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J. Anim. Sci. 2003. 81:1754-1763
© 2003 American Society of Animal Science

Ammonia, volatile fatty acids, phenolics, and odor offensiveness in manure from growing pigs fed diets reduced in protein concentration1,2

E. R. Otto*,3, M. Yokoyama*, S. Hengemuehle*, R. D. von Bermuth{dagger}, T. van Kempen{ddagger} and N. L. Trottier*,4

* Department of Animal Science and and {dagger} Department of Agricultural Engineering, Michigan State University, East Lansing 48824; and and {ddagger} Department of Animal Science, North Carolina State University, Raleigh 27695

4 Correspondence:
2209 Anthony Hall (phone: 517-432-5140; fax: 517-432-0190; E-mail:
trottier{at}pilot.msu.edu).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The objective of this study was to investigate whether reducing dietary CP concentration decreases fecal VFA, manure ammonia (NH3) emission and odor, and urinary phenolic metabolites. Six barrows were allotted to one of six dietary treatments in a Latin square design. Treatments consisted of four corn–soybean meal based diets containing 15, 12, 9, and 6% CP, a casein-based diet containing 15% CP, and a protein-free diet (0% protein). Crystalline AA were included in the 12, 9, and 6% CP diets. The casein-based and protein-free diets were used to determine basal endogenous contribution of VFA, phenolics, NH3, and manure odor. Pigs were housed individually in metabolism cages to allow total collection of feces and urine. Feces and urine were collected and pooled within pig and period. Feces and urine were analyzed for VFA and phenolic metabolite concentrations, respectively. Feces and urine were then mixed, stored, and fermented at room temperature for 30 d. For NH3 determination, headspace air was sampled from manure slurries at 24, 48, and 72 h after fermentation. Slurry samples were placed into vials, capped, and randomized before odor panel evaluation. Odor offensiveness was classified on severity: 1 = non-offensive; 2 = mildly offensive; 3 = moderately offensive; 4 = strongly offensive; and 5 = extremely offensive. Reducing dietary CP increased (P < 0.05) fecal VFA concentrations but did not affect phenolic concentrations in urine. Manure NH3 emission was reduced (P < 0.05) as dietary CP concentration decreased from 15 to 0%. The 15% diet had the least offensive manure slurry with odor qualitative ranking of 2.58 (i.e., mild-moderately offensive). Compared with the 15% CP diet, manure from the 9 and 6% CP diets was found to be more offensive (P < 0.05), with qualitative rankings of 2.92 and 3.10, respectively. Odor qualitative rank for the 12% CP, protein-free diet, and casein-based diet did not differ from that of the 15% CP diet. These results indicate that reduction in dietary CP concentrations decreases manure NH3 emission, but it does not diminish manure odor offensiveness and fecal VFA concentrations.

Key Words: Ammonia • Manures • Odors • Phenolic Compounds • Pigs • Volatile Fatty Acids


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Nitrogen, ammonium (), and volatile organic compounds (VOC) are major components of pig manure contributing to environmental pollution (Zahn et al., 1997). Excessive land application of swine manure results in nitrate () contamination of surface and ground water (Jongbloed et al., 1997). Unutilized N contributes to ammonia (NH3) and VOC emission into the air (Miner, 1999). Volatile fatty acids represent a large portion of VOC and are responsible for a significant proportion of odor in emission plumes from swine production facilities (Zahn et al., 2001). Exposure to noxious odors and NH3 causes eye and respiratory irritations, headache and drowsiness, and increases the incidence of mood disturbances and negative emotions in people (Schiffman et al., 1995; Schiffman, 1998). Elevated aerial NH3 concentrations in confinement swine facilities may also delay the onset of puberty in gilts (Malayer et al., 1987). Consequently, nutritional and/or managerial means of reducing both NH3 and odor emission from livestock facilities may be necessary to ensure a sustainable production. Reducing dietary CP concentration decreases concentration in both fresh and stored manure (Sutton et al., 1996; 1999), and NH3 emission from manure (Turner et al., 1996; Canh et al., 1998). The effect of reducing CP on VOC concentration in manure or VOC emission is unclear. No information is available on whether decreasing dietary CP concentration decreases odor offensiveness. Currently, there are no federal guidelines regulating odors in the environment (Mackie et al., 1998). With increasingly restrictive environmental regulations, it is critical that more information be provided on manure characteristics from pigs fed a wide range of dietary CP concentration. Our main objective was to determine whether reducing dietary CP concentration below 15% reduces manure odor and NH3 emission, fecal VFA concentration, and urinary phenolic concentrations.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
Animals, Experimental Design, and Diets

Six barrows ([Yorkshire x Landrace] x Duroc), with an initial BW of 44.7 ± 1.8 kg were allocated to six dietary treatments in a 6 x 6 Latin square design. Pigs were penned individually in stainless steel metabolism pens (1.2 x 0.75 m) equipped with low-pressure water nipples providing free access to water. Pens had wire flooring that allowed feces to be collected on a fine-mesh wire screen. Stainless steel pans were placed below the screens to funnel urine into plastic collection vessels. Pigs were housed in an environmentally controlled room maintained at 21°C. Treatments consisted of four corn–soybean meal based diets containing 15, 12, 9, and 6% CP from the corn–soybean meal mixture, one diet containing no protein, and one casein-based diet containing 15% CP. Ammonia emission arising from obligatory endogenous N losses was determined using the protein-free diet and the casein-based diet. The protein-free diet was chosen to determine ammonia emission arising from nonspecific endogenous N losses, and the casein-based diet was used to determine ammonia emission arising from nonspecific endogenous N losses in the presence of a highly digestible dietary protein. Ingredient and nutrient composition for diets containing 15, 12, 9, and 6% CP are provided in Tables 1Go and 2Go, respectively; ingredient and nutrient composition for the casein-based and protein-free diet are provided in Tables 3Go and 4Go, respectively. A basal blend consisting of corn and soybean meal was prepared first and then used to mix all experimental diets. The basal blend was diluted with cornstarch to obtain the 12, 9, and 6 % CP. This was done to maintain an equal AA profile arising from protein-bound AA in corn and soybean meal. Diets were formulated to meet NRC (1998) recommended apparent ileal digestible AA and energy requirement for the 50-kg growing pig. Crystalline AA were added to the 12, 9 and 6% CP diets. L-Glutamic acid was added to the 9 and 6% CP diets to balance the N ratio of indispensable AA to dispensable AA to be 45:55 (Lenis et al., 1999). Corn oil was included in all diets to improve palatability and reduce dust. Solka floc was included as a source of indigestible fiber in all reduced-protein diets to insure proper bowel movement. Additional vitamin premix was provided in the 9 and 6% CP diets due to deficiency in biotin. The calculated and analyzed CP concentration for the 12, 9, and 6% CP diets were higher than the calculated CP concentration from the intact protein mixture of corn and soybean meal because these diets included the supplemental crystalline AA. The amount of feed offered was 3.5% of each pig’s BW, and it was divided into three equivalent meals per day (given at 800, 1200 and 1600). To reduce feed wastage, water was added to the meal (approximately 100 mL/300 g) and mixed to form a gruel. Body weights were measured on d 1 of each period.


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  		Table 1. Ingredient composition of experimental diets, as-fed basis
 

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  		Table 2. Nutrient composition of experimental diets, as-fed basis
 

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  		Table 3. Ingredient composition of casein-based and protein-free diets, as-fed basis
 

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  		Table 4. Nutrient composition of casein-based and protein-free diets, as-fed basis
 
Manure Slurry Preparation

At the conclusion of each collection period, stock manure slurries were prepared in the following manner. Fresh feces (200 g) was mixed with 1,000 mL of fresh urine (1:5, wt/vol) for each respective pig. The stock slurries were stored in 3.8-L plastic containers at room temperature (21°C) and allowed to ferment for a period of 30 d.

Ammonia Emission Testing

On d 30 of the fermentation period, manure slurries were manually shaken for approximately 30 s to disrupt any crust formation on the surface of the slurry sample and to homogenize the sample. Then, 25 mL of slurry was transferred into 100-mL glass beakers in duplicate. Beakers were covered tightly with aluminum foil and allowed to ferment for an additional 24 h. Using Gastec ammonia detector tubes (Gastec Corp., Gastec detector tube No. 3M, Kanagawa, Japan) the foil seal was punctured and headspace air was sampled approximately 2.5 cm above the slurry surface at a rate of 100 mL/min. Following air sampling, each slurry beaker was gently stirred with a wooden stick applicator to disrupt any crusting, and covered with aluminum foil. Headspace measurement was repeated 24 and 48 h later. Ammonia was averaged over the 3-d head space measurements.

Manure Odor

Approval for use of human subjects was granted by the Michigan State University Committee on Research Involving Human Subjects. Odor from d-30 manure was evaluated by static olfactometry in an odor panel (Schiffman and Williams, 1999; Armstrong et al., 2000) based on a direct scaling method (Sneath, 1994). Offensiveness represents one of the four factors defining odor nuisance referred to as FIDO (i.e., frequency, intensity, duration, and offensiveness) (Mackie et al., 1998). Odor offensiveness referring to the unpleasantness or character of the odor (Mackie et al., 1998) was rated according to a scale of 1 to 5, where 1 = not offensive, 2 = mildly offensive, 3 = moderately offensive, 4 = strongly offensive, and 5 = extremely offensive. Six samples of manure slurry per diet (10 mL each) were transferred from the stock manure slurries into a plastic vial containing a cotton ball and capped. The six sets of vials were allowed to rest for 1 h and double randomized prior to panelist evaluation. Every sample set contained all diets per collection period. The temperature of the ventilated laboratory where the odor panel was conducted was maintained at 20 to 22°C. The laboratory air had no detectable odors that would interfere with the panel evaluation. Four evaluation stations were located on lab benches throughout the laboratory.

A total of 34 volunteers (22 males and 12 females) participated throughout the duration of the odor panel evaluation. Volunteers were not trained panelists. However, a selection criterion was that the participant be familiar with livestock manure odors. The number of participants per panel averaged 13, with the number ranging from 7 to 17 participants. Thirteen of the volunteers participated three times or more. The panel participants were asked to sniff each sample individually and pause for a minimum of 3 min before sniffing the next sample. Individuals were asked to classify the severity of odor offensiveness. Responses were recorded by the participant immediately following the evaluation of each sample.

Volatile Organic Compounds

Volatile Fatty Acids. Feces from each pig, period, and diet were analyzed for VFA. Previously frozen fecal samples were thawed and 2-g samples were taken. Each fecal sample was diluted with 8 mL of distilled water and two drops of concentrated HCl, mixed, and centrifuged at 17,400 x g for 10 min at 4°C. The supernatant was filtered using a 0.22-µm filter (Millipore Co., Bedford, MA) and pipetted into 2.0-mL gas chromatography vials (Supelco, Cat. No. 27265, Bellefonte, PA). The VFA concentrations were determined using a gas chromatograph (Varian model 3700 FID, Varian, Inc., Walnut Grove, CA) equipped with a 2 m x 3.2 mm i.d. glass column packed with 10% SP-1200 and 1% H3PO4 on 80/100 Chromosorb (Supelco). Nitrogen was used as a carrier gas with a flow rate of 25 mL/min. Air and hydrogen gas were used for combustion with a flow rate of 30 mL/min. Samples were manually injected (2 µL) with temperature programming starting at an initial temperature of 110°C for 5 min, increasing to 127°C at a rate of 3°C/min, and holding at 127°C for 3 min to insure complete VFA volatilization. A standard solution containing 10 mmol/mL of each of the following VFA: acetate, propionate, isobutyrate, butyrate, isovalerate and valerate, was injected (2 µL) and a standard curve was determined.

Phenolic Compounds. Urine samples were thawed and centrifuged at 27,200 x g, 50°C, for 25 min. Supernatants were filtered (Whatman filter paper, No. 4), and 1 mL was transferred in duplicate into 2-mL gas chromatograph crimp top vials (Supelco, 2 mL, cat. no. 27058) containing 0.5 mL of a 3-ppm NaCl solution. Samples were analyzed using a gas chromatograph-mass spectrophotometer (Varian gas chromatograph CP-3800, Varian mass spectrophotometer Saturn 2000, Varian, Inc.). Two different polar solvent absorption fibers (polyacylate and polydimethylsioxane) of similar polarity were used.

Statistical Analysis

For each VFA and for p-cresol and 4-ethyl phenol, {chi}2 analysis (SAS Inst., Inc., Cary, SC) was performed prior to ANOVA to determine the frequency of responses (i.e., compound detection in sample analysis). Any diet with a frequency of VFA detection in the chemical analysis equal to or less than 50% was not included in the ANOVA. Analysis of variance for the dependant variables NH3, total VFA, acetate, propionate, isobutyrate, butyrate, isovalerate, and valerate, p-cresol, and 4-ethyl phenol were performed using the PROC MIXED procedure of SAS (SAS Inst., Inc.). The model included the effects of pig, period, and diet. Least squares means differences for NH3, VFA, total VFA, individual VFA as a percentage of total VFA, and phenolics were separated using the Tukey-Kramer multiple comparison test (Younger, 1998). Statistical significance was based on an experiment-wise type-I error rate of 0.05.

The odor panel results were analyzed using the GENMOD modeling procedures of SAS to estimate differences in manure odor offensiveness between diets. The statistical model included the dependent variable odor offensiveness (qualitative ranking) and the effects of panelist, gender of panelist, order in which sample was sniffed, pig, period, and diet. Estimates were reported as log odds ratios relative to the 15% CP diet. Log odds ratio differences between diets were nonorthogonally compared at P < 0.05.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Ammonia Emission

Headspace air NH3 from manure slurry from pigs fed the protein-free (0% protein), 6%, and 9% diets were similar, and were lower (P < 0.05) than that from the 12 and 15% CP diets (Figure 1Go). Manure slurry from the 15% CP and casein-based diets had similar NH3, which was higher than that from the 12% CP diet (P < 0.05).



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  		Figure 1. Ammonia in headspace air from fermented manures. Pigs (50 kg) were fed corn–soybean meal-based diets containing 15, 12, 9, and 6% CP, a casein-based diet containing 15% CP (15% Cas), and a protein-free diet (PF). Data are least squares means. Least squares means that do not have a common letter differ (P < 0.05).

 
Volatile Organic Compounds

Frequency of VFA, p-cresol, and 4-ethyl phenol detection in sample analysis are presented in Table 5Go. Diet affected the frequency of detection for isobutyric acid and butyric acid (P < 0.05), valeric acid (P < 0.1; trend), and for p-cresol and 4-ethyl phenol (P < 0.001). In pigs fed the casein-based diet, detection for most of the VFA in feces was only 50%. Thus, least squares means for VFA concentrations in Table 6Go were not reported for the casein-based diet (indicated by "—"). Volatile fatty acid concentrations in feces are reported in Table 6Go. Total VFA increased (P < 0.05) when feeding 12, 9, and 6% CP diets as compared to feeding the 15% CP, casein-based, or protein-free diets. Acetic acid concentration was not different among diets. Compared with the 15% CP diet, propionic acid concentration was not different from that in the 12 or 6% CP diets (P = 0.26) and was higher (P < 0.05) in the 9% CP diet. Isobutyric acid was not detected in feces from pigs fed the 15% CP diet. Isobutyric acid was not different among the 12, 9, and 6% CP diets. Butyric acid, isovaleric acid, and valeric acid concentrations were all higher (P < 0.05) in feces from pigs fed 12, 9, and 6% CP diets compared with those of the 15% CP diet. Propionic acid, isobutyric acid, butyric acid, isovaleric acid, and valeric acid concentration decreased (P < 0.05) in feces of pigs fed the protein-free diet when compared with those in feces of pigs fed the 15, 12, 9, and 6% CP diets. Of the phenolic metabolites measured, only p-cresol and 4-ethyl phenol were detected in urine samples and no differences among diets were found (Table 6Go).


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  		Table 5. Frequency of volatile fatty acid detection in feces and phenolic compounds in urine from pigs fed various dietary crude protein concentrations, a protein-free diet, or a casein-based dieta
 

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  		Table 6. Volatile organic compounds in fresh feces and urine from pigs fed various dietary crude protein (CP) concentration, a protein-free diet, or a casein-based dietab
 
Percentages of individual VFA relative to total VFA concentration in feces are presented in Table 7Go. The proportion of acetic acid and propionic acid to total VFA fecal concentration was lower (P < 0.05) in the 12, 9, and 6% CP diets compared with those of the 15% CP diet. Isobutyric acid, butyric acid, isovaleric acid, and valeric acid as a percentage of total VFA were higher (P < 0.05) in feces of pigs fed the 12, 9, and 6% CP diet compared with those of the 15% CP diet. Acetic acid was the main VFA contributing to total fecal VFA in pigs fed the protein-free diet and was higher (P < 0.05) than that in feces of pigs fed any other diets. Other fecal VFA contributed minimally to the total VFA in pigs fed the protein-free diet.


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  		Table 7. Individual fecal volatile fatty acids (VFA) relative to total fecal VFA from pigs fed diets varying in crude protein concentrationa,b
 
Odor Offensiveness

Mean odor offensiveness rankings were 2.58, 2.77, 2.92, and 3.10 for the 15, 12, 9%, and 6% CP diets respectively. Mean odor offensiveness rankings were 2.70 and 2.81 for the protein-free and casein-based diets, respectively. Odor offensiveness rankings for each diet are reported as log odds ratios relative to the 15% CP (Figure 2Go) and indicates the likelihood of increased odor offensiveness. Differences in log odds ratios between the reduced CP diets and the 15% CP diet were significant (P < 0.05) for the 9 and 6% CP diets, indicating that manure odor from pigs fed the 9 and 6% CP diets were more offensive compared with that of the 15% CP diet. Differences in log odds ratios between the 15% CP, 12% CP, protein-free, and casein-based diets were not significant.



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  		Figure 2. Odor offensiveness of manure. Pigs (50 kg) were fed corn–soybean meal-based diets containing 15, 12, 9, and 6% CP, a casein-based diet containing 15% CP (15% Cas), and a protein-free diet (PF). Log odds index are relative to the 15% CP diet (Index = 100) and indicates the likelihood of increased or decreased odor offensiveness. Indices without a common letter differ (P < 0.05). Standard error of the log odds ratio difference between the 15% CP diet and the 12 % CP, 9% CP, 6% CP, PF, and casein-based diets are 0.305, 0.349, 0.637, 0.320, and 0.357, respectively.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
The primary aim of this study was to determine manure odor and NH3 emission, fecal VFA concentration, and urinary phenolic compound concentrations from pigs fed a wide range of dietary CP concentrations. We hypothesized that decreasing dietary CP concentration reduces manure NH3 emission and fecal VOC concentrations, and consequently decreases manure odor offensiveness. It is known that NH3 is a major pollutant (Debruyckere and Vansteelant, 1992) and decreases air quality (Zhang et al., 1998). Manure arises from postgut oxidative deamination of excess AA through removal of {alpha}-amino-N. Ammonia is converted to urea in the liver, which in turn is excreted in the urine (Jackson et al., 1986). When urine comes in contact with fecal matter, urinary urea is converted back to via the action of bacterial urease present in feces (Jackson, et al., 1986; Hartung and Phillips, 1994). Ammonia is also produced by bacterial and enzymatic degradation of other nitrogenous components found in urine (Jackson, et al., 1986; Hartung and Phillips, 1994). Both ionized () and unionized (NH3) forms of ammonia are present in manure slurry, but the unionized form is also volatile, hence found in the air (Spoelstra, 1980). In this study, NH3 emission decreased nearly 80% by reducing dietary CP from 15 to 9%. This is in close agreement with Turner et al. (1996), who reported a 79% reduction in ammonia emission measured in vitro when dietary CP was reduced from 16 to 12% during the growing phase, and 58% reduction when dietary CP was reduced from 14 to 10% during the finishing phase. Practical feeding studies report lower reduction in NH3 emission; Kay and Lee (1997) reported 47 to 59% reductions in NH3 emission in pigs fed diets reduced in dietary CP from 4 to 6 percentage units during the growing (21 vs. 15% CP) and finishing phase (19 vs. 13.5% CP), respectively; Richert and Sutton (2000) reported a 33% decrease in NH3 emission when dietary CP was reduced from 14 to 10%. The NH3 emission data reported in this study parallels the results of the N balance study by Otto et al. (2002), where decreasing CP concentration from 15 to 12% caused a 20% reduction in total N excretion, and a further decrease to 9% CP caused approximately 40% reduction in total N excretion. However, unlike N excretion data, reduction in CP concentration below 9% did not yield further reduction in NH3 emission despite the previous observation that feeding the 9% CP diet resulted in an additional 26% decrease in total N excretion (Otto et al., 2002). The reduction in N excretion when feeding a 6 vs. 9% CP diet was mainly of fecal origin (Otto et al., 2002). Consequently, the impact on concentration in the manure slurry and NH3 emission would be minimal. Our study provides information relative to the limit at which reduction in dietary CP concentration contributes to NH3 emission. Basal endogenous N losses contributed up to 60 and 34% of the total N excretion in pigs fed the 6 and 9% CP diets, respectively (Otto et al., 2002). Our results indicate that basal endogenous N losses were the main contributor to NH3 emission in both the 9 and 6% CP diets. Additionally, it is possible that crystalline AA, which contributed 11 and 30% of the total dietary AA in the 9 and 6% diets, respectively, may have contributed to a decrease in urinary pH, as demonstrated by Sutton et al. (1996), hence promoting ionization and reducing NH3 formation and volatilization. Our results indicate that the decrease in N excretion (Otto et al., 2000) and NH3 emission is linear only over a certain range of dietary CP intake where N utilization is not maximized. In this study, NH3 emission decreased approximately 16% for each percentage unit of CP reduction from 15 to 9%. Similar results have been reported by Canh et al. (1998).

Total VFA concentration in feces observed in the present study were similar to total VFA concentration reported in cecal content (Hankins et al., 2000) and in fresh feces (Imoto and Namioka, 1978) of growing pigs. Total VFA concentration in feces of the present study increased when pigs were fed the 12, 9, and 6% CP diets compared to that in pigs fed the 15% CP diet. These results agree with other reports (Imoto and Namioka, 1978; Cromwell et al., 1999; Hankins et al., 2000). Hankins et al. (2000) reported higher total VFA concentration, specifically acetate, propionate, and butyrate in fresh manure when a 10% CP diet containing crystalline lysine, threonine, tryptophan, and 5% cellulose was fed compared with a 13% CP diet. In our study, cellulose was only added at 0.6, 1.2, and 1.75 g/kg of diet in the 12, 9, and 6% CP diets, respectively, to ensure proper gastric clearance rate and match the fiber content of the 15% CP diet. Therefore, it is unlikely that cellulose contributed to the increase in total VFA concentration in those diets compared with the 15% diet.

The reason for an increase in VFA with a reduction in dietary CP concentration found in this study and others (Imoto and Namioka, 1978; Cromwell et al., 1999; Hankins et al., 2000) is unclear. Volatile fatty acids originate in part from AA deamination by anaerobic bacteria in the gastrointestinal tract and feces (Mackie et al., 1998). Hence, reducing dietary CP concentration and providing crystalline AA, which are completely absorbed before reaching the hindgut (Chung and Baker, 1992), should reduce the availability of substrates (i.e., undigested AA) for bacterial fermentation and VFA synthesis.

Production of certain VFA is also the result of anaerobic microbial fermentation of soluble carbohydrates (Argenzio and Southworth, 1974; Mackie et al., 1998). Because a reduction of dietary CP concentration in a corn–soybean meal-based diet is usually achieved by increasing the proportion of corn, more soluble carbohydrates may be available to the intestinal microflora. In this study, we diluted the 12, 9, and 6% CP diets by adding cornstarch to keep a similar AA profile across diets. We assumed that cornstarch would be completely digested and absorbed before reaching the hindgut, where most anaerobic fermentation occurs since approximately 94% of total starch in a corn-based diet is digested by pigs at the point of the ileum (Keys and DeBarthe, 1974). Ileal digestibility of starch in various hybrid corn grains vary between 80 to 95% when fed to growing pigs (Lin et al., 1987; Andersen et al., 2000). Hence, pure cornstarch should be even more digestible than starch from corn grain. Indeed, cornstarch and glucose are nearly 100% digested in the small intestine of pigs and therefore are not appreciably available for hindgut fermentation (Lin et al., 1987). However, fermentation in itself contributes to nutrient disappearance, and whereas fermentation mostly occurs in the hindgut, highly digestible feeds, such as soluble carbohydrates, have been shown to promote upper-tract fermentation (Radecki and Yokoyama, 1991). For instance, fecal acetate, a direct product of soluble carbohydrate fermentation, was found in its highest concentration in the present study in pigs fed the protein-free diets, which contained 82% corn starch. Additionally, the protein-free diet used in this study may favor a higher intestinal pH, thus in turn favoring acetate production.

Another possible mechanism for the increased VFA production is a decrease in microbial cell population. It is well known that maximizing ruminal microbial yield through provision of N in dairy cows decreases the production of fermentation acids and that N shortage with ample provision of organic matter favors production of fermentation acids (van Kessel and Russell, 1996; Allen, 1997). Thus, the presence of increased soluble carbohydrates in reduced CP diets fed to pigs in combination with lower N availability may contribute to the increase in VFA production. Conversely, in pigs fed such diets as a protein-free or casein-based, where little to no dietary amino acids reached the hindgut, concentration of VFA in feces was minimal to undetectable.

Previous research (Imoto and Namioka, 1978) found the proportion of VFA in feces to be about 50:40:10 for acetate, propionate, and butyrate, respectively, for pigs fed either a low- or high-carbohydrate diet. In this study, pigs fed the 15% CP diet had proportions of VFA in feces similar to those reported by Imoto and Namioka (1978) for pigs fed a corn–soybean meal-based diet. The proportion of individual VFA to total VFA concentration has been deemed extremely significant in relation to odor offensiveness (O’Neill and Phillips, 1992). Of the VFA, the long-chain VFA contribute to manure odor quality (Spoelstra, 1980). Thus, acetic and propionic acid concentrations have been considered unimportant when investigating odor quality (Spoelstra, 1980). Therefore any decrease in the proportion of long-chain and branched-chained VFA relative to short-chain VFA has the potential to reduce odor emanating from pig manure.

In the present study, the proportion of isobutyrate, butyrate, isovalerate, and valerate increased, and the proportion of acetate and propionate were reduced in feces from pigs fed the 12, 9, and 6% CP diets compared with those in pigs fed the 15% CP diet. Analysis of the odor panel responses demonstrated that manure from pigs fed the 6 and 9% CP diets were more offensive when compared with manure from pigs fed the 15% CP diet. Therefore, the increased concentrations of isobutyrate, butyrate, isovalerate, and valerate in the reduced CP diets may have contributed to the increased odor offensiveness. Alternatively, because NH3 in itself is not classified as a malodorous compound, NH3 emission from manure slurries originating from the 15 and 12% CP diets may have "scaled down" the odor offensiveness or "masked" odors relative to the 9 and 6% CP diets. This suggestion remains to be tested with more vigorous and objective odor panel methods in the presence and absence of NH3. In practical situations, the increased fecal VFA concentration may have a lesser impact on odor because fecal dry matter excretion decreased from 266 to 140 g/d as dietary CP decreased from 15 to 6%, respectively (data not shown). However, because there was a threefold increase in fecal VFA concentration in this study relative to the 15% CP diet, total daily VFA production would be higher in the 12, 9, and 6% CP diet compared with the 15% CP diet. The other volatile components primarily excreted in urine, p-cresol, and 4-ethyl phenol were detected in very small concentrations, with no differences in concentrations found across diets. Both p-cresol and 4-ethyl phenol originate from the intestinal degradation of tyrosine (Macfarlane and Macfarlane, 1995). Urinary concentrations of these phenolic compounds measured in the present study were lower than values reported in the literature (Yokoyama et al., 1982; Yasuhara, et al., 1984), but were approximately 10-fold higher than those measured in fresh manure (Hobbs et al., 1996). Concentrations of phenolic compounds in fresh urine of growing pigs were found to increase as urine aged, possibly because trace amounts of fecal matter contamination occurred at the time of collection, resulting in the release of phenolic metabolites by bacterial enzymatic action on glucuronide conjugates (Yasuhara et al., 1984). So far, only limited research has been conducted on the impact of dietary CP reduction on indolic and phenolic metabolites excretion. Little research comparing urinary phenolic compound concentrations in growing pigs fed reduced dietary CP diets has been reported. Hobbs et al. (1996) reported that concentrations of phenolic metabolites, such as 4-methyl phenol and 4-ethyl phenol, and indole metabolites in manure slurry were reduced as dietary CP was reduced from approximately 20 to 13%; however, no odor evaluation was conducted. The role of phenolics contributing to odor offensiveness in our study is inconclusive because only p-cresol and 4-ethyl phenol were identified in urine. Because no differences were found between dietary treatments, they may have contributed equally to the odor quality.

In conclusion, reducing dietary CP and providing crystalline AA to meet digestible AA requirements significantly decreased NH3 emission from swine manure but did not improve odor quality of manure or decrease fecal VFA concentration. Because a reduction in dietary CP concentration is achieved by increasing the proportion of corn to soybean meal, a larger provision of carbohydrate may favor fermentation acid production, in particular long-chain and branched-chain VFA, and thus odor production.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
This study demonstrated that reducing dietary crude protein concentration from 15 to 9% minimizes ammonia emission from manure slurry in 50-kg growing pigs. However, our results also suggest that a reduction of dietary crude protein concentration in corn–soybean meal-based diets to reduce fecal volatile fatty acids and to improve manure odor quality should be reevaluated. Further research is imperative to determine the potential use of alternative feed ingredients to decrease dietary crude protein concentration and their effect on manure odor quality.


   Footnotes
 
1 This project was funded by the Natl. Pork Prod. Council and the Michigan Agric. Exp. Stn. Back

2 The authors wish to thank the Michigan State Swine Research Farm staff for their assistance in animal handling and care. Back

3 Current address: United Feeds, Inc., P.O. Box 108, 4310 St. RD 38W, Sheridan, IN 46069. Back

Received for publication September 26, 2001. Accepted for publication February 28, 2003.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


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