J. Anim. Sci. 2003. 81:2496-2504
© 2003 American Society of Animal Science
Use of carbohydrases in corn–soybean meal-based nursery diets1
S. W. Kim*,2,
D. A. Knabe
,
K. J. Hong
and
R. A. Easter
* Department of Animal and Food Sciences and
and
Department of Plant and Soil Sciences, Texas Tech University, Lubbock 79409;
and
Department of Animal Sciences, Texas A&M University, College Station 77843;
and
Department of Animal Sciences, University of Illinois, Urbana–Champaign 61802
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Abstract
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Three experiments were conducted to test the hypothesis that supplementing nursery pig diets with a mixture of carbohydrases (CS) will improve pig performance and nutrient digestibility. The CS used in these experiments contained 7 units/g of 
-1,6-galactosidase, 22 units/g of ß-1,4-mannanase, ß-1,4 mannosidase, and trace amounts of other enzymes. In Exp. 1, 108 pigs weaned at d 21 of age were fed one of three diets containing 0 (control), 0.1, or 0.2% CS for 5 wk, based on a three-phase feeding program (1, 2, and 2 wk). Over the entire 35-d period, ADG was not affected (P > 0.05) by treatment, but supplementing 0.1% CS increased (P < 0.05) gain:feed by 9%. Experiment 2 used 10 gilts fitted with simple T-cannula in the terminal ileum at 3 wk of age. After cannulation, pigs were fed the same control Phase I and II diets, but the Phase III diet contained either 0 or 0.1% CS. Ileal samples were collected for the 3 d following the 5-d adjustment period during Phase III. Apparent ileal digestibility of GE, lysine, threonine, and tryptophan was greater (P < 0.05) in the CS diet. In Exp. 3, 90 pigs weaned at 21 d of age were fed the same control Phase I and II diets, but the Phase III diet contained either 0 or 0.1% CS. Phase III diets were fed for 3 wk. Average daily gain of the CS group was greater (P < 0.05) than the control group during wk 3. Gain:feed ratio was greater (P < 0.05) for the carbohydrase group during the entire Phase III period. Four pigs per treatment were killed at the end of Exp. 3 to measure villus height and to determine the concentration of raffinose and stachyose in different parts of the gastrointestinal tract. Average villus height was greater (P < 0.05) in pigs fed the CS diet. Carbohydrase supplementation decreased (P < 0.05) the concentration of stachyose in freeze-dried digesta from the proximal and distal small intestine. Raffinose concentration, on the other hand, was decreased (P < 0.05) by CS supplementation only in the distal small intestine. These lower concentrations suggest that CS improved the digestibility of carbohydrate in soybean meal. In conclusion, the addition of CS to Phase I and Phase II nursery diets containing low levels of soybean meal did not improve pig performance, but its addition to corn–soybean meal-based Phase III nursery diets improved gain:feed ratio and energy and AA digestibility.
Key Words: Carbohydrates • Digestibility • Ileum • Pigs • Soybean Oilmeal • Villi
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Introduction
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Soybean meal is the most common protein source for pigs. However, soybeans contain antinutritional compounds that are well characterized and reviewed (Huisman and Tolman, 1992
; Liener, 1994). Most of the antinutritional compounds in soybeans are heat labile and can be eliminated during the processing of soybeans into soybean meal (Liener, 1994). However, galactosyl poly- and oligo-saccharides (i.e., ß-galactomannans and -1,6-galactosides), known as flatulence-producing compounds (FPC), still exist after soybean meal processing (Hartwig et al., 1997; Rackis, 1981). Contents of -1,6-galactosides (raffinose, 1.0%; stachyose, 4.6%) and ß-galactomannans (1.2%) are relatively high in soybean meals (Trugo et al., 1995), and these FPC are not digestible by pigs because they lack enzymes targeting -1,6-galactosyl bonds and ß-1,4-mannosyl bonds (Pluske and Lindemann, 1998; Veum and Odle, 2001). Undigested FPC negatively affect energy and protein digestibility and growth (Veldman et al., 1993; Gdala et al., 1997) due to increased osmolarity and rate of passage through the gut (Wiggins, 1984). Flatulence-producing factor is used largely by hindgut microorganisms producing gases (Rackis et al., 1970) and causing nausea and discomfort (Calloway et al., 1966; Fleming, 1981).
One efficient approach to alleviate the antinutritional effects of -1,6-galactosides and ß-galactomannans in soybean meal is applying exogenous enzymes, such as -1,6-galactosidase, ß-1,4-mannanase, and ß-1,4-mannosidase (Sugimoto and Van Buren, 1970; McGhee et al., 1978). Use of exogenous enzymes may also provide opportunities for pigs to utilize -1,6-galactosides and ß-galactomannan as energy sources. The objective of this study was to test the hypothesis that supplementing corn-soybean meal based diets of nursing pigs with an exogenous enzyme preparation composed of -1,6-galactosidase, ß-1,4-mannanase, and ß-1,4-mannosidase will improve performance, increase nutrient digestibility, and preserve villus integrity.
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Materials and Methods
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Enzyme Source
The carbohydrase supplement was composed of dehydrated fermentation products from Aspergillus niger (PRL 2351), Aspergillus oryzae (ATCC 66222; 40% by weight), and dehydrated barley malt sprouts (60% by weight). The primary active enzymes in this product were -1,6-galactosidase, ß-1,4-mannanase, and ß-1,4-mannosidase. Some minor residual enzymes were ß-1,4-glucanase, ß-1,4-glucanase, ß-glucosidase, cellobiase, xylosidase, arabinosidase, amiloglucosidase, and -glucosidase. The final carbohydrase product was manufactured by EasyBio System, Inc. (Seoul, Korea). Enzymatic potency provided by the manufacturer were: 7 U/g for -1,6-galactosidase (one unit is the enzyme activity required to hydrolyze 1 µmol of p-nitrophenyl-ß-D-galactopyranoside (pNPG) within 1 min at 30°C and pH 4.0) and 22 U/g for ß-1,4-mannanase (one unit is the enzyme activity required to release 1 mg of total reducing sugars–glucose equivalent within 1 min at 30°C and pH 4.0.)
Animal Care
The animal care protocols were approved by the Laboratory Animal Care Committee of the University of Illinois at Urbana–Champaign (#00190 for Exp. 1 and 2) and by the Animal Care and Use Committee of Texas Tech University (#01097 for Exp. 3).
Experiment 1
Design and Animals.
One hundred eight pigs (Camborough-22 x line 326; PIC, Franklin, KY), weaned at d 21.0 ± 0.1 postpartum and averaging 6.29 ± 0.08 kg, were used to evaluate the effects of supplemental carbohydrases (Endopower, EasyBio System Inc) on growth performance during a 5-wk postweaning period. Pigs were allotted to one of three treatment groups: a control group (no carbohydrase) and two groups with different carbohydrase supplementation levels (0.1 or 0.2%) providing 7 U of -1,6-galactosidase and 22 U of ß-1,4-mannanase or 14 U of -1,6-galactosidase and 44 U of ß-1,4-mannanase in 1 kg of complete diet with 0.1 or 0.2% carbohydrase supplementation, respectively. Six replicates with six animals per replicate pen were assigned to each treatment. A three-phase feeding program (Table 1) was used. The Phase I diet was fed for the first 7 d postweaning, followed by the Phase II diet for the next 14 d, and finally the Phase III diet for the last 14 d. Pigs had free access to feed and water, and feed intake and BW were measured weekly. The pigs were housed in raised-deck pens (1.2 m x 1.2 m) with plastic-coated steel flooring. Ventilation was provided by a mechanical system, and lighting was automatically regulated to approximate the seasonal day length. Ambient temperature within the room was approximately 30°C immediately after weaning and it was adjusted to approximately 22°C by the end of the experiment.
Experiment 2
Design and Animals.
Carbohydrases used in Exp. 1 were tested to evaluate their effects on apparent ileal digestibility of energy and AA in the Phase III diets (Table 1
). Level of carbohydrase supplementation was set to 0.10% based on the results from Exp. 1 providing 7 U of -1,6-galactosidase and 22 U of ß-1,4-mannanase in 1 kg of complete diet. Ten 3-wk-old gilts (Camborough-22 x line 326; PIC) were fitted with simple T-cannulas (10 mm i.d.; length, 40 mm; made from plastic pipe) at the terminal ileum using a modification of the procedure described by Kim and Easter (2001). The pigs were housed individually in raised-deck pens (1.2 m x 1.2 m) equipped with solid sidewalls and plastic-coated steel flooring. Ventilation was provided by a mechanical system and lighting was automatically regulated to approximate the seasonal day length. Ambient temperature within the room was approximately 30°C immediately after weaning, and it was adjusted to approximately 22°C by the end of the experiment.
Cannulated pigs were fed common Phase I, II, III diets until d 48 postpartum based on the same feeding program as that described in Exp. 1. On d 48.6 ± 0.2 of age, pigs (16.77 ± 0.66 kg) were weighed and allotted to two treatment groups and experimental diets were provided based on their BW (daily feed allowance, kg = 0.09 x BW0.75). Experimental diets contained 0.25% chromium oxide as an external marker. Diets were provided three times per day (0700, 1300, and 1900) during 5-d adjustment and 3-d collection phases.
Sampling and Chemical Analysis.
Digesta were collected into sterile sampling bags (Fisher Scientific, Pittsburgh, PA) attached to the cannula barrel from 0800 to 2000 during the collection phase. Collected samples were placed in plastic containers and stored at -20°C before freeze drying. Dried samples were ground using an analytical mill (A10 S2, IKA-Labortechnik, Staufen, Germany).
Samples were assayed for DM, ash, chromium, GE, and AA content. Dry matter content was measured by desiccation at 105°C for 4 h, and ash content was measured by combustion of dried samples at 500°C for 8 h. Gross energy was measured by adiabatic bomb calorimetry (Parr 1261, Parr Instrument Co., Moline, IL). Chromium content was measured from ashed samples (Williams et al., 1962). Separation and analysis of the AA was performed on an AA analyzer (Beckman 6300, Beckman Coulter, Inc., Fullerton, CA) equipped with a high-performance cation exchange resin column with AA detection accomplished with postcolumn ninhydrin derivatization. Norleucine was utilized as the internal standard.
Experiment 3
Design and Animals.
Ninety pigs (Newsham, Colorado Springs, CO), weaned at d 24.8 ± 0.26 postpartum and averaging 8.0 ± 0.1 kg, were used to evaluate the effect of supplemental carbohydrases (Endopower) on gut morphology and growth performance during a 3-wk Phase III period. Nine replicate pens of five pigs each were allotted to control or carbohydrase (0.1%) treatments providing 7 U of -1,6-galactosidase and 22 U of ß-1,4-mannanase in 1 kg of complete diet. Pigs were fed a three-phase feeding program as described in Exp. 1, except that Phase III lasted 21 d (age 43 to 63 d). Pigs were fed the same control diet during Phase I and II, and fed either control or enzyme supplemented diet (Table 2) during Phase III.
Sampling.
At the end of the study, eight pigs (two barrows and two gilts from each treatment) were selected. Pigs with BW close to the average of each treatment were selected for sampling (17.8 ± 0.2 kg for control and 18.5 ± 0.2 kg for carbohydrase). Pigs were killed with CO2, followed by exsanguination. Digesta samples were taken from the stomach, small intestine, and cecum. The small intestine was removed from the abdominal cavity, the mesentery cut, and its length measured. Digesta samples were taken from the segments corresponding to 10 to 30% (proximal) and 70 to 90% (distal) of the small intestine length. Samples were frozen at -20°C and freeze-dried before chemical analysis. Weight of empty stomach and empty small and large intestines were recorded. Length of the large intestine was measured.
Tissue samples from the small intestine were taken at 15 (proximal), 50 (mid), and 85% (distal) of its length. Samples were fixed in 10% buffered formalin (Protocol Fisher Scientific), and then processed and stained using standard procedures (Carson, 1997) before histological evaluation. Stained tissues on glass plates were examined microscopically and photographed digitally (SPOT-RT, Diagnostic Instruments, Inc., Sterling Heights, MI). Length of villus was measured using a micrometer (MA285, Meiji Techno, San Jose, CA)
Analyses of Digesta Samples.
After freeze-drying, digesta samples were ground using an analytic mill (A10 S2, IKA-Labortechnik) and analyzed for raffinose and stachyose. Approximately 0.5 g of freeze-dried ground sample was weighed and transferred into a homogenizer reservoir (Omni ES homogenizer, Omni, Warrenton, VA). Twenty milliliters of water was added to the reservoir. The mixture was homogenized at 8,500 rpm for 10 min and rinsed into a plastic bottle with approximately 4 mL of water. The bottle was sealed and placed in an 80°C water bath for 1 h. During incubation, the sample was mixed every 10 min. After incubation, the sample was allowed to cool to room temperature, transferred to a 25-mL volumetric flask, and brought up to volume with water. This mixture was filtered into a Büchner funnel containing a Whatman No. 541 filter paper supported in a 125-mL side-arm filter flask. Filtrate (15 mL) was filtered further centrifugally through a 10-kDa cutoff filter (Centriprep 10, Amicon, Inc., Beverly, MA). After centrifugation, 50 uL of filtrate was injected into an HPLC (LC-Avp10, Shimadzu, Columbia, MD) equipped with Chromegabond carbohydrate column (250 x 4.6mm, 155221-CARB, ES Industries, West Berlin, NJ). The degassed mobile phase consisted of 120 mM NaOH initially, increasing linearly to 150 mM NaOH for 10 min, followed by a linear increase to 240 mM NaOH for 10 min. At this time, the concentration of NaOH was changed to 300 mM, which was maintained for 10 min to clean the column. The column then was re-equilibrated for 10 min with 120 mM NaOH. Flow rate was constant at 1.0 mL/min, and the elution was conducted at room temperature. Eluted oligosaccharides and sucrose were detected using an evaporative light scattering detector (Sedex model 75, Sedere, France). Total run time per sample was 40 min. Appropriate dilutions of a solution containing sucrose (Sigma Chemicals, St. Louis, MO), raffinose, and stachyose (Megazyme Int., Bray, Ireland) were used as calibration standards.
Statistical Analysis
Data from Exp. 1, 2, and 3 were analyzed as a randomized block design. Analysis of variance was performed using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC). Carbohydrase supplement was the main effect. Pen was the experimental unit for Exp.1 and 3, and pig was the experimental unit for Exp. 2. Least squares means, probability of differences, and standard errors were obtained to evaluate differences among treatment means.
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Results
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Experiment 1
Average daily gain during Phase I and II was not different among the treatments (Table 3). However, pigs fed the 0.10% carbohydrase diet tended to have a higher (P = 0.069) ADG during wk 4 postweaning than did pigs fed the control diet. There were no differences in ADG among the treatments during the whole experimental period. Average daily feed intake of pigs fed the control diet was higher (P < 0.05) than that of pigs fed the 0.10% carbohydrase diet during Phase II. However, ADFI during Phase III and during the whole experimental period was similar among the treatments. Gain:feed ratio of pigs fed the 0.1% carbohydrase diet was higher (P < 0.05) than that of pigs fed the control diet during Phase III as well as during the whole experimental period.
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Table 3. Effect of different levels of carbohydrase supplementation on growth performance of nursery pigs (Exp. 1)a
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Experiment 2
The initial weights of cannulated pigs used for Exp. 2 were 16.8 ± 0.7 kg, and a fixed diet allowance was 750 g/d (250 g/meal). Apparent ileal digestibility of GE, lysine, threonine, tryptophan, histidine, and total AA was greater (P < 0.05) in the carbohydrase diet than that in the control diet (Table 4). Improvements due to carbohydrase supplementation were 4 percentage units for GE and 1 to 4 percentage units for the AA. The apparent ileal digestibility of methionine, branched-chain AA, and most of nonessential AA did not differ between the treatments
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Table 4. Effect of carbohydrase supplementation on apparent ileal digestibility (%) of energy and amino acids in Phase III diets by nursery pigs (Exp. 2)a
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Experiment 3
Average daily gain was similar for pigs on both treatments during wk 1 and 2 of Phase III, but during wk 3, ADG of pigs fed the carbohydrase diet was greater (P < 0.05) than that of pigs fed the control diet (Table 5). Average daily feed intake of pigs was not affected by treatment. Increased ADG during wk 3 resulted in greater (P < 0.05) gain:feed ratio for pigs fed the carbohydrase diet during wk 3 and over the total Phase III period.
There were no differences in stomach weight:BW ratio, small intestine weight:BW ratio, cecum weight:BW ratio, and small intestine length:BW ratio between the treatments (Table 6). However, pigs fed the control diet had a tendency for having a higher (P = 0.063) large intestine weight:BW ratio (g/kg) and higher (P = 0.063) large intestine length:BW ratio (cm/kg) than pigs fed the carbohydrase supplemented diet. Villus heights were greater at all intestinal sites (Figure 1) for pigs fed the carbohydrase diet, but differences were significant (P < 0.05) only in the distal small intestine, and the average for all three intestinal sites.
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Figure 1. Villus height of small intestines from pigs either fed a control diet or an enzyme supplemented diet during Phase III. a,bMeans with different superscripts differ (P < 0.05).
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Concentration of raffinose in freeze-dried digesta of pigs fed the control and carbohydrase diets (respectively) were as follows: proximal small intestine 1.35 vs. 1.00%; distal small intestine, 0.47 vs. 0.07%; cecum, 0.30 vs. 0.05% (Figure 2). Differences between treatments were significant (P < 0.05) at the distal small intestine. For both treatments, concentration of raffinose was greater (P < 0.05) in the proximal small intestine than in the distal small intestine or cecum.
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Figure 2. Raffinose concentration (%) in dry matter of digesta samples from proximal, and distal part of jejunum and cecum. a,bMeans with different superscripts between control and enzyme differ (P < 0.05) x,yMeans with different superscripts among the locations differ (P < 0.05).
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The effect of carbohydrase supplementation on stachyose concentrations in freeze-dried digesta was dramatic (Figure 3). Carbohydrase supplementation reduced (P < 0.05) stachyose concentration from 0.66 to 0.06% in the proximal small intestine, and from 0.39 to 0% in the distal small intestine. Cecal stachyose concentrations were similar (0.04 vs. 0%) between treatments. Concentration of stachyose in the proximal and distal small intestine were greater (P < 0.05) than concentration in the cecum for pigs fed the control diet, but no differences were found for pigs fed the carbohydrase diet due to the low levels of stachyose at all sites.
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Figure 3. Stachyose concentration (%) in dry matter of digesta samples from proximal, and distal part of jejunum and cecum. a,bMeans with different superscript between control and enzyme differ (P < 0.05) x,yMeans with different superscripts among the locations differ (P < 0.05).
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Discussion
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These experiments suggest that supplementation of this specific cabohydrase source will cause improvements (7 to 9%) in gain:feed during the latter part of the nursery period by increasing digestibility of GE, AA, raffinose, and stachyose. The lack of positive responses to carbohydrase supplementation during the Phase I and II periods likely reflects the lower soybean meal content of these diets and lower daily feed intake during the first 3-wk postweaning. Based on a FPC content of 5.5% for soybean meal (Kuo et. al., 1988), the FPC contents of Phase I, II, and III diets were 1.10, 1.38, and 1.78%; corresponding daily intakes of FPC averaged 1.8, 7.5, and 16.2 g/d.
Baucells et al. (2000) reported that supplementing -1,6-galactosidase in diets of 25-kg pigs improved gain:feed by 6%, but did not (P > 0.05) affect ADG or ADFI. These findings support the current research. The greater improvements (7 to 9%) in gain:feed ratio during Phase III of the current studies may be due to the fact that our enzyme mixture contained ß-1,4-mannanase and ß-1,4-mannosidase, in addition to -1,6-galactosidase. All three enzymes are required for the complete digestion of ß-galactomannans (Reid, 1985; Reid and Edwards, 1995).
In Exp. 2, the apparent ileal digestibility of GE and AA were increased by 6.5 and 2.9%, respectively, by carbohydrase supplementation. Gdala et al. (1997) reported that supplementing -1,6-galactosidase improved ileal digestibility of GE and some AA in lupin seed by young pigs. Veldman et al. (1993) demonstrated that the addition of 2.75% -1-6-galactosides to pig diets reduced ileal digestibility of protein and organic matter by 25%. These findings suggest FPC depresses nutrient digestibility.
Wiggins (1984) and Cummings et al. (1986) reported that FPC increased rate of digesta passage through the gastrointestinal tract of humans. Wiggins (1984) suggested that FPC in the small intestine increased fluid retention by osmotic effects, which in turn increased the rate of passage of digesta and could affect nutrient absorption.
Trevino et al. (1990) reported that the presence of FPC in poultry diets caused distension of the gastrointestinal tract due to the high gas volume produced from bacterial fermentation of the FPC. In the current study, weight and length of large intestine from the pigs fed the carbohydrase-supplemented diet tended to be smaller (P = 0.063) than those from the control group, supporting the data from Trevino et al. (1990). There was a 14.0% reduction in the length of large intestine/BW (cm/kg) and a 19.5% reduction in the weight of large intestine/BW (g/kg) by the carbohydrase supplementation. This result suggests that the removal of FPC by the carbohydrase supplementation may reduce distention of the large intestine that may limit nutrient utilization. The limited number of replicates per treatment (four pigs per treatment) may have been the reason for the lack of significant differences observed in organ weight.
Concentration of raffinose and stachyose in freeze-dried digesta from the small intestine were higher than those in the diets, supporting the fact that FPC are poorly digested in pigs’ small intestine. The proximal small intestine appeared to be the major site of stachyose hydrolysis by carbohydrase, whereas the distal section of small intestine appeared to be the major site for raffinose hydrolysis. Some portion of hydrolysis also may have occurred before that specific site as well. It is not clear at this point why hydrolysis of raffinose and stachyose occurred at different location in the small intestine. Possibly supplemental carbohydrase hydrolyzed stachyose in the proximal small intestine liberating one galactose from the galactosyl end of stachyose leaving raffinose for further hydrolysis in the distal small intestine.
There were no differences in concentration of raffinose and stachyose between treatments when measured at the cecum. Mayhara et al. (1998) and Krause et al. (1994) demonstrated that hindgut microorganisms, including Clostridium perfringens, Bacteroides fragilis, and Peptostreptococcus products, utilized undigested FPC producing gasses.
In pigs fed the control diet, the concentration of stachyose and raffinose in the digesta decreased from the proximal to distal small intestine. Although the difference was significant only for raffinose, this decline suggests that resident microflora in the small intestine are capable of fermenting these compounds. Jensen (2001) indicated that the distal part of a pigs’ small intestine is capable of fermentation.
These studies support the idea that use of exogenous enzymes is an efficient, practical method of reducing the antinutritional effects of FPC in soybeans (Sugimoto and Van Buren, 1970). Older methods of removing FPC, such as extraction (Ku et. al., 1976) and soaking and germination of soybeans (East et al., 1972; Kim et al., 1973), are costly and not feasible.
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Implications
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Supplementation of carboyhydrases that digest flatulence-producing carbohydrates in soybean meal can benefit nursery pigs by improving nutrient digestibility and, in turn, growth performance. This application will be most beneficial for nursery diets that contain soybean meal as a major protein ingredient.
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Footnotes
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1 The authors acknowledge the financial support of EasyBio System, Inc., Seoul, Korea. 
Correspondence: Box 2141, 123 Animal Science Bldg. (phone: 806-742-2532; fax: 806-742-2335; E-mail: sungwoo.kim{at}ttu.edu).
Received for publication February 12, 2003.
Accepted for publication July 7, 2003.
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Abstract
Introduction
