A comparison of the carcase characteristics of pigs immunized with a ‘gonadotrophin-releasing factor (GnRF)’ vaccine against boar taint with physically castrated pigs

A comparison of the carcase characteristics of pigs immunized with a ‘gonadotrophin-releasing factor (GnRF)’ vaccine against boar taint with physically castrated pigs

Meat Science 83 (2009) 702–705 Contents lists available at ScienceDirect Meat Science journal homepage: www.elsevier.com/locate/meatsci A compariso...

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Meat Science 83 (2009) 702–705

Contents lists available at ScienceDirect

Meat Science journal homepage: www.elsevier.com/locate/meatsci

A comparison of the carcase characteristics of pigs immunized with a ‘gonadotrophin-releasing factor (GnRF)’ vaccine against boar taint with physically castrated pigs Thilo Fuchs a, Heiko Nathues a, Annika Koehrmann b, Stuart Andrews c, Fiona Brock c, Nadine Sudhaus d, Guenter Klein d, Elisabeth grosse Beilage a,* a

Field Station for Epidemiology, University of Veterinary Medicine Hannover, Buescheler Str. 9, D-49456 Bakum, Germany Pfizer Animal Health, Pfizerstraße 1, D-76139 Karlsruhe, Germany c Pfizer Animal Health, Ramsgate Road, Sandwich, Kent, CT13 9NJ, UK d Institute for Food Quality and Food Safety, University of Veterinary Medicine Hannover, Bischofsholer Damm 15, D-30173 Hannover, Germany b

a r t i c l e

i n f o

Article history: Received 11 November 2008 Received in revised form 15 July 2009 Accepted 3 August 2009

Keywords: Pigs Castration GnRF vaccine Carcase traits Lean meat percentage Vaccination Boar taint

a b s t r a c t Evaluating the effect of using a GnRF vaccine against boar taint on the carcase characteristics of boars, vaccinated pigs were compared with physically castrated. In total, 554 male pigs were randomly assigned to treatment groups. T01 comprised physically castrated pigs in the first week of life, T02 comprised pigs vaccinated twice before slaughtering. There was neither significant difference between the groups in terms of average liveweight nor in the hot carcase weight. The mean dressing percentage was 1.5% higher for T01 than for T02 (P < 0.0001). The lean meat percentage was significantly higher in T02 (P < 0.0001). Backfat and backmuscle thickness were significantly higher in T01 (P < 0.0001 and P = 0.0099, respectively). Within the EUROP grading vaccinated pigs were in favour (P = 0.0034). There were no significant differences using the AutoFOM system: weights of the boned ham, boned shoulder and loin (P = 0.5102, P = 0.8881 and P = 0.1919, respectively). The weight of the belly was significantly higher (P = 0.0042) in T01 while the lean meat percentage of belly was significantly higher (P < 0.0001) in T02. Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction Entire male pigs are known to be superior to physical castrates with regards to lean meat production and growth performance, which could lead to more profitable pig production (Bussen et al., 1997; Dunshea et al., 2001; Turkstra et al., 2002). Nevertheless, physical castration of male pigs is still a common procedure in many countries of the European Union (EU) and worldwide. Every year an estimated 100 million pigs are physically castrated in the then 25 countries of the EU (Thun, 2006). The reason for castration is primarily to prevent sexually mature boars developing an unpleasant taste and flavor of the meat. This so-called boar taint is mainly caused by the two lipophilic substances androstenone and skatole. Androstenone is a steroid produced in the testicles for which production starts in the young piglet (Booth, 1975) and rises to maximal levels during puberty (Zamaratskaia, Babol, Madej, Squires, & Lundström, 2004). It is perceived as a characteristic and unpleasant smell of urine or sweat by

* Corresponding author. Tel.: +49 4446 9599115; fax: +49 4446 9599112. E-mail address: [email protected] (E. grosse Beilage). 0309-1740/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2009.08.007

those individuals who are sensitive to it. Skatole is a bacterial breakdown product of tryptophan that is reabsorbed from the colon and causes a faecal smell of the meat (Claus, Loesel, Lacorn, Mentschel, & Schenkel, 2003). Its production also rises during puberty (Babol, Zamaratskaia, Juneja, & Lundström, 2004; Zamaratskaia et al., 2004). The reasons for lower skatole levels in sows and castrates are not fully understood but the higher production of skatole in the gut as well as lower metabolism of skatole in the liver of boars are two theories which are discussed (Babol, Squires, & Lundström, 1999; Claus et al., 2003). A few countries have stopped the castration of piglets completely, for example, the United Kingdom and Ireland, or, in parts, for example (about 70%) Spain and Portugal. In these countries pigs are usually slaughtered shortly after reaching puberty but before sexual maturity to prevent tainted meat (Walstra et al., 1999). Slaughtering of younger pigs produces a smaller carcase with a higher concentration of unsaturated fats that are not suitable for producing special meat products. Dry-cured ham and loin, for example, require large pieces of meat with abundant fat for processing. The presence of boar taint in meat, often detected when meat is heated during cooking, reduces the value of slaughtering sexually mature boars. In processed meat, boar taint is less

T. Fuchs et al. / Meat Science 83 (2009) 702–705

pronounced and therefore better tolerated by the consumers (Banon, Costa, Gil, & Garrido, 2003). In recent years, a GnRF vaccine has been introduced in several countries. It acts via the hypothalamic-pituitary-gonad axis and suppresses testicular function through the induction of antibodies against GnRF (Zamaratskaia et al., 2008). As the main effect of this vaccination occurs after the second dose of vaccine, administered four to six weeks before slaughtering, the positive characteristics of boars in growth performance should be maintained for most of the fattening period. The main objective of this study was to investigate the carcase characteristics of pigs immunized with a GnRF vaccine compared with physically castrated pigs. Pigs were raised under field conditions in a conventionally managed farm in Germany. 2. Material and methods 2.1. Inclusion/exclusion criteria All piglets were clinically examined before enrolment onto the study. All healthy male piglets, born within one week, from a single group of farrowing sows were included. Cryptorchids, piglets with inguinal hernia or piglets which were not deemed healthy were excluded. 2.2. Animals and management A group of 554 terminal crossbred male pigs was used for this study. The maternal line was a homozygote stress gene (hal) negative three-way crossbred with Large White, Landrace and Piétrain genetics. The paternal line was a heterozygote stress gene (hal) positive Piétrain breed. Pigs were randomly allocated to study groups in the first week of life in accordance with a random treatment allocation plan produced; this was day 0 of the study. The study groups consisted of one group of 274 pigs that were physically castrated during the first week of life (T01) and one group of 280 piglets that would later be vaccinated with a GnRF vaccine (T02). The pigs were examined daily by farm personnel and weekly by the Examining Veterinarian (Fuchs). In case of necessary medical intervention, the reason and type of treatment were recorded. Necropsies were performed on all pigs that died during the study to ascertain the cause of death. Pigs that had to be moved to single pens for animal welfare reasons were removed from the study without necropsy. 2.3. Distribution of pigs to pens within the fattening units, and mortalities On day 88 when pigs were 13–14 weeks old, the 252 pigs of group T01 and 258 pigs of group T02 (the numbers then remaining in both groups) were moved into a fattening barn of 32 pens, divided into two units with 16 pens either side of a central corridor. The two treatment groups were randomly allocated to the pens with five pens per unit for T01 and five pens per unit for T02 with a maximum of 26 pigs per pen. The difference in the number of pigs in the groups from the start of the study to slaughtering is due either to animals being removed from the study for animal welfare reasons or due to mortalities. 2.4. Environment In the fattening unit each pen had a floor space of 20 m2, a 1.5 m long feeder and one nipple waterer. The slatted floor was made of concrete. Fresh air was provided by a perforated channel under the ceiling.

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2.5. Feeding regime Four different diets were fed throughout the fattening period, switching to the second, third and fourth diets in the 15th, 17th and 20th week of the pigs’ life respectively. The pigs received the first diet with 13.4 NEv (MJ)/kg and 1.05% lysine, the second with 13.2 NEv (MJ)/kg and 1.0% lysine, the third with 13.0 NEv (MJ)/kk and 0.95% lysine and the fourth diet with 12.9 NEv (MJ)/kg and 0.92% lysine. The feed was offered with water in a ratio of 1:3. The feeders in the pens were equipped with sensors, which recognize if the feeder was empty or filled. New feed was only offered if the feeder was empty. From the 13th to 17th week of the pigs’ life the time between feedings was 1 h, from the 18th week onwards the time between feedings was 2 h. The first feeding in the morning was at 6 am, the last at 10 pm and the feedings were only carried out in those pens where the sensor reported an empty feeder.

2.6. Treatments The pigs in treatment group T02 were vaccinated twice with 2.0 ml of Improvac (commercial formulation), Pfizer Animal Health. This vaccine comprises of a synthetic, incomplete analogue of natural gonadotrophin-releasing factor (GnRF) which is conjugated to a carrier protein. The first vaccination was administered when the pigs were moved into the fattening unit on study day 88 at 13–14 weeks of age. The second vaccination was administered on day 135, when the pigs were 20–21 weeks of age, four weeks before the first pigs were expected to be slaughtered. On each occasion, vaccine was administered subcutaneously in the upper neck region using sterile standard needle (TerumoTM, 19G  1’’) and 2 ml sterile syringe. The pigs of group T01 were not injected with placebo, because the purpose of the study was to measure the effect of the vaccination procedure versus physically castrated pigs, corresponding to the current practice.

2.7. Carcase characteristics All pigs were weighed individually three days before slaughter of the first batch of pigs in the 24th week (the cut-off date, day 160). Those animals which were slaughtered in the second batch were additionally weighed four days before slaughter in the 26th week (day 173). All pigs of groups T01 and T02 that weighed 110 kg or more on day 160 were slaughtered in the first batch. Overall, 242 pigs met these criteria. The remaining 241 pigs were slaughtered in the 26th week. The pigs were transported to a commercial EU approved abattoir and slaughtered according to the European regulations for commercial slaughterhouses (Anonymous, 2004). At slaughter, testes were removed from each carcase and hot carcase weight determined. Lean meat percentage was measured using the Hennessy grading probe which is commonly used at German slaughterhouses, and calculated with the formula: lean meat (%) = 58.6688 0.82809  (S) + 0.18306  (F). The thickness (mm) of backfat (S) and backmuscle (F) was measured on the halved carcase, about 7 cm lateral of the division on the level of the second/ third last rib. The boned ham, boned shoulder, loin and belly weights alongside the lean meat percentage of belly were measured with the AutoFOM ultrasound system. Carcases were categorised, using the EUROP* grading system based on the lean meat percentage: >55% lean meat were rated E, 50–54.9% lean meat were categorised as U and 45–49.9% were rated R (*In some other countries a SEUROP grading system is used, where the carcases with a lean meat percentage greater than 60% are rated S).

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2.8. Good clinical practice (veterinary) The entire study was run in compliance with the standards of ‘good clinical practice’ (Anonymous, 2000). Housing and management of animals were based on the rules of ‘good farming practice’. In addition, the present study was performed under license for experimenting on animals from the German Federal State Veterinary Administration Office (LAVES, Oldenburg, License No. 23.1– 41401/4).

were significantly thicker in physically castrated pigs. The belly weight, as calculated by AutoFOM, was significantly higher (P = 0.0042) in physically castrated pigs while the lean meat percentage of belly was significantly higher (P < 0.0001) in vaccinated pigs. No statistically significant differences were detected in the weight of either the boned ham or the boned shoulder, which were both heavier in vaccinated pigs and the weight of the loin, which was heavier in physically castrated pigs (Table 2). 3.3. Carcase classification

2.9. Statistical analyses Data were analysed using SAS (SAS Institute, Cary, NC, USA). The effect of treatment on the carcase variables of back fat, back muscle, belly percentage and weight, carcase weight, ham (boned), lean meat, loin, shoulder (boned) and dressing percentage was evaluated using linear mixed models, with treatment as a fixed effect and random effects for fattening pen, and fattening pen within fattening block. The dressing percentage, defined as 100 carcase weight divided by slaughter weight, was summarised by animal and analysed with a linear mixed model with treatment as fixed effect and random effects for fattening block and fattening pen within fattening block. Treatment group differences with the EUROP carcase classification were analysed with a Fisher’s exact test. 3. Results 3.1. Live bodyweight, carcase weight and dressing percentage Before the first (cut-off date) and before the second slaughtering day the average liveweight of the physically castrated pigs (group T01) was higher, but not significantly different, than the vaccinated pigs (group T02). Average carcase weight of the physically castrated pigs was higher than the vaccinated pigs, but again not statistically significantly different (Table 1). The dressing percentage was 79.4% (95% CI 79.0–79.7) for the physically castrated pigs and 77.9% (95% CI 77.5–78.2) for the vaccinated pigs (P < 0.0001). 3.2. Carcase traits The lean meat percentage was statistically significantly higher in vaccinated pigs than in the physically castrated pigs (P < 0.0001). The backfat (P < 0.0001) and backmuscle (P = 0.0099)

Within the EUROP grading the 242 carcases of the physically castrated pigs were rated as follows: 87 (36%) graded E, 133 (55%) graded U and 22 (9%) graded R. In comparison, the 240 carcases of the vaccinated pigs were rated as follows: 118 (49%) graded E, 113 (47%) graded U and 9 (4%) graded R. The differences were statistically significant in favour of the carcases from the vaccinated pigs (P = 0.0034) (Table 3). 4. Discussion In this study differences in carcase characteristics between physically castrated pigs and vaccinated pigs were evaluated. There were no statistically significant differences between the physically castrated pigs and those immunized with a GnRF vaccine in terms of either the average live bodyweight of pigs before first or second slaughtering day (P = 0.0648; P = 0.6999, respectively), or the carcase weights after slaughtering (both batches combined, P = 0.0682). The dressing percentage of the carcases of the vaccinated pigs was significantly lower (P < 0.0001) compared with those from the physically castrated pigs in this study. Dunshea et al. (2001) also reported higher dressing percentages in physically castrated pigs compared with either vaccinated pigs or boars. No sex-related differences in dressing percentage were observed by Hansson, Lundström, and Malmfors (1975). Andersson et al. (1997) suggested the additional weight of genitalia as a possible reason for the lower dressing percentage in entire male pigs. Differences in feed intake and gut fill between vaccinated boars and entire males were given as possible reasons by Dunshea et al. (2001). Using the formula of the Hennessy grading probe, the various results for each carcase trait examined were calculated. As the overall carcase composition is typically different between gilts, castrates and boars, the use of this formula can produce different

Table 1 Effect of immunization with a GnRF vaccine on average liveweight and carcase weight. Physical castrates (T01)

Liveweight, 24th week (kg) Liveweight, 26th week (kg) Carcase weight (kg)

GnRF vaccinates (T02)

P-value

LS mean

SE

95% CI

LS mean

SE

95% CI

110.2 120.7 91.5

0.97 1.00 0.62

108.3–112.2 118.7–122.7 90.2–92.8

107.6 121.3 89.8

1.01 1.07 0.62

105.6–109.6 119.2–123.4 88.5–91.1

0.0648 0.6999 0.0682

Table 2 Effect of immunization with a GnRF vaccine on carcase parameters. Physical castrates (T01)

Back fat (mm) Back muscle (mm) Lean meat (%) Belly (kg) Belly, lean meat (%) Ham, boned (kg) Loin (kg) Shoulder, boned (kg)

GnRF vaccinates (T02)

P-value

LS mean

SE

95% CI

LS mean

SE

95% CI

17.3 64.9 53.8 14.6 50.5 17.2 6.8 7.9

0.19 0.30 0.19 0.11 0.29 0.13 0.06 0.05

16.9–17.7 64.3–65.5 53.2–54.4 14.4–14.9 49.9–51.2 16.9–17.4 6.7–6.9 7.7–8.0

15.6 63.8 54.8 14.1 52.6 17.3 6.7 7.9

0.20 0.30 0.19 0.11 0.29 0.13 0.06 0.05

15.2–16.0 63.2–64.4 54.2–55.4 13.9–14.3 52.0–53.2 17.0–17.6 6.5–6.8 7.8–8.0

<0.0001 0.0099 <0.0001 0.0042 <0.0001 0.5102 0.1919 0.8881

T. Fuchs et al. / Meat Science 83 (2009) 702–705 Table 3 Effect of immunization with a GnRF vaccine on EUROP grading of carcase; number of pigs (%). Grading

Physical castrates (T01)

GnRF vaccinates (T02)

E U R O P

87 (36%) 133 (55%) 22 (9%) – –

118 (49%) 113 (47%) 9 (4%) – –

Lean meat percentage of carcase E: >55%; U: 50–54.9%; R: 45–49.9%; O: 40–44.9%; P: <40%.

results compared to the use of manual dissection. If a carcase is dissected manually, more exact values of the lean meat content can be determined. The lean meat percentage measured commercially by using the Hennessy grading probe revealed statistically significantly higher values in vaccinated pigs compared with physically castrated pigs (P < 0.0001). In contrast, this method used in a study of Zamaratskaia et al. (2008) revealed no statistically significant differences for the lean meat percentage in vaccinated compared with physically castrated pigs. However, in the same study a significantly higher lean meat percentage in the vaccinated pigs could be confirmed when it was estimated by partial dissection of the carcase instead of using the Hennessy grading probe. Commercial grading also underestimated the lean meat percentage of entire male pigs in studies of Andersson, Hansson, Lundström, and Karlsson (1995) and Andersson et al. (1997). According to the overall lean meat content, the lean meat percentage in the belly was significantly higher (P < 0.0001) in the vaccinated pigs compared with the physically castrated pigs. The back fat thickness of vaccinated pigs was significantly lower than that of physically castrated pigs (P < 0.0001) which compares to results of Hennessy, Bernal, and Hodge (2006) and Dunshea et al. (2001). Surprisingly, the back muscle thickness was also significantly lower in vaccinated than in physically castrated pigs (P = 0.0099). The rating of the different carcase parts using the AutoFOM system shows that there were no significant differences with exception of the weight of the belly. This was significantly higher in physically castrated pigs than in vaccinated pigs (P = 0.0042). Loin, ham and shoulder were nearly equal in weight, albeit the carcases of the vaccinated pigs where lighter. To our knowledge, this is the first time that data comparing AutoFOM results of vaccinated with physically castrated pigs have been published. The results of the AutoFOM rating are also reflected in the EUROP carcase grading. More vaccinated pigs were rated in the best category E (49%) compared to the physically castrated pigs (36%). The grading differences between the groups were significant (P = 0.0034). 5. Conclusions Immunization with a GnRF vaccine improves lean meat content, EUROP grading score and reduces backfat thickness. Despite a lower dressing percentage, no adverse effects on the weights of valuable parts of the carcase as ham, loin and shoulder could be detected; that was with the exception of a lower belly weight and a lower back muscle thickness. The use of a GnRF vaccine to control boar taint could contribute to producing pigs with leaner and more muscular carcasses. Conflict of interest statement Dr. Annika Koehrmann, Dr. Stuart Andrews and Fiona Brock were in charge of this study as employees of Pfizer Animal Health

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and acted as Study Monitor and Sponsor Representative/Assistant Study Monitor and Biometrician, respectively. The other authors have no financial or personal relationship with Pfizer or other people or organisations that could inappropriately influence or bias the content of the paper. The study was approved by the Ethical Review Committee of Pfizer Animal Health, UK. Acknowledgment The authors thank Pfizer Animal Health for financial support of this study and also acknowledge the assistance of Nicola Clamp and Aidan Shanks of PAH with data management and the staff of the Field Station for Epidemiology, University of Veterinary Medicine Hannover for their assistance in animal handling and the collection of samples. References Andersson, K., Hansson, I., Lundström, K., & Karlsson, A. (1995). Influence of sex and breed on the precision of the official Swedish pig carcase grading. Swedish Journal of Agricultural Research, 25, 51–59. Anonymous (2000). Guideline on good clinical practices. VICH Topic GL9. London: The European Agency for the Evaluation of Medicinal Products. Anonymous (2004). Regulation (EC) No 853/2004 of the European Parliament and of the council of 29 April 2004 laying down specific hygiene rules for on the hygiene of foodstuffs. (Official Journal of the EU, L139 Vol. 47). Babol, J., Squires, E. J., & Lundström, K. (1999). Relationship between metabolism of androstenone and skatole in intact male pigs. Journal of Animal Science, 77, 84–92. Babol, J., Zamaratskaia, G., Juneja, R. K., & Lundström, K. (2004). The effect of age on distribution of skatole and indole levels in entire male pigs in four breeds: Yorkshire, Landrace, Hampshire and Duroc. Meat Science, 67(2), 351–358. Banon, S., Costa, E., Gil, M. D., & Garrido, M. D. (2003). A comparative study of boar taint in cooked and dry-cured meat. Meat Science, 63, 389–395. Booth, W. D. (1975). Changes with age in the occurence of C 19 steroids in the testis and submaxillary gland of the boar. Journal of Reproduction and Fertility, 42(3), 459–472. Bussen, S. S., Steck, T., Andersson, K., Schaub, A., Andersson, K., Lundstroem, K., Thomke, S., & Hansson, I. (1997). The effects of feeding system, lysine levels and gilt contact on performance, skatole levels and economy of entire male pigs. Livestock Production Science, 51, 131–140. Claus, R., Loesel, D., Lacorn, M., Mentschel, J., & Schenkel, H. (2003). Effects of butyrate on apoptosis in the pig colon and its consequences for skatole formation and tissue accumulation. Journal of Animal Science, 81, 239– 248. Dunshea, F. R., Colantoni, C., Howard, K., McCauley, I., Jackson, P., Long, K. A., et al. (2001). Vaccination of boars with a GnRH vaccine (Improvac) eliminates boar taint and increases growth performance. Journal of Animal Science, 79, 2524–2535. Hansson, I., Lundström, K., & Malmfors, B. (1975). Effect of sex and weight on growth, feed efficiency and carcase characteristics of pigs. 2. Carcase characteristics of boars, barrows and gilts, slaughtered at four different weights. Swedish Journal of Agricultural Research, 5, 69–80. Hennessy, D. P., Bernal, G., & Hodge, A. (2006). Growth performance and carcase quality in male pigs given the boar taint vaccine ImprovacÒ compared to physical castrates. In Proceedings of the 19th IPVS congress, 16–19 July 2006, Copenhagen, Denmark. O.62-04 (Vol. 1), side 292. Thun, R. (2006). Kastration oder keine Kastration: Ein Tierschutz- und Produktionsaspekt. Pfizer symposium, symposium proceedings of the 19th IPVS congress 16–19 July 2006, Copenhagen, Denmark (pp. 3–7). Turkstra, J. A., Zeng, X. Y., van Diepen, J. T. M., Jongbloed, A. W., Oonk, H. B., van de Weil, D. F. M., et al. (2002). Performance of male pigs immunized against GnRH is related to the time of onset of biological response. Journal of Animal Science, 80, 2953–2959. Walstra, P., Claudi-Magnussen, C., Chevillon, P., von Seth, G., Diestre, A., Matthews, K. R., et al. (1999). An international study on the importance of androstenone and skatole for boar taint: Levels of androstenone and skatole by country and season. Livestock Production Science, 62, 15–28. Zamaratskaia, G., Babol, J., Madej, A., Squires, E. J., & Lundström, K. (2004). Age related variation of plasma concentrations of skatole, androstenone, testosterone, oestradiol-17b, oestrone sulphate, dehydroepiandrostenone sulphate, triiodothyronine and IGF-1 in six entire male pigs. Reproduction in Domestic Animals, 39, 168–172. Zamaratskaia, G., Andersson, H. K., Chen, G., Andersson, K., Madej, A., & Lundström, K. (2008). Effect of a gonadotrophin-releasing hormone vaccine (ImprovacTM) on steroid hormones, boar taint compounds and performance in entire male pigs. Reproduction in Domestic Animals, 43(3), 351–359.