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J. Anim Sci. 2006. 84:3329-3336. doi:10.2527/jas.2006-048
© 2006 American Society of Animal Science
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ANIMAL NUTRITION

Effects of feed restriction and subsequent refeeding on energy utilization in growing pigs

P. A. Lovatto*,1, D. Sauvant{dagger}, J. Noblet{ddagger}, S. Dubois{ddagger} and J. van Milgen{ddagger}

* Universidade Federal de Santa Maria, Departamento de Zootecnia, Santa Maria, RS 97105-900, Brazil; and {dagger} INRA-INAPG UMR Physiologie de la Nutrition et Alimentation, 16, rue Claude Bernard, 75231 Paris CEDEX 05, France; and and {ddagger} Institut National de la Recherche Agronomique, UMR SENAH, 35590 Saint Gilles, France


   Abstract
Top
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
An experiment was carried out to evaluate the metabolic utilization of energy in crossbred barrows during feed restriction and subsequent refeeding. Ten pigs, initially weighing 52 kg, were used in 5 blocks of 2 littermates each. A 7-d adaptation period (P1) was used in which pigs were offered feed at 2.60 MJ of ME·kg of BW–0.60·d–1. This adaptation period was followed by a 7-d period (P2), in which 1 pig of each block continued to receive feed at the same level of feeding, whereas for its littermate a 40% reduction in feed intake was imposed (i.e., 1.55 MJ of ME·kg of BW–0.60·d–1). During the subsequent 7-d period (P3), both pigs were offered feed at 2.60 MJ of ME·kg of BW–0.60·d–1. After P3, pigs were fasted for 1 d. Heat production (HP) was measured for all pigs during the last 3 d of P1 and on all days for P2 and P3. Heat production was measured using an open-circuit respiration chamber. Energy and N balances were determined for P1, P2, and P3. The HP was partitioned into HP due to physical activity, the short-term thermic effect of feeding, and resting HP. Feed restriction during P2 decreased (P < 0.01) total HP, resting HP, short-term thermic effect of feeding, and retained energy, whereas HP due to physical activity was not affected by feed restriction (P = 0.50). Likewise, fecal and urinary N loss, protein gain, lipid gain, and ADG were reduced during feed restriction (P < 0.01). There were no differences in components of HP and metabolic utilization of energy between the 2 groups during P1 and P3. Nevertheless, urinary N loss was decreased (P < 0.05) and ADG increased (P < 0.01) during P3 for pigs that were restricted in P2. Compensatory growth after a period of feed restriction does not seem to be related to a change in the metabolic utilization of energy for gain but more likely is due to gain in water and gut contents.

Key Words: compensatory growth • feed restriction • heat production • pig


   INTRODUCTION
Top
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Periods of feed restriction in growing pigs can occur as part of farm strategy or as a result of external factors. For instance, imposed feed restrictions may be due to economic reasons or to prevent excessive lipid deposition during the finishing period. On the other hand, the animal may voluntarily restrict its feed intake through physiological controls, such as during heat stress (Collin et al., 2001Go) or disease (Laevens et al., 1999Go). In both instances of feed restriction, the pig adjusts its metabolism to maintain homeostasis. This adjustment primarily occurs by reducing the mass of organs that have a high turnover rate (e.g., viscera; Hornick et al., 2000Go) thereby reducing the energy expenditure. During feed restriction, a greater fraction of retained energy (RE) is retained as protein (rather than lipid) resulting in leaner pigs.

After periods of feed restriction, pigs may show an increased growth rate, often referred to as compensatory growth (Chiba et al., 1999Go; Whang et al., 2003Go; Chwalibog et al., 2004Go). Factors of compensatory growth that have been studied include nutrient supply (protein and energy), diet type, and duration of the refeeding period. Compensatory growth may be due to increased feed intake during refeeding (compensatory feed intake), increased efficiency of nutrient utilization, or to a change in partitioning of energy gain between protein and fat.

The aim of the present experiment was to test the hypothesis that, after a short period of severe feed restriction, growing pigs utilize nutrients and energy more efficiently than nonrestricted control pigs when given the same quantity of feed.


   MATERIALS AND METHODS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Animals and Diets
An authorization to experiment on living animals was issued by the French Ministry of Agriculture to J. van Milgen and J. Noblet. All pigs originated from the INRA herd in Saint-Gilles, France. Five blocks of 2 Piétrain x (Large White x Landrace) littermate barrows, with an initial mean BW of 52 kg, were used. During the study, pigs were housed individually in metabolic crates located in a temperature-controlled room (23 ± 1°C). All pigs were offered the same diet (Table 1Go) formulated to contain 0.79% of digestible Lys.


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  		Table 1. Composition of experimental diet, as-fed basis
 
Experimental Design
Ten days before the experiment started, the pigs were adapted to the diet, feed intake, and metabolic cages. Feeding level progressively increased to reach 2.60 MJ of ME·kg of BW–0.60·d–1 after 6 d of adaptation. The experiment consisted of 3 successive periods. Period 1 (P1) was the initial 7-d adaptation. In P1, all pigs were offered feed at the same feeding level (2.60 MJ of ME·kg of BW–0.60·d–1). Period 2 (P2) was the second 7-d period, during which the feed restriction was imposed to 1 pig in each block. In P2, 1 pig in each block (referred to as normal feeding, NF) continued to receive feed at the same feeding level as in P1, whereas the other pig in the block (referred to a restricted feeding, RF) was offered feed at a level of 1.55 MJ of ME·kg of BW–0.60·d–1. Period 3 (P3) was the last 7-d, or refeeding, period, during which the same amount of feed (2.60 MJ of ME·kg of BW–0.60·d–1) was offered to both pigs in each block. After these 3 periods, feed was withheld from the pigs for 1 d (P4) to measure fasting heat production (HP). Pigs were held in respiration chambers during the last 3 d of P1 and during the entire time for P2, P3, and P4.

During P2, RF pigs were expected to have not only a lower growth rate but also a lower gut fill. Pigs within a block were pair-fed during P1 and P3. Consequently, RF pigs received slightly more feed (expressed as MJ of ME·kg of BW–0.60·d–1) during P3 than NF pigs because of their lower BW after the feed restriction. Feed was offered in 4 equal meals at 0900, 1300, 1700, and 2100. The quantity of feed distributed was adjusted twice weekly based on the anticipated BW gain.

Two open-circuit respiration chambers, based on a design described by Noblet et al. (2001)Go, were used to measure HP. The volume of each chamber was approximately 12 m3. Temperature was maintained at 24 ± 0.1°C, and relative humidity was maintained at 70%. Artificial light was used between 0815 and 2115. Each chamber contained an individual metabolic cage, which was placed on 4 force sensors that produced an electric signal proportional to the physical activity of the pig. The weight of the trough was measured continuously by a load cell, and periods of instability were assumed to correspond to feed consumption (Noblet et al., 2001Go).

Measurements
Pigs were weighed at the beginning of P1, P2, P3, and at the beginning and end of the fasting period. Feed spillage was collected daily and analyzed for DM content. Feces were collected daily, stored at 2°C, and pooled over successive days, and at the end of each period were weighed, mixed, subsampled, and freeze-dried for chemical analysis. Total excreted urine was collected daily in a H2SO4 solution (30 mL of a 10% H2SO4 solution per liter of anticipated urine excretion) and weighed. To avoid handling and sampling large quantities of urine at the end of each period, a 5% sample of the daily urine production was taken and pooled by animal. To evaluate the change in N retention during feed restriction and refeeding, a daily urine sample (100 mL) was taken during P2 and P3. Nitrogen losses as ammonia in condensed water and outgoing air were measured according to the methods described by Noblet et al. (1987)Go.

During the periods in the respiration chamber, gas concentrations (CO2, O2, and CH4) of outgoing air and ventilation were continuously measured as described by van Milgen et al. (1997)Go. The O2 concentration was measured by a paramagnetic differential analyzer (Oxygor 6N, Maihak AG, Hamburg, Germany), whereas CO2 and CH4 were measured by infrared analyzers (Unor 6N, Maihak AG, Hamburg, Germany). As only 1 CH4 analyzer was available, an alternating scheme of 3 or 4 d of measurement was used for pigs in a block and per period. Gas extraction was measured by a mass gas flow meter (Hasting, HFM 2000B, Hampton, VA). Gas concentrations, signals of the force sensors, trough weight, and physical conditions in the chamber (i.e., temperature, humidity, and barometric pressure) were measured 60 times per second, averaged over 10 s intervals, and recorded for further calculations.

Chemical Analyses
Representative samples of feed and feces (1 sample per period) were analyzed for DM, ash, and N according to the AOAC (1990)Go. The GE content was measured using an adiabatic bomb calorimeter (IKA, C5000, Staufen, Germany). Samples of urine, condensed water, and extracted air were analyzed for N using fresh material. The energy content of urine was obtained after freeze-drying of approximately 50 mL of urine in polyethylene bags.

Calculations
Nitrogen retention of each pig was calculated as the difference between N intake and N losses in feces, urine, and gas. The DE and ME values of the diet were calculated according to methods described by Noblet et al. (1987)Go. For the ME calculation, the average CH4 production was applied to all pigs.

Heat production was calculated based on gas exchanges (indirect calorimetry) according to the formula of Brouwer (1995)Go, including methane production and urinary N excretion. Retained energy was calculated as the difference between ME intake and HP over the measurement period. Retained energy as protein was calculated from the N balance, and energy retained as lipids was calculated as the difference between RE and energy retained as protein (Noblet et al., 1987Go).

Simultaneous measurements of O2 and CO2 concentrations, physical activity (i.e., the signal of force sensors), and eating events (i.e., the signal of the load cells) in the respiration chamber, and physical characteristics of gas in the chamber were used as inputs to calculate the components of HP using a compartmental model of an animal in a respiration chamber (van Milgen et al., 1997Go; van Milgen and Noblet, 2000Go). The idea behind this model is to relate the dynamics of O2 and CO2 concentrations in the chamber to events in the respiration chamber. In practice, on days when the pigs are fed, the model provides estimates of gas exchanges due to resting (L/h), physical activity (L/unit of force), and feed intake (L/g). During fasting, it provides estimates of gas exchanges due to fasting (L/h) and physical activity during fasting.

Variable estimates for gas exchange components were obtained using ACSL/Optimize (AEgis Simulation Inc., 1999Go). Components of total HP were calculated from the respective estimated O2 consumption and CO2 production (Brouwer, 1995Go), excluding the correction for urinary N and methane production. On days when the pigs were fed, HP was considered as the sum of resting HP, the short-term thermal effect of feeding (TEFst), and HP due to physical activity. The respiratory quotient was calculated as the ratio between CO2 production and O2 consumption. Data related to the energy balance were expressed relative to BW raised to the power of 0.60 (Noblet et al., 1999). For these calculations, the average BW within a period was used. The fasting HP was expressed relative to the BW of the morning before the fasting period.

Statistical Analyses
The data were subjected to ANOVA using the GLM procedure (SAS Inst. Inc., Cary, NC). The dietary treatment, period, their interaction, and block (replication) were included in the model. When the interaction between the treatment and period was significant, the effect of dietary treatments within a period was assessed by comparing the least squares means using a t-test. For P1, no difference between treatments was anticipated. During P2, the reduced energy intake in the restricted animals would be anticipated to affect energy deposition and, perhaps, the efficiency of energy utilization. Consequently, it was anticipated that the interaction between treatment and period would be significant because of a treatment effect during P2 and perhaps during P3.


   RESULTS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Performance data during P1 through P3 are presented in Table 2Go. As anticipated, during P1 weight gain was similar for both groups of pigs. During P2, feed restriction resulted in a 70% reduction of daily weight gain compared with NF pigs (0.33 vs. 1.07 kg·d–1; P < 0.01). During the refeeding period (P3), daily weight gain was 41% higher in RF pigs than in NF pigs (1.45 vs. 1.03 kg·d–1; P < 0.01). Despite the increased weight gain in RF pigs during P3, the body weight at the end of the refeeding period remained lower compared with NF pigs (71.4 vs. 74.0 kg; P < 0.01).


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  		Table 2. Performance and N balance of growing pigs during feed restriction and refeeding1
 
Nitrogen balances during P1, P2, and P3 are shown in Table 2Go. During P1, no significant differences were observed for fecal and urinary N losses between the 2 groups. The 40% reduction in N intake during P2 for RF pigs resulted in a 32% reduction in fecal N losses and a 40% reduction in urinary N losses. Retained N was 43% lower in RF pigs compared with NF pigs (17.2 vs. 30.3 g·d–1; P < 0.01). No differences were observed in fecal N digestibility in P2 (85.4% in RF and 86.8% in NF pigs). During P3, urinary N losses were 15% lower in RF pigs compared with NF pigs (20.1 vs. 23.6 g·d–1; P < 0.05). The day-to-day pattern of urinary N loss is illustrated in Figure 1Go. Statistical difference between both treatments was apparent only during the last 2 d of P2 and first 2 d of P3. No difference was observed in fecal N digestibility in P3 (85.0% in RF and 86.2% in NF pigs).


Figure 1
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  		Figure 1. Daily urinary N loss in growing pigs fed normal ({square}) or restricted ({blacksquare}) diets during P2 and fed normally during P3. Each point represents the average of 5 pigs. *Indicates a difference between treatments (P < 0.01).

 
Energy utilization during the 3 main periods is shown in Table 3Go. During P1, no differences were observed in energy utilization between RF and NF pigs. During P2, the 40% reduction in feed intake for RF pigs resulted in a 20% reduction in HP (1.16 vs. 1.45 MJ·kg of BW–0.60·d–1; P < 0.01). This reduction was mainly due to a 48% reduction in TEFst (0.14 vs. 0.27 MJ·kg of BW–0.60·d–1; P < 0.01) and a 15% reduction in resting HP (0.84 vs. 0.99 MJ·kg of BW–0.60·d–1; P < 0.01). During the restriction period, no differences were observed in HP due to physical activity. The RE was reduced (P < 0.01) by 63% during feed restriction. The reduction in RE was greater for lipid (73% reduction; P < 0.01) than for protein (42% reduction; P < 0.01). No differences were observed in energy digestibility during feed restriction (88.6% in RF and 88.8% in NF pigs). During the refeeding period, no differences were observed in HP and its components. Although small differences existed, some of these are due to the mode of expressing the results (e.g., the difference in ME intake during P3 is due to the pair-feeding of pigs that have different weights following P2). During the refeeding period, restricted pigs in P2 period retained more (P < 0.01) energy (total, as protein, and as fat). No differences were observed in energy digestibility during P3 (88.4% in RF and 88.6% in NF pigs). The fasting HP (measured after 7 d of refeeding) was not different between 2 groups.


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  		Table 3. Utilization of energy during feed restriction and refeeding in growing pigs
 

   DISCUSSION
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
IMPLICATIONS
 LITERATURE CITED
 
Effects During Feed Restriction
The decrease in growth rate as a consequence of feed restriction observed in this study has been previously demonstrated (Prince et al., 1983Go; Stamataris et al., 1991Go; Fabian et al., 2002Go). Feed restriction reduces nutrient availability for production (growth) and modifies the metabolic utilization of energy. This changes the lipid to protein deposition ratio and body composition (Prince et al., 1983Go; Pond and Mersmann, 1990Go; van Milgen et al., 2000Go). The energy partitioning between lipid and protein deposition was 68/32 for both groups during P1. During feed restriction, both lipid and protein deposition were reduced, but lipid deposition was affected more than protein deposition. During feed restriction, 50% of RE was retained as lipid and 50% was retained as protein. This change in energy partitioning as a function of energy intake is consistent with previous observations in our laboratory (Quiniou et al., 1996Go). Differences in energy partitioning are also partly reflected in changes in BW. A reduction in feed intake does not necessarily lead to a proportional reduction in growth rate (de Greef et al., 1992Go). The effect of feed restriction on weight gain is mediated through 2 opposing mechanisms. During feed restriction, a greater part of ME will be used for maintenance. At the same time, a greater fraction of RE will be retained as protein. Due to the association of water with protein, the reduction in BW gain may be less than proportional when the feed intake reduction is small. However, for a strong reduction in feed intake (as in this experiment), the reduction in ADG is greater than the reduction in feed intake due to the increased relative importance of maintenance.

It has been shown that a reduction in feed intake reduces the size of metabolic active organs (Koong et al., 1982Go; Campbell and Dunkin, 1983Go; Koong and Ferrell, 1990Go). The current study could not provide direct evidence of reduced metabolic activity. The lower energy expenditure was partly due to a reduced thermic effect of feeding, whereas the ratio of TEFst/ME was numerically 10% lower during feed restriction. As indicated earlier, during feed restriction, relatively more protein is deposited. This, combined with the knowledge that protein deposition is energetically less efficient than lipid deposition, would lead to the hypothesis that pigs should be energetically less efficient during feed restriction. However, the energetic efficiency (i.e., 1 – TEFst/ME) was increased, rather than decreased, during the feed restriction. A reduction in protein turnover (and thus a reduction in energy expenditure) seems to be the most plausible reason for this observation. The reduced urinary N loss during feed restriction may also suggest a decrease in protein turnover. This study did not confirm that feed restriction increases nutrient digestibility, as suggested by Wenk et al. (1980)Go. Similarly, feed restriction did not result in a reduced physical activity, although the small number of observations and the specific housing conditions make it difficult to generalize this result.

Effects During the Refeeding
The compensatory gain of pigs during a refeeding period depends on the severity and time of restriction (Lister and McCance, 1967Go; Mersmann, 1986Go), feed quality and feeding strategy (Pond and Mersmann, 1990Go), and length of refeeding period. In this experiment, the restriction period and the refeeding period were relatively short (7 d). The RF pigs did not reach the BW of NF pigs at the end of refeeding period, during which pair-feeding was used. The controlled feed intake and short refeeding period may have limited the potential of compensatory gain (Kyriazakis and Emmans, 1991Go; Kyriazakis et al., 1991Go).

The changes in energy partitioning during the refeeding period may partially explain the decrease in HP (Muller and Kirchgessner, 1984Go). In this study, daily HP in previously restricted pigs was 13.5, 3.7, and 1.5% lower during d 1, 2, and 3 of refeeding. These differences may be associated with a reduced thermic effect of feeding (van Milgen et al., 1998Go; van Milgen and Noblet, 2000Go; Lovatto et al., 2002Go). Nevertheless, it seems that following a period of feed restriction, pigs benefit very little (and for a very short period of time) from an increased energetic efficiency when offered the same quantity of feed during refeeding. Three days after refeeding, the HP was virtually the same for both groups. Chwalibog et al. (2004)Go observed that same phenomenon after a 4-d fasting. The observation that the fasting HP (measured after P3) was not different between both treatments is consistent with the idea that the metabolic adaptation occurs rapidly. In conclusion, there is no strong evidence that compensatory gain is due to increased energetic efficiency.

There is nevertheless a contradiction between performance and metabolic results of restricted pigs. During refeeding, BW gain measured in restricted pigs was 41% higher than normally fed pigs (1.45 vs. 1.03 kg/d, respectively). The difference in lipid and protein gain between the 2 treatments corresponds to about 126 g/d of gain. The difference between BW gain and tissue gain, as calculated from balance trials, is probably due to differences in gut fill after P2. Consequently, this may bias not only the compensatory growth observed in P3 but also the reduced growth during P2 for the restricted pigs. In addition to differences in gut fill, BW gain differences may be related to the recovery of the mass of digestive organs, as shown in pigs (Critser et al., 1995Go; Bikker et al., 1996aGo) and sheep (Kabbali et al., 1992Go). Body weight gain could be associated with water gain in digestive organs, which is not considered in balance trials, because the water content in digestive organs is higher than in the carcass.

In this experiment, the increased growth rate seemed to occur mainly at beginning of the refeeding period, as shown previously (Owen et al., 1971Go; Bikker et al., 1996bGo). During the same period, the energy requirements for additional BW gain may be relatively low, because this gain is mainly in protein and water (de Greef et al., 1992Go; Chiba, 1994Go; Bikker et al., 1996bGo).

During the refeeding period, no conclusive evidence for compensatory growth was found. Although in general, no effect was observed for the full 7-d refeeding period, urinary N excretion and HP were lower for the first 2 to 3 d of refeeding following the feed restriction. Chwalibog et al. (2004)Go also observed that, after a 4-d fasting period, it required 3 d to reach a urinary N excretion level similar to that observed before fasting. The response of urinary N excretion may be due partly to a mechanical delay. Urine was collected once daily and thus reflected N metabolism of the preceding day(s).


   IMPLICATIONS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
LITERATURE CITED
 
Compensatory growth after a short period of feed restriction is not related to an improved metabolic utilization of energy. After a period of feed restriction and when pair-fed, compensatory weight gain is mostly likely due to water gain or gut fill or both. In general, it seems more likely that the basis of compensatory growth is compensatory feed intake than an improved efficiency of nutrient utilization.

1 Corresponding author: lovatto{at}smail.ufsm.br

Received for publication January 25, 2006. Accepted for publication July 19, 2006.


   LITERATURE CITED
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 


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