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 Otto, E. R.
Right arrow Articles by Trottier, N. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Otto, E. R.
Right arrow Articles by Trottier, N. L.
J. Anim. Sci. 2003. 81:1743-1753
© 2003 American Society of Animal Science

Nitrogen balance and ileal amino acid digestibility in growing pigs fed diets reduced in protein concentration1,2

E. R. Otto*,3, M. Yokoyama*, P. K. Ku*, N. K. Ames{dagger} and N. L. Trottier*,4

* Department of Animal Science and and {dagger} College of Veterinary Medicine, Michigan State University, East Lansing, 48824

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 and Discussion
 Implications
 Literature Cited
 
Two studies were conducted to assess the effect of dietary protein reduction on N utilization, N excretion, and AA digestibility in growing pigs. The objective was to determine whether pigs fed diets with a reduced CP concentration could maintain the same N retention as pigs fed an adequate diet. The second objective was to test whether reducing dietary CP concentration decreases AA digestibility. In each study, 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. Crystalline AA were included in the 12, 9, and 6% CP diets. The indispensable:dispensable AA ratio was maintained at 45:55 with the addition of L-glutamic acid to the 9 and 6% CP diets. The casein-based and protein-free diets were used to determine endogenous total tract N and ileal AA losses. In the first study, total N losses and N absorbed decreased linearly (P < 0.001) as dietary CP concentration decreased from 15 to 6%. Both a linear (P < 0.001) and a quadratic (P < 0.05) decrease in N retention were found with decreasing dietary CP concentration. Nitrogen retained as a percentage of intake and absorbed increased (P < 0.001) as dietary CP concentration was reduced from 15 to 6%. In the second study, six barrows were surgically fitted with a T-cannula at the terminal ileum to determine ileal AA digestibility. For all dispensable and most indispensable AA, apparent and standardized ileal digestibility increased linearly (P 0.01, and for arginine, P < 0.05) as dietary CP concentration decreased. These results indicate that dietary CP concentration can be decreased from 15 to 12% with crystalline AA supplementation to meet an ideal AA profile without adversely affecting N retention, and that decreasing dietary CP concentration from 15 to 6% increases both dispensable and indispensable AA ileal digestibility.

Key Words: Amino Acids • Digestibility • Nitrogen Balance • Nitrogen Retention • Pigs


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 Implications
 Literature Cited
 
Growing concerns about environmental pollution arising from intensified swine production have forced researchers to study protein and AA nutrition of the pig beyond their requirements for maximal growth and performance. Reducing N excretion in swine manure can be effectively accomplished by reducing dietary CP intake. There is general agreement in the literature that reducing CP concentration by 2 to 3% with crystalline AA inclusion does not reduce growth performance of growing and finishing pigs (Lopez et al., 1994; Tuitoek et al., 1997; Liu et al., 1999). However, despite the inclusion of AA, when dietary CP concentration is reduced by more than 3 percentage units, N retention decreases (Pierce et al., 1994; Kendall et al., 1999; Zervas and Zijlstra, 2002b), and feed efficiency and ADG are reduced (Tuitoek et al., 1997; Liu et al., 1999). The reason(s) for depression in N retention and growth performance is (are) unclear. Reducing protein concentration of diets containing more than one feed ingredient, with no supplemental crystalline AA, decreases apparent and standardized ileal AA digestibility (Stein, 1998). Protein-bound AA absorption may be reduced in complete diets containing low protein concentrations and might contribute to impaired growth performance. It is unknown whether digestibility of both protein-bound indispensable and dispensable AA are affected when crystalline AA are supplemented to reduced CP diets. Our first objective was to test if N retention of growing pigs fed diets of reduced dietary CP concentrations could be maintained to that of pigs fed a nonreduced CP diet when crystalline AA are provided to meet AA and amino-N requirements on an ileal digestible basis. Our second objective was to test whether reducing dietary CP concentration of a corn-soybean meal-based diet decreases protein-bound indispensable and dispensable AA ileal digestibility in the presence of supplemental crystalline AA.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 Implications
 Literature Cited
 
Animals, Experimental Design, and Diets
Experiment 1.
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. Obligatory endogenous protein losses were determined using the protein-free diet and the casein-based diet. The protein-free diet was chosen to determine nonspecific endogenous N losses, and the casein-based diet was used to determine 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 ensure 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.


View this table:
[in this window]
[in a new window]
  		Table 1. Ingredient composition of experimental diets, as-fed basis
 

View this table:
[in this window]
[in a new window]
  		Table 2. Nutrient composition of experimental diets, as-fed basis
 

View this table:
[in this window]
[in a new window]
  		Table 3. Ingredient composition of casein-based and protein-free diets, as-fed basis
 

View this table:
[in this window]
[in a new window]
  		Table 4. Nutrient composition of casein-based and protein-free diets, as-fed basis
 
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.

Experiment 2.
Six barrows ([Landrace x Yorkshire] x Duroc) with an initial BW of 35.5 ± 0.1 kg were surgically fitted with stainless steel T-cannula at the terminal ileum according to the procedures of Stein et al. (1998). Penicillin G procaine (3 x 105 IU/mL) and flunizin meglumine (50 mg/mL, Shering-Plough Animal Health, Kenilworth, NJ) were administered i.m. at the recommended dosage (6,615 IU/kg and 1 mg/kg, respectively) for 3 d following surgery. Pigs were allowed to recover for 3 wk in individual pens (1.5 x 0.75 m) with smooth-sided panels made of polyvinyl chloride. Each pen was equipped with a suspended water line fitted with a low-pressure nipple and wire flooring. The environmental temperature of the room was maintained at 21°C.

Pigs were randomly allocated to six dietary treatments in a 6 x 6 Latin square design. The average BW at the initiation of the experiment was 53.1 ± 1.8 kg. The six dietary treatments consisted of the same diets as described for Exp 1. Feed was provided in three equal meals per day (800, 1200, and 1600) at five times the energy requirement for maintenance (106 kcal of ME/kg of BW0.75). This daily ration was provided to closely match the pigs’ voluntary feed intake level as predetermined in 50-kg barrows of similar genetics. The casein-based and protein-free diets were mixed with water (500 mL/meal) to increase palatability and reduce feed wastage. Amount of feed provided was adjusted at the beginning of each collection period based on average daily gains of pigs obtained from Exp. 1.

This study was approved by Michigan State University All University Committee on Animal Use and Care.

Sample Collection
Experiment 1.
The experiment consisted of six collection periods. Each period lasted 10 d. Feces and urine were collected for a duration of 5 d from each pig following a 5-d adaptation period to the diets. Ferric oxide was used as an indigestible marker to indicate the initiation and termination of collection for fecal matter. Each pig received 5 g of ferric oxide mixed with 100 g of feed at the first meal on d 1 and 6. The remaining meal allotment was fed after the ferric oxide-feed mixture was consumed completely. Total daily fecal samples were collected once daily, weighed, and stored at 4°C for 5 d. Fecal samples were homogenized for 15 min using a Hobart mixer (model A-200, Hobart Manufacturing, Troy, Ohio). Subsamples were collected (500 g) and stored in 490-mL plastic containers and frozen at -20°C. For urine collection, 10 mL of 6N HCl was added daily to each collection vessels to reduce urine pH and NH3 volatilization (Russell et al., 1983). The funnel attached to the collection bucket contained glass wool to prevent fecal and other particulate matter from contaminating the urine. The urine was filtered again through four layers of cheesecloth into a clean bucket. Approximately 20% of daily urine was stored at 4°C. At the end of each collection period, daily urine samples were pooled and mixed, and a sample of pooled urine was stored at -20°C.

Experiment 2.
The experiment consisted of six collection periods. Chromic oxide (0.25% of diet) was used as an indigestible marker for determination of AA digestibility. Digesta was collected from each pig over two consecutive days for 12 h each day following a 5-d adaptation period to the test diets. Digesta samples were collected from the T-cannula at the terminal ileum as described by Stein et al. (1998). Digesta was kept on ice throughout the sampling period, pooled into 4-L plastic bottles, and stored at 4°C until the 2-d sampling period was completed. Pooled digesta was homogenized for each pig and stored in plastic bottles at -20°C.

Sample Analysis
For chemical analysis, fecal and digesta samples were freeze-dried (VirTis model 25-SRC, VirTis Co., Gardiner, NY). Fecal, digesta, and feed samples were finely ground using a cyclone mill (Cyclotec sample mill 1093, Hoganas, Sweden) with a 1-mm mesh screen. Nitrogen content in feces and feed was determined using an automated N analyzer (Leco FP-2000, Leco Co., St. Joseph, MI; AOAC No. 990.03). Dry matter of feces, digesta, and feed was determined following a 12-h drying period at 70°C using a vacuum oven (model 583/Full View, National Appliance Co., Portland, Oregon). Urine was filtered (Whatman filter paper No.4, Whatman Int. Ltd., Maidstone, England) and N concentration was measured using the same procedure as described for feed and feces. Amino acid analysis was performed on feed and digesta samples using the Pico-Tag method (Waters Co., Milford, MA) following a 24-h acid hydrolysis in 6 N HCl at 105°C and 121 mm Hg. Samples were derivatized with phenylisothiocyanate and analyzed using a Waters HPLC (Waters Co.) fitted with a 15-cm hydrolysate column. Sulfur amino acids were preoxidized with performic acid and analyzed following post-column derivatization with ninhydrin (Thermo Quest, Thermo Separation Products, San Jose, CA).

Chromium concentration in feed and digesta was determined using a modified procedure for perchloric digestion described by Arthur (1970). Briefly, feed and digesta (0.3 g) were digested using 20 mL of concentrated nitric acid and heated to boiling, followed by oxidation of Cr3+ with 10 mL of perchloric acid, and Cr6+ determination by atomic absorption spectrophotometry (Unicam 93, TJA Unicam Co., Cambridge, U.K.).

Calculations
Apparent ileal AA digestibility (AID), endogenous AA losses (EAL), and standardized ileal AA digestibility (SID) were calculated in the following manner:


where AAf is the AA concentration in diet, AAd is the AA concentration in digesta, Crf is the analyzed chromium concentration in diet, and Crd is the analyzed chromium concentration in digesta.

Statistical Analysis
Data were subjected to ANOVA using the PROC MIXED procedure of SAS (SAS Inst., Inc., Cary, NC). Effects of pig, period, and diet were included in all statistical models. Differences between all pair-wise mean comparisons were evaluated using the Tukey-Kramer test (Younger, 1998). Relationships between dietary CP concentration and N balance parameters and between dietary CP concentration and AA digestibility were determined using contrast (linear and quadratic) comparisons with orthogonal polynomials. Coefficients used for contrasts were based on the calculated CP concentration in the intact corn-soybean meal mixture, i.e., 15, 12, 9, and 6%. Statistical significance was based on an experiment-wise type-I error rate of 0.05.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
Implications
 Literature Cited
 
Nitrogen Excretion
Nitrogen intake and losses data, as affected by dietary CP concentration and protein-free and casein-based diets are presented in Table 5Go. Total N losses decreased (P < 0.05) by 21, 37, 63, and 79% when feeding the 12, 9, 6, and 0% (protein-free) CP diet, respectively, compared with feeding the 15% CP diet (Table 5Go). Our values are lower than previously reported, where N excretion in growing pigs was reduced by 40 and 80% when dietary CP concentration was decreased from 16 to 14% (Hobbs et al., 1996) and from 17 to 11% (Kephart and Sherritt, 1990), respectively, but are very close to an average as reviewed by Kerr (1995). Daily fecal N losses and fecal DM output in pigs fed the protein-free or the casein-based diet were similar (P > 0.05). The protein-free and casein-based diets revealed that approximately 1.85 g of N excreted per day (averaged between 1.63 g from protein-free and 2.02 g from casein-based diet) was of endogenous origin (Table 5Go). Thus, nonspecific endogenous N alone contributed 22 to 48% of the daily fecal N output in pigs fed a 15 to 6% intact CP diet, respectively. Fecal N did not differ among the 9, 12, and 15% CP diets; hence, fecal N was not a major contributor to reducing total N losses. Similarly, fecal N excretion was not different in growing pigs fed diets with reduced CP concentration from 17 to 11% (Kephart and Sherritt, 1990) and from 16 to 12% (Kerr and Easter, 1995). Thus in this study, the largest contribution to reduction in total N losses when decreasing CP concentration from 15 to 9% was of urinary origin. Urinary N decreased (P < 0.05) by approximately 50% when dietary CP concentration was reduced from 15 to 9%. Similar findings have been reported by others (Russell et al., 1983; Kephart and Sherritt, 1990; Kerr and Easter, 1995). On the other hand, further reduction in CP from 9 to 0% (protein-free diet) reduced total N excretion mainly via a decrease in fecal N. Taken together, within practical feeding conditions, the largest impact of dietary CP reduction is on urinary N excretion.


View this table:
[in this window]
[in a new window]
  		Table 5. Comparison of daily N excretion and fecal DM output between 50-kg pigs fed reduced protein diets and pigs fed a protein-free or casein-based dieta
 
Nitrogen Balance
Nitrogen absorption, retention, digestibility and utilization data, as affected by dietary CP reduction, are presented in Table 6Go. Nitrogen losses and N absorbed decreased linearly (P < 0.001) with decreasing CP concentration. Both a linear (P < 0.001) and a quadratic (P < 0.05) decrease in N retention were found with decreasing dietary CP concentration. Nitrogen retention appeared to remain at a plateau in pigs fed the 15 and 12% CP diet, but decreased (P < 0.001) as dietary CP concentration decreased further to 9 and 6%. Others (Kerr and Easter, 1995; Shriver et al., 2000) have also reported no difference in N retention values between growing pigs fed standard diets and pigs fed diets with 3% unit reduction in dietary CP concentration. In contrast, N retention in 30-kg pigs fed diets containing 15.7% CP was reduced by 12% compared with that in pigs fed a diet containing 18.5% CP (Zervas and Zijlstra, 2002a). Nitrogen retention also decreased in 32-kg pigs when diets containing either 16.9% CP or 13.8% CP were fed compared with that in pigs fed a control diet containing 19.7% CP (Zervas and Zijlstra, 2002b). In the current study, despite the inclusion of crystalline AA to meet the ileal digestible AA requirement as outlined in NRC (1998), N retention decreased as dietary CP concentration decreased to 6 and 9% unit reduction, agreeing with Zervas and Zijlstra (2000a,b).


View this table:
[in this window]
[in a new window]
  		Table 6. Nitrogen balance in 50-kg pigs fed a protein-adequate diet (15% CP) or reduced-protein dietsa
 
Shriver et al. (2000) found no difference in ADG, ADFI, and gain:feed in early growing and finishing pigs fed a 14 vs. 18%, 12 vs. 16%, and 10 vs. 12% CP diets, respectively. Liu et al. (2000) reported no decrease in growth performances in 60-kg pigs fed diets containing 10.4 vs. 15.4% CP. In contrast, other studies report feed efficiency reductions and depressed growth in 18- to 35-kg pigs where dietary CP concentration was lowered from 16 to 12% (Russell et al., 1983) or from 17 to 11% (Kephart and Sherritt, 1990).

Approximately 11 and 30% of the total dietary AA were of crystalline origin in the 9 and 6% CP diets, respectively. However, it is unlikely that the reduction in daily N retention was due to a decreased utilization of these crystalline AA because pigs were offered feed three times daily. Indeed, N retained as a percentage of that absorbed increased linearly (P < 0.001) as dietary CP concentration decreased (Table 6Go), despite the fact that all pigs were fed at 3.5% of BW. Recently, Zervas and Zijlstra (2002a) reported a decrease in N retention in 30-kg pigs offered restricted access to a 15.6% CP diet compared with that in pigs fed 18.5% CP diet, but only a tendency to differ in N retention when pigs were offered unlimited access to those diets. The latter may thus explain to some extent the N retention response seen in this study. Liu et al. (1999) also indicated that isoleucine and/or valine intake may limit performance in late-finishing pigs fed reduced CP diet (4 percentage units reduction).

Alternatively, such a large reduction in dietary CP may reduce the availability of AA in the form of di- and tripeptides. In the adult human, approximately 33% of protein is absorbed as AA and as much as 67% as small peptides (Zaloga, 1990). It is well recognized that certain small peptides are utilized preferentially as a source of AA over free AA for protein synthesis by both myogenic (Yuanlong et al., 1996) and mammary cells (Backwell et al., 1994; Wang et al., 1996). It is well documented that a large gap exists between the metabolic fate of AA arising from AA-based diets compared with those arising from more complex protein-based diets. In adult humans, dietary leucine derived from intact casein is utilized more efficiently for whole-body protein synthesis compared with an equivalent intake of free AA (Metges et al., 2000). Reducing dietary protein may limit peptide availability to gut cells for synthesis of intestinal constitutive proteins. Amino acid-based diets have been shown to increase gut atrophy (Birke et al., 1990) and gut permeability (Alverly et al., 1988), and to reduce N retention and growth in rats (Poullain et al., 1989). The gut as an organ has one of the highest rate of protein synthesis of any tissue in the body (Reeds and James, 1983). Taken together, reducing dietary CP below a certain concentration may impair gut functions and as such affect whole body N retention.

L-Glutamic acid was provided as a source of amino N. Thus, amino N availability was unlikely a limiting factor. Conversely, decreased absorption rate of dispensable AA in reduced-CP diets may contribute to a decrease in amino-N. Aspartate and proline uptake by enterocytes determined in everted sacs from adult male rats decreased with decreasing protein concentration, whereas dietary protein concentration per se had only minor effect on lysine and leucine uptake by enterocytes (Karasov et al., 1987; Ferraris and Vinnakota, 1993; Casirola et al., 1994). In growing pigs fed soybean meal-based diets with varied concentrations of dietary CP ranging from 4 to 24%, ileal apparent AA digestibility decreased at CP concentration below 8% but remained unchanged at CP concentrations above 12% (Fan et al., 1994). Similarly, in rats fed diets consisting of meat and bone meal as the sole feed ingredient, with 2.5 to 20% CP, ileal apparent AA digestibility decreased when dietary CP concentration fell below 9.5% (Donkoh and Moughan, 1995). Donkoh and Moughan (1994) reported that ileal AA digestibility, when accounting for endogenous AA losses and thus expressed on a true basis, did not decrease when dietary CP was reduced. However, Stein (1998) found that all AA expressed on an ileal apparent basis and most AA digestibility expressed on a standardized basis decreased in a corn-soybean meal-based diet that was reduced to 10% CP with no supplemental crystalline AA when compared with a corn-soybean meal-based diet containing 16% CP. Currently, no information is available on apparent and standardized ileal digestibility of AA in reduced CP diets containing multiple feed ingredients and supplemented with crystalline AA. To test whether the decrease in N retention observed in our first experiment in pigs fed the 9 and 6% CP diets was related to a decrease in dispensable AA absorption, we determined ileal AA digestibility of these same diets in a second experiment.

Ileal Amino Acid Digestibility
Endogenous AA Losses.
Endogenous AA losses found in the digesta of pigs consuming the protein-free diet (Table 7Go) were in agreement with values reported by Leterme et al. (1992) and Stein et al. (1999). However, results of EAL from feeding pigs a casein-based diet (Table 7Go) were lower than published values of Liebholz (1982), Chung and Baker (1992), and Butts et al. (1993). Similar to Wang and Fuller (1989), most indispensable and dispensable AA in the endogenous losses estimated by the protein-free and casein-based diets were not different. However, endogenous losses for arginine, alanine, and tyrosine were lower (P < 0.05) when the casein-based diet was fed compared with the protein-free diet. Based on a comparison of our results to others, we have chosen to present our standardized AA digestibility calculated using EAL from pigs fed the protein-free diet.


View this table:
[in this window]
[in a new window]
  		Table 7. Endogenous amino acid losses in 50-kg pigs estimated using a protein-free or casein-based diet, mg/kg
 
Ileal Apparent and Standardized AA Digestibility.
For all dispensable and most indispensable AA, apparent (Table 8Go) and standardized (Table 9Go) ileal digestibility increased linearly (P < 0.01, and for arginine, P < 0.05) as dietary CP concentration decreased. The increase in digestibility for the indispensable AA as dietary CP decreased was in part due to the large contribution of free AA from crystalline AA supplementation. However, indispensable AA, such as arginine, histidine, leucine, and phenylalanine, were not supplemented in the 9% CP diet. Donkoh and Moughan (1994) demonstrated that dietary CP concentrations had no effect on standardized ileal AA digestibility of feed ingredient fed as a single source of protein. The current study reports ileal AA digestibility from a mixture of multiple feed ingredients and crystalline AA. Therefore, the increase in ileal AA digestibility in this study was not solely due to crystalline AA inclusion per se. This is in agreement with the earlier suggestion by Christensen (1984) that the small intestine responds to restricted dietary protein intake by increased intestinal AA absorption. Ileal digestibility of some AA improves when the observed true digestibility AA values are compared to calculated values in diets containing multiple feed ingredients (Imbeah et al., 1988). Although not previously documented, results of the second study suggest that ileal digestibility of AA arising from a mixture of crystalline and intact protein source maybe additive. Hence, differences between the results of our study and those of Stein (1998) may be due to the presence of crystalline AA in our reduced CP diets.


View this table:
[in this window]
[in a new window]
  		Table 8. Apparent ileal amino acid digestibility of an adequate corn-soybean meal-based diet and corn-soybean meal-based diets of reduced protein concentration fed to 50-kg growing pigs, % (DM basis)a
 

View this table:
[in this window]
[in a new window]
  		Table 9. Standardized ileal amino acid digestibility of an adequate corn-soybean meal-based diet and corn-soybean meal-based diets of reduced protein concentration fed to 50-kg growing pigs, % (DM basis)a
 
It is unknown whether an interaction occurs for gut absorption between crystalline AA and protein-bound AA. Reducing dietary CP and providing indispensable crystalline AA may offer a better balance of AA for uptake across the gut by reducing competition for AA transport by enterocytes. Amino acid transport systems can interact with multiple AA (Torras Llort, 1996; Soriano Garcia et al., 1998; 1999). For example, it has been demonstrated that L-methionine and L-lysine share transport systems with cationic and neutral AA in the intestine of chickens. Inhibition or competition for uptake in the presence of other AA occurs between L-methionine and L-lysine (Torras Llort, 1998; Soriano Garcia et al., 1998; 1999). Uptake of lysine by pig jejunal enterocytes is inhibited by leucine (Matthews et al., 1996). In this study, no crystalline leucine was provided, and dietary leucine concentration decreased as dietary CP concentration was reduced (Table 2Go). Amino acids themselves are inducers of AA transport systems (Diamond and Karasov, 1987) and pancreatic peptidases (Johnson, 2001); thus the presence of readily available AA of crystalline origin may increase the absorption rate of peptide- and protein-bound AA.

In conclusion, reducing dietary CP concentration from 15 to 12% did not reduce N retention but significantly reduced total N losses via an increase in N utilization and a consequential decrease in urinary N excretion. Further reduction in CP concentration lowered total N losses mainly via an increase in ileal AA digestibility and a consequential reduction in fecal N excretion, but it also decreased N retention. Therefore, the reduction in N retention was not related to a decrease in ileal digestibility of dispensable AA. Indeed, decreasing dietary CP concentration beyond 12% increased ileal digestibility of both protein-bound dispensable and indispensable AA. Basal N endogenous losses contributed to an important percentage of total N losses, and this contribution increased as dietary CP concentration decreased. The impact of an increased endogenous N contribution to total N losses with reduction in CP concentration with regard to waste odor issues is yet to be determined.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 Implications
Literature Cited
 
This study reaffirmed that dietary crude protein concentration can be decreased from 15 to 12% in 50-kg growing pigs without compromising N retention. This decrease in crude protein resulted in an approximately 20% reduction in total N output, with the majority being of urinary origin. Our study also supports the finding of others, whereby reduction in crude protein concentration exceeding four percentage units decreases N retention, despite both the inclusion of amino N via crystalline L-glutamic acid and dietary formulation based on an ideal digestible amino acid profile. Our results suggest that dietary amino acid inclusion rates may be limited; however, the cause of this limitation is currently unknown. Because ileal amino acid digestibility is not compromised in diets with reduced crude protein concentrations, but rather improved, other factors contributing to reduction in N retention are involved. Identification of these factors is imperative to better design nutritional strategies leading to a decrease in N losses without compromising growth performance.


   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 care and assistance in animal handling. 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 and Discussion
 Implications
 Literature Cited
 


Alverly, J. C., E. Aoys, and G. S. Moss. 1988. Total parenteral nutrition promotes bacterial translocation from the gut. Surgery 104:185–190.[Medline]

Arthur, D. 1970. The determination of chromium in animal feed and excreta by atomic absorption spectrophotometry. Can. Spectrosc. 15:134–140.

Backwell, F. R. C., B. J. Bequette, D. Wilson, A. G. Calder, J. A. Metcale, D. Wray-Cahen, J. C. MacRae, D. E. Beever, and G. E. Lobley. 1994. The utilization of dipeptides by the caprine mammary gland for milk protein synthesis. Am. J. Physiol. 267:R1–R6.

Birke, H., O. Thorlacus-Ussing, and I. Hessov. 1990. Trophic effect of dietary peptides on mucosa in the rat small bowel. JPEN 14:26S (Abstr).

Butts, C. A., P. J. Moughan, W. C. Smith, and D. H. Carr. 1993. Endogenous lysine and other amino acid flows at the terminal ileum of the growing pig (20 kg body weight): The effect of protein-free, synthetic amino acid, peptide and protein alimentation. J. Sci. Food Agric. 61:31–40.

Casirola, D. M., R. R. Vinnakota, and R. P. Ferraris. 1994. Intestinal amino acid transport in mice is modulated by diabetes and diet. J. Nutr. 124:842–852.

Christensen, H. N. 1984. The regulation of amino acid and sugar absorption by diet. Nutr. Rev. 42:237–242.[Medline]

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]

Diamond, J. M., and W. H. Karasov. 1987. Adaptive regulation of intestinal nutrient transporters. Biochemistry 84:2242–2245.

Donkoh, A., and P. J. Moughan. 1994. The effect of dietary crude protein content on apparent and true ileal nitrogen and amino acid digestibilities. Br. J. Nutr. 72:59–68.[Medline]

Donkoh, A., P. J. Moughan, and P. C. H. Morel. 1995. Comparison of methods to determine the endogenous amino acid flow at the terminal ileum of the growing rat. J. Sci. Food Agric. 67:359–366.

Fan, M. Z., W. C. Sauer, R. T. Hardin, and K. A. Lien. 1994. Determination of apparent ileal amino acid digestibility in pigs: Effect of dietary amino acid level. J. Anim. Sci. 72:2851–2859.[Abstract]

Ferraris, R. P., and R. R. Vinnakota. 1993. Regulation of intestinal nutrient transport is impaired in aged mice. J. Nutr. 123:502–511.

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

Imbeah, M., W. C. Sauer, and R. Mosenthin. 1988. The prediction of the digestible amino acid supply in barley-soybean meal or canola meal diets and pancreatic enzyme secretion in pigs. J. Anim. Sci. 66:1409–1417.[Abstract/Free Full Text]

Johnson, L. R. 2001. Pancreatic secretion. Page 102 in Gastrointestinal Physiology. L. R. Johnson, ed. Mosby Inc., St. Louis, MO.

Karasov, W. H., D. H. Solberg, and J. M. Diamond. 1987. Dependence of intestinal amino acid uptake on dietary protein or amino acid levels. Am. J. Physiol. 252:G614–G625.

Kendall, D. C., B. T. Richert, A. L. Sutton, J. W. Frank, S. A. DeCamp, K. A. Bowers, D. Kelly, and M. Cobb. 1999. Effects of fiber addition (10% soybean hulls) to a reduced crude protein diet supplemented with synthetic amino acids verses a standard commercial diet on pig performance, pit composition, odor and ammonia levels in swine buildings. J. Anim. Sci. 77(Suppl.1):176. (Abstr.)

Kephart, 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. 1995. Nutritional strategies for waste reduction-management: Nitrogen. Pages 47–68 in New Horizons in Animal Nutrition and Health. Proc. 11th Ann. Carolina Nutr. Conf., Raleigh.

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]

Leibholz, J. 1982. The flow of endogenous nitrogen in the digestive tract of young pigs. Br. J. Nutr. 48:509–518.[Medline]

Lenis, N. P., H. T. M. van Diepen, P. Bikker, A. W. Jongbloed, and J. van der Meulen. 1999. Effect of the ratio between essential and nonessential amino acids in the diet on utilization of nitrogen and amino acids by growing pigs. J. Anim. Sci. 77:1777–1787.[Abstract/Free Full Text]

Leterme, P., L. Pirard, and A. Thewis. 1992. A note on the effect of wood cellulose level in protein-free diets on the recovery and amino acid composition of endogenous protein collected from the ileum in pigs. Anim. Prod. 54:163–165.

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.)

Liu, H., G. L. Allee, K. J. Touchette, J. W. Frank, and J. D. Spencer. 2000. Effect of reducing protein and adding amino acids on performance, carcass characteristics, and nitrogen excretion, and the valine requirement of early-finishing barrows. J. Anim. Sci. 78(Suppl. 2):69. (Abstr.)[Abstract/Free Full Text]

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]

Matthews, J. C., E. A. Wong, P. K. Bender, and K. E. Webb Jr. 1996. Demonstration and characterization of the transport system capable of lysine and leucine absorption that in encoded in porcine jejunal epithelium by expression of mRNA in Xenopus laevis oocytes. J. Anim. Sci. 74:127–137.[Abstract]

Metges, C. C., A. E. El-Khoury, A. B. Selvaraj, R. H. Tsay, A. A. Atkinson, M. R. Regan, B. J. Bequette, and V. R. Young. 2000. Kinetics of L-[1-13C]leucine when ingested with free amino acids, unlabeled or intrinsically labeled casein. Am. J. Physiol. Endocrinol. Metab. 278:1000–1009.

NRC. 1998. Pages 113–114 in Nutrient Requirements of Swine. 10th rev. ed. Natl. Acad. Press. Washington, DC.

Pierce, J. L., K. L. Enright, G. L. Cromwell, L. W. Turner, and T. C. Bridges. 1994. Dietary manipulation to reduce the N and P excretion by finishing pigs. J. Anim. Sci. 72(Suppl.1):331. (Abstr.)

Poullain, M. G., J. P. Cezard, L. Roger, and F. Mendy. 1989. Effect of whey proteins, their oligopeptide hydrolysates, and free amino acid mixtures on growth and nitrogen retention in fed and starved rats. JPEN 13:382–386.[Abstract]

Reeds, P. J., and W. P. T. James. 1983. Nutrition: The changing scene. Lancet 12:571–574.

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.

Shriver, J. A., S. D. Carter, L. A. Pettey, and B. W. Senne. 2000. Effects of adding fiber sources to low protein, amino acid-supplemented diets on nitrogen excretion and performance of finishing pigs. J. Anim. Sci. 78(Suppl. 2):168. (Abstr.)

Soriano Garcia, J. F., M. Torras Llort, R. Ferrer, and M. Moreto. 1998. Multiple pathways for L-methionine transport in brush-border membrane vesicles from chicken jejunum. J. Physiol. (Lond.) 509:527–539.[Abstract/Free Full Text]

Soriano Garcia, J. F., M. Torras Llort, M. Moreto, and R. Ferrer. 1999. Regulation of L-methionine and L-lysine uptake in chicken jejunal brush-border membrane by dietary methionine. Am. J. Physiol. 277:R1654–1661.

Stein, H. H. 1998. Comparative amino acid digestibilities in growing pigs and sows. Ph.D. Diss., Univ. of Illinois, Urbana.

Stein, H. H., C. F. Shipley, and R. A. Easter. 1998. Technical note: A technique for inserting a T-cannula into the distal ileum of pregnant sows. J. Anim. Sci. 76:1433–1436.[Abstract/Free Full Text]

Stein, H. H., N. L. Trottier, C. Bellaver, and R. A. Easter. 1999. The effect of feeding level and physiological status on total flow and amino acid composition of endogenous protein at the distal ileum in swine. J. Anim. Sci. 77:1180–1187.[Abstract/Free Full Text]

Torras Llort, M., R. Ferrer, J. F. Soriano Garcia, and M. Moreto. 1996. L-Lysine transport in chicken jejunal brush border membrane vesicles. J. Membr. Biol. 152:183–193.[Medline]

Torras Llort, M., J. F. Soriano Garcia, R. Ferrer, and M. Moreto. 1998. Effect of a lysine-enriched diet on L-lysine transport by the brush-border membrane of the chicken jejunum. Am. J. Physiol. 274:69–75.

Tuitoek, K., L. G. Young, C. F. M. d. Lange, and B. J. Baker. 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]

Wang, T. C., and M. F. Fuller. 1989. The optimum dietary amino acid pattern for growing pigs. 1. Experiments by amino acid deletion. Br. J. Nutr. 62:77–89.[Medline]

Wang, S., K. E. Webb Jr., and M. R. Akers. 1996. Peptide-bound methionine can be a source of methionine for the synthesis of secreted proteins by mammary tissue explants from lactating mice. J. Nutr. 126:1622–1672.

Younger, M. S. 1998. SAS Companion for P.V. Rao’s Statistical Research Methods in the Life Sciences. Duxbury Press. Pacific Grove, CA.

Yuanlong, P., P, K. Bender, M. Akers, and K. E. Webb Jr. 1996. Methionine-containing peptides can be used as methionine sources for protein accretion in cultured C2C12 and MAC-T cells. J. Nutr. 126:232–241.

Zaloga, G. P. 1990. Physiological effects of peptide-based enteral formulas. Nutr. Clin. Prac. 5:231–237.

Zervas, S., and R. T. Zijlstra. 2002a. Effects of dietary protein and fermentable fiber on nitrogen excretion patterns and plasma urea in grower pigs. J. Anim. Sci. 80:3247–3256.[Abstract/Free Full Text]

Zervas, S., and R. T. Zijlstra. 2000b. Effects of dietary protein and oathull fiber on nitrogen excretion patterns and postprandial plasma urea profiles in growing pigs. J. Anim. Sci. 80:3238–3246.


This article has been cited by other articles:


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
F. Guay and N. L. Trottier
Muscle growth and plasma concentrations of amino acids, insulin-like growth factor-I, and insulin in growing pigs fed reduced-protein diets
J Anim Sci, November 1, 2006; 84(11): 3010 - 3019.
[Abstract] [Full Text] [PDF]

Home page
 J. Environ. Qual.Home page
D. M. Panetta, W. J. Powers, H. Xin, B. J. Kerr, and K. J. Stalder
Nitrogen excretion and ammonia emissions from pigs fed modified diets.
J. Environ. Qual., July 1, 2006; 35(4): 1297 - 1308.
[Abstract] [Full Text] [PDF]

Home page
 J ANIM SCIHome page
F. Guay, S. M. Donovan, and N. L. Trottier
Biochemical and morphological developments are partially impaired in intestinal mucosa from growing pigs fed reduced-protein diets supplemented with crystalline amino acids
J Anim Sci, July 1, 2006; 84(7): 1749 - 1760.
[Abstract] [Full Text] [PDF]

Home page
 J ANIM SCIHome page
F. O. Opapeju, A. Golian, C. M. Nyachoti, and L. D. Campbell
Amino acid digestibility in dry extruded-expelled soybean meal fed to pigs and poultry
J Anim Sci, May 1, 2006; 84(5): 1130 - 1137.
[Abstract] [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 Otto, E. R.
Right arrow Articles by Trottier, N. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Otto, E. R.
Right arrow Articles by Trottier, N. L.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS