Plasma skatole and androstenone levels in entire male pigs and relationship between boar taint compounds, sex steroids and thyroxine at various ages

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Abstract

The objectives of the study were to investigate the age-associated variations of plasma skatole and androstenone levels and their relationship to testosterone, estrone sulphate and thyroxine in plasma from entire male pigs. Effect of photoperiod on boar taint compounds in plasma was also investigated. In total, 47 uncastrated crossbred male pigs, siblings from 13 litters, were divided into three groups: Control group (natural photoperiod), Spring/Summer group (artificial spring conditions) and Autumn/Winter group (artificial autumn conditions). Blood samples were collected every 2 weeks at the average age from 8 weeks until slaughter at the age of 20–24 weeks. Neither skatole nor androstenone levels in plasma were affected by photoperiod. Skatole concentrations in plasma varied with age and were high at the age of 8–10 weeks. The early increase of skatole levels related to no other investigated compounds. At the older age, skatole levels in plasma were positively correlated to androstenone (r=0.30; 20 weeks of age), testosterone and estrone sulphate levels (r=0.43 and 0.54, respectively; 22 weeks of age) and negatively to thyroxine levels (r=−0.44; 22 weeks of age, and r=−0.72; 24 weeks of age). Plasma androstenone levels were positively correlated to levels of testosterone and estrone sulphate from approximately 14 to 24 weeks of age, not at younger age, with correlation coefficients ranging from 0.34 to 0.79. Negative correlations between androstenone and thyroxine levels in plasma were found at the ages of 16, 18 and 20 weeks (r=−0.42, −0.35 and −0.30, respectively). Skatole and androstenone levels in fat at slaughter, 20–24 weeks of age, were highly correlated (r=0.68; P<0.001).

Introduction

An unpleasant odour in heated pork, called boar taint, is caused principally by the presence of androstenone (5-alpha-androst-16-en-3-one) and skatole (3-methylindole) in the adipose tissue from some entire male pigs. The threshold levels of androstenone and skatole in fat are suggested to be from 0.5 to 1 μg/g and from 0.20 to 0.25 μg/g, respectively. Androstenone is synthesised in the testicles and skatole is produced from the amino acid tryptophan in the large intestine of pigs. Both compounds are metabolised in the liver. Androstenone levels increase at puberty in parallel with other testicular steroids; besides, the amount of expressed androstenone in fat is genetically regulated Bonneau, 1982, Sellier et al., 2000, Quintanilla et al., 2003. Skatole levels depend on genetic factors Lundström et al., 1994, Pedersen, 1998, feeding system (Jensen and Jensen, 1997), environmental conditions (Walstra et al., 1999) and the activity of liver enzymes involved in skatole metabolism Babol et al., 1998, Diaz and Squires, 2000. Factors involved in intestine development, such as IGF-1 or thyroid hormones, might be important for skatole production (Claus and Raab, 1999). Skatole levels vary with age Zamaratskaia et al., 2001, Babol et al., 2003 although the nature of these variations remains unknown. Skatole levels seem to increase at the age close to puberty (Babol et al., 2003) possibly as a result of an involvement of sex steroids in the regulation of skatole metabolism in the liver (Babol et al., 1999). Neither female nor castrated male pigs exhibit fat skatole in increased amounts, which also suggests that testicular steroids affect skatole levels.

Thyroid hormones are involved in puberty onset by affecting testis development (Cooke, 1996). Specific nuclear binding sites for thyroid hormones have been found in testis (Palmero et al., 1995). Thus, thyroid hormones might also affect variations of skatole and androstenone levels at puberty through affecting testicular functions.

Claus and Weiler (1985) suggested that puberty onset is related to photoperiod. The seasonal variations in the levels of androstenone and skatole Claus et al., 1983, Walstra et al., 1999 might also be explained by maturity related factors. Andersson et al. (1998b) have shown an effect of day length on off-odour expression in fat from male pigs at slaughter age, as evaluated by sensory methods.

The aims of the present study were to investigate the relationships between skatole, androstenone, testosterone, estrone sulphate and thyroxine in entire male pigs at various ages. The effect of day length on skatole and androstenone levels in plasma was also investigated.

Section snippets

Animals and sample collection

In total, 47 entire male pigs (Yorkshire×Hampshire), siblings from 13 litters, were included in this study. The pigs were part of a project on photoperiodic effects on pubertal maturation in crossbred boars (Andersson et al., 1998b). Details of treatments and animal handling are given in Andersson et al. (1998b). Briefly, siblings were randomly divided into groups with three lighting-controlled treatments: Control group, Spring/Summer group and Autumn/Winter group. The Control group was exposed

Results

Light regime affected neither skatole nor androstenone levels in plasma (P=0.12 and 0.42, respectively).

The mean concentrations of all investigated compounds at young (from 8 to 10 weeks), prepubertal (from 12 to 18 weeks) and slaughter (from 20 to 24 weeks) ages are given in Table 1. Plasma skatole levels varied with age (P<0.001) and were high at young age and significantly decreased between 10 and 12 weeks of age (P<0.001; Fig. 1; Table 1). At older age, the levels of skatole increased after

Discussion

In this study plasma concentrations of skatole were measured by a simplified HPLC method, after deproteinising the samples with an equal volume of acetonitrile. Since this method requires few manipulations during sample preparation and does not require the use of diethylether, which is a potential fire hazard, it may be useful in the routine laboratory setting.

Neither skatole nor androstenone levels in fat were significantly affected by photoperiod in the present study. Photoperiod was

Conclusions

Light regime affected neither skatole nor androstenone levels in plasma. Androstenone levels in plasma increased simultaneously with plasma levels of testosterone and estrone sulphate as puberty development progressed. Levels of skatole in plasma from some boars reached high values at young age, 8 and 10 weeks. This increase of skatole levels was related to no other investigated compounds. Further studies on the age-related changes in skatole levels are needed to determine the nature of skatole

References (41)

  • K Lundström et al.

    Skatole, androstenone and taint in boars fed two different diets

    Livest Prod. Sci.

    (1988)
  • K Lundström et al.

    Skatole levels in pigs selected for high lean tissue growth rate on different dietary protein levels

    Livest Prod. Sci.

    (1994)
  • P Sellier et al.

    Responses to restricted index selection and genetic parameters for fat androstenone level and sexual maturity status of young boars

    Livest Prod. Sci.

    (2000)
  • P Walstra et al.

    An international study on the importance of androstenone and skatole for boar taint: levels of androstenone and skatole by country and season

    Livest Prod. Sci.

    (1999)
  • J.L Xue et al.

    Comparison of the accuracies of chemical and sensory tests for detecting taint in pork

    Livest Prod. Sci.

    (1996)
  • N Agergaard et al.

    Absorption of skatole to portal vein blood and liver turnover in entire male pigs using an in vivo animal model

  • Ø Andresen

    Concentrations of fat and plasma 5alpha-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. Reprod. Fertil.

    (1976)
  • J Babol et al.

    Investigation of factors responsible for the development of boar taint

    Food Res. Int.

    (1996)
  • J Babol et al.

    Hepatic metabolism of skatole in pigs by cytochrome P4502E1

    J. Anim. Sci.

    (1998)
  • J Babol et al.

    Relationship between metabolism of androstenone and skatole in intact male pigs

    J. Anim. Sci.

    (1999)
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    Present address: MRC Human Reproductive Sciences Unit, The University of Edinburgh, Chancellor's Building, 49 Little France Crescent, Old Dalkeith Road, Edinburgh EH16 4SB, UK.

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