Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T04:36:54.506Z Has data issue: false hasContentIssue false
  • English
  • Français

Skatole metabolites in urine as a biological marker of pigs with enhanced hepatic metabolism

Published online by Cambridge University Press:  15 April 2016

C. Brunius ,
J. K. Vidanarachchi ,
J. Tomankova ,
K. Lundström ,
K. Andersson  and
G. Zamaratskaia
C. Brunius*
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, BioCenter, PO Box 7051, SE-750 07 Uppsala, Sweden
J. K. Vidanarachchi
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, BioCenter, PO Box 7051, SE-750 07 Uppsala, Sweden Department of Animal Science, University of Peradeniya, 20400 Peradeniya, Sri Lanka
J. Tomankova
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, BioCenter, PO Box 7051, SE-750 07 Uppsala, Sweden
K. Lundström
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, BioCenter, PO Box 7051, SE-750 07 Uppsala, Sweden
K. Andersson
Affiliation:
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, PO Box 7024, SE-750 07 Uppsala, Sweden
G. Zamaratskaia
Affiliation:
Department of Food Science, Swedish University of Agricultural Sciences, BioCenter, PO Box 7051, SE-750 07 Uppsala, Sweden
*
†E-mail: carl.brunius@slu.se
Get access

Abstract

Boar taint is a quality defect in meat, related to accumulation of skatole and androstenone in male pigs. The levels of skatole and its main metabolites in plasma and urine samples were measured with a validated liquid chromatography-MS method and related to activity of hepatic cytochrome P450 (CYP450) in order to identify ‘fast metabolizing’ pigs. Urine (n=46), blood (n=12), liver (n=25) and adipose tissue (n=46) were sampled from a total of 46 entire male pigs. Skatole levels in fat were negatively correlated to CYP2E1 activity and positively to 3-hydroxy-3-methyloxindole (HMOI), indole-3-carboxylic acid (ICA) and 2-aminoacetophenone in urine. HMOI and ICA levels in urine were the best predictors of high skatole levels in fat. In summary, the present study provided further evidence for the key role of CYP2E1 in skatole metabolism and suggested that measurement of HMOI and/or ICA in urine might provide information about skatole levels in live pigs.

Keywords

pigskatole3-hydroxy-3-methyloxindole (HMOI)indole-3-carboxylic acid (ICA)cytochrome P450 (CYP450)
Type
Research Article
Information
animal , Volume 10 , Issue 10 , October 2016 , pp. 1734 - 1740
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderton, MJ, Manson, MM, Verschoyle, RD, Gescher, A, Lamb, JH, Farmer, PB, Steward, WP and Williams, ML 2004. Pharmacokinetics and tissue disposition of indole-3-carbinol and its acid condensation products after oral administration to mice. Clinical Cancer Research 10, 5233–5241.Google Scholar
Babol, J, Squires, EJ and Lundström, K 1998. Hepatic metabolism of skatole in pigs by cytochrome P4502E1. Journal of Animal Science 76, 822–828.CrossRefGoogle ScholarPubMed
Bæk, CÆ, Hansen-Møller, J, Friis, C, Cornett, C and Hansen, SH 1997. Identification of selected metabolites of skatole in plasma and urine from pigs. Journal of Agricultural and Food Chemistry 45, 2332–2340.CrossRefGoogle Scholar
Borrisser Pairó, F, Rasmussen, M, Ekstrand, B and Zamaratskaia, G 2015. Gender-related differences in the formation of skatole metabolites by specific CYP450 in porcine hepatic S9 fractions. Animal 9, 635–642.CrossRefGoogle ScholarPubMed
Brunius, C, Rasmussen, M, Ekstrand, B, Lacoutiere, H, Andersson, K and Zamaratskaia, G 2012. Expression and activities of hepatic cytochrome P450 (CYP1A, CYP2A and CYP2E1) in entire and castrated male pigs. Animal 6, 271–277.CrossRefGoogle ScholarPubMed
Brunius, C and Zamaratskaia, G 2012. Validation of a modified HPLC method for simultaneous quantification of skatole and indole in porcine plasma without the use of acetonitrile. Acta Veterinaria Brno 81, 153–158.CrossRefGoogle Scholar
Byrd, DJ, Kochen, W, Idzko, D and Knorr, E 1974. The analysis of indolic tryptophan metabolites in human urine. Thin-layer chromatography and in situ quantitation. Journal of Chromatography 94, 85–106.Google Scholar
Chen, G, Zamaratskaia, G, Madej, A and Lundström, K 2006. Effect of hCG administration on the relationship between testicular steroids and indolic compounds in fat and plasma in entire male pigs. Meat Science 72, 339–347.Google Scholar
Diaz, GJ, Skordos, KW, Yost, GS and Squires, EJ 1999. Identification of phase I metabolites of 3-methylindole produced by pig liver microsomes. Drug Metabolism and Disposition 27, 1150–1156.Google ScholarPubMed
Diaz, GJ and Squires, EJ 2000. Metabolism of 3-methylindole by porcine liver microsomes: responsible cytochrome P450 enzymes. Toxicological Sciences 55, 284–292.CrossRefGoogle ScholarPubMed
Duijvesteijn, N, Knol, EF, Merks, JW, Crooijmans, RP, Groenen, MA, Bovenhuis, H and Harlizius, B 2010. A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6. BMC Genetics 11, 42.Google Scholar
England, DB, Merey, G and Padwa, A 2007. Substitution and cyclization reactions involving the quasi-antiaromatic 2H-indol-2-one ring system. Organic Letters 9, 3805–3807.Google Scholar
Gregersen, VR, Conley, LN, Sørensen, KK, Guldbrandtsen, B, Velander, IH and Bendixen, C 2012. Genome-wide association scan and phased haplotype construction for quantitative trait loci affecting boar taint in three pig breeds. BMC Genomics 13, 22.CrossRefGoogle ScholarPubMed
Grindflek, E, Berget, I, Moe, M, Oeth, P and Lien, S 2010. Transcript profiling of candidate genes in testis of pigs exhibiting large differences in androstenone levels. BMC Genetics 11, 4.Google Scholar
Gunawan, A, Sahadevan, S, Neuhoff, C, Große-Brinkhaus, C, Gad, A, Frieden, L, Tesfaye, D, Tholen, E, Looft, C, Uddin, MJ, Schellander, K and Cinar, MU 2013a. RNA deep sequencing reveals novel candidate genes and polymorphisms in boar testis and liver tissues with divergent androstenone levels. PLoS One 8, e63259.Google Scholar
Gunawan, A, Sahadevan, S, Cinar, MU, Neuhoff, C, Große-Brinkhaus, C, Frieden, L, Tesfaye, D, Tholen, E, Looft, C, Wondim, DS, Hölker, M, Schellander, K and Uddin, MJ 2013b. Identification of the novel candidate genes and variants in boar liver tissues with divergent skatole levels using RNA deep sequencing. PLoS One 8, e72298.CrossRefGoogle ScholarPubMed
Haberland, AM, Luther, H, Hofer, A, Tholen, E, Simianer, H, Lind, B and Baes, C 2014. Efficiency of different selection strategies against boar taint in pigs. Animal 8, 11–19.Google Scholar
Hauder, J, Winkler, S, Bub, A, Rüfer, CE, Pignitter, M and Somoza, V 2011. LC-MS/MS quantification of sulforaphane and indole-3-carbinol metabolites in human plasma and urine after dietary intake of selenium-fortified broccoli. Journal of Agricultural and Food Chemistry 59, 8047–8057.Google Scholar
Jonsson, P and Andresen, Ø 1979. Experience during two generations of within lines performance testing, using 5-androst-16-ene-3-one (5-androstenone) and an olfactory judgement of boar taint. Annales de Génétique et de Sélection Animale 11, 241–250.CrossRefGoogle Scholar
Matal, J, Matuskova, Z, Tunkova, A, Anzenbacherova, E and Anzenbacher, P 2009. Porcine CYP2A19, CYP2E1 and CYP1A2 forms are responsible for skatole biotransformation in the reconstituted system. Neuro Endocrinology Letters 30 (suppl. 1), 36–40.Google ScholarPubMed
Rydhmer, L, Hansson, M, Lundström, K, Brunius, C and Andersson, K 2013. Welfare of entire male pigs is improved by socialising piglets and keeping intact groups until slaughter. Animal 7, 1532–1541.Google Scholar
Sellier, P, Le Roy, P, Fouilloux, MN, Gruand, J and Bonneau, M 2000. Responses to restricted index selection and genetic parameters for fat androstenone level and sexual maturity status of young boars. Livestock Production Science 63, 265–274.Google Scholar
Smith, DJ, Skiles, GL, Appleton, ML, Carlson, JR and Yost, GS 1993. Identification of goat and mouse urinary metabolites of the pneumotoxin, 3-methylindole. Xenobiotica 23, 1025–1044.Google Scholar
Terner, MA, Gilmore, WJ, Lou, Y and Squires, EJ 2006. The role of CYP2A and CYP2E1 in the metabolism of 3-methylindole in primary cultured porcine hepatocytes. Drug Metabolism and Disposition 34, 848–854.Google Scholar
Wesoly, R and Weiler, U 2012. Nutritional influences on skatole formation and skatole metabolism in the pig. Animals (Basel) 2, 221–242.CrossRefGoogle ScholarPubMed
Wiercinska, P, Lou, Y and Squires, EJ 2011. The roles of different porcine cytochrome P450 enzymes and cytochrome b5A in skatole metabolism. Animal 6, 834–845.Google Scholar
Willeke, H, Claus, R, Müller, E, Pirchner, F and Karg, H 1987. Selection for high and low level of 5 α-androst-16-en-3-one in boars. I. Direct and correlated response of endocrinological traits. Journal of Animal Breeding and Genetics 104, 64–73.Google Scholar
Willeke, H and Pirchner, F 1989. Selection for high and low level of 5α-androst-16-en-3-one in boars. II. Correlations between growth traits and 5-androstenone. Journal of Animal Breeding and Genetics 106, 312–317.CrossRefGoogle Scholar
Zamaratskaia, G, Babol, J, Andersson, H and Lundström, K 2004a. Plasma skatole and androstenone levels in entire male pigs and relationship between boar taint compounds, sex steroids and thyroxine at various ages. Livestock Production Science 87, 91–98.Google Scholar
Zamaratskaia, G, Babol, J, Madej, A, Squires, EJ and Lundström, K 2004b. Age-related variation of plasma concentrations of skatole in relation to androstenone, sex hormones, triiodothyronine and IGF-1 in six entire male pigs. Reproduction in Domestic Animals 39, 168–172.CrossRefGoogle ScholarPubMed
Zamaratskaia, G and Squires, EJ 2009. Biochemical, nutritional and genetic effects on boar taint in entire male pigs. Animal 3, 1508–1521.Google Scholar
Zamaratskaia, G, Squires, EJ, Babol, J, Andersson, HK, Andersson, K and Lundström, K 2005. 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. Livestock Production Science 95, 83–88.CrossRefGoogle Scholar
Zamaratskaia, G and Zlabek, V 2009. EROD and MROD as markers of cytochrome P450 1A activities in hepatic microsomes from entire and castrated male pigs. Sensors (Basel) 9, 2134–2147.Google Scholar