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Nitrogen metabolism and growth performance of gilts fed standard corn-soybean meal diets or low-crude protein, amino acid-supplemented diets¹

Department of Animal Science, University of Nebraska, Lincoln 68583-0908

³ Correspondence:
C206 Animal Sciences (phone: 402-472-6423; fax: 402-472-6362; E-mail:
alewis2{at}unl.edu).

	Abstract

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Two experiments were conducted to determine the CP concentration below which N retention and growth performance are reduced when low-protein, amino acid-supplemented, corn-soybean meal diets are fed. In a N balance trial (Exp. 1), 12 gilts (initial weight 41 kg) were fitted with urinary catheters and fed six different diets during three 7-d periods in an incomplete block design. The diets were: 1) 18% CP; 2) 14% CP + AA; 3) 16% CP; 4) 12% CP + AA; 5) 14% CP; and 6) 10% CP + AA. Amino acids (lysine, threonine, tryptophan, and methionine) were supplemented such that the concentrations in the low-protein diets were equal to those in their standard (4% CP higher) counterparts. Nitrogen retention (g/d) decreased (P < 0.01) as CP decreased, in both standard (27.10, 24.53, and 20.99) and low-protein (21.51, 19.18, and 15.83) diets, but was lower (P < 0.01) in low-protein diets. There were no differences among treatments (P > 0.05) in biological value (68.2% standard vs 71.0% low-protein). In a growth performance trial (Exp. 2), 36 gilts (initial weight 19.5 kg) were penned individually and fed one of six diets for 35 d in a randomized complete block design. Dietary treatments were a 16% CP standard diet and low-protein diets formulated to contain 15, 14, 13, 12, and 11% CP supplemented with crystalline lysine, tryptophan, threonine, and methionine to equal the total concentrations in the standard diet. Protein concentration affected (P 0.05) ADG, ADFI, feed efficiency, fat-free lean gain, longissimus muscle area, plasma urea, and plasma concentrations of most essential AA. For most of these traits, the major difference was poor performance of pigs fed the 11% CP diet. Thus, in Exp. 1, at AA concentrations from deficient to excess, low-protein, amino acid-supplemented diets failed to produce the same N retention as the equivalent corn-soybean meal diets. However in Exp. 2, the same performance was obtained with 16, 15, 14, 13, and 12% CP. Based on these data, we suggest that N balance is more sensitive than growth to amino acid adequacy and that other AA (e.g., isoleucine and valine) may limit growth performance when the protein concentration is reduced by more than four percentage units.

Key Words: Amino Acids • Growth • Nitrogen Balance • Pigs

	Introduction

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Concern about environmental pollution by N from swine enterprises has renewed interest in low-protein diets for pigs (Kornegay and Verstegen, 2001). Kerr and Easter (1995) estimated that each one percentage unit reduction in dietary protein (when accompanied by appropriate AA supplementation) resulted in 8% less N excreted in manure.

There are, however, conflicting data about the extent to which the protein content of the diets of growing pigs can be reduced. A reduction of two or three percentage units of protein is possible with no reduction in ADG or feed efficiency when AA are supplemented (Cromwell, 1996; Tuitoek et al., 1997b). In some experiments, reductions of more than three percentage units also have produced no reductions in ADG or feed efficiency (Hahn et al., 1995; Kerr et al., 1995), but this has not always been observed (Hansen et al., 1993; Gómez et al., 2002a). Differences between standard diets and low-protein, AA-supplemented diets are most evident when carcass leanness or N retention is measured (Tuitoek et al., 1997a, b; Knowles et al., 1998).

One explanation for differences among experiments is that in some cases the standard diet may have exceeded the AA requirements, whereas in other experiments the standard diet may have only just met or been slightly below the AA requirements. With this in mind, we devised an experiment to evaluate the effect on nitrogen retention of reducing the dietary protein concentration by four percentage units in situations in which the standard diets ranged in protein content from excess to clearly deficient. In a second experiment, our objective was to determine the CP concentration (from 16 to 11% CP) at which growth performance is reduced when corn-soybean meal, AA-supplemented diets are fed to growing pigs.

	Materials and Methods

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Exp. 1
Three standard, corn-soybean meal diets and three low-protein counterpart diets (4% CP below each standard diet) were formulated and mixed. The low-protein diets were supplemented with L-lysine, L-tryptophan, L-threonine, and DL-methionine to achieve AA concentrations (on a total basis) equal to those of the counterpart standard diets. Thus, the six diets (Tables 1 and 2) were as follows: 1) 18% CP; 2) 14% CP + AA; 3) 16% CP; 4) 12% CP + AA; 5) 14% CP; and 6) 10% CP + AA. Diets were fed to 12 Large White x Landrace x Duroc x Hampshire gilts. The treatment arrangement consisted of 12 incomplete blocks (gilts), with the six diets being assigned in three 7-d periods in an arrangement designed to avoid carry-over effects. Gilts were housed in metabolism crates and allowed ad libitum access to feed and water. Room temperature was maintained at 22°C. The weight of the gilts averaged over the start of the three periods was 40.6 ± 0.66 kg. Five days before the beginning of the experiment, gilts were anesthetized and urinary catheters (Allegiance No. 14; Allegiance Healthcare Corp., McCaw Park, IL) were inserted into the bladder.

Diet and freeze-dried fecal samples were ground through a 1-mm screen before analysis. The N content of feed, feces, and urine was determined using the Kjeldahl method (AOAC, 1990). Gross energy of feed, feces, and urine was determined in an adiabatic bomb calorimeter. Urine was analyzed for urea (Marsh et al., 1965) and creatinine concentration (Chasson et al., 1961). Other N in urine was calculated by subtracting urea N and creatinine N from total N. For AA (other than tryptophan) analysis, diet samples were hydrolyzed for 20 h in 6 N HCl at 105°C. Sulfur AA were determined in samples that were preoxidized with performic acid before acid hydrolysis. Amino acids were separated using ion-exchange chromatography. The AA analyzer contained a cation exchange column and AA were eluted by a gradient of lithium buffers. After elution from the column, the AA were quantified fluorometrically using o-phthalaldehyde as the derivatization agent. Tryptophan was determined after hydrolysis with 5 N NaOH at 121°C for 20 h using the method of Hess and Udenfriend (1959) as modified by Lewis et al. (1976).

Data were analyzed by ANOVA using PROC GLM of SAS (SAS Inst. Inc., Cary, NC). Each gilt was considered an experimental unit. The model used was an incomplete block design with 12 incomplete blocks. Initial weight and feed intake were included as covariates in the analysis for all traits except feed intake, for which only initial weight was included. Linear and quadratic effects of protein level, the effect of AA source (standard or low-protein), and interactions were tested.

Exp. 2
A standard, 16% CP, corn-soybean meal diet and five low-protein diets supplemented with crystalline lysine, tryptophan, threonine, and methionine were formulated and mixed. The six diets (Tables 3 and 4) were as follows: 1) 16% CP, standard diet; 2) 15% CP; 3) 14% CP; 4) 13% CP; 5) 12% CP; and 6) 11% CP. Corn and soybean meal sources were analyzed for protein content before formulating the diets. The protein content of each diet was formulated by adjusting the amounts of corn and soybean meal. Additions of crystalline AA to Diets 2 to 6 were designed to achieve AA concentrations (on a total basis) equal to those in Diet 1. Diets were analyzed for protein and AA using the procedures described for Exp. 1.

Blood was collected from the anterior vena cava on d 0, 14, and 35. Bleeding was started at 0700 and all pigs were bled within 45 to 60 min. Feed was not withheld before the bleeding period. Evacuated tubes containing heparin were used to collect the blood, and samples were placed on ice until all pigs had been bled. Plasma was separated by centrifugation, decanted, and frozen until analyzed. Blood plasma was analyzed for urea using the method of Marsh et al. (1965) and for AA using ion-exchange chromatography as described for diets. Before analysis of AA concentrations, plasma was deproteinized with 30 mg of sulfosalicylic acid per milliliter of plasma and centrifuged at 820 x g for 20 min.

Data were analyzed by ANOVA as a randomized complete block design (six blocks) using PROC GLM of SAS. Pig was considered the experimental unit. In addition to the main effect of treatment, linear, quadratic, and cubic effects of dietary protein concentration were tested.

	Results

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Exp. 1
Growth Performance.
The growth performance data (Table 5) are based on 7-d periods only, and should be interpreted cautiously. Nevertheless, ADG of gilts fed AA-supplemented diets were lower (P < 0.01) than those of gilts fed standard, counterpart diets, even though each pair of diets contained equal amounts of lysine, tryptophan, threonine, and methionine (Table 2). When FFLG was calculated from N retention data, the results reflected the differences in ADG (P < 0.01), and there was also a linear decrease (P < 0.01) in FFLG as dietary protein concentration decreased. There were no dietary effects (P > 0.10) on ADFI or G/F. In this experiment ADFI was approximately 3.8% of BW.

Nitrogen excreted in feces reflected the differences in N intake, although the differences were not as significant (P < 0.05). There was an interaction of effect of protein level x source of AA (P < 0.05), with a greater decrease in standard diets than in AA-supplemented diets as dietary protein decreased.

The apparent digestibility of N was higher (P < 0.01) in standard diets than in AA-supplemented diets. There was also an interaction between the effect of protein level x source of AA (P < 0.01). Digestibility of N increased in standard diets, but decreased in AA-supplemented diets, as dietary protein decreased.

Type of diet had a large effect on the excretion of N in urine (P < 0.01), with less urinary N from AA-supplemented diets than from standard diets. However, there was no effect (P > 0.10) of dietary protein concentration on N excretion in urine. The separation of urine N into its components (urea N, creatinine N, and other N) showed that most of the change in total urine N was caused by a change in urea N. The excretion of urea N was higher (P < 0.01) in gilts fed standard diets than in gilts fed AA-supplemented diets, but there were no differences (P > 0.10) in creatinine N or other N due to dietary treatments.

We expected that AA supplementation would increase the apparent biological value of the N ingested (measured as: N intake - [N in feces + N in urine]/N intake - N in feces). Diets that were supplemented with AA seemed to have a higher apparent biological value than their respective standard diets, but these differences were not significant (P > 0.20).

Nitrogen retention was reduced as dietary CP was reduced in both standard and AA-supplemented diets (P < 0.01). In addition, N retention was consistently lower (P < 0.01) in AA-supplemented diets than in corresponding standard diets, even though they contained equal concentrations of the first four limiting AA. Contrary to our expectations, there was no interaction (P > 0.80) between dietary protein concentration and AA supplementation. When N retention was expressed as a percentage of N intake, there was no effect (P > 0.30) of dietary protein concentration or source of AA.

Energy Metabolism.
Dietary treatment had no effect on GE intake. Although there was an interaction (P < 0.05) between the effect of protein concentration and type of diet, energy excretion in feces was reduced as dietary protein was reduced (P < 0.05). As a consequence, the apparent digestibility of energy was affected by dietary protein concentration (linear, P < 0.01; quadratic, P < 0.05). The amount of energy excreted in urine was small and not influenced (P > 0.50) by dietary treatment.

Despite differences in energy digestibility, there were no differences (P > 0.80) in ME when expressed in terms of megacalories per day. However, when ME was expressed as a percentage of GE intake, there was a small increase (P < 0.05) as dietary protein was reduced.

Exp. 2
Growth Performance.
Average daily gain (Table 6) was highest in pigs fed diets that contained 13 and 14% CP, and decreased dramatically as the protein concentration decreased from 12 to 11% (linear, P < 0.05; quadratic, P < 0.01; cubic, P < 0.05). There was a similar response in ADFI, which also was highest in pigs fed diets that contained 13 and 14% CP and lowest in pigs fed the 11% CP diet (quadratic, P < 0.01). Averaged across the six dietary treatments, ADFI was approximately 5% of BW. Feed efficiency changed little as protein content was decreased from 16 to 12%, but was much lower in pigs fed the 11% CP diet (linear, P < 0.01; quadratic, P < 0.01; cubic, P < 0.01). For both ADG and G/F, individual t-tests revealed that only pigs fed the 11% CP diet had values that were different (P < 0.05) from those of pigs fed the 16% CP control diet.

Carcass Traits.
Although there was no effect (P > 0.10) on backfat thickness, gilts fed 15, 14, 13, or 12% CP diets had somewhat greater backfat thickness than gilts fed 11 and 16% CP diets. Longissimus muscle area decreased as dietary protein concentration decreased (linear, P < 0.01; quadratic, P < 0.05; cubic, P < 0.05). Gilts fed the 11% CP diet had lower longissimus muscle areas than gilts fed all other diets.

Plasma Urea and Amino Acid Concentrations.
Plasma urea concentrations on both d 14 and 35 decreased linearly (P < 0.01) as the protein concentration of the diet was reduced (Table 7). For all dietary treatments, plasma urea concentrations were higher on d 35 than on d 14.

Less consistent effects were observed on plasma concentrations of nonessential AA. Plasma alanine (linear, P < 0.01; quadratic, P < 0.05), glutamic acid (linear, P < 0.05), glycine (linear, P < 0.01; quadratic, P < 0.05), and serine (linear, P < 0.05) concentrations increased, whereas plasma aspartic acid (quadratic, P < 0.05), citrulline (linear, P < 0.01; quadratic, P < 0.05), and ornithine (linear, P < 0.01) concentrations decreased as protein decreased in the diets. Plasma glutamine concentrations were not affected (P > 0.30) by the dietary protein concentration.

	Discussion

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Nitrogen Balance
The results of the N balance experiment were unexpected and not consistent with our initial hypothesis. We had anticipated that reducing the dietary protein content from 18 to 14% plus AA would have little or no effect on N retention, because the 18% CP diet would have provided excess amounts of all the essential AA. On the other hand, when the initial diet was barely adequate (16% CP) or deficient (14% CP), we expected that a four percentage unit reduction in dietary protein content might reduce N retention. However, we observed that N retention was reduced by the same amount (approximately 5.4 g/d) regardless of whether the initial protein concentration was 18, 16, or 14%.

Our results indicate that N retained/N intake ranged from 58 to 62%, and did not differ among diets. Consequently, the amount of N retained was directly related to the amount of N consumed, which was much higher for the standard diets. We had anticipated that low-protein, AA-supplemented diets would result in higher apparent biological value than standard diets and this would compensate for the lower N intake. Although values were numerically higher for the AA-supplemented diets, differences were not large enough to offset the decreases in the amounts of N absorbed.

Low-protein, AA-supplemented diets did reduce the amounts of N excreted in manure (feces plus urine). These reductions ranged from 21% when the reduction was from 18 to 14% CP to 30% when the reduction was from 14 to 10% CP. These estimates are similar to, but somewhat lower than, the estimate of 8% for each one percentage unit reduction in dietary protein calculated by Kerr and Easter (1995). Almost all of the reduction in manure N was due to reduction in urinary urea, because there were only small differences in fecal N excretion and no differences in urinary creatinine N or other N in urine.

A comparison of the N balance of gilts fed the 14% CP diet with that of gilts fed the 14% CP plus AA diet reveals some important points. Gilts fed these two diets ingested and absorbed similar amounts of N, and apparent biological values were similar. As a consequence, the amount of N retained was similar (20.99 vs 21.51 g/d). This suggests that the 14% CP diet was not limiting in lysine, tryptophan, threonine, and methionine. However, when the dietary protein percentage was increased from 14 to 16 to 18%, there was a large and progressive increase in N retention (20.99 to 24.53 to 27.10 g/d). Clearly the additional protein promoted N retention that the supplemental AA did not. This finding is difficult to explain unless an additional essential AA or a source of nonessential N was limiting. Although this possibility cannot be eliminated, it seems unlikely based on all the previous research and also the results of our second experiment.

Another possibility is that in short-term N balance studies, high-protein diets promote retention of N that is not protein accretion. This possibility is supported by the FFLG data, which were calculated from N retention using factors suggested in the NRC (1998) publication. The estimate of FFLG of gilts fed the 18% CP diet was 432 g/d, which is much higher than the 350 g/d assumed by NRC (1998) for "pigs with high lean growth rates." The estimate also is much greater than the estimates of approximately 300 g/d calculated in our growth experiment. Although it is well known that balance experiments overestimate nutrient retention relative to growth and comparative slaughter experiments, perhaps by as much as 20% (Rao and McCracken, 1990), this does not explain the large differences among treatments. Similar findings have been reported by others. Russell et al. (1983) found that AA supplementation of a 12% CP diet resulted in ADG equal to that produced by a 16% diet. However, N retention was 14% lower in pigs fed the 12% CP diet. In a comparative slaughter experiment, Noblet et al. (1987) found that lysine supplementation of a low-protein diet resulted in ADG equal to a higher protein diet, but N retention was 6% lower. It seems that short-term N balance experiments may not provide a satisfactory measure to compare standard diets with low-protein, AA-supplemented diets.

Growth and Carcass Traits
In contrast to N retention in Exp. 1, growth traits (including estimated FFLG) in Exp. 2 were maintained when the dietary protein was reduced from 16 to 12%. This confirms work by others who have shown that supplementation with combinations of lysine, tryptophan, threonine, and methionine enable reductions of four percentage units of protein with no reductions in ADG and G/F (Lopez et al., 1994; Kerr and Easter, 1995; Kerr et al., 1995).

Growth traits decreased precipitously when dietary protein was reduced from 12 to 11%. Analysis of the 11% CP diet revealed that the actual protein content was 10% (Table 4), and this probably explains why the decrease was so large. Nevertheless, it is clear that the 11% CP diet was limiting in nutrient(s), probably essential AA, that were not limiting in the other diets.

Although differences were not statistically significant, there was a tendency for backfat to increase as dietary protein was reduced from 16 to 12%. Longissimus muscle area decreased as dietary protein decreased from 16 to 15%, but there was little difference between the 15 and 12% CP diets. These types of changes have been an almost universal observation in experiments of this type (Page et al., 1993; Smith et al., 1999; Gómez et al., 2002b). Pigs fed the 11% CP diet had less backfat and smaller longissimus muscle areas than pigs fed other diets, undoubtedly because they weighed much less at the end of the experiment.

Plasma Urea and Amino Acid Concentrations
To determine whether other AA may become limiting in low-protein diets, plasma concentrations of urea and AA were analyzed. Urea concentrations decreased as dietary protein concentration decreased, indicating more efficient utilization of N, but there was no clear breakpoint, even between the 12 and 11% CP diets. Plasma urea concentrations increased as the experiment progressed (i.e., between d 14 and 35). We have noted similar increases in blood urea concentration in previous experiments (Chen et al., 1999; Gómez et al., 2000).

We had anticipated that the concentration of AA that were supplemented in the diets (lysine, tryptophan, threonine, and methionine) would increase in blood plasma as the dietary protein content declined. This was because diets were formulated to have equal amounts of these AA on a total basis. Crystalline AA are assumed to be more bioavailable than the AA in corn and soybean meal. Thus, the available content of lysine, tryptophan, threonine, and methionine would have increased as the dietary protein content was decreased. Although there was some variation, concentrations of lysine, threonine, and methionine did increase as dietary protein content decreased. Tryptophan concentrations were unchanged. These results suggest that these four AA were not limiting in these diets, particularly not in the 11% CP diet.

Concentrations of all other essential AA (valine, isoleucine, leucine, histidine, phenylalanine, tyrosine, and arginine) decreased as dietary protein content decreased, reflecting the lower dietary content of these AA. Decreases for some AA were much greater than for others. In particular, concentrations of isoleucine and valine decreased 76 and 75%, respectively, whereas all other essential AA decreased by 60%. Furthermore, large decreases for these two AA occurred between the 12 and 11% CP diets (45% for isoleucine and 37% for valine). These findings indicate that isoleucine and/or valine may have become limiting in the 11% CP diet. This conclusion is consistent with the results of Russell et al. (1987), who reported that pig performance was improved when both isoleucine and valine were added to an 11% CP diet.

	Implications

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Although with adequate amino acid supplementation it is possible to reduce the protein content of growing pigs’ diets by four percentage units with no reduction in weight gain and feed efficiency, there is a reduction in carcass leanness. Nitrogen balance is greater in pigs fed standard diets than in pigs fed corresponding low-protein, amino acid-supplemented diets, but the reasons for this are unclear. When the protein content is reduced by more than four percentage units, isoleucine and/or valine may become limiting.

	Footnotes

 
¹ A contribution of the Univ. of Nebraska Agric. Res. Div., Lincoln 68583-0704. Journal Series No. 13522.

² Present address: Colegio de Postgraduados en Ciencias Agrícolas, Montecillo, Texcoco, Edo. de México, 56230, México.

⁴ Present address: CENIFMA-INIFAP, Apdo. Postal 2-29, Querétaro, México.

Received for publication October 18, 2001. Accepted for publication July 2, 2002.

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