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Diets Containing Escherichia coli-Derived Phytase on Young Chickens and Turkeys: Effects on Performance, Metabolizable Energy, Endogenous Secretions, and Intestinal Morphology

V. Pirgozliev^*,1, O. Oduguwa^*,2, T. Acamovic^* and M. R. Bedford

^* Avian Science Research Centre, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, Scotland; and Syngenta Animal Nutrition Inc., Chestnut House, Beckhampton, Marlborough, Wiltshire SN8 1QJ, UK

¹ Corresponding author: vasil.pirgozliev{at}sac.ac.uk

	ABSTRACT

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The aim of this experiment was to compare the responses of young broiler chickens directly with the responses of turkeys to different dietary phytase concentrations. Nine hundred sixty birds (480 female Ross 308 broilers, and 480 female BUT6 turkeys) were reared in 64 floor pens from 0 to 21 d of age. Each species was fed a nutritionally complete (12.79 MJ/kg of AME, 231 g/kg of CP vs. 11.75 MJ/kg of AME, 285 g/kg of CP for chickens and turkeys, respectively), low-P (28 and 37 g/kg available P for chickens and turkeys, respectively) corn (maize)-soy feed supplemented with either 0, 250, 500, or 2,500 phytase units (phytase/kg of feed) to give a total of 4 diets per species. The study was conducted in a split-plot design and each dietary treatment was replicated 8 times. Performance, AME, sialic acid (SA) excretions, and ileal villus morphology of 21-d-old broiler chickens and turkeys were determined. Overall, chickens grew faster and consumed more than turkeys throughout the study period. Dietary enzyme concentrations linearly increased the feed intake and weight gain of birds. The results were improved, on average, as follows: feed intake by 11.2 and 6.5%, gain by 10.2 and 13.2%, feed efficiency by 0 and 7.6%, AME by 1.4 and 5.7%, and AME intake by 13.1 and 9.8% for chickens and turkeys, respectively. The AME data were subject to a species x phytase interaction, whereby increasing the phytase dosage led to significant increments in parameters for turkeys but not broilers; broilers recovered significantly more energy from the ration than did turkeys. A quadratic relationship existed between dietary AME and phytase concentrations. Turkeys excreted more SA than did chickens in the absence of phytase, whereas supplementation with phytase (250 and 500 phytase units) reduced the excretion of SA in turkeys. Enzyme supplementation did not affect the ileal villus morphometry of the 2 species. We concluded that both species can tolerate phytase concentrations much higher than 1,000 phytase units and that these concentrations have further beneficial effects compared with lower phytase concentrations. The work reported here supports the hypothesis that supplementing turkey diets with phytase will need to be considered independently of chicken diets, considering the components in the diets, such that optimal responses can be obtained.

Key Words: phytase • chicken • turkey • performance • endogenous excretion

	INTRODUCTION

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About two-thirds of the phosphorus present in cereals and legumes is in a complex form that includes phytic acid and phytates (myo-inositol hexakis-dihydrogenphosphate, IP6). Phytic acid is a fully phosphorylated myo-inositol ring that exists in a chair conformation in dilute solution but as crystals in grains, and which can have antinutritive properties (Johnson and Tate, 1969; Bryden et al., in press). Phytic acid chelates mineral cations and reduces the availability of these cations for animals (Cowieson et al., 2007; Bryden et al., 2007). Phytates also reduce the availability of dietary carbohydrates and amino acids in pigs and poultry, either directly through interaction with digestive enzymes or by interaction with proteins. It has been suggested that the efficacy and amount of endogenous phytase produced in the gastrointestinal tract (GIT) of monogastrics is insufficient to hydrolyze phytate to remove these effects. In addition, Cowieson et al. (2004a) reported that ingestion of phytic acid by poultry could increase the excretion of endogenous compounds, which may further impair the performance of poultry and exacerbate nutrient requirements.

Phytases (myo-inositol hexaphosphate phosphohydrolases) are enzymes that can hydrolyze the ester bonds between the phosphate groups and the inositol ring in phytates, increasing the dietary available P (Irving and Cosgrove, 1974; Cowieson et al., 2004a,b). Initially, poultry diets were supplemented with exogenous phytase to reduce the inclusion of inorganic P and allow better utilization of phytate-P (Nelson et al., 1971). However, later studies demonstrated that the benefits of using dietary phytases are not restricted to improving mineral retention, but also may improve performance, energy, and amino acid availability (Ravindran et al., 1999; Selle et al., 2000; Newkirk and Classen, 2001; Ravindran et al., 2001; Rutherfurd et al., 2002; Pirgozliev et al., 2005; Cowieson et al., 2006a,b).

Recent research (Cowieson et al., 2004b; Pirgozliev et al., 2005) has also demonstrated that supplementing diets with phytase significantly reduces the endogenous secretions, measured as sialic acid (SA), from the GIT of broiler chickens. Sialic acid is a generic term for a family of acidic monosaccharides found at the terminal ends of sugar chains attached to cell surfaces and to soluble glycoproteins (Angata and Varki, 2002). An increased concentration of SA is often associated with health problems such as cellular senescence, bacterial infections (e.g., Campylobacter), certain pathological conditions, and osmotic fragility. The most widely distributed SA is N-acetylneuraminic acid, which is believed to be a biosynthetic precursor of all other SA molecules. Sialic acid is associated with the gastrointestinal mucin (Montagne et al., 2000), so SA excretion can be used as an indicator of mucin losses from the GIT of experimental animals (Larsen et al., 1993). It has been hypothesized that reduced GIT secretion—and thus improved gut health in the presence of phytase—is one mechanism involved in the mode of action of dietary phytases (Cowieson et al., 2004b; Pirgozliev et al., 2005). Although a significant number of studies have shown the effect of phytase on most individual farmed poultry species, information comparing different species directly is lacking. Dietary phytase is known to improve nutrient availability and bird performance; however, it is not clear whether different species follow the same pattern of response. Rodehutscord and Dieckmann (2005) found that chickens, turkeys, ducks, and quail have different capacities to utilize plant P because of their different intestinal absorption characteristics and differences in endogenous P losses from the GIT among species. Phytate hydrolysis in the intestines also depends on the phytase activity of the feed ingredients (Eeckhout and De Paepe, 1994), intestinal pH (Simon and Igbasan, 2002), microflora (Kerr et al., 2000), and endogenous phytase activity (Maenz and Classen, 1998; Applegate et al., 2003), suggesting that feeding the same phytase concentrations can provoke different responses among species. The responses of different poultry species to phytases in the diet are commercially very important for optimizing the use of phytases for the individual species.

The objective of this experiment was to directly compare the responses of young broiler chickens and turkeys to different dietary phytase concentrations. Performance, AME, SA excretions, and ileal villus morphology of 21-d-old broiler chickens and turkeys were determined.

	MATERIALS AND METHODS

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Animal Ethics
The study was approved by The Animal Experimental Committee of SAC.

Diet Formulations
Eight cornsoy-based diets were prepared and were supplemented with an evolved Escherichia coli-derived phytase. Diets were manufactured to be nutritionally adequate for each of the species but were designed to have a relatively low P content (Table 1). The basal diets were supplemented with exogenous phytase (Quantum 2500 D, EC 3.1.3.26 [EC] ; Syngenta Biotechnology Inc., Research Triangle Park, NC) 250, 500, or 2500 phytase units (FTU; phytase activity, units per kilogram of diet), respectively. The enzyme was added to the diets in powder form by serial dilution, and all diets were fed as mash. All diets were supplied with 5 g/kg of TiO₂ as a marker.

Wire-meshed metabolic cages equipped with trays were used for excreta collection. At d 21, 3 birds from each floor pen were placed in a metabolic cage for 1 h and the excreta were collected from the trays.

DM Digestibility and ME Determination
The analytical methods used in this work were described elsewhere and are summarized briefly here (Cowieson et al., 2006a,b). Excreta were freeze-dried, milled (0.75 mm mesh), analyzed for Ti in feed, and analyzed by inductively coupled plasma spectrometry (Optima 4300 DV dual-view ICP-OE spectrometer; PerkinElmer, Beaconsfield, UK) after sulfuric acid digestion. The gross energy (GE) of feed and excreta was determined using a bomb calorimeter (Parr-1755; Parr Instrument Company, Moline, IL). The DM digestibility coefficient (DMD) was calculated using the following equation:

where Ti_excreta and Ti_feed are the concentrations of Ti in the excreta and diet, respectively. Apparent ME calculations were based on DMD results:

SA Determination
The concentration of fecal SA was determined by the periodate-resorcinol method as described by Jourdian et al. (1971). The method involves conversion of free and glycosidically bound SA to chromogenic substances by treatment with periodic acid followed by resorcinol. The color of the samples was stabilized by 2-methyl-propan-2-ol, and after centrifugation the absorbance of the supernatant was determined spectrophotometrically at 630 nm (Spectronic 301; Milton Roy Company, Ivyland, PA). This procedure detects total, free, and glycosidically bound N-acetyl neuraminic (sialic) acid.

Ileal Villus Morphometry
On d 21, 1 bird from 4 pens of each treatment was killed by cervical dislocation. Approximately 4 cm of the middle part of the ileum was sampled and stored for 2 wk in 10% formalin-buffered saline. The samples were embedded in paraffin wax, sectioned at approximately 5 µm, and 4 gut segments were fixed in each slide. Morphometric measurements were determined on 20 villi for each slide (stereo binocular microscope, Olympus, Tokyo, Japan; CCD camera and monitor, JVC, Tokyo, Japan; image analysis software, Bioscan Optimas 3.01 for Windows, Bioscan Inc., Edmonds, WA). The length of the villus was represented by the distance from the crypt opening to the tip on the right side of the villus, as explained by Sigleo et al. (1984). Villus thickness was measured at a point one-third from the villus tip.

Statistical Analysis
Statistical analyses were performed using the Genstat VII statistical software package (IACR Rothamstead, Hertfordshire, UK). Comparisons among performance, AME, DMD, SA, and ileal morphometry were performed by ANOVA (following a split-plot design). A regression analysis was used to test the relationships between AME of the feed, BW, dietary enzyme concentration, and excreted SA.

	RESULTS

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No health problems were associated with use of the enzyme throughout the experiment, and there were no obvious leg health problems. Mortality was low (< 1%) and not treatment associated.

The average weights of the chickens and turkeys at 21 d of age were 670 and 466 g, respectively. Chickens clearly grew faster (P < 0.001; Table 2) and consumed more (P < 0.05) than turkeys throughout the study period.

The concentration of excreted SA was higher (P < 0.05) in chickens than in turkeys (Table 2), and no relationship was found with enzyme concentrations, but there was a significant species x enzyme interaction (Table 2). For turkeys, the highest phytase activity (2,500 FTU) also apparently tended to increase the SA secretions by turkeys compared with birds fed diets with lower phytase activities. To reduce the effect of variation in DM intake, SA excretion was presented on a metabolic BW basis (W^0.75; Table 2). An interaction between species and phytase was also detected for SA excretion per W^0.75. It is notable that the loss of SA (W^0.75) was higher from turkeys than chickens in the absence of phytase, whereas supplementation with phytase (250 and 500 FTU) reduced (P < 0.05) the excretion of SA in turkeys. A negative linear relationship was observed between AME and SA excretion (r² = 0.62, P < 0.001; Figure 1). Although there was a trend (P = 0.196) for chickens to have longer villi compared with turkeys, enzyme supplementation did not significantly affect ileal villus morphometry of the 2 species (Table 2).

View larger version (10K): [in this window] [in a new window]   Figure 1. Relationship between dietary AME and sialic acid excretion for broiler chickens (•) and turkeys ().

	DISCUSSION

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It should be noted that the AME determined in the diets for chickens was higher than expected and thus may have limited improvements in performance. However, the extent of AME improvement (P = 0.003) upon phytase supplementation in this study is in agreement with previously published results for a corn-soy feed (Pirgozliev et al., 2005; Cowieson et al., 2006b). The quadratic relationship between dietary AME and phytase concentrations (r² = 0.43; P < 0.001) was similar to the pattern reported by Cowieson et al. (2006b). In the study reported here, birds fed diets with 500 FTU had higher overall AME, which is in accordance with the results of Cowieson et al. (2006b), who reported a maximum AME at 150 to 300 FTU, although phytase concentrations varied between 150 and 24,000 FTU. This pattern of AME response to phytase was explained by the reduced capacity of lower molecular weight inositol phosphate esters to interact with starches and stimulate an increase in endogenous losses (Cowieson et al., 2004a,b). The consequence of this is that most of the improvements in AME associated with phytase addition may be expected to be achieved by the removal of 1 or 2 phosphate groups, with further improvements increasingly unlikely as each subsequent phosphate is cleaved (Cowieson et al., 2006b). Although logical, however, this theory cannot explain the linear relationship between phytase activity and improved bird performance in this study. The theory of enzymatic breakdown of phytate compounds distinguishes between liberation of phytate molecules from complexes with other tissue components and enzymatic cleavage of phosphate residues on the myo-inositol ring (Zyla et al., 2004). The stepwise manner of dephosphorylation of IP6 (Venekamp et al., 1995; Greiner et al., 2000) will lead to a release of different myo-inositol isomers and phosphates. The conditions in the GIT of poultry are not ideal for phytase to function effectively, so the exogenous phytase will not be able to completely dephosphorylate dietary phytates. However, the increased amount of different myo-inositol isomers should be considered. Waagbo et al. (1998) demonstrated that feeding fish inositol-supplemented diets improved their performance. However, dietary myo-inositol did not provide an advantage when P-sufficient diets were fed to broiler chickens (Pearce, 1975; Zyla et al., 2004). Interestingly, when myo-inositol was added to P-deficient diets, it improved the weight gain of the birds (Zyla et al., 2004), suggesting that myo-inositol by itself acts as a growth promoter. The existence of inositol phosphates in biology has been known for over 80 yr (Posternak, 1919), and its biological importance is well documented (Irvine and Schell, 2001; Beemster et al., 2002; Fisher et al., 2002). However, there is a lack of information about the effect of inositol on nutrient availability and performance when fed to poultry. The performance results from this study suggest that increased phytase concentrations linearly increased the dephosphorylation of IP6, providing more myo-inositol isomers of lower relative molecule mass. The linear relationship between dietary enzyme concentrations and weight gain (r² = 0.88; P < 0.001)—because birds fed 2,500 FTU increased their weight gain by 19% compared with control—may be due to the reduced adverse effects of phytate but also to beneficial effects of inositol esters of lower relative molecule mass. Although the role of inositol in nutrition is not well understood, the results from this study support previous findings (Zyla et al., 2004). To study the mode of action of dietary phytases, more attention should be paid to myo-inositol isomers released after phytase activity.

In this study, no relationship was found between dietary AME and performance. It is not unusual that AME values do not adequately predict the nutritive quality of poultry feeds. Rose and Bedford (1995) and Ravindran et al. (1999) also did not observe a correlation between dietary AME and performance when broilers were fed plain or enzyme-supplemented wheat-based diets. The main criticism of AME is that it does not account for intermediate metabolism (Chudy, 2000). The lack of relationship between bird performance and dietary AME in this study supports the previous finding that although convenient, ME is not the best way to evaluate the nutritive quality of poultry feed (De Groote, 1974; Hoffmann and Schiemann, 1980; Emmans, 1994; Pirgozliev and Rose, 1999). Better performance of the birds fed phytase suggests that these birds can utilize more energy and protein from the feed; however, this cannot be detected by dietary AME, which suggests that intermediary metabolism is affected by phytases, thereby increasing dietary available (net) energy. This hypothesis is also supported by the average increase of the metabolizability coefficients of GE by 1.4 and 2.1% for broilers and turkeys, respectively, in comparison with a 13% improvement in weight gain for both species.

The results from ileal villus morphometry were similar to previous work (Langhout et al., 1999; Pirgozliev et al., 2001). Although not significantly different (P > 0.05), we noted that birds fed 500 FTU had a slightly increased villus width compared with all other birds. In support of this observation, Koutsos et al. (2005) also reported that when diets containing 600 FTU were fed to laying hens, there was an increase in the duodenal villus width. Perhaps the phytase influences the type of microflora within the GIT (Steer and Gibson, 2002), and thus their adherence and any damage that they may cause to the GIT.

The results for SA were in the ranges reported elsewhere (Cowieson et al., 2004b; Pirgozliev et al., 2005). Although no direct correlation was detected between SA excretion and supplemented phytase activities, there was a significant negative relationship between dietary AME (r² = 0.62; P < 0.001) and excreted SA per kilogram of metabolic BW. The negative relationship with dietary AME in this study suggests that phytase supplementation improves gut health. Mucins are rich in nitrogen and amino acids, so increased mucin production is nutritionally very expensive and inevitably leads to increased endogenous loss (Nyachoti et al., 1997) while increasing the energy for maintenance. It also should be mentioned that the untreated phytate in the control diets is likely to reduce the release of dietary minerals, starch, and amino acids within the GIT and leads to an unbalanced nutrient supply in the intestinal lumen. Cowieson et al. (2004b) demonstrated that phytic acid, a major component of dietary phytate, irritates the GIT and increases the excretion of endogenous amino acids, minerals, and SA. Phytates may irritate the gut wall directly or by enhancing the growth of intestinal microflora, causing inflammation and provoking further immune response and increased production of cytokines (McKay and Baird, 1999). However, activation of the immune system of the bird (e.g., increased production of antibodies in response of invading agents) is another energy-demanding process (Klasing, 1998; Klasing and Calvert, 1999; Eraud et al., 2005). It has also been suggested that a strong immune response will increase the risk of tissue damage (Svensson et al., 1998), increase the production of free radicals (Finkel and Holbrook, 2000), and cause further deleterious effects on the organism. Karadas et al. (2005, 2006) reported that broilers fed phytase-supplemented diets had reduced hepatic oxidative stress and increased antioxidant status compared with birds fed nonsupplemented diets low in P. It may be that the combination of an irritant and an unbalanced supply of nutrients will compromise the gut health of the birds and may help to explain the negative relationship (P < 0.001) between AME and excreted mucin, measured as SA in this study. However, it is difficult to explain the increased excretion of SA in turkeys fed 2,500 FTU although this tendency was also observed in chickens; it may be a function of feed intake and thereby confound the interpretation. Even though the mechanism is not clear, dietary phytases may be capable of reducing the immune response and production of free radicals in broiler chickens.

It can be concluded that both chickens and turkeys can tolerate phytase activities much higher than 1,000 FTU and that these have further beneficial effects compared with lower phytase activities. The results of this study show that dietary phytase influences secretions from the GIT and that these secretions are species and phytase activity dependent, which may alter gut health. However, to increase our knowledge regarding the mode of action of dietary phytases, further research on lower molecular mass myo-inositol isomers, immune response, and antioxidant stress should be completed. Furthermore, the work reported here supports the hypothesis that supplementation of turkey diets needs to be considered independently from supplementation of chicken diets so that optimal responses can be obtained.

	ACKNOWLEDGMENTS

 
The SAC receives funding from the Scottish Executive Environment and Rural Affairs Department (SEERAD). O. Oduguwa is grateful for financial support from the Commonwealth Fellowship Commission in the UK and the University of Agriculture, Abeokuta, Nigeria.

	FOOTNOTES

 
² Visiting scientist from the University of Agriculture, P.M.B. 2240, Abeokuta, Nigeria.

Received for publication June 29, 2006. Accepted for publication November 18, 2006.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Angata, T., and A. Varki. 2002. Chemical diversity in the sialic acids and related -keto acids: An evolutionary perspective. Chem. Rev. 102:439–469.[ISI][Medline]

Applegate, T. J., R. Angel, and H. L. Classen. 2003. Effect of dietary calcium, 25-hydroxycholecalciferol, or bird strain on small intestinal phytase activity in broiler chickens. Poult. Sci. 82:1140–1148.[Abstract/Free Full Text]

Beemster, P., P. Groenen, and R. Steegers-Theunissen. 2002. Involvement of inositol in reproduction. Nutr. Rev. 60:80–87.[ISI][Medline]

Bryden, W. L., P. H. Selle, V. Ravindran, and T. Acamovic. 2007. Phytate: An anti-nutritive factor in animal diets. Pages 279–284 in Poisonous Plants: Global Research and Solutions. K. E. Panter, T. L. Wieregna, and J. A. Pfister, ed. CABI Publishing, Wallingford, Oxon, UK.

Chudy, A. 2000. Model for the interpretation of energy metabolism in farm animals. Pages 329–346 in Modelling Nutrient Utilization in Farm Animals. P. McNamara, J. France, and D. E. Beever, ed. CAB International, Wallingford, Oxfordshire.

Cowieson, A. J., T. Acamovic, and M. R. Bedford. 2004a. The effect of phytic acid and phytase on the digestibility of maize starch for growing broiler chickens. Poult. Sci. 83(Suppl. 1):1971. (Abstr.)

Cowieson, A. J., T. Acamovic, and M. R. Bedford. 2004b. The effects of phytase and phytic acid on the loss of endogenous amino acids and minerals from broiler chickens. Br. Poult. Sci. 45:101–108.[ISI][Medline]

Cowieson, A. J., T. Acamovic, and M. R. Bedford. 2006a. Phytic acid and phytase: Implications for protein utilization by poultry. Poult. Sci. 85:878–885.[Abstract/Free Full Text]

Cowieson, A. J., T. Acamovic, and M. R. Bedford. 2006b. Supplementation of corn-soy-based diets with high concentrations of an Escherichia coli-derived phytase: Effects on broiler chick performance and the digestibility of amino acids, minerals, and energy. Poult. Sci. 85:1389–1397.[Abstract/Free Full Text]

De Groote, G. 1974. A comparison of a new net energy system with the metabolizable energy system in broiler diet formulation, performance and profitability. Br. Poult. Sci. 15:75–95.

Eeckhout, W., and M. De Paepe. 1994. Total phosphorus, phytate-phosphorus and phytase activity in plant feedstuffs. Anim. Feed Sci. Technol. 47:19–29.

Emmans, G. 1994. Effective energy: A concept of energy utilization applied across species. Br. J. Nutr. 71:801–821.[ISI][Medline]

Eraud, C., O. Duriez, O. Chastel, and B. Faivre. 2005. The energetic cost of humoral immunity in the collared dove, Streptopelia decaocto: Is the magnitude sufficient to force energy-based trade-offs? Funct. Ecol. 19:110–118.

Esteve-Garcia, E., A. M. Perez-Vendrell, and J. Broz. 2005. Phosphorus equivalence of a consensus phytase produced by Hansenula polymorpha in diets for young turkeys. Arch. Anim. Nutr. 59:53–59.[Medline]

Finkel, T., and N. Holbrook. 2000. Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247.[Medline]

Fisher, S. K., J. E. Novak, and B. W. Agranoff. 2002. Inositol and higher inositol phosphates in neutral tissues: Homeostasis, metabolism and functional significance. J. Neurochem. 82:736–754.[ISI][Medline]

Greiner, R., N.-G. Carlsson, and M. L. Alminger. 2000. Stereo-specificity of myo-inositol hexakisphosphate dephosphorylation by a phytate-degrading enzyme of Escherichia coli. J. Biotechnol. 84:53–62.

Hoffmann, L., and R. Schiemann. 1980. Von der Kalorie zum Joule: Neue Größenbeziehungen bei Messungen des Energieumsatzes und bei der Berechnung von Kennzahlen der energetischen Futterbewertung. Arch. Tierernähr. 30:733–742.

Irvine, F. R., and M. J. Schell. 2001. Back in the water: The return of the inositol phosphates. Nat. Rev. Mol. Cell Biol. 2:327–338.[ISI][Medline]

Irving, G. C., and D. J. Cosgrove. 1974. Inositol phosphate phosphatases of microbial origin. Some properties of the partially purified phosphatases of Aspergillus ficuum NRRL 3135. Aust. J. Biol. Sci. 27:361–368.[Medline]

Johnson, L. F., and M. E. Tate. 1969. The structure of myo-inositol pentaphosphates. Ann. N. Y. Acad. Sci. 165:526–532.[ISI][Medline]

Jourdian, G. W., L. Dean, and S. Roseman. 1971. A periodate-resorcinol method for the quantitative estimation of free sialic acids and their glycosides. J. Biol. Chem. 246:430–435.[Abstract/Free Full Text]

Karadas, F., V. R. Pirgozliev, T. Acamovic, and M. R. Bedford. 2005. The effects of dietary phytase activity on the concentration of coenzyme Q₁₀ in the liver of young turkeys and broilers. Br. Poult. Abstr. 1:1–2.

Karadas, F., V. R. Pirgozliev, A. Pappas, T. Acamovic, and M. R. Bedford. 2006. The effects of dietary phytase on the concentration of antioxidants including coenzyme Q₁₀ in the liver of growing broilers. Br. Poult. Abstr. 2:18–19.

Kerr, M. J., H. L. Classen, and R. W. Newkirk. 2000. The effects of gastrointestinal tract micro-flora and dietary phytase on inositol hexaphosphate hydrolysis in the chicken. Poult. Sci. 79(Suppl. 1):11. (Abstr.)

Kornegay, E. T. 1996. Effect of Natuphos phytase on protein and amino acid digestibility and nitrogen retention of poultry. Pages 493–514 in Phytase in Animal Nutrition and Waste Management. M. B. Coelho and E. T. Kornegay, ed. BASF Corporation, Mount Olive, NJ.

Koutsos, E. A., C. L. Wyatt, and P. D. Bass. 2005. Effect of dietary phytase level and source on second cycle commercial lying hens. I. Effects on hen body weight, carcass composition and intestinal histology. Page 16 in Int. Poult. Sci. Forum Abstracts, January 24–25, Atlanta, GA. (Abstr.)

Klasing, K. C. 1998. Nutritional modulation of resistance to infectious diseases. Poult. Sci. 77:1119–1125.[Abstract/Free Full Text]

Klasing, K. C., and C. C. Calvert. 1999. The care and feeding of an immune system: An analysis of lysine needs. Pages 253–264 in Proc. VIIIth Int. Symp. Protein Metab. and Nutr. G. Lobley, A. White, and C. MacRae, ed. Aberdeen, UK, September 1–4. Wageningen Press, the Netherlands.

Langhout, D. J., J. B. Schutte, P. V. Van Leeuwen, J. Wiebenga, and S. Tamminga. 1999. Effect of dietary high- and low-methylated citrus pectin on the activity of the ileal microflora and morphology of the small inteastinal wall of broiler chickens. Br. Poult. Sci. 40:340–347.[ISI][Medline]

Larsen, F. M., P. J. Moughan, and M. N. Wilson. 1993. Dietary fiber viscosity and endogenous protein excretion at the terminal ileum of growing rats. J. Nutr. 123:1898–1904.[Abstract/Free Full Text]

Ledoux, D. R., J. N. Broomhead, and I. Kühn. 2005. Efficacy and safety of a novel phytase in turkeys fed diets to market weight. Pages 198–200 in Proc. 15th Eur. Symp. Poult. Nutr., Balatonfured, Hungary, September 25–29. F. Bogenfurst, K. Dublecz, P. Horn, M. Mezes, A. Molnar, and M. Vetesi, ed. World’s Poult. Sci. Assoc., Hungarian Branch, Budapest.

Maenz, D. D., and H. L. Classen. 1998. Phytase activity in the small intestinal brush border membrane of the chicken. Poult. Sci. 77:557–563.[Abstract/Free Full Text]

McKay, D. M., and A. W. Baird. 1999. Cytokine regulation of epithelial permeability and ion transport. Gut 44:283–289.[Free Full Text]

Montagne, L., R. Toullec, and J. P. Lalles. 2000. Calf intestinal mucin: Isolation, partial characterization, and measurement in ileal digesta with an enzyme-linked immunosorbent assay. J. Dairy Sci. 83:507–517.[Abstract]

NRC (National Research Council). 1994. Nutrient Requirements of Poultry. National Academy Press, Washington, DC.

Nelson, T. S., T. R. Shien, R. J. Wodzinski, and J. H. Ware. 1971. Effect of supplemental phytase on the utilization of phytate phosphorus by chicks. J. Nutr. 101:1289–1294.[Abstract/Free Full Text]

Newkirk, R. W., and H. L. Classen. 2001. The non-mineral impact of phytate in canola meal fed to broiler chicks. Anim. Feed Sci. Technol. 91:115–128.

Nyachoti, C. M., C. F. M. de Lange, B. W. McBride, and H. Schulze. 1997. Significance of endogenous gut nitrogen losses in the nutrition of growing pigs: A review. Can. J. Anim. Sci. 77:149–163.

Pearce, J. 1975. The effects of choline and inositol on hepatic lipid metabolism and the incidence of the fatty liver and kidney syndrome in broilers. Br. Poult. Sci. 16:565–570.[ISI][Medline]

Pirgozliev, V., O. Oduguwa, T. Acamovic, and M. R. Bedford. 2005. Effect of dietary phytase on performance, metabolizable energy and endogenous losses of broiler chickens. Pages 319–321 in Proc. 15th Eur. Symp. Poult. Nutr., Balatonfured, Hungary, September 25–29. F. Bogenfurst, K. Dublecz, P. Horn, M. Mezes, A. Molnar, and M. Vetesi, ed. World’s Poult. Sci. Assoc., Hungarian Branch, Budapest.

Pirgozliev, V. R., and S. P. Rose. 1999. Net energy systems for poultry feeds: A quantitative review. World’s Poult. Sci. J. 55:23–36.

Pirgozliev, V., S. P. Rose, P. S. Kettlewell, and M. R. Bedford. 2001. Dietary amylose:amylopectin ratio in starch for broiler chickens. Br. Poult. Sci. 42:S122–S123.

Posternak, S. 1919. Sur la synthese de l’ether hexaphosphorilique de l’inosite avec le principle phosphoorganique de reserve des plantes vertes. Compt. Rend. Acad. Sci. 169:138–140.

Ravindran, V., S. Cabahug, G. Ravindran, and W. L. Bryden. 1999. Influence of microbial phytase on apparent ileal amino acid digestibility of feedstuffs for broilers. Poult. Sci. 78:699–706.[Abstract/Free Full Text]

Ravindran, V., P. H. Selle, G. Ravindran, P. C. H. Morel, A. K. Kies, and W. L. Bryden. 2001. Microbial phytase improves performance, apparent metabolizable energy, and ileal amino acid digestibility of broilers fed a lysine-deficient diet. Poult. Sci. 80:338–344.[Abstract/Free Full Text]

Rodehutscord, M., and A. Dieckmann. 2005. Comparative studies with three-week-old chickens, turkeys, ducks, and quails on the response in phosphorus utilization to a supplementation of monobasic calcium phosphate. Poult. Sci. 84:1252–1260.[Abstract/Free Full Text]

Rose, S. P., and M. R. Bedford. 1995. Relationship between the metabolizable energies of wheat samples and the productive performance of broilers. Br. Poult. Sci. 36:864–865.

Rutherfurd, S. M., T. K. Chung, and P. J. Moughan. 2002. The effect of microbial phytase on ileal phosphorus and amino acid digestibility in the broiler chicken. Br. Poult. Sci. 44:598–606.

Selle, P. H., V. Ravindran, R. A. Caldwell, and W. L. Bryden. 2000. Phytate and phytase: Consequences for protein utilization. Nutr. Res. Rev. 13:255–278.

Sigleo, S., M. Jackson, and G. Vahouny. 1984. Effects of dietary fiber constituents on intestinal morphology and nutrient transport. Am. J. Physiol. 246 (Gastrointest. Liver Physiol. 9):G34–G39.

Simon, O., and F. Igbasan. 2002. In vitro properties of phytases from various microbial origins. Int. J. Food Sci. Technol. 37:813–822.

Steer, T. E., and G. R. Gibson. 2002. The microbiology of phytic acid metabolism by gut bacteria and relevance for bowel cancer. Int. J. Food Sci. Technol. 37:783–790.

Svensson, E., L. Ra °berg, C. Koch, and D. Hasselquist. 1998. Energetic stress, immunosuppression and the costs of an antibody response. Funct. Ecol. 12:912–919.

Venekamp, J., A. Tas, and W. A. C. Somers. 1995. Developments in phytase activity determination: An NMR-approach. Pages 151–156 in Proc. 2nd Eur. Symp. Feed Enzymes. W. van Hartingsveldt, M. Hessing, J. P. van der Lugt, and W. A. C. Somers, ed. Wageningen Press, the Netherlands.

Waagbo, R., K. Sandnes, and Ø. Lie. 1998. Effects of inositol supplementation on growth, chemical composition and blood chemistry in Atlantic salmon, Salmo salar L., fry. Aqua-cult. Nutr. 4:53–59.

Zyla, K., M. Mika, B. Stodolak, A. Wikiera, J. Koreleski, and S. Swiatkiewicz. 2004. Towards complete dephosphorylation and total conversion of phytates in poultry feeds. Poult. Sci. 83:1175–1186.[Abstract/Free Full Text]

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