Surgical castration with pain relief affects the health and productive performance of pigs in the suckling period

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Morales et al. Porcine Health Management (2017) 3:18 DOI 10.1186/s40813-017-0066-1 RESEARCH Open Access Surgical castration with pain relief affects the health and productive performance of pigs in the suckling period Joaquin Morales1* , Andre Dereu2, Alberto Manso1, Laura de Frutos1, Carlos Piñeiro1, Edgar G. Manzanilla3 and Niels Wuyts2 Abstract Background: Surgical castration is still practiced in many EU countries to avoid undesirable aggressive behavior and boar taint in male pigs. However, evidence shows that castration is painful and has a detrimental influence on pig health. This study investigated the clinical and productive effects of surgical castration in the suckling period. A total of 3696 male pigs, 3 to 6 days old, comprising of 721 litters from two different farms were included in the study. Within each litter, half of the males were kept as intact males (IM) and half were surgically castrated (CM). Surgical castration was conducted by a trained farmer. Average daily gain (ADG), body weight at weaning (BWW), percentage of pre-weaning mortality (PWM) and antibiotic usage were measured. Pig major acute phase protein (PigMAP) serum concentrations were analyzed prior to castration, and on days 1 and 10 after castration. Productive performance data were analyzed using a linear mixed model. Mortality and percentage of pigs treated with antibiotics were analyzed using the Fisher’s exact test. Results: No overall differences in BWW and ADG were observed between the two groups. However, differences were observed when the same effects were analyzed in the 25% lightest, 50% medium and 25% heaviest pigs at birth. PWM was higher in CM than in IM groups (6.3% vs 3.6%; p < 0.001), especially in the light (12.2% vs 6.2%; p = 0.02) and in the medium (5.5% vs 2.7%; p

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PWM was higher in CM than in IM groups (6.3% vs 3.6%; p < 0.001), especially in the light (12.2% vs 6.2%; p = 0.02) and in the medium (5.5% vs 2.7%; p = 0.04) weight groups. In the heaviest pigs group PWM was not affected by castration, but IM tended to show higher ADG (p = 0.06) and showed higher BWW (8.0 kg vs 7.8 kg; p = 0.05) than CM. There were no differences in percentage of pigs treated with antibiotics between the two groups (5.8% vs 5.8%; p = 0.98) in this study. Furthermore, PigMAP was increased in CM the day after castration (0.944 mg/ml vs 0.847 mg/ml; p = 0.025), but there was no difference between CM and IM groups at day 10. Conclusions: Surgical castration has a negative impact on production in the suckling period because it causes an increase in PWM, especially in pigs in the three lower quartiles for body weight, and negatively affects the BWW in pigs born in the highest quartile for body weight. Keywords: Boar breeding, Entire boars, Pre-weaning pig mortality, Stop castration, Suckling piglet, Surgical castration, Swine * Correspondence: joaquin.morales@pigchamp-pro.com 1 PigCHAMP Pro Europa S.L. c, Santa Catalina, 10, Segovia, Spain Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made

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f changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Morales et al. Porcine Health Management (2017) 3:18 Page 2 of 6 Background day 14 of age to the piglets ad libitum. Following normal Intact male pigs have better feed conversion and can practice in both farms, teeth clipping and tail docking have higher growth rates than surgically castrated pigs were performed on all piglets enrolled in this study be- (barrows) [1]. However, in many countries, male pigs are fore Study Day 0. Male pigs were individually identified routinely castrated to prevent boar taint that results by ear tagging, weighed and randomized on Study Day 0 from the presence of androstenone or skatole [2], and (day 3 to 6 of life). Randomization was done within litter also to reduce undesirable aggressive and sexual behav- at individual animal level and based on body weight. A iour following the onset of puberty [3, 4]. different randomization list was used for each litter. Dir- Current European legislation allows surgical castration ectly after randomization piglets in CM group were sur- up to an age of 7 days of age [5]. However, as castration gically castrated. Cross-fostering was only allowed before of pigs is also a substantial animal welfare problem, Study Day 0. The study observations ended on weaning European agreements specified that from 2012 onwards at 28 days of age of the piglets. Normal animal housing physical castration of pigs should be performed with and management procedures usually employed on the prolonged analgesia and/or anesthesia and that it should farms were used throughout the experimental period be abandoned totally by 2018 [6].

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d on the prolonged analgesia and/or anesthesia and that it should farms were used throughout the experimental period be abandoned totally by 2018 [6]. Available evidence and animals were managed in compliance with the Euro- shows that castration is both painful and stressful for the pean farm animal welfare regulations [5]. animal during and for some time after the castration [7, 8]. Potential complications associated with surgical Surgical castration procedure castration include hemorrhage, excessive swelling or A non-steroidal anti-inflammatory drug (NSAID) edema and infection: these can reduce performance, com- (meloxicam; 0.4 mg meloxicam/kg body weight, Conta- promise health and, in some cases, increase mortality. A cera®: Zoetis) was administered 30 min before castration meta-analysis of 15 studies in 2009 showed that male pig- to mitigate pain, following recommendations proposed lets that had been surgically castrated had significantly by O’Connor et al. [10]. The use of NSAIDs was not a higher mortality rates than their intact littermates [9]. common practice in the two farms selected, but the However, existing literature provides little consistent in- study aimed to represent the ‘best practice’ as it should formation about the effects of surgical castration on the be applied according to the 2012 European agreement timing and causes of mortality, the incidence of different [6]. Farm workers, previously trained by a veterinarian in disease problems and on how the growth rate of the cas- order to standardise the procedure between farms, per- trated pigs is affected in the suckling period. formed the castration according to normal farm practice This study aims to evaluate the clinical and productive between days 3 and 6 of life. In brief, piglets were re-

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ion according to normal farm practice This study aims to evaluate the clinical and productive between days 3 and 6 of life. In brief, piglets were re- effects of surgical castration with pain relief in the suck- strained by the farmer workers. Two vertical incisions ling period and to describe the different causes of mor- were made in the scrotum and the testes were removed tality associated with this surgical procedure. after tearing off the spermatic cord. After castration, a topical antibiotic was administered on the injury area Methods (oxytetracycline; Tenicol spray: MSD) for 5 s. Routine Animals, facilities and experimental design use of an antibiotic spray was used in this study in order This research was carried out at two one-site commer- to ensure optimal post-surgical recovering in the cas- cial swine herd farms, located in Segovia, Spain. Both trated group. farms were farrow-to-finish farms and were located in the same geographical area, had the same genetic lines Observations and measurements and feed provider and similar size (630 and 570 repro- A general physical examination was performed for all ductive sows in Farm 1 and Farm 2, respectively). The enrolled pigs on Study Day 0. Body weight was mea- experimental design was a randomized block design, in- sured from all piglets on Study Day 0 (3–6 days of age) cluding surgical castration as the main effect, resulting and at weaning (28 days of age), and average daily gain in two experimental treatment groups with surgically (ADG) in the study period was calculated. Daily general castrated males (CM) and male pigs kept as intact males health observations were carried out by the farm (IM). workers and ill or injured piglets were promptly exam- Any sows with a clinical history of high incidence of ined and

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re carried out by the farm (IM). workers and ill or injured piglets were promptly exam- Any sows with a clinical history of high incidence of ined and treated by the veterinarian. For all treatments abortions, high percentage of stillborn or high percent- the following information was recorded: animal identifi- age of pre-weaning mortality were excluded from the cation, date, product used, dose, frequency, as well as study. At day 107 of gestation sows were moved from reason for treatment (the routine use of the post castra- the gestation barn to farrowing pens. In both farms, each tion antibiotic spray was not recorded or analysed as a farrowing pen had a partially slatted floor and a heat treatment in the study observation period). In addition, bulb for the piglets. A blank creep feed was offered from for any piglet found dead or euthanized on welfare Morales et al. Porcine Health Management (2017) 3:18 Page 3 of 6 grounds during the study, a necropsy was conducted PigMAP serum concentrations were analyzed using a and the reason for death was recorded. Piglets in very linear mixed model (proc MIXED) with the fixed effects poor health were removed from the study and placed of treatment, parity, farm and second degree interac- with a nurse sow to give them a chance to recover. All tions effect. adverse health observations were recorded. The different Data on casualties and medication was analyzed using reasons for mortality or removals were listed as deaths generalized linear models (proc GLIMMIX) including associated to complications following the surgical castra- treatment, parity, farm, body weight group and all their tion procedure, meningitis, diarrhoea, runt piglets and second level interactions as fixed factors. When the fre- other causes that could be related

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r tion procedure, meningitis, diarrhoea, runt piglets and second level interactions as fixed factors. When the fre- other causes that could be related to post-castration quency of events (casualties or medication) observed complications. Meningitis was assigned to piglets that was 0 in any level of the independent variables (treat- showed nervous signs (leaning head, pedaling and con- ment, BW group or their interaction), the model did not vulsions) before death or sudden deaths. Diarrhoea was converge, and the analysis was done using Fisher’s exact assigned to piglets showing liquid faeces, dehydration, test. and poor body condition before death. Runt piglets were All statistical analyses were carried out using SAS ver- piglets which showed poor body condition and cachexia sion 9.4. as the only clinical signs before death. All other minor causes of death or removal (e.g. dermatitis) were classi- fied as ‘other’. Results Different reasons for antibiotic treatment interventions A total of 3696 crossbred (Large White & Landrace x were classified as diarrhoea, dermatitis, runt piglets, Pietrain) male pigs from 721 litters were included in the meningitis, respiratory signs (coughing, rapid breathing, study. In Farm 1, a total of 1950 piglets from 363 litters discharges from the eyes-conjunctivitis, sneezes, etc) and and in Farm 2, 1746 piglets from 358 litters were in- lameness (arthritis). cluded in the study. A total of 1848 piglets were assigned An acute phase-protein, PigMAP (Major Acute Phase- to each treatment group (IM, CM). protein of Pigs), was used as an unspecific biomarker to Productive performance (Table 1) showed an inter- quantify inflammation and/or stress. Fifty litters from action between surgical castration and weight group Farm 1 and 40 litters

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1) showed an inter- quantify inflammation and/or stress. Fifty litters from action between surgical castration and weight group Farm 1 and 40 litters from Farm 2 were randomly se- (body weight at weaning, p = 0.084). Castration did not lected using a random number table for blood sampling. affect performance of light or medium piglets but heavy In each of these 90 litters, two piglets (1 CM and 1 IM) CM animals tended to have a lower ADG (p = 0.059) were also randomly selected (180 piglets in total; 100 in and had a lower body weight at weaning (p = 0.05). Pre- Farm 1 and 80 in Farm 2) and were blood sampled by weaning mortality (Table 2) also showed an interaction venopunction of the vena cava on day 0 (before castra- between surgical castration and weight group tion), day 1 (the day after castration) and day 10. Serum (p = 0.063). Mortality was almost double for light was immediately removed after centrifugation at 3500 g (p = 0.017) and medium (p = 0.041) weight CM piglets for 5 min, and kept frozen (−20 °C) until their analysis. but was not different for heavy CM animals (p = 0.327). PigMAP concentration in serum was measured by sand- No other variable or interaction affected productive per- wich ELISA with two monoclonal antibodies, using a formance or pre-weaning mortality. commercial kit (pigMAP kit ELISA, Acuvet biotech, The percentages for different causes of death are pre- Zaragoza, Spain) as described earlier [11]. sented in Fig. 1. Percentage of mortality associated with the procedure of castration, with meningitis and losses of runt piglets were higher in CM than in IM group. In Statistical analysis total 17 CM piglets died due to castration: 4 of them All treatment differences were assessed at the 2-sided had a non-detected testicular hernia and died

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l 17 CM piglets died due to castration: 4 of them All treatment differences were assessed at the 2-sided had a non-detected testicular hernia and died during the 0.05 alpha level of significance and trends were reported surgical procedure; 3 piglets died within 1 h after the for alpha = 0.10. In all cases of an interaction with surgical procedure showing an haemorrhage in the p < 0.10, the interaction was studied. Multiple compari- wound area and the other 10 died within 5 days after sons were adjusted using Tukey’s correction. the procedure of castration showing an infection in the Piglets were classified based on their weight at day 0 surgical area. No differences between CM and IM were in quartiles: light (25% lightest pigs), medium and heavy observed in the other reasons of mortality or removal. (25% heaviest pigs). The primary variables average Odds ratios for mortality were 2.3 (1.1, 4.8) for meningi- weight at weaning and ADG were analyzed using a gen- tis and 2.8 (1.3, 6.0) for runt pigs, when surgical castra- eral linear model (proc GLM) including treatment, par- tion was applied. Body weight group affected mortality ity, farm and body weight group (light, medium, heavy) associated to castration (0.75, 0.54 and 0.00% for light, and all their second degree interactions as fixed factors. medium and heavy piglets respectively; p = 0.021), Morales et al. Porcine Health Management (2017) 3:18 Page 4 of 6 Table 1 Effect of surgical castration on growth rate in the suckling period by initial body weight groupa Item Intact Males Castrated Males SEMb P value3 Light pigs Initial number of pigs 476 459 Body weight, day 0 (kg) 1.43 1.42 0.008 0.528 Body weight, day 28 (kg) 5.69 5.77 0.062 0.367 Average daily gain (g/day) 182.3 185.5 2.648 0.379 Medium pigs Initial

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day 0 (kg) 1.43 1.42 0.008 0.528 Body weight, day 28 (kg) 5.69 5.77 0.062 0.367 Average daily gain (g/day) 182.3 185.5 2.648 0.379 Medium pigs Initial number of pigs 921 931 Body weight, day 0 (kg) 1.96 1.97 0.006 0.226 Body weight, day 28 (kg) 6.83 6.79 0.041 0.540 Average daily gain (g/day) 210.0 208.5 1.768 0.535 Heavy pigs Initial number of pigs 451 458 Body weight, day 0 (kg) 2.55 2.57 0.012 0.388 Body weight, day 28 (kg) 7.97 7.81 0.063 0.050 Average daily gain (g/day) 237.4 230.4 2.615 0.059 a Pigs were split in three groups according to their initial body weight: light pigs (25% pigs with the lightest initial body weight), medium pigs (50% pigs with medium initial body weight) and heavy pigs (25% pigs with the heaviest initial body weight) b Standard Error of Mean 3 P-value for surgical castration treatment effect (Intact vs. Castrated male pigs) obtained by multiple comparisons using Tukey’s correction crushing (2.78, 1.03 and 0.77%; p = 0.002), and meningi- In the present study, castration was conducted under tis (1.60, 0.76, 0.33%; p = 0.012). commercial conditions by two experienced farmers. In No differences in antibiotic treatment due to castra- brief, meloxicam was administered about 30 min prior tion were observed in this study. Highest frequency of to castration in male pigs in CM group, and a topical antibiotic treatment was to treat diarrhoea (4.20%) antibiotic was applied on the injury wounds after castra- followed by treatment of meningitis (0.98%). Body tion. No other manipulations were imposed, to replicate weight group affected antibiotic treatment for meningitis commercial situations as much as possible. Under these (2.99, 1.46 and 0.66% for light, medium and heavy pig- conditions, surgical castration almost doubled the per- lets

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s as much as possible. Under these (2.99, 1.46 and 0.66% for light, medium and heavy pig- conditions, surgical castration almost doubled the per- lets respectively; p = 0.002). centage of pre-weaning mortality, mainly associated with PigMAP serum concentration was significantly higher runting of affected piglets, with fatal meningitis, and in CM than in IM groups the day after castration, and with the intra- and the post-surgery mortality. Most these differences disappeared by day 10 (Table 3). studies evaluating the consequences of castration rarely mention pre-weaning mortality [12], suggesting that Discussion there is no effect. However, analysis of data from com- Castration is a surgical procedure commonly performed mercial herds shows that poor hygiene at castration in non-optimal hygiene conditions on 3–6 days-old pig- could promote the occurrence of arthritis, which itself lets and results in open wounds. Until now, very little re- may result in death of piglets [13]. In another study, a search quantifying the health and performance impact of lower antibody response to an immune challenge in cas- castration on male piglets, especially in the suckling trated piglets compared to entire piglets was observed period, has been published. [14], probably attributable to the stress reaction, which Table 2 Effect of surgical castration on percentage of mortality in the suckling period by initial body weight groupa Item Intact Males (%) Castrated Males (%) Odds ratiob (95% CI) P value3 Light 6.3 12.2 2.2 (1.09, 4.25) 0.017 Medium 2.7 5.5 2.1 (1.02, 4.22) 0.041 Heavy 2.4 1.5 0.6 (0.15, 2.51) 0.327 a Pigs were split in three groups according to their initial body weight: light pigs (25% pigs with the lightest initial body weight), medium pigs (50% pigs with medium initial

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groups according to their initial body weight: light pigs (25% pigs with the lightest initial body weight), medium pigs (50% pigs with medium initial body weight) and heavy pigs (25% pigs with the heaviest initial body weight) b Odds ratio of death 3 P-value for surgical castration treatment effect (Intact vs. Castrated male pigs) obtained by multiple comparisons and using Tukey’s correction Morales et al. Porcine Health Management (2017) 3:18 Page 5 of 6 Fig. 1 Different reasons of losses in intact and in castrated male pigs during the suckling period in percent. Number of cases is detailed in each column could explain the higher mortality. In our study, Pig- the suckling period. However, taking into account our MAP serum concentration was significantly higher in observation that the mortality rate was almost double in CM than in IM the day after castration, confirming that CM group compared to the IM group, an alternative ex- physical castration causes tissue damage, inflammation planation is more likely: i.e. that there is a dispropor- and stress. This result is in accordance with a previous tional impact on weakest pigs (those with lowest study [15], where a significant increase of haptoglobin bodyweight) in the CM group with higher mortality serum concentration, another acute phase protein, 24 h whilst in the IM group the survival rate of these low after physical castration was also observed, likely associ- weight piglets was higher. The mean growth perform- ated with stress or with an inflammatory process. Since ance picture in the whole group obscures the effect of in this study most antibiotic interventions were not spe- these opposite interactions. cific to castration, it was not possible to make an assess- Reduced health recovery may be related to less time

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not spe- these opposite interactions. cific to castration, it was not possible to make an assess- Reduced health recovery may be related to less time ment about antibiotic usage as a result of castration or nursing and more time lying down of castrated pigs non-castration. Furthermore, it should be noted that all [17]. Adequate colostrum intake and regular con- piglets in the CM group received a topical antibiotic sumption of milk are required for control of gastro- (spray) as a post-surgery prophylactic measure. intestinal diseases, hypoglycemia, starvation, and Castration reduces undesirable aggressive and sexual crushing of the pre-weaned pig [18]. In addition, behaviors, but it also stimulates fat deposition and has a lightweight pigs are most susceptible to diseases [19, 20], negative effect on feed conversion [12]. In another study, which was confirmed by the results of the present study. a decrease in the growth rate of piglets was observed This observation is especially important in the current sta- only in the days following surgery when it was carried tus of the swine industry, where selection for maximum out shortly after birth (3 days) [16]. These differences in prolificacy has resulted in an increase in litter size and weight gain had disappeared by weaning, as was also ob- more piglets weaned per litter. This rapid increase in litter served in the present study, prompting the conclusion size has resulted in an increase of light-birth-weight pig- that castration does not have long-term implications in lets [21], thus exacerbating the (negative) effects of cas- tration as a critical management parameter. Moreover, in the group of pigs with the heaviest birth weight, even Table 3 Effect of surgical castration on PigMAPa serum if surgical castration did not

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eover, in the group of pigs with the heaviest birth weight, even Table 3 Effect of surgical castration on PigMAPa serum if surgical castration did not result in higher mortality, concentration (mg/ml) at three different study days it compromised growth rates to weaning. This observa- Item Intact Males Castrated Males SEMb P value tion could be associated with stress and discomfort Day 0 0.903 0.841 0.032 0.167 promoted by the castration procedure, affecting milk Day 1 0.847 0.944 0.030 0.025 consumption. As a consequence of both higher mortal- Day 10 0.990 0.902 0.073 0.392 ity rate in the light pigs and poorer growth performance a Pig major acute phase protein in the heavy pigs, surgical castration applied in 3 to b Standard Error of Mean 6 days of age male piglets has a negative impact on Day 0 = sampling before castration, day 1 = 1 day after castration, and day 10 = 10 days after castration in castrated males. In intact male piglets, the health, performance and economic production cost in days correspond to the intervention in their litter mates the suckling period. Morales et al. Porcine Health Management (2017) 3:18 Page 6 of 6 Conclusions 3. Cronin GM, Dunshea FR, Butler KL, McCauly I, Barnett JL, Hemsworth PH. Surgical castration promotes productive losses in the The effects of immune- and surgical castration on the behaviour and consequently growth of group-housed, male finisher pigs. Appl Anim Behav suckling period by causing an increase in pre-weaning Sci. 2010;81:111–26. mortality in pigs born with the lowest body weights, and 4. Rydhmer L, Lundström K, Andersson K. Inmunocastration reduces negatively affects growth rate and weaning body weight aggressive and sexual behaviour in male pigs. Animal. 2010;4:965–72. 5. European Union. Council Directive

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affects growth rate and weaning body weight aggressive and sexual behaviour in male pigs. Animal. 2010;4:965–72. 5. European Union. Council Directive 2008/120/EC of 18 December 2008 in pigs born with highest body weights. Main causes of laying down minimum standards for the protection of pigs. OJ L 47, mortality related to surgical castration were runt pigs, 18.2.2009. meningitis and the surgical and post-surgical complica- 6. European Commission. European Declaration on alternatives to surgical castration of pigs. https://ec.europa.eu/food/sites/food/files/animals/docs/ tions of the castration procedure. aw_prac_farm_pigs_cast-alt_declaration_en.pdf. Accessed 19 May 2017. 7. Hay M, Vulin A, Genin S, Sales P, Prunier A. Assessment of pain induced by Abbreviations castration in piglets: behavioral and physiological responses over the ADG: Average daily gain; BWW: Body weight at weaning; CM: Surgically subsequent 5 days. Appl Anim Behav Sci. 2003;82:201–18. castrated male pigs; IM: Intact male pigs; PigMAP: Pig major acute phase 8. Kluivers-Poodt M, Houx BB, Robben SRM, Koop G, Lambooij E, Hellebrekers protein; PWM: Pre-weaning mortality LJ. Effects of a local anaesthetic and NSAID in castration of piglets, on the acute pain responses, growth and mortality. Animal. 2012;6:1469–75. Acknowledgements 9. Allison J, Pearce M, Brock F, Crane JA. 2010. A comparison of mortality The farmers and their stockmen are greatly acknowledged for agreeing to (animal withdrawal) rates in male fattening pigs reared using either physical engage in the trial and for working in good cooperation with the investigation castration or vaccination with Improvac® as the method to reduce boar team. taint. Proc. 21st IPVS Congress, Vancouver, Canada. July 18-21. 2010, p. 1139. 10. O’Connor

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cination with Improvac® as the method to reduce boar team. taint. Proc. 21st IPVS Congress, Vancouver, Canada. July 18-21. 2010, p. 1139. 10. O’Connor A, Anthony R, Bergamasco L, Coetzee J, Gould S, Johnson AK, Availability of data and material Karriker LA, Marchant-Forde JN, Martineau GS, McKean J, Millman ST, Data are available from the authors upon reasonable request and with Niekamp S, Pajor EA, Rutherford K, Sprague M, Sutherland M, von Borell E, permission of Joaquin Morales (corresponding author). Dzikamunhenga RS. Pain management in the neonatal piglet during routine management procedures. Part 2: Grading the quality of evidence and the Funding strength of recommendations. Anim Health Res Rev. 2014;15:39–62. Zoetis Inc. funded the study. 11. Piñeiro M, Lampreave F, Alava MA. Development and validation of an ELISA for the quantification of pig major acute phase protein (Pig-MAP). Vet Authors’ contributions Immunol Immunop. 2009;127:228–34. JM was investigator of the study and wrote the manuscript; AD monitored 12. Prunier A, Bonneau M, von Borell EH, Cinotti S, Gunn M, Fredriksen B, Giersing the study and participated in the experimental design of the study; AM was M, Morton DB, Tuyttens FAM, Velarde A. A review of the welfare consequences Clinical Research Manager; LF participated in animal manipulations and data of surgical castration in piglets and the evaluation of non-surgical methods. collection; CP participated in the experimental design and in the discussion Anim Welf. 2006;15:277–89. of results; EM performed the statistical study and reviewed the manuscript; 13. Strom I. Arthritis in piglets. Dansk Veterinaertidsskrift. 1996;79:575–7. NW participated in the experimental design, reviewed the manuscript and 14. Lessard M, Taylor AA,

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piglets. Dansk Veterinaertidsskrift. 1996;79:575–7. NW participated in the experimental design, reviewed the manuscript and 14. Lessard M, Taylor AA, Braithwaite L, Weary DM. Humoral and cellular wrote the conclusion. All authors read and approved the final manuscript. immune responses of piglets after castration at different ages. Can J Anim Sci. 2002;82:519–26. Ethics approval and consent to participate 15. Lackner A, Goller K, Ritzmann M, Heinritzi K. 2002. Acute phase proteins in An owner consent was completed by the farmers prior to the enrolment of castration of piglets. Proc. 17th IPVS Congress, Ames, IA, USA. June 2-5. his animals in the study. This study was conducted in compliance with the 2002, Vol 2 p. 253. Good Clinical Practice Guidance Document #85, May 9, 2001 (VICH GL9). 16. Kielly J, Dewey CE, Cochran M. Castration at 3 days of age temporarily slows Animal care and experimental procedures used in this study followed growth of pigs. Swine Health Prod. 1999;7:151–3. regulations and guidelines of the Spanish government for the protection of 17. McGlone JJ, Nicholson RI, Hellman JM, Herzog DN. The development of animals used for scientific research (Real Decreto Español 223/88 BOE pain in young pigs associated with castration and attempts to prevent 67: 8509–8511). castration: Induced behavioral changes. J Anim Sci. 1993;71:1441–6. 18. Roy B, Kumar A, Lakhani GP, Jain A. Causes of pre-weaning mortality in Consent for publication India. Schol J Agric Sci. 2014;4:485–93. All authors consent to the publication of the present manuscript. 19. Beaulieu AD, Aalhus JL, Williams N, Patience JF. Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, Competing interests carcass quality, muscle composition, and

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ct of piglet birth weight, birth order, and litter size on subsequent growth performance, Competing interests carcass quality, muscle composition, and eating quality of pork. J Anim Sci. AD and NW are employees from the company sponsor. 2010;88:2767–78. 20. Fix JS, Cassady JP, Holl JW, Herring WO, Cusbertson MS, See MT. Effect of piglets birth weight on survival and quality of commercial market swine. Publisher’s Note Livest Sci. 2010;132:98–106. Springer Nature remains neutral with regard to jurisdictional claims in 21. Bérard J, Kreuzer M, Bee G. Effect of litter size and birth weight on growth, published maps and institutional affiliations. carcass and pork quality, and their relationship to postmortem proteolysis. J Anim Sci. 2008;86:2357–68. Author details 1 PigCHAMP Pro Europa S.L. c, Santa Catalina, 10, Segovia, Spain. 2Zoetis Inc, Hoge Wei 10, 1930 Zaventem, Belgium. 3Teagasc, Pig Development Department, Moorepark, Fermoy, Co Cork, Ireland. Received: 12 April 2017 Accepted: 7 July 2017 References 1. Bonneau M. Use of entire males for pig meat in the European Union. Meat Sci. 1998;49:S257–72. 2. Zamaratskaia G, Squires EJ. Biochemical, nutritional and genetic effects on boar taint in entire male pigs. Animal. 2009;3:1508–21.