the current duck breeder control diet (vitamin D3 = 3000 IU/kg) and progeny duck diet (vitamin D3 = 400 IU/kg) are sufficient in vitamin D3 for supporting progeny's post-hatch skeletal development. In conclusion, a progeny dietary high vitamin regimen could partially prevent maternal CX-derived progeny shank pigmentation from bleaching. Maternal dietary CX and 25-OH-D3 supplementation was more effective in improving progeny antioxidant status when duck breeders were old or progeny ducks were a under low vitamin regimen. A 3,000 IU/kg vitamin D3 diet is sufficient for duck breeders when using progeny tibiotarsus quality as a response parameter. Acknowledgements This project is financially supported by National and Sichuan Provincial Science and Technology Projects (2014BAD13B02, 2014NZ0030, 2013NC0047, and 2011GB2F000002) as well as DSM Nutritional Products (China) Ltd. The authors thank members of 720-Poultry Nutrition Research Laboratory at the Sichuan Agricultural University for their kind help in animal care and sample collection. REFERENCES Atencio A., Edwards H., Pesti G.. 2005a. Effect of the level of cholecalciferol supplementation of broiler breeder hen diets on the performance and bone abnormalities of the progeny fed diets containing various levels of calcium or 25-hydroxycholecalciferol. Poult. Sci.  84: 1593– 1603. Google Scholar CrossRef Search ADS   Atencio A., Edwards H., Pesti G., Ware G.. 2006. The vitamin D3 requirement of broiler breeders. Poult. Sci.  85: 674– 692. Google Scholar CrossRef Search ADS PubMed  Atencio A., Edwards J. H. M., Pesti G.. 2005b. 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Effects of maternal dietary canthaxanthin and 25-hydroxycholecalciferol supplementation on antioxidant status and calcium-phosphate metabolism of progeny ducks

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Abstract

Abstract Three experiments were conducted to investigate the effects of maternal dietary canthaxanthin (CX) and 25-hydroxycholecalciferol (25-OH-D3) supplementation on antioxidant status and calcium-phosphate metabolism of progeny ducks. Cherry Valley duck breeders (38 wk old) were fed either a control diet or the same diet plus CX (6 mg/kg) and 25-OH-D3 (0.069 mg/kg) for 32 weeks. Experiments 1, 2, and 3 were conducted with progeny ducks hatched from eggs laid by duck breeder hens at 54, 62, and 70 wk of age, respectively. Progeny ducks from both maternal treatments were fed with the same NRC (1994) vitamin regimen starter (1 to 14 d) and finisher (15 to 35 d) diets in experiments 1 and 2, and fed with the same high vitamin regimen starter (1 to 14 d) and finisher (15 to 35 d) diets in experiments 3. High vitamin regimen had higher levels of all vitamins, except biotin, than the NRC (1994) vitamin regimen. In experiment 1, maternal CX and 25-OH-D3 increased (P < 0.05) shank pigmentation and tibiotarsus ash and tended to decrease (P < 0.1) liver total superoxide dismutase activity (T-SOD) of one-day-old progeny ducks; and increased (P < 0.05) shank pigmentation, decreased (P = 0.05) liver protein carbonyl, and tended to increase (P < 0.1) liver total antioxidant capacity (T-AOC) of 14-day-old progeny ducks. In experiment 2, maternal CX and 25-OH-D3 increased (P < 0.05) shank pigmentation and liver T-AOC and decreased (P < 0.05) liver protein carbonyl of one-day-old progeny ducks, but increased (P < 0.05) the serum phosphate level of 14-day-old progeny ducks. In experiment 3, maternal CX and 25-OH-D3 increased (P < 0.05) shank pigmentation of one-, 14-, and 35-day-old progeny ducks and tended to increase (P < 0.1) liver T-SOD and tibiotarsus ash, but decrease (P < 0.1) liver malondialdehyde of one-day-old progeny ducks. It can be concluded that progeny dietary high vitamin regimen could partially prevent maternal CX-derived progeny shank pigmentation from bleaching. Maternal CX- and 25-OH-D3-derived effects are influenced by the hen's age and progeny's dietary vitamin regimen. INTRODUCTION The nutritional and physiological relationship between mother and progeny has been widely studied in oviparous, ovoviviparous, and viviparous species (Kidd, 2003; Uller and Olsson, 2006; Victora et al., 2008). In poultry, the nutritional status of breeder hens can affect the nutrient profile of breeder eggs and subsequently influence embryonic development and progeny performance (Wilson, 1997; Kidd, 2003). The possibility of using maternal dietary strategies to overcome problems (e.g., oxidant stress, skeletal disorder) that cause significant economic loss pre- and post hatch has been the subject of poultry science research for many years (Surai, 2000; Driver et al., 2006b). The presence of canthaxanthin (CX, a powerful carotenoid antioxidant) in chicken eggs was documented as early as the 1950s (Paust, 1991). Later, scientists realized that the dietary CX level of breeder hens is positively correlated to CX concentration and antioxidant status of egg yolk, embryo, and post-hatched chicks (Grashorn and Steinberg, 2002; Surai et al., 2003; Rosa et al., 2012; Surai, 2012; Bonilla et al., 2017). Recent studies show that the supplementation of 6 mg/kg CX in maternal diet (sufficient in antioxidants) can benefit the progeny broilers (increases antioxidant status and decreases mortality) in the first 21 d (Zhang et al., 2011; Rosa et al., 2017). Also interesting is the use of maternal dietary 25-hydroxycholecalciferol (25-OH-D3, biologically active metabolite of vitamin D3) to improve skeletal heath of progeny chicks. In the study of Zang et al. (2011), egg yolk 25-OH-D3 concentration was increased by 170% (12.82 vs. 34.63 μg/kg) when 0.035 mg/kg 25-OH-D3 was supplemented to a NRC (1994) based laying hen diet. In the broiler breeder experiment conducted by Atencio et al. (2005c), the relative biological value of 25-OH-D3 in comparison to vitamin D3, calculated using slope ratio, was 111% for progeny body ash content. It would be safe to conclude that, for poultry breeders, 25-OH-D3 is a good source of vitamin D3. We have previously demonstrated the application of the combination of CX and 25-OH-D3 in duck breeder diet (Ren et al., 2016a,b,c; Ren et al., 2017). Basically, the observations in these studies were in good agreement with either CX or 25-OH-D3 experiments mentioned in the last paragraph. However, a few questions still remain to be answered: 1) The effects of maternal CX and 25-OH-D3 may be different in duck breeders at different ages. 2) The effects of maternal CX and 25-OH-D3 may be different in progeny ducks under different vitamin regimens. Hence, 3 experiments were conducted here to investigate these issues using progeny ducks from duck breeders at the ages of 54, 62, and 70 wk, respectively. MATERIALS AND METHODS All animal procedures used in this study were approved by the Animal Nutrition Institute Animal Care and Use Committee at the Sichuan Agricultural University. The duck breeder trial was conducted at Jinyan breeding farm (6,000 egg-laying duck breeders in dimensions) located at Mianzhu City (Sichuan Province, China). Cherry Valley duck breeders (38 wk old) were fed either a control diet or the same diet plus CX (6 mg/kg) and 25-OH-D3 (0.069 mg/kg) for 32 wk (from June 2012 to January 2013). Each treatment had 390 females and 78 males (the hen: drake ratio was 5:1). Duck breeders were raised on semi-open sheds (straw litter floors, with no heating) with an outside area including a swimming pool, a drinker, and a feeder. Feed and water were provided ad libitum, and a 17L:7D photoperiod was used during the trial. According to lab analysis conducted by DSM Nutritional Products Ltd. (Wurmisweg, Switzerland), no CX or 25-OH-D3 were detected in the control diet, while 5.67 mg/kg CX and 0.070 mg/kg 25-OH-D3 were detected in the diet supplemented with CX and 25-OH-D3. Composition and nutrient levels of the control diet are the same as the regular vitamin regimen duck breeder diet listed in Ren et al. (2016a). Experiments 1, 2, and 3 were conducted with progeny ducks hatched from eggs laid by duck breeder hens at 54 (October 2012), 62 (December 2012), and 70 (January 2013) wk of age, respectively. Experiments 1, 2, and 3 Progeny trials were performed in an environmentally controlled room at the Poultry Nutrition Research Laboratory (Sichuan Agricultural University, Yaan, Sichuan, China). Feed and water were provided ad libitum, and a 24L:0D photoperiod was used during the trials. In experiment 1, progeny ducks from each maternal treatment were allotted to 8 cages (15 birds in each cage). Progeny ducks from both maternal treatments received the same starter (from 1 to 14 d) and grower (from 15 to 35 d) diets. Composition and nutrient levels of the starter diet are the same as the NRC (1994) vitamin regimen starter diet listed in Ren et al. (2017). Composition and nutrient levels of the grower diet, which is also under the NRC (1994) vitamin regimen, are listed in Table 1. Experiment 2 was conducted in the same manner as experiment 1 (the only difference between experiment 1 and 2 is that progeny ducks were from duck breeders at a different age). Experiment 3 was conducted in the same manner as experiments 1 and 2, except both starter and grower diets were under a high vitamin regimen, which had higher levels of all vitamins, except biotin, than the NRC (1994) vitamin regimen (see footnote of Table 1). Table 1. Composition and nutrient levels of the basal diet (as-fed basis). Item (%, unless noted)  Progeny diet (15 to 35 d)  Corn  46.5  Wheat bran  15  Rice bran  8  Soybean meal, 43%  8  Rapeseed meal  8  Cottonseed meal  6  Rapeseed oil  3.88  Calcium carbonate  0.96  Dicalcium phosphate, 2H2O  1.175  L-Lysine-HCl  0.27  D, L-Methionine  0.126  Threonine, 98.5%  0.044  Tryptophan, 98.5%  0.032  Sodium chloride  0.4  Choline chloride, 50%  0.1  Bentonite  0.913  Mineral premix1  0.5  Vitamin premix2  0.1  Analyzed nutrient content    ME (Kcal/kg, calculated)  2814  CP (analyzed)  18.12  Calcium (analyzed)  0.84  Total phosphorus (analyzed)  0.74  Nonphytate phosphorus (calculated)  0.378  Item (%, unless noted)  Progeny diet (15 to 35 d)  Corn  46.5  Wheat bran  15  Rice bran  8  Soybean meal, 43%  8  Rapeseed meal  8  Cottonseed meal  6  Rapeseed oil  3.88  Calcium carbonate  0.96  Dicalcium phosphate, 2H2O  1.175  L-Lysine-HCl  0.27  D, L-Methionine  0.126  Threonine, 98.5%  0.044  Tryptophan, 98.5%  0.032  Sodium chloride  0.4  Choline chloride, 50%  0.1  Bentonite  0.913  Mineral premix1  0.5  Vitamin premix2  0.1  Analyzed nutrient content    ME (Kcal/kg, calculated)  2814  CP (analyzed)  18.12  Calcium (analyzed)  0.84  Total phosphorus (analyzed)  0.74  Nonphytate phosphorus (calculated)  0.378  1Supplied per kilogram of diet: copper, 8 mg; iron, 80 mg; zinc, 90 mg; manganese, 70 mg; selenium, 0.3 mg; iodine, 0.4 mg. 2Supplied per kilogram of diet. NRC vitamin regimen: vitamin A, 2500 IU; vitamin D3, 400 IU; vitamin K3, 0.5 mg; vitamin E, 10 mg; vitamin B1, 1.8 mg; vitamin B2, 4 mg; vitamin B6, 2.5 mg; vitamin B12, 0.01 mg; nicotine acid, 55 mg; pantothenic acid, 11 mg; biotin, 0.15 mg; folic acid, 0.55 mg. HIGH vitamin regimen: vitamin A, 15,000 IU; vitamin D3, 5000 IU; vitamin K3, 5 mg; vitamin E, 80 mg; vitamin B1, 3 mg; vitamin B2, 9 mg; vitamin B6, 7 mg; vitamin B12, 0.04 mg; nicotine acid, 80 mg; pantothenic acid, 15 mg; biotin, 0.15 mg; folic acid, 2 mg; vitamin C, 200 mg; 25-hydroxycholecalciferol, 0.069 mg. View Large Sample Collection and Analysis On d 1 of each experiment, 12 newly hatched progeny ducks were randomly selected from each maternal treatment. Shank pigmentation of these progeny ducks was measured using a DSM Color Fan (DSM Nutritional Products Ltd.). Then, progeny ducks were euthanized for liver and tibiotarsus (both sides) sample collection. On d 14 and 35 of each experiment, one progeny duck was randomly selected from each cage, and livers and tibiotarsi (both sides) were sampled after shank pigmentation measurement and blood collection (bled via wing venipuncture at 10 am; blood samples were clotted at room temperature for 2 h, then centrifuged at 1,200 × g for 10 min at 4°C to obtain serum, and stored at −20°C). Liver samples were analyzed as previously described for the levels of malondialdehyde (MDA), total superoxide dismutase (T-SOD), total antioxidant capacity (T-AOC), and protein carbonyl (Ren et al., 2016c). Tibiotarsus ash content was determined according to method 942.05 in AOAC (2006). Tibiotarsus strength was determined as described in Ren et al. (2016c). Plasma levels of calcium and phosphate were quantified using colorimetric assay kits purchased from Nanjing Jiancheng Bioengineering Institute (Nanjing, Jiangsu Province, P. R. China). Statistical Analysis The differences between progeny ducks from maternal control group and maternal CX and 25-OH-D3 supplemented groups were demonstrated using 2-tailed independent Student t test (SPSS 23, IBM Corp., Chicago, IL). Data are shown as means and pooled standard error of the means (SEM). The results were considered significant at the P ≤ 0.05, and a trend at 0.05 < P ≤ 0.1. RESULTS Experiment 1 (Duck Breeders Aged 54 wk) As presented in Table 2, maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P < 0.001) and tibiotarsus ash content (P = 0.046) and tended to decrease liver T-SOD activity (P = 0.086) of one-day-old progeny ducks. Maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P = 0.005), tended to increase liver T-AOC (P = 0.071), and decreased liver protein carbonyl level (P = 0.050) of 14-day-old progeny ducks. Shank pigmentation of 35-day-old progeny ducks tended to be increased (P = 0.075) by maternal dietary supplementation of CX and 25-OH-D3. No difference (P > 0.1) was observed on liver MDA level, tibiotarsus strength, or serum calcium and phosphate levels. Table 2. Effects of maternal dietary CX and 25-OH-D3 supplementation on shank pigmentation, liver antioxidant status, tibia quality, and serum levels of calcium and phosphate in progeny ducks (experiment 1).1 Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.50  10.63***  0.85  <0.001   14 d  3.56  6.06***  0.48  0.005   35 d  5.00  6.50*  0.42  0.075  Liver MDA (nmol/mg protein)           1 d  5.41  4.62  0.47  0.416   14 d  2.95  2.68  0.12  0.286   35 d  2.86  2.79  0.11  0.762  Liver T-SOD (U/mg protein)           1 d  190  171*  5  0.086   14 d  122  128  4  0.472   35 d  106  113  5  0.514  Liver T-AOC (U/mg protein)           1 d  4.10  4.60  0.45  0.592   14 d  2.10  2.57*  0.13  0.071   35 d  2.57  2.66  0.13  0.731  Liver protein carbonyl (nmol/mg protein)           1 d  31.7  30.5  1.2  0.631   14 d  30.7  25.8**  1.3  0.050   35 d  25.4  23.3  1.1  0.343  Tibiotarsus strength (kg force)           1 d  1.25  1.37  0.04  0.132   14 d  8.0  8.2  0.3  0.663   35 d  19.4  19.7  0.6  0.809  Tibiotarsus ash (%)           1 d  36.7  37.7**  0.2  0.046   14 d  50.3  50.8  0.7  0.757   35 d  55.8  57.8  1.1  0.382  Serum calcium (mmol/L)           14 d  1.73  1.94  0.07  0.132   35 d  1.47  1.49  0.12  0.941  Serum phosphate (mmol/L)           14 d  4.81  4.66  0.10  0.470   35 d  4.45  4.66  0.10  0.308  Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.50  10.63***  0.85  <0.001   14 d  3.56  6.06***  0.48  0.005   35 d  5.00  6.50*  0.42  0.075  Liver MDA (nmol/mg protein)           1 d  5.41  4.62  0.47  0.416   14 d  2.95  2.68  0.12  0.286   35 d  2.86  2.79  0.11  0.762  Liver T-SOD (U/mg protein)           1 d  190  171*  5  0.086   14 d  122  128  4  0.472   35 d  106  113  5  0.514  Liver T-AOC (U/mg protein)           1 d  4.10  4.60  0.45  0.592   14 d  2.10  2.57*  0.13  0.071   35 d  2.57  2.66  0.13  0.731  Liver protein carbonyl (nmol/mg protein)           1 d  31.7  30.5  1.2  0.631   14 d  30.7  25.8**  1.3  0.050   35 d  25.4  23.3  1.1  0.343  Tibiotarsus strength (kg force)           1 d  1.25  1.37  0.04  0.132   14 d  8.0  8.2  0.3  0.663   35 d  19.4  19.7  0.6  0.809  Tibiotarsus ash (%)           1 d  36.7  37.7**  0.2  0.046   14 d  50.3  50.8  0.7  0.757   35 d  55.8  57.8  1.1  0.382  Serum calcium (mmol/L)           14 d  1.73  1.94  0.07  0.132   35 d  1.47  1.49  0.12  0.941  Serum phosphate (mmol/L)           14 d  4.81  4.66  0.10  0.470   35 d  4.45  4.66  0.10  0.308  ***P ≤ 0.01, **0.01 < P ≤ 0.05, *0.05 < P ≤ 0.1 when compared with control group. 1CX+25-OH-D3 = 6 mg/kg canthaxanthin + 0.069 mg/kg 25-hydroxycholecalciferol in maternal diet; MDA = malondialdehyde; T-SOD = total superoxide dismutase; T-AOC = total antioxidant capacity; SEM = standard error of the mean. 2Shank pigmentation of progeny ducks was measured using a DSM Color Fan. A higher number indicates a higher degree of pigmentation. View Large Experiment 2 (Duck Breeders Aged 62 wk) Maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P < 0.001, Table 3) and liver T-AOC (P < 0.001) and decreased liver protein carbonyl level (P = 0.029) of one-day-old progeny ducks. The serum phosphate level of 14-day-old progeny ducks was increased (P = 0.040) by maternal dietary supplementation of CX and 25-OH-D3. No difference (P > 0.1) was observed on liver MDA level, liver T-SOD activity, tibiotarsus strength, tibiotarsus ash content, or serum calcium level. No difference was observed in 35-day-old progeny ducks (P > 0.1). Table 3. Effects of maternal dietary CX and 25-OH-D3 supplementation on shank pigmentation, liver antioxidant status, tibia quality, and serum levels of calcium and phosphate in progeny ducks (experiment 2).1 Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  3.19  9.25***  0.85  <0.001   14 d  5.38  6.31  0.41  0.264   35 d  6.81  6.25  0.26  0.287  Liver MDA (nmol/mg protein)           1 d  2.53  2.21  0.17  0.352   14 d  2.79  2.95  0.13  0.544   35 d  2.95  2.86  0.13  0.731  Liver T-SOD (U/mg protein)           1 d  207  191  9  0.413   14 d  153  165  10  0.573   35 d  142  132  4  0.250  Liver T-AOC (U/mg protein)           1 d  2.84  6.87***  0.54  <0.001   14 d  2.51  2.76  0.11  0.264   35 d  2.19  2.26  0.08  0.695  Liver protein carbonyl (nmol/mg protein)           1 d  33.8  26.0**  1.8  0.029   14 d  22.0  22.5  0.8  0.793   35 d  19.2  19.3  0.3  0.923  Tibiotarsus strength (kg force)           1 d  1.19  1.24  0.04  0.510   14 d  6.7  6.5  0.3  0.804   35 d  15.7  15.3  0.3  0.558  Tibiotarsus ash (%)           1 d  33.5  33.7  0.7  0.880   14 d  50.8  50.7  0.5  0.923   35 d  55.9  57.7  0.9  0.323  Serum calcium (mmol/L)           14 d  2.12  2.19  0.09  0.733   35 d  2.31  2.44  0.06  0.300  Serum phosphate (mmol/L)           14 d  4.42  5.30**  0.22  0.040   35 d  4.93  5.05  0.27  0.833  Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  3.19  9.25***  0.85  <0.001   14 d  5.38  6.31  0.41  0.264   35 d  6.81  6.25  0.26  0.287  Liver MDA (nmol/mg protein)           1 d  2.53  2.21  0.17  0.352   14 d  2.79  2.95  0.13  0.544   35 d  2.95  2.86  0.13  0.731  Liver T-SOD (U/mg protein)           1 d  207  191  9  0.413   14 d  153  165  10  0.573   35 d  142  132  4  0.250  Liver T-AOC (U/mg protein)           1 d  2.84  6.87***  0.54  <0.001   14 d  2.51  2.76  0.11  0.264   35 d  2.19  2.26  0.08  0.695  Liver protein carbonyl (nmol/mg protein)           1 d  33.8  26.0**  1.8  0.029   14 d  22.0  22.5  0.8  0.793   35 d  19.2  19.3  0.3  0.923  Tibiotarsus strength (kg force)           1 d  1.19  1.24  0.04  0.510   14 d  6.7  6.5  0.3  0.804   35 d  15.7  15.3  0.3  0.558  Tibiotarsus ash (%)           1 d  33.5  33.7  0.7  0.880   14 d  50.8  50.7  0.5  0.923   35 d  55.9  57.7  0.9  0.323  Serum calcium (mmol/L)           14 d  2.12  2.19  0.09  0.733   35 d  2.31  2.44  0.06  0.300  Serum phosphate (mmol/L)           14 d  4.42  5.30**  0.22  0.040   35 d  4.93  5.05  0.27  0.833  ***P ≤ 0.01, **0.01 < P ≤ 0.05 when compared with control group. 1CX+25-OH-D3 = 6 mg/kg canthaxanthin + 0.069 mg/kg 25-hydroxycholecalciferol in maternal diet; MDA = malondialdehyde; T-SOD = total superoxide dismutase; T-AOC = total antioxidant capacity; SEM = standard error of the mean. 2Shank pigmentation of progeny ducks was measured using a DSM Color Fan. A higher number indicates a higher degree of pigmentation. View Large Experiment 3 (Duck Breeders Aged 70 wk) Maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation (P < 0.001, Table 4), tended to increase liver T-SOD activity (P = 0.059) and tibiotarsus ash content (P = 0.080), and tended to decrease liver MDA level (P = 0.092) of one-day-old progeny ducks. Shank pigmentation of 14- (P = 0.004) and 35-day-old (P = 0.010) progeny ducks was increased by maternal dietary supplementation of CX and 25-OH-D3. No difference (P > 0.1) was observed on liver T-AOC, liver protein carbonyl level, tibiotarsus strength, or serum calcium and phosphate levels. Table 4. Effects of maternal dietary CX and 25-OH-D3 supplementation on shank pigmentation, liver antioxidant status, tibia quality, and serum levels of calcium and phosphate in progeny ducks (experiment 3).1 Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.75  9.94***  0.74  <0.001   14 d  5.13  7.38***  0.43  0.004   35 d  6.38  7.50***  0.23  0.010  Liver MDA (nmol/mg protein)           1 d  4.40  3.40*  0.30  0.092   14 d  2.72  2.55  0.17  0.654   35 d  2.76  2.67  0.19  0.828  Liver T-SOD (U/mg protein)           1 d  145  167*  6  0.059   14 d  119  108  6  0.389   35 d  120  126  6  0.678  Liver T-AOC (U/mg protein)           1 d  7.75  8.45  0.64  0.595   14 d  2.53  2.61  0.11  0.753   35 d  2.41  2.44  0.06  0.834  Liver protein carbonyl (nmol/mg protein)           1 d  32.2  30.0  1.8  0.567   14 d  20.1  21.4  0.5  0.213   35 d  20.2  20.8  0.3  0.250  Tibiotarsus strength (kg force)           1 d  1.19  1.22  0.03  0.702   14 d  6.3  6.2  0.2  0.818   35 d  14.3  14.6  0.5  0.743  Tibiotarsus ash (%)           1 d  36.0  37.5*  0.4  0.080   14 d  45.9  47.4  1.4  0.614   35 d  57.8  58.2  0.9  0.803  Serum calcium (mmol/L)           14 d  2.37  2.41  0.07  0.788   35 d  2.46  2.29  0.05  0.708  Serum phosphate (mmol/L)           14 d  4.54  4.25  0.10  0.150   35 d  4.52  4.19  0.22  0.458  Item  Control  CX+25-OH-D3  SEM  P-value  Shank pigmentation2           1 d  4.75  9.94***  0.74  <0.001   14 d  5.13  7.38***  0.43  0.004   35 d  6.38  7.50***  0.23  0.010  Liver MDA (nmol/mg protein)           1 d  4.40  3.40*  0.30  0.092   14 d  2.72  2.55  0.17  0.654   35 d  2.76  2.67  0.19  0.828  Liver T-SOD (U/mg protein)           1 d  145  167*  6  0.059   14 d  119  108  6  0.389   35 d  120  126  6  0.678  Liver T-AOC (U/mg protein)           1 d  7.75  8.45  0.64  0.595   14 d  2.53  2.61  0.11  0.753   35 d  2.41  2.44  0.06  0.834  Liver protein carbonyl (nmol/mg protein)           1 d  32.2  30.0  1.8  0.567   14 d  20.1  21.4  0.5  0.213   35 d  20.2  20.8  0.3  0.250  Tibiotarsus strength (kg force)           1 d  1.19  1.22  0.03  0.702   14 d  6.3  6.2  0.2  0.818   35 d  14.3  14.6  0.5  0.743  Tibiotarsus ash (%)           1 d  36.0  37.5*  0.4  0.080   14 d  45.9  47.4  1.4  0.614   35 d  57.8  58.2  0.9  0.803  Serum calcium (mmol/L)           14 d  2.37  2.41  0.07  0.788   35 d  2.46  2.29  0.05  0.708  Serum phosphate (mmol/L)           14 d  4.54  4.25  0.10  0.150   35 d  4.52  4.19  0.22  0.458  ***P ≤ 0.01, *0.05 < P ≤ 0.1 when compared with control group. 1CX+25-OH-D3 = 6 mg/kg canthaxanthin + 0.069 mg/kg 25-hydroxycholecalciferol in maternal diet; MDA = malondialdehyde; T-SOD = total superoxide dismutase; T-AOC = total antioxidant capacity; SEM = standard error of the mean. 2Shank pigmentation of progeny ducks was measured using a DSM Color Fan. A higher number indicates a higher degree of pigmentation. View Large DISCUSSION Color is an important attribute for customer acceptance of poultry products (Yang and Jiang, 2005). In this study, maternal dietary CX and 25-OH-D3 supplementation increased shank pigmentation of newly hatched ducklings in all 3 experiments. These observations are consistent with our previous data (Zhang et al., 2011; Ren et al., 2016b,c; Ren et al., 2017). In China, while regional color preference exists, poultry producers define the quality of one-day-old ducklings/chicks using a variety of characteristics, including shank color (Yang and Jiang, 2005). Hence, maternal dietary carotenoid supplementation may benefit producers who want to enhance shank pigmentation of their newly hatched ducklings/chicks. In the study of Johnson-Dahl et al. (2017), dietary CX (6 mg/kg) supplementation increased egg yolk CX content from 0 to 300 μg/egg in 7 days. That means a quick shank pigmentation regulation could be conducted in one-day-old chicks/ducklings, according to market. Also important is the shank color of slaughter-age ducks/broilers. In general, it is well accepted that progeny dietary carotenoid is the dominant factor that regulates shank color of slaughter-age ducks/broilers, because maternal carotenoids-derived progeny skin pigmentation can fade a few d post hatch due to chemical or physical breakdown (Zhang et al., 2011; Ren et al., 2016c). Interestingly, here in experiment 3, maternal dietary CX and 25-OH-D3 supplemetation increased shank pigmentation of 35-day-old progeny ducks when progeny ducks were fed a high vitamin regimen diet, which is effective in improving body antioxidant status (Ren et al., 2016c; Ren et al., 2017). While a pigmentation increase from 6.38 to 7.5 does not necessarily mean an increase in customer acceptance, the current results do suggest that dietary antioxidant status should be considered in order to increase shank pigmentation of slaughter-age ducks/broilers (through either the maternal or progeny way). It is reported that antioxidant vitamins (e.g., vitamin A and E) can prevent carotenoids from bleaching (Hartley and Kennedy, 2004; Leclaire et al., 2011). In this study, hens and drakes were mixed, and under the same diet and management. Although breeding eggs came from hens, future studies should investigate the effects of drakes. Both CX and 25-OH-D3 have been shown as effective in improving body antioxidant status (Foote and Denny, 1968; Foote et al., 1970; Garcion et al., 1999). As expected, in this study, maternal dietary CX and 25-OH-D3 supplementation increased antioxidant status of newly hatched ducklings. The question is, how do CX and 25-OH-D3 enhance the antioxidant system? Basically, CX increases body antioxidant status by improving the non-enzymatic antioxidants system (Kennedy and Liebler, 1991; Kennedy and Liebler, 1992), while 25-OH-D3 has been reported to enhance the enzymatic antioxidants system (Sardar et al., 1995; Garcion et al., 1999). In our previous studies, either T-AOC (non-enzymatic antioxidants) or T-SOD (enzymatic antioxidants system) of one-day-old ducklings was increased by maternal supplementation of CX and 25-OH-D3 (Ren et al., 2016b,c). In this study, maternal dietary CX and 25-OH-D3 increased liver T-AOC, but not T-SOD, of one-day-old ducklings in experiment 2 (duck breeders aged 62 wk); however, they tended to increase T-SOD, but not T-AOC, of one-day-old ducklings in experiments 1 and 3 (duck breeders aged 54 and 70 wk). These results suggest that, other than CX and 25-OH-D3, factors such as hen age also may influence the development of the embryonic antioxidant system. Similarly, Johnson-Dahl et al. (2017) reported that both hen age and CX level could affect maternal CX-derived progeny non-enzymatic antioxidants system enhancement. The antioxidant status of 35-day-old progeny ducks was not expected to be affected by maternal CX and 25-OH-D3 supplementation because of depletion and dilution of maternal CX and 25-OH-D3 as the progeny ducks grew. Interestingly, antioxidant status of 14-day-old progeny ducks was increased by maternal dietary CX and 25-OH-D3 in experiment 1, but not in experiments 2 and 3. These results, along with the findings in Ren et al. (2016c) and Johnson-Dahl et al. (2017), suggest: 1) The positive effects of maternal CX and 25-OH-D3 on progeny antioxidant system wane faster in old duck breeders, and 2) a progeny dietary high vitamin regimen may cover up the positive effects of maternal CX and 25-OH-D3 on the progeny antioxidant system. The concept that vitamin D3 mobilizes calcium from the eggshell to the avian embryo was documented as early as the 1970s (Moriuchi and Deluca, 1974; Sunde et al., 1978). In recent literatures (Atencio et al., 2005a,b,c, 2006; Driver et al., 2006a), much work has been conducted to establish the optimal levels and forms of vitamin D3 that can benefit poultry embryonic skeletal development. In Atencio et al. (2005a), chicks from hens fed the highest levels of vitamin D3 (4,000 IU/kg) had the highest tibiotarsus ash content. Similarly, in this study, the supplementation of CX and 25-OH-D3 to a 3,000 IU/kg vitamin D3 basal diet increased tibiotarsus ash content of one-day-old ducklings in experiment 1 (duck breeders aged 54 wk), and tended to increase that in experiment 3 (duck breeders aged 70 wk). However, in experiment 2 (duck breeders aged 62 wk) and a previous study [duck breeders aged 46 wk (Ren et al., 2016c)], maternal dietary supplementation of CX and 25-OH-D3 had no effect on tibiotarsus ash of one-day-old ducklings. These different observations may be due to different egg yolk vitamin D3 deposition efficiency in duck breeders in different laying periods (Mattila et al., 2004). Progeny duck tibiotarsus ash content after d 1 was not affected by maternal dietary supplementation of CX and 25-OH-D3, suggesting the current duck breeder control diet (vitamin D3 = 3000 IU/kg) and progeny duck diet (vitamin D3 = 400 IU/kg) are sufficient in vitamin D3 for supporting progeny's post-hatch skeletal development. In conclusion, a progeny dietary high vitamin regimen could partially prevent maternal CX-derived progeny shank pigmentation from bleaching. Maternal dietary CX and 25-OH-D3 supplementation was more effective in improving progeny antioxidant status when duck breeders were old or progeny ducks were a under low vitamin regimen. A 3,000 IU/kg vitamin D3 diet is sufficient for duck breeders when using progeny tibiotarsus quality as a response parameter. 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Poultry ScienceOxford University Press

Published: Apr 1, 2018

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