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J. Anim. Sci. 2003. 81:416-422
© 2003 American Society of Animal Science

The effects of ractopamine on the behavior and physiology of finishing pigs1,2

J. N. Marchant-Forde*,{dagger},3, D. C. Lay, Jr.{dagger}, E. A. Pajor*, B. T. Richert* and A. P. Schinckel*

* Department of Animal Sciences and and {dagger} USDA, ARS, Livestock Behavior Research Unit, Purdue University, West Lafayette, IN 47907

3 Current address and correspondence:
USDA, ARS, Livestock Behavior Research Unit, 219 Poultry Science Bldg. (phone: 765-494-6358; fax: 765-496-1993; E-mail:
marchant{at}purdue.edu).


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The objectives of this study were to examine the effects of ractopamine (RAC) on the behavior and physiology of pigs during handling and transport. Twenty-four groups of three gilts were randomly assigned to one of two treatments 4 wk before slaughter: finishing feed plus RAC (10 ppm) or finishing feed alone. Pigs were housed in the same building in adjacent pens with fully slatted floors and ad libitum access to feed and water. Behavioral time budgets were determined in six pens per treatment over a single 24-h period during each week. Behavioral responses of these pigs to routine handling and weighing were determined at the start of the trial and at the end of each week. Heart-rate responses to unfamiliar human presence were measured in all pigs and blood samples were taken from a single pig in each pen on different days during wk 4. At the end of wk 4, all pigs were transported for 22 min to processing. Heart rate was recorded from at least one pig per pen during transport and a postmortem blood sample was taken from those pigs that were previously sampled. During wk 1 and 2, RAC pigs spent more time active (P < 0.05), more time alert (P < 0.05), and less time lying in lateral recumbency (P < 0.05). They also spent more time at the feeder in wk 1 (P < 0.05). At the start of the trial, there were no differences in behavioral responses to handling. However, over each of the next 4 wk, fewer RAC pigs exited the home pen voluntarily, they took longer to remove from the home pen, longer to handle into the weighing scale and needed more pats, slaps, and pushes from the handler to enter the scales. At the end of wk 4, RAC pigs had higher heart rates in the presence of an unfamiliar human (P < 0.05) and during transport (P < 0.05), but not during loading and unloading. Also at the end of wk 4, RAC pigs had higher circulating catecholamine concentrations (P < 0.05) than control pigs. Circulating cortisol concentrations and cortisol responses to transport did not differ between treatments. The results show that ractopamine affected behavior, heart rate, and catecholamine profile of finishing pigs and made them more difficult to handle and potentially more susceptible to handling and transport stress.

Key Words: Behavior • Catecholamines • Handling • Heart Rate • Pigs • Ractopamine


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The feed additive ractopamine (RAC), a ß-adrenergic agonist, acts as a repartitioning agent, promoting lean tissue deposition in sheep (Baker et al., 1984), cattle (Ricks et al., 1984), and pigs (Watkins et al., 1990). It has been widely researched over the last 20 yr and has been shown to give improvements in ADG, feed conversion efficiency, dressing percentage, and carcass lean content (Gu et al., 1991a,b). Its use may also confer environmental benefits (Sutton et al., 2001). It was approved for use in swine in the United States in 1999 (FDA, 2000) and subsequently in several other countries.

Production advantages of RAC are relatively brief. Performance measures peak and then decline with the greatest response occurring during the first 14 d (Williams et al., 1994). In recent studies, pigs fed a constant level of RAC had slower growth rates and poorer feed conversion efficiency than control pigs by wk 5 on tests (Schinckel et al., 2002a,b). At a cellular level, the change in response may be due to down-regulation of the ß-adrenergic receptors and RAC’s partial agonist activity (Liu et al., 1994; Mills, 2001). However, at a whole-animal level, and of concern in terms of well-being, the decrease in effectiveness may be partly due to the possible effects of RAC on mobility and behavior. These include increased gait problems and increased behavioral reactivity, especially in stressful situations. The behavioral research carried out so far has confirmed that after 6 wk of RAC, pigs spent more time lying and less time walking (Schaefer et al., 1992), but there was no evidence of decreased joint soundness (He et al., 1993), and there is no scientific evidence of behavioral or physiological responses to stress.

The objective of this study was to examine the behavior and physiology of pigs during the conventional RAC administration period and in response to stressors encountered during routine handling, weighing and transport.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Animals, Housing, and Husbandry

Animals were housed in accordance with FASS (1999) guidelines, and the project was approved by the Purdue Animal Care and Use Committee. A total of 72 gilts were used, offspring of Newsham XL terminal sires on Newsham US parent gilts. They were blocked by weight into two rows of 12 adjacent pens separated by a central corridor in the same wing of the Purdue University Swine Evaluation Unit. Each pen (1.8 x 3.0 m) housed three pigs and had fully-slatted floors—the rear two-thirds were concrete slats, the front one-third was plastic-coated expanded metal. A single partition-mounted drinker was situated toward the rear of the pen, and a single-space feeder was situated at the front of each pen. Both water and feed were available ad libitum. When the pigs had reached an average BW of 85.5 kg, the pens were randomly assigned within block to one of two treatments for the final 4 wk before slaughter: 1) finishing feed plus RAC (10 ppm; CP 19.2%, lysine 1.14%) or 2) finishing feed alone (CP 19.2%, lysine 1.14%). The major constituents of the diets were corn (64.4%), soybean meal (29.2%), and added fat (2.5%). The room was maintained at a minimal temperature of 18.5°C and naturally ventilated above the minimal level with air going through a heat exchanger.

All pigs were weighed individually on a weekly basis to monitor growth performance, and pen feed intakes were recorded daily. At the end of the 4-wk trial period, pigs were loaded onto a flat-bed truck and transported to the slaughter facility at the Purdue University West Lafayette campus, a distance of approximately 12.5 km. At the abattoir facility, they were off-loaded and held in lairage for up to 1 h before slaughter. After slaughter, individual hot carcass weights and carcass ultrasounds of loin and backfat depth measurements were collected.

Behavior

The behavior of gilts in 12 pens (six per treatment) was recorded over a 22-h period once a week during each of the 4 wk using ceiling-mounted cameras (Panasonic WV-CD110AE, Matsushita Electric Industrial Co. Ltd., Osaka, Japan) attached to time-lapse video recorders (Panasonic AG6720A, Matsushita Electric Industrial Co. Ltd.). The 22-h period avoided the 2 h during which daily husbandry routines, such as refilling feed hoppers and cleaning, were carried out since these could vary in the amount of disturbance that different pens were subject to, depending on their position in the barn. The video data were analyzed using a scan-sampling technique, with behavior, location, and posture of each pig in a pen recorded every 5 min. The behaviors recorded were inactive, active (including walking, rooting, manipulating pen mates and pen components, and belly-nosing), alert, chewing, engaged in agonistic interactions, drinking, and feeding, Data from each pig were then combined to give a behavioral time budget with each pen as an experimental unit. Also, once a week over the 4 wk, pigs were subjected to a behavioral disturbance test where, when lying, all pigs in a pen were made to stand and the time taken for them to return to lying down was recorded.

All pigs were weighed five times—once at the start of the trial and once at the end of each week of treatment. Weighing was carried out in the central corridor by two handlers. The same pair of handlers carried out the weighing on wk 0, 1, and 3, but on wk 2 and 4, one of the pair of handlers was different. Static barriers were placed across the corridor about 7.0-m apart, forming a "pen." A rear-entry/rear-exit weighing crate was placed towards one end of the "pen." The door to the pigs’ home pen was opened and the pigs were allowed to exit voluntarily. Once in the corridor, an individual pig was selected and driven by one handler towards the open weighing crate, using a solid board as a guide and hands and legs to push when necessary. The other handler stood to the side of the crate and closed the door once the pig was inside. Once the weight was taken, the crate handler opened the crate door and the pig either reversed out voluntarily or was tapped on the head by the crate handler with her hand. Any pigs that did not exit the home pen voluntarily to be weighed were forced out of the pen by the board handler and weighed in the same way. Once all three pigs had been weighed, the pigs were herded back into the home pen by both handlers and the gate was shut. The weighing process was videotaped using a hand-held camcorder for later analysis by a skilled observer. Although the observer was not blind to the treatments, the measures taken were entirely objective, and were therefore unaffected by potential observer bias. The measures taken over the weighing process included: 1) the number of pigs exiting the home pen voluntarily; 2) the time taken for each individual pig to exit the home pen; 3) the time taken to get the pig into the weighing crate, from the first contact with the board handler until the crate gate was shut; 4) the number of pats, hand pushes, and knee pushes needed to get the pig into weighing crate; 5) the time taken to get the pig out of the weighing crate, from the crate gate opening until the pigs front feet were out of the crate; 6) the number of pats, slaps, and hand pushes needed to get the pig out of the weighing crate; and 7) the time taken to get all three pigs back into the home pen, from the first contact with a handler until the pen gate was shut.

Heart Rate

Heart-rate responses to unfamiliar human presence were measured in all pigs once during wk 4 of the trial. Twelve pens of pigs were recorded on each of two afternoons. The human entered each pen and fitted each of the three pigs with a Polar Vantage NV (Polar Electro Oy, Kempele, Finland) heart-rate monitor (see methodology in Marchant et al., 1995), which was set to record and store successive interbeat intervals. Once the last pig’s monitor had been fitted, all monitors were started and the experimenter then knelt in one corner of the pen and interacted with the pigs. The interactions took the form of reaching out and stroking and scratching any of the pigs that approached and were carried out for 10 min from the time that the last watch in the pen was started. At the end of this period, the experimenter stood up and removed the equipment and repeated the procedure in all the other pens.

After each set of three pens, the heart-rate data were downloaded from the receivers by "wire-free" contact via a Polar Interface (Polar Electro Oy) to a PC. The data were displayed in graphical and numerical form using Polar Precision Performance Analysis Software (Version 2.1, Polar Electro Oy) and analyzed to determine mean heart rate in beats per min (bpm) every 1 min over the 10-min period, with each pen as an experimental unit.

Heart rate was also measured during transportation to the campus slaughter facility. Transportation took place on four separate mornings, with 18 pigs transported each day from 12 of the pens. Due to equipment constraints, the heart rate of only eight pigs could be recorded each day. Thus, a total of 32 pigs were recorded, with at least one pig recorded from each of the 24 pens. On transport days, the eight randomly selected pigs were fitted with heart-rate monitors, as detailed above, but with the transmitter belt and receivers then entirely covered with Vetrap (3M, St. Paul, MN) to prevent the equipment from being damaged by other pigs during transport.

Once the monitors had been fitted, four of the monitor-fitted pigs were released into the central corridor together with five other study pigs, each randomly selected from separate pens. They were then herded down the corridor onto a hydraulic trailer lowered to floor level, situated in the central handling room between the two wings of the Evaluation Center. Once the pigs were on the trailer, it was raised and pulled 20 m outside to one of two similar flatbed trucks. The pigs were then herded off the trailer onto the truck, and the truck departed immediately for the slaughter facility. The other four pigs with monitors then underwent the same procedure onto the second truck, which also departed immediately after loading. The loading procedure took approximately 2 min. The number of pigs with and without monitors for each truck was balanced across treatments. Once at the slaughter facility, after an 18-min journey, the pigs were off-loaded straight into a lairage room and the heart-rate equipment was removed, again over 2 min. The heart-rate data were downloaded as above and analyzed to determine mean heart rate every 2 min over the 22-min period, in bpm, with each pig as an experimental unit

Circulating Hormone Concentrations

Blood samples were taken from a single pig in each pen once during wk 4 of the trial. Twelve pigs had blood samples taken on each of two mornings, on days different from the heart-rate recording. During sampling, two experimenters entered the pen and randomly selected a single pig. The pig was restrained by one experimenter using a nose snare, while the other experimenter took a blood sample by jugular vena-puncture. An additional postslaughter blood sample was taken from the same pigs during exsanguination, and this was analyzed for cortisol concentrations only. Blood was collected into EDTA-treated tubes and immediately stored on ice. After transportation to the laboratory, the blood samples were centrifuged at 700 x g for 15 min at 4°C and plasma aliquots were stored at -80°C until further analysis. For plasma catecholamine analysis, duplicate samples were acidified and deproteinized with 4 M perchloric acid, and a commercial alumina-based solid-phase extraction kit (ESA, Inc., Chelmsford, MA) was used to extract catecholamines from the plasma. Following extraction and injection onto the reverse-phase column, norepinephrine and epinephrine were detected using HPLC with electrochemical detection. All assays were done in a single batch. The intraassay CV for norepinephrine was 0.49% and 1.60% for epinephrine. Plasma cortisol was measured in quadruplicate using a competitive binding radioimmunoassay kit (GammaCoat, DiaSorin, Stillwater, MN) as validated previously (Haussmann et al., 2000). The concentration of cortisol was calculated from a reference curve that ranged from 0 ng/mL (99.61% binding) to 600 ng/mL (17.63% binding) with a correlation coefficient of 0.9997. Again, all assays were done in a single batch and the intraassay CV for cortisol was 3.19%.

Statistical Analyses

The experiment was a repeated-measures design with repeated measurements of animals (main units) over time (subunits). Behavior and heart-rate data were analyzed using the repeated option of Proc GLM of SAS (SAS Inst., Inc., Cary, NC). Diet treatment, time, and time x treatment interactions were included in the model. Student’s t-tests were used to compare the hormone concentrations of the pigs, with treatment as the between-subjects factor. The data were transformed as appropriate when the assumption of normality was not fulfilled (Sokal and Rohlf, 1981). Because the behavioral time budget data were expressed as proportions of total time, these data were transformed using arcsine-root transformation.


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

During wk 1 and 2, pigs fed RAC spent more time active, more time alert, more time lying in sternal recumbency, and spent less time lying in lateral recumbency (Table 1Go). They also spent more time at the feeder in wk 1. There were no differences in time budgets in any of the other behaviors measured during wk 1 and 2, and there were no differences in any behaviors during wk 3 and 4. Overall, RAC-treated pigs spent more time active, feeding, and lying sternally, and less time lying laterally. Following behavioral disturbance, pigs on RAC took longer to settle than control pigs, but only during wk 1 and 2 (Table 1Go).


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Table 1. Mean proportion of time spent in various behaviors and postures by finishing pigs on ractopamine-added or control diets (only behaviors in which significant differences were found are included)
 
At the start of the trial, there were no differences in behavioral responses to handling. However, over the next 4 wk, 51% fewer RAC-treated pigs, on average, exited the home pen voluntarily compared with control pigs. RAC-fed pigs also took 136% longer to remove from the home pen, 83% longer to handle into the weighing scale, and needed 52% more pats, slaps, and pushes from the handler to enter the scales (Figure 1Go). There was no significant effect of the handling team on behavioral responses to handling, and thus, RAC-fed pigs were more difficult to handle regardless of the familiarity of the handlers. There also seemed to be no habituation to the procedure, inasmuch as none of the measures of handling decreased over time.



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Figure 1. Measures of ease of handling during weighing for finishing pigs on control ({square}) or ractopamine-added ({blacksquare}) diets. {dagger}P < 0.10, *P < 0.05, **P < 0.01. A) Overall treatment effect, P < 0.01; time effect, P < 0.01. B) Overall treatment effect, P < 0.05; time effect, P < 0.001. C) Overall treatment effect, P < 0.05; time effect, P < 0.05. D) Overall treatment effect, P < 0.05; time effect, P < 0.01.

 
Heart Rate

In response to the presence of the experimenter, at the end of wk 4, pigs fed RAC had higher mean heart rates overall during the test (144.6 ± 3.2 vs 136.4 ± 2.7 bpm, P < 0.05). When separated into 1-min periods, heart rates showed similar temporal patterns and were initially not different between the two treatments (Figure 2Go). However, it became, and remained, significantly different from 3 min onward (Figure 2Go). During transport, pigs fed RAC had similar mean heart rates overall (P > 0.10). When separated into 2-min periods, heart rates showed similar temporal patterns and were not different between treatments when heart rate was highest during loading and unloading (Figure 3Go).



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Figure 2. Mean ± SEM heart rate in beats/min of finishing pigs during exposure to an unfamiliar human. {dagger}P < 0.10, *P < 0.05, **P < 0.01). Overall treatment effect, P < 0.05; time effect, P < 0.001.

 


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Figure 3. Mean ± SEM heart rate in beats per min of finishing pigs during transport. {dagger}P < 0.10, **P < 0.01). Overall treatment effect, P > 0.10; time effect, P < 0.001.

 
Hormones

At the end of wk 4, pigs fed RAC had increased circulating concentrations of epinephrine (253.0 ± 55.0 vs 101.5 ± 15.0 pg/mL, P < 0.05) and norepinephrine (991 ± 150 vs 480 ± 58 pg/mL, P < 0.01) than control pigs. Circulating cortisol concentrations did not differ between treatments either before (RAC = 40.9 ± 5.2 ng/mL, control = 45.5 ± 5.1 ng/mL, P = 0.54) or after transport (RAC = 71.5 ± 7.5 ng/mL, control = 64.6 ± 6.3 ng/mL, P = 0.49). There was also no significant difference between treatments in percentage change in cortisol levels from baseline, in response to transportation.

Production

Pigs fed RAC had higher ADG and gain:feed ratios and heavier hot carcass weights at slaughter than control pigs (Table 2Go). Pigs fed RAC also tended to have lower 10th-rib backfat levels, larger longissimus muscle area, and a higher percentage of lean than control pigs (Table 2Go). There were no differences in daily feed intake or last-rib backfat levels.


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Table 2. Mean production measures of finishing pigs onractopamine-added or control diets
 

    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
The results indicate that RAC affected the behavior and physiology of finishing pigs in this study. In terms of time budget differences, pigs fed RAC were more active and alert, spent more time in sternal recumbency, and less time in lateral recumbency than control pigs. They also tended to take longer to settle after disturbance. These results seem to counter the results of the only other study carried out on RAC-fed pigs (Schaefer et al., 1992), which noted only that pigs on RAC were less active. However, the different timing of behavioral observations between this study and the previous study means that these results are not necessarily in conflict. In this study, the pigs were observed from the time that RAC was fed over 4 wk up to slaughter. Schaefer et al. (1992) observed the pigs after they had been on RAC for between 5 and 6 wk. From our results, the effects on behavioral time budgets were predominantly during wk 1 and 2 and had all but disappeared by wk 3, with only very few differences during wk 4. It is also known that the production benefits of feeding pigs a constant level of RAC is minimized by wk 5 on test (Schinckel et al., 2002a, b), and that at a cellular level, there is down-regulation of the ß-adrenergic receptors (Liu et al., 1994; Mills, 2001). Therefore, it is probable that the observations carried out in the previous study (Schaefer et al., 1992) occurred at the wrong time to answer the questions that were posed.

The behavioral responses to handling also indicated that as well as being more active, pigs fed RAC were generally more difficult to handle. They were less likely to exit the pen voluntarily and they took longer and needed more physical interaction with the handler to get onto the weighing scale (i.e., their behavior induced more negative behavior from the handler). These differences became apparent very quickly after feeding of RAC had started and, unlike the time budget differences, they continued over the entire 4-wk period. The fact that the differences in handling between treatments continued up to the end of the experiment could be indicative of the RAC-fed pigs learning that their weighing experience was particularly negative and thus remaining difficult to handle after any direct effect of the drug had disappeared. This result may have serious implications for the well being of market-weight pigs at the point of slaughter and may have financial implications in terms of time input. Pigs that are difficult to load and unload during transportation to the slaughterhouse are more likely to be subject to rough handling (Geverink et al., 1998) and take longer to handle.

There appeared to be no habituation to the handling and weighing routine, even though the process was carried out five times over 4 wk in a fairly standardized way. However, this was the case for all the pigs, including those on the control diet; therefore, it may be that the weighing routine either was not carried out frequently enough or was spread over a long enough time for habituation to occur. Other studies that have specifically investigated the effects of handling on pig behavior have usually imposed handling regimes two to five times per week over 8 to 10 wk (e.g., Gonyou et al., 1986; Hemsworth and Barnett, 1991; Geverink et al., 1998).

Ractopamine seems to chronically elevate heart rate compared to control-fed pigs. It has been shown that chronic administration of other ß-agonists results in a shift of intrinsic autonomic balance toward sympathetic dominance (Jartti et al., 1998), resulting in elevated basal heart rate. Chronic administration of RAC over this 4-wk period did not seem to affect cardiac responses to external stimuli, such as those encountered during handling, but a more detailed and arguably longer-term study of cardiac function, from the start of RAC administration, would be required to elucidate this.

Pigs fed RAC also had elevated catecholamine levels when measured during wk 4 of administration. Pigs fed RAC also had greater concentrations of epinephrine and norepinephrine when measured during wk 4 of administration. It is likely that a down-regulation of ß-adrenergic receptors occurred throughout the body of the pig. This down-regulation could cause the sympathetic nervous system to increase its production (and capability to produce) of both epinephrine and norepinephrine in order to optimize its binding to the fewer available receptors, thus maintaining its ability to effectively regulate the sympathetic system. This increase in capacity to produce and release epinephrine and norepinephrine would then be responsible for the increase in heart rates and activity of the pigs fed RAC.


    Implications
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Pigs fed ractopamine were more difficult to handle and had elevated heart rates and catecholamine concentrations after 4 wk of administration. Pigs that are more difficult to move are more likely to be subjected to rough handling and increased stress during transportation. Further research is needed to determine why ractopamine-fed pigs are more difficult to handle and to elucidate ways to ameliorate adverse behavioral responses to handling.


    Footnotes
 
1 This work was supported by the Dept. of Animal Sciences and USDA, ARS, funding the sabbatical visit of J. N. Marchant-Forde from the U.K. The authors thank C. Robson, R. Byrd, and the other Swine Unit staff for technical assistance. We also thank P. Singleton for running the assays. Back

2 The use of a trade, firm, or corporation in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the USDA or the ARS of any product or service to the exclusion of others that may be suitable. Back

Received for publication June 14, 2002. Accepted for publication October 23, 2002.


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


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Gu, Y., A. P. Schinckel, J. C. Forrest, C. H. Kuei, and L. E. Watkins. 1991a. Effects of ractopamine, genotype, and growth phase on finishing performance and carcass value in swine: II. Estimation of lean growth rate and lean feed efficiency. J. Anim. Sci. 69:2694–2702.[Abstract]

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