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METABOLISM AND NUTRITION |
* Department of Poultry Science, North Carolina State University, Raleigh 27695-7608; USDA, Agricultural Research Service, Northwest Irrigation and Soils Research Laboratory, 3793 N 3600 E, Kimberly, ID 83341-5076; Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, VA 24061; Department of Animal Science, North Carolina State University, Raleigh 27695-7621; and # USDA, Agricultural Research Service, Soybean and Nitrogen Fixation Research Unit, 3271 Ligon Street, Raleigh, NC 27607
2 Corresponding author: jbrake{at}ncsu.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: broiler • phosphorus • soybean meal • phytate • environment
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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To improve the utilization of P from SBM, low-phytate (LP) varieties of soybeans have been selectively bred that have similar nutritive value and total P concentrations but contained considerably reduced levels of phytate P (Wilcox et al., 2000; Raboy, 2002). However, reducing the dietary phytate P concentration by including LP grains would also presumably increase the M-ratio of Ca:phytate P in the intestine, which would influence the fate of phytate P (Wise, 1983). Early findings by Nelson et al. (1968b) demonstrated a 50% reduction in the Ca requirement for maximum bone ash when the dietary phytate P content was reduced in broiler diets. This was hypothesized to be caused by the ability of 1% phytate in a diet to chelate 0.36% Ca, thus decreasing the amount of Ca absorbed and increasing the dietary Ca concentration required for maximum bone ash, which would also alter the optimum dietary ratio of Ca:NPP. The potential effect of dietary phytate on the optimum ratio of Ca:P was further supported by Van der Klis and Versteegh (1996), who suggested that the optimum ratio of Ca:available P in broilers was reduced when diets contained less phytate. However, these authors did not quantify the effects of dietary Ca on the intestinal digestibility and overall retention of Ca and P from phytate when diets contained varying levels of both Ca and phytate.
Therefore, the objective of this study was to quantify the effects of dietary Ca on Ca and P absorption from the intestine, overall P retention, and the optimum ratio of Ca:P when diets contained different phytate P concentrations from inclusion of either high-phytate (HP), conventional, or LP varieties of SBM.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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All animal work was approved by the Institutional Animal Care and Use Committee of North Carolina State University. Broiler chicks were hatched from eggs obtained from the resident flock of Ross 344 x 508 broiler breeders. Chicks were feather-sexed at hatching, and 816 male chicks were permanently identified with neck tags and 17 chicks randomly allocated to each of 48 electrically heated battery brooders located within 2 environmentally controlled brooding rooms. To reduce vertical temperature and lighting differences among the cages in the battery brooders, only the middle 4 tiers of cages in each 6-tier battery brooder were utilized. Brooding temperatures within cages were initially set at 33°C and reduced gradually to 25°C by 21 d of age. From 1 to 15 d, all birds had ad libitum access to feed and water and received a standard corn-soy broiler starter diet containing 3,150 kcal of ME/kg, 23.0% CP, 0.90% Ca, and 0.45% NPP.
Dietary Treatments
To obtain practical broiler diets with different phytate P concentrations, SBM made from 3 different cultivars of soybeans that differed in their natural phytate content was utilized (Table 1
). The HP Prolina SBM (Burton et al., 1999) and the LP SBM (Wilcox et al., 2000) were processed from soybeans selected for either improved protein or LP P content. A commercial SBM with similar protein and amino acid concentration and intermediate in its phytate concentration was selected as a control. Further, to increase the range of phytate P in the final diets, degermed dehulled (DGDH) corn with a low level of phytate P was used in the formulations.
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). Finely ground limestone was added to each of the basal diets at the expense of washed sand to obtain graded levels of dietary Ca (0.47, 0.70, 0.93, and 1.16%). Titanium dioxide and celite were included in diets as indigestible markers to allow the calculation of apparent nutrient digestibility and overall retention. To further reduce differences between diets, the soy oil added to diets was held constant at 6.2%, and the formulated moisture content was fixed at 11.5% by varying the inclusion of water. The analyzed phytate P levels were 0.28, 0.24, and 0.10% for the HP Prolina, commercial, and LP SBM diets, respectively (Table 2). All diets were mixed in two 25-kg batches in a bakery-style vertical mixer, and each batch was sampled and analyzed individually.
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Sample Collection and Analyses
Excreta were collected from metal pans lined with clean plastic beneath each cage during each of two 24-h periods. Excreta collection I (16 to 17 d) commenced after birds had been fasted for 16 h and placed on experimental treatments. Excreta collection II (19 to 20 d) commenced at 19 d after an adaptation period of 72 h. After each collection, the excreta from each pan were homogenized, subsampled, and immediately frozen. At 21 d of age, 10 chicks from each pen were weighed, killed by cervical dislocation, and the terminal 13 cm of ileum was removed 3 cm anterior to the ileocecal junction. The ileal digesta were gently expressed, pooled per cage, and frozen. Feeders were weighed at the start and end of excreta collection I and again at the end of excreta collection II to calculate the mean feed intake per bird.
Frozen samples of feed, ileal digesta, and excreta were lyophilized and finely ground before analyzing all samples in duplicate for total elements and phytate as follows: (i) total elements (Ca and P) were determined by microwave-assisted digestion of a 0.5-g dried sample with 8 mL of concentrated HNO3 and 2 mL of 30% H2O2 (vol/vol) with all elements quantified using inductively coupled plasma optical-emission spectrometry detection (4300DV, Perkin-Elmer, Wellesley, MA), and (ii) phytate [inositol phosphate (IP) 6] was determined by acid extraction followed by HPLC analysis (Agilent HPLC 1100 series, Agilent Technologies, Wilmington, DE; Kwanyuen and Burton, 2005). The phytate-bound P was subsequently calculated by multiplying the analyzed phytate content by a factor of 0.2818, which represented the M-proportion of P in phytate (Angel et al., 2002). The TiO2 of diets, ileal, and excreta samples was determined using the method of Short et al. (1996).
Calculations and Statistical Analyses
The apparent percentage of prececal nutrient digestibility (PcND%) and overall percentage of nutrient retention (TNR%), expressed as a percentage of DM nutrient concentration, were calculated using the index method based on the following equation of Dilger and Adeola (2006):
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where TiOdiet = the initial TiO2 concentration in the diet; Nutdiet = the initial dietary concentration of the nutrient being assessed; and TiOout and Nutout = the respective concentrations of either TiO2 or nutrient in the ileal digesta or excreta, respectively.
To account for differences in dietary nutrient concentrations, the apparent amount (g) of nutrients absorbed per kilogram of DM intake (DMI) at the terminal ileum (PcNAg), as well as the total retention of dietary nutrients per kilogram of DMI, (TNRg), was calculated using the equation:
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where PcNA% or TNR% = the percentage of nutrient digestibility or retention calculated in [1]. Further, the nutrient output per kilogram of DMI at the terminal ileum (PcNEg,) or total nutrients excreted (TNEg) per kilogram of DMI were calculated using the ratio of TiO2 intake to TiO2 output (Dilger and Adeola, 2006):
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where NcE = the concentration of the respective nutrient in the ileal digesta or excreta; TiOdiet = the initial TiO2 concentration in the diet; and TiOout = the concentration of TiO2 in the ileal digesta or excreta. Finally, the sum of
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All data were analyzed using the mixed-models procedure (SAS Institute, 2004). There were 4 replicate cages per treatment arranged in a randomized complete block design. There were 4 blocks with 2 blocks of 4 cages located in each of 2 rooms. A cage of birds served as the experimental unit. Data were analyzed using a factorial effects model that included SBM source (3 levels), dietary Ca (4 levels), and all 2-way interactions as fixed effects with block as a random effect. Orthogonal polynomial contrasts were used to assess the significance of linear or quadratic models to describe the response in the dependent variable to increasing Ca level. Where appropriate, means separation was carried out using Tukey’s honestly significant difference with an 
level of 0.05. Further, the breakpoint in the dietary Ca dose at which a plateau in total P retention and output of P in the excreta was reached was determined using segmented regression models in PROC NLIN (SAS Institute, 2004). Correlation coefficients between specific independent and dependent variables were determined using the PROC CORR function of SAS (SAS Institute, 2004). Statements of statistical significance were based upon P < 0.05 unless otherwise stated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. The majority of IP found was in the form of IP6, with decreasing concentrations of the lower IP esters. The concentration of IP esters was lower in the LP SBM than the other SBM sources with the exception of IP3. The HP Prolina SBM had a greater concentration of IP5, which accounted for ~19% of the total IP content, whereas there was only ~11% IP5 in both the commercial and LP SBM.
The calculated and analyzed nutrient content of diets are presented in Table 3. Analyzed dietary CP, amino acids, Ca, and P levels were in good agreement with formulated values, and small deviations in the analyzed Ca and P values were attributed to sampling and analytical error. The analyzed phytate P concentration of samples of SBM (Table 1) was determined from samples of SBM drawn at the time of diet mixing and was lower compared with values used in diet formulation, which had been obtained from initial screening of HP Prolina SBM several months before the onset of the study. Therefore, although all diets had been formulated to contain the same calculated NPP of 0.35% by variable addition of feed-grade monobasic Ca phosphate (CaH4[PO4]2·H2O), differences between formulated and analyzed phytate P levels of the diets resulted in the analyzed diet NPP values of the HP Prolina diets being higher (0.40%) than the commercial and LP SBM diets (0.31 and 0.32%, respectively).
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Apparent Prececal Digestibility and Output of P, Ca, and Phytate P at the Distal Ileum
The apparent prececal digestibility of P decreased in a curvilinear manner with increasing dietary Ca and was significantly higher for diets containing the LP SBM compared with either commercial or HP SBM (Table 4, Figure 1a). The apparent prececal P absorption per kilogram of DMI was not different between the commercial and LP SBM diets (Table 4, Figure 1b) but as a result of the higher analyzed NPP levels was greater in diets that contained HP Prolina SBM compared with diets with commercial or LP SBM. Further, a significant interaction of dietary Ca level and SBM source suggested that increasing dietary Ca concentration reduced the amount of prececal P absorbed at the distal ileum from the HP Prolina SBM more rapidly than from commercial or LP SBM, for which the response in P absorption and P output per kilogram of DMI at the distal ileum was similar (Table 4, Figure 1b,c).
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). However, differences in the initial diet phytate P intake per kilogram of DMI resulted in more phytate P absorbed from HP Prolina and commercial SBM diets (Table 4, Figure 2a,b), whereas the output of intact phytate P in the excreta was lowest for the LP SBM (Table 5, Figure 2c). Increasing dietary Ca concentrations also increased the output of phytate P per kilogram of DMI at the distal ileum and was independent of the dietary phytate P concentration.
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). The prececal Ca digestibility increased 2-fold when dietary Ca level was increased from 0.47 to 1.16% (Table 4). However, in spite of more Ca being absorbed, the increase in dietary Ca from 0.47 to 1.16% also resulted in a significant stepwise increase in the output of Ca from the distal ileum from 2.78 g/kg to as high as 7.92 g/kg of DMI (Table 4). Total Retention and Excretion of P, Ca, and Phytate P in the Excreta During the First 24 h (Collection I) or After a 3-d Adaptation Period (Collection II)
There was a strong negative correlation between the percentage of P retention and the analyzed dietary phytate P concentration during both excreta collection I (r = –0.916; P < 0.0001) and during collection II (r = –0.922; P < 0.0001). During excreta collection I, the percentage of dietary P that was retained increased from 32.01 to 39.37% when commercial SBM replaced HP Prolina SBM in diets and to 53.78% when LP SBM replaced HP Prolina SBM (Table 5). After the 3-d adaptation period, the percentage of P retained during excreta collection II was 38.95, 46.89, and 63.37% for the HP Prolina, commercial, and LP SBM, respectively.
Increasing the dietary Ca level resulted in a linear increase in P retention during excreta collection I (Table 5), whereas the response in P retention to increasing Ca levels during excreta collection II differed among sources of SBM, which could be described by a quadratic function that reached a definite plateau (Figure 3a,b). Segmented regression analysis of the response in P utilization (i.e., retention and excretion) with increasing dietary Ca determined the breakpoint in the dietary Ca at which the plateau in P utilization was reached, which was 0.996 ± 0.057% Ca for the HP Prolina SBM diets, 0.739 ± 0.038% Ca for the commercial SBM, and 0.743 ± 0.053% Ca for the LP SBM diets (Figure 3a,b,c). Total P excretion per kilogram of DMI during collection II generally reflected differences in P retention, and the significant interaction of SBM and Ca level suggested that the initial reduction in excreta P output per kilogram of DMI with increasing dietary Ca concentration differed among sources of SBM, being lower for diets that contained LP SBM (Figure 3c). There was no interaction of dietary Ca level and source of SBM for phytate P output per kilogram of DMI in the excreta from collection II, but phytate P was 4-fold lower when LP SBM, rather than HP Prolina SBM, was included in the diet.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The higher determined NPP concentration of the HP Prolina SBM diets was unintentional and resulted from a lower-than-expected analyzed phytate concentration determined in a sample of SBM that was drawn when diets were mixed, compared with a previous sample drawn from the HP Prolina SBM 14 mo earlier. It was not known if the differences in analyzed phytate in the HP Prolina SBM were due to sampling error or if there had been some hydrolysis of the phytate to lower-order IP esters during storage.
Phytate P Disappearance and Apparent Digestibility of P at the Distal Ileum
The antagonism of dietary Ca on the apparent digestibility and absorption of P from the small intestine has been well established and was shown to be dependent on both the absolute Ca and P concentrations and the ratio of Ca to P in the diet (Hurwitz and Bar, 1971; Van der Klis and Versteegh, 1996). Several other studies have also found reduced P digestibility (Al-Masri, 1995), broiler performance, and bone mineralization (Waldroup et al., 1963b; Qian et al., 1997; Driver et al., 2005) when the Ca:P ratio was widened in diets with low levels of P. The negative effect of Ca on the apparent digestibility of P in the intestines has been thought to result from 2 potential mechanisms. In the first instance, elevated concentrations of dietary Ca were hypothesized to increase the formation of insoluble Caphytate complexes that reduced phytate P hydrolysis by endogenous or exogenous phytase enzymes (Nelson, 1980; Wise, 1983; Qian et al., 1997). Second, excess Ca relative to inorganic P increased the formation of inorganic Ca-P precipitates, which decreased the concentrations of soluble forms of P in the intestinal lumen and reduced P digestibility (Hurwitz and Bar, 1971). Given these 2 separate mechanisms whereby dietary Ca could potentially reduce the apparent digestibility of P, we hypothesized at the onset of this study that the response in apparent prececal P digestibility and overall P utilization (retention and excretion) to increasing dietary Ca concentration may be different when diets contained different concentrations of phytate.
There was no interaction of dietary Ca and phytate from SBM on apparent P digestibility, which improved from 51.69 and 52.54% to 65.44% when LP SBM was included in diets in place of either commercial SBM or HP Prolina, respectively (Table 4). The effects of Ca and phytate concentration on ileal P digestibility and absorption can be evaluated by comparing the response of the LP SBM and commercial SBM diets. The respective analyzed concentrations of NPP were 0.32 and 0.31%, whereas diets with LP SBM and commercial SBM had large differences in the concentration of phytate P (0.10 and 0.24%, respectively) and large differences in the levels of added monobasic Ca phosphate (0.59 or 1.09%, respectively). In spite of the substantial differences in the phytate P of the commercial and LP SBM diets, there was no difference in the rate at which prececal P digestibility or absorption was reduced when dietary Ca was increased from 0.47 to 1.16%. The observed reduction in P digestibility with increasing Ca was consistent with previous research (Van der Klis and Versteegh, 1996). Importantly, at the same analyzed NPP level, the inclusion of the LP SBM in place of commercial SBM resulted in similar amounts of P absorbed per kilogram of DMI but decreased total P output in the excreta by 49%. This suggested that the inclusion of the LP SBM in diets was able to replace the additional 0.12% P from monobasic Ca phosphate that had been added to commercial SBM diets to maintain a similar level of dietary NPP.
The higher apparent P absorption per kilogram of DMI in diets containing the HP Prolina SBM and the significant interaction observed between Ca and SBM source for apparent P absorption per kilogram of DMI were most likely caused by the higher analyzed NPP concentration in the HP Prolina SBM that resulted in a more rapid decrease in apparent P absorption when dietary Ca concentrations were increased. The improved P digestibility and retention of P in diets containing LP SBM were consistent with previous studies that compared LP vs. conventional sources of SBM (Sands et al., 2003), corn (Li et al., 2000), and barley (Thacker et al., 2003). In contrast to these findings, Dilger and Adeola (2006) found no significant difference in the apparent prececal P digestibility of LP or conventional SBM, which was 85 and 82.6%, respectively. However, in the study by Dilger and Adeola (2006), diets contained no added Ca or P from inorganic mineral sources. Tamin et al. (2004) showed that in the absence of added Ca from CaCO3 to diets, broilers were able to hydrolyze 69.2% of the dietary phytate P, which was reduced to 25.4% when 0.5% Ca from CaCO3 was added to a corn-soy diet. Therefore, in the study of Dilger and Adeola (2006), the absence of added Ca and inorganic P sources would presumably have facilitated a high rate of phytate P hydrolysis, which may have ameliorated any differences in P digestibility between sources of SBM with low or high concentrations of phytate P.
In our study, the mean disappearance of phytate P at the distal ileum when diets contained 0.47% Ca was 20.15% (Table 4), which was lower than the previous estimates of Leske and Coon (1999) of 34.9% in diets with 0.5% Ca. The lower phytate P hydrolysis in our study was most likely due to the younger age of birds and the inclusion of higher levels of NPP, both of which have been shown to reduce the extent of phytate P utilization by broilers (Nelson, 1980; Van der Klis and Versteegh, 1996). Based on a lower percentage of phytate hydrolysis with increased dietary Ca, Wise (1983) suggested that the M-ratio of Ca:phytate in diets was one of the main factors determining the fate of phytate P. At a single level of dietary Ca, diets containing LP SBM in the present study would have had a M-ratio of Ca:phytate P in the intestine over 2-fold higher than diets containing the commercial or HP Prolina SBM. However, this increase in the Ca:phytate ratio did not affect the mean percentage of phytate P disappearance by the time digesta had reached the distal ileum. However, in agreement with previous findings (Nelson and Walker, 1963; Van der Klis and Versteegh, 1996; Tamin et al., 2004), a high dietary Ca concentration linearly decreased the percentage of disappearance of phytate P at the distal ileum, which would have contributed to the decrease from 64.32 to 50.50% in the apparent prececal digestibility of P at the highest level of dietary Ca. Therefore, these data suggested that the percentage of dietary phytate hydrolyzed in the small intestine may be affected to a greater extent by the concentration of Ca added to diets as CaCO3 than by the ratio of Ca:phytate.
Effects of Ca:NPP Ratio and Phytate P Concentration on Overall P Retention
Although low levels of dietary Ca consistently increased phytate hydrolysis and the amount of P absorbed from the intestines, overall P retention responded positively to increasing dietary Ca concentrations and reached a plateau after which no further improvements occurred. This was consistent with previous observations by Van der Klis and Versteegh (1996), who showed that increasing the dietary Ca concentration reduced the digestibility of P at the ileum but increased the overall retention of P. These opposing effects of Ca on P digestibility vs. P retention at low dietary Ca levels could be attributed to an imbalance in the Ca:P ratio that was absorbed by the terminal ileum. Therefore, although lower dietary Ca levels increased phytate hydrolysis and P absorption in the intestines, the concurrent increase in P excretion suggested that there was insufficient Ca to allow the incorporation of the P into bone. Because the kidney plays an important role in the regulation of Ca and P levels in the plasma (Al-Masri, 1995), any excess circulating P would have been excreted in the urine, which was reflected in the higher total P in the excreta and reduced P retention at low dietary Ca concentrations.
Segmented regression analyses estimated the optimum Ca concentration at which P retention was maximized to be 0.74% Ca when diets contained commercial SBM (0.31% NPP) or LP SBM (0.32% NPP). Maximum P retention was reached in the HP Prolina SBM diet at 1.00% dietary Ca, but mean analyzed NPP levels of these diets were also higher (0.40% NPP). Therefore, the Ca:NPP ratio at which P retention was maximized was approximately 2.53:1 for the HP Prolina SBM diets, 2.40:1 for the commercial SBM diets, and 2.34:1 for the LP SBM diets.
The Ca:NPP ratio for maximum P retention and minimal P excretion estimated in the present study was similar to the optimal Ca:available P ratio of 2.2:1 and 2.3:1 estimated by Van der Klis and Versteegh (1996) for LP and HP diets, respectively. Also, a Ca:NPP ratio of 2.22:1 can be calculated from the NRC (1994) estimate of the Ca and NPP requirements of 1.00 and 0.45%, respectively, for 0-to 3-wk-old broilers.
The absence of any clear effect of dietary phytate concentration on Ca digestibility and retention was in contrast to earlier observations that the Ca requirement of 3-wk-old chicks was increased by at least 50% when dietary phytate levels were increased from 0.0 to 1.25% (Nelson et al., 1968b). The increased Ca requirement demonstrated in the study by Nelson et al. (1968b) was hypothesized to be caused by increased binding of Ca in the intestine, because 1% phytate was found to be able to bind 0.36% Ca. The differences in the effects of phytate on Ca digestibility observed in the present study may be attributed to lower phytate concentrations from SBM. The large range in phytate of 1.25% in the study by Nelson et al. (1968b) was obtained by adding sodium phytate to semisynthetic diets, which may have contributed to the reported effects of phytate on the dietary Ca requirement.
In conclusion, the present study suggested that although including LP SBM significantly increased ileal digestibility of P, there was no effect of phytate level on Ca digestibility. Ileal P digestibility decreased when dietary Ca increased from 0.47 to 1.16%. In contrast, a minimum level of dietary Ca was required for retention of P that had been absorbed in the intestines. The optimum ratio of Ca:NPP at which P retention was maximized was dependent upon the dietary phytate level, increasing from 2.3:1 to 2.5:1 when phytate P increased from 0.10 to 0.28%. Further research may be needed to ascertain the effects of such a wide Ca:P ratio on long-term broiler performance and economic returns.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Received for publication June 5, 2007. Accepted for publication November 23, 2007.
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REFERENCES |
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