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ANIMAL NUTRITION |
* Departments of Animal and Poultry Science,
and
Land Resources, and
and
Agricultural Economics, University of Guelph, Guelph, Ontario N1G 2W1, Canada
Abstract
The excretion of major odor-causing and acidifying compounds in response to dietary supplementation of chicory inulin extract was investigated with six Yorkshire barrows, with an average initial BW of 30 kg, according to a balanced two-period cross-over design. The animals were fed a control diet containing no inulin extract and a treatment diet with 5% inulin extract (as-fed basis) at the expense of cornstarch. Each diet was formulated (as-fed basis) to contain 16% CP from corn (51%) and soybean meal (29%). Each experimental period lasted 14 d, with 10 d for dietary adaptation and 4 d for collection of fecal and urine samples. The fecal samples were analyzed for four major classes of odor-causing and acidifying compounds: 1) VFA; 2) N-containing compounds, including total N and ammonia; 3) volatile sulfides measured as hydrogen sulfide units; and 4) phenols and indoles, including p-cresol, indole, and skatole. Supplementation of chicory inulin at 5% had no effects on the fecal excretion of VFA (P = 0.29), ammonia (P = 0.96), total volatile sulfides (P = 0.56), p-cresol (P = 0.56), and indole (P = 0.75). Fecal excretion of total N (inulin = 6.13 vs. control = 5.10 g/kg DMI) was increased (P < 0.05), whereas urinary total N excretion (inulin = 15.1 vs. control = 16.4 g/[pig•d]) was not affected (P = 0.17) by the inulin supplementation compared with the control group. Furthermore, fecal excretion of skatole (inulin = 9.07 vs. control = 18.93 mg/kg DMI) was decreased (P < 0.05) by the inulin supplementation compared with the control group. In conclusion, dietary supplementation of 5% chicory inulin extract is effective in decreasing the fecal excretion of skatole in growing pigs fed corn and soybean meal diets.
Key Words: Chicory Inulin • Feces • Odor-Causing Compounds • Pigs
Introduction
The progression toward sustainable swine production must involve nutrient management procedures that minimize the excretion and emission of odor-causing and acidifying compounds into the environment (Honeyman, 1996
). Several pressing issues surround the environmental loss of these compounds. Firstly, offensive odor compounds that are emitted from swine-holding units have strained the strong relationship that once existed between swine farmers and surrounding communities (Honeyman, 1996; Miner, 1999). Secondly, odor compounds may compromise the health and well-being of the people and animals that are constantly exposed to them (Schiffman, 1998). Thirdly, volatile compounds that are emitted from swine manure, particularly ammonia (NH3) and volatile sulfides, contribute to the production of acid rain and the acidification of surface soil and water resources (van Breemen et al., 1982; Ferm, 1990; Jongbloed and Lenis, 1998). The supplementation of indigestible dietary fiber components in the form of nonstarch polysaccharides (NSP) has been effective in altering nutrient excretion patterns and reducing the fecal loss of odor components (Canh et al., 1997; Mroz et al., 2000). Inulin, a NSP extracted from the chicory root, has been shown to be an effective dietary supplement for decreasing the volatilization of NH3 from swine manure slurry (Cromwell et al., 1999). Thus, it is likely that the dietary supplementation of chicory inulin may alter the patterns of microbial fermentation in the large intestine to decrease the biogenesis and excretion of major odor-causing and acidifying compounds in the pig during feeding.
Therefore, the objective of this study was to examine the excretion of major odor-causing and acidifying compounds, including VFA, N-containing compounds, volatile sulfides, phenols, and indoles, in response to dietary supplementation of 5% chicory inulin extract in growing pigs fed corn and soybean meal diets.
Materials and Methods
Animals, Diets, and Experimental Design
Six Yorkshire barrows, with an average initial BW of 30 kg, were acquired from the Arkell Swine Research Station at the University of Guelph and transported to the animal wing of the Department of Animal and Poultry Science of the university. The barrows were placed in an environmentally controlled room at 20°C and were individually housed in stainless-steel metabolic crates (height = 83 cm, length = 145 cm, width = 86 cm) that allowed for separate collection of fecal and urine samples. Water for each pig was suspended from the ceiling in 9-L storage containers and was available from a low-pressure drinking nipple, which allowed water intake to be monitored throughout the experiment.
Two corn/soybean meal-based diets were formulated to contain the same levels of CP and AA (Table 1). The dietary contents of DE, CP, essential AA, minerals, and vitamins were formulated to meet the levels recommended by NRC (1998). The nutrient composition of the diets was similar but differed in the inclusion level of the chicory inulin extract. The control diet contained no inulin extract, whereas the treatment diet included 5% chicory inulin extract at the expense of cornstarch. As information regarding the available energy contribution from inulin in a corn/soybean diet is not presently available, it was considered to be negligible. Chromic oxide was included at a level of 0.3% as an indigestible marker to measure and express the fecal excretion of various volatile compounds on a DMI basis. The diets were administered twice daily at 0900 and 1600, respectively, close to ad libitum intake (5.5% of BW/d).
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The experiment was conducted according to a balanced two-period crossover design according to Kuehl (2000). Each experimental period lasted 14 d, with 10-d adaptation to the diets and a 4-d sample collection period.
Sample Collection and Processing
Fecal grab samples were collected in the daytime after the morning feeding between d 11 and 14 of each experimental period. Fresh fecal samples were collected at 2-h intervals in containers with sealed lids and were immediately stored at 4°C for the duration of the period. The collected fecal and diet samples were freeze-dried and ground into a homogenous mixture with a mortar and pestle.
Urine samples were obtained by using a funnel-shaped metal tray secured to the base of the webbed floor of the metabolic crate. Urine flowed from the metal tray into a collection container placed in an electronic cooler beneath the metabolic crate. The coolers were maintained at a temperature of 4°C to reduce microbial activity and avoid urea degradation and NH3 loss during the collection period. The total volume of urine collected each day was recorded and stored at 4°C for the remainder of the experimental period.
Chemical Analyses
Fecal and diet samples were analyzed for DM content according to AOAC procedures (1993). Total N content in diet, freeze-dried fecal samples, and urine samples was analyzed according to the combustion method (Dumas procedure) on a Leco FP-428 N Analyser (Leco Corporation, St. Joseph, MI) according to AOAC (1993) procedures. Contents of NDF and ADF in the feed ingredients (corn and soybean meal) were determined on a FiberTec System (Tecator, Hoganas, Sweden) according to Goering and van Soest (1970). Heat-stable 
-amylase was used during the fiber analyses of these samples.
Chromic oxide contents in diets, and freeze-dried fecal samples were determined with an atomic absorption spectrometer (SpectrAA-10/20; Varian, Mulgrave, Australia) at 375 nm with a slit width of 0.5 nm according to Saha and Gilbreath (1981). Approximately 1.0 g of diet and 0.4 to 0.6 g of feces were weighed into 100-mL Pyrex beakers and ashed overnight at 550°C. Chromic oxide, as part of the resulting ash, was then oxidized to dichromate by digestion in 6 mL of phosphoric acid (16.7 mM)—manganese sulfate (13.5 mM) solution and mixed with 8 mL of potassium bromate (0.27 mM) solution on a hot plate. Potassium dichromate was used as the standard compound.
For the determination of fecal pH, approximately 2.0 g of fresh feces was weighed into a glass beaker and mixed with 50 mL of distilled and deionized water. Fecal pH values were measured at room temperature (20°C) as the mixture was stirred on a magnetic stirring plate using a pH/ATC combination probe (Accumet Basic AB15; Fisher Scientific, Pittsburgh, PA).
For the determination of fecal NH3-N content, a 2.0-g freshly frozen sample, mixed with 30 mL of distilled and deionized water, was homogenized with a Power Gen homogenizer (700D, Fisher Scientific) at 10,000 rpm for 2 min and centrifuged at 800 x g for 15 min. The supernatant was removed, and an aliquot of the sample was taken for the determination of total NH3-N content, including both ammonia and ammonium by spectrophotometric analysis at 625 nm according to Weatherburn (1967).
For the determination of total fecal volatile sulfide content, a 2.0-g freshly frozen sample, mixed with 25 mL of cadmium hydroxide (18 mM cadmium sulfate and 7.5 mM sodium hydroxide) solution was homogenized with a Power Gen homogenizer (700D, Fisher Scientific) at 10,000 rpm for 2 min and was centrifuged at 800 x g for 15 min. The supernatant was removed and analyzed for total volatile sulfide content as hydrogen sulfide (H2S) units by spectrophotometric analysis at 670 nm by using sodium sulfide (Na2S) as the standard compound according to Jacobs et al. (1957).
For the analyses of other volatile odor compounds, including VFA, phenols, and indoles, pulverized freshly frozen fecal samples (2 g) were extracted with 100% methanol (6 mL). Following the extraction procedure, the samples were homogenized with a Power Gen homogenizer (700D, Fisher Scientific) at 10,000 rpm for 2 min and centrifuged at 800 x g for 20 min. Decanol (0.1244 g per tube) was added at the beginning of the extraction as an internal standard for quantification. The supernatant was analyzed by a gas chromatography-mass spectrometer (GC-MS) with a 6890-GC coupled with a Hewlett-Packard 5973N mass selective detector (Agilent Technologies Inc., Wilmington, DE). The mass spectrometer was operated on the electron impact mode at 70 eV, with typical scanned ranges of 35 to 400. The GC-MS system was programmed and controlled using a Hewlett-Packard Vectra 486/66U computer with Hewlett-Packard ChemStation software. A HP-1 capillary GC column (30 m x 0.32 mm i.d. x 5 µm film thickness, Agilent Technologies Inc.) was used for the chromatographic separation. The injection port of the GC was maintained at a temperature of 220°C. The column temperature was programmed to increase from 60 to 225°C at 5°C/min. Sample injection volume was 1 µL with a 1:2 split ratio. Target compounds were identified by matching the mass spectra of the total ion chromatographic peaks to reference spectra from a Wiley NBS mass spectral reference library carried by the GC-MS system. Compound identities were further confirmed by comparing the retention time and mass spectra to those of authentic standard compounds in the solvent. The major volatile compounds identified and well-quantified were acetic acid, butyric acid, p-cresol, indole, and skatole.
Calculations and Statistical Analyses
Fecal excretion of major odor-causing volatile compounds was calculated according to Eq. [1] (Fan and Sauer, 1997).
 | [1] |
where Cd represents fecal excretion expressed on the basis of DMI (grams per kilogram DMI); Cs is fecal content of odor compounds (grams per kilogram DM feces); Md is marker content in the diets (%, on DM basis); and Mf is marker content in the feces (%, on DM basis).
The individual pig was the experimental unit. Data were subjected to ANOVA according to a two-period crossover design using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). All end point measurements were compared at the significance level of P < 0.05.
Results
The animals remained healthy throughout the duration of the experimental periods and no difference in feed and water (P = 0.39) intakes were observed between the control and the inulin-supplemented group (Table 2). Although all the individual short-chain fatty acids and the total VFA contents were numerically high in the inulin group (Table 2), there were no differences (P > 0.05, see Table 2 for individual P-values) in the fecal excretion of VFA between the control and the inulin-supplemented group. However, the inulin-fed group did have a lower (P < 0.05) fecal pH value than that of the control group.
|
). However, the total urinary N loss (inulin = 15.1 ± 0.5 vs. control = 16.4 ± 0.5 g/[pig•d], mean ± SEM; n = 6; P = 0.17) and urinary total N content (inulin = 6.20 ± 0.50 vs. control = 5.91 ± 0.50 g/L; mean ± SEM; n = 6; P = 0.48) were similar between the two groups. Furthermore, there were no differences in the fecal content and excretion of total ammonia N (P = 0.96), including both NH3 and ammonium, and total volatile sulfides (P = 0.56), in response to dietary supplementation of chicory inulin (Table 3).
|
). However, there was a decrease (P < 0.05) in the fecal content and excretion of skatole in the inulin-supplemented group when compared with the control (Table 3). Discussion
The objective of this study was to examine possible changes in the excretion of major odor-causing and acidifying compounds from growing pigs fed corn/soybean meal diets in response to dietary supplementation of 5% chicory inulin extract.
Three underlying factors were influential in establishing the 5% inulin supplementation level. To begin, previous work in our laboratory determined that supplementing apple pectin, a water-soluble NSP, at a level of 4.5% to corn/soybean meal-based diets decreased the emission of both NH3 and volatile sulfides from the fresh manure slurry of growing pigs (Gao et al., 2000). Secondly, owing to processing factors, the crude inulin extract had a bitter flavor and a preliminary feeding trial suggested that dietary supplementation at a level exceeding 6% decreased feed intake (data not shown). Thirdly, there was a concern that the dietary inclusion of excessive levels of the inulin extract could compromise nutrient digestibility and increase fecal loss of essential endogenous nutrients, such as amino acids, calcium, and phosphorus.
Although bacterial fermentation in pigs contributes substantially to the digestion of dietary and endogenous nutrients (Alpers, 1994; Grieshop et al., 2001), this microbial activity also produces such compounds as VFA, indoles, and phenols that contribute to swine odor and environmental acidification (Mackie et al., 1998). The VFA profiles reported in the present investigation are atypical in that the concentration of propionate was higher than that of acetate. Although it has been speculated that the relatively high molecular weight of inulin compared with similar NSP may contribute to an unusual VFA profile on fermentation (Nyman, 2002), it is unknown why a similar response was observed in the control-fed pigs. Whereas inulin consumption generally yields high levels of VFA in the rat model (Levrat et al., 1993; Younes et al., 2001), the majority of research conducted with human subjects has indicated no effects of inulin consumption on fecal VFA concentrations (Gibson et al., 1995; Alles et al., 1996). The decreased fecal pH of the inulin-supplemented group observed in the current study is difficult to explain in the absence of a statistically significant change in fecal VFA content. However, the numerical increase in fecal VFA excretion in the inulin-supplemented group, although not statistically significant, may nonetheless provide a biological explanation for the decreased fecal pH.
Volatile sulfides represent a wide range of sulfur-containing compounds produced through both in vivo fermentation in the hindgut and in vitro anaerobic fermentation of manure slurry during storage (Kadota and Ishida, 1972; Avery et al., 1975; Banwart and Bremner, 1975). In a related study, chicory inulin was shown to be effective in decreasing (P < 0.05) the sulfide content (22.20 vs. 38.11 µg/g DM) in the fresh manure slurry of growing-finishing pigs (Rideout et al., 2001). Chicory inulin supplementation did not affect the fecal content and excretion of total volatile sulfides in the current study. Therefore, it seems that any reduction in the production and excretion of volatile sulfides in response to inulin supplementation may be related to differences in the postabsorptive urinary loss of inorganic sulfur-containing compounds and the time period allowed for anaerobic in vitro fermentation during the manure storage.
Dietary supplementation of inulin at 7, 15, and 45% has also been shown to enhance total fecal N loss in beagles, rats, and humans (Levrat et al., 1993; Diez et al., 1998). Inulin is considered unlikely to depress dietary protein digestibility in the upper gastrointestinal tract (Levrat et al., 1993; Younes et al., 1995). The apparent depressive effect of inulin on protein digestibility often reflects an increase in microbial protein synthesis and/or augmented endogenous protein loss. If the increased N excretion observed in the present investigation was indeed of microbial origin, one might expect a net flux of urea N from the blood to the intestine and a concomitant decrease in total urinary N excretion. Indeed, such a shift in N excretion from the renal to the intestinal site has been shown in rats adapted to diets containing 15% chicory inulin (Levrat et al., 1993). As no such shift in total urinary N excretion is evident in the present investigation, it is possible that any increases in microbial growth from the breakdown of inulin may have been sustained with increases of N excretion from the endogenous sources. Therefore, the increased total fecal-N loss might have been of the endogenous origin. However, the authors are not aware of any literature reports regarding the effect of inulin consumption on the endogenous N loss in pigs and this deserves future investigation.
The concomitant increase in fecal-N loss and decrease in fecal skatole excretion may seem contradictory, but it can be reconciled in light of the main factors that potentially regulate skatole production in the hindgut. Two important factors that regulate intestinal skatole production are the activity of the resident proteolytic bacteria and colonic pH (Jensen et al., 1995). Previous work has shown that the production of protein metabolites from microbial fermentation may be reduced by the addition of an alternative energy source, such as nonstarch polysaccharides. Thus, the preferential metabolism of inulin by carbohydrate-fermenting bacteria may have decreased the activity of the proteolytic bacteria and effectively reduced the breakdown of tryptophan into skatole (Yokoyama and Carlson, 1979; Jensen et al., 1995; Boyd and Lichstein, 1955). Furthermore, microbial proteases have been shown to function optimally at neutral or alkaline pH (MacFarlane and Cummings, 1991). The lower fecal pH associated with the inulin group, although not entirely reflective of the conditions in the large bowel, may nonetheless explain the decreased skatole excretion. As indole is also produced by the microbial degradation of tryptophan, it is surprising that inulin supplementation did not affect the excretion of indole to the same extent as skatole. However, because the factors influencing the relative production of indole and skatole have not been fully elucidated (Jensen et al., 1995), more research is needed to clarify the role of inulin in the production of tryptophan metabolites. Alternatively, the increased microbial biomass that is often observed in response to dietary fiber consumption may serve as a source of tryptophan for the synthesis of indoles (Lundstrom et al., 1988). Indeed, previous work has shown an increase in the daily fecal excretion of skatole and indole in pigs fed a diet supplemented with sugar-beet pulp (Hawe et al., 1992). In a similar manner, it is possible that the presence of inulin may have indirectly led to increased skatole production but simultaneously altered colonic conditions that favored skatole absorption from the hindgut. Lundstrom et al. (1988) reported that the consumption of dietary fiber in the form of wheat bran, oat bran, hay meal, and yellow peas increased the concentration of skatole in fat compared with low-fiber diets. Unfortunately, as plasma skatole levels were not measured in the present investigation, it is unclear whether inulin supplementation led to an increase in the production and ultimate absorption of microbially produced skatole in the plasma.
In conclusion, dietary supplementation of 5% (as-fed basis) chicory inulin extract did not affect the fecal content and excretion of VFA, NH3, volatile sulfides, p-cresol, and indole from growing pigs fed corn/soybean meal-based diets. Furthermore, although chicory inulin supplementation at 5% seemed to be ineffective in decreasing the fecal and urinary N excretion, it decreased the fecal excretion of skatole. Further research is needed to clarify the mechanism(s) by which dietary inulin reduces the fecal excretion of skatole in growing pigs.
Implications
Skatole is usually present in a very trace amount in swine manure, and its biogenesis via large intestinal fermentation is partially responsible for swine odor. The supplementation of chicory inulin at 5% (as-fed basis) to corn/soybean meal diets may be a practical strategy for decreasing swine odor associated with the biogenesis and fecal excretion of skatole.
Footnotes
1 This research was supported by grants from Ontario Pork Producers’ Marketing Board, Ontario Ministry of Agriculture and Food—Univ. of Guelph Animal and Resources Management and Environment Research Programs, and Quali-Tech Foods, Toronto, Ontario, Canada (to M. Z. Fan). We are grateful to D. Wey and P. Devries for assistance with animal management, and to M. Hansel and I. McMillan for help with chemical and statistical analyses. 
2 Correspondence: Room 250, #70 Animal Science/Nutrition Building (phone: 519-824-4120, ext. 53656; fax: 519-836-9873; e-mail: mfan{at}uoguelph.ca).
Received for publication March 24, 2003. Accepted for publication February 12, 2004.
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