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The Effect of Levels of -Galactosidase Enzyme on Performance of Broilers Fed Diets Based on Corn and Soybean Meal1
P. W. Waldroup,2 C. A. Keen, F. Yan, and K. Zhang Department of Poultry Science, University of Arkansas, Fayetteville, AR 72701
DESCRIPTION OF PROBLEM
Soybean meal (SBM) is widely recognized as a high-quality protein source and is the leading protein supplement for poultry diets in the United States, Brazil, and many other major poultry-producing countries. Approximately
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one-third of SBM is carbohydrate, and the digestibility of this fraction by poultry is considered very poor. Honig and Rackis [1] noted that the carbohydrate fraction is made up almost equally of various oligosaccharides and polysaccharides. The polysaccharides make up approximately 15 to 18% of SBM. The starch
Published with approval of the Director, Arkansas Agricultural Experiment Station, Fayetteville AR 72701. Mention of a trade name, proprietary product, or specic equipment does not constitute a guarantee or warranty by the University of Arkansas and does not imply its approval to the exclusion of other products that may be suitable. 2 Corresponding author: waldroup@uark.edu
WALDROUP ET AL.: BROILER PERFORMANCE content is very low (<0.5%); thus, most of the polysaccharides are acidic polysaccharides, arabinogalactan, and cellulosic material, which are essentially nondigestible. The oligosaccharide fraction makes up approximately 15% of the meal and contains 7.4 to 9.9% sucrose, 4.7 to 4.8% stachyose, 1.0 to 1.1% rafnose, and traces of verbascose [2, 3, 4, 5, 6, 7, 8]. Sucrose is highly digestible by poultry, but the others are considered poorly digestible. The poor digestibility of the oligosaccharide fraction leads to covert losses to the poultry industry. One of the most obvious is the loss of potential energy. Early studies to determine the metabolizable energy of common poultry feedstuffs indicate that SBM and dehulled SBM contain about 5 to 6% more gross energy than corn but 54 and 42% less metabolizable energy, respectively [9, 10, 11, 12]. This nding indicates that some component of the 2 SBM are poorly digested and metabolized. Numerous studies indicate that the protein fraction of SBM is highly digested, in the range of 87 to 99% [13, 14, 15, 16, 17, 18, 19]. Few studies have directly determined the digestibility of the carbohydrate fraction of SBM. Pierson et al. [18] reported that male turkeys digested only 4% of the carbohydrate in dehulled SBM; however, after adjusting for the uric acid and other N-containing metabolic end products the N-free extract of the SBM was calculated to be about 61% digested [20]. Carbohydrates in SBM are reported to be 40% available in chicks [21]. The -galactosides of sucrose (rafnose, stachyose, and verbascose) cannot be broken down in the small intestine of monogastric animals due to the absence of endogenous -(1,6)galactosidase [22]. In addition to loss of potential energy to the chick, the presence of these sugars in the gastrointestinal tract may cause additional problems related to uid retention and increased ow rate that could adversely affect the overall nutrient use [23]. Numerous studies have evaluated different approaches to overcoming the adverse effects of oligosaccharides in SBM, including extraction by various means, breeding varieties with lower oligosaccharide content, and application of exogenous enzymes with considerable controversy regarding the nutritional signicance
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of the oligosaccharides. Removal of the -galactosides using ethanol extraction resulted in an improvement in digestion of nonstarch polysaccharide and an increase of up to 20.5% in the TMEn of SBM [24, 25, 26, 27]. However, it has been pointed out that interpretation of these data is confounded by the simultaneous extraction of other meal components [28]. Parsons et al. [29] evaluated several genetic lines of soybeans selected for low levels of rafnose and stachyose compared with those found in conventional soybeans. The 2 soybean lines with the lowest total rafnose, stachyose, and galactinol levels had average TMEn values that were 9.8% higher than their respective genetic controls. In contrast to these results, the removal of oligosaccharides using endogenous soybean galactosidase failed to produce any benecial effects on the apparent nutritional value of soy akes, as measured by growth rate and feed conversion and by AMEn studies with young broilers and TMEn studies with adult roosters [30]. Irish et al. [28] used ethanol extraction and incubation of SBM with -galactosidase to decrease the concentrations of -galactosides in SBM from 6.50 to 0.81 and 1.43%, respectively. However, there were no improvements in TMEn when those meals were precision fed to adult cockerels. Irish et al. [28] concluded that removal of up to approximately 90% of the -galactosides of sucrose has no benecial effect on the nutritional value of SBM for chickens. Addition of exogenous -galactosidase enzymes to soybean-based diets for chicks has led to variable results [31, 32, 33, 34, 35, 36]. In a previous report from our laboratory [37] we were unable to detect an improvement in the energy value of SBM as a result of addition of -galactosidase enzyme, alone or in the presence of Avizyme 1502. In these studies the galactosidase enzyme was added at the rate suggested by the supplier and was estimated to provide 45 -galactosidase units (GALU) [38]/ kg of SBM. Knap et al. [34] observed a dose response relationship to their specic product to elicit an 8% improvement in the metabolizable energy of SBM. Therefore, the objective of the present study was to evaluate usage levels
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Table 1. Composition (g/kg) and calculated nutrient content of broiler diets with and without a 10% assumed increase in metabolizable energy from soybean meal (SBM) as a result of enzyme supplementation Enzyme added to diet Starter Ingredient Yellow corn Dehulled SBM Poultry oil Dicalcium phosphate Ground limestone Vitamin premix1 Iodized salt Sodium bicarbonate DL-Methionine L-Lysine HCl Trace minerals2 L-Threonine Coban-603 BMD-504 Lincomycin5 Enzyme or sand6 Total ME, kcal/kg (adjusted)7 ME, kcal/kg (unadjusted)8 CP, % Ca, % Nonphytate P, % Met, % Lys, % Trp, % Thr, % TSAA, % Na, %
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Grower Yes 582.63 344.00 24.07 17.10 12.45 5.00 4.31 2.00 2.68 1.14 1.00 0.31 0.75 0.50 0.00 2.06 1,000.00 3,085.57 3,003.06 22.03 0.92 0.44 0.59 1.30 0.26 0.88 0.98 0.25 No 598.43 315.38 42.34 15.23 10.87 5.00 4.32 2.00 2.64 1.05 1.00 0.49 0.75 0.50 0.00 0.00 1,000.00 3,140.70 3,140.70 20.77 0.82 0.40 0.57 1.21 0.25 0.85 0.94 0.25 Yes 613.48 312.66 28.08 15.20 10.90 5.00 4.31 2.00 2.63 1.11 1.00 0.50 0.75 0.50 0.00 1.88 1,000.00 3,140.64 3,065.62 20.77 0.82 0.40 0.57 1.21 0.25 0.84 0.94 0.25 No
Finisher Yes 665.67 260.02 30.91 13.36 12.09 5.00 4.30 2.00 2.20 0.56 1.00 0.33 0.00 0.00 1.00 1.56 1,000.00 3,195.81 3,133.43 18.55 0.81 0.36 0.51 1.02 0.22 0.74 0.84 0.25
No 566.05 346.99 39.75 17.14 12.42 5.00 4.32 2.00 2.70 1.08 1.00 0.30 0.75 0.50 0.00 0.00 1,000.00 3,085.57 3,085.57 22.03 0.92 0.44 0.60 1.30 0.27 0.88 0.98 0.25
653.16 262.28 42.76 13.39 12.06 5.00 4.31 2.00 2.21 0.51 1.00 0.32 0.00 0.00 1.00 0.00 1,000.00 3,195.81 3,195.81 18.55 0.81 0.36 0.51 1.02 0.22 0.74 0.84 0.25
Provided per kilogram of diet: vitamin A, 7,714 IU; cholecalciferol, 2,204 IU; vitamin E, 16.53 IU; vitamin B12, 0.013 mg; riboavin, 6.6 mg; niacin, 39 mg; pantothenic acid, 10 mg; menadione, 1.5 mg; folic acid, 0.9 mg; choline, 1,040 mg; thiamin, 1.54 mg; pyridoxine, 2.76 mg; D-biotin, 0.066 mg; ethoxyquin, 125 mg; Se, 0.1 mg. 2 Provides per kilogram of diet: Mn (from MnSO4 H2O), 100 mg; Zn (from ZnSO4 7H2O), 100 mg; Fe (from FeSO4 7H2O), 50 mg; Cu (from CuSO4 5H2O), 10 mg; I from Ca(IO3)2 H2O), 1 mg. 3 Elanco Animal Health division of Eli Lilly & Co., Indianapolis, IN. 4 Alpharma, Inc., Ft. Lee, NJ. 5 Pzer Inc., New York, NY. 6 Quantity of enzyme supplementation or washed builders sand. 7 Energy value from assumed increase in ME from enzyme treatment of SBM. 8 Energy value based on standard SBM and assuming no improvement from enzyme.
5 broiler producers in a leading agricultural survey [39]. No animal protein was used so as to allow for maximum usage of SBM. The diets were formulated to be isocaloric within each age period, based on an assumed increase of 10% in energy content of the SBM. Corn and SBM of known moisture and crude protein content were used as intact sources of crude protein with nutrient values adjusted accordingly. In formulating the test diets, SBM was assigned different energy values based on the premise
WALDROUP ET AL.: BROILER PERFORMANCE that the addition of the enzyme would improve the energy value of the SBM by 0 or 10%, based on the reports of Knap et al. [34], Ghazi et al. [32], and Graham et al. [33]. A similar approach was used by Mendonca and Jensen [40] for evaluating the metabolizable energy content of poultry by-product meal in broiler diets. For normal SBM, the assigned ME value in this study was 2,399 kcal/kg, and for the improved SBM the assigned ME value was 2,639 kcal/kg. The diet with normal ME values for SBM (positive control) was formulated at an energy level consistent with the addition of approximately 4% poultry oil. Composition of the diets is shown in Table 1. A large batch of the negative control diet was prepared and divided into aliquots for blending with the enzyme. The supplier of the enzyme recommends a usage level of 1.5 g enzyme/kg of SBM. Portions of the negative control diet were supplemented with the -galactosidase enzyme product [41] at the rate of 0, 1.5, 3.0, 4.5, or 6.0 g enzyme/kg of SBM used in the diet to provide approximately 0, 45, 90, 135, or 180 GALU/kg of SBM by assigning constant ingredient ratios in a commercial feed formulation program [42]. Inert ller (washed builders sand) was added as needed to adjust for differences in quantity of added enzyme. This resulted in 6 dietary treatments (positive control and negative control with 5 levels of enzyme). To avoid the possibility that the enzyme might be heat labile, diets were fed in mash form. Birds and Housing Male chicks of a commercial broiler strain [43] were obtained from a local hatchery where they had been vaccinated in ovo for Mareks disease and had received vaccinations for Newcastle disease and infectious bronchitis posthatch via a coarse spray. They were randomly assigned to litter-oor pens in a house of commercial design. New softwood shavings over concrete oors served as litter. Eight pens of 30 birds were assigned to each of the test diets and fed the test diets from 1 to 42 d of age with feed changes at 14 and 35 d. Care and management of the birds followed recommended guidelines [44]. Measurements
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Birds were group weighed by pen at 1, 14, 35, and 42 d of age, and feed consumption was measured. Any bird that died or was culled to remove possible suffering was weighed to adjust feed efciency (g of gain/g of feed consumed). From these data, mean body weights at 1, 14, 35, and 42 d were determined. Likewise, feed efciency was determined from 1 to 14, 1 to 35, and 1 to 42 d. From the calculated ME content of the diets, calorie consumption was estimated and calorie conversion ratios were calculated (kcal of ME/kg of gain). The calorie conversion was calculated 2 ways: one using the ME value of the diet assuming the energy of the SBM was improved by 10% from enzyme supplementation and one using the ME value of the diet assuming that the energy of the SBM was not improved by enzyme supplementation. Statistical Analysis Data were analyzed as a one-way ANOVA using the GLM option of SAS [45]. Signicant differences among means were separated by repeated t-tests using the least square means option of SAS. All statements of statistical signicance were based on P < 0.05.
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Table 2. Effects of 10% assumed increase in metabolizable energy from soybean meal (SBM) as the result of supplementation with -galactosidase enzyme on body weight of male broilers (means of 8 pens of 30 birds/pen) Enzyme addition (g/kg of SBM) soy soy soy soy soy ME2 ME ME ME ME 0 0 1.5 3.0 4.5 6.0 Body weight (kg) GALU1 (U/kg of SBM) 0 0 45 90 135 180 14 d 0.436 0.432 0.434 0.435 0.435 0.435 0.99 0.005 3.12 35 d 2.198 2.147 2.177 2.167 2.157 2.168 0.62 0.021 2.75 42 d 2.841 2.792 2.835 2.820 2.811 2.818 0.85 0.028 2.79
Treatment Positive control +10% increase in +10% increase in +10% increase in +10% increase in +10% increase in Probability > F SEM CV
1
One galactosidase unit (GALU) is the amount of enzyme that hydrolyzes 1 mmol of p-nitropheny--D-galactopyranoside/ min under standard conditions (pH 5.5; 37C; 15 min; optical density of 405 nm). 2 This diet is the negative control.
than the positive control with the exception of 42 d BW of birds fed the negative control diet with 45 GALU/kg of the -galactosidase enzyme. Feed efciency was not signicantly affected by dietary treatment (Table 3). Feed efciency by birds fed the negative control diet with no supplementation with -galactosidase was reduced by 0.26, 1.84, and 1.82% at 14, 35, and 42 d, respectively, compared with the positive control group. Addition of the enzyme had no consistent effect on feed efciency at any age period, even at levels that were 4 times in excess of the recommended level of 45 GALU/kg.
The poultry industry evaluates diets on the basis of caloric efciency; that is, the calories needed to produce a unit of gain. This value was calculated using 2 assumptions. The rst assumption was that there was no increase in the ME of the SBM as a result of supplementation with the -galactosidase enzyme, using the unadjusted energy values presented in Table 1. With the unadjusted energy values, there was a signicant improvement in caloric efciency at 14 d of age of birds fed the negative control diets as compared with those fed the positive control group (Table 4). However, the addition of the -galactosidase enzyme had no apparent benecial effect on further improvement in ca-
Table 3. Effects of 10% assumed increase in metabolizable energy from soybean meal (SBM) as the result of supplementation with -galactosidase enzyme on feed efciency by male broilers (means of 8 pens of 30 birds per pen) Enzyme addition (g/kg of SBM) soy soy soy soy soy ME2 ME ME ME ME 0 0 1.5 3.0 4.5 6.0 Gain:feed ratio GALU1 (U/kg of SBM) 0 0 45 90 135 180 114 d 0.768 0.766 0.770 0.766 0.774 0.760 0.73 0.006 2.16 135 d 0.651 0.639 0.640 0.640 0.635 0.637 0.09 0.004 1.76 142 d 0.606 0.595 0.601 0.599 0.597 0.601 0.18 0.003 1.42
Treatment Positive control +10% increase in +10% increase in +10% increase in +10% increase in +10% increase in Probability > F SEM CV
1
One galactosidase unit (GALU) is the amount of enzyme that hydrolyzes 1 mmol of p-nitropheny--D-galactopyranoside/ min under standard conditions (pH 5.5; 37C; 15 min; optical density of 405 nm). 2 This diet is the negative control.
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Table 4. Energy efciency by male broilers assuming no increase in metabolizable energy from soybean meal (SBM) as the result of supplementation with -galactosidase enzyme (means of 8 pens of 30 birds/pen) Enzyme addition (g/kg of SBM) soy soy soy soy soy ME2 ME ME ME ME 0 0 1.5 3.0 4.5 6.0 ME:gain (kcal/kg) GALU1 (U/kg of SBM) 0 0 45 90 135 180 114 d 4,020a 3,921b 3,899b 3,923b 3,882b 3,955ab 0.04 32.68 2.20 135 d 4,810 4,785 4,777 4,776 4,811 4,799 0.92 30.03 1.77 142 d 5,196 5,174 5,120 5,135 5,155 5,122 0.26 27.52 1.41
Treatment Positive control +10% increase in +10% increase in +10% increase in +10% increase in +10% increase in Probability > F SEM CV
a,b 1
Means within columns with common superscripts do not differ signicantly (P < 0.05). One galactosidase unit (GALU) is the amount of enzyme that hydrolyzes 1 mmol of p-nitropheny-ga-D-galactopyranoside/ min under standard conditions (pH 5.5; 37C; 15 min; optical density of 405 nm). 2 This diet is the negative control.
loric efciency. These results suggest that the composition of the diets, rather than an effect of the enzyme, was responsible for the difference in caloric use. An evaluation of the composition of the diets in Table 1 indicated that the primary differences observed between positive and negative control diets was an increase in corn with a slight reduction of SBM coupled with a considerable reduction in the quantity of poultry oil in the negative control diets. Therefore, it is possible that the energy values assigned to these various ingredients [46] might not be indicative of their true values. At 35 and 42 d of age, the caloric efciency of the birds fed the negative control diet was numerically less than that of birds fed the positive control diet with little if any indication of improvement by addition of the -galactosidase enzyme. A second comparison of caloric efciency was made with the assumption that the ME of the SBM was improved by 10% as a result of the addition of the -galactosidase enzyme, using the adjusted ME value from Table 1. With these values, no signicant differences in caloric efciency were observed among treatments (Table 5). Birds fed the negative control diet tended to have higher (less efcient) caloric efciency than those fed the positive control diet, and there was little or no indication of improvement with addition of the -galactosidase enzyme. Mortality was not signicantly affected by the dietary treatments (Table 6). In one study,
Kidd et al. [35] reported reduced mortality during heat stress in birds fed an enzyme with galactosidase activity. However, no heat stress was encountered in the present trial without indication of improvement in chick livability. Studies in which TME determinations were made of soybeans varying in oligosaccharide content due to ethanol extraction or from genetic selection generally show improved digestibility of energy and protein [24, 29], indicating that chicks do not use these fractions well. In contrast to these results, the removal of oligosaccharides using endogenous soybean -galactosidase failed to produce any benecial effects on the apparent nutritional value of soy akes, as measured by growth rate and feed conversion and by AMEn studies with young broilers and TMEn studies with adult roosters [30]. Trials in which chicks have been fed diets using supplements with -galactosidase activity in an attempt to improve the use of these oligosaccharides have demonstrated variable results. Ghazi et al. [31] mixed SBM with a protease and -galactosidase enzyme (no activity of either enzyme was given) in various combinations and precision fed to broilers to determine N retention and TMEn. In the absence of protease, the addition of the highest level of galactosidase increased N retention by 10.8% and TMEn by 15.6%. The addition of protease inuenced the response to the -galactosidase. In further studies by Ghazi et al. [32] the au-
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Table 5. Energy efciency by male broilers assuming a 10% increase in metabolizable energy from soybean meal (SBM) as the result of supplementation with -galactosidase enzyme (means of 8 pens of 30 birds/pen) Enzyme addition (g/kg of SBM) soy soy soy soy soy ME2 ME ME ME ME 0 0 1.5 3.0 4.5 6.0 ME:gain (kcal/kg) GALU1 (U/kg of SBM) 0 0 45 90 135 180 114 d 4,020 4,029 4,006 4,030 3,988 4,064 0.70 33.41 2.20 135 d 4,810 4,905 4,896 4,895 4,931 4,919 0.10 30.61 1.77 142 d 5,196 5,296 5,240 5,255 5,277 5,242 0.18 28.12 1.42
Treatment Positive control +10% increase in +10% increase in +10% increase in +10% increase in +10% increase in Probability > F SEM CV
1 One galactosidase unit (GALU) is the amount of enzyme which hydrolyzes 1 mmol of p-nitropheny--D-galactopyranoside/ min under standard conditions (pH 5.5; 37C; 15 min; optical density of 405 nm). 2 This diet is the negative control.
thors concluded that interactions between galactosidase and other enzymes need careful consideration. Graham et al. [33] treated SBM with -galactosidase and incorporated it into diets for broilers. The enzyme treatment degraded rafnose and stachyose in SBM by 69 and 54%, respectively, and increased the TMEn of the meal by 11.9%. When fed to broilers in 3 experiments, rafnose and stachyose were totally absent in the feces of chicks fed the treated SBM; however there were no signicant differences in body weight, daily feed intake, or gain:feed ratio when the meals were incorporated into diets in the same amounts. Knap et al. [34] reported an 8% increase in the TMEn of SBM by supplementation with -galactosidase
enzyme. In a subsequent feeding trial with broilers, Knap et al. [34] noted that body weight, corrected for differences in feed intake, was signicantly improved at 21 d and numerically improved at 42 d. Feed conversion was improved by 2.83% at 21 d and 1.73% at 42 d. No diet composition was given so it was impossible to estimate potential improvement in energy use. Kidd et al. [35] used an enzyme that consisted primarily of -galactosidase but which also contained -amylase, -glucanase, protease, xylanase, and cellulase activity. This product was added over the top postpelleting to nutritionally complete corn SBM diets in a study in which birds were grown to 49 d in hot
Table 6. Effects of 10% assumed increase in metabolizable energy from soybean meal (SBM) as the result of supplementation with -galactosidase enzyme on mortality by male broilers (means of 8 pens of 30 birds/pen) Enzyme addition (g/kg of SBM) soy soy soy soy soy ME2 ME ME ME ME 0 0 1.5 3.0 4.5 6.0 Mortality (%) GALU1 (U/kg of SBM) 0 0 45 90 135 180 114 d 0.42 0.42 0.00 1.25 1.67 2.08 0.14 0.617 179.41 135 d 0.83 1.25 1.67 2.50 2.50 3.75 0.35 0.983 133.52 142 d 1.25 2.50 2.08 4.58 4.58 3.75 0.27 1.205 109.02
Treatment Positive control +10% increase in +10% increase in +10% increase in +10% increase in +10% increase in Probability > F SEM CV
1
One galactosidase unit (GALU) is the amount of enzyme that hydrolyzes 1 mmol of p-nitropheny--D-galactopyranoside/ min under standard conditions (pH 5.5; 37C; 15 min; optical density of 405 nm). 2 This diet is the negative control.
WALDROUP ET AL.: BROILER PERFORMANCE summer temperatures. Birds fed the enzymesupplemented diets had signicantly improved feed conversion and lower mortality than the birds fed the unsupplemented control diets with no signicant difference in live weight, carcass yield, or breast yield. In a second study in which birds were maintained in battery brooders and fed the test diets to 18 d, no signicant differences in BW, feed intake, feed conversion, or mortality were noted. In a second report, Kidd et al. [36] evaluated an enzyme that consisted primarily of -galactosidase activity but which also contained activities of -amylase, -glucanase, protease, xylanase, and cellulase. The enzyme was added to diets of broilers reared in thermoneutral and warm weather conditions. The enzyme treatment signicantly improved feed conversion in warm and thermoneutral conditions; oddly enough, however, no differences in calorie conversion were noted. Other than the study by Knap et al. [34] few of these studies specically note the activity of the enzyme used. Many of the products tested also contained side activities of other enzymes that may have inuenced the response to the -galactosidase. In a previous report from our laboratory [37] the addition of Avizyme 1502 to diets supplemented with -galactosidase had no apparent benecial effect. It would appear that a response to -galactosidase enzyme
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might require the concomitant addition of other enzymes to be benecial. It is important to determine how precisely the chick can adjust to differences in ME content of the diet. For a number of years it was assumed that young chicks tended to eat to meet their energy needs, assuming that the diet was adequate in essential nutrients [47]. However, more recent research has consistently shown that if essential dietary nutrients are maintained in relation to dietary energy, an increased growth rate and improved feed efciency are observed with increasing levels of dietary energy [48, 49, 50, 51, 52, 53, 54]. This improvement in growth rate is attributed to the fact that the modern broiler has been primarily selected to consume feed at almost full capacity regardless of the dietary energy level [55, 56, 57]. In recent work from our laboratory [58] the productive response of the broiler to diets with increasing nutrient density was characterized, and it was noted that addition of up to 6% supplemental poultry oil, body weight, and feed efciency responses were improved in a linear manner as diet ME increased. This nding suggests that if the ME of SBM is improved by addition of enzymes it should be reected in improved performance. Results from various trials are not consistent in demonstrating such an improvement.
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5. Black, L. T., and E. T. Bagley. 1978. Determination of oligosaccharides in soybeans by high pressure liquid chromatography using an internal standard. J. Am. Oil Chem. Soc. 55:228232. 6. Openshaw, S. J., and H. H. Hadley. 1978. Maternal effects on sugar content in soybean seeds. Crop Sci. 18:581584. 7. Kuo, T. M., J. F. Van Middlesworth, and W. J. Wolf. 1988. Content of rafnose oligosaccharides and sucrose in various plant seeds. J. Agric. Food Chem. 36:3236. 8. Bach Knudsen, K. E., and B. W. Li. 1991. Determination of oligosaccharides in protein-rich feedstuffs by gas-liquid chromatography and high-performance liquid chromatography. J. Agric. Food Chem. 39:689694. 9. Hill, F. W., D. L. Anderson, R. Renner, and L. B. Carew, Jr. 1960. Studies on the metabolizable energy of grains and grain products for chickens. Poult. Sci. 39:573579. 10. Hill, F. W., and R. Renner. 1960. The metabolizable energy of soybean oil meals, soybean millfeeds and soybean hulls for the growing chick. Poult. Sci. 39:579583. 11. Potter, L. M., and E. D. Matterson. 1960. Metabolizable energy of feed ingredients for chickens. Rep. 9. Conn. Agric. Exp. Sta. Program, New Haven. 12. Sibbald, I. R., and S. J. Slinger. 1962. The metabolizable energy of materials fed to growing chicks. Poult. Sci. 41:1612 1613. 13. Ivy, C. A., D. B. Bragg, and E. L. Stephenson. 1971. The availability of amino acids from soybean meal for the growing chick. Poult. Sci. 50:408410. 14. Flipot, P., R. J. Belzile, and G. J. Brisson. 1971. Availability of the amino acids in casein, sh meal, soya protein, and zein as measure in the chicken. Can. J. Anim. Sci. 51:801802. 15. Nwokolo, E. N., D. B. Bragg, and W. D. Kitts. 1976. The availability of amino acids from palm kernel, soybean, cottonseed, and rapeseed meal for the growing chick. Poult. Sci. 55:23002304. 16. Likuski, H. J. A., and H. G. Dorrell. 1978. A bioassay for rapid determination of amino acid availability values. Poult. Sci. 57:16581660. 17. El Boushy, A. R., and A. E. Roodbeen. 1980. Amino acid availability in Lavera yeast compared with soybean and herring meal. Poult. Sci. 59:115118. 18. Pierson, E. E. M., L. M. Potter, and R. D. Brown, Jr. 1980. Amino acid digestibility of dehulled soybean meal by adult turkeys. Poult. Sci. 59:845848. 19. Parsons, C. M., L. M. Potter, and R. D. Brown, Jr. 1981. True metabolizable energy and amino acid digestibility of soybean meal. Poult. Sci. 60:26872696. 20. Potter, L. M., and M. Potchanakorn. 1985. Digestibility of the carbohydrate fraction of soybean meal. Pages 218224 in: Proc. World Soybean Conference. R. Shibles, ed. Westview, Boulder, CO. 21. Lodhi, G. N., R. Renner, and D. R. Clandinin. 1969. Available carbohydrate in rapeseed meal and soybean meal as determined by a chemical method and a chick bioassay. J. Nutr. 99:413418. 22. Gitzelmann, R., and S. Auricchio. 1965. The handling of soy alpha-galactosidase by a normal and galactosemic child. Pediatrics 36:231232. 23. Wiggins, H. S. 1984. Nutritional value of sugars and related compounds undigested in the small gut. Proc. Nutr. Soc. 43:6975. 24. Coon, C. N., K. L. Leske, O. Akavanichan, and T. K. Cheng. 1990. Effect of oligosaccharide-free soybean meal on true metabolizable energy and ber digestion in adult roosters. Poult. Sci. 69:787793. 25. Leske, K. L., O. Akavanichan, T. K. Cheng, and C. N. Coon. 1991. Effect of ethanol extraction on nitrogen-corrected true metabolizable energy for soybean meal with broilers and roosters. Poult. Sci. 70:892895. 26. Leske, K. L., C. J. Jevne, and C. N. Coon. 1993. Extraction methods for removing soybean alpha-galactosides and improving
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of abdominal fat and the size of internal organs. Korean J. Anim. Sci. 25:319324. 53. Bartov, I. 1992. Effects of energy concentration and duration of feeding on the response of broiler chicks to growth promoters. Br. Poult. Sci. 33:10571068. 54. Leeson, S., L. Caston, and J. D. Summers. 1996. Broiler responses to energy or energy and protein dilution in the nisher diet. Poult. Sci. 75:522528. 55. Nir, I., Z. Nitsan, Y. Dror, and N. Shapira. 1978. Inuence of overfeeding on growth, obesity, and intestinal tract in young chicks of light and heavy breeds. Br. J. Nutr. 39:2735. 56. Barbato, G. F. 1994. Genetic control of food intake in chickens. J. Nutr. 124:1341S1348S. 57. Barbato, G. F., P. B. Siegel, J. A. Cherry, and I. Nir. 1984. Selection of body weight at eight weeks of age. 17. Overfeeding. Poult. Sci. 63:1118. 58. Saleh, E. A., S. E. Watkins, A. L. Waldroup, and P. W. Waldroup. 2004. Effects of dietary nutrient density on performance and carcass quality of male broilers grown for further processing. Int. J. Poult. Sci. 3:110.