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Compensatory growth and nitrogen balance in grower-finisher pigs¹

Department of Animal Sciences, Auburn University, AL 36849-5415

	Abstract

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Sixteen castrated male pigs (averaging 21.2 ± 4.9 kg) were used in two trials to investigate the effect of dietary amino acid content during the grower phase on growth performance and N balance. In each trial, pigs were assigned randomly to corn-soybean meal grower diets formulated to contain 5.0 or 11.0 g lysine/kg (as-fed basis). Common Finisher 1 and 2 diets were offered when pigs reached 51.2 ± 3.3 and 79.5 ± 3.4 kg, respectively. Pigs were placed in metabolism crates for a 9-d period during each of the grower, Finisher 1, and Finisher 2 phases when they weighed 43.3 ± 3.9, 70.4 ± 4.9, and 90.5 ± 3.8 kg, respectively, to determine N balance. Blood samples were taken from each pig periodically after an overnight fast. Pigs were allowed ad libitum access to feed and water, except during the three adaptation/collection periods. There were no diet x trial interactions; thus, the data were combined. Pigs fed the low-amino acid grower diet grew more slowly and less efficiently (P < 0.001) during the grower phase and had more ultrasound backfat (P = 0.010) at the end of the grower phase than those fed the high-amino acid grower diet. During the Finisher 1 phase, however, pigs fed the low-amino acid diet grew more efficiently (P = 0.012) than those fed the high-amino acid diet, and the grower diet had no effect on overall weight gain, carcass traits, lean accretion, or meat quality scores. Although pigs fed the low-amino acid diet had less serum urea N (P < 0.001) and more glucose (P = 0.009) at 43.3 kg, there seemed to be no clear, long-term effect of the grower diet on serum metabolites. During the grower phase, pigs fed the high-amino acid diet consumed more N (P < 0.001), had higher apparent N digestibility (P = 0.041), N utilization (P = 0.027), and N retention (P < 0.001), and excreted more fecal (P = 0.034) and urinary (P < 0.001) N than those fed the low-amino acid diet. Pigs fed the low-amino acid grower diet, however, had a higher N utilization (P = 0.024) during the Finisher 1 phase, and excreted less urinary N during both the Finisher 1 (P = 0.029) and 2 (P = 0.027) phases than those fed the high-amino acid grower diet. These results indicate that pigs subjected to early dietary amino acid restrictions compensated completely and decreased N excretion during both the restriction and realimentation phases. Compensatory growth can, therefore, have a positive effect not only on the overall efficiency of pig production but also on environment.

Key Words: Compensatory Growth • Dietary Restrictions • Nitrogen Balance • Pigs

	Introduction

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The management of wastes and odors has become a major issue facing the pig industry (Chiba, 2000). For a sustainable pig industry, it is necessary to alleviate public concerns about the environmental issues. Likewise, improving the efficiency of nutrient utilization is equally important for successful pig production, and this is especially true for protein sources because of the cost (Chiba, 2001) and the fact that the average retention of dietary N in pigs has been reported to be much less than 50% (Kornegay and Verstegen, 2001). Efficient nutrient utilization can, therefore, have a positive effect not only on the efficiency and success of pig production but also on the environment by reducing excretion of unused nutrients.

The main goal of the commercial pig production is to maximize profits, which does not necessarily imply maximal animal performance (Chiba, 2000). Compensatory growth responses after dietary restrictions in grower pigs have been reported (Chiba, 1994, 1995; Fabian et al., 2002). Zimmerman and Khajarern (1973) suggested that compensatory growth response may reflect a change in metabolism, and their contention was supported by findings of other researchers (Prince et al., 1983; Valaja et al., 1992; Chiba et al., 2002). If pigs have the ability to grow faster and/or more efficiently in the subsequent phase after a period of dietary restrictions, it can reduce feed costs and also excretion of unused nutrients during both the restriction and realimentation phases.

Compensatory N retention following the N deprivation in pigs has been demonstrated (Whittemore et al., 1978; Tullis et al., 1986), but a long-term effect of dietary restrictions on N balance in grower-finisher pigs has not been elucidated fully. The present study was conducted to investigate the effect of dietary amino acid restrictions during the grower phase on growth performance, serum metabolites, carcass and meat quality, and N balance in grower-finisher pigs.

	Experimental Procedures

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General.

A total of 16 crossbred (Yorkshire x Duroc) castrated male pigs averaging 21.2 ± 4.9 kg were used in two trials. Eight pigs used in the first trial averaged 17.4 ± 1.0 kg initially, whereas the average initial weight for eight pigs used in the second trial was 26.3 ± 2.5 kg. The number of pigs per treatment necessary to attain the desired precision was determined based on estimated CV of 7 to 8% for growth performance up to 14 to 16% for selected N balance data and expected treatment differences of 15 to 20% for growth performance up to more than 25 to 30% for selected N balance data ( = 0.05 and ß = 0.20; Cochran and Cox, 1957).

In each trial, pigs were housed in individual pens (4.4 m²) with solid concrete floors in an open-front building equipped with the water mister system. Pigs were randomly assigned to one of two grower diets, and, after the grower phase, they were offered common Finisher 1 and Finisher 2 diets. Pigs were allowed ad libitum access to feed and water throughout the study, except during the three adaptation/collection periods (or collection periods) to determine N balance. Pig weights and feed consumption data were collected weekly. In addition, pigs were weighed before and after each collection period. The study was initiated in early spring and terminated in midsummer. All pigs were slaughtered at the end of each trial. Before the first collection period, one pig from each treatment group in the second trial was removed from the study because of illness unrelated to the treatment. The protocol for animal care was approved by the Auburn University Institutional Animal Care and Use Committee.

Experimental Diets.

The purpose of using two grower diets (Table 1) differing in the lysine content (5.0 or 11.0 g lysine/kg, as-fed basis) was to create clear differences in growth performance and body composition during the grower phase. Corn and soybean meal were used as sources of amino acids and energy to formulate practical diets, and no effort was made to maintain a constant amino acid balance or DE content. The proportions of indispensable amino acids relative to lysine were, however, above the balanced protein (NRC, 1998), and the DE content was relatively similar (14.4 and 14.6 MJ/kg) for two grower diets. Common corn-soybean meal Finisher 1 and Finisher 2 diets (Table 1) were formulated to meet the total lysine requirements (NRC, 1998). Minerals and vitamins for all diets were provided in amounts calculated to meet or exceed the NRC (1998) requirements. The grower, Finisher 1, and Finisher 2 diets were fed from 21.2 ± 4.9 to 51.2 ± 3.3 kg, 51.2 ± 3.3 to 79.5 ± 3.4 kg, and 79.5 ± 3.4 to 107.5 ± 5.9 kg, respectively. Feed samples taken from every batch of feed were pooled, and subsamples were analyzed for DM and N (AOAC, 1990). During the collection period, feed samples were taken before feeding and pooled within each period, and subsamples were analyzed for DM and N.

For the total collection of feces and urine to determine N balance (Adeola, 2001), pigs were placed individually in stainless steel metabolism crates for a 9-d period during each of the grower, Finisher 1, and Finisher 2 phases when they weighed 43.3 ± 3.9, 70.4 ± 4.9, and 90.5 ± 3.8 kg, respectively. Adjustable metabolism crates (a maximum dimension, 56 x 122 cm) were located in an adjacent, open-front building identical to the unit where pigs were housed, and the building was equipped with the water mister system (away from crates) and fans. Average daily minimum and maximum temperatures in the building during the months of May, June, and July were 18.2 ± 2.3 and 29.2 ± 2.9°C, respectively. Pigs had a 3-d adjustment period before a 4-d total collection period (Adeola, 2001). Each day, pigs were fed twice (0800 and 1600) up to their appetite, but no more than 4% of their BW.

After each feeding, a feeder was cleaned and feed refusal was recorded, and fresh water was provided in the feeder until the next feeding. Orts were collected daily, dried and weighed, and feed intake was corrected for orts. Chromic oxide was used as an indigestible marker to signal the initiation and the termination of fecal collection. Feces were collected twice daily. Urine was collected continuously during the 4-d collection into a bottle, which was acidified daily with 25 mL of 6 N HCl. Urine volume was measured daily, filtered through glass wool, and a 5% aliquot was taken. All samples were stored at –20°C until the end of each collection period. Fecal and urine samples were thawed and mixed separately. Urine samples were filtered again through glass wool. Representative subsamples were taken and stored frozen at –20°C until analysis. Fecal samples were thawed and dried at 65°C before grinding with a Wiley mill through a 1-mm screen. The fecal and urine samples were analyzed for N (AOAC, 1990).

Ultrasound Measurements and Blood Samples.

All pigs were subjected to ultrasound backfat measurements at the end of the grower and Finisher 1 phases. Backfat thickness was measured 4 to 5 cm from the midline on the right side at the 10th rib using a real-time ultrasound instrument (SSD-500; Aloka Co. Ltd., Wallingford, CT). Blood samples were taken from each pig at the beginning; at the end of the grower, Finisher 1, and Finisher 2 phases; and before each of the three collection periods via vena cava puncture using a sterile needle and an evacuated tube after overnight fast (approximately 16 h). Serum was separated by centrifugation, and an aliquot was stored at –20°C until analyzed for urea N, glucose, and total protein (Sigma Diagnostics, St. Louis, MO), and triglycerides (Roche Diagnostics Systems Inc., Nutley, NJ).

Slaughter Procedures.

At an average weight of 107.5 ± 5.9 kg, all pigs were slaughtered at Auburn University Meat Laboratory using conventional procedures. The eviscerated carcass was split longitudinally through the vertebral midline, and warm carcass weight was recorded. After chilling for 24 h at 2°C, the LM of the right side was exposed by a perpendicular cut between the 10th and 11th ribs, and the LM area was traced using acetate paper. Backfat thickness at the 10th rib (about 3/4 distance along the LM toward the belly) was also measured. The exposed LM area was used to determine subjective meat quality scores (NPPC, 1991). The rate of carcass lean accretion was estimated by the equation reported by NPPC (1991):

where WCWT is warm carcass weight (kg), LMA is LM area (cm²), BF is 10th-rib backfat thickness (mm), IWT is initial weight (kg), and day is the number of days on study.

Statistical Analysis.

Data were subjected to an ANOVA using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). The effects of the grower diet, trial, and diet x trial interaction were included in the model for the growth performance, ultrasound backfat, periodic serum metabolite, carcass and meat quality, and nitrogen balance data. Animals and sampling periods were also included in the model for the overall serum metabolite data, and the effects of the grower diet, trial, and grower diet x trial interaction were tested using the animal effect as the error term. The initial and final weights were included in the model as covariates for the statistical analysis of the growth performance data, whereas the appropriate BW was used as a covariate for ultrasound, carcass, and N balance data. For the analysis of the N balance data during the Finisher 1 and Finisher 2 phases, the number of days from the end of the grower phase until collection was also included in the model as a covariate to account for the variation that was due to facility constraints. The initial serum values were used as covariates for the serum metabolite data. The results were considered significant if P 0.05.

	Results

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General.

There were no grower diet x trial interactions; thus, data from the two trials were combined. The analyzed CP (N x 6.25) content of the grower and finisher diets offered during the noncollection periods were generally similar to the intended values (Table 1). However, the analysis indicated that a batch of Finisher 2 diet fed to six pigs (three from each grower diet group) during the collection period may have been mixed incorrectly. The results, therefore, should be viewed with such oversight in mind, even though the equal number of pigs from each diet group were fed the batch of the diet in question only during the 3-d adaptation and 4-d collection period. In addition to the N balance data, feed intake, weight gain, and feed efficiency data are presented to provide some indication of growth performance during the collection periods.

Growth Performance and Ultrasound Backfat.

During the grower phase, pigs fed the diet containing 5.0 g lysine/kg grew more slowly and less efficiently (P < 0.001) and had more ultrasound backfat (P = 0.010) than those fed the diet containing 11.0 g lysine/kg (Table 2). During the Finisher 1 phase, however, pigs fed the low-amino acid grower diet grew more efficiently (P = 0.012) than those fed the high-amino acid diet. At the end of the Finisher 1 phase, pigs fed the low-amino acid grower diet had more ultrasound backfat (P = 0.033) compared with pigs fed the high-amino acid diet. The grower diet had no effect on growth performance during the Finisher 2 phase or weight gain during the grower-finisher phase.

Before the grower phase collection period (43.3 kg), pigs fed the low-amino acid grower diet had less serum urea N (P < 0.001) and more glucose (P = 0.009) than those fed the high-amino acid diet (Figure 1). At the end of the grower phase (51.2 kg), pigs fed the low-amino acid grower diet had less (P < 0.001) serum total protein than those fed the high-amino acid diet (Figure 2). There was no other effect of the grower diet on serum metabolites until pigs reached the slaughter weight. Pigs fed the high-amino acid grower diet had more serum glucose at 107.5 kg (P = 0.034).

View larger version (50K): [in this window] [in a new window]   Figure 1. Serum urea nitrogen and glucose concentrations in pigs offered the low-amino acid (5.0 g lysine/kg) or high-amino acid (11.0 g lysine/kg) diet during the grower phase (43.3 ± 3.9 and 51.2 ± 3.3 kg in this figure). Pigs were offered common diets during the Finisher 1 and 2 phases (70.4 ± 4.9 to 107.5 ± 5.9 kg in this figure). Least squares means were based on seven individually housed castrated males per treatment. The initial serum metabolite concentrations at 21.2 ± 4.9 kg were used as covariates. For urea N, P = 0.001 (***), 0.148, 0.746, 0.531, 0.901, and 0.802 at 43.3 ± 3.9 to 107.5 ± 5.9 kg, respectively; for glucose, P = 0.009 (**), 0.182, 0.582, 0.678, 0.817, and 0.034 (*) at 43.3 ± 3.9 to 107.5 ± 5.9 kg, respectively.

View larger version (44K): [in this window] [in a new window]   Figure 2. Serum triglyceride and total protein concentrations in pigs offered the low-amino acid (5.0 g lysine/kg) or high-amino acid (11.0 g lysine/kg) diet during the grower phase (43.3 ± 3.9 and 51.2 ± 3.3 kg in this figure). Pigs were offered common diets during the Finisher 1 and 2 phases (70.4 ± 4.9 to 107.5 ± 5.9 kg in this figure). Least squares means were based on seven individually housed castrated males per treatment. The initial serum metabolite concentrations at 21.2 ± 4.9 kg were used as covariates. For triglycerides, P = 0.053, 0.687, 0.249, 0.120, 0.463, and 0.649 at 43.3 ± 3.9 to 107.5 ± 5.9 kg, respectively; for total protein, P = 0.067, 0.001 (***), 0.246, 0.347, 0.974, and 0.079 at 43.3 ± 3.9 to 107.5 ± 5.9 kg, respectively.

There was no effect of the grower diet on carcass weight, length, 10th-rib backfat, LM area, or estimated rate of lean accretion (Table 3). Similarly, the lysine content of grower diets had no effect on subjective meat color, marbling, or firmness scores.

During the grower phase collection period, pigs fed the low-amino acid diet grew more slowly (P = 0.012) and utilized feed less efficiently for weight gain (P < 0.001) than those fed the high-amino acid diet (Table 4). Pigs fed the high-amino acid grower diet consumed more N (P < 0.001) and had a higher apparent N digestibility (P = 0.041), a higher net N utilization (P = 0.027), and a greater N retention (P < 0.001) than those fed the low-amino acid diet. Pigs fed the high-amino acid grower, however, excreted more fecal (P = 0.034) and urinary (P < 0.001) N than those fed the low-amino acid diet.

	Discussion

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During the Finisher 1 phase, previously restricted pigs utilized feed more efficiently for weight gain than those unrestricted pigs. Furthermore, there was no effect of the grower diet on overall weight gain because of the numeric reversal observed during the Finisher 1 phase. Therefore, pigs subjected to early amino acid restrictions in the present study exhibited compensatory growth in terms of growth performance during the realimentation phase. Similar compensatory responses have been observed previously (Chiba, 1994, 1995; Fabian et al., 2002).

There was a difference in ultrasound backfat at the end of grower phase between pigs fed the low- and high-amino acid diets, but the difference in body composition was not present in the subsequent phases as indicated by carcass data. The lysine content of the grower diet had no effect on carcass traits or lean accretion rate, which agrees with the findings of previous research (Chiba, 1994, 1995; Fabian et al., 2002). In addition, the grower diet had no effect on subjective meat quality scores in the present study. Along with the growth performance data, therefore, these results indicate that pigs subjected to dietary restrictions during the grower phase compensated completely in terms of growth performance and body composition by the time they reached market weight.

During the grower phase, serum urea N concentration was lower in pigs fed the low-amino acid diet than those fed the high-amino acid diet, which can be a reflection of simply a decrease in N intake (Eggum, 1970) and/or an increase in the efficiency of N (Berschauer et al., 1983) or lysine (Chiba et al., 1991) utilization. Alternatively, serum glucose was increased in pigs fed the low-amino acid grower diet. The high carbohydrate content of the low-amino acid diet and/or a decrease in insulin concentration associated with protein restriction (Atinmo et al., 1976b) may explain the results observed in the present study. Dietary amino acid restrictions resulted in decreased serum total protein concentration, which agrees with other reports (Atinmo et al., 1976c; Pond et al., 1980; Pond and Yen, 1984).

The concentrations of serum metabolites in pigs subjected to early dietary amino acid restrictions, however, returned to normal during the realimentation period, which agrees with other findings (Atinmo et al., 1976a; Pond et al., 1980). These results indicate that the early dietary restrictions did not have a long-term effect on serum metabolites. The effect of grower diet on serum glucose concentration observed at the end of the Finisher 2 phase was unexpected and cannot be explained because of the absence of any indication during the early- and mid-realimentation phase.

Ratcliffe and Fowler (1980) reported that compensatory growth response, which persisted for several weeks following severe dietary restrictions, was mainly due to an increase in feed intake relative to BW. Conversely, Zimmerman and Khajarern (1973) indicated that compensatory responses in growth performance are not due to an increased appetite, but rather reflect a change in metabolism. Their contention is supported by findings of other researchers (Prince et al., 1983; Valaja et al., 1992; Chiba et al., 2002), who reported that pigs subjected to a period of dietary restrictions utilized feed more efficiently during the realimentation phase than unrestricted pigs. As mentioned previously, pigs subjected to dietary restrictions utilized feed more efficiently for growth during the initial realimentation phase than those fed the high-amino acid diet. This and findings of other researchers indicate that early dietary restrictions can have a positive effect on metabolism of nutrients.

Several researchers reported that N digestibility (Cole et al., 1967; Fuller, 1983) or N retention (Quiniou et al., 1995; Canh et al., 1998; Heo et al., 2000) can be decreased by reducing dietary protein. On the other hand, Canh et al. (1998) observed a considerable decrease in urinary N excretion by reducing the dietary protein content, indicating that there might be an opportunity to decrease N excretion by feeding diets low in protein. In the present study, feeding the low-amino acid grower diet resulted in decreases in N digestibility, utilization, and retention during the grower phase. Pigs fed the low-amino acid grower diet, however, excreted 17% less N in the feces and 34% less N in the urine during the grower phase than those fed the high-amino acid grower diet.

There was some evidence of carryover effects of early dietary amino acid restrictions on the N metabolism during the realimentation phase. During the Finisher 1 phase, pigs fed the low-amino acid grower diet had a greater net N utilization and a numerically greater N retention (P = 0.081) and, consequently, decreased urinary N excretion by 28% compared with pigs fed the high-amino acid grower diet. Similarly, urinary N excretion in pigs fed the low-amino acid diet was reduced by 16% during the Finisher 2 phase. These results may indicate that pigs subjected to early dietary restrictions exhibited compensatory N retention. Whittemore et al. (1978) also reported that grower pigs exhibited compensatory N retention following a 12-d N deprivation, and Tullis et al. (1986) demonstrated that such enhanced N retention can be maintained for an extended period of time. It is possible that compensatory N retention is responsible for compensatory growth responses observed after a period of dietary restrictions in many studies.

The possible mechanisms involved in compensatory N retention are still not fully understood. The adaptation to a low-protein diet may involve a decrease in the rate of protein synthesis in most body tissues, with the most marked changes occurring in skin and intestine (Wykes et al., 1996). It has been reported that pigs fed a high-protein diet during the early phase of growth had a higher rate of protein turnover in the subsequent phase than pigs fed a low-protein diet (Vaughan et al., 1962), indicating a possible carryover effect of such alterations. Tullis et al. (1986) suggested that compensatory N retention following a period of N depletion in pigs may be related to the replenishment of labile N stores, such as N in viscera, skin, and plasma, but not in skeletal muscle tissues. Their contention can be supported by the report of Bikker et al. (1996), who indicated that compensatory protein retention occurred after a feed restriction during the grower phase, but only in the internal organs. Alternatively, there was no effect of the grower diet restrictions on carcass traits or lean accretion rate in the present study and many others (Chiba, 1994, 1995; Fabian et al., 2002), indicating a complete compensation in pigs subjected to early amino acid restrictions. Further research is needed to fully address the issue of early dietary restrictions and compensatory growth.

In summary, pigs subjected to dietary amino acid restrictions grew more slowly and less efficiently during the grower phase and had more ultrasound backfat at the end of grower phase compared with the unrestricted pigs. Those differences, however, seemed to disappear in the subsequent phases, indicating that the restricted pigs compensated completely in terms of growth rate and body composition by the time they reached market weight. Pigs fed the low-amino acid grower diet had decreased N excretion during the restriction phase, and they tended to retain more N in the subsequent phase, implying that compensatory growth responses in pigs subjected to a period of dietary restrictions may be associated with compensatory N retention during the realimentation phase. Because of compensatory N retention, N excretion in the subsequent phase was reduced by early dietary amino acid restrictions.

	Implications

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Pigs have the ability to achieve compensatory growth, and by taking advantages of this potential, feed costs and excretion of unutilized N during the restriction phase can be decreased. Furthermore, pigs subjected to early dietary restrictions can grow faster and more efficiently during the realimentation phase, thereby decreasing feed costs and excretion of unused N further because of compensatory N retention. Compensatory growth can, therefore, have a positive effect not only on the overall efficiency of pig production, but also on the environment.

	Footnotes

 
¹ The technical assistance of B. Anderson, B. Brown, M. Carroll, S. Dale, C. Dowdell, R. Johnson, C. M. Lin, and C. Morgan is gratefully acknowledged.

² Present address: Babolna Feed Ltd., P.O. Box 16, 2942 Nagyigmand, Hungary.

³ Correspondence: 303C Ann S. Upchurch Hall (phone: 334-844-1560; fax: 334-844-1519; e-mail: chibale{at}auburn.edu).

Received for publication July 11, 2003. Accepted for publication May 11, 2004.

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