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Microbial production of skatole in the hind gut of pigs given different diets and its relation to skatole deposition in backfat

Published online by Cambridge University Press:  02 September 2010

M. T. Jensen*
Affiliation:
Department of Animal Physiology and Biochemistry, Danish Institute of Animal Science, Research Centre Foulum, PO Box 39, DK-8830 Tjele, Denmark
R. P. Cox
Affiliation:
Institute of Biochemistry, Odense University, Campusvej 55, DK-5230 Odense M, Denmark
B. B. Jensen
Affiliation:
Department of Animal Physiology and Biochemistry, Danish Institute of Animal Science, Research Centre Foulum, PO Box 39, DK-8830 Tjele, Denmark
*
Corresponding author
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Abstract

The intestinal production of skatole and its deposition in backfat was investigated in 35 uncastrated crossbred male pigs. The pigs were fed five purified non-commercial diets containing either casein or brewers yeast slurry as protein source. The yeast slurry diet was used alone or supplemented with either wheat bran (200 g/kg), sugar-beet pulp (200 g/kg), or soya oil (100 g/kg).

Skatole concentrations in backfat, and in digesta in different sections of the gastro-intestinal tract were measured at slaughter (mean weight 112 kg). There were large variations in skatole concentrations in the hind gut of different animals given the same diet. Although there was some correlation between skatole in intestinal contents and deposition in adipose tissue, there were also large variations between individual animals in their response to intestinal skatole. Nevertheless, there was a clear effect of diet on both intestinal skatole production and skatole deposition in backfat. The use of casein as a protein source decreased microbial skatole production, the total amount in the gut, and the concentration in the backfat. Addition of sugar-beet pulp to the yeast slurry diet increased microbial activity in the intestine (measured as ATP content, concentration of short-chain fatty acids, and lowering of digesta pH). There was a decreased rate of skatole production during in vitro incubations of intestinal content, and less skatole in the hind gut and backfat.

In vitro fermentations of freeze-dried Heal effluent inoculated with faecal bacteria, and addition of substrates to in vitro incubations of intestinal contents, demonstrated that tryptophan availability rather than microbial activity was the limiting factor for skatole production.

The results show that skatole production depends on the amount of protein entering the hind gut and the proteolytic activity of the intestinal microbiota. Protein fermentation in the hind gut can be decreased either by using more readily digestible protein sources (for example casein rather than yeast slurry) which reduce the amount of protein passing through to the hind gut, or by adding an alternative energy source which is more readily metabolized by the hind gut microbiota (for example supplementation of the yeast slurry diet with sugar-beet pulp). This provides a basis for the rational design of diets which will decrease skatole concentrations in the carcass.

Type
Research Article
Copyright
Copyright © British Society of Animal Science 1995

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References

Agergaard, N. and Laue, A. 1993. Absorption from the gastrointestinal tract and liver turnover of skatole. In Measurement and prevention of boar taint and entire male pigs, Roskilde, Denmark, 1992 (ed. Bonneau, M.), Institut de la Recherche Agronomique, les colloques no. 60, pp. 107111.Google Scholar
Bach Knudsen, K. E., Jensen, B. B. and Hansen, I. 1993. Digestion of polysaccharides and other major components in the small and large intestine of pigs fed on diets consisting of oat fractions rich in β-D-glucan. British Journal of Nutrition 70: 537556.Google Scholar
Claus, R., Dehnhard, M., Herzog, A., Bernal-Barragan, H. and Giminez, T. 1993. Parallel measurements of indole and skatole (3-methylindole) in faeces and blood plasma of pigs by HPLC. Livestock Production Science 34: 115126.CrossRefGoogle Scholar
Clemens, E. T., Stevens, C. E., and Southworth, M. 1975. Sites of organic acid production and pattern of digesta movement in the gastrointestinal tract of swine. Journal of Nutrition 105: 759768.CrossRefGoogle ScholarPubMed
Friis, C. 1993. Distribution, metabolic fate and elimination of skatole in the pig. Measurement and prevention of boar taint in entire male pigs, Roskilde, Denmark, 1992, (ed. Bonneau, M.), Institut de la Recherche Agronomique, les colloques no. 60, pp. 113115.Google Scholar
Gill, B. P., Hardy, B., Perrott, J. G., Wood, J. D. and Hamilton, M. 1993. The effect of dietary fibre on the meat eating and fat quality of finishing pigs fed ad libitum. Animal Production 56: 421422 (abstr.).Google Scholar
Hansen, L. L., Larsen, A. E., Jensen, B. B., Hansen-Meller, J. and Barton-Gade, P. 1993. [Influence of stocking rate and temperature on faeces deposition in the pen and its consequences on skatole concentration (boar taint) in subcutaneous fat.] National Institute of Animal Science [N1AS], Denmark, research report no. 2.Google Scholar
Hansen-Møller, J. 1993. HPLC methods for determination of indole, skatole and related indoles in pig backfat. In Measurement and prevention of boar taint in entire male pigs, Roskilde, Denmark, 1992, (ed. Bonneau, M.), Institut de la Recherche Agronomique, les colloques no. 60, pp. 3539.Google Scholar
Hawe, M., Moss, B. W., Walker, N. and Porter, M. 1989. Distribution of skatole and indole compounds in pigs: influence of dietary factors. Proceedings of the thirty-fifth international congress of meat science and technology, vol. 3, pp. 10361038.Google Scholar
Hawe, S. M. and Walker, N. 1991. The effect of involuntary coprophagy on the production of skatole in growing pigs. Animal Production 53: 105109.Google Scholar
Hawe, S. M., Walker, N. and Moss, B. W. 1992. The effects of dietary fibre, lactose and antibiotic on the levels of skatole and indole in faeces and subcutaneous fat in growing pigs. Animal Production 54: 413419.Google Scholar
Jandacek, R. J. 1982. The effect of nonabsorbable lipids on the intestinal absorption of lipophiles. Drug Metabolism Reviews 13: 695714.CrossRefGoogle ScholarPubMed
Jensen, B. B. 1990. [Skatole (boar taint). Microbial production of skatole in the gastro-intestinal tract of pigs.] National Institute of Animal Science (NIAS), Denmark, communication no. 772.Google Scholar
Jensen, B. B. and Jensen, M. T. 1993. In vitro measurement of microbial production of skatole in the digestive tract of pigs. In Measurement and prevention of boar taint in entire male pigs, Roskilde, Denmark, (ed. Bonneau, M.), Institut de la Recherche Agronomique, les colloques no. 60, pp. 99105.Google Scholar
Jensen, M. T. and Jensen, B. B. 1994. Gas chromatographic determination of indole and 3-methylindole (skatole) in bacterial culture media, intestinal contents and faeces. Journal of Chromatography 655: 275280.CrossRefGoogle ScholarPubMed
Just, A., Jargensen, H., Fernandez, J. A., Bech-Andersen, S. and Hansen, N. E. 1983. The chemical composition, digestibility, energy and protein value in different feedstuffs for pigs. Report, National Institute of Animal Science, Denmark, no. 556.Google Scholar
Kjeldsen, N. 1993. Practical experience with production and slaughter of entire male pigs. In Measurement and prevention of boar taint in entire male pigs, Roskilde, Denmark, 1992, (ed. Bonneau, M.), Institut National de la Recherche Agronomique, les colloques no. 60, pp. 137144.Google Scholar
Kumemura, M., Hashimoto, F., Fujii, C., Matsuo, K., Kimura, H., Miyazoe, R., Okamatsu, H., Inokuchi, T., Ito, H., Oizumi, K. and Oku, T. 1992. Effects of administration of 4G-β3-D-galactosylsucrose on microflora, putrefactive products, short-chain fatty acids, weight, moisture and pH, and subjective sensation of defecation in the elderly with constipation. Journal of Clinical Biochemistry and Nutrition 13: 199210.Google Scholar
Laue, A., Agergaard, N. and Kalm, E. 1993. Plasma profiles of skatole in male slaughter pigs related to the absorption patterns and liver metabolism of microbial produced as well as administrated synthetic 3-methylindole. Proceedings of the forty-fourth annual meeting of the European Association for Animal Production, Aarhus, Denmark, p. 214.Google Scholar
Lundström, K., Malmfors, B., Malmfors, G., Stern, S., Petersson, H., Mortensen, A. B., and Sarensen, S. E. 1988. Skatole, androstenone and taint in boars fed two different diets. Livestock Production Science 18: 5567.CrossRefGoogle Scholar
McElroy, W. D. 1947. The energy source for bioluminicence in an isolated system. Proceedings of the National Academy of Sciences USA 33: 342345.Google Scholar
MacFarlane, G. T. and Allison, C. 1986. Utilisation of protein by human gut bacteria. FEMS Microbiology Ecology 38: 1924.Google Scholar
MacFarlane, G. T. and Cummings, J. H. 1991. The colonic flora, fermentation, and large bowel digestive function. The large intestine. Physiology, pathophysiology and disease (ed. Philips, S. F., Pemberton, J. H. and Shorter, R. G.), pp. 5192. Raven Press, New York.Google Scholar
MacFarlane, G. T., Cummings, J. H. and Allison, C. 1986. Protein degradation by human intestinal bacteria. Journal of General Microbiology 132: 16471656.Google ScholarPubMed
Mortensen, H. P. and Madsen, A. 1990. [Contents of skatole in male pigs fed malt or liquid yeast of different origin.] Danish Meat Research Institute, Roskilde, Denmark, report no. 01.708.Google Scholar
Mortensen, P. B., Holtug, K., Bonnen, H. and Clausen, M. R. 1990. The degradation of amino acids, proteins, and blood to short-chain fatty acids in colon is prevented by lactulose. Gastroenterology 98: 353360.Google Scholar
Nonboe, U. 1991. [Biological mechanisms behind skatole concentration in backfat.] Ph.D. thesis, The Royal Veterinary and Agricultural University, Copenhagen, Denmark.Google Scholar
Pedersen, J. K., Mortensen, A. B., Madsen, A., Mortensen, H. P. and Hyldegaard-Jensen, J. 1986. [The influence of feed on boar taint in meat from pigs.] National Institute of Animal Science, (NIAS), Denmark, communication no. 638.Google Scholar
Rasmussen, H. S., Holtug, K. and Mortensen, P. B. 1988. Degradation of amino acids to short-chain fatty acids in humans. Scandinavian Journal of Gastroenterology 23: 178182.CrossRefGoogle ScholarPubMed
Richardson, A. J., Calder, A. G., Stewart, C. S. and Smith, A. 1989. Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Letters in Applied Microbiology 9: 58.CrossRefGoogle Scholar
Terada, A., Hara, H., Kataoka, M. and Mitsuoka, T. 1992a. Effect of lactulose on the composition and metabolic activity of the human faecal flora. Microbial Ecology in Health and Disease 5: 4350.CrossRefGoogle Scholar
Terada, A., Hara, H., Oishi, T., Matsui, S., Mitsuoka, T., Nakajyo, S., Fujimori, I. and Hara, K. 1992b. Effect of dietary lactosucrose on faecal flora and faecal metabolites in dogs. Microbial Ecology in Health and Disease 5: 8792.Google Scholar
Thore, A. 1979. Technical aspects of the bioluminicent firefly luciferase assay of ATP. Science Tools 26: 3034.Google Scholar
Void, E. 1970. Fleischproduktionseigenschaften bei ebern und kastraten. Scientific Reports of the Agricultural College of Norway 49: 125.Google Scholar
Wood, D. J., Nute, G. R., Whittington, F. M., Kay, R. M. and Perrott, J. G. 1994. Effects of molassed sugar-beet feed on pigmeat quality. Animal Production 58: 471472 (abstr.).Google Scholar
Yokoyama, M. T. and Carlson, J. R. 1979. Microbial metabolites of tryptophan in the intestinal tract with special reference to skatole. American Journal of Clinical Nutrition 32: 173178.CrossRefGoogle ScholarPubMed