J. Anim Sci.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shriver, J. A.
Right arrow Articles by Pettey, L. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shriver, J. A.
Right arrow Articles by Pettey, L. A.
J. Anim. Sci. 2003. 81:492-502
© 2003 American Society of Animal Science

Effects of adding fiber sources to reduced-crude protein, amino acid-supplemented diets on nitrogen excretion, growth performance, and carcass traits of finishing pigs1,2

J. A. Shriver*, S. D. Carter*,3, A. L. Sutton{dagger}, B. T. Richert{dagger}, B. W. Senne* and L. A. Pettey*

* Department of Animal Science, Oklahoma State University, Stillwater 74078 and and {dagger} Department of Animal Sciences, Purdue University, West Lafayette, IN 47907

3 Correspondence:
212 Animal Science (phone: 405-744-8869; E-mail:
carters{at}okstate.edu).


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Two experiments were conducted to evaluate the effects of adding fiber sources to reduced-crude protein (CP), amino acid-supplemented diets on N excretion, growth performance, and carcass traits of growing-finishing pigs. In Exp. 1, six sets of four littermate barrows (initial weight = 36.3 kg) were allotted randomly to four dietary treatments to determine N balance and slurry composition. Dietary treatments were: 1) fortified corn–soybean meal, control, 2) as fortified corn–soybean meal with CP lowered by 4 percentage units and supplemented with lysine, threonine, methionine, tryptophan, isoleucine, and valine (LPAA), 3) same as Diet 2 plus 10% soybean hulls, and 4) same as Diet 2 with 10% dried beet pulp. Nitrogen intake, absorption, and retention (g/d) were reduced (P < 0.04) in pigs fed the low- protein diets, but they were not affected (P > 0.10) by addition of fiber sources to the LPAA diet. However, N absorption, as a percentage of intake, was not affected (P > 0.10) by dietary treatment. Nitrogen retention, expressed as a percentage of N intake, was increased (P < 0.02) in pigs fed the low-protein diets, but it was not affected by fiber addition to the LPAA diet. Urinary and total N excretion was reduced (P < 0.01) by 50 and 40%, respectively, in pigs fed the low- protein diets, but it was not affected (P > 0.10) by fiber addition. However, fiber addition to the LPAA diet tended to result in a greater proportion of N excreted in the feces than in the urine. Slurry pH, ammonium N content, and urinary urea N excretion were reduced (P < 0.10) in pigs fed LPAA, and a further reduction (P < 0.06) in slurry ammonium N content and urinary urea N was observed with fiber addition. Also, fiber addition to the LPAA diet increased (P < 0.02) slurry VFA concentrations. In Exp. 2, 72 pigs were blocked by body weight and sex and allotted randomly to three dietary treatments that were similar to those in Exp. 1, with a corn–soybean meal control diet, LPAA diet, and a LPAA diet with 10% soybean hulls. Pigs were fed the diets from 28.6 to 115 kg, and all pigs were killed for collection of carcass data. Growth performance and most carcass traits were not affected (P > 0.10) by dietary treatment. These data suggest that reducing CP with amino acid supplementation markedly decreased N excretion without influencing growth performance. Fiber addition to a LPAA diet had little effect on overall N balance or growth performance, but tended to further reduce slurry ammonium N concentration and increase volatile fatty acid concentrations.

Key Words: Amino Acids • Crude Protein • Excretion • Fiber • Pigs • Pig Slurry


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Dietary manipulation has been shown to be an effective method to reduce N excretion by growing-finishing pigs and ammonia emissions from slurry. Some of these manipulations include the formulation of diets on an ideal protein basis, reduction in CP content of diets, and addition of fermentable carbohydrate sources to diets (Kornegay and Verstegen, 2001). Carter et al. (1996) and Sutton et al. (1996) reported that a reduction of 3 to 4 percentage units in CP with AA supplementation decreased total N excretion by approximately 28 to 36%. Furthermore, ammonia emissions from the slurry of pigs fed reduced-CP, AA-supplemented diets have been markedly decreased (Turner et al., 1996; Kay and Lee, 1997).

Recent results suggest that the addition of soybean hulls, dried beet pulp, cellulose, or sucrose oligosaccharide to swine diets altered the excretory patterns of N, increased manure VFA concentrations, and reduced ammonia emissions (Cahn et al., 1997; 1998a,b; Sutton et al., 1997). Sutton et al. (1997) reported that addition of cellulose or a sucrose oligosaccharide to a reduced- protein, AA-supplemented diet further reduced N in the slurry, suggesting an additive effect of fermentable carbohydrates and reduced-protein, AA-supplemented diets on N excretion. However, many of the diets used in these previous experiments were composed of ingredients that are not typical of U.S. corn–soybean meal diets. In addition, the addition of fiber sources to swine diets may decrease growth performance, and the feeding of reduced-protein, AA-supplemented diets has been shown, in some cases, to be detrimental to growth performance and carcass traits (Kerr et al., 1995; Tuitoek et al., 1997).

Therefore, the objectives of the present experiments were to determine the effects of addition of fiber sources to reduced protein, AA-supplemented corn–soybean meal diets on N balance, slurry composition, growth performance, and carcass traits of growing-finishing pigs.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Experiment 1
General Procedures.
Six sets of four littermate barrows (PIC, Hennessey, OK) with an average initial BW of 36.3 kg were used to evaluate the effects of dietary fiber addition to reduced-protein, AA-supplemented diets on N absorption and excretion. Pigs were housed individually in an environmentally controlled room in metabolism chambers. The chambers (0.76 x 0.91 m) allowed for the separate but total collection of urine, feces, and refused feed. The room temperature was maintained at 24°C. The 15-d experimental period consisted of a 10-d adaptation period to allow pigs to become accustomed to the chambers and to their dietary treatments followed by a 5-d collection period.

Pigs within litter were allotted randomly to one of four dietary treatments in a randomized complete block design. Dietary treatments were: 1) fortified corn–soybean meal-based diet serving as the control, 2) same as Diet 1 with CP lowered by 4 percentage units with the addition of L-lysine • HCl, DL-methionine, L-threonine, L-tryptophan, L-isoleucine, and L-valine (LPAA), 3) same as Diet 2 plus 10% soybean hulls (SBH), and 4) same as Diet 2 plus 10% dried beet pulp (DBP) (Table 1Go). Soybean hulls (12.6% CP, 0.63% Lys) or dried beet pulp (8.5% CP, 0.50% Lys) were obtained from a local feedmill and analyzed for CP and AA prior to diet formulation. The stepwise procedure to formulate the diets was as follows: First, the control diet consisting of corn and soybean meal as sources of N was formulated to contain 18% CP. Second, in order to specifically evaluate the effects of fiber addition to the LPAA diet on N balance, the level of soybean meal in the low-protein diets was held constant. Because the soybean hulls contained greater concentrations of CP and AA than the dried beet pulp, the level of soybean meal in the SBH diet was used as the basis for the constant level of soybean meal (14.4%) in the low-protein diets. Casein was added as needed to the LPAA and DBP diets in order to maintain the 4-percentage unit decrease in CP concentration and a constant soybean meal concentration across all the low-protein diets. L-Lysine • HCl was added as needed to the low-protein diets to reduce CP concentration by 4 percentage units. All diets were formulated on a total lysine basis (0.96% Lys). Crystalline amino acids were added to the low-protein diets to achieve an ideal ratio to digestible lysine (Baker, 1997; NRC, 1998). Soybean hulls and beet pulp replaced cornstarch in the LPAA diet on an equivalent weight basis. Digestibility coefficients for amino acids in soybean hulls and dried beet pulp were obtained from Heartland Lysine, Inc. (Chicago, IL). Assuming the digestibility of N in casein and crystalline AA exceeds 90% (Kies et al., 1986; Chung and Baker, 1992), the replacement of cornstarch in the LPAA diet with either soybean hulls or dried beet pulp would allow for the specific evaluation of replacing a starch source with a fiber source on N balance. Thus, this arrangement of dietary treatments would allow not only for the determination of reducing CP by 4 percentage units on N balance, but also for the evaluation of the specific effects of fiber addition to the LPAA diet.


View this table:
[in this window]
[in a new window]
 
Table 1. Composition of diets (as-fed basis)—Exp. 1
 
Balance Procedures.
Ten days prior to the 5-d collection period, pigs were placed in the metabolism chambers. A 5-d total collection of feces and urine followed the adaptation period. On d 0 and 5 of the collection period, chromic oxide was included at 0.15% of the diet to alter the fecal color so that an exact beginning and endpoint of the collection period could be established for each pig. Fecal output, urine volume, and refused feed were collected and recorded daily. Pigs had ad libitum access to feed and water, and pigs and feeders were weighed on d 0 and 5 of the collection period to monitor ADG, ADFI, and gain:feed (G:F).

One aliquot (approximately 150 mL) of the daily urine output from each pig was saved and stored frozen (-20°C) until the end of the collection period. The daily urine samples from each pig were allowed to thaw at 4°C, and then they were pooled by combining 1% of the daily urine output from each pig. The composite urine samples were stored frozen (-20°C) until analysis for N was performed.

The total quantity of feces collected over the 5-d period were pooled and freeze-dried to a constant weight. The dried fecal matter was ground using a Wiley Mill (model No. 3, Arthur H. Thomas Co., Philadelphia, PA) equipped with a 1-mm screen. The ground fecal matter was stored at 4°C until it was analyzed for N.

Following the 5-d collection period, pigs remained on their respective diets for an additional 3 d for the collection of slurry. The slurry from each pig was mixed well and subsampled for analyses.

Chemical Analyses.
The diets were analyzed for CP by Kjeldahl methodology (N x 6.25; AOAC, 1998). Amino acid analysis of the diets was performed by the Experiment Station Chemical Laboratories at the University of Missouri according to AOAC (1984) methods using a Beckman 6300 AA analyzer (Beckman Instruments, Inc., Fullerton, CA). Urine and fecal N content was determined as described for the diets. Dry matter content of the diets and feces was determined by drying a 3-g sample of the diets and feces from each pig at 100°C for 24 h. Slurry samples were analyzed for total and ammonium N concentration by micro-Kjeldahl procedures as described by Nelson and Sommers (1972) and Bremmer and Keeney (1965), respectively. Individual and total VFA concentrations in the slurry were determined with the use of gas chromatography procedures of Playne (1985).

Experiment 2
Seventy-two crossbred (Yorkshire x Hampshire) pigs with an average initial BW of 28.6 kg were used to evaluate the effects of the addition of dietary fiber to reduced-CP, AA-supplemented diets. There were six pen replicates per treatment and four pigs per pen. Pigs were housed in 2.1 x 2.4 m pens in a well-ventilated enclosed finishing barn with concrete slatted floors.

Pigs were blocked by BW and sex and allotted randomly to three dietary treatments in a randomized complete block design. Dietary treatments were: 1) control diet, 2) LPAA, and 3) SBH. Soybean hulls used in Diet 3 contained 11.4% CP, and they were added at the expense of corn and soybean meal (Table 2Go). Crystalline AA were added to Diets 2 and 3 to achieve an ideal ratio to digestible lysine (Baker, 1997; NRC, 1998). All other nutrients met or exceeded NRC (1998) standards.


View this table:
[in this window]
[in a new window]
 
Table 2. Composition of Phase 1 (35 to 50 kg) diets (as-fed basis)—Exp. 2a
 
Pigs were fed in three dietary phases. Phase 1 diets (35 to 50 kg) were formulated to 0.95% lysine, Phase 2 diets (51 to 82 kg) contained 0.80% lysine, and Phase 3 diets (83 to 113 kg) were formulated to contain 0.65% total lysine. Dietary CP for the control diet was 17, 15, and 13% for the three phases, respectively. Dietary CP for Diets 2 and 3 was reduced by 4 percentage units in each phase. Pigs had ad libitum access to feed and water, and pigs and feeders were weighed at 2-wk intervals to monitor ADG, ADFI, and G:F.

Pigs were bled by jugular venipuncture at the end of each dietary phase. Blood was centrifuged and plasma harvested for plasma urea N analysis. Plasma urea N (PUN) was determined by colorimetric procedures (kit No. 535, Sigma Chemical Co., St. Louis, MO). When pigs reached approximately 113 kg, they were transported to a commercial packing plant and were killed by electrocution followed by exsanguination. Following scalding, scraping, and evisceration, the carcasses were weighed and chilled for 24 h. Standard carcass measures including backfat thickness and longissimus muscle area at the 10th rib were collected. Carcass lean percentage was calculated using hot carcass weight, 10th-rib backfat and longissimus muscle area (NRC, 1998).

Statistical Analyses.
In each experiment, data were analyzed as a randomized complete block design using ANOVA procedures as described by Steel et al. (1997). The model included the effects of block (replication), treatment, and block x treatment (error). In Exp. 1, orthogonal contrasts were used to separate treatment means and consisted of (1) control vs the mean of LPAA, SBH, and DBP diets, (2) LPAA diet vs the mean of LPAA diets with fiber, and (3) LPAA + SBH vs LPAA + DBP. In Exp. 2, orthogonal comparisons were (1) control vs the mean of LPAA and SBH diets, and (2) LPAA vs LPAA + SBH. In both studies, pen served as the experimental unit.


    Results
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Analysis of Diets
Results of the chemical analysis of the diets for CP and AA concentrations are shown in Table 3Go. In general, analyzed values were close to formulated values. In Exp. 1, CP was reduced by 4.0, 4.5, and 3.7% units for LPAA, LPAA+SBH, and LPAA+DBP, respectively. In Exp. 2, the average reduction in CP for the LPAA diets, averaged across phases, was 3.6 percentage units. Lysine and other AA concentrations in diets in Exp. 1 and 2 also were very close to targeted values. Thus, although we not did achieve an exact 4 percentage unit reduction in CP in the LPAA diets, total lysine and other AA concentrations were similar among diets in each experiment.


View this table:
[in this window]
[in a new window]
 
Table 3. Analyzed crude protein and amino acid composition of diets in Exp. 1 and 2 (as-fed basis)
 
Experiment 1
Daily gain, ADFI, and G:F averaged 1.06, 1.93, and 0.54 kg for the 5-d collection period, respectively. Dietary treatment did not affect (P > 0.10) growth performance (data not shown). Furthermore, DM excretion (g/d or %) was not affected (P > 0.10) by dietary treatment (Table 4Go).


View this table:
[in this window]
[in a new window]
 
Table 4. Effects of reducing crude protein with amino acid supplementation and fiber addition on N balance—Exp. 1a
 
Lowering CP and adding crystalline AA reduced N intake (P < 0.01) by 23% compared to pigs fed the control diet (Table 4Go). However, addition of fiber sources to the LPAA diet did not affect (P > 0.10) N intake. Overall, fecal N excretion was not affected (P > 0.10) by diet. Urinary N excretion was reduced (P < 0.01) by lowering dietary CP and adding AA.

Addition of SBH or DBP to the LPAA diet resulted in a greater proportion of total N excretion in the feces compared with the urine. Pigs fed the control diet excreted 74% of total N as urinary N, whereas pigs fed the LPAA, SBH, and DBP excreted 61, 58, and 57% as urinary N. Urinary urea N excretion for the respective dietary treatments was 15.9, 7.7, 6.6, and 5.6 g/d. Lowering CP with AA supplementation reduced (P < 0.01) urinary urea N excretion. A further reduction in urinary urea N excretion was observed (P < 0.05) when the fiber sources were added to the LPAA diet.

Due to the reduction in total N intake, pigs fed the LPAA diet absorbed less (P < 0.01) N (g/d) compared with pigs fed the control diet (Table 4Go). Addition of SBH or DBP to the LPAA diet did not affect (P > 0.10) N absorption. Also, N retention, on a grams/day basis, was reduced (P < 0.04) in pigs fed the LPAA diet compared with pigs fed the control diet. Absolute N retention (g/d) was not affected (P > 0.10) by fiber source. On the other hand, N retention, as a percentage of intake, was increased (P < 0.02) by lowering dietary CP and adding AA. Again, the addition of fiber sources to the LPAA diet did not affect (P > 0.10) N retention as a percentage of intake.

Slurry composition for pigs fed the four dietary treatments is shown in Table 5Go. Slurry pH produced from pigs fed the low-protein diets tended to be reduced (P < 0.09) compared with pigs fed the control diet. However, dietary fiber source did not affect (P > 0.10) pH. Total N content of the slurry on a DM basis was reduced (P < 0.01) with pigs fed the low-protein diets compared with those fed the control diet. Likewise, ammonium N content (DM basis) of the slurry was reduced (P < 0.01) by lowering CP and adding AA. Addition of fiber sources to the LPAA diet tended to further reduce (P < 0.06) ammonium N concentration (DM basis) of the slurry. Furthermore, slurry ammonium N content tended to be lower (P < 0.09) for pigs fed DBP than for pigs fed SBH. Although the average VFA concentrations for pigs fed the low-protein diets was similar (P > 0.10) to pigs fed the control diet, a simple, nonorthogonal comparison between pigs fed LPAA and the control diet (112.4 vs 92.7 mM/L) indicated a decrease (P < 0.04) in total VFA concentration. However, the addition of fiber sources to the LPAA diet increased (P < 0.02) VFA concentrations in the slurry.


View this table:
[in this window]
[in a new window]
 
Table 5. Effects of reducing crude protein with amino acid supplementation and fiber addition on slurry composition—Exp. 1a
 
Experiment 2
The effect of dietary treatment on pig performance is shown in Table 6Go. Although, pigs fed the LPAA diets had numerically lower ADG and G:F compared with pigs fed the control diet, these differences were not statistically significant (P > 0.10). The addition of 10% soybean hulls to the reduced-CP, AA-supplemented diet had no effect (P > 0.10) on pig performance.


View this table:
[in this window]
[in a new window]
 
Table 6. Effects of reducing CP with AA supplementation and fiber addition on growth performance and carcass traits—Exp. 2a
 
With the exception of average backfat, no effects (P > 0.10) of dietary treatment on carcass characteristics were observed. There were no differences (P > 0.10) in average backfat when pigs fed the control diet were compared to those fed the low-protein diets, but pigs fed LPAA had increased (P < 0.03) average backfat compared with pigs fed the control diet (29.8 vs 3.29 cm). However, the addition of soybean hulls to the reduced protein, AA-supplemented diet reduced (P < 0.02) average backfat thickness. Longissimus muscle area and fat-free lean gain were not affected (P > 0.10) by treatment.

As expected, plasma urea N concentrations were reduced (P < 0.01) markedly by lowering CP and adding AA. Addition of soybean hulls to the reduced CP, AA-supplemented diet had minor effects (P > 0.10) on plasma urea N concentration.


    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Several reports during the last decade suggest that the potential exists to decrease N excretion and ammonia concentrations of swine waste via dietary manipulation. Suggested dietary manipulations to reduce N excretion by swine include the use of phase feeding to more closely match the protein (AA) content of the diet to the requirement of the pig, the use of highly digestible protein sources, and lowering CP concentration of the diet with AA supplementation. Of these, dietary manipulation to reduce CP concentration of the diet with AA supplementation offers the greatest potential to reduce N excretion.

Reducing CP content of the diet with AA supplementation reduces excess total N intake and, thus, has been reported to dramatically decrease N excretion. A 2-percentage unit decrease in dietary CP with lysine supplementation has been reported to decrease N excretion by 17 to 22% (Cromwell, 1993). A more profound decrease in N excretion is observed when CP content of the diet is reduced by 3 to 4 percentage units with appropriate AA supplementation. Carter et al. (1996) reported that N excretion could be reduced in growing and finishing pigs by approximately 35% by reducing CP concentration with supplementation of lysine, methionine, threonine, and tryptophan. Sutton et al. (1996) reported a 28% reduction in N excretion from pigs fed reduced-CP, AA-supplemented diets.

In Exp. 1, reducing CP by 4 percentage units with the addition of crystalline AA reduced total N excretion by 40%. Furthermore, urinary N excretion was reduced by 50%. This marked reduction in urinary and total N excretion is similar to other reports (Aarnink et al., 1993; Carter et al., 1996; Hobbs et al., 1996; Sutton et al., 1999). Additionally, Kerr and Easter (1995) suggested that for every 1% reduction in CP content of the diet with AA supplementation, total N excretion could be reduced by 8%. Our results suggest a 10% reduction in total N excretion is possible for every 1% reduction in CP content of the diet with AA supplementation; however, this would be a slight overestimation due to the inclusion of cornstarch and casein in the LPAA diet.

The addition of fermentable carbohydrates such as soybean hulls and dried beet pulp to diets fed to growing-finishing swine has been shown to affect the partitioning of N excretion between the urine and the feces (Mroz et al., 1993). Furthermore, fermentable carbohydrates have been reported to decrease urinary urea N excretion (Schulze et al., 1995; Canh et al., 1997). Urinary urea N is a substrate for the enzyme urease found in the feces, which is associated with ammonia emissions from the slurry. Therefore, by reducing urinary urea N, less substrate is present in the slurry for ammonia production (Cahn et al., 1998a,b). However, the addition of fiber to swine diets also has been shown to increase N excretion, particularly fecal N excretion (Cummings et al., 1976; Fahey et al., 1980; Malmlof and Hakansson, 1984).

In Exp. 1, fecal N excretion was increased slightly with a concomitant slight decrease in urinary N excretion in pigs fed the reduced-CP, AA-supplemented diets with 10% soybean hulls or dried beet pulp. Unlike many previous reports (Cummings et al., 1976; Fahey et. al., 1980; Malmlof and Hakansson, 1984), total N excretion was not affected by dietary fiber addition. However, the level and source of dietary fiber was lower in our experiment compared with these previous reports, which may account for the lack of an effect of soybean hulls or beet pulp on total N excretion. In addition, Canh et al. (1997) reported that total N excretion was not affected in pigs fed dried beet pulp.

The marked decrease in urinary N excretion by pigs fed the LPAA diet resulted in a greater proportion of N excretion in the feces, such that the ratio of N in the feces to the N in the urine increased. Pigs fed the control diet excreted approximately 26% of N as fecal N. In contrast, those fed LPAA excreted approximately 38% of N as fecal N. In addition, the urinary urea N excretion was reduced by 51% by pigs fed LPAA vs the control. This marked reduction in urinary urea N excretion has been associated with lower ammonia emissions from the slurry of pigs fed LPAA (Turner et al., 1996). Furthermore, the addition of SBH or DBP to the LPAA diet tended to increase the proportion of N excreted in the feces, and further reduce urinary urea N excretion. However, these effects were more pronounced for pigs fed the LPAA diet with DBP as compared with those fed SBH. Canh et al. (1997) reported that the addition of 30% sugar beet pulp increased the proportion of total N excretion in the feces from 55 to 66%, without affecting total N excretion. Similar results have been reported by Cummings et al. (1976) and Morgan and Whittemore (1988).

Because total N intake was reduced in pigs fed the LPAA diet, absolute N absorption (g/d) was reduced. However, N absorption as a percentage of intake was similar between pigs fed the control diet and those fed the LPAA diets. The total amount of N retained per day was decreased slightly in pigs fed the LPAA diets. Similar effects on N retention have been observed in pigs fed reduced protein, AA-supplemented diets (Kephardt and Sherritt, 1990; Kerr and Easter, 1995; Carter et al., 1996). However, Kerr and Easter (1995) reported that addition of dispensible AA to a LPAA (12% CP) diet containing lysine, tryptophan, and threonine improved N retention. Thus, dispensible AA could have been moderately limiting in pigs fed the LPAA diet in Exp. 1, resulting in a slight reduction in N retention. However, growth performance was not affected by diet. Nitrogen retention, as a percentage of intake, was improved by lowering CP with AA supplementation, which is similar to results of Kerr and Easter (1995).

The addition of SBH or DBP to the LPAA diet had little effect on N absorption. Nitrogen retention was increased numerically with the addition of SBH or DBP to the LPAA diet. This slight increase in N retention could be due to the N retained for growth of microorganisms in the hindgut (Malmlof and Hakansson, 1984). However, these authors also reported that N retained in the hindgut leads to an increase in fecal N output. Our results would suggest that the addition of SBH or DBP to the LPAA diet did not affect N balance or the efficiency of N utilization.

The use of reduced-protein, AA-supplemented diets also has been shown to markedly reduce ammonium N concentration of the slurry and ammonia emissions (Aarnick et al., 1993; Sutton et al., 1996; Turner et al., 1996). In Exp. 1, slurry N content was reduced approximately 20 to 36% by lowering CP with AA addition. Sutton et al. (1996) reported a 28% reduction in slurry N content when CP was lowered by 3 percentage units with AA supplementation. In addition, pH of the slurry from pigs fed LPAA was reduced, which is in agreement with other reports (Sutton et al., 1996). The addition of fiber sources to the LPAA diet resulted in slight reductions in pH, total N (DM basis) and ammonium N concentration of the slurry. Canh et al. (1997; 1998a,b) reported more dramatic effects of SBH or DBP on slurry N concentrations than those reported here; however, these authors used much greater inclusion levels of SBH or DBP. Our results are very similar to a recent report of Hankins et al. (2001), which indicated that the addition of SBH or DBP to an LPAA diet resulted in slight decreases in pH and total and ammonium N concentrations. Similar to our results, DBP resulted in the greatest decrease in slurry N concentrations.

A more profound effect of diet was found for slurry VFA concentrations. Lowering CP with AA supplementation reduced VFA concentration of the slurry. However, the addition of fiber sources to LPAA diet increased VFA concentrations. This increase in VFA concentration of the slurry when SBH or DBP were added to the diet agrees with other reports (Canh et al., 1997, 1998ab; Sutton, 1997; Hankins et al., 2001). The increase in VFA concentrations with fiber addition was associated with a decrease in urinary urea N concentration in the urine, particularly for pigs fed DBP. These results would suggest that SBH or DBP addition to the LPAA diet increased the flow of fermentable carbohydrate (energy) to the large intestine, which in turn enhanced microbial growth. The increase in microbial growth induced the secretion of urea from the blood into the large intestine (Low, 1985) for microbial protein synthesis and the concomitant production of VFA (Imoto and Namioka, 1978). The reduction in urinary urea N concentration and slurry N content in pigs fed LPAA with SBH or DBP would likely result in lower ammonia emission from the slurry (Canh et al., 1997; 1998a,b).

Although lowering CP of the diet by 3 to 5 percentage units with selective AA supplementation has resulted in consistent reductions in N excretion, the effects on growth performance and carcass traits have been inconsistent. Cromwell et al. (1983) and Russell et al. (1983; 1986) demonstrated that growth performance was not affected by reducing CP by 4 percentage units with additions of lysine, tryptophan, and threonine. Furthermore, similar results have been reported by Lopez et al. (1994), Hahn et al. (1995), and Kerr et al. (1995) when CP was reduced by 3 to 4 percentage units with selective essential AA additions. On the other hand, reductions in growth performance of pigs fed diets with CP reduced by >=3 percentage units with AA supplementation have been reported (Kephardt and Sherritt, 1990; Kerr and Easter, 1995; Tuitoek et al., 1997). Similarly, Knowles et al. (1998) found that growth performance was not affected in two experiments, but G:F was reduced in a third experiment when CP was reduced by 4 percentage units with lysine, threonine, methionine, tryptophan, isoleucine, and valine addition on an ideal protein basis. Results from Exp. 2 tend to support those studies where no effects on growth performance were observed.

Furthermore, the addition of 10% SBH to the LPAA diet did not affect growth performance. Similarly, Kornegay (1981) reported that the addition of up to 15% SBH to the diet of growing-finishing pigs did not affect growth performance. Shriver et al. (1999) and Knowles et al. (1998) suggested that up to 20% wheat middlings may be added to LPAA diets without affecting growth performance. These results, when taken together, suggest that relatively low additions of fiber-containing feedstuffs to LPAA diets do not affect growth performance of growing-finishing pigs.

In general, carcass traits of pigs consuming LPAA were similar to those consuming the control diet. These results are in agreement with other reports (Lopez et al., 1994; Hahn et al., 1995; Knowles et al., 1998; Shriver et al., 1999). Although 10th-rib fat depth was not affected in pigs fed LPAA there was a numerical decrease in longissimus muscle area. Several studies have reported decreases in measures of carcass muscle (longissimus muscle area, trimmed ham weight; Tuitoek et al., 1997; Freisen et al., 1999; Liu et al., 1999) or increases in backfat thickness (Easter and Baker, 1980; Cromwell et al., 1996; Tuitoek et al., 1997).

The addition of SBH to the LPAA diet had minor effects on carcass traits. However, average backfat decreased and 10th-rib fat depth was numerically reduced with the addition of SBH to the LPAA diet. Knowles et al. (1998) reported that fiber addition via wheat middlings or rice hulls to LPAA diets did not affect carcass traits. Additionally, Shriver et al. (1999) reported that the addition of 20% wheat middlings to LPAA diets did not affect carcass traits. The NE content of SBH is approximately 65% of the NE content of wheat middlings (NRC, 1998). Thus, the lower NE value of SBH would have reduced the NE content of the diet more so than the addition of wheat middlings as reported by Knowles et al. (1998), which may have led to the 10% reduction in 10th-rib fat depth in pigs fed LPAA+SBH.

The reduction in plasma urea N in pigs fed the reduced-CP, AA-supplemented diet is indicative of a reduction in excess AA in these diets, which agrees with the reduction in urinary urea N in Exp. 1. Several other reports also have found reductions in plasma or serum urea N (Russell et al., 1983; Kerr and Easter, 1995; Knowles et al., 1998). The addition of SBH to the LPAA diet, although not significant, numerically decreased PUN, which agrees well with the reduction in urinary urea N excretion reported for pigs fed SBH or DBP in Exp. 1. This slight reduction in PUN could be a result of the microorganisms in the large intestine utilizing urea N as a source of N for microbial protein production in the presence of fermentable carbohydrates (Low, 1985). We speculate that the use of urea N for microbial protein synthesis would decrease the amount of N available for excretion in the urine as demonstrated by the slight, numerical decreases in urinary N excretion associated with fiber addition to the LPAA diet in Exp. 1.

Results from the Exp. 2 suggest that growth performance and carcass traits of pigs fed reduced protein, AA-supplemented diets were comparable to pigs fed a standard corn–soybean meal diet. The amino acids selected for inclusion in the low-protein, AA-supplemented diets were based on reports of Knowles et al. (1998) and Liu et al. (1999). Whether we would have observed similar responses in growth performance and carcass traits with the inclusion of fewer crystalline amino acids is unclear based on previous research. Also, even though ME, and digestible and true amino acid concentrations varied among diets, these data suggest that this variation had no effect on growth performance or carcass traits.

Although determining dietary costs associated with the manipulations employed in these experiments was not an objective, dietary cost is a major issue in decisions concerning the use of low-protein, AA-supplemented diets. Our recent data (Ancev et al., 2002) using the results presented here in a Decision Support System (Stoecker et al., 1998) suggest that, whereas feeding these low-protein diets was economically unfeasible, waste management costs were reduced markedly in the instance a producer has limited land available for manure application.


    Implications
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The public concern related to the potential for water and air pollution from swine facilities demands that alternative management practices be developed. Dietary manipulation offers a potential method to reduce nutrient excretion by swine. Results from our experiments suggest that lowering crude protein by four percentage units with addition of amino acid can reduce total nitrogen excretion by 40%. Also, fiber addition via soybean hulls or dried beet pulp to a low-protein, amino acid-supplemented diet further reduced ammonium nitrogen content of the slurry and urinary urea nitrogen excretion, which could possibly result in lower ammonia emissions. These reductions in nitrogen excretion were possible without affecting growth or carcass traits, although the cost associated with this dietary manipulation remains an issue.


    Footnotes
 
1 Approved for publication by the Director, Oklahoma Agric. Exp. Stn. This project was supported under project H-2379. Back

2 The authors thank NPPC and USDA-CSREES (Federal Initiative Grant) for partial financial support, E. Wilson and J. Poppelwell (PIC, Inc., Hennessey, OK) for supplying the pigs for Exp. 1, and K. Brock for assistance in pig care and data collection. Back

Received for publication October 26, 2001. Accepted for publication October 11, 2002.


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


Aarnink, A. J. A., P. Hoeksma, and E. N. J. van Ouwerkerk. 1993. Factors affecting ammonium concentration in slurry from fattening pigs. Pages 413–420 in Nitrogen Flow in Pig Production and Environmental Consequences. M. W. A. Verstegen, L. A. den Hartog, G. J. M. van Kempen, and J. H. M. Metz, ed. EAAP Publ. No. 69, Pudoc, Wageningen, The Netherlands.

Ancev, T., S. D. Carter, and A. L. Stoecker. 2002. Responsiveness of swine waste management costs to feeding low crude protein diets. Am. J. Agric. Econ. 84: (In press).

AOAC. 1984. Official Methods of Analysis. 14th ed. Assoc. Offic. Anal. Chem., Arlington, VA.

AOAC. 1998. Official Methods of Analysis. 16th ed. Assoc. Offic. Anal. Chem., Arlington, VA.

Baker, D. H. 1997. Ideal amino acid profiles for swine and poultry and their applications in feed formulation. Biokyowa Technical Review-9. NutriQuest, Inc., Chesterfield, MO

Bremmer, J. M., and D. R. Keeney. 1965. Steam distillation methods for determination of ammonium, nitrate, and nitrite. Anal. Chim. Acta 32:485–495.

Canh T. T., A. J. A. Aarnink, M. W. A. Verstegen, and J. W. Schrama. 1998a. Influence of dietary factors on the pH and ammonia emission of slurry from growing-finishing pigs. J. Anim. Sci. 76:1123–1130.[Abstract/Free Full Text]

Canh, T. T., A. L. Sutton, A. J. A. Aarnink, M. W. A. Verstegen, J. W. Schrama, and G. C. M Bakker. 1998b. Dietary carbohydrates alter the fecal composition and pH and the ammonia emission from slurry of growing pigs. J. Anim. Sci. 76:1887–1895.[Abstract/Free Full Text]

Canh, T. T., M. W. A. Verstegen, A. J. A. Aarnink, and J. W. Schrama. 1997. Influence of dietary factors on nitrogen partitioning and composition of urine and feces of fattening pigs. J. Anim. Sci. 75:700–706.[Abstract/Free Full Text]

Carter, S. D., G. L. Cromwell, M. D. Lindemann, L. W. Turner, and T. C. Bridges. 1996. Reducing N and P excretion by dietary manipulation in growing and finishing pigs. J. Anim. Sci. 74 (Suppl. 1):59. (Abstr.)

Chung, T. K., and D. H. Baker. 1992. Apparent and true amino acid digestibility of a crystalline amino acid mixture and of casein: comparison of values obtained with ileal-cannulated pigs and cecectomized cockerels. J. Anim. Sci. 70:3781–3790.[Abstract]

Cromwell, G. C., and R. D. Coffey. 1993. Future strategies to diminish nitrogen and phosphorus in swine manure. Pages 20–32 in Proc. NPPC Environ. Symp. "Meeting the Environmental Challenge,", Minneapolis, MN.

Cromwell, G. L., M. D. Lindemann, G. R. Parker, K. M. Laurent, R. D. Coffey, H. J. Monegue, and J. R. Randolph. 1996. Low protein, amino acid supplemented diets for growing-finishing pigs. J. Anim. Sci. 74 (Suppl. 1):174. (Abstr.)

Cromwell, G. L., T. S. Stahly, V. Gomez-Rojas, and H. J. Monegue. 1983. Amino acid supplementation of a low-protein diet for finishing pigs. J. Anim. Sci. 57 (Suppl. 1):88. (Abstr.)

Cummings, J. H., M. J. Hill, D. J. A. Jenkins, J. R. Pearson, and H. S. Wiggins. 1976. Changes in fecal composition and colonic function due to cereal fiber. Am. J. Clin. Nutr. 29:1468–1473.[Abstract/Free Full Text]

Easter, R. A., and D. H. Baker. 1980. Lysine and protein levels in corn-soybean meal diets for growing-finishing pigs. J. Anim. Sci. 50:467–471.

Fahey, G. C., Jr., G. R. Frank, A. H. Jensen, and S. S. Masters. 1980. Influence of various purified and isolated cell wall fibers on the utilization of certain nutrients by swine and hamsters. J. Food. Sci. 45:1675–1680.

Freisen, K. G., B. J. Kerr, L. L. Southern, and T. D. Bidner. 1999. Effect of variable net energy content of low crude protein, crystalline amino acid-supplemented diets for growing-finishing pigs. J. Anim. Sci. 77 (Suppl. 1):182. (Abstr.)

Hahn, J. D., R. R. Biehl, and D. H. Baker. 1995. Ideal digestible lysine level for early- and late-finishing swine. J. Anim. Sci. 73:773–784.[Abstract]

Hankins, S. L., A. L. Sutton, J. A. Patterson, B. T. Richert, A. J. Heber, D. T. Kelly, K. B. Kephardt, R. Mumma, E. Bogus, and S. D. Carter. 2001. Reduction of odorous compounds in pig manure through dietary fiber manipulation. J. Anim. Sci. 79 (Suppl. 1):86. (Abstr.)

Hobbs, P. J., B. F. Pain, R. M. Kay, and P. A. Lee. 1996. Reduction of odorous compounds in fresh pig slurry by dietary control of crude protein. J. Sci. Food Agric. 71:508–514.

Imoto, S., and S. Namioka. 1978. Volatile fatty acid production in the pig large intestine. J. Anim. Sci. 47:467–478.

Kay, R. M., and P. A. Lee. 1997. Ammonia emission from pig buildings and characteristics of slurry produced by pigs offered low crude protein diets. Pages 245–252 in Proc. Int. Symp. Ammonia and Odour Control from Anim. Prod. Facilities, Vinkeloord, The Netherlands.

Kephardt, K. B., and G. W. Sherritt. 1990. Performance and nutrient balance in growing swine fed low-protein diets supplemented with amino acids and potassium. J. Anim. Sci. 68:1999–2008.[Abstract]

Kerr, B. J., and R. A. Easter. 1995. Effect of feeding reduced protein, amino acid-supplemented diets on nitrogen and energy balance in grower pigs. J. Anim. Sci. 73:3000–3008.[Abstract]

Kerr, B. J., F. K. McKeith, and R. A. Easter. 1995. Effect on performance and carcass characteristics of nursery to finisher pigs fed reduced crude protein amino acid-supplemented diets. J. Anim. Sci. 73:433–440.[Abstract]

Kies, Jr., J. E., P. J. Moughan, and W. C. Smith. 1986. The apparent and true ileal digestibility of nitrogen and amino acids in lactic casein for the growing pig. Anim. Feed Sci. Technol. 16:169–178.

Knowles, T. A., L. L. Southern, T. D. Bidner, B. J. Kerr, and K. G. Friesen. 1998. Effect of dietary fiber or fat in low-crude protein, crystalline amino acid-supplemented diets for finishing pigs. J. Anim. Sci. 76:2818–2832.[Abstract/Free Full Text]

Kornegay, E. T. 1981. Soybean hull digestibility by sows and feeding value for growing-finishing swine. J. Anim. Sci. 53:138–145.[Abstract/Free Full Text]

Kornegay, E. T., and M. W. A. Verstegen. 2001. Swine nutrition and environmental pollution and odor control. Pages 609–603 in Swine Nutrition. 2nd ed. E. T. Kornegay and M. W. A. Verstegen, ed. CRC Press LLC, Boca Raton, FL.

Liu, H., G. L. Allee, J. J. Berkemeyer, K. J. Touchette, J. D. Spencer, and I. B. Kim. 1999. Effect of reducing protein level and adding amino acids on growth performance and carcass characteristics of finishing pigs. J. Anim. Sci. 77 (Suppl. 1):69. (Abstr.)

Lopez, J., R. D. Goodband, G. L. Allee, G. W. Jesse, J. L. Nelssen, M. D. Tokach, D. Spiers, and B. A. Becker. 1994. The effects of diets formulated on an ideal protein basis on growth performance, carcass characteristics, and thermal balance of finishing gilts housed in a hot, diurnal environment. J. Anim. Sci. 72:367–379.[Abstract]

Low, A. G. 1985. Role of dietary fibre in pig diets. Page 87–112 in Recent Advances in Animal Nutrition. W. Haresign and D. J. A. Cole, ed. Butterworths, London.

Malmlof, K., and J. Hakansson. 1984. The effect of dietary fiber level on the diurnal pattern of urinary nitrogen excretion in swine. Swed. J. Agric. Res. 14:53–57.

Morgan, C. A., and C. T. Whittemore. 1988. Dietary fibre and nitrogen excretion and retention by pigs. Anim. Feed Sci. Technol. 19:185–189.

Mroz, Z., A. W. Jongbloed, S. Beers, P. A. Kemme, L. DeJong, A. K. van Berkum, and R. A. van der Lee. 1993. Preliminary studies on excretory patterns of nitrogen and anaerobic deterioration of fecal protein. Pages 247–252 in Nitrogen Flow in Pig Production and Environmental Consequences. M. W. A. Verstegen, L. A. den Hartog, G. J. M. van Kempen, and J. H. M. Metz, ed. EAAP Publ. No. 69, Pudoc, Wageningen, The Netherlands.

Nelson, D. W., and L. E. Sommers. 1972. A simple digestion procedure for estimation of total nitrogen in soils and sediments. J. Environ. Qual. 1:423–425.[Abstract/Free Full Text]

NRC. 1998. Nutrient Requirements of Swine. 10th ed. Natl. Acad. Press, Washington, DC.

Playne, M. J. 1985. Determination of ethanol, volatile fatty acids, lactic acid and succinic acids in fermentation liquids by gas chromatography. J. Sci. Food Agric. 36:638.

Russell, L. E., G. L. Cromwell, and T. S. Stahly. 1983. Tryptophan, threonine, isoleucine, and methionine supplementation of a 12% protein, lysine-supplemented, corn-soybean meal diet for growing pigs. J. Anim. Sci. 56:1115–1123.

Russell L. E., R. A. Easter, V. Gomez-Rojas, G. L. Cromwell, and T. S. Stahly. 1986. A note on the supplementation of low-protein, maize-soyabean meal diets with lysine, tryptophan, threonine, and methionine for growing pigs. Anim. Prod. 42:291–295.

Schulze, H., P. van Leeuwen, M. W. A. Verstegan, and J. W. O. van den Berg. 1995. Dietary level and source of neutral detergent fiber on ileal endogenous nitrogen flow in pigs. J. Anim. Sci. 73:441–448.[Abstract]

Shriver, J. A., S. D. Carter, B. W. Senne, and L. A. Pettey. 1999. Effects of adding wheat midds to low crude protein, amino acid supplemented diets for finishing pigs. J. Anim. Sci. 77 (Suppl. 1):189. (Abstr.)

Steel, R. G. D., J. H. Torrie, and D. A. Dickey. 1997. Principles and Procedures of Statistics: A Biometrical Approach. 3rd ed. McGraw-Hill Book Co., New York.

Stoecker , A. L., C. Fulhage, J. Hoehne, R. Massey, J. Lory, D. Hamilton, and J. Williams. 1998. Spreadsheet for design and economic analysis of swine production and waste management systems. Pages 431–437 in Proc. Int. Conf. Odor, Water Quality, Nutrient Management, and Socioeconomic Issues. Vol. 2. Iowa State Univ. Press, Ames.

Sutton, A. L., K. B. Kephardt, J. A. Patterson, R. Mumma, D. T. Kelly, E. Bogus, D. D. Jones, and A. Heber. 1996. Manipulating swine diets to reduce ammonia and odor emissions. Pages 445–452 in Proc. 1st Int. Conf. Air Pollution from Agric. Operations, Kansas City, MO.

Sutton, A. L., K. B. Kephardt, M. W. A. Verstegen, T. T. Canh, and P. J. Hobbs. 1999. Potential for reduction of odorous compounds in swine manure through diet modification. J. Anim. Sci. 77:430–439.[Abstract/Free Full Text]

Sutton, A. L., K. B. Kephardt, J. A. Patterson, R. Mumma, D. T. Kelly, E. Bogus, D. D. Jones, and A. Heber. 1997. Dietary manipulation to reduce ammonia and odor compounds in excreta and anaerobic manure storages. Pages 245–252 in Proc. Int. Symp. Ammonia and Odour Control from Anim. Prod. Facilities, Vinkeloord, The Netherlands.

Tuitoek, K., L. G. Young, C. F. M. de Lange, and B. J. Kerr. 1997. The effect of reducing excess dietary amino acids on growing-finishing pig performance: An evaluation of the ideal protein concept. J. Anim. Sci. 75:1575–1583.[Abstract/Free Full Text]

Turner, L. W., G. L. Cromwell, T. C. Bridges, S. Carter, and R. S. Gates. 1996. Ammonia (NH3) emission from swine waste as influenced by diet manipulation. Pages 453–458 in Proc. 1st Int. Conf. Air Pollution from Agric. Operations, Kansas City, MO.


This article has been cited by other articles:


Home page
J ANIM SCIHome page
J. K. Htoo, B. A. Araiza, W. C. Sauer, M. Rademacher, Y. Zhang, M. Cervantes, and R. T. Zijlstra
Effect of dietary protein content on ileal amino acid digestibility, growth performance, and formation of microbial metabolites in ileal and cecal digesta of early-weaned pigs
J Anim Sci, December 1, 2007; 85(12): 3303 - 3312.
[Abstract] [Full Text] [PDF]


Home page
Poult. Sci.Home page
S. A. Roberts, H. Xin, B. J. Kerr, J. R. Russell, and K. Bregendahl
Effects of Dietary Fiber and Reduced Crude Protein on Ammonia Emission from Laying-Hen Manure
Poult. Sci., August 1, 2007; 86(8): 1625 - 1632.
[Abstract] [Full Text] [PDF]


Home page
Poult. Sci.Home page
S. A. Roberts, H. Xin, B. J. Kerr, J. R. Russell, and K. Bregendahl
Effects of Dietary Fiber and Reduced Crude Protein on Nitrogen Balance and Egg Production in Laying Hens
Poult. Sci., August 1, 2007; 86(8): 1716 - 1725.
[Abstract] [Full Text] [PDF]


Home page
J ANIM SCIHome page
J. K. Htoo, W. C. Sauer, Y. Zhang, M. Cervantes, S. F. Liao, B. A. Araiza, A. Morales, and N. Torrentera
The effect of feeding low-phytate barley-soybean meal diets differing in protein content to growing pigs on the excretion of phosphorus and nitrogen
J Anim Sci, March 1, 2007; 85(3): 700 - 705.
[Abstract] [Full Text] [PDF]


Home page
J ANIM SCIHome page
B. J. Kerr, C. J. Ziemer, S. L. Trabue, J. D. Crouse, and T. B. Parkin
Manure composition of swine as affected by dietary protein and cellulose concentrations
J Anim Sci, June 1, 2006; 84(6): 1584 - 1592.
[Abstract] [Full Text] [PDF]


Home page
J. Environ. Qual.Home page
O. G. Clark, S. Moehn, I. Edeogu, J. Price, and J. Leonard
Manipulation of Dietary Protein and Nonstarch Polysaccharide to Control Swine Manure Emissions
J. Environ. Qual., August 9, 2005; 34(5): 1461 - 1466.
[Abstract] [Full Text] [PDF]


Home page
J ANIM SCIHome page
T. A. T. G. van Kempen, D. H. Baker, and E. van Heugten
Nitrogen losses in metabolism trials
J Anim Sci, October 1, 2003; 81(10): 2649 - 2650.
[Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Shriver, J. A.
Right arrow Articles by Pettey, L. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Shriver, J. A.
Right arrow Articles by Pettey, L. A.


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS