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Articles

The Ratio of Insoluble to Soluble Fiber Components in Soybean Hulls Affects Ileal and Total-Tract Nutrient Digestibilities and Fecal Characteristics of Dogs¹

Department of Animal Sciences, University of Illinois, Urbana, IL 61801 and ^* Department of Grain Science and Industry, Kansas State University, Manhattan, KS 66506

³To whom correspondence should be addressed. E-mail: nmerchen{at}uiuc.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
An experiment was conducted to evaluate the effects of soybean hulls (SH) containing varying ratios of insoluble:soluble fiber (I:S) on nutrient digestibilities and fecal characteristics of dogs. Ileally cannulated dogs (n = 6) were fed seven diets in a 6 x 7 Youden square arrangement of treatments. The seven diets included five SH-containing diets with I:S of 1.9, 2.7, 3.2, 5.2 or 7.2 and two diets containing either beet pulp (BP) or no supplemental fiber (control). Ileal digestibilities of DM, OM, CP, total dietary fiber (TDF), fat and gross energy (GE) were lower (P < 0.05) for dogs fed diets containing supplemental fiber compared with dogs fed the control diet. Fiber inclusion had a modest negative effect (P < 0.05) on total-tract DM, OM, fat and GE digestibilities compared with the control diet. Ileal digestibilities of DM and OM by dogs fed the SH treatments responded quadratically (P < 0.05) to I:S, with digestibility coefficients decreasing as the I:S approached 3.2. Highest ileal digestibilities were observed for diets with an I:S of 1.9 and 7.2. Similarly, a quadratic response (P < 0.05) was observed for digestibility of total amino acids at the ileum. Fecal outputs were lower (P < 0.001) when dogs consumed the control diet vs. fiber-containing diets. Among the SH-containing diets, there was a linear increase in fecal output as I:S increased (P = 0.031). The I:S in the diet affects DM and OM digestibilities at the ileum and affects fecal output, indicating that optimization of this ratio is desirable.

KEY WORDS: • dogs • insoluble fiber • soluble fiber • digestibility • soybean hulls

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
The canine population of the United States totals 56 million animals, with 37.6% of all U.S. households owning at least one dog (1) . Barring major illness, the largest pet-related expense for dog owners is food. With this in mind, nutritionists are constantly researching new ways of formulating pet food to better meet the needs of the animal and the desires of the owner.

More research is warranted on the role of dietary fiber (DF)⁵ in pet foods. Many benefits have been linked to fiber in human diets, such as positive influences on colon cancer, type II diabetes and obesity, and as an aid in establishing bowel movement regularity (2) . Dietary fiber may be an important ingredient in dog diets when considering the long-term health and well-being of the pet.

Fiber is a nutritionally, chemically and physically heterogeneous material. This heterogeneous mix can be categorized into two major subclasses, i.e., soluble-viscous-fermentable fiber (soluble) and insoluble-nonviscous-nonfermentable fiber (insoluble). The two subclasses have different roles in the digestive/absorptive processes within the gastrointestinal tract. The ratio of insoluble to soluble fiber (I:S) in a DF source can affect overall diet utilization and appears to be important in the formulation of diets to provide optimal fecal characteristics and intestinal fermentation.

The objectives of the research reported here were to investigate the effects of inclusion of selected soybean hull (SH) samples, with varying I:S, in dog diets on nutrient intakes, digestion proximal to the terminal ileum, total-tract digestibilities and fecal characteristics.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Five samples of SH were obtained from four U.S. processing plants. The SH are by-products from the production of 48% crude protein (CP) dehulled soybean meal. The SH were ground through a 2-mm screen in a Wiley mill (Thomas-Wiley, Swedesboro, NJ) and analyzed for dry matter (DM), organic matter (OM), CP (3) and total dietary fiber (TDF) (4) . Insoluble fiber was determined by the method of Prosky et al. (5) . Soluble fiber was calculated by subtracting the insoluble fiber fraction from the TDF fraction. Values for the composition of SH sources are presented in Table 1 .

Adult female dogs (n = 6) with hound bloodlines (Butler Farms, Clyde, NY), an average initial weight of 25 kg and a functional ileal cannula were used in a 6 x 7 Youden square design. Ileal cannulation was conducted according to the procedure of Walker et al. (11) . The dogs were housed in 1.2 x 2.4 m² clean floor pens in the College of Agricultural, Consumer and Environmental Sciences Animal Care Facility. The pens were housed in a temperature-controlled (22°C) room. An 8-h dark:16-h light cycle was used. Animal care procedures were conducted under a research protocol approved by the Campus Laboratory Animal Care Advisory Committee, University of Illinois, Urbana-Champaign, and complied with the NIH guidelines (12) . Euthanasia was not performed during or after the trial; animals were retained for future research.

Each dog was offered 200 g of diet (as-is basis) at 0800 and 2000 h for a total of 400 g/d. Any feed refusals from the previous feeding were weighed, recorded, labeled and stored. The dogs had ad libitum access to water.

Chromic oxide was used as a digestibility marker. Each dog was dosed orally with a gelatin capsule containing 0.5 g of chromic oxide at 0800 and 2000 h, before feeding. A total of 1 g marker/d was dosed starting on d 3 of each period to the end of each period.

Each period was 11 d long. A 7-d diet adaptation phase preceded a 4-d collection of ileal digesta and total feces in each period. Adaptation time and collections were similar to adaptation time and collections in past ileal-cannulated studies conducted in our laboratory (8 ,13 ,14) . The digesta were collected every 4 h, rotating up 1 h/d, with each collection lasting 1 h. Consequently, a digesta sample representing each hour between 0800 and 2000 h was obtained. Ileal digesta were collected by attaching a Whirlpak bag to the exterior portion of the cannula. Generally, 15–30 mL of ileal digesta were collected at each sampling. Due to the low concentration of DM in digesta (15%), collections did not significantly affect the flow of digesta or fecal output. Dogs were encouraged to move about freely during ileal collections. Dogs were continually observed to ensure that they would not remove the bag from their cannula.

During the 4-d collection phase in each period, digesta samples were collected, frozen (-4°C) and composited. Feces excreted were collected from the pen floor, weighed, scored, frozen (-4°C) and composited. Fecal scores were estimated at each collection. Scoring was determined as follows: 1 = hard, dry pellets: small, hard mass; 2 = hard, formed, dry stool: remains firm and soft; 3 = soft, formed moist; softer stool that retains shape; 4 = soft, unformed: stool assumes shape of container, pudding-like; 5 = watery: liquid that can be poured. Feces and ileal digesta were freeze-dried (FTS-Triphilizer MP, Stone Ridge, NY), ground through a Wiley mill (Model 3375-E10, Thomas-Wiley, Swedesburo, NJ) with a 2-mm screen and stored for analyses.

Feed, feces, and ileal digesta were analyzed for DM, OM, ash, CP and fat using AOAC (3) methods. Gross energy was determined by oxygen bomb calorimetry (Parr Instruments, Moline, IL). Total dietary fiber was determined as outlined by Prosky et al. (4) . Soluble fiber and insoluble fiber were determined as outlined by Prosky et al. (5) . Chromium was analyzed according to Williams et al. (15) . All of the above analyses were performed in duplicate, and values were accepted when there was <5% difference between duplicates. Feed and ileal digesta were prepared for amino acid analysis by hydrolyzing 150 mg sample in 15 mL of 6 mol/L HCl for 22 h at 105°C according to Spitz (16) . The amino acid concentrations of the hydrolysates were determined using ion-exchange chromatography (GoldDV711 chromatograph, Beckman, Fullerton, CA). Methionine and cystine were determined using the performic acid oxidation method described by Moore (17) except that excess performic acid was removed by freeze-drying.

Dry matter (g/d) output at the ileum and fecal DM output were calculated by dividing the Cr intake (mg/d) by ileal or fecal Cr concentrations (mg Cr/g ileal or fecal DM), respectively. Ileal and fecal nutrient outputs were calculated by multiplying the DM output by the concentration of the nutrient in the ileal or fecal DM. Ileal and total-tract nutrient digestibilities were calculated as nutrient intake (g/d) minus the ileal or fecal nutrient output (output, g/d), divided by nutrient intake (g/d). This method of measuring nutrient outputs at the ileum and total-tract has been used in many studies in our laboratory (6 ,8 ,13 ,14 ,18) .

A 30-g sample of each diet was collected 1 d before the collection phase of the period, composited, ground and analyzed. The seven diets were analyzed for DM, OM, CP, amino acids, fat, TDF, insoluble fiber and soluble fiber as described earlier.

Data were analyzed as a 6 x 7 Youden square arrangement of treatments by the General Linear Models procedure of SAS (19) . Model sums of squares were separated into treatment, period and animal effects. Treatment mean comparisons were conducted by single degree of freedom contrasts. The contrasts included the following: 1) control diet vs. fiber-containing diets, 2) BP diet vs. the SH-containing diets, and the SH-containing diets were evaluated for 3) linear, 4) quadratic and 5) cubic effects of the ratio of I:S. Contrasts with P < 0.05 were considered statistically significant.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Dogs.

Dog weights were similar before and after the trial. All dogs were at maintenance and in good health throughout the trial. There was no observable change in hair coat or skin condition during the trial. All dogs accepted all diets with little or no feed refusal.

Diets.

The control diet refers to the diet containing no supplemental fiber, the BP diet refers to the diet containing 7.5% BP and the SH-containing diets will be referred to by their analyzed I:S (diets 1.86, 2.65, 3.17, 5.18 and 7.21).

Chemical composition.

Chemical composition of the five sources of SH used as fiber sources in dog diets is reported in Table 1 . Values for DM and OM were similar among sources. Dry matter ranged from 91.3 to 94.7%, and OM ranged from 94.3 to 95.1%. Crude protein values were highest for the samples from Quincy Soybean (15.5%) and lowest for the samples from Cargill (9.2%). However, because SH were incorporated into the diet at only 7.5%, this variation did not significantly alter total CP concentration of the diets. The TDF concentration was highest for the sample obtained from Central Soya (80.7%) and lowest for the sample from Quincy Soybean (63.8%). The average TDF value from the five sources was 74.7%, which is similar to the 75.0% value determined by Lo (20) and the 75.6% value determined by Slavin (21) . Among SH sources, the concentration of insoluble fiber was higher than the concentration of soluble fiber. The average insoluble fiber value was 66.8% compared with 59.4 and 71.0% reported by Lo (20) and Slavin (21) , respectively. The average soluble fiber value was 7.9% compared with 15.4 and 4.0% reported by Lo (20) and Slavin (21) , respectively. On average, 89% of the TDF in our samples was insoluble fiber and 11% was soluble fiber. However, when I:S was calculated, it revealed a wide range of values, from 15.4 (Quincy Soybean) to 5.0 (Jones-A). The chemical composition of the SH can be affected by many factors including time of harvest, conditions under which the plant was grown and processing technologies used to prepare the fiber source (22) .

The chemical composition of the experimental diets is reported in Table 3 . The seven diets contained similar concentrations of DM, OM, CP and fat. Lower TDF concentrations were observed in the control diet (3.2%) and BP-containing diet (6.6%) compared with the SH-containing diets (avg. 8.0%). Within the SH-containing diets, TDF concentrations were highest for diet 3.17 (8.6%) and lowest for diets 1.86 (7.4%) and 5.18 (7.4%). Due to the use of different SH sources in the diets, the percentages of dietary insoluble and soluble fiber were different, as intended. Concentrations of essential (EAA) and nonessential amino acids (NEAA) were similar among diets.

Extrusion alters the ratio of I:S in the extrudate. Gualberto et al. (23) studied the effects of extrusion on I:S for wheat, oat and rice bran. It was found that the insoluble fiber content decreased and the soluble fiber content increased in all brans after extrusion (P < 0.05). The high temperatures, pressure and shear force that the diet is exposed to during extrusion will change the physical characteristics of the hemicelluloses of the fiber. When hemicelluloses are extruded, particle size changes, thus altering solubility and the I:S of the diet (24) . Pederson et al. (25) studied the effects of processing on the composition of three pale-seeded varieties of Amaranthus caudatus. When heat was applied to the seeds, the proportion of soluble fiber was increased in one of the three varieties. The other two varieties did not show any increase in soluble fiber. This indicates that different varieties within the same plant genus and species can have different responses to heat processing. Little research has been done on the effects of processing on SH.

Insoluble to soluble fiber ratios of the diets herein were calculated on the basis of the composition of the control diet and SH source. The following equation was used to calculate the pre-extrusion I:S of the SH-containing diets:

where A is the insoluble fiber percentage of the basal mix (BM) or control diet; B is the percentage of BM in the SH-containing diets; C is the insoluble fiber percentage of SH; D is the percentage of SH in the SH-containing diets; E is the soluble fiber percentage of BM; and F is the soluble fiber percentage of SH.

The calculated and measured ratios of I:S in extruded diets containing SH are presented in Table 4 . When extruded, the five diets responded differently. Compared with the calculated ratios, the measured I:S of two diets increased, two diets decreased and the calculated I:S of one diet was similar to that of the actual I:S. There is relatively little research that has documented the effect of extrusion on I:S in the diet. It is clear that extrusion processing effects on I:S require further investigation.

Nutrient intake and digestibility data are reported in Table 5 . Intakes of DM, OM, CP, fat and GE were similar among diets. Due to differences in dietary TDF concentrations, dogs consuming the control diet had lower (P < 0.01) TDF intakes than dogs consuming the fiber-containing diets. Also, dogs consuming the BP-containing diet had lower (P < 0.01) TDF intakes than dogs consuming the SH-containing diets. No differences in TDF intake were observed among the SH-containing diets.

Ileal digestibilities of DM, OM, CP, fat and GE were lower (P < 0.05) for dogs fed the fiber-containing diets than for dogs fed the control diet. Schultz et al. (26) found a similar depression in ileal digestibilities of DM, OM and CP in pigs as the amount of DF increased. The apparent digestibility of dietary nutrients decreases with fiber supplementation due to the replacement of digestible nutrients with components that are not digested or absorbed in the small intestine, and possibly to an increase in endogenous secretions in response to some types of fiber (27 ,28) . Cole et al. (6) fed a diet containing no supplemental fiber with an ingredient composition identical to the control used in this study. Ileal digestibility values for DM (76.6%), OM (81.8%), CP (71.1%), fat (94.5%) and GE (83.7%) closely resembled digestibility values of the control in this study.

Despite the slightly higher TDF intakes of the dogs fed the SH-containing diets compared with those fed the BP-containing diets, there were no differences in digestibilities of any nutrients at the terminal ileum of dogs fed the BP vs. SH-containing diets. In a similar study by Cole et al. (6) , there were no differences in ileal digestibilities of nutrients between SH-containing diets and a BP-containing diet. Replacement of BP by SH as a fiber source in extruded, premium dog diets does not seem to have a negative effect on nutrient digestibility at the ileum. Within the BP and SH-containing diets, we observed negative TDF digestibilities. The negative values can be attributed to low levels of TDF in the diet. A small increase in analyzable TDF could be amplified to a large negative digestibility value.

Among the SH-containing diets, ileal digestibilities of DM and OM demonstrated quadratic effects (P < 0.05) in response to increasing I:S of the diet. The SH-containing diets with the highest (5.18, 7.21) and the lowest I:S (1.86) resulted in the highest digestibilities of DM and OM. The SH-containing diets with intermediate I:S of 2.65 and 3.17 resulted in lower digestibilities of DM and OM. Trends for quadratic effects in response to increasing I:S of the diet occurred for ileal digestibilities of CP (P = 0.062) and fat (P = 0.085). No differences were observed in TDF or GE digestibilities at the ileum. Overall, when dogs were fed the two SH-containing diets with intermediate I:S (2.65 and 3.17), a decrease in ileal digestibilities of nutrients was observed. The implication is that there is an intermediary I:S that is detrimental to ileal digestibilities of DM, OM, CP and fat compared with higher or lower I:S ratios.

To understand how the intermediate I:S could have a greater negative effect on ileal digestibilities compared with higher levels of either insoluble or soluble fiber alone, the differential effects of insoluble vs. soluble fiber on physiologic events that could influence digestion must be discussed. Insoluble fiber is associated with a decreased intestinal transit time, increased fecal bulk and poor fermentability (29) . Soluble fiber is associated with delayed gastric emptying, decreased glucose absorption rate, reduced intraluminal pH, altered cecocolonic microflora and hypocholesterolemic effects (30) . According to Blaxter et al. (31) , the effect of soluble fibers on small intestinal nutrient absorption is associated with their ability to hydrate rapidly and form a viscous gel. This delays gastric emptying and reduces the rate of absorption of glucose and other digestion end-products from the small intestine.

In this experiment, ileal digestibilities were decreased in dogs consuming diets with fiber compared with the control diet, probably as a result of decreased intestinal transit time (high I:S) and negative effects on absorption due to increased viscosity (low I:S). It is our hypothesis that the dogs fed the diets with intermediate I:S displayed greater decreases in ileal digestibilities due to a synergistic effect of the higher viscosity of soluble fiber and the decrease in transit time associated with insoluble fiber. Each of these effects alone would be likely to decrease digestibility, and a combination of these effects elicited by the presence of both fiber types may account for the observed quadratic effect in ileal digestibilities around the intermediate I:S.

Apparent total-tract digestibilities.

As expected, the control diet resulted in the highest total-tract digestibilities. Compared with the control, diets containing supplemental fiber had lower (P < 0.05) digestibilities of DM, OM, fat and GE. Similarly, Cole et al. (6) found negative linear effects (P < 0.05) of fiber inclusion on total-tract digestibilities of DM, OM and GE. In a similar study, a depression in total-tract digestibility of DM, CP and fat was observed in dogs fed supplemental fiber (32) . The decrease in total-tract digestibilities can be attributed in part to the replacement of digestible nutrients with less digestible components.

Total-tract digestibility of OM by dogs fed the diet containing BP was higher (P < 0.05) than values for dogs consuming diets containing SH. There were trends for DM (P = 0.109) and GE (P = 0.079) digestibilities to be higher for dogs consuming the BP-containing diet compared with dogs consuming the SH-containing diets. There were no differences in CP or fat digestibilities for the BP vs. SH-containing diets. The differences in DM, OM and GE digestibilities between the BP and SH-containing diets could be due in part to the differences in TDF intakes. Dogs consuming the BP-containing diet consumed less (P < 0.01) TDF than dogs fed the SH-containing diets. As stated earlier, an increase in TDF intake will decrease total-tract DM, OM and GE digestibilities. The differences in digestibility also may be affected by the fiber source. Sunvold et al. (9) studied the effects of single sources and blends of dietary fibers in dog foods and reported that total-tract digestibilities of dietary nutrients can be affected by dietary fiber source.

Total-tract digestibilities of nutrients were not affected by I:S ratio among the SH-containing diets. Statistically, there was a linear effect (P = 0.05) on total-tract TDF digestibilities as I:S increased within the diet. However, the biological importance of this effect is doubtful because the TDF total-tract digestibilities were -8.5, -9.6, 11.6, -7.3 and -10.4 for diets 1.86, 2.65, 3.17, 5.18 and 7.21, respectively. Cole et al. (6) also reported negative total-tract digestibility values for TDF in SH diets fed to dogs. Again, negative TDF digestibilities can be attributed to low levels of TDF in the diet (average TDF = 8% of SH diets). Therefore, a small increase in analyzable TDF in feces will be amplified to a large negative digestibility value. A small decrease in analyzable TDF could account for the 11.6% digestibility for diet 3.17. Also, there are substances such as chondroitin sulfate and hyaluronic acid present in the poultry by-product meal that will analyze as TDF.

Amino acid intakes and apparent ileal digestibilities.

There were no differences in intakes of any amino acids when the control diet is compared with the fiber-containing diets, or the BP-containing diet with the SH-containing diets (Table 6 ). Also, there were no effects of increasing I:S within the SH-containing diets on intakes of amino acids.

Soluble dietary fiber can increase viscosity of digesta. Larsen et al. (27) studied the effects of dietary fiber viscosity on apparent ileal amino acid digestibility. Rats were fed purified casein-based diets containing carboxymethylcellulose of low, medium and high viscosity. They found that delayed passage rate of the more viscous digesta may have resulted in greater absorption of amino acids. Ileal digestibility values for most amino acids were higher for rats consuming the high viscosity diets compared with the low viscosity diets. Insoluble dietary fiber decreases digesta transit time and may also affect ileal digestibility of amino acids. Lenis et al. (33) found that the addition of wheat bran NDF to diets of pigs decreased (P < 0.001) ileal digestibility of most amino acids. Larsen et al. (27) found that as fiber viscosity increased, there was a significant linear increase in the output of endogenous amino acids at the terminal ileum of growing rats. Thus, increased outputs of endogenous amino acids could have resulted in a decrease in apparent digestibility of amino acids in dogs in the current experiment. These three studies demonstrate the variable effects that soluble and insoluble dietary fiber can have on ileal digestibilities of amino acids.

In our study, the SH-containing diets had higher concentrations of insoluble dietary fiber. However, the proportion of I:S was different in each of the SH-containing diets. It is hypothesized that the variant combinations of insoluble and soluble fiber produced different combinations of effects than the insoluble or soluble fibers alone. Differences in viscosity, transit time and endogenous secretions may have interacted and led to a decrease in apparent ileal digestibility of amino acids at the intermediate I:S ratios for the SH-containing diets.

Fecal characteristics.

Corrected fecal outputs (g wet feces/100 g DM intake) were lower (P < 0.001) when dogs consumed the control diet vs. the fiber-containing diets (Table 8 ). There was no difference in corrected fecal output between the BP-containing diet and the SH-containing diets. Diez et al. (34) studied the influence of sugar-beet fiber, guar gum and inulin on fecal output. They found that all fibers increased wet fecal output. Cole et al. (6) also found that a diet containing no added fiber resulted in lower fecal excretion compared with fiber-containing diets.

The BP-containing diet had 70% moisture in the feces (100% - 30% DM) compared with an average of 65% moisture in the SH-containing diets. The feces of the dogs consuming the BP-containing diet had a significantly (P = 0.001) higher water holding capacity. However, we observed no differences when comparing the fecal scores.

We conclude that varying I:S in dog diets results in changes in fecal characteristics and digestibilities at the terminal ileum. As the ratio increases, there is an increase in fecal output. A SH-containing diet with a low I:S (<2) decreases the amount of wet feces excreted and minimizes negative effects on ileal digestibilities of nutrients in the diet. Diets containing SH that have higher I:S fiber ratio (>5) will also minimize detrimental effects on nutrient digestibilities at the ileum, but will result in higher wet fecal output.

	FOOTNOTES

 
¹ Supported in part by a grant from the United Soybean Board (SBA USB 7310 FAH), St. Louis, MO.

² The senior author was supported by a Jonathan Baldwin Turner Graduate Fellowship awarded by the University of Illinois College of Agricultural, Consumer and Environmental Sciences.

⁴ Present address: The Iams Company, Lewisburg, OH 45338-0189.

⁵ Abbreviations used: AAFCO, Association of American Feed Control Officials; BP, beet pulp; CP, crude protein; DF, dietary fiber; DM, dry matter; EAA, essential amino acids; GE, gross energy; I:S, ratio of insoluble to soluble fiber; NEAA, nonessential amino acids; OM, organic matter; PBM, poultry by-product meal; SH, soybean hulls; TAA, total amino acids; TDF, total dietary fiber.

Manuscript received January 16, 2001. Initial review completed February 26, 2001. Revision accepted April 18, 2001.

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