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J. Anim. Sci. 2005. 83:216-222
© 2005 American Society of Animal Science

ANIMAL PRODUCTION

Effects of castration, tooth resection, or tail docking on plasma metabolites and stress hormones in young pigs1

A. Prunier*,2, A. M. Mounier* and M. Hay{dagger}

* UMR Veau et Porc, Institut National de la Recherche Agronomique, 35590 Saint-Gilles, France; and and {dagger} Ecole Nationale Vétérinaire de Toulouse, 31076 Toulouse, France


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Changes in the activity of the sympathetic nervous system or in the hypothalamo-pituitary-adrenal axis have been extensively used to evaluate pain induced by castration or tail docking in numerous species. Such data are missing in pigs. Therefore, three experiments were conducted to determine the effects of castration, tail docking, or tooth resection on stress hormones. Glucose and lactate also were measured because catecholamines stimulate mobilization of glycogen, which results in glucose and lactate release. In Exp.1, 18 male pigs from seven litters (two or three pigs per litter) were catheterized surgically into one jugular vein, under general anesthesia, at 5 or 6 d of age. Two days later, they were submitted either to bilateral castration, control handling, or no handling (n = 6 per group). Blood samples were collected before (– 15 and –2 min) and after (5, 15, 30, 60, 90, 180 min) the experimental treatment. In Exp. 2, 27 female pigs from 12 litters (one to four pigs per litter) were submitted either to tooth clipping with pliers, tooth resection with a grinder apparatus, control handling, or no handling (n = 6 or 7 per group) at 1 d of age. In Exp. 3, 17 female pigs from nine litters (one to three pigs per litter) were submitted to one of the following treatments: 1) tail docking with an electric-heated scissor docking iron, 2) control handling, and 3) no handling (n = 5 or 6 per group) at 1 d of age. Castration induced significant (P < 0.05) increases in adrenocorticotropin hormone (ACTH; from 5 to 60 min), cortisol (from 15 to 90 min), and lactate (from 5 to 30 min). These variations are indicative of stress and tissue damage following castration. In contrast, neither tail docking nor tooth resection had marked effects on plasma cortisol, ACTH, glucose, and lactate. Measurements of plasma cortisol, lactate, and ACTH could be useful for validating treatments designed to relieve the distress reaction induced by castration in pigs.

Key Words: Adrenocorticotropic Hormone • Cortisol • Husbandry Procedures • Lactate • Pig


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
In most countries, young pigs are submitted routinely to husbandry procedures such as tooth resection, tail docking, and castration without any anesthesia or analgesia. These practices are carried out with two main justifications. First, they are supposed to improve the overall welfare of the animals by decreasing injuries to pigs and the teats of sows (tooth resection), preventing caudophagy (tail docking), and decreasing aggressiveness in castrated males. Second, the economic benefits should outweigh the welfare cost. Indeed, carcasses of testes-intact males are often depreciated, and rear parts of carcasses may be condemned in bitten pigs. However, tooth resection, tail docking, and castration are criticized because they are thought to be painful (SVC, 1997Go). Moreover the efficiency of tail docking and tooth resection to improve the overall welfare of the animals is in debate (SVC, 1997Go). Surprisingly, studies designed to evaluate the distress experienced by the pigs during and after these procedures are scarce and mainly focused on behavioral changes (tooth resection and tail docking, Noonan et al., 1994Go; castration, McGlone and Hellman, 1988Go; McGlone et al., 1993Go; White et al., 1995Go; Hay et al., 2003Go) or histopathological observations (tail docking, Simonsen et al., 1991Go; tooth resection, Hutter et al., 1994Go; Hay et al., 2004Go). Measurement of plasma cortisol to identify and quantify acute pain related to tail docking and/or castration has been successfully used in sheep and calves (for review, see Molony and Kent, 1997Go; Mellor et al., 2000Go). Plasma adrenocorticotropin hormone (ACTH) also was measured in bull calves to compare various methods of castration (Fisher et al., 1996Go), but such data are missing in pigs. Therefore, the objectives of the present experiments were to 1) determine the variations of plasma cortisol and ACTH in pigs around castration, tooth resection, or tail docking, and 2) determine glucose and lactate concentration changes because catecholamines are known to stimulate mobilization of glycogen which results in glucose and lactate release.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
All pigs were born from Large White xLandrace sows inseminated with Piétrain semen. Sows were kept in individual farrowing crates (2 m x 2.5 m) equipped with warming lamps. The floor was solid concrete spread with fresh straw every day. Pigs were freely moving and had full access to the dam. When necessary, litters were equalized to 8 to 12 pigs by adoptions within 2 d after birth.

Experiment 1
Eighteen male pigs from seven different litters were fitted with a jugular catheter at 5 or 6 d of age (two or three experimental pigs per litter). The catheter was inserted surgically into the right jugular vein under general anesthesia using halothane. It was affixed to the back of the animals with surgical tape. Immediately after surgery, pigs were returned to the farrowing crate but remained in a plastic box until they were fully awake. At that time (i.e., 10 to 30 min after surgery), they were let free. To limit stress when handling, which was necessary at blood sampling (see below), the pigs were handled two or three times by a technician and placed for 2 to 3 min in a box containing straw and a nonexperimental pig.

Two days after surgery, pigs were allocated within litters to one of the three experimental groups (n = 6 per group): castration (CAST), sham castration (SHAM), and no handling (NOHA). Pigs submitted to castration were restrained between the handler’s legs to expose their anogenital region. A scalpel was used to make an incision on each side of the scrotum. A second incision was made to free each testicle from the surrounding tissue. The testes were then removed by cutting the testicular cord. A disinfectant was applied into the open wound and pigs were immediately returned to their pen. Pigs submitted to sham castration were restrained for 45 s (mean duration of restraining for castrated pigs) and handled similarly but without any cutting.

From 1 to 2 h before blood sampling, catheter patency was checked and surgical tape was replaced with a bandage that fit the pig more tightly. Blood samples (1.5 to 2.0 mL per sample) were collected at –15, –2, 2, 15, 30, 60, 90, 120, and 180 min relative to the time of treatment for each animal. Pains were taken to avoid stress at blood collection and, whenever possible, animals were not handled. The tip of the catheter was gently removed from the bandage, opened, and blood was drawn with a 2-mL syringe. If necessary (animal walking or running), pigs were placed in a box during sampling as described previously, and this intervention was recorded. Immediately after collection, blood was transferred to tubes containing 10 µL of EDTA (0.8 M), placed on ice, and centrifuged at 3,000 x g and 4°C. Aliquots were kept at –20°C until assays were performed.

Experiments 2 and 3
Pigs (n = 49) from 20 litters were catheterized in the umbilical artery immediately after birth (two to four experimental pigs per litter). Catheter insertion was performed under general anesthesia (halothane inhalation as described by Le Dividich et al., 1991Go). Catheters were affixed to the back of the animals using surgical tape. To prevent catheters and bandages from coming in contact with urine, only females were catheterized. Within 10 min of birth, animals were returned to their dams. The day after in both Exp. 1 and 2, pigs were allocated within litters to experimental groups. Groups (n = 7 or 8 per group) in Exp 2 were as follows: tooth clipping (CLIP) with pliers, tooth grinding (GRIND) with a rotative electric grinder, sham clipping (SHAMC), or NOHA. Groups (n = six or seven per group) in Exp. 3 were as follows: tail docking with an iron docking (DOCK), sham docking (SHAMD), or NOHA. Pigs submitted to tail docking, tooth resection, or sham treatments were restrained in one technician’s arm during treatment.

Blood samples (1.0 to 1.5 mL per sample) were collected at –15, –2, 2, 15, 30, 60, 90, 120, 180 min relative to the time of treatment for each animal as described in Exp. 1. Blood and plasma were collected as described previously, except that aliquots for ACTH were obtained only at –2, 5, 15, 30, and 60 min after treatment, to decrease the volume of blood that was drawn.

Assays
The ACTH was measured in 200 µL of plasma using a two-site 125I immunoradiometric assay (Nichols Institute Diagnostic; San Juan Capitiano, CA). The quantification limit of the assay was 6 pg/mL plasma, and the intra- and interassay CV were 3.0 and 7.8% at 35 pg/mL, respectively. Cortisol was measured in 25 µL (1-d-old pigs) or 50 µL (7- or 8-d-old pigs) of plasma using a competitive 125I RIA kit (Immunotech, Marseille, France). The quantification limit of the assay was 8 ng/mL plasma, and the intra- and interassay CV were 4.2 and 10.0% at 71 ng/mL, respectively. Plasma concentrations of glucose and lactate were measured by automated enzymatic methods (Bio-Mérieux kits, Marcy l’Etoile, France) with a Cobas Mira multichannel analyzer (Hoffmann-LaRoche, Basil, Switzerland).

Statistical Analyses
Concentrations of hormones and metabolites of samples collected when pigs were placed in the box or immediately after were carefully examined because such handling may have induced an increment in ACTH and cortisol. A statistical analysis was not possible because these samples were collected occasionally on a non-controlled time schedule, but no obvious increase was observed (visual exam).

All plasma concentrations were analyzed by ANOVA using MIXED procedures of SAS (SAS Inst., Inc., Cary, NC) after logarithmic transformation to fit a normal distribution. First, data were analyzed using a repeated model with individual pigs as experimental units. The complete model included the main effects of treatment, litter and time, and the treatment x time interaction. The REPEATED statement of SAS was used with a covariance structure depending on the variable analyzed (heterogenous compound symmetry for cortisol, antedependence for ACTH, and banded for glucose and lactate). When a significant (P < 0.05) treatment effect was found, comparison between treatments was made with the Bonferroni’s test (SAS). When a significant (P < 0.05) time effect was found, each sample collected from 2 to 180 min was compared with those collected at –15 and –2 min with the CONTRAST statement. When the treatment x time interaction was significant (P < 0.05), new analyses were run for each time of sampling with main effects being treatment and litter.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Experiment 1
One castrated piglet was removed from statistical analyses because its plasma concentrations of ACTH and cortisol were extremely high after surgery (ACTH > 300 pg/mL and cortisol > 300 ng/mL from 30 min onward). This animal died the day after and was not replaced.

None of the effects in the model were significant (P ≥ 0.08) for glucose. A treatment x time interaction was detected (P < 0.01) for ACTH, cortisol, and lactate (Table 1Go). Comparisons among experimental groups for each time of sampling showed numerous differences (Figure 1Go). Plasma ACTH was higher in CAST than in SHAM and NOHA pigs from 5 to 60 min (P < 0.05), whereas SHAM and NOHA pigs had similar (P > 0.10) concentrations throughout the experiment. Plasma cortisol was higher in CAST than in SHAM and NOHA pigs from 15 to 90 min (P < 0.05), whereas no significant differences were found between SHAM and NOHA pigs. With respect to lactate, significant differences (P < 0.05) were observed among the three groups at 5 min (CAST > SHAM > NOHA) and between CAST and the two other groups at 15 and 30 min.


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  		Table 1. Main effects and treatment x time interactions (P-values) in the three experiments designed to assess the effects of castration, tail docking or tooth resection on plasma variables in pigs
 


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  		Figure 1. Plasma profiles of adrenocorticotropin hormone (ACTH), cortisol, and lactate in 7- or 8-d-old pigs from Exp. 1 (CAST = surgical castration; SHAM = sham castration; NOHA = no handling; n = 5 or 6 per group). Values shown are means ±SEM. The treatment x time interaction was significant (P < 0.01) for the three variables. Within time of sampling, an asterisk indicates a treatment effect at P < 0.05.

 
Experiments 2 and 3
Three pigs (two CLIP and one NOHA) from Exp. 2 and two pigs (one SHAMC and one NOHA) from Exp. 3 and were dropped from the study as a result of loss of catheter function; they were not replaced. Therefore, there were six pigs in the CLIP group and seven pigs in the GRIND, NOHA, and SHAMC groups in Exp. 2; six pigs in the DOCK and SHAMD groups; and five pigs in the NOHA group in Exp. 3.

No treatment xtime interaction was significant (P ≥ 0.29; Table 1Go). Significant effects of treatment (P < 0.05) were observed only for lactate in Exp. 2 (plasma lactate was higher in GRIND than in SHAMC and CLIP pigs and intermediate in NOHA pigs) and for glucose in Exp. 3 (plasma glucose was lower in SHAMD than in DOCK and NOHA pigs). Time-related variations were of low amplitude in both experiments (Figures 2Go and 3Go); however, they were significant for ACTH, cortisol, and lactate in Exp. 2 (P ≤ 0.02; Table 1Go). Compared with –15 and –2 min, a significant (P < 0.05) increase was observed at +5 and +15 min for cortisol and ACTH and at 5 min for lactate (Figure 2Go).



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  		Figure 2. Plasma profiles of adrenocorticotropin hormone (ACTH), cortisol, and lactate in 1-d-old pigs from Exp. 2 (CLIP = tooth clipping; GRIND = tooth grinding; SHAMC = sham clipping; NOHA = no handling; n = 6 or 7 per group). Values shown are means ±SEM. For ACTH and cortisol, treatment and time x treatment interaction were not significant. The treatment was significant only for lactate, with GRIND pigs having higher concentrations (P < 0.05) than SHAMC and NOHA pigs across time.

 


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  		Figure 3. Plasma profiles of adrenocorticotropin hormone (ACTH), cortisol, and lactate in 1-d-old pigs from Exp. 3 (DOCK = tail docking; SHAMD = sham docking; NOHA = no handling; n = 5 or 6 per group). Values shown are means ±SEM. Treatment and time x treatment interaction were not significant.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
To our knowledge, this is the first time that plasma patterns of stress hormones and metabolites around castration, tail docking, or tooth resection are reported in the pig. They clearly demonstrate that surgical castration without anesthesia and analgesia induces a strong activation of the pituitary-adrenocortical axis in 7- or 8-d-old pigs, whereas tail docking or tooth resection has no clear effect in 1-d-old pigs.

An increase in plasma ACTH was shown from 5 to 60 min after castration, followed by an increase in plasma cortisol lasting from 15 to 90 min after castration. The increase in plasma ACTH was intense (40-fold) and rapid, with the highest values detected at the first sample following surgery (i.e., 5 min after castration). The increase in cortisol was slightly delayed, with peak values occurring between 30 and 60 min after surgery. Cortisol then returned to presurgery level within 3 h. The increase in plasma cortisol was of much lower amplitude (fourfold) than that of ACTH. The short-lasting increment of plasma cortisol after castration is in agreement with the lack of variation in urinary cortico-steroids within the 3 d following surgery (Hay et al., 2003Go). Similar patterns of plasma cortisol have been observed in other species after surgical castration plus tail docking (lambs, Mellor and Murray, 1989Go; Wood et al., 1991Go) or after surgical castration alone (calves, Molony et al., 1995Go). However, in some studies, cortisol was increased for a longer duration (>6 h) after castration (lambs, Lester et al., 1991Go, 1996Go; Kent et al., 1993Go; calves, Cohen et al., 1990Go; Fisher et al., 1996Go, 1997Go; Earley and Crowe, 2002Go). A sharp and short-lasting increase in ACTH was observed in bull calves castrated at 5 mo of age (Fisher et al., 1997Go).

The increases in ACTH and cortisol after castration are mainly due to castration itself because they were of much lower amplitude and duration in pigs submitted to simulated castration, and they may be related to pain or tissue damage. Indeed, the painful character of castration was demonstrated in pigs by the activation of the protein c-Fos expression in neurons from the spinal cord dorsal horn after castration (Nyborg et al., 2000Go). Using local anesthesia decreased this activation (Nyborg et al., 2000Go), as well as the increase in heart rate during castration in that species (White et al., 1995Go). It would be informative to analyze the pattern of plasma ACTH and cortisol following castration after local anesthesia and analgesic treatment.

A sharp increase in plasma lactate (2.5-fold) was observed in castrated pigs, whereas glucose did not change. The increment in lactate is probably due to the mobilization of muscular glycogen stores after epinephrine stimulation (Mayes, 1995Go). Indeed, measurement of plasma epinephrine on pools of plasma from the pigs of the present experiment showed a sharp increase at 5 min, followed by a progressive decrease until 30 min in the CAST group but not in other groups (data not shown). Because the main product of glycogen metabolism at the hepatic level is glucose (Mayes, 1995Go), the lack of glucose increment after castration may be explained by an insufficient level of hepatic glycogen stores in young pigs. In heavier pigs (100 kg BW), stress associated with aggression between animals resulted in a more pronounced increase in plasma lactate (tenfold) than in plasma glucose (1.2-fold; Fernandez et al., 1995Go). Pain-related increases in glucose and lactate after surgery have been described in adult men and newborn infants (Anan, 1986Go, 1990Go).

Lack of effect of tooth resection or tail docking on plasma ACTH and cortisol can be explained by four main hypotheses: 1) the pituitary-adrenocortical axis is not responsive to stress in 1-d-old pigs; 2) the pituitary-adrenocortical axis is highly responsive to stress in 1-d-old pigs, but the variation related to the manipulation of the animals associated with blood sampling masks the effects of the experimental procedures; 3) the pituitary-adrenocortical axis activity is markedly stimulated around birth, and it is not able to respond to any supplementary stimulation; and 4) nociceptive stimuli due to tooth resection and tail docking are not sufficient to elicit a physiological stress response. Data are too scarce to discuss these hypotheses in detail. Nevertheless, it has been shown that the cortisol increment after exogenous ACTH stimulation was similar at 3, 7, 21, and 35 d of age, despite changes in pretreatment cortisol concentrations (Otten et al., 2001Go). Similarly, Klemcke and Pond (1991)Go did not show any difference in the cortisol response of piglets to maternal deprivation at 3, 10, 17, or 24 d of age.

Concerning the fourth hypothesis, it should be noted that, when the effects of tail docking and surgical castration were compared in 28- to 37-d-old sheep, the increase in plasma cortisol was of lower amplitude and duration in tailed sheep than in castrated ones (Lester et al., 1991Go). Moreover, behavioral perturbations induced by tail docking or tooth resection in pigs (Noonan et al., 1994Go; Meunier-Salaün et al., 2002Go) seem of lower amplitude and of shorter duration than those elicited by castration (McGlone and Hellman, 1988Go; McGlone et al., 1993Go; Hay et al., 2003Go). Therefore, lower intensity of tissue damage-related stimuli may explain, at least in part, the lower activation of the pituitary-adrenocortical axis in pigs after tail docking or tooth resection than after castration. It would be of interest to evaluate plasma stress hormone profiles of pigs castrated at 1 d of age, especially because it is common to castrate pigs at that age in commercial herds. Even though tail docking or tooth resection did not seem to elicit physiological stress reactions in the first 2 h, animals may experience pain in the weeks or months after, as pointed out by the observation of neuromas at the tip of docked tails (Simonsen et al., 1991Go) and the histological detection of numerous lesions in teeth and surrounding tissues of resected pigs (Hay et al., 2004Go).


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
Results of the present study indicate that surgical castration without anesthetic or analgesic is stressful for 7- or 8-d-old pigs. Based on physiological measurements, tail docking or tooth resection seems to be less stressful in 1-d-old pigs. If surgical castration cannot be avoided, the welfare of piglets should be improved by local anesthesia combined with prolonged analgesic treatment. Measurements of plasma lactate, cortisol, and adrenocorticotropin hormone may be useful to assess stress associated with alternative regimens.


   Footnotes
 
1 Supported by project funding from the Direction Générale de l’Alimentation (Paris, France) and the Institut National de la Recherche Agronomique (Paris, France). The authors thank all staff of UMRVP for their technical assistance. Back

2 Correspondence-phone: +33 299 285 056; fax: +33 299 285 080; e-mail: armelle.prunier{at}rennes.inra.fr.

Received for publication June 25, 2004. Accepted for publication October 6, 2004.


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


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Cohen, R. D. H., B. D. King, L. R. Thomas, and E. D. Janzen. 1990. Efficacy and stress of chemical versus surgical castration of cattle. Can. J. Anim. Sci. 70:1063–1072.

Earley, B., and M. A. Crowe. 2002. Effects of ketoprofen alone or in combination with local anaesthesia during the castration of bull calves on plasma cortisol, immunological, and inflammatory responses. J. Anim. Sci. 80:1044–1052.[Abstract/Free Full Text]

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