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Effect of dietary high non-phytate phosphorus level on growth performance and metabolism of calcium and phosphorus in Lion-head geese
Animal Feed Science and Technology 236 (2018) 115–121
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Effect of dietary high non-phytate phosphorus level on growth performance and metabolism of calcium and phosphorus in Lionhead geese Y.W. Zhua,1, C.Y. Wanga,1, J. Wenb, W.C. Wanga, L. Yanga,
T
⁎
a
Guangdong Provincial Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou 510000, China b Institute of Integrated Agricultural Science, Qingyuan 511515, China
AR TI CLE I NF O
AB S T R A CT
Keywords: Geese Non-phytate phosphorus Growth performance Serum characteristics
The aim of this study was to investigate the effect of dietary high non-phytate phosphorus (NPP) level on the growth performance and metabolism of Ca and P in Lion-head geese during starter and grower-finisher periods. A total of 384 goslings at d 1 and 240 geese at d 29 were divided into 3 treatments with 4 replicate pens each treatment for Exp. 1 (the starter period for d 1–21) and Exp. 2 (the grower-finisher period for d 29–72), respectively. The 3 supplemental NPP levels (Ca: NPP ratio) in diets were 0.40% (2.38), 0.60% (1.58) and 0.80% (1.19) for Exp. 1 and were 0.30% (2.83), 0.50% (1.70) and 0.70% (1.21) for Exp. 2. In Exp. 1, final body weight, average daily gain and average daily feed intake of goslings fed a diet containing 0.80% NPP (Ca: NPP ratio,1.19) were decreased (P < 0.05) compared to birds fed a diet containing 0.60% NPP (Ca: NPP ratio, 1.58) at the starter period, with no difference (P > 0.05) between the two diets containing NPP of 0.40% (Ca: NPP ratio, 2.38) and 0.80% (Ca: NPP ratio,1.19). At d 21 of goslings, the concentrations of Ca, P, parathyroid hormone and bone gla-protein, and alkaline phosphatase activity in serum were decreased (P < 0.05) linearly in response to the increasing NPP level and decreasing Ca: NPP ratio in diets. At d 72 of geese, tibia bone Ca content was decreased (P < 0.05) linearly as dietary NPP level increased and Ca: NPP ratio decreased. Our results indicated that dietary high NPP level along with low Ca: NPP ratio can reduce growth performance and disrupt Ca and P metabolism together with the changes of serum characteristics in goslings at the starter period.
1. Introduction Phosphorus (P) as an essential nutrient plays a great role in bone mineralization for poultry (Berndt and Kumar, 2009). The P nutrition for optimal growth and bone development in poultry has been well demonstrated (Almquist, 1954). Recently, the nonphytate P (NPP) requirements than the recommendation of National Research Council (1994) for broilers have been well revaluated to reduce P excretion (Jiang et al., 2016; Liu et al., 2017). However, the NPP requirement recommended by National Research Council (1994) for geese from the research for more than five decades (Aitken et al., 1958) might not be applicable to modern classes
Abbreviations: ADFI, average daily feed intake; ADG, average daily gain; ALP, alkaline phosphatase; BGP, bone gla-protein; BW, body weight; Ca, calcium; CT, calcitonin; FG, feed gain ratio; ME, metabolizable energy; NPP, non-phytate phosphorus; P, phosphorus; PTH, parathyroid hormone ⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (L. Yang). 1 These authors contributed equally to the present study https://doi.org/10.1016/j.anifeedsci.2017.12.009 Received 17 May 2017; Received in revised form 24 October 2017; Accepted 12 December 2017 0377-8401/ © 2017 Published by Elsevier B.V.
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of geese and diets. In the practical production, an over-supplementation of NPP requirement as an insurance factor is adopted for modern geese to prevent skeletal problems and leg abnormality in the manufacture of feed production (Joshi, 2011). As a large breed of goose, modern Lion-head geese with greater feed intake have higher daily NPP intake than the geese reported previously (Aitken et al., 1958). Additionally, the supplementation of phytase and vitamin D3 in the modern goose diets can effectively increase P availability (Tian et al., 2013). However, few studies about the influences of dietary NPP excess have been well evaluated in geese. Previous reports in human (Kemi et al., 2006, 2010) and rats (Siu et al., 1981; Hernandez et al., 1996) have demonstrated that dietary high NPP level with low calcium (Ca): NPP ratio impairs the growth performance and inhibits the metabolism of Ca and P and results in the loss of bone mineralization. Dietary high NPP intake also induces related physiological and biochemical changes to regulate the metabolism of Ca and P, such as elevated parathyroid hormone (PTH) secretion (Almaden et al., 1998) and reduced alkaline phosphatase (ALP) activity (Liu et al., 2017). So far, it is unclear whether dietary high NPP level along with imbalance Ca: NPP ratio could induce the negative effects on growth performance and metabolism of Ca and P in Lion-head geese. Therefore, the objective of this study was to investigate the effect of dietary high NPP levels on the growth performance and serum and tibia bone characteristics in Lion-head geese at the starter and grower-finisher periods.
2. Materials and methods 2.1. Animals and diets All experimental procedures were approved by the Institutional Animal Care and Use Committee of South China Agricultural University. The study included 2 experiments with birds of the starter and grower-finisher periods. Two experiments of similar design were conducted. Total of 384 birds of goslings (192 males and 192 females) at 1 d of age (Exp. 1, d 1–21) and 240 birds of geese (120 males and 120 females) at 29 d of age (Exp. 2, d 29–72) were weighed individually and divided into 3 treatments with 4 replicate pens each treatment. Therefore, 32 birds (16 males and 16 females) and 20 birds (10 males and 10 females) per pen were obtained for Exp. 1 and 2, respectively. The three supplemental NPP levels (Ca: NPP ratio) in diets were 0.40% (2.38), 0.60% (1.58) and 0.80% (1.19) for Exp. 1 and were 0.30% (2.83), 0.50% (1.70) and 0.70% (1.21) for Exp. 2, respectively. The basal diets were formulated to meet or exceed nutrition requirements recommended by National Research Council (1994) for geese at the starter and growerfinisher periods (Table 1). The basal diets contained 0.40% NPP and 0.95% Ca for the starter period and contained 0.30% NPP and 0.85% Ca for the grower-finisher period. The basal diets were blended in appropriate amounts to provide a series of diets ranging in NPP content (0.40, 0.60 and 0.80% for Exp. 1, and 0.30, 0.50 and 0.70% for Exp. 2). The anhydrous dibasic calcium phosphate was supplemented to increment the NPP content. All the experimental diets were analyzed for Ca and NPP contents to ensure adequate mixing. All the birds were provided the experimental diets and tap water for consumption ad libitum during d 1–21 and d 29–70. At 21 and 70 d of age, after 12 h feed withdrawal, birds were weighed and feed consumption was recorded by each replicate pen. The ADG, ADFI, and feed:gain ratio (F:G) were calculated. Based on the average BW of birds in each pen, the six geese (3 males and 3 females) were taken for blood sampling, and two of these birds were killed by CO2 inhalation, and the right tibias were removed for bone used for bone sampling at the end of the two experiments.
2.2. Sample preparations and analyses Blood samples were obtained via a wing vein (3.5 mL/bird), immediately placed on ice, and then centrifuged at 2000 × g for 15 min in a refrigerated centrifuge to prepare serum. The serum samples were stored at −20 °C for the analysis of Ca and P concentrations and biochemical parameters. The tibia bone was separated and the length was measured using a vernier caliper and an index of tibia length relative to BW was calculated. They were dried at 105 °Cfor 24 h, and then defatted 48 h in ethyl alcohol followed by a 48 h extraction in ethyl ether, and then dried for 12 h at 110 °C. Tibia bone ash percentage were determined by ashing overnight at 550 °C with a muffle furnace. Total Ca contents of bone ash and diets were determined using an atomic absorption and mass spectrophotometer. Total P contents of bone ash and diets were determined using a spectrophotometer (method 985.01; Association of Official Analytical Chemists, 1990). Phytate P (PP) contents of the experimental diets was analyzed according to the ferric precipitation method as described by Rutherfurd et al. (2004) and then dietary NPP was calculated with the formula of total P – PP. The Ca and P concentrations and ALP activity in serum was determined by HITACHI 7180 automatic biochemical analyzer (Hitachi Ltd., Tokyo, Japan) with commercial kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). The serum PTH, calcitonin (CT), and bone gla-protein (BGP) were measured by radioimmunoassay using commercial kits (Beijing North Institute of Biological Technology, Beijing, China).
2.3. Statistical analyses All values were subjected to one-way ANOVA by using the General Linear Model procedure of SAS (SAS Institute, 1992). The treatment comparisons for significant differences were tested by the LSD method. Orthogonal polynomials were applied for linear and quadratic effects of dependent variables to independent variables. Each replicate served as the experimental unit for all statistical analyses. Significant differences were set at P ≤ 0.05. 116
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Table 1 Composition and nutrient levels of the experimental diets (as-fed basis). Ingredient, %
Dietary NPP level (d 1–21, Exp. 1)
Dietary NPP level (d 29–72, Exp. 2)
0.40%
0.60%
0.80%
0.30%
0.50%
0.70%
Corn Wheat bran Soybean meal Corn gluten meal Oil/Fat powder Dicalcium phosphate Limestone DL-Methionine L-lysine·HCl (98.5%) Bentonite Sodium chloride Vitamin and mineral premix1 Total
60.8 6.8 19.1 8.31 0.56 1.55 1.43 0.12 0.36 0.52 0.35 0.1 100
59.6 6.8 19.1 8.50 0.56 2.75 0.71 0.12 0.36 1.05 0.35 0.1 100
59.6 6.8 19.1 8.50 0.56 3.90 0.0 0.12 0.36 0.61 0.35 0.1 100
61.5 19.0 13.0 1.14 1.56 0.90 1.58 0.18 0.31 0.38 0.35 0.1 100
61.5 18.0 13.0 1.40 1.56 2.15 0.84 0.18 0.31 0.61 0.35 0.1 100
61.5 18.0 13.0 1.40 1.56 3.35 0.10 0.18 0.31 0.15 0.35 0.1 100
Nutrient composition Calculated value, % ME, MJ/kg Crude protein Lysine Methionine Methionine + cysteine Ca Total P NPP Ca: NPP ratio
12.13 20 1.05 0.43 0.76 0.95 0.64 0.40 2.38
12.13 20 1.05 0.43 0.76 0.95 0.84 0.60 1.58
12.13 20 1.05 0.43 0.76 0.95 1.03 0.80 1.19
11.72 15 0.85 0.36 0.63 0.85 0.58 0.30 2.83
11.72 15 0.85 0.36 0.63 0.85 0.76 0.50 1.70
11.72 15 0.85 0.36 0.63 0.85 0.97 0.70 1.21
Analyzed value,2 % Calcium Total P NPP
0.93 0.65 0.40
0.91 0.80 0.58
0.92 0.99 0.77
0.90 0.55 0.28
0.83 0.75 0.52
0.90 0.93 0.68
NPP, non-phytate phosphorus. 1 Provided per kilogram of diet for geese at d 1–21: vitamin A, 10, 000 IU; vitamin D3, 1, 500 IU; vitamin E, 10 IU; thiamine, 1.8 mg; riboflavin, 3.6 mg; pyridoxine, 3.0 mg; vitamin B12, 0.003 mg; calcium pantothenate, 10 mg; folate, 0.25 mg; niacin, 35 mg; biotin, 0.10 mg Choline (Choline chloride), 500 mg; Cu (CuSO4·5H2O), 8 mg; Fe (FeSO4·7H2O), 100 mg; Zn (ZnSO4·7H2O), 100 mg; Mn (MnSO4·H2O), 120 mg; Se (NaSeO3), 0.3 mg; I (KI), 0.7 mg. Provided per kilogram of diet for geese at d 29–72: vitamin A, 5, 000 IU; vitamin D3, 1, 000 IU; vitamin E, 5 IU; thiamine, 1.3 mg; riboflavin, 1.8 mg; pyridoxine, 3.0 mg; vitamin B12, 0.009 mg; calcium pantothenate, 15 mg; folate, 0.55 mg; niacin, 55 mg; biotin, 0.15 mg Choline (Choline chloride), 1300 mg; Cu (CuSO4·5H2O), 3 mg; Fe (FeSO4·7H2O), 80 mg; Zn (ZnSO4·7H2O), 50 mg; Mn (MnSO4·H2O), 50 mg; Se (NaSeO3), 0.1 mg; I (KI), 0.35 mg. 2 Analysed values based on triplicate determinations.
3. Results 3.1. Growth performance Dietary NPP level affected (P ≤ 0.05) final BW, ADFI and ADG quadraticly in goslings during d 1–21 (Table 2). The goslings fed a diet containing 0.80% NPP (Ca: NPP ratio, 1.19) had lower (P < 0.05) final BW (−111 g), ADG (−14.0%) and ADFI (−10.5%) compared to those fed a diet containing 0.60% NPP (Ca: NPP ratio, 1.58) at the starter period, with no difference (P > 0.05) between Table 2 Effect of dietary non-phytate phosphorus level on growth performance of geese during 1–21 d of age. Item1
BW, g ADFI, g/d/bird ADG, g/d/bird F: G, g/g
Dietary NPP level, %2
Pooled SEM
0.40
0.60
0.80
1255a,b 95.3a,b 53.6a,b 1.78
1291a 99.8a 55.4a 1.80
1180b 87.5b 50.1b 1.75
33.3 2.95 1.56 0.02
P-value NPP level
Linear
Quadratic
0.04 0.03 0.05 0.45
NS NS NS –
0.03 0.02 0.04 –
NPP, non-phytate phosphorus; ADFI, average daily feed intake; ADG, average daily gain; BW, body weight; F: G, feed: gain ratio; NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.38, 1.58 and 1.19, respectively.
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Table 3 Effect of dietary non-phytate phosphorus level on growth performance of geese during 29–72 d of age. Item1
BW, g ADFI, g/d/bird ADG, g/d/bird F: G, g/g
Dietary NPP level, %2
Pooled SEM
0.30
0.50
0.70
5550 372 93.5 3.98
5560 370 93.9 3.95
5800 386 99.1 3.90
215 14.7 4.83 0.07
P-value NPP level
Linear
Quadratic
0.22 0.56 0.27 0.76
– – – –
– – – –
NPP, non-phytate phosphorus; ADFI, average daily feed intake; ADG, average daily gain; BW, body weight; F: G, feed: gain ratio. 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.83, 1.70 and 1.21, respectively.
the two diets containing NPP of 0.40% (Ca: NPP ratio, 2.38) and 0.60% (Ca: NPP ratio, 1.58) or between the two diets containing NPP of 0.40% (Ca: NPP ratio, 2.38) and 0.80% (Ca: NPP ratio, 1.19). Dietary NPP level had no effect (P > 0.05) on the above mentioned indices in geese during d 29–72 (Table 3) 3.2. Serum characteristics The data of Ca, P, PTH, CT and BGP concentrations and ALP activity in serum of geese at 21 d and 72 d of age were presented in Tables 4 and 5, respectively. Serum Ca, P, PTH and BGP concentrations and ALP activity were decreased (P ≤ 0.05) linearly in response to dietary increasing NPP level and decreasing Ca: NPP ratio. No effect (P > 0.05) on serum CT concentration was observed in goslings at d 21. The diets with 0.60% and 0.80% NPP levels both had lower serum Ca (P < 0.05), P (P < 0.01), PTH (P < 0.01) and BGP (P < 0.01) concentrations and ALP activity (P < 0.05) in goslings at d 21 compared to the diet with 0.40% NPP. Dietary NPP level did not affect (P > 0.05) all the above measured indices in serum of geese at d 72. 3.3. Bone characteristics Data of the relative bone length and contents of ash, Ca and P in bone of geese at d 21 and 72 were listed in Tables 6 and 7, respectively. Dietary NPP level affected (P < 0.05) relative bone length quadraticly, and had no influences (P > 0.09) on other measured indices in bone of geese at d 21. Geese fed a diet with 0.60% NPP had lower (P < 0.05) relative bone length compared to that from birds fed diets with NPP of 0.40% and 0.80% at d 21. At d 72 of geese, tibia bone Ca content was decreased (P < 0.05) linearly along with the increasing NPP level and decreasing Ca: NPP ratio in diet. No differences (P > 0.10) were observed in other measured indices in geese at d 72. 4. Discussion In the present study, the final BW, ADG and ADFI were significantly decreased in goslings fed the diet containing 0.80% NPP (Ca: NPP = 1.19) compared to those in birds fed the diet containing 0.60% NPP (Ca: NPP = 1.58) at the starter period. However no differences in the above measured indices were observed between the two diets with 0.40% NPP (Ca: NPP = 2.38) and 0.80% NPP (Ca: NPP = 1.19). It is implied that the appropriate dietary Ca: NPP ratio might be a predominant factor in affecting growth performance of goslings. The growth depression due to dietary high NPP supplementation and improper Ca: NPP ratio was confirmed in ducklings at early growth period reported by Lin and Shen (1979). On the one hand, the diet with the highest NPP level significantly Table 4 Effect of dietary non-phytate phosphorus level on serum characteristics of geese at 21 d of age. Item1
Dietary NPP level, %2 0.40
Ca, mmol/L P, mmol/L PTH, ug/mL CT, pg/mL BGP, ng/mL ALP, U/L
Pooled SEM
0.60 a
2.48 2.40a 11.6a 26.2 19.9a 753a
0.80 b
2.24 1.99b 11.0a 21.7 16.4b 612b
b
2.28 1.83b 9.50b 21.7 15.1b 611b
0.06 0.07 0.5 2.0 1.0 46
P-value NPP level
Linear
Quadratic
0.03 0.005 0.01 0.22 0.006 0.05
0.04 0.002 0.005 – 0.005 0.04
NS NS NS – NS NS
NPP, non-phytate phosphorus; CT, calcitonin; BGP, bone gla-protein; PTH, parathyroid hormone; ALP, alkaline phosphatase. NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.38, 1.58 and 1.19, respectively.
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Table 5 Effect of dietary non-phytate phosphorus level on serum characteristics of geese at 72 d of age. Item1
Dietary NPP level, %2
Ca, mmol/L P, mmol/L PTH, ug/mL CT, pg/mL BGP, ng/mL ALP, U/L
Pooled SEM
0.30
0.50
0.70
2.33 1.95 9.74 41.7 15.9 783
2.19 1.78 8.15 41.1 17.4 633
2.12 1.74 7.83 36.2 20.1 835
0.11 0.12 0.75 2.6 1.6 52
P-value NPP level
Linear
Quadratic
0.54 0.42 0.20 0.22 0.15 0.06
– – – – – –
– – – – – –
NPP, non-phytate phosphorus; CT, calcitonin; BGP, bone gla-protein; PTH, parathyroid hormone; ALP, alkaline phosphatase. 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.83, 1.70 and 1.21, respectively. Table 6 Effect of dietary non-phytate phosphorus level on tibia bone characteristics of geese at 21 d of age. Item1
Dietary NPP level, %2 0.40
Relative length, mm/kg Ash, %4 Ca, %5 P, %4
3
98.7 44.3 32.6 14.5
Pooled SEM
0.60 a
b
94.2 45.5 32.3 15.7
0.80 a
101 44.7 33.3 15.9
1.4 0.7 0.8 3.5
P-value NPP level
Linear
Quadratic
0.008 0.57 0.68 0.10
NS – – –
0.003 – – –
NPP level
Linear
Quadratic
0.54 0.27 0.04 0.11
– – 0.03 –
– – NS –
NPP, non-phytate phosphorus; NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.38, 1.58 and 1.19, respectively. 3 Bone length was expressed in relative to body weight. 4 Bone ash content was expressed as a percentage of dry-defated tibia weight. 5 Bone Ca and P contents were expressed as percentages of tibia ash weight. Table 7 Effect of dietary non-phytate phosphorus level on tibia bone characteristics of geese at 72 d of age. Item1
Relative length, mm/kg Ash, %4 Ca, %5 P, %4
Dietary NPP level, %2
3
Pooled SEM
0.30
0.50
0.70
31.3 51.6 29.9a 12.0
31.3 53.4 28.9a,b 12.3
30.6 49.1 22.8b 9.10
0.5 1.0 1.9 3.5
P-value
NPP, non-phytate phosphorus; NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the three diets were 2.83, 1.70 and 1.21, respectively. 3 Bone length was expressed in relative to body weight. 4 Bone ash content was expressed as a percentage of dry-defated tibia weight. 5 Bone Ca and P contents were expressed as percentages of tibia ash weight.
reduced feed intake and then prevented excess NPP consumption in goslings. Subsequently, other nutrients intake was markedly decreased and growth rate was declined for these birds. On the other hand, the imbalance Ca: NPP ratio was able to form insoluble complexes and then lowered the utilization of mineral and energy (Plumstead et al., 2008; Govers et al., 1996). However, no significant effects on growth were observed in broilers at the starter period fed the diets with NPP of 0.88% (Ca: NPP = 1.12; Orban and Roland, 1990) and 1.15% (Ca: NPP = 1.30; Bailey et al., 1986), in which NPP levels were 2-fold higher than National Research Council (1994) recommendation. The above inconsistent results suggested that geese might have less tolerance for dietary NPP excess than broilers at the starter period. The NPP requirement recommended by National Research Council (1994) for geese from the research for more than five decades (Aitken et al., 1958) might not be applicable to modern large breed of Lion-head geese. In the practical production, an over-supplementation of NPP requirement as an insurance factor is adopted for modern geese to prevent skeletal problems and leg abnormality in the manufacture of feed production (Joshi, 2011). Additionally, the supplementation of 119
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phytase and vitamin D3 in the modern goose diets can effectively increase P availability (Tian et al., 2013). Therefore, the potential detrimental effect of high NPP level and lower Ca: NPP ratio should be worth considering in the formulation of goose diets. During the grower-finisher periods, the increasing dietary NPP levels had no effects on the growth performance of geese. The inconsistent results between the two phases suggested that the tolerance of dietary NPP excess and lower Ca: NPP ratio for geese was increased with age. Similar results were confirmed in broilers in response to the increase of dietary NPP level (Jiang et al., 2016; Liu et al., 2017). As for P deficiency in broilers, previous studies also demonstrated that broilers at the finisher phase exhibited a greater tolerance for dietary P deficiency compared to those at the starter phase (Skinner et al., 1992; Dhandu and Angel, 2003). The effect of excess P intake on Ca and P metabolism has been studied in animal (Schryver et al., 1971; Orban and Roland, 1990; Katsumata et al., 2015) and human (Spencer et al., 1965; Kemi et al., 2006). Plasma Ca and P concentrations within a narrow physiological range are sensitive to reflect the body Ca and P metabolism (Veum, 2010). In the current study, when dietary Ca level was kept at 0.95%, serum Ca and P concentrations were decreased linearly as dietary NPP level increased in goslings at 21 d of age, implying that Ca and P metabolism of geese at the starter period was inhibited as dietary Ca: NPP ratio decreased. The imbalanced Ca: P ratio in the high NPP diet resulted in the formation of insoluble complexes with Ca and P in the intestinal tract and negatively affect Ca and P metabolism (Schiller et al., 1989). Additionally, dietary higher NPP level (lower Ca/P ratio) decreased small intestine type IIb sodium-phosphate cotransporter gene mRNA expression level (Jiang et al., 2016; Liu et al., 2017) and then reduced P digestibility (Bradbury et al., 2014). However, there was no significant effect of high dietary NPP on plasma Ca and P concentrations in geese at the grower-finisher period. Leske and Coon (2002) have demonstrated that when broilers were received higher P levels than the physiological threshold for maximum utilization and retention, the additional P could be eliminated through the kidney. Calcium and P and their interaction are essential for bone development and mineralization (Veum, 2010). High P intake negatively affect Ca metabolism and induced the loss of bone mineralization in rats (Kemi et al., 2006) and broilers (Proszkowiec-Weglarz and Angel, 2013). In the present study, tibia Ca content was significantly decreased in geese fed a diet with 0.70% NPP (Ca: NPP = 1.21) compared to the birds fed a diet with 0.30% NPP (Ca: NPP = 2.83) at the grower-finisher period. The negative effect of high P intake on bone Ca contents was agreed with the previous studies in rat (Howe and Beecher, 1981) and women (Kemi et al., 2006). As reported in mice, Masuyama et al. (2003) demonstrated that dietary lower Ca: P ratio reduced bone mineralization by inhibiting the intestinal Ca and P absorption. However, no differences in bone ash contents were observed in geese during the two periods as dietary NPP level increased, which was inconsistent with the studies about NPP requirement in broilers (Jiang et al., 2016; Liu et al., 2017). On the one hand, it might be due to that supplemental Ca and P levels of the two experiment diets used in our study meet and exceed the requirement recommended by National Research Council (1994) for geese at the two periods and can maintain the basic bone development and mineralization. For instance, Katsumata et al. (2015) reported that adequate Ca supplementation can prevent the bone loss induced by a high-P diet. On the other hand, relative bone ash content was expressed as a percentage of dry-defated tibia weight in the present study. In fact, the absolute weight of both bone ash and dry-defated tibia (data were not provided) were declined in goslings fed the high NPP diet. Therefore, the influence of dietary NPP levels on tibia ash content might have not been well characterized. The Ca and P concentrations in plasma and bone are regulated within a normal physiological range through feedback mechanisms (Almaden et al., 1998; Iki et al., 2006), such as the secretion of PTH, BGP and ALP. PTH is secreted by the parathyroid glands and is the most important regulator of Ca and P levels in the blood and within the bones (Palmer et al., 2011). Previous studies has shown that a high-P diet increased PTH secretion and gene expression and then caused an ongoing process in bone reabsorption in rats (Hernandez et al., 1996) and patients (Calvo et al., 1988; Almaden et al., 1998). Low Ca: NPP ratio in habitual diets resulted in the elevated serum PTH concentration in women with adequate Ca intake (Kemi et al., 2010). However, there is a linear decrease on serum PTH concentration in goslings in response to dietary increasing supplementary NPP level and decreasing Ca: NPP ratio in the present study. It was believed that PTH secretion was mainly regulated by changes in ionized Ca and 1, 25-dihydroxyvitamin D3 (1, 25-(OH)2 D3) (Delmez et al., 1989). It is speculated that the reduced serum Ca concentration subjected to the high P diets in the current study might directly activate renal 1α-hydroxylase and 1, 25-(OH)2 D3 in the intestine, kidney, and bones as reported by Delmez et al. (1989). Subsequently, the higher 1, 25-(OH)2 D3 level could inhibit PTH production in the parathyroid glands through the feedback mechanisms (Delmez et al., 1989). Levels of serum BGP and ALP, as new biochemical markers of bone formation process (Iki et al., 2006), were analyzed in geese at two growth periods in the present study. Higher serum BGP levels are relatively well correlated with increases in bone mineral density (Sowers et al., 1999). In the present study, serum BGP concentration was decreased linearly in goslings at the starter period as dietary NPP level increased and Ca: NPP ratio decreased, implying that the degree of bone mineralization might be declined. This finding was consistent with the study that feeding high P diet led to a reduced circulating BGP concentration in pig (Carter et al., 1996). The ALP enzyme activity, which is localized in the plasma membrane of osteoblasts before extracellular release, correlates with bone reabsorption and the release of minerals (Golub and Boesze-Battaglia, 2007). The present study found that serum ALP activity was decreased as dietary NPP level increased in goslings at d 21, which was in agreement with the previous study of broilers (Liu et al., 2017). It is suggested that dietary higher P levels have inhibitory effect on the transfer of P from bone storage pools to blood (Marks et al., 2010), partly contributing to the decline of serum P concentration. In conclusion, the results from the present study indicate that dietary high NPP level along with low Ca: NPP ratio might reduce growth performance and disrupt Ca and P metabolism together with the changes of serum characteristics in goslings at the starter period. Conflict of interest The authors declare that they have no conflicts of interest. 120
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Acknowledgments This study was sponsored by Special Fund for Agro-scientific Research in the Public Interest (201303143) and National Waterfowl Industry Program in China (CARS-42-15). References Aitken, J.R., Lindblad, G.S., Hunsaker, W.G., 1958. The calcium and phosphorus requirements of goslings. Poult. Sci. 37, 1180. Almaden, Y., Hernandez, A., Torregrosa, V., Canalejo, A., Sabate, L., Fernandez Cruz, L., Campistol, J.M., Torres, A., Rodriguez, M., 1998. High phosphate level directly stimulates parathyroid hormone secretion and synthesis by human parathyroid tissue in vitro. J. Am. Soc. Nephrol. 9, 1845–1852. Almquist, H.J., 1954. The phosphorus requirement of young chicks and poults—a review. Poult. Sci. 33 (5), 936–944. Association of Official Analytical Chemists, 1990. Official Methods of Analysis, 15th ed. Assoc. Anal. Chem., Arlington, VA. Bailey, C.A., Linton, S., Brister, R., Creger, C.R., 1986. 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Delmez, J.A., Tindira, C., Grooms, P., Dusso, A., Windus, D.W., Slatopolsky, E., 1989. Parathyroid hormone suppression by intravenous 1,25-dihydroxyvitamin D. A role for increased sensitivity to calcium. J. Clin. Invest. 83, 1349–1355. Dhandu, A.S., Angel, R., 2003. Broiler nonphytin phosphorus requirement in the finisher and withdrawal phases of a commercial four-phase feeding system. Poult. Sci. 82, 1257–1265. Govers, M.J., Termont, D.S., Lapre, J.A., Kleibeuker, J.H., Vonk, R.J., Van der Meer, R., 1996. Calcium in milk products precipitates intestinal fatty acids and secondary bile acids and thus inhibits colonic cytotoxicity in humans. Cancer Res. 56, 3270–3275. Golub, E.E., Boesze-Battaglia, K., 2007. The role of alkaline phosphatase in mineralization. Curr. Opin Orthop. 18 (5), 444–448. Hernandez, A., Concepcion, M.T., Rodriguez, M., Salido, E., Torres, A., 1996. High phosphorus diet increases preproPTH mRNA independent of calcium and calcitriol in normal rats. Kidney Int. 50, 1872–1878. Howe, J.C., Beecher, G.R., 1981. Effect of dietary protein and phosphorus levels on calcium and phosphorus metabolism of the young fast growing rat. J. Nutr. 111, 708–720. Iki, M., Morita, A., Ikeda, Y., Sato, Y., Akiba, T., Matsumoto, T., Nishino, H., Kagamimori, S., Kagawa, Y., Yoneshima, H., Grp, J.S., 2006. Biochemical markers of bone turnover predict bone loss in perimenopausal women but not in postmenopausal women-the Japanese Population-based Osteoporosis (JPOS) Cohort Study. Osteoporosis Int. 17, 1086–1095. Jiang, Y., Lu, L., Li, S.F., Wang, L., Zhang, L.Y., Liu, S.B., Luo, X.G., 2016. An optimal dietary non-phytate phosphorus level of broilers fed a conventional corn-soybean meal diet from 4 to 6 weeks of age. Animal 10, 1626–1634. Joshi, L.R., 2011. A review on nutrient requirement of duck and goose. Age (Weeks) 20, 320C. Katsumata, S., Matsuzaki, H., Uehara, M., Suzuki, K., 2015. 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Liu, S.B., Liao, X.D., Lu, L., Li, S.F., Wang, L., Zhang, L.Y., Jiang, Y., Luo, X.G., 2017. Dietary non-phytate phosphorus requirement of broilers fed a conventional cornsoybean meal diet from 1 to 21 d of age. Poult. Sci. 96, 151–159. Marks, J., Debnam, E.S., Unwin, R.J., 2010. Phosphate homeostasis and the renal-gastrointestinal axis. Am. J. Physiol. Renal. Physiol. 299, F285–296. Masuyama, R., Nakaya, Y., Katsumata, S., Kajita, Y., Uehara, M., Tanaka, S., Sakai, A., Kato, S., Nakamura, T., Suzuki, K., 2003. Dietary calcium and phosphorus ratio regulates bone mineralization and turnover in vitamin D receptor knockout mice by affecting intestinal calcium and phosphorus absorption. J. Bone Miner. Res. 18, 1217–1226. National Research Council, 1994. Nutrient Requirements of Poultry, 9th ed. Natl. Acad. Press, Washington, DC. Orban, J.I., Roland Sr., D.A., 1990. Response of four broiler strains to dietary phosphorus above and below the requirement when brooded at two temperatures. Poult. Sci. 69, 440–445. Palmer, S.C., Hayen, A., Macaskill, P., Pellegrini, F., Craig, J.C., Elder, G.J., Strippoli, G.F., 2011. Serum levels of phosphorus parathyroid hormone, and calcium and risks of death and cardiovascular disease in individuals with chronic kidney disease: a systematic review and meta-analysis. JAMA 305, 1119–1127. Plumstead, P.W., Leytem, A.B., Maguire, R.O., Spears, J.W., Brake, J., 2008. Interaction of calcium and phytate in broiler diets. 1: effects on apparent prececal digestibility and retention of phosphorus. Poult. Sci. 87, 449–458. Proszkowiec-Weglarz, M., Angel, R., 2013. Calcium and phosphorus metabolism in broilers: effect of homeostatic mechanism on calcium and phosphorus digestibility. J. Appl. Poult. Res. 22, 609–627. Rutherfurd, S.M., Chung, T.K., More, P.C., Moughan, P.J., 2004. Effect of microbial phytase on ileal digestibility of phytate phosphorus, total phosphorus, and amino acids in a low phosphorus diet for broilers. Poult. Sci. 83, 61–68. 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Effect of dietary high non-phytate phosphorus level on growth performance and metabolism of calcium and phosphorus in Lionhead geese Y.W. Zhua,1, C.Y. Wanga,1, J. Wenb, W.C. Wanga, L. Yanga,
T
⁎
a
Guangdong Provincial Key Laboratory of Animal Nutrition Control, College of Animal Science, South China Agricultural University, Guangzhou 510000, China b Institute of Integrated Agricultural Science, Qingyuan 511515, China
AR TI CLE I NF O
AB S T R A CT
Keywords: Geese Non-phytate phosphorus Growth performance Serum characteristics
The aim of this study was to investigate the effect of dietary high non-phytate phosphorus (NPP) level on the growth performance and metabolism of Ca and P in Lion-head geese during starter and grower-finisher periods. A total of 384 goslings at d 1 and 240 geese at d 29 were divided into 3 treatments with 4 replicate pens each treatment for Exp. 1 (the starter period for d 1–21) and Exp. 2 (the grower-finisher period for d 29–72), respectively. The 3 supplemental NPP levels (Ca: NPP ratio) in diets were 0.40% (2.38), 0.60% (1.58) and 0.80% (1.19) for Exp. 1 and were 0.30% (2.83), 0.50% (1.70) and 0.70% (1.21) for Exp. 2. In Exp. 1, final body weight, average daily gain and average daily feed intake of goslings fed a diet containing 0.80% NPP (Ca: NPP ratio,1.19) were decreased (P < 0.05) compared to birds fed a diet containing 0.60% NPP (Ca: NPP ratio, 1.58) at the starter period, with no difference (P > 0.05) between the two diets containing NPP of 0.40% (Ca: NPP ratio, 2.38) and 0.80% (Ca: NPP ratio,1.19). At d 21 of goslings, the concentrations of Ca, P, parathyroid hormone and bone gla-protein, and alkaline phosphatase activity in serum were decreased (P < 0.05) linearly in response to the increasing NPP level and decreasing Ca: NPP ratio in diets. At d 72 of geese, tibia bone Ca content was decreased (P < 0.05) linearly as dietary NPP level increased and Ca: NPP ratio decreased. Our results indicated that dietary high NPP level along with low Ca: NPP ratio can reduce growth performance and disrupt Ca and P metabolism together with the changes of serum characteristics in goslings at the starter period.
1. Introduction Phosphorus (P) as an essential nutrient plays a great role in bone mineralization for poultry (Berndt and Kumar, 2009). The P nutrition for optimal growth and bone development in poultry has been well demonstrated (Almquist, 1954). Recently, the nonphytate P (NPP) requirements than the recommendation of National Research Council (1994) for broilers have been well revaluated to reduce P excretion (Jiang et al., 2016; Liu et al., 2017). However, the NPP requirement recommended by National Research Council (1994) for geese from the research for more than five decades (Aitken et al., 1958) might not be applicable to modern classes
Abbreviations: ADFI, average daily feed intake; ADG, average daily gain; ALP, alkaline phosphatase; BGP, bone gla-protein; BW, body weight; Ca, calcium; CT, calcitonin; FG, feed gain ratio; ME, metabolizable energy; NPP, non-phytate phosphorus; P, phosphorus; PTH, parathyroid hormone ⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (L. Yang). 1 These authors contributed equally to the present study https://doi.org/10.1016/j.anifeedsci.2017.12.009 Received 17 May 2017; Received in revised form 24 October 2017; Accepted 12 December 2017 0377-8401/ © 2017 Published by Elsevier B.V.
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of geese and diets. In the practical production, an over-supplementation of NPP requirement as an insurance factor is adopted for modern geese to prevent skeletal problems and leg abnormality in the manufacture of feed production (Joshi, 2011). As a large breed of goose, modern Lion-head geese with greater feed intake have higher daily NPP intake than the geese reported previously (Aitken et al., 1958). Additionally, the supplementation of phytase and vitamin D3 in the modern goose diets can effectively increase P availability (Tian et al., 2013). However, few studies about the influences of dietary NPP excess have been well evaluated in geese. Previous reports in human (Kemi et al., 2006, 2010) and rats (Siu et al., 1981; Hernandez et al., 1996) have demonstrated that dietary high NPP level with low calcium (Ca): NPP ratio impairs the growth performance and inhibits the metabolism of Ca and P and results in the loss of bone mineralization. Dietary high NPP intake also induces related physiological and biochemical changes to regulate the metabolism of Ca and P, such as elevated parathyroid hormone (PTH) secretion (Almaden et al., 1998) and reduced alkaline phosphatase (ALP) activity (Liu et al., 2017). So far, it is unclear whether dietary high NPP level along with imbalance Ca: NPP ratio could induce the negative effects on growth performance and metabolism of Ca and P in Lion-head geese. Therefore, the objective of this study was to investigate the effect of dietary high NPP levels on the growth performance and serum and tibia bone characteristics in Lion-head geese at the starter and grower-finisher periods.
2. Materials and methods 2.1. Animals and diets All experimental procedures were approved by the Institutional Animal Care and Use Committee of South China Agricultural University. The study included 2 experiments with birds of the starter and grower-finisher periods. Two experiments of similar design were conducted. Total of 384 birds of goslings (192 males and 192 females) at 1 d of age (Exp. 1, d 1–21) and 240 birds of geese (120 males and 120 females) at 29 d of age (Exp. 2, d 29–72) were weighed individually and divided into 3 treatments with 4 replicate pens each treatment. Therefore, 32 birds (16 males and 16 females) and 20 birds (10 males and 10 females) per pen were obtained for Exp. 1 and 2, respectively. The three supplemental NPP levels (Ca: NPP ratio) in diets were 0.40% (2.38), 0.60% (1.58) and 0.80% (1.19) for Exp. 1 and were 0.30% (2.83), 0.50% (1.70) and 0.70% (1.21) for Exp. 2, respectively. The basal diets were formulated to meet or exceed nutrition requirements recommended by National Research Council (1994) for geese at the starter and growerfinisher periods (Table 1). The basal diets contained 0.40% NPP and 0.95% Ca for the starter period and contained 0.30% NPP and 0.85% Ca for the grower-finisher period. The basal diets were blended in appropriate amounts to provide a series of diets ranging in NPP content (0.40, 0.60 and 0.80% for Exp. 1, and 0.30, 0.50 and 0.70% for Exp. 2). The anhydrous dibasic calcium phosphate was supplemented to increment the NPP content. All the experimental diets were analyzed for Ca and NPP contents to ensure adequate mixing. All the birds were provided the experimental diets and tap water for consumption ad libitum during d 1–21 and d 29–70. At 21 and 70 d of age, after 12 h feed withdrawal, birds were weighed and feed consumption was recorded by each replicate pen. The ADG, ADFI, and feed:gain ratio (F:G) were calculated. Based on the average BW of birds in each pen, the six geese (3 males and 3 females) were taken for blood sampling, and two of these birds were killed by CO2 inhalation, and the right tibias were removed for bone used for bone sampling at the end of the two experiments.
2.2. Sample preparations and analyses Blood samples were obtained via a wing vein (3.5 mL/bird), immediately placed on ice, and then centrifuged at 2000 × g for 15 min in a refrigerated centrifuge to prepare serum. The serum samples were stored at −20 °C for the analysis of Ca and P concentrations and biochemical parameters. The tibia bone was separated and the length was measured using a vernier caliper and an index of tibia length relative to BW was calculated. They were dried at 105 °Cfor 24 h, and then defatted 48 h in ethyl alcohol followed by a 48 h extraction in ethyl ether, and then dried for 12 h at 110 °C. Tibia bone ash percentage were determined by ashing overnight at 550 °C with a muffle furnace. Total Ca contents of bone ash and diets were determined using an atomic absorption and mass spectrophotometer. Total P contents of bone ash and diets were determined using a spectrophotometer (method 985.01; Association of Official Analytical Chemists, 1990). Phytate P (PP) contents of the experimental diets was analyzed according to the ferric precipitation method as described by Rutherfurd et al. (2004) and then dietary NPP was calculated with the formula of total P – PP. The Ca and P concentrations and ALP activity in serum was determined by HITACHI 7180 automatic biochemical analyzer (Hitachi Ltd., Tokyo, Japan) with commercial kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). The serum PTH, calcitonin (CT), and bone gla-protein (BGP) were measured by radioimmunoassay using commercial kits (Beijing North Institute of Biological Technology, Beijing, China).
2.3. Statistical analyses All values were subjected to one-way ANOVA by using the General Linear Model procedure of SAS (SAS Institute, 1992). The treatment comparisons for significant differences were tested by the LSD method. Orthogonal polynomials were applied for linear and quadratic effects of dependent variables to independent variables. Each replicate served as the experimental unit for all statistical analyses. Significant differences were set at P ≤ 0.05. 116
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Table 1 Composition and nutrient levels of the experimental diets (as-fed basis). Ingredient, %
Dietary NPP level (d 1–21, Exp. 1)
Dietary NPP level (d 29–72, Exp. 2)
0.40%
0.60%
0.80%
0.30%
0.50%
0.70%
Corn Wheat bran Soybean meal Corn gluten meal Oil/Fat powder Dicalcium phosphate Limestone DL-Methionine L-lysine·HCl (98.5%) Bentonite Sodium chloride Vitamin and mineral premix1 Total
60.8 6.8 19.1 8.31 0.56 1.55 1.43 0.12 0.36 0.52 0.35 0.1 100
59.6 6.8 19.1 8.50 0.56 2.75 0.71 0.12 0.36 1.05 0.35 0.1 100
59.6 6.8 19.1 8.50 0.56 3.90 0.0 0.12 0.36 0.61 0.35 0.1 100
61.5 19.0 13.0 1.14 1.56 0.90 1.58 0.18 0.31 0.38 0.35 0.1 100
61.5 18.0 13.0 1.40 1.56 2.15 0.84 0.18 0.31 0.61 0.35 0.1 100
61.5 18.0 13.0 1.40 1.56 3.35 0.10 0.18 0.31 0.15 0.35 0.1 100
Nutrient composition Calculated value, % ME, MJ/kg Crude protein Lysine Methionine Methionine + cysteine Ca Total P NPP Ca: NPP ratio
12.13 20 1.05 0.43 0.76 0.95 0.64 0.40 2.38
12.13 20 1.05 0.43 0.76 0.95 0.84 0.60 1.58
12.13 20 1.05 0.43 0.76 0.95 1.03 0.80 1.19
11.72 15 0.85 0.36 0.63 0.85 0.58 0.30 2.83
11.72 15 0.85 0.36 0.63 0.85 0.76 0.50 1.70
11.72 15 0.85 0.36 0.63 0.85 0.97 0.70 1.21
Analyzed value,2 % Calcium Total P NPP
0.93 0.65 0.40
0.91 0.80 0.58
0.92 0.99 0.77
0.90 0.55 0.28
0.83 0.75 0.52
0.90 0.93 0.68
NPP, non-phytate phosphorus. 1 Provided per kilogram of diet for geese at d 1–21: vitamin A, 10, 000 IU; vitamin D3, 1, 500 IU; vitamin E, 10 IU; thiamine, 1.8 mg; riboflavin, 3.6 mg; pyridoxine, 3.0 mg; vitamin B12, 0.003 mg; calcium pantothenate, 10 mg; folate, 0.25 mg; niacin, 35 mg; biotin, 0.10 mg Choline (Choline chloride), 500 mg; Cu (CuSO4·5H2O), 8 mg; Fe (FeSO4·7H2O), 100 mg; Zn (ZnSO4·7H2O), 100 mg; Mn (MnSO4·H2O), 120 mg; Se (NaSeO3), 0.3 mg; I (KI), 0.7 mg. Provided per kilogram of diet for geese at d 29–72: vitamin A, 5, 000 IU; vitamin D3, 1, 000 IU; vitamin E, 5 IU; thiamine, 1.3 mg; riboflavin, 1.8 mg; pyridoxine, 3.0 mg; vitamin B12, 0.009 mg; calcium pantothenate, 15 mg; folate, 0.55 mg; niacin, 55 mg; biotin, 0.15 mg Choline (Choline chloride), 1300 mg; Cu (CuSO4·5H2O), 3 mg; Fe (FeSO4·7H2O), 80 mg; Zn (ZnSO4·7H2O), 50 mg; Mn (MnSO4·H2O), 50 mg; Se (NaSeO3), 0.1 mg; I (KI), 0.35 mg. 2 Analysed values based on triplicate determinations.
3. Results 3.1. Growth performance Dietary NPP level affected (P ≤ 0.05) final BW, ADFI and ADG quadraticly in goslings during d 1–21 (Table 2). The goslings fed a diet containing 0.80% NPP (Ca: NPP ratio, 1.19) had lower (P < 0.05) final BW (−111 g), ADG (−14.0%) and ADFI (−10.5%) compared to those fed a diet containing 0.60% NPP (Ca: NPP ratio, 1.58) at the starter period, with no difference (P > 0.05) between Table 2 Effect of dietary non-phytate phosphorus level on growth performance of geese during 1–21 d of age. Item1
BW, g ADFI, g/d/bird ADG, g/d/bird F: G, g/g
Dietary NPP level, %2
Pooled SEM
0.40
0.60
0.80
1255a,b 95.3a,b 53.6a,b 1.78
1291a 99.8a 55.4a 1.80
1180b 87.5b 50.1b 1.75
33.3 2.95 1.56 0.02
P-value NPP level
Linear
Quadratic
0.04 0.03 0.05 0.45
NS NS NS –
0.03 0.02 0.04 –
NPP, non-phytate phosphorus; ADFI, average daily feed intake; ADG, average daily gain; BW, body weight; F: G, feed: gain ratio; NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.38, 1.58 and 1.19, respectively.
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Table 3 Effect of dietary non-phytate phosphorus level on growth performance of geese during 29–72 d of age. Item1
BW, g ADFI, g/d/bird ADG, g/d/bird F: G, g/g
Dietary NPP level, %2
Pooled SEM
0.30
0.50
0.70
5550 372 93.5 3.98
5560 370 93.9 3.95
5800 386 99.1 3.90
215 14.7 4.83 0.07
P-value NPP level
Linear
Quadratic
0.22 0.56 0.27 0.76
– – – –
– – – –
NPP, non-phytate phosphorus; ADFI, average daily feed intake; ADG, average daily gain; BW, body weight; F: G, feed: gain ratio. 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.83, 1.70 and 1.21, respectively.
the two diets containing NPP of 0.40% (Ca: NPP ratio, 2.38) and 0.60% (Ca: NPP ratio, 1.58) or between the two diets containing NPP of 0.40% (Ca: NPP ratio, 2.38) and 0.80% (Ca: NPP ratio, 1.19). Dietary NPP level had no effect (P > 0.05) on the above mentioned indices in geese during d 29–72 (Table 3) 3.2. Serum characteristics The data of Ca, P, PTH, CT and BGP concentrations and ALP activity in serum of geese at 21 d and 72 d of age were presented in Tables 4 and 5, respectively. Serum Ca, P, PTH and BGP concentrations and ALP activity were decreased (P ≤ 0.05) linearly in response to dietary increasing NPP level and decreasing Ca: NPP ratio. No effect (P > 0.05) on serum CT concentration was observed in goslings at d 21. The diets with 0.60% and 0.80% NPP levels both had lower serum Ca (P < 0.05), P (P < 0.01), PTH (P < 0.01) and BGP (P < 0.01) concentrations and ALP activity (P < 0.05) in goslings at d 21 compared to the diet with 0.40% NPP. Dietary NPP level did not affect (P > 0.05) all the above measured indices in serum of geese at d 72. 3.3. Bone characteristics Data of the relative bone length and contents of ash, Ca and P in bone of geese at d 21 and 72 were listed in Tables 6 and 7, respectively. Dietary NPP level affected (P < 0.05) relative bone length quadraticly, and had no influences (P > 0.09) on other measured indices in bone of geese at d 21. Geese fed a diet with 0.60% NPP had lower (P < 0.05) relative bone length compared to that from birds fed diets with NPP of 0.40% and 0.80% at d 21. At d 72 of geese, tibia bone Ca content was decreased (P < 0.05) linearly along with the increasing NPP level and decreasing Ca: NPP ratio in diet. No differences (P > 0.10) were observed in other measured indices in geese at d 72. 4. Discussion In the present study, the final BW, ADG and ADFI were significantly decreased in goslings fed the diet containing 0.80% NPP (Ca: NPP = 1.19) compared to those in birds fed the diet containing 0.60% NPP (Ca: NPP = 1.58) at the starter period. However no differences in the above measured indices were observed between the two diets with 0.40% NPP (Ca: NPP = 2.38) and 0.80% NPP (Ca: NPP = 1.19). It is implied that the appropriate dietary Ca: NPP ratio might be a predominant factor in affecting growth performance of goslings. The growth depression due to dietary high NPP supplementation and improper Ca: NPP ratio was confirmed in ducklings at early growth period reported by Lin and Shen (1979). On the one hand, the diet with the highest NPP level significantly Table 4 Effect of dietary non-phytate phosphorus level on serum characteristics of geese at 21 d of age. Item1
Dietary NPP level, %2 0.40
Ca, mmol/L P, mmol/L PTH, ug/mL CT, pg/mL BGP, ng/mL ALP, U/L
Pooled SEM
0.60 a
2.48 2.40a 11.6a 26.2 19.9a 753a
0.80 b
2.24 1.99b 11.0a 21.7 16.4b 612b
b
2.28 1.83b 9.50b 21.7 15.1b 611b
0.06 0.07 0.5 2.0 1.0 46
P-value NPP level
Linear
Quadratic
0.03 0.005 0.01 0.22 0.006 0.05
0.04 0.002 0.005 – 0.005 0.04
NS NS NS – NS NS
NPP, non-phytate phosphorus; CT, calcitonin; BGP, bone gla-protein; PTH, parathyroid hormone; ALP, alkaline phosphatase. NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.38, 1.58 and 1.19, respectively.
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Table 5 Effect of dietary non-phytate phosphorus level on serum characteristics of geese at 72 d of age. Item1
Dietary NPP level, %2
Ca, mmol/L P, mmol/L PTH, ug/mL CT, pg/mL BGP, ng/mL ALP, U/L
Pooled SEM
0.30
0.50
0.70
2.33 1.95 9.74 41.7 15.9 783
2.19 1.78 8.15 41.1 17.4 633
2.12 1.74 7.83 36.2 20.1 835
0.11 0.12 0.75 2.6 1.6 52
P-value NPP level
Linear
Quadratic
0.54 0.42 0.20 0.22 0.15 0.06
– – – – – –
– – – – – –
NPP, non-phytate phosphorus; CT, calcitonin; BGP, bone gla-protein; PTH, parathyroid hormone; ALP, alkaline phosphatase. 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.83, 1.70 and 1.21, respectively. Table 6 Effect of dietary non-phytate phosphorus level on tibia bone characteristics of geese at 21 d of age. Item1
Dietary NPP level, %2 0.40
Relative length, mm/kg Ash, %4 Ca, %5 P, %4
3
98.7 44.3 32.6 14.5
Pooled SEM
0.60 a
b
94.2 45.5 32.3 15.7
0.80 a
101 44.7 33.3 15.9
1.4 0.7 0.8 3.5
P-value NPP level
Linear
Quadratic
0.008 0.57 0.68 0.10
NS – – –
0.003 – – –
NPP level
Linear
Quadratic
0.54 0.27 0.04 0.11
– – 0.03 –
– – NS –
NPP, non-phytate phosphorus; NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the 3 diets were 2.38, 1.58 and 1.19, respectively. 3 Bone length was expressed in relative to body weight. 4 Bone ash content was expressed as a percentage of dry-defated tibia weight. 5 Bone Ca and P contents were expressed as percentages of tibia ash weight. Table 7 Effect of dietary non-phytate phosphorus level on tibia bone characteristics of geese at 72 d of age. Item1
Relative length, mm/kg Ash, %4 Ca, %5 P, %4
Dietary NPP level, %2
3
Pooled SEM
0.30
0.50
0.70
31.3 51.6 29.9a 12.0
31.3 53.4 28.9a,b 12.3
30.6 49.1 22.8b 9.10
0.5 1.0 1.9 3.5
P-value
NPP, non-phytate phosphorus; NS, not significant. a Means within a row lacking a common superscript differ (P < 0.05). b Means within a row lacking a common superscript differ (P < 0.05). 1 Data represent the means of 4 replicate cages (n = 4). 2 The Ca: NPP ratios in the three diets were 2.83, 1.70 and 1.21, respectively. 3 Bone length was expressed in relative to body weight. 4 Bone ash content was expressed as a percentage of dry-defated tibia weight. 5 Bone Ca and P contents were expressed as percentages of tibia ash weight.
reduced feed intake and then prevented excess NPP consumption in goslings. Subsequently, other nutrients intake was markedly decreased and growth rate was declined for these birds. On the other hand, the imbalance Ca: NPP ratio was able to form insoluble complexes and then lowered the utilization of mineral and energy (Plumstead et al., 2008; Govers et al., 1996). However, no significant effects on growth were observed in broilers at the starter period fed the diets with NPP of 0.88% (Ca: NPP = 1.12; Orban and Roland, 1990) and 1.15% (Ca: NPP = 1.30; Bailey et al., 1986), in which NPP levels were 2-fold higher than National Research Council (1994) recommendation. The above inconsistent results suggested that geese might have less tolerance for dietary NPP excess than broilers at the starter period. The NPP requirement recommended by National Research Council (1994) for geese from the research for more than five decades (Aitken et al., 1958) might not be applicable to modern large breed of Lion-head geese. In the practical production, an over-supplementation of NPP requirement as an insurance factor is adopted for modern geese to prevent skeletal problems and leg abnormality in the manufacture of feed production (Joshi, 2011). Additionally, the supplementation of 119
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phytase and vitamin D3 in the modern goose diets can effectively increase P availability (Tian et al., 2013). Therefore, the potential detrimental effect of high NPP level and lower Ca: NPP ratio should be worth considering in the formulation of goose diets. During the grower-finisher periods, the increasing dietary NPP levels had no effects on the growth performance of geese. The inconsistent results between the two phases suggested that the tolerance of dietary NPP excess and lower Ca: NPP ratio for geese was increased with age. Similar results were confirmed in broilers in response to the increase of dietary NPP level (Jiang et al., 2016; Liu et al., 2017). As for P deficiency in broilers, previous studies also demonstrated that broilers at the finisher phase exhibited a greater tolerance for dietary P deficiency compared to those at the starter phase (Skinner et al., 1992; Dhandu and Angel, 2003). The effect of excess P intake on Ca and P metabolism has been studied in animal (Schryver et al., 1971; Orban and Roland, 1990; Katsumata et al., 2015) and human (Spencer et al., 1965; Kemi et al., 2006). Plasma Ca and P concentrations within a narrow physiological range are sensitive to reflect the body Ca and P metabolism (Veum, 2010). In the current study, when dietary Ca level was kept at 0.95%, serum Ca and P concentrations were decreased linearly as dietary NPP level increased in goslings at 21 d of age, implying that Ca and P metabolism of geese at the starter period was inhibited as dietary Ca: NPP ratio decreased. The imbalanced Ca: P ratio in the high NPP diet resulted in the formation of insoluble complexes with Ca and P in the intestinal tract and negatively affect Ca and P metabolism (Schiller et al., 1989). Additionally, dietary higher NPP level (lower Ca/P ratio) decreased small intestine type IIb sodium-phosphate cotransporter gene mRNA expression level (Jiang et al., 2016; Liu et al., 2017) and then reduced P digestibility (Bradbury et al., 2014). However, there was no significant effect of high dietary NPP on plasma Ca and P concentrations in geese at the grower-finisher period. Leske and Coon (2002) have demonstrated that when broilers were received higher P levels than the physiological threshold for maximum utilization and retention, the additional P could be eliminated through the kidney. Calcium and P and their interaction are essential for bone development and mineralization (Veum, 2010). High P intake negatively affect Ca metabolism and induced the loss of bone mineralization in rats (Kemi et al., 2006) and broilers (Proszkowiec-Weglarz and Angel, 2013). In the present study, tibia Ca content was significantly decreased in geese fed a diet with 0.70% NPP (Ca: NPP = 1.21) compared to the birds fed a diet with 0.30% NPP (Ca: NPP = 2.83) at the grower-finisher period. The negative effect of high P intake on bone Ca contents was agreed with the previous studies in rat (Howe and Beecher, 1981) and women (Kemi et al., 2006). As reported in mice, Masuyama et al. (2003) demonstrated that dietary lower Ca: P ratio reduced bone mineralization by inhibiting the intestinal Ca and P absorption. However, no differences in bone ash contents were observed in geese during the two periods as dietary NPP level increased, which was inconsistent with the studies about NPP requirement in broilers (Jiang et al., 2016; Liu et al., 2017). On the one hand, it might be due to that supplemental Ca and P levels of the two experiment diets used in our study meet and exceed the requirement recommended by National Research Council (1994) for geese at the two periods and can maintain the basic bone development and mineralization. For instance, Katsumata et al. (2015) reported that adequate Ca supplementation can prevent the bone loss induced by a high-P diet. On the other hand, relative bone ash content was expressed as a percentage of dry-defated tibia weight in the present study. In fact, the absolute weight of both bone ash and dry-defated tibia (data were not provided) were declined in goslings fed the high NPP diet. Therefore, the influence of dietary NPP levels on tibia ash content might have not been well characterized. The Ca and P concentrations in plasma and bone are regulated within a normal physiological range through feedback mechanisms (Almaden et al., 1998; Iki et al., 2006), such as the secretion of PTH, BGP and ALP. PTH is secreted by the parathyroid glands and is the most important regulator of Ca and P levels in the blood and within the bones (Palmer et al., 2011). Previous studies has shown that a high-P diet increased PTH secretion and gene expression and then caused an ongoing process in bone reabsorption in rats (Hernandez et al., 1996) and patients (Calvo et al., 1988; Almaden et al., 1998). Low Ca: NPP ratio in habitual diets resulted in the elevated serum PTH concentration in women with adequate Ca intake (Kemi et al., 2010). However, there is a linear decrease on serum PTH concentration in goslings in response to dietary increasing supplementary NPP level and decreasing Ca: NPP ratio in the present study. It was believed that PTH secretion was mainly regulated by changes in ionized Ca and 1, 25-dihydroxyvitamin D3 (1, 25-(OH)2 D3) (Delmez et al., 1989). It is speculated that the reduced serum Ca concentration subjected to the high P diets in the current study might directly activate renal 1α-hydroxylase and 1, 25-(OH)2 D3 in the intestine, kidney, and bones as reported by Delmez et al. (1989). Subsequently, the higher 1, 25-(OH)2 D3 level could inhibit PTH production in the parathyroid glands through the feedback mechanisms (Delmez et al., 1989). Levels of serum BGP and ALP, as new biochemical markers of bone formation process (Iki et al., 2006), were analyzed in geese at two growth periods in the present study. Higher serum BGP levels are relatively well correlated with increases in bone mineral density (Sowers et al., 1999). In the present study, serum BGP concentration was decreased linearly in goslings at the starter period as dietary NPP level increased and Ca: NPP ratio decreased, implying that the degree of bone mineralization might be declined. This finding was consistent with the study that feeding high P diet led to a reduced circulating BGP concentration in pig (Carter et al., 1996). The ALP enzyme activity, which is localized in the plasma membrane of osteoblasts before extracellular release, correlates with bone reabsorption and the release of minerals (Golub and Boesze-Battaglia, 2007). The present study found that serum ALP activity was decreased as dietary NPP level increased in goslings at d 21, which was in agreement with the previous study of broilers (Liu et al., 2017). It is suggested that dietary higher P levels have inhibitory effect on the transfer of P from bone storage pools to blood (Marks et al., 2010), partly contributing to the decline of serum P concentration. In conclusion, the results from the present study indicate that dietary high NPP level along with low Ca: NPP ratio might reduce growth performance and disrupt Ca and P metabolism together with the changes of serum characteristics in goslings at the starter period. Conflict of interest The authors declare that they have no conflicts of interest. 120
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