Email updates

Keep up to date with the latest news and content from Acta Veterinaria Scandinavica and BioMed Central.

This article is part of the supplement: Prevention of Boar Taint in Pig Production: The 19th Symposium of the Nordic Committee for Veterinary Scientific Cooperation

Open Access Oral presentation

Moving towards taint-free pork – alternatives to surgical castration

Kerstin Lundström* and Galia Zamaratskaia

  • * Corresponding author: Kerstin Lundström

Author Affiliations

Department of Food Science, Swedish University of Agricultural Sciences, Uppsala, Sweden

For all author emails, please log on.

Acta Veterinaria Scandinavica 2006, 48(Suppl 1):S1  doi:10.1186/1751-0147-48-S1-S1


The electronic version of this article is the complete one and can be found online at:


Published:7 August 2006

© 2006 Lundström and Zamaratskaia; licensee BioMed Central Ltd.

Introduction

Surgical castration of entire male pigs is routinely performed to eliminate the risk of boar taint, an off-flavour in heated pork products. Boar taint occurs in some entire male pigs at slaughter weight and is primarily due to high levels of androstenone and/or skatole in pig carcasses. Although castration reduces the levels of both compounds and, therefore, decreases boar taint, this approach is not entirely satisfactory. Entire male pigs compared to castrates have an improved feed conversion and carcass leanness. Additionally, surgical castration is more and more viewed as a profit at the expense of reducing animal health and welfare. Therefore, to prevent boar taint, methods other than castration are desirable. To facilitate the development of such method(s), factors affecting the levels of skatole and androstenone have to be well understood.

Multiple factors regulate the levels of skatole and androstenone in pig carcasses and this subject has been regularly reviewed [1-5]. The purpose of the present mini-review is to update the existing data gathered over the past few years, and highlight selected aspects of the boar taint problem. Further points and suggestions for future research will be proposed.

Factors affecting boar taint

In entire male pigs at slaughter weight, the levels of skatole and androstenone vary considerably. The main factors responsible for these variations are summarised in Figure 1. Physiological factors (rate of synthesis and metabolic clearance, and overall hormonal status) are crucial in the regulation of the levels of both compounds. Genetic and environmental sources for the variation in skatole and androstenone levels have also been identified. The present review will focus on some of these factors.

thumbnailFigure 1. Factors affecting skatole and androstenone in entire male pigs.

Biosynthesis and metabolism

Androstenone is a steroid produced in the Leydig cells of the testis near sexual maturity. The andien-β synthase enzyme system is responsible for the first step of androstenone biosynthesis [6]. Androstenone is metabolised in the liver with the formation of two major metabolites, 3α- and 3β-androstenol [7,8]. Part of the androstenone is transported to the saliva where it serves as a pheromone to stimulate the sexual responses in female pigs. Part of the androstenone is accumulated in the adipose tissue. Androstenone levels are low in blood and tissues of young male pigs and then dramatically increase near sexual maturity [9,1]. In sexually mature pigs, androstenone production primarily depends on the individual ability of the pig to produce [10] and probably metabolise [8] androstenone.

Skatole is produced by bacteria in the large intestine of the pigs from tryptophan. Part of the skatole is excreted with faeces and the residual part is absorbed through the intestinal walls, released to the blood and metabolised in the liver by cytochrome P450 enzymes (CYP450) and aldehyde oxidase [11,12]. Un-metabolised skatole can accumulate in adipose tissue, causing faecal-like odour in the heated meat. The impact of liver metabolism on skatole levels in fat has been well documented [11,13-15]. Pigs with high skatole production and low levels and activities of hepatic CYP450 will accumulate high skatole levels in fat.

Genetics

There is increasing evidence that the levels of both skatole and androstenone show large genetic variation. Genomic regions to harbour QTL for the variation of skatole and androstenone levels in fat have been identified [16]. Recent molecular genetic studies have indicated that genetic polymorphisms in the enzymes involved in skatole metabolism and androstenone production, such as cytochrome P4502A6 [17], thermostable phenol sulphotransferase SULT1A1 [18] and cytochrome b5 [19], might be associated with the risk of boar taint development.

Nutrition

The production of skatole to a great extent depends on the intestinal micro-flora and the availability of the substrate, which may be altered by dietary means. Recent studies have indicated that a reduction in skatole levels in fat may be achieved by using carbohydrate-rich diets, although conflicting results with carbohydrate feeding have also been reported. For example, feeding with sugar beet pulp significantly reduced fat skatole levels in some studies [20,21], whereas other [22] found no effect of sugar beet pulp on skatole levels. Over the last few years interest is growing in the use of raw potato starch (RPS) as a skatole-reducing additive. The inclusion of RPS into the diet repeatedly decreases skatole levels in tissues of boars (fat and plasma, [23]), barrows (fat and plasma, [24]), and gilts (liver, [25]).

There is limited information about the effect of nutrition on androstenone levels. It is generally believed that feeding intensity rather then specific dietary components influences androstenone levels by accelerating puberty. However, our recent study demonstrated that androstenone levels in fat slightly decreased after feeding RPS for 2 weeks, although this decrease did not reach statistical significance. The levels of androstenone in plasma (measured after extraction with ethyl acetate) were significantly lower in the pigs fed RPS. These data offer new challenges. Maybe, increased feeding period with RPS (above 2 weeks) will decrease androstenone in fat below threshold levels.

Effect of surgical castration on androstenone and skatole

The levels of androstenone and skatole are usually undetectable in the fat of castrated male pigs. Surgical castration simply removes the source of androstenone production (and also the production of anabolic hormones); thus, androstenone levels drop rapidly and remain low. The reasons for the reduction of skatole levels in castrated pigs are not well understood. It is likely that testicular steroids are important regulators of either skatole production or metabolism. Claus et al. [2] suggested the role of anabolic hormones in intestinal turnover and thus skatole synthesis. However, recent studies showed that testicular steroids are also involved in the regulation of skatole metabolism. It was shown that pubertal increase in the levels of testosterone, oestrone sulphate and androstenone coincided with decreased activities of CYP2E1 and CYP2A6, the main enzymes of skatole metabolism [26]. The role of androstenone in skatole metabolism was investigated in in vitro studies, and androstenone was recognised as an inhibitor of the skatole-induced CYP2E1expression [27]. Our own results (unpublished) suggested that androstenone might also be involved in skatole metabolism directly through the inhibition of CYP2E1 activity. We also found that oestradiol has an inhibitory effect on the activity of CYP2E1 (unpublished), although the mechanisms by which androstenone and oestradiol influence CYP2E1 are not identical. The close correlation between skatole and oestrone sulphate [28,23] suggested that besides androstenone, oestrogens might be involved in the regulation of skatole levels.

Alternatives to surgical castration and future research

If surgical castration is to be banned, a reliable alternative is needed to reduce the risk of high levels of taint in the carcasses. Some possible alternatives are listed in Table 1. It is not yet possible to be totally confident that any of the alternatives provide a reliable method to produce taint-free pork. The advantages and disadvantages of the alternatives should be cautiously studied before the final decision is made how to prevent boar taint without surgical castration.

Table 1. Some alternatives to surgical castration

Several issues need to be clarified in future research. The elimination of boar taint from the meat of entire male pigs should be achieved without negative effects on other carcass characteristics and economic efficiency. Indeed, slaughter at lower weight might reduce (though incompletely) the risk of tainted carcasses, but is not attractive from an economical point of view. Selection against high androstenone levels might lead to the reduction in anabolic hormone levels and, therefore, negatively affect growth performance and age at puberty [29,30] unless appropriate genetic markers are used. Selection against high skatole levels has not been performed. Any genetic selection would have to be performed with caution in order not to affect overall carcass quality. Additionally, it should be remembered that some genotypes would perform better in certain environments. For example, pigs with high potential to accumulate skatole (genetic component e.g. low skatole metabolism) would not necessarily produce tainted carcasses if the environment would not favour high skatole production.

Additionally, more work needs to be done on the role of other compounds potentially leading to boar taint such as indole, androstenol and phenylbutenone.

Active immunisation against gonadotropin-releasing hormone (GnRH), so called immunocastration, is a potential alternative to surgical castration [31,32]. Besides reduction in boar taint, immunocastration improves meat and carcass characteristics relative to surgical castrates, and reduce male aggressive behaviour relative to entire males. However, the consumer reaction to the products from immunocastrated pigs needs to be investigated.

Finally, solving the "castration problem" also depends on collaborative connections. Building strong research collaboration should be the primary goal for multidisciplinary projects investigating factors affecting boar taint and alternatives to surgical castration.

Other considerations

Animal welfarist's concerns are mainly focused on the negative consequences of surgical castration. However, animal behaviour is a central part of animal welfare. Entire male pigs show a higher frequency of aggressive behaviour compared to castrated males and females [33]. The housing and management of entire male pigs is an issue that should be considered if castration is to be banned.

Conclusion

Nowadays, there is no suitable alternative to surgical castration to produce taint-free pork. More research is needed to clarify the factors involved in the development of boar taint and to find a method to prevent the accumulation of high concentrations of skatole and androstenone in fat.

References

  1. Bonneau M: Compounds responsible for boar taint, with special emphasis on androstenone: a review.

    Livest Prod Sci 1982, 9:687-705. Publisher Full Text OpenURL

  2. Claus R, Weiler U, Herzog A: Physiological aspects of androstenone and skatole formation in the boar-a review with experimental data.

    Meat Sci 1994, 38:289-305. Publisher Full Text OpenURL

  3. Babol J, Squires EJ: Quality of meat from entire male pigs.

    Food Res Int 1995, 28:201-212. Publisher Full Text OpenURL

  4. Bonneau M: Use of entire males for pig meat in the European Union.

    Meat Sci 1998, 49:S257-S272. OpenURL

  5. EFSA: Welfare aspects of the castration of piglets. Scientific Report of the Scientific Panel for Animal Health and Welfare on a request from the Commission related to welfare aspects of the castration of piglets, European Food Safety Authority- AHAW/04-087.

    2004, 100.

  6. Davis SM, Squires EJ: Association of cytochrome b5 with 16-androstene steroid synthesis in the testis and accumulation in the fat of male pigs.

    J Anim Sci 1999, 77:1230-1235. PubMed Abstract | Publisher Full Text OpenURL

  7. Doran E, Whittington FW, Wood JD, McGivan JD: Characterisation of androstenone metabolism in pig liver microsomes.

    Chem Biol Interact 2004, 147:141-149. PubMed Abstract | Publisher Full Text OpenURL

  8. Sinclair PA, Hancock S, Gilmore WJ, Squires EJ: Metabolism of the 16-androstene steroids in primary cultured porcine hepatocytes.

    J Steroid Biochem Mol Biol 2005, 96:79-87. PubMed Abstract | Publisher Full Text OpenURL

  9. Andresen Ø: Concentrations of fat and plasma 5-α-androstenone and plasma testosterone in boars selected for rate of body weight gain and thickness of back fat during growth, sexual maturation and after mating.

    J Repod Fert 1976, 48:51-59. OpenURL

  10. Bonneau M: Effects of age and live weight on fat 5α-androstenone levels in young boars fed two planes of nutrition.

    Reprod Nutr Dev 1987, 27:413-422. PubMed Abstract OpenURL

  11. Diaz GJ, Squires EJ: Metabolism of 3-methylindole by porcine liver microsomes: responsible cytochrome P450 enzymes.

    Toxicol Sci 2000, 55:284-292. PubMed Abstract | Publisher Full Text OpenURL

  12. Diaz GJ, Squires EJ: The role of aldehyde oxidase in the hepatic meatabolism of 3-methylindole in pigs.

    J Food Agric Chem 2000, 48:833-837. Publisher Full Text OpenURL

  13. Babol J, Squires EJ, Lundström K: Hepatic metabolism of skatole in pigs by cytochrome P4502E1.

    J Anim Sci 1998, 76:822-828. PubMed Abstract | Publisher Full Text OpenURL

  14. Babol J, Squires EJ, Lundström K: Relationship between oxidation and conjugation metabolism of skatole in pig liver and concentrations of skatole in fat.

    J Anim Sci 1998, 76:829-838. PubMed Abstract | Publisher Full Text OpenURL

  15. Zamaratskaia G, Squires EJ, Babol J, Andersson HK, Andersson K, Lundström K: Relationship between the activities of cytochromes P4502E1 and P4502A6 and skatole content in fat in entire male pigs fed with and without raw potato starch.

    Livest Prod Sci 2005, 95:83-88. Publisher Full Text OpenURL

  16. Lee GJ, Archibald AL, Law AS, Lloyd S, Wood J, Haley CS: Detection of quantitative trait loci for androstenone, skatole and boar taint in a cross between Large White and Meishan pigs.

    Anim Genet 2005, 36:14-22. PubMed Abstract | Publisher Full Text OpenURL

  17. Lin Z, Lou Y, Squires EJ: Molecular cloning, expression and functional characterization of the cytochrome P450 2A6 gene in pig liver.

    Anim Genet 2004, 35:314-316. PubMed Abstract | Publisher Full Text OpenURL

  18. Lin Z, Lou Y, Squires EJ: Molecular cloning and functional analysis of porcine SULT1A1 gene and its variant: a single mutation SULT1A1 causes a significant decrease in sulfation activity.

    Mamm Genome 2004, 15:218-226. PubMed Abstract | Publisher Full Text OpenURL

  19. Lin Z, Lou Y, Peacock J, Squires EJ: A novel polymorphism in the 5' untranslated region of the porcine cytochrome b5 (CYB5) gene is associated with decreased fat androstenone level.

    Mamm Genome 2005, 16:367-373. PubMed Abstract | Publisher Full Text OpenURL

  20. Jensen MT, Cox RP, Jensen BB: Microbial production of skatole in the hind gut of pigs given different diets and its relation to skatole deposition in backfat.

    Anim Sci 1995, 61:293-304. OpenURL

  21. Whittington FM, Nute GR, Hughes SI, McGivan JD, Lean IJ, Wood JD, Doran E: Relationships between skatole and androstenone accumulation, and cytochrome P4502E1 expression in Meishan×Large White pigs.

    Meat Sci 2004, 67:569-576. Publisher Full Text OpenURL

  22. Van Oeckel MJ, Warnants N, De Paepe M, Casteels M, Boucqué ChV: Effect of fibre-rich diets on the backfat skatole content of entire male pigs.

    Livest Prod Sci 1998, 56:173-180. Publisher Full Text OpenURL

  23. Zamaratskaia G, Babol J, Andersson HK, Andersson K, Lundström K: Effect of live weight and dietary supplement of raw potato starch on the levels of skatole, androstenone, testosterone and oestrone sulphate in entire male pigs.

    Livest Prod Sci 2005, 93:235-243. Publisher Full Text OpenURL

  24. Claus R, Lösel D, Lacorn M, Mentschel J, Schenkel H: Effects of butyrate on apoptosis in the pig colon and its consequences for skatole formation and tissue accumulation.

    J Anim Sci 2003, 81:239-248. PubMed Abstract | Publisher Full Text OpenURL

  25. Zamaratskaia G, Chen G, Lundström K: Effects of sex, weight, diet and hCG administration on levels of skatole and indole in the liver and hepatic activities of cytochromes P4502E1 and P4502A6 in pigs.

    Meat Sci 2005, in press. OpenURL

  26. Zamaratskaia G: Factors involved in the development of boar taint. Doctoral Thesis, Swedish University of Agricultural Sciences, Uppsala; 2004. PubMed Abstract | Publisher Full Text OpenURL

  27. Doran E, Whittington FW, Wood JD, McGivan JD: Cytochrome P450IIE1 (CYP2E1) is induced by skatole and this induction is blocked by androstenone in isolated pig hepatocytes.

    Chem Biol Interact 2002, 140:81-92. PubMed Abstract | Publisher Full Text OpenURL

  28. Babol J, Squires EJ, Lundström K: Relationship between metabolism of androstenone and skatole in intact male pigs.

    J Anim Sci 1999, 77:84-92. PubMed Abstract | Publisher Full Text OpenURL

  29. Willeke H, Pirchner F: Selection for high and low level of 5-androst-16-en-3- one in boars. II. Correlations between growth traits and 5-androstenone.

    J Anim Breed Genet 1989, 106:312-317. OpenURL

  30. Sellier P, Le Roy P, Fouilloux MN, Gruand J, Bonneau M: Responses to restricted index selection and genetic parameters for fat androstenone level and sexual maturity status of young boars.

    Livest Prod Sci 2000, 63:265-274. Publisher Full Text OpenURL

  31. Bonneau M, Dufour R, Chouvet C, Roulet C, Meadus W, Squires EJ: The effects of immunization against luteinizing hormone-releasing hormone on performance, sexual development, and levels of boar taint-related compounds in intact male pigs.

    J Anim Sci 1994, 72:14-20. PubMed Abstract | Publisher Full Text OpenURL

  32. Dunshea FR, Colantoni C, Howard K, McCauley I, Jackson P, Long KA, Lopaticki S, Nugent EA, Simons JA, Walker J, Hennessy DP: Vaccination of boars with a GnRH vaccine (Improvac) eliminates boar taint and increases growth performance.

    J Anim Sci 2001, 79:2524-2535. PubMed Abstract | Publisher Full Text OpenURL

  33. Cronin GM, Dunshea FR, Butler KL, McCauley I, Barnett JL, Hemsworth PH: The effects of immuno- and surgical-castration on the behaviour and consequently growth of group-housed, male finisher pigs.

    Appl Anim Behav Sci 2003, 81:111-126. Publisher Full Text OpenURL

  34. Mortensen AB, Sørensen SE: Relationship between boar taint and skatole determined with a new analytical method.

    Proceedings of the European Meeting of Meat Research Workers 1984, 30:394-396. OpenURL

  35. Squires EJ: Studies on the suitability of a colorimetric test for androst-16-ene steroids in the submaxillary gland and fat of pigs as a simple chemical test for boar taint.

    Can J Anim Sci 1990, 70:1029-1040. OpenURL

  36. Annor-Frempong IE, Nute GR, Wood JD, Whittington FW, West A: The measurement of the responses to different odour intensities of 'boar taint' using a sensory panel and an electronic nose.

    Meat Sci 1998, 50:139-151. Publisher Full Text OpenURL

  37. Aldal I, Andresen Ø, Egeli AK, Haugen J.-E, Grødum A, Fjetland O, Eikaas JLH: Levels of androstenone and skatole and the occurrence of boar taint in fat from young boars.

    Livest Prod Sci 2005, 95:121-129. Publisher Full Text OpenURL

  38. Rideout TC, Fan MZ, Cant JP, Wagner-Riddle C, Stonehouse P: Excretion of major odor-causing and acidifying compounds in response to dietary supplementation of chicory inulin in growing pigs.

    J Anim Sci 2004, 82:678-684. OpenURL

  39. Johnson LA: Sexing mammalian sperm for production of offspring: the state-of-the-art.

    Anim Reprod Sci 2000, 60–61:93-107. Publisher Full Text OpenURL