Prevention of boar taint in pig production. Factors affecting the level of skatole
- Bent Borg Jensen1
© Jensen.; licensee BioMed Central Ltd. 2006
Published: 7 August 2006
The indolic compound skatole is produced by microbial degradation of the amino acid tryptophan and has been detected in the rumen of cows and the caecum and colon of pigs. Together with the testicular steroid androstenone skatole is considered to be the main contributor to boar taint.
Several studies in our laboratory have shown that microbial degradation of tryptophan by pig gastrointestinal bacteria results mainly in the two volatile indolic compounds indole and skatole, skatole via a transient accumulation of indole acetic acid (IAA). Analogously with indole and skatole, indole propionic acid is also an end product of tryptophan metabolism, and has recently been shown to be produced in small amounts in the hind gut of pigs . While the conversion of tryptophane to indole and IAA is performed by a variety of bacteria, only very few bacteria species are capable of further degradation of IAA to skatole . The production of skatole increases through the colon and reaches a maximum in the distal part of the large intestine. From the intestinal tract, a portion of the produced skatole is absorbed to the blood and transported via the portal vein to the liver, where more than half of the amount absorbed is degraded by cytochrome P450. It has been demonstrated that the liver extraction is relatively constant within the individual animal, but varies between animals, and between sexes, showing a lower elimination rate of skatole in male pigs than female pigs . Skatole avoiding degradation in the liver is deposited in peripheral tissues and due to the lipophilic characteristics of skatole the majority accumulates in the adipose tissue. To summarize, the amount of skatole stored in adipose tissue depends on the concentration in the peripheral blood, which is influenced by the production in the large intestine and the degradation capacity of the liver. As the production of skatole is the incipient cause of tainted meat a limitation of the microbial fermentation of tryptophan in the large intestine would be an effective approach to solve the problem with boar odour caused by skatole.
Factors affecting the level of skatole
The exact mechanism of how fibre-rich diets affect skatole deposition in back fat is not known, but several contradictory hypotheses have been presented. Firstly, in the presence of extra dietary fibre, more undigested protein will reach the large intestine with consequently more degradation of tryptophan to skatole. Secondly, more fermentable carbohydrates in the hindgut will increase the microbial activity in the gastrointestinal tract  resulting in more tryptophan incorporated as bacterial protein, further increased amounts of carbohydrates will decrease the activity of the proteolytic bacteria resulting in less tryptophan available for skatole production. Thirdly, extra dietary fibre results in more bulky material in the large intestine and an increased water binding capacity, leading to a dilution of skatole resulting in less contact of skatole with the intestinal wall and consequently, decreased skatole absorption . Further, dietary fibre decreases the intestinal transit time and as such may decrease skatole absorption from the gut. Recently it has been hypotized that carbohydrates with high pre-ceacal digestibility will increase cell debris formation in the small intestine, resulting in more tryptophan entering the large intestine and as such higher skatole formation . On the other hand carbohydrates with low pre-caecal digestibility will decrease skatole production due to an increased butyrate production that inhibits apoptosis and as such less tryptophan available for skatole production.
Influence of dietary fibre on microbial degradation of tryptophan (TRP) to indole, indole propionic acid (IPA) and skatole in the hind gut of male pigs.
Basic production in the hind gut, 12 h
Total production following infusion of TRP, 12 h
Production caused by infusion of TRP
Percent of infused TRP converted
Approximately 70% of the produced skatole was recovered in the portal blood. On the high fibre diet, however, only 6% of the infused tryptophan was converted to skatole in the gastrointestinal tract, resulting in a lower increase in portal blood skatole concentration. Again approximately 70% of the skatole produced in the hindgut was absorbed to the portal blood. Also the basal skatole production in the hindgut and absorption to the portal blood were affected by the fibre content in the diet. With the high fibre diet only 230 μmol skatole was produced during the 12 hours, while more than twice as much (480 μmol) was produced on the low fibre diet. These results strongly show the usefulness of in vitro measurements of skatole production and the use of portal absorption to study the effect of diet on the production and absorption of microbial metabolites in the large intestine, and confirm the important effect of diet composition on the amount of skatole produced and absorbed from the gut. Further, the results point at the use of fibre rich diets as a relevant way to reduce boar taint due to skatole in practical pig production.
Two feeding strategies that have a marked effect on the gastrointestinal ecosystem are liquid feeding  and the structure of the feed (pellets vs. meal/fine vs. gorse) . While use of liquid feed has been shown to reduce the level of skatole , it has never been investigated if the feed structure has any effect on skatole levels.
Feed intake (fasting)
Studies with different feeding levels during the growth period of the pigs showed that the general feed intake had no effect on the skatole level, whereas a 12 hours redraw of feed from the pigs prior to slaughter did reduce the skatole level . This is in agreement with that reduced amount of digesta entering the large intestine results in a lower fermentation of non-digested protein and the very rapid degradation of skatole in the liver. However, Anderson et al. , were unable to confirm that a 12 hours redraw of feed reduced skatole.
Androstenone and other testicular steroids might be involved in the skatole level by regulation of skatole metabolism in the liver . Androstenone is a pheromonal steroid produced in the testes of mature male pigs together with other steroids and its levels are primarily affected by puberty stage. Using in vitro experiments Doran et al.  have shown that androstenone suppress the induction of enzymes involved in skatole metabolism. Zamaratskaia et al.  found a positive correlation between the testicular hormones testosterone and oestrone sulphate and skatole level suggesting that these compounds have an influence on skatole pattern, and the authors suggest that slaughter of entire male pigs at a weight below 100 kg can be used to avoid boar taint.
There are strong indications of genetic influences on skatole levels in pigs. These include differences in skatole levels between breeds , significant heritability estimates for levels of skatole in fat  as well as indications of the presence of a major gene affecting boar taint due to skatole .
- Knarreborg A, Beck J, Jensen MT, Laue A, Agergaard N, Jensen BB: Effect of non-starch polysaccharides on production and absorption of indolic compounds in entire male pigs. Animal Science. 2002, 74: 445-453.Google Scholar
- Jensen BB, Jensen MT: Microbial production of skatole in the digestive tract of entire pigs. Skatole and boar taint. Edited by: Jensen WK. 1998, Roskilde. Denmark: Danish Meat Research Institute, 293-304.Google Scholar
- Friis C: Distribution, metabolic fate and elimination of skatole in the pig. Measurement and prevention of boar taint in entire male pigs. 1993, Roskilde Denmark. INRA, Paris (Les Collogues no. 60), 113-115. 12–14 October 1992Google Scholar
- Jensen BB: Impact of feed composition and feed processing on the gastrointestinal ecosystem in pigs. Nutrition and gastrointestinal physiology – today and tomorrow. 1999, (red. AJM Jansman and J Huisman) TNO Nutrition and Food Research Institute, Wageningen, The Netherlands, 43-56.Google Scholar
- Boyd WL, Lichstein HC: The effect of carbohydrates on the tryptophanase activity of bacteria. Journal of Bacteriology. 1995, 69: 584-589.Google Scholar
- Misir R, Sauer WC: Effect of starch infusion at the terminal ileum on nitrogen balance and apparent digestibilities of nitrogen and amino acids in pigs fed meat-and-bone and soybean diets. Journal of Animal Science. 1982, 64: 448-456.Google Scholar
- Jensen BB: [Skatole (boar taint). Microbial production of skatole in the gastro-intestinal tract of pigs]. 1990, Communication 772. Danish Institut of Agricultural Science, Tjele, DenmarkGoogle Scholar
- Jensen MT, Cox RP, Jensen BB: Microbial production of skatole in the hindgut of pigs given different diets and its relation to skatole deposition in backfat. Animal Science. 1995, 61: 293-304.View ArticleGoogle Scholar
- Øverland M, Berg J, Matre T: The effect of feed and feeding regime on skatole and androstenone levels and on sensory attributes of entire male and female pigs. Proceeding of the EAAP Working Group, Production and Utilisation of Meat from Entire Male Pigs. 1995, Milton Keynes, UKGoogle Scholar
- Van Oeckel MJ, Warnants N, De Paepe M, Casteels M, Bouequé Ch.V: Effect of fibre-rich diets on the backfat skatole content of entire male pigs. Livestock Production Science. 1998, 56: 173-180. 10.1016/S0301-6226(98)00190-0.View ArticleGoogle Scholar
- Kjeldsen N: Practical experience from field studies with entire male pigs. Skatole and boar taint. Edited by: Jensen WK. 1998, Roskilde. Denmark: Danish Meat Research Institute, 129-136.Google Scholar
- Whittingthon FM, Nute GR, Huges SI, McGivan JD, Lean LJ, Wood JD, Doran E: Relationships between skatole and androstenone accumulation and cytochrome P450E1 expression in Meishan × Large White pigs. Meat Science. 2004, 67: 569-576. 10.1016/j.meatsci.2003.12.010.View ArticleGoogle Scholar
- Xu ZR, Hu CH, Wang MQ: Effects of frugtooligosaccharides on conversion of L-tryptophan to skatole and indole by mixed populations of pig fecal bacteria. Journal of General Applied Microbiology. 2002, 48: 83-90. 10.2323/jgam.48.83.View ArticlePubMedGoogle Scholar
- Russell TJ, Kerley MS, Allee GJ, Howard MD: Fructooligosaccharides improves nitrogen metabolism and reduce fecal excretion of odour metabolites in the weaned pig. UMC Animal Science Department Rep. 1998, 79-83.Google Scholar
- Lösel D, Claus R: Dose-dependent effects of resistant potato starch in the diet on intestinal skatole formation and adipose tissue accumulation in the pig. Journal of Veterinary Medicine. 2005, 52: 209-212. 10.1111/j.1439-0442.2005.00716.x.View ArticlePubMedGoogle Scholar
- Zamaratskaia G, Babol J, Anderson 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. Livestock Production Science. 2005, 93: 235-243. 10.1016/j.livprodsci.2004.10.007.View ArticleGoogle Scholar
- Jensen BB, Jørgensen BB: Effect of dietary fibre on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Applied and Environmental Microbiology. 1994, 60: 1897-1904.PubMed CentralPubMedGoogle Scholar
- Claus RD, Lösel M, Lacorn M, Mentschel J, Schenkel H: Effects of butyrate on apoptosis in the pig colon and its consequences for skatole formation and tissue accumulation. Journal of Animal Science. 1996, 81: 239-248.Google Scholar
- Agergaard N, Jensen BB, Laue A, Jensen MT: Production and absorption of skatole to the portal vein blood following tryptophan infusion to the hind gut. Skatole and boar taint. Edited by: Jensen WK. 1997, Roskilde. Denmark: Danish Meat Research Institute, 97-110.Google Scholar
- Jensen BB, Mikkelsen LL: Feeding liquid diets to pigs. Recent advances in Animal Nutrition. Edited by: Garnsworthy PC, Cole DJA. 1998, Nottingham University Press, 105-124.Google Scholar
- Mikkelsen LL, Naughton PJ, Hedemann MS, Jensen BB: Effects of physical properties of feed on microbial ecology and survival of Salmonella enterica Serovar Typhimurium in the pig gastrointestinal tract. Appl Environ Microbiol. 2004, 70: 3485-3492. 10.1128/AEM.70.6.3485-3492.2004.PubMed CentralView ArticlePubMedGoogle Scholar
- Anderson K, Schaub A, Anderson K, Lundström K, Thomke S, Hansson I: The effect of feeding systems, lysine level and gilt contact on performance, skatole levels and economy of entire male pigs. Livestock Production Science. 1997, 51: 131-140. 10.1016/S0301-6226(97)00097-3.View ArticleGoogle Scholar
- Walstra P, Claudi-Magnussen C, Chevillon P, von Seth G, Diestre A, Matthews KR, Homer DB, Bonneau M: 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. 1999, 62: 15-28. 10.1016/S0301-6226(99)00054-8.View ArticleGoogle Scholar
- Hansen LL, Larsen AE, Jensen BB, Hansen-Møller J, Barton-Gade P: Influence of stocking rate and faeces deposition in the pen at different temperatures on skatole concentration (boar taint) in subcutaneous fat. Animal Production. 1994, 59: 99-110.View ArticleGoogle Scholar
- Doran E, Whittington FW, Wood JD, McGivan JD: Cytochrome P450IIEI (CYP2E1) is inducedby skatole and this induction is blocked by Androstenone in isolated pig hepatocytes. Chemico-Biological Interactions. 2002, 104: 81-82. 10.1016/S0009-2797(02)00015-7.View ArticleGoogle Scholar
- Babol J, Zamaratskaia G, Juneja RK, Lundström K: The effect of age on distribution of skatole and indole levels in entire male pigs in four breeds: Yokshire, Landrace, Hampshire and Duroc. Meat Science. 2004, 67: 351-358. 10.1016/j.meatsci.2003.11.008.View ArticlePubMedGoogle Scholar
- Pedersen B: Heritability of skatole in back fat. Skatole and boar taint. Edited by: Jensen WK. 1998, Roskilde. Denmark: Danish Meat Research Institute, 129-136.Google Scholar
- Lundström K, Malmfors B, Stern S, Rydhymer L, Eliasson-Selling L, Mortensen AB, Mortensen HP: Skatole levels in pigs selected for high lean tissue growth rate on different protein levels. Livestock Production Science. 1994, 38: 125-132. 10.1016/0301-6226(94)90056-6.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd.