Hydrolysable tannin fed to entire male pigs affects intestinal production, tissue deposition and hepatic clearance of skatole

Veterinary Journal

Volumn 204, Issue 2, 2015, Pages 162-167

  Candek Potokar M ^a,b   Skrlep M ^a   Batorek Lukac N ^a   Zamaratskaia, G ^c   Prevolnik Povse M ^b   Velikonja Bolta, S ^a   Kubale, V ^d   Bee, G ^e  

^a AGRICULTURAL INSTITUTE OF SLOVENIA   (Slovenia)

^b UNIVERSITY OF MARIBOR   (Slovenia)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

^e Agroscope Institute for Livestock Sciences   (Switzerland)

Author keywords

Androstenone; Cytochrome P450; Pig; Skatole; Tannins

Indexed keywords

CYTOCHROME P450; SKATOLE; TANNIN;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; BIOACCUMULATION; BOAR (MALE PIG); CHEMICAL ANALYSIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FOOD COMPOSITION; GROWTH RATE; MALE; NONHUMAN; ORGAN WEIGHT; PAROTID ENLARGEMENT; SALIVARY GLAND; SUBCUTANEOUS FAT; ANALYSIS; ANIMAL; ANIMAL FOOD; CHEMISTRY; DIET; DRUG EFFECTS; GENE EXPRESSION REGULATION; INTESTINE; LIVER; MALE GENITAL SYSTEM; METABOLISM; PIG; STOMACH JUICE; TISSUE DISTRIBUTION; VETERINARY;

PIERIS BRASSICAE; SUIDAE;

ANIMAL FEED; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; DIET; GASTROINTESTINAL CONTENTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENITALIA, MALE; HYDROLYZABLE TANNINS; INTESTINES; LIVER; MALE; SALIVARY GLANDS; SKATOLE; SWINE; TISSUE DISTRIBUTION;

EID: 84929656369     PISSN: 10900233     EISSN: 15322971     Source Type: Journal    
DOI: 10.1016/j.tvjl.2015.02.012     Document Type: Article

References (52)

1. Aluwe M., Langedries K.C.M., Bekaert K.M., Tuyttens F.A.M., De Brabander D.L., De Smet S., Millet S. Effect of surgical castration, immunocastration and chicory-diet on the meat quality and palatability of boars. Meat Science 2013, 94:402-407.
2. Babol J., Squires E.J., Lundström K. Hepatic metabolism of skatole in pigs by cytochrome P4502E1. Journal of Animal Science 1998, 76:822-828.
3. Batorek N., Škrlep M., Prunier A., Louveau I., Noblet J., Bonneau M., Čandek-Potokar M. Effect of feed restriction on hormones, performance, carcass traits, and meat quality in immunocastrated pigs. Journal of Animal Science 2012, 90:4593-4603.
4. Biagi G., Cipollini I., Paulicks B.R., Roth F.X. Effect of tannins on growth performance and intestinal ecosystem in weaned piglets. Archives of Animal Nutrition 2010, 64:121-135.
5. Cappai M.G., Wolf P., Große Leistner V., Kastner A., Nieddu G., Pinna W., Kamphues J. Effect of whole acorns (Quercus pubescens) shred based diet on parotid gland in growing pigs in relation to tannins. Livestock Science 2010, 134:183-186.
6. Cappai M.G., Wolf P., Pinna W., Kamphues J. Dose-response relationship between dietary polyphenols from acorns and parotid gland hypertrophy in pigs. Food and Nutrition Sciences 2012, 3:1261-1268.
7. Carlson D.M. Salivary proline-rich proteins: Biochemistry, molecular biology, and regulation of expression. Critical Reviews in Oral Biology and Medicine 1993, 4:495-502.
8. Chen G., Zamaratskaia G., Andersson H.K., Lundström K. Effect of dietary supplement of raw potato starch and liveweight on the levels of skatole, indole and androstenone measured by different methods. Food Chemistry 2007, 101:439-448.
9. Chen G., Cue R.-A., Lundström K., Wood J.H., Doran O. Regulation of cytochrome P450 2A6 protein expression by skatole, indole and testicular steroids in primary cultured porcine hepatocytes. Drug Metabolism and Deposition 2008, 36:56-60.
10. Chung K.-T., Wei C.-I., Johnson M.G. Are tannins a double-edged sword in biology and health?. Trends in Food Science and Technology 1998, 9:168-175.
11. Claus R., Weiler U., Herzog A. Physiological aspects of androstenone and skatole formation in the boar - A review with experimental data. Meat Science 1994, 38:289-305.
12. 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. Journal of Animal Science 2003, 81:239-248.
13. Denhard M., Bernal-Barragan H., Claus R. Rapid and accurate high-performance liquid chromatographic method for the determination of 3-methylindole (skatole) in faeces of various species. Journal of Chromatography 1991, 566:101-107.
14. Diaz G.J., Squires E.J. Role of aldehyde oxidase in the hepatic in vitro metabolism of 3-methylindole in pigs. Journal of Agricultural and Food Chemistry 2000, 48:833-837.
15. Diaz G.J., Squires E.J. Metabolism of 3-methylindole by porcine liver microsomes: Responsible cytochrome P450 enzymes. Toxicological Sciences 2000, 55:284-292.
16. Doran E., Whittington F.W., Wood J.D., McGivan J.D. Cytochrome P450IIIE1 (CYP2E1) is induced by skatole and this induction is blocked by androstenone in isolated pig hepatocytes. Chemical-Biological Interactions 2002, 140:81-92.
17. Fischer J., Wüst M. Quantitative determination of the boar taint compounds androstenone, skatole, indole, 3α-androstenol and 3β-androstenol in wild boars (Sus scrofa) reveals extremely low levels of the tryptophan-related products. Food Chemistry 2012, 135:2128-2132.
18. Frandson R.D., Wilke W.L., Fails A.D. Anatomy and Physiology of Farm Animals 2009, 356. Wiley-Blackwell, Ames, IA, USA. Seventh Ed.
19. Frankič T., Salobir J. In vivo antioxidant potential of Sweet chestnut (Castanea sativa Mill.) wood extract in young growing pigs exposed to n-3 PUFA-induced oxidative stress. Journal of the Science of Food and Agriculture 2011, 91:1432-1439.
20. Goel G., Puniya A.K., Aguilar C.N., Singh K. Interaction of gut microflora with tannins in feeds. Die Naturwissenschaften 2005, 92:497-503.
21. Gower D.B. 16-Unsaturated C19 steroids. A review of their chemistry, biochemistry and possible physiological role. Journal of Steroid Biochemistry 1972, 3:45-103.
22. Haslam E. Vegetable tannins - Lessons of a phytochemical lifetime. Phytochemistry 2007, 68:2713-2721.
23. ISO 5983-1 Animal feeding stuffs - Determination of nitrogen content and calculation of crude protein content. Part 1: Kjeldahl method 2005.
24. Jansman A.J., Verstegen M.W., Huisman J., van den Berg J.W. Effects of hulls of faba beans (Vicia faba L.) with a low or high content of condensed tannins on the apparent ileal and faecal digestibility of nutrients and the excretion of endogenous protein in ileal digesta and faeces of pigs. Journal of Animal Science 1995, 73:118-127.
25. Jensen B.B. Prevention of boar taint in pig production. Factors affecting the level of skatole. Acta Veterinaria Scandinavica 2006, 48(Suppl. 1):S6.
26. Jensen M.T., Hansen L.L. Feeding with chicory roots reduces the amount of odorous compounds in colon and rectal contents of pigs. Animal Science 2006, 82:369-376.
27. Jensen M.T., Cox R.P., Jensen B.B. Microbial production of skatole in the hind gut of the pigs given different diets and its relation to skatole deposition in backfat. Animal Science 1995, 61:293-304.
28. Jorgie-Brahim S., Feldman D., Oh Y. Unraveling insulin-like growth factor binding protein-3 actions in human disease. Endocrine Reviews 2009, 30:417-437.
29. Knarreborg A., Beck J., Jensen M.T., Laue A., Agergard N., Jensen B.B. Effect of non-starch polysaccharides on production and absorption of indolic components in entire male pigs. Animal Science 2002, 74:445-453.
30. Lizardo R., Peiniau J., Aumaitre A. Effect of sorghum on performance, digestibility of dietary components and activities of pancreatic and intestinal enzymes in the weaned piglet. Animal Feed Science and Technology 1995, 56:67-82.
31. Mariscal-Landín G., Avellaneda J.H., Reis de Souza T.C., Aguilera A., Borbolla G.A., Mar B. Effect of tannins in sorghum on amino acid ileal digestibility and on trypsin (E.C.2.4.21.4) and chymotrypsin (E.C.2.4.21.1) activity of growing pigs. Animal Feed Science and Technology 2004, 117:245-264.
32. Mueller-Harvey I. Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 2006, 86:2010-2037.
33. Payne A.H., Hales D.B. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrine Reviews 2004, 25:947-970.
34. Pinna W., Cappai M.G., Moniello G., Nieddu G. Tannins concentration and ultrastructural peculiarities of starch granules in acorns of Quercus ilex, Quercus pubescens Willd. and Quercus ruber L 2007, 96. In: Proceedings of the 11th Congress of the European Society of Veterinary and Comparative Nutrition, Leipzig, Germany.
35. Pithayanukul P., Nithitanakool S., Bavovada R. Hepatoprotective potential of extracts from seeds of Areca catechu and nutgalls of Quercus infectoria. Molecules 2009, 14:4987-5000.
36. Priolo A., Vasta V., Fasone V., Lanza C.M., Scerra M., Biondi L., Bella M., Whittington F.M. Meat odour and flavour and indoles concentration in ruminal fluid and adipose tissue of lambs fed green herbage or concentrates with or without tannins. Animal: An International Journal of Animal Bioscience 2009, 3:454-460.
37. Rasmussen M., Ekstrand B., Zamaratskaia G. Comparison of cytochrome P450 concentrations and metabolic activities in porcine hepatic microsomes prepared with two different methods. Toxicology in Vitro 2011, 25:343-346.
38. Rasmussen M.K., Brunius C., Zamaratskaia G., Ekstrand B. Feeding dried chicory root to pigs decrease androstenone accumulation in fat by increasing hepatic 3β hydroxysteroid dehydrogenase expression. Journal of Steroid Biochemistry and Molecular Biology 2012, 130:90-95.
39. Rideout T.C., Fan M.Z., Cant J.P., Wagner-Ridle C., Stonehouse P. Excretion of major odor-causing and acidifying components in response to dietary supplementation of chicory inulin in growing pigs. Journal of Animal Science 2004, 82:1678-1684.
40. Robic A., Larzul C., Bonneau M. Genetic and metabolic aspects of androstenone and skatole deposition in pig adipose tissue: A review. Genetics, Selection, Evolution 2008, 40:129-143.
41. Rodríguez-Estévez V., Sánchez-Rodríguez M., García A., Gómez-Castro A.G. Feed conversion rate and estimated energy balance of free grazing Iberian pigs. Livestock Science 2010, 132:152-156.
42. Roy N.C., Fraser K., Lane G.A., Reynolds G.W., Deighton M.H., Peters J.S., Sinclair B.R., Death A.F., McNabb W.C. The effects of condensed-tannins on the flux of skatole and indole across the mammary gland and their secretion in milk of lactating ewes fed fresh sulla (Hedysarum coronarium). Proceedings of the Australian Society on Animal Production 2002, 24:189-192.
43. Serrano J., Puupponen-Pimiä R., Dauer A., Aura A.-M., Saura-Calixto F. Tannins: Current knowledge of food sources, intake, bioavailability and biological effects. Molecular Nutrition & Food Research 2009, 53(Suppl. 2):310-329.
44. Shimada T. Salivary proteins as a defense against dietary tannins. Journal of Chemical Ecology 2006, 32:1149-1163.
45. Wesoly R., Weiler U. Nutritional influences on skatole formation and skatole metabolism in the pig. Animals 2012, 2:221-242.
46. Zakon o zaščiti živali Uradni list Republike Slovenije, 43/07 2007, Uradni list Republike Slovenije, Ljubljana, Slovenija.
47. Zamaratskaia G., Squires E.J. Biochemical, nutritional and genetic effects on boar taint in entire male pigs. Animal: An International Journal of Animal Bioscience 2009, 3:1508-1521.
48. Zamaratskaia G., Babol J., Andersson H.K., Anderson K., Lundström K. Effect of liveweight 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.
49. Zamaratskaia G., Gilmore W.J., Lundström K., Squires E.J. Effect of testicular steroids on catalytic activities of cytochrome P450 enzymes in porcine liver microsomes. Food and Chemical Toxicology 2007, 45:676-681.
50. Zamaratskaia G., Zlabek V., Chen G., Madej A. Modulation of porcine cytochrome P450 enzyme activities by surgical castration and immunocastration. Animal: An International Journal of Animal Bioscience 2009, 3:1124-1132.
51. Zhao T., Sun Q., del Rincon S.V., Lovato A., Marques M., Witcher M. Gallotannin imposes S phase arrest in breast cancer cells and supresses the growth of triple-negative tumors in vivo. PLoS ONE 2014, 9:e92853.
52. Zlabek V., Zamaratskaia G. Comparison of three fluorescent CYP3A substrates in two vertebrate models, pig and Atlantic salmon. Animal: An International Journal of Animal Bioscience 2012, 6:633-640.