Preliminary Test of the Reduction Capacity for the Intestinal Adsorption of Skatole and Indole in Weaning Piglets by Pure and Coated Charcoal
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals and Housing
2.2. Diets and Feeding Concept
2.3. Experimental Procedure
2.4. Dissection
2.5. Sample Preparation and Analyses
2.6. Skatole and Indole Adsorption In Vitro
2.7. Statistical Analysis
3. Results and Discussions
3.1. Reduction in Skatole and Indole In Vitro
3.2. Performance Parameters
3.3. Reduction in Skatole and Indole In Vivo
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Lundström, K.; Matthews, K.; Haugen, J.-E. Pig meat quality from entire males. Animal 2009, 3, 1497–1507. [Google Scholar] [CrossRef] [Green Version]
- Øverland, M.; Kjos, N.; Fauske, A.; Teige, J.; Sørum, H. Easily fermentable carbohydrates reduce skatole formation in the distal intestine of entire male pigs. Livest. Sci. 2011, 140, 206–217. [Google Scholar] [CrossRef]
- Claus, R.; Weiler, U.; Herzog, A. Physiological aspects of androstenone and skatole formation in the boar—A review with experimental data. Meat Sci. 1994, 38, 289–305. [Google Scholar] [CrossRef]
- Garcia-Regueiro, J.; Diaz, I. Evaluation of the contribution of skatole, indole, androstenone and androstenols to boar-taint in back fat of pigs by HPLC and capillary gas chromatography (CGC). Meat Sci. 1989, 25, 307–316. [Google Scholar] [CrossRef]
- Deslandes, B.t.; Gariépy, C.; Houde, A. Review of microbiological and biochemical effects of skatole on animal production. Livest. Prod. Sci. 2001, 71, 193–200. [Google Scholar] [CrossRef]
- Doran, E.; Whittington, F.W.; Wood, J.D.; McGivan, J.D. Cytochrome P450IIE1 (CYP2E1) is induced by skatole and this induction is blocked by androstenone in isolated pig hepatocytes. Chem.-Biol. Interact. 2002, 140, 81–92. [Google Scholar] [CrossRef]
- Leong, J.; Morel, P.C.; Purchas, R.W.; Wilkinson, B.H. Effects of dietary components including garlic on concentrations of skatole and indole in subcutaneous fat of female pigs. Meat Sci. 2011, 88, 45–50. [Google Scholar] [CrossRef]
- Agergaard, N.; Laue, A. Absorption from the gastrointestinal tract and liver turnover of skatole. In Measurement and Prevention of Boar Taint in Entire Male Pigs; Bonneau, M., Ed.; INRA: Paris, France, 1993; pp. 107–111. [Google Scholar]
- Borg Jensen, B.; Jensen, M.T. 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; Bonneau, M., Ed.; INRA: Paris, France, 1993; pp. 99–105. [Google Scholar]
- Hansen-Møller, J. Analytical methods for determination of boar taint compounds. Skatole Boar Taint 1998, 21–40. [Google Scholar]
- 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. J. Anim. Sci. 2003, 81, 239–248. [Google Scholar] [CrossRef] [PubMed]
- Zamaratskaia, G.; Babol, J.; Andersson, H.; 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. Livest. Prod. Sci. 2005, 93, 235–243. [Google Scholar] [CrossRef]
- Hansen, L.L.; Mejer, H.; Thamsborg, S.M.; Byrne, D.V.; Roepstorff, A.; Karlsson, A.H.; Hansen-Møller, J.; Jensen, M.T.; Tuomola, M. Influence of chicory roots (Cichorium intybus L.) on boar taint in entire male and female pigs. Anim. Sci. 2006, 82, 359–368. [Google Scholar] [CrossRef] [Green Version]
- Knarreborg, A.; Beck, J.; Jensen, M.; Laue, A.; Agergaard, N.; Jensen, B.B. Effect of non-starch polysaccharides on production and absorption of indolic compounds in entire male pigs. Anim. Sci. 2002, 74, 445–453. [Google Scholar] [CrossRef]
- Whittington, F.; Nute, G.; Hughes, S.; McGivan, J.; Lean, I.; Wood, J.; Doran, E. Relationships between skatole and androstenone accumulation, and cytochrome P4502E1 expression in Meishan× Large White pigs. Meat Sci. 2004, 67, 569–576. [Google Scholar] [CrossRef] [PubMed]
- Van Oeckel, M.; Warnants, N.; De Paepe, M.; Casteels, M.; Boucqué, C.V. Effect of fibre-rich diets on the backfat skatole content of entire male pigs. Livest. Prod. Sci. 1998, 56, 173–180. [Google Scholar] [CrossRef]
- Sander, S.; Osterhues, A.; Tabeling, R.; Kamphues, J. Boar taint-influences of genetics, feeding and housing. Übers. Tierernähr. 2012, 40, 65–111. [Google Scholar]
- Jen, K.; Squires, E. Efficacy of non-nutritive sorbent materials as intestinal-binding agents for the control of boar taint. Animal 2011, 5, 1814–1820. [Google Scholar] [CrossRef]
- European Union. VERORDNUNG (EU) Nr. 68/2013 Der Kommission Vom 16. Januar 2013 Zum Katalog Der Einzelfuttermittel (Text Von Bedeutung Für Den EWR); EU Commission, E., Ed.; EU Commission: Brussels, Belgium, 2013. [Google Scholar]
- Schmidt, H.-P.; Hagemann, N.; Draper, K.; Kammann, C. The use of biochar in animal feeding. PeerJ 2019, 7, e7373. [Google Scholar] [CrossRef] [Green Version]
- Choi, J.; Shinde, P.; Kwon, I.; Song, Y.; Chae, B.-J. Effect of Wood Vinegar on the Performance, Nutrient Digestibility and Intestinal Microflora in Weanling Pigs. Asian-Australas. J. Anim. Sci. 2009, 22, 267. [Google Scholar] [CrossRef]
- Witte, F.; Menger, F.; Schubert, D.; Heinz, V.; Visscher, C.; Terjung, N. Reduction of Skatole and Indole in Fat, Liver and Lean Meat by a Feeding Approach with Charcoal. In Proceedings of the 65th ICoMST—International Congress of Meat Science and Technologies, Potsdam, Germany, 4–9 August 2019; pp. 286–287. [Google Scholar]
- Schubert, D.C.; Chuppava, B.; Witte, F.; Terjung, N.; Visscher, C. Effect of two different biochars as a component of compound feed on nutrient digestibility and performance parameters in growing pigs. Front. Anim. Sci. 2021, 2, 760. [Google Scholar] [CrossRef]
- Lanthier, F.; Lou, Y.; Terner, M.; Squires, E. Characterizing developmental changes in plasma and tissue skatole concentrations in the prepubescent intact male pig. J. Anim. Sci. 2006, 84, 1699–1708. [Google Scholar] [CrossRef] [Green Version]
- Gesellschaft für Ernährungsphysiologie. Empfehlungen Zur Energie- Und Nährstoffversorgung Von Schweinen; DLG Verlag: Frankfurt, Germany, 2006. [Google Scholar]
- Gibis, M.; Dehnhard, M.; Fischer, A. Einfluss der Substanzen Indol und Skatol auf die Schweinefleischqualität. Z. Lebensm.-Forsch. 1991, 220–223. [Google Scholar] [CrossRef]
- Naumann, C.; Bassler, R. Methoden der landwirtschaftlichen Forschungs-und Untersuchungsanstalt, Biochemische Untersuchung von Futtermitteln. In Methodenbuch III (Einschließlich Der Achten Ergänzungen); VDLUFA: Darmstadt, Germany, 2012. [Google Scholar]
- Jen, K.; Squires, E. In vitro assessment of the effectiveness of non-nutritive sorbent materials as binding agents for boar taint compounds. Animal 2011, 5, 1821–1828. [Google Scholar] [CrossRef] [PubMed]
- Man, K.Y.; Chow, K.L.; Man, Y.B.; Mo, W.Y.; Wong, M.H. Use of biochar as feed supplements for animal farming. Crit. Rev. Environ. Sci. Technol. 2021, 51, 187–217. [Google Scholar] [CrossRef]
- Lanthier, F.; Lou, Y.; Squires, E. Skatole metabolism in the intact pre-pubescent male pig: The relationship between hepatic enzyme activity and skatole concentrations in plasma and fat. Livest. Sci. 2007, 106, 145–153. [Google Scholar] [CrossRef]
- Kjos, N.; Øverland, M.; Fauske, A.; Sørum, H. Feeding chicory inulin to entire male pigs during the last period before slaughter reduces skatole in digesta and backfat. Livest. Sci. 2010, 134, 143–145. [Google Scholar] [CrossRef]
- Aluwé, M.; Millet, S.; Nijs, G.; Tuyttens, F.; Verheyden, K.; De Brabander, H.; De Brabander, D.; Van Oeckel, M. Absence of an effect of dietary fibre or clinoptilolite on boar taint in entire male pigs fed practical diets. Meat Sci. 2009, 82, 346–352. [Google Scholar] [CrossRef]
- Baltic, M.; Raicevic, S.; Tadic, I.; Drljacic, A. Influence of zeolite on skatole content of swine fat tissue. In Boar Taint in Entire Male Pigs, Proceedings of the Meeting of the EAAP Working Group Production and Utilisation of Meat from Entire Male Pigs, Stockholm, Sweden, 1–3 October 1997; Wageningen Pers: Wageningen, The Netherlands, 1997. [Google Scholar]
Item | Percentage |
---|---|
Barley | 35.0 |
Wheat | 16.0 |
Soybean meal * | 15.0 |
Maize | 15.0 |
Waffle meal | 4.0 |
Wheat bran | 4.0 |
Beet pulp | 1.0 |
Sunflower extraction meal | 1.0 |
Fish protein concentrate | 1.0 |
Premix ** | 8.0 |
CON | PURE | COAT | ||
---|---|---|---|---|
Organic matter | g/kg DM | 947 | 947 | 946 |
Crude protein | 192 | 186 | 189 | |
Ether extract | 50.6 | 61.2 | 51.8 | |
Crude fibre | 52.4 | 55.7 | 53.3 | |
NfE 1 | 652 | 644 | 652 | |
Calcium | 7.17 | 7.55 | 7.75 | |
Phosphorus | 5.43 | 5.34 | 5.53 | |
Potassium | 7.22 | 7.10 | 7.09 | |
Magnesium | 2.16 | 2.12 | 2.16 | |
Copper | mg/kg DM | 51.5 | 49.5 | 51.2 |
Zinc | 153 | 164 | 152 | |
Iron | 409 | 455 | 406 |
Indole Reduction (%) | Skatole Reduction (%) | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
PURE | COAT | FAT | PURE | COAT | FAT | |||||||
Colon chyme | 18.80 ± 4.22 | a 0.005 | 14.53 ± 0.73 | a 0.019 | 1.00 ± 0.00 | b | 17.57 ± 1.82 | a 0.007 (to b) | 9.17 ± 1.12 | b 0.008 (to c) | 1.00 ± 0.00 | c < 0.001 (to a) |
Caecum chyme | 24.40 ± 0.81 | a < 0.001 | 17.53 ± 3.20 | a 0.003 | 1.60 ± 0.60 | b | 22.10 ± 0.32 | a < 0.001 | 14.20 ± 3.31 | a 0.007 | 1.00 ± 0.00 | b |
Water | 90.03 ± 0.20 | a <0.001 | 19.80 ± 1.08 | b < 0.001 | 1.00 ± 0.00 | c < 0.001 | 99.73 ± 0.09 | a < 0.001 | 33.43 ± 2.97 | b < 0.001 | 1.00 ± 0.00 | c < 0.001 |
Colon Chyme | Caecum Chyme | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Indole (µg/g DM) | Skatole (µg/g DM) | Indole (µg/g DM) | Skatole (µg/g DM) | |||||||||
CON | PURE | COAT | CON | PURE | COAT | CON | PURE | COAT | CON | PURE | COAT | |
8.11 ± 0.69 a | 12.28 ± 1.28 a | 1.32 ± 0.00 a | 62.39 ± 3.83 a c | 21.51 ± 1.84 a | 1.32 ± 0.00 a | 41.30 ± 1.80 a | 15.65 ± 3.39 a | 27.86 ± 1.88 a | 13.83 ± 0.08 a | 2.04 ± 0.00 a | 2.91 ± 0.00 a | |
12.18 ± 0.95 a | 1.40 ± 0.00 b | 3.08 ± 0.41 a | 169.01 ± 11.61 b | 84.11 ± 9.40 b | 51.68 ± 4.53 b | 9.26 ± 1.19 b | 2.48 ± 0.00 b | 2.68 ± 0.49 b | 26.93 ± 6.27 a | 3.67 ± 0.60 a b | 2.30 ± 0.11 a | |
8.83 ± 0.25 a | 5.14 ± 1.02 b | 1.66 ± 0.00 a | 38.01 ± 1.45 a | 35.17 ± 2.66 a | 38.43 ± 0.49 c | 5.90 ± 1.11 b | 12.72 ± 0.87 a b | 2.38 ± 0.00 b | 2.27 ± 0.00 a | 2.04 ± 0.00 b | 2.63 ± 0.18 a | |
23.46 ± 3.32 b | 2.30 ± 0.58 b | 1.59 ± 0.00 a | 73.31 ± 5.08 c e | 85.28 ± 6.43 b | 46.72 ± 2.28 bc | 8.22 ± 0.50 b | 38.20 ± 1.90 c | 2.11 ± 0.00 b | 81.16 ± 5.84 b | 46.43 ± 3.47 c | 13.90 ± 2.40 b | |
24.12 ± 1.83 b | 27.57 ± 2.06 c | 1.55 ± 0.00 a | 4.18 ± 0.43 d | 69.02 ± 5.10 b | 20.57 ± 1.59 d | 23.93 ± 4.65 a b | 45.82 ± 4.92 c | 2.36 ± 0.14 b | 2.44 ± 0.00 a | 2.94 ± 0.00 a b | 2.22 ± 0.00 a | |
14.38 ± 1.41 a | 33.02 ± 1.98 c | 32.19 ± 3.31 b | 95.83 ± 6.82 e | 13.33 ± 0.80 a | 37.29 ± 2.11 c | 48.23 ± 5.30 a b | 11.17 ± 1.16 a b | 10.35 ± 1.27 c | 18.38 ± 2.34 a | 2.83 ± 0.37 a b | 2.59 ± 0.00 a | |
Mean | 15.18 ± 1.67 A | 13.62 ± 3.04 A | 6.90 ± 2.79 A | 73.79 ± 12.62 A | 51.40 ± 7.32 AB | 32.67 ± 4.21 B | 18.25 ± 3.62 AB | 21.01 ± 3.87 A | 7.96 ± 2.30 B | 22.48 ± 6.82 A | 9.99 ± 3.99 AB | 4.42 ± 1.08 B |
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Witte, F.; Pajic, A.; Menger, F.; Tomasevic, I.; Schubert, D.C.; Visscher, C.; Terjung, N. Preliminary Test of the Reduction Capacity for the Intestinal Adsorption of Skatole and Indole in Weaning Piglets by Pure and Coated Charcoal. Animals 2021, 11, 2720. https://doi.org/10.3390/ani11092720
Witte F, Pajic A, Menger F, Tomasevic I, Schubert DC, Visscher C, Terjung N. Preliminary Test of the Reduction Capacity for the Intestinal Adsorption of Skatole and Indole in Weaning Piglets by Pure and Coated Charcoal. Animals. 2021; 11(9):2720. https://doi.org/10.3390/ani11092720
Chicago/Turabian StyleWitte, Franziska, Aleksandar Pajic, Florian Menger, Igor Tomasevic, Dana Carina Schubert, Christian Visscher, and Nino Terjung. 2021. "Preliminary Test of the Reduction Capacity for the Intestinal Adsorption of Skatole and Indole in Weaning Piglets by Pure and Coated Charcoal" Animals 11, no. 9: 2720. https://doi.org/10.3390/ani11092720