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Digestibility of nitrogen and amino acids in soybean meal with added soyhulls^1,2

R. N. Dilger^*, J. S. Sands, D. Ragland and O. Adeola^*,3

^* Department of Animal Sciences and and Department of Veterinary Clinical Sciences, Purdue University, West Lafayette, IN and and Danisco Animal Nutrition, Marlborough, Wiltshire, U.K.

Abstract

This study was designed to quantify the effect of soyhulls on N and AA digestibilities of soybean meal for growing pigs. Soyhulls were incorporated into 17% CP diets containing 33.25% soybean meal (SBM) at 0, 3, 6, or 9% (as-fed basis) and fed to 35-kg barrows to determine their effect on apparent and true digestibility of DM, GE, N, and AA measured at the terminal ileum. Positive and negative control diets containing 1.05% lysine were formulated with 35% SBM and 27% soy protein concentrate (SPC), respectively. A low-protein, casein-based diet was used to estimate endogenous AA losses. Soyhulls were incorporated into experimental diets at the expense of cornstarch, and SBM levels were adjusted to accommodate the contribution of CP from soyhulls. Fourteen pigs were surgically fitted with simple T-cannula at the distal ileum and fed the seven semipurified cornstarch diets based on a replicated 7 x 7 Latin square design. Each period lasted 7 d, with diet acclimation from d 1 to 5 and ileal sample collection for 12 h on d 6 and 7. Feed was offered at a level of 90 g/kg BW^0.75 in two equal portions at 0800 and 2000. Apparent ileal digestibilities of DM and GE decreased approximately six percentage units with the addition of soyhulls (linear, P < 0.05), whereas N was not affected. Both apparent and true ileal digestibilities of arginine, histidine, lysine, phenylalanine, aspartic acid, serine, and tyrosine also exhibited a decrease (linear, P < 0.05) of up to five percentage units with the addition of soyhulls. True ileal lysine digestibility of SBM decreased from 90.3 to 87.7% with the addition of 9% soyhulls. The endogenous nutrient fraction measured at the distal ileum was rich in proline, glutamic acid, and glycine, with losses greater than 1,000 mg/kg of DMI for each AA, and contained minimal amounts of tryptophan, methionine, and cystine. The current data suggest that a 0.2% decrease in some true ileal indispensable AA digestibilities may result with each 1% increase in soyhull inclusion in semipurified diets containing SBM as the sole source of AA as fed to growing pigs.

Key Words: Amino Acids • Cannulation • Digestibility • Pigs • Soybean Meal • Soyhulls

Introduction

Due to the nutritionally advantageous characteristics of soybean meal (SBM), such as its AA profile, which complements that of cereal grains, this feedstuff has been the predominant protein source used to supplement swine diets in the United States. Therefore, it is important to fully identify intrinsic factors compromising the utilization of SBM to maximize animal growth and profitability in modern swine production systems. Additionally, environmental issues continue to gain momentum, with more emphasis being placed upon efficient use of protein supplements such as SBM. Fibrous soybean hulls are removed during processing of soybeans to produce a 48% CP meal, which is typically used in poultry and weanling pig diets. Removal of the fibrous components results in a more easily digested product for the young pig, which lacks digestive capacity for both simple and complex carbohydrates (Jensen et al., 1997).

Soyhulls contain mainly insoluble nonstarch oligosaccharides, two-thirds of which is cellulosic in nature (Lo, 1989). The presence of this large fiber fraction was reported by Kornegay (1978) to have negative effects on digestibility of nutrients such as DM and protein as well as gross energy. Mitaru et al. (1984) confirmed these results, noting decreases in these nutrient digestibilities at an inclusion level of 15% soyhulls. Whereas soybean meal serves as a good dietary source of AA in commercial swine diets, improvements could be achieved through the characterization of inherent factors affecting nutrient digestibility. Soyhulls constitute one of the differences between 48% CP and 44% CP soybean meals, and therefore may be a factor affecting dietary nutrient utilization of SBM. As part of a larger collaborative effort to investigate factors affecting nutrient utilization of soybean meal, this study was designed to quantify the effect of soyhulls on ileal N and AA digestibilities of soybean meal as fed to growing pigs.

Materials and Methods

Dietary Treatments
Four 17% CP diets (Table 1) were formulated to contain graded levels of soyhulls at 0, 3, 6, or 9% (as-fed basis). Dehulled SBM in these four diets was obtained from the Purdue University feed-processing facility (hereafter referred to as "local SBM") and used in Diets 1 to 4. In addition, two control diets (Diets 5 and 6) were fed as part of a larger project such that the digestibility values obtained from these diets could be compared between experiment stations. Diet 6 contained dehulled SBM (hereafter referred to as "common SBM") and Diet 5 contained soy protein concentrate (SPC), both ingredients originating from The Ohio State University. Diet 7 was a low-protein (4.4% CP) diet containing 5% casein and was used in the quantification of endogenous nutrient excretion. Diets were semipurified, consisting primarily of cornstarch, sucrose, dextrose, and protein ingredient. All substitutions were made at the expense of cornstarch, and SBM levels were adjusted to accommodate the contribution of CP by soyhulls in Diets 1 to 4. All seven diets were formulated to meet or exceed current NRC (1998) recommendations. Feed allowance was based on the mean BW of all pigs determined at the beginning of each period and was calculated to be 90 g/kg BW^0.75. Half this amount was fed twice daily (0800 and 2000), with identical amounts being fed between pigs within any given period. Chromic oxide was incorporated into the diets (5 g/kg, as-fed) to calculate ileal nutrient digestibilities via the index method.

The cannulas were secured in place and the longitudinal intestinal incision closed using a continuous suture pattern that extended to the barrel of the cannula. The cannulas were exteriorized through a defect created in the last intercostal space by attaching a bullet-shaped device to the threads of the cannula barrel. With an attached string, this device was used to pull the cannula through the intercostal defect, effectively protecting the structural integrity of the cannula while providing an easy means of positioning the piece. Finally, the cannula was secured in place with a retainer plate and capped. Pigs were allowed at least 10 d to recover from surgery before initiation of the study. The cannulation protocol was approved by the Purdue University Animal Care and Use Committee.

Animals and Chemical Analyses
Pigs were randomly assigned to metabolism crates (1.02 x 0.73 m) equipped with stainless steel feeders and low-pressure, automatic water nipples. The pigs were housed in an environmentally controlled building maintained between 21 to 23°C and given 12 h of artificial lighting per day. Experimental diets were fed to the 14 pigs according to a replicated 7 x 7 Latin square design with each period lasting 7 d. Days 1 through 5 were used for diet acclimation and ileal digesta was collected for 12 h on each of d 6 and 7 by attaching a plastic tubular bag to the externalized T-cannula. The bags contained 10 mL of 5% formic acid to reduce microbial proliferation, and ileal contents were stored at -20°C between collections. Ileal digesta were thawed, pooled for each pig for the 2-d collection, subsampled, and lyophilized.

Diets and freeze-dried ileal digesta were ground to a fine powder in a coffee grinder (Braun, Boston, MA) and analyzed for the following components. Dry matter content was determined by drying the samples at 100°C for 24 h. Amino acid and chromium analyses were conducted at the University of Missouri Experiment Station Chemical Laboratory. Samples for AA analysis were prepared using a 24-h hydrolysis in 6 N HCl at 110°C under nitrogen atmosphere. For methionine and cysteine, performic acid oxidation occurred prior to acid hydrolysis. Samples for tryptophan analysis were hydrolyzed using barium hydroxide. Amino acids in hydrolysate were determined by HPLC after postcolumn derivatization (AOAC, 2000; 982.30 E [a, b, c]). Amino acid concentrations were not corrected for incomplete recovery resulting from hydrolysis. Chromium concentration of samples was determined by the inductively coupled plasma atomic emission spectroscopy method (AOAC, 2000; 990.08) following nitric/perchloric acids wet ash digestion. Nitrogen content of diet and ileal samples was determined by the combustion method (AOAC, 2000; 990.03) (model FP2000, LECO Corp., St. Joseph, MI) using EDTA as a standard and gross energy content determined by adiabatic bomb calorimetry (model 1261, Parr Instrument Co., Moline, IL) using benzoic acid as a standard. Acid and neutral detergent fiber contents of local soybean meal, soyhulls, and diets were determined by the method of Jeraci and Van Soest (1990).

Digestibility Calculations
Apparent ileal digestibility values were calculated using the index method according to the following equation:

where AID_X is the apparent ileal digestibility of DM, GE, N, or an AA; Cr_I is the chromium concentration of dietary intake; Cr_O is the chromium concentration of ileal output; N_O is the nutrient concentration of ileal output; and N_I is the nutrient concentration of dietary intake. All values for Cr_I, Cr_O, N_O, and N_I are expressed as mg/kg of DM.

By feeding the casein diet, endogenous nutrient losses (ENL) could be determined by the following equation:

where ENL is the endogenous loss of N or an AA on a mg/kg of DMI basis, Cr_IC is the chromium concentration of the casein diet, Cr_OC is the chromium concentration of ileal output from pigs fed the casein diet, and N_OC is the nutrient concentration of ileal output (mg/kg of DM) from pigs fed the casein diet. The endogenous nutrient losses from all pigs fed the low-protein, casein diet were averaged to correct apparent ileal digestibilities. Therefore, true ileal digestibility values were determined by the following formula:

where TID_X is the true ileal digestibility of N or an AA, N_I is the nutrient concentration of dietary intake, and ENL is the average endogenous nutrient loss as calculated above.

Statistical Analysis
Data were analyzed by ANOVA using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC) based on a replicated 7 x 7 Latin square experimental design. The model for this analysis included replicates (with 1 df), pigs within replicates (with 12 df), periods within replicates (with 12 df), and diets (with 6 df). Nonorthogonal contrasts were used to determine treatment effects on apparent and true ileal digestibilities including: linear and quadratic effects of soyhulls in local SBM diets (Diets 1, 2, 3, and 4) and SPC vs. common SBM (Diet 5 vs. 6). An alpha level of 0.05 was used to determine statistical significance in all analyses and individual pig was considered the experimental unit. For true ileal indispensable AA digestibilities exhibiting a linear response to soyhull inclusion, a linear regression analysis was conducted in order to quantify the effect of soyhull inclusion in diets containing SBM as the sole protein source for growing pigs.

Results

Throughout the experiment, pigs remained healthy and consumed their daily feed allowances. At the conclusion of the first replicate, one pig had a displaced cannula, which resulted in one less pig for the subsequent periods. This pig had consumed only the 6% soyhull diet. Additionally, an inadequate amount of ileal digesta was collected for chemical analysis from the pig fed the 0% soyhull diet during this first period. Postmortem examination of all pigs after the study revealed no intestinal adhesions or abnormalities as a result of the cannulation procedure.

The nutrient profiles of ingredients used to formulate experimental diets are presented in Table 2. Common and local SBM were quite similar in DM, GE, N, and AA composition. In addition, the nutritional profiles of these two meals were similar to those listed by NRC (1998). The local SBM contained lower levels of tryptophan compared with the common SBM (0.70 vs. 0.91%, respectively). The analyzed fiber composition of soyhulls used in this study was 32.1, 44.8, and 55.1% on an as-fed basis for CF, ADF, and NDF, respectively. Analyzed AA values of ingredients were used to calculate AA levels of experimental diets (Table 3).

The purpose of this study was to characterize and quantify the extent to which soyhull inclusion affects N and AA digestibilities in diets containing SBM as the sole protein source. After removal during processing, using a soyhull protein level of 8.5%, it is estimated that soyhulls are reincorporated into 48% CP SBM at approximately 10% to produce the industry standardized, 44% CP meal. Intuitively, inclusion of both soluble and insoluble fiber fractions via soyhulls would alter nutritional characteristics of 48% CP SBM by simply diluting the more digestible nutrients and therefore producing a lower-energy, higher-bulk feedstuff. As a result, studies have shown an increase in quantitative amounts of dietary nutrients excreted via the nonruminant animal attributed to decreased nutrient digestibilities (Kornegay, 1978; Mitaru et al., 1984).

In the current study, decreases in both apparent DM and GE digestibilities resulted from the direct replacement of highly digestible cornstarch with fibrous soyhulls. Similar to previous reports, some apparent ileal AA digestibilities were affected by the addition of soyhulls, including the limiting AA, lysine (Mitaru et al., 1984). Apparent ileal AA digestibilities of both dehulled SBM sources (local and common) were quite similar to NRC (1998) values with the exception of tryptophan. Apparent ileal tryptophan digestibility values were 88.9 and 90.2% for the local and common SBM, respectively, compared with 81% reported by both NRC (1998) and Knabe et al. (1989). In comparison, Traylor et al. (2001) reported an apparent ileal tryptophan digestibility nearly identical to that observed in the present study. This variability may have resulted from low dietary tryptophan levels found in SBM along with the minimal requirement of this AA by the pig. Overall, apparent ileal digestibilities of the remaining indispensable AA reported by Traylor et al. (2001) were 3 to 8% higher than in the current study for the common SBM. This observation is surprising because the same protein source was used by both experiment stations in identically formulated diets. Differences in experimental conditions may explain some of the variation.

As suggested by others (Moughan and Schuttert, 1991; Furuya and Kaji, 1992), aspartic and glutamic acids, glycine, proline, and serine constitute the largest proportion of the total endogenous fraction measured at the terminal ileum. Additionally, these AA would most likely be present as intact proteins instead of as free AA (Moughan and Schuttert, 1991). Proline was the most abundant AA quantified in ileal digesta from pigs fed the low-protein, casein diet in the current study. This phenomenon was reported previously (Adeola et al., 1986; Moughan and Schuttert, 1991; Furuya and Kaji, 1992), and it was attributed to the state of protein depletion in the pig. Therefore, caution must be exercised when interpreting true ileal proline digestibilities due to the endogenous abundance of this AA as well as high pig-to-pig variability. The branched-chain AA (isoleucine, leucine, and valine), as well as threonine, were the indispensable AA present at the highest concentrations in the endogenous output collected at the terminal ileum. High turnover rates of sources containing these AA may provide an explanation for their relatively high endogenous concentration. Adeola et al. (1986) also reported that threonine was the most abundant indispensable AA in endogenous ileal output. The minimal concentration of both methionine and tryptophan in the endogenous fraction is likely a reflection of the low requirements of these two AA by the pig. Comparison of endogenous losses with values previously reported by collaborating experiment stations (Traylor et al., 2001; Smiricky et al., 2002; van Kempen et al., 2002) shows endogenous losses observed in the current experiment are within a typical range.

The decreases observed in some true ileal AA digestibilities provide evidence of a negative soyhull effect on digestion in addition to simple dilution of the diet by a poorly available AA source. The analyzed AA composition of soyhulls in this study shows that the lysine:CP ratio (0.08) is similar to that of both dehulled SBM sources (~0.06). Therefore, it appears that the protein quality of soyhulls is equivalent to SBM, as suggested by others (Kornegay, 1978) with the main effect on digestion arising largely from the high dietary fiber content. Additionally, Laplace and Darcy-Vrillon (1989) reported apparent ileal indispensable AA digestibilities of soyhulls to be greater than 80% in a casein-cornstarch diet containing 332 g/kg of DM of soyhulls. True ileal AA digestibility values of SBM reported by NRC (1998) were approximately 0.5 to 4 percentage units lower for most of the indispensable AA compared with the present study, the largest difference again being tryptophan. Additionally, Traylor et al. (2001) and van Kempen et al. (2002) both reported values similar to those of the present study. Most likely, the observed decreases in true ileal digestibilities arose from dietary fiber-induced increases in the endogenous nutrient loss. The quantitative increase in various fiber fractions supplied by soyhulls may have induced greater losses of AA-containing sources such as digestive enzymes, enterocytes, and mucins. Grala et al. (1998) provided similar evidence of a dietary fiber influence on N utilization by feeding rapeseed products designed to cause different losses of endogenous nutrients. It was determined that the rapeseed hull fiber itself was the primary antinutritive factor responsible for the increased endogenous loss of nutrients. Therefore, extrapolating this evidence to soyhulls, a byproduct of similar fiber composition, may help explain the observed decreases in true ileal AA digestibilities of soybean meal in the current study.

True ileal nutrient digestibilities of the soy protein concentrate control diet were similar compared with the common SBM control diet for nitrogen and most of the amino acids. As soy protein concentrate is more processed than SBM (with raffinose and stachyose removed), similarities in nutrient utilization between these diets likely means the occurrence of antinutritional oligosaccharides was minimal in the common SBM. Therefore, due to similarities in nutrient digestibilities between the common SBM diet and the 0% soyhull diet containing local SBM, it may be deduced that the local SBM was relatively free of additional confounding antinutritional factors that may have affected ileal nutrient digestibilities and confounded the observed effect of soyhulls.

When studying the overall effect of a fibrous feedstuff on nutrient metabolism, one approach is to explain observations in terms of the effects of purified fiber fractions. A plethora of data exist on different fiber fractions and their likely effect on nutrient utilization within the digestive tract (Li et al., 1994; Mosenthin et al., 1994; Schulze et al., 1994). By building on such research, it becomes possible to explain the role of complex fiber sources such as soyhulls on nutrient utilization. Soyhulls are composed of approximately 75% nonstarch polysaccharide, 60% of which is cellulosic in nature (i.e., 45% cellulose on DM basis) (Lo, 1989). This insoluble fiber fraction has historically been the main reason to exclude soyhulls from swine diets due to limited fermentative characteristics. However, some studies have shown that dietary cellulose has little effect on ileal AA digestibilities as fed in semipurified diets containing up to 13.3% Solkafloc (Li et al., 1994) or 10% Celufil, a purified fiber source containing 86.5% cellulose (Mitaru et al., 1984). Dietary inclusion of insoluble fiber above these levels is believed to negatively affect ileal AA digestibilities, a threshold effect (Li et al., 1994) that was likely not breached in the current study. Additionally, Schulze et al. (1994) showed that nearly 20% of ingested NDF was digested prior to reaching the terminal ileum, but ileal N digestibility decreased 5.2 percentage units. By providing purified NDF to growing pigs at a level of 15%, Lenis et al. (1996) observed a similar effect, with decreases in ileal AA digestibilities of 2 to 5.5 percentage units. Therefore, taking into account the fiber composition and graded inclusion levels of soyhulls in the current study, the observed negative effect on N and AA digestibilities may have resulted from a combination of individual fibrous components. Further research is necessary to elucidate the primary fiber fraction responsible for the observed effects.

A brief discussion of hindgut fermentation and its likely role in energy metabolism is appropriate here due to the level of soyhull inclusion. The consequence of a decrease in ileal DM digestibility with increasing levels of dietary soyhulls is the availability of more substrates for hindgut fermentation. Digestion of the primarily cellulosic soyhulls by endogenous enzymes is minimal and therefore undigested material becomes a fermentative substrate for the resident anaerobic microflora in the cecum and ascending colon (Kornegay, 1978). There was a linear increase in the disappearance of DM and GE, but a linear decrease in N disappearance in the hindgut with increasing dietary soyhull level (data not shown). Laplace and Darcy-Vrillon (1989) found that fiber contained in soyhulls is readily fermentable by the microbes found in the hindgut of growing pigs, which may be partly due to presence of a pectin fraction. Subsequent colonic absorption of fermentation by-products, especially volatile fatty acids, will spare the energy requirement of the pig, and previous research has reported that 10 to 30% of the maintenance energy requirement was fulfilled in this manner (Kass et al., 1980; Rérat et al., 1987). The small contribution of energy from volatile fatty acids toward overall energy metabolism probably resulted from the lower efficiency by which energy is derived from this source compared with the moderately efficient glucose pathway. It is also possible that presence of a readily fermentable fiber fraction found in soyhulls may have altered the proliferation rate and/or colonization location of microbes within the pig by providing a substrate for microbes within the midgut (Laplace and Darcy-Vrillon, 1989; Schulze et al., 1994). Therefore, digestion of dietary nutrients and availability of fermentation products may have been influenced by microbial action prior to reaching the end of the absorptive region in the midgut. For instance, Fadel et al. (1989) observed that more than 75% of dietary nonstarch polysaccharides were degraded by the nonruminant animal before reaching the terminal ileum and partly attributed this observation to the action of resident prececal microbes.

It is duly important to consider how nutrient utilization is affected by the soluble fiber fraction, of which soyhulls contain approximately 25%. One such fraction shown to negatively affect nutrient digestibilities is dietary pectin. Even low levels of this galacturonic acid-containing polysaccharide are able to induce a highly viscous environment within the alimentary tract and therefore affect gastrointestinal function through a variety of mechanisms, as reviewed by Vahouny and Cassidy (1985). First, slowed gastric emptying may result in response to viscous material; therefore an adjustment is made to lengthen the duration of proteolysis in the stomach. Larsen et al. (1994) provided support of this hypothesis, adding that pepsin activity is actually decreased during extended gastric residence to provide a balance and therefore, overall proteolysis is only slightly altered. Secondly, gastric pH may be increased due to the buffering capacity of fiber per se with the indirect result being reduction in gastrin secretion in response to the more alkaline environment. Increased chyme viscosity may lead to slower intestinal transit time, thus allowing more contact of digestive enzymes with dietary substrates. This increased viscosity may then reduce pancreatic enzyme diffusion and therefore lessen the extent to which all nutrients are digested at the mucosal surface. At the same time, soluble fiber fractions may bind these digestive enzymes and render their activity unavailable, leading to higher excretion rates of endogenous protein. Specifically, the viscous nature of chyme produced by gelling properties of pectin may impede nutrient transport through the mucosal surface by creating a thicker unstirred water layer. Mosenthin et al. (1994) showed that guar gum and pectin both inhibit uptake of free AA within the intestine as a result of viscosity changes. These researchers provided direct evidence of this effect by feeding pectin at a level of 7.5%, which resulted in apparent ileal indispensable AA digestibilities decreasing an average of 14.1 percentage units. Pectin has also been implicated in negatively affecting nutrient digestibilities in other studies (Mitaru et al., 1984) and has been thought to increase the total amount of carbohydrate byproducts available for absorption due to the ease of fermentation of this derivative (Salyers et al., 1985).

Implications

The decreases in amino acid digestibilities observed from adding soyhulls to diets containing soybean meal as the sole source of amino acids as fed to growing pigs call for exercising care when feeding this by-product. When soyhulls are added at graded levels up to 9% (as-fed basis), there were also decreases in ileal digestibilities of dry matter and gross energy. These effects likely resulted from a combination of both insoluble and soluble fiber fractions in soyhulls. The current data suggest that a 0.2% decrease in some true ileal indispensable amino acid digestibilities may result with each 1% increase in soyhull inclusion in semipurified diets containing SBM. Therefore, it seems that growing pigs are fairly tolerant of the fiber contained in this by-product of soybean processing.

Footnotes

¹ Journal paper No. 16977 of Purdue University Agricultural Research Programs.

² Financial support provided in part by the National Soybean Meal Research Laboratory, Urbana, IL.

³ Correspondence—phone: 765-494-4848; fax: 765-494-9346; e-mail: ladeola{at}purdue.edu.

Received for publication January 3, 2003. Accepted for publication November 6, 2003.

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