Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-10T11:32:56.723Z Has data issue: false hasContentIssue false

Feeding Jerusalem artichoke reduced skatole level and changed intestinal microbiota in the gut of entire male pigs

Published online by Cambridge University Press:  11 November 2011

S. G. Vhile
Affiliation:
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, PO Box 5003, N-1432 Ås, Norway
N. P. Kjos*
Affiliation:
Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, PO Box 5003, N-1432 Ås, Norway
H. Sørum
Affiliation:
Department of Food Safety and Infection Biology, Norwegian School of Veterinary Science, Ullevålsveien 72, PO Box 8146 Dep., N-0033 Oslo, Norway
M. Øverland
Affiliation:
Aquaculture Protein Centre, CoE, Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, PO Box 5003, N-1432 Ås, Norway
*
E-mail: nils.kjos@umb.no
Get access

Abstract

Different levels of dried Jerusalem artichoke were fed to entire male pigs 1 week before slaughter. The objective was to investigate the effect on skatole level in the hindgut and in adipose tissue, as well as the effect on microflora and short-chain fatty acids (SCFA) in the hindgut. Five experimental groups (n = 11) were given different dietary treatments 7 days before slaughtering: negative control (basal diet), positive control (basal diet + 9% chicory-inulin), basal diet + 4.1% Jerusalem artichoke, basal diet + 8.1% Jerusalem artichoke and basal diet + 12.2% Jerusalem artichoke. Samples from colon, rectum, faeces and adipose tissue were collected. Effect of dietary treatment on skatole, indole and androstenone levels in adipose tissue and on skatole, indole, pH, dry matter (DM), microbiota and SCFA in the hindgut was evaluated. Feeding increasing levels of Jerusalem artichoke to entire male pigs reduced skatole in digesta from colon and in faeces (linear, P < 0.01). There was also a tendency towards a decreased level of skatole in adipose tissue (linear, P = 0.06). Feeding Jerusalem artichoke decreased DM content in colon and faeces and pH in colon (linear, P < 0.01). Increasing levels of Jerusalem artichoke resulted in a reduced level of Clostridium perfringens in both colon and rectum (linear, P < 0.05) and a tendency towards decreased levels of enterobacteria in colon (linear, P = 0.05). Further, there was an increase in total amount of SCFA (linear, P < 0.05), acetic acid (linear, P < 0.05) and valerianic acid (linear, P < 0.01) in faeces. In conclusion, adding dried Jerusalem artichoke to diets for entire male pigs 1 week before slaughter resulted in a dose-dependent decrease in skatole levels in the hindgut and adipose tissue. The reduced skatole levels might be related to the decrease in C. perfringens and the increase in SCFA with subsequent reduction in pH.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2011

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

Andresen, Ø 1974. Development of a radioimmunoassay for 5alpha-androst-16-en-3-one in pig peripheral plasma. Acta Endocrinologica 76, 377387.Google ScholarPubMed
Apanavicius, CJ, Powell, KL, Vester, BM, Karr-Lilienthal, LK, Pope, LL, Fastinger, ND, Wallig, MA, Tappenden, KA, Swanson, KS 2007. Fructan supplementation and infection affect food intake, fever, and epithelial sloughing from Salmonella challenge in weanling puppies. The Journal of Nutrition 137, 19231930.CrossRefGoogle ScholarPubMed
Asp, NG 1993. Nutritional importance and classification of food carbohydrates. In Plant Polymeric Carbohydrates (ed. F Meuser, DJ Manners and W Seibel), pp. 121126. Royal Society of Chemistry, Cambridge, UK.CrossRefGoogle Scholar
Attwood, G, Li, D, Pacheco, D, Tavendale, M 2006. Production of indolic compounds by rumen bacteria isolated from grazing ruminants. Journal of Applied Microbiology 100, 12611271.CrossRefGoogle ScholarPubMed
Babol, J, Squires, EJ, Lundström, K 1999. Relationship between metabolism of androstenone and skatole in intact male pigs. Journal of Animal Science 77, 8492.CrossRefGoogle ScholarPubMed
Bonneau, M 1982. Compounds responsible for boar taint, with special emphasis on androstenone: a review. Livestock Production Science 9, 687705.CrossRefGoogle Scholar
Claus, R, Lösel, D, Lacorn, M, Mentchel, J, Schenkel, H 2003. Effects of butyrate on apoptosis in the pig colon and its consequences for skatole formation and tissue accumulation. Journal of Animal Science 81, 239248.CrossRefGoogle ScholarPubMed
Doerner, KC, Cook, KL, Mason, BP 2009. 3-Methylindole production is regulated in Clostridium scatologenes ATCC 25775. Letters in Applied Microbiology 48, 125132.CrossRefGoogle ScholarPubMed
Doran, E, Whittington, FW, Wood, JD, McGivan, JD 2002. Cytochrome P450IIE1 (CYP2E1) is induced by skatole and this induction is blocked by androstenone in isolated pig hepatocytes. Chemico-Biological Interactions 140, 8192.CrossRefGoogle ScholarPubMed
Flamm, G, Glinsmann, W, Kritchevsky, D, Prosky, L, Roberfroid, M 2001. Inulin and oligofructose as dietary fiber: a review of the evidence. Critical Reviews in Food Science and Nutrition 41, 353362.CrossRefGoogle ScholarPubMed
Gibis, M 1994. Einfluβ der Substanzen Indol und Skatol auf die Schweinefleichqualität. PhD, University of Hohenheim, Stuttgart, Germany.Google Scholar
Gibson, GR, Roberfroid, MB 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of Nutrition 125, 14011412.CrossRefGoogle ScholarPubMed
Gibson, GR, Beatty, ER, Wang, X, Cummings, JH 1995. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975982.CrossRefGoogle ScholarPubMed
Hansen, CF, Phillips, ND, La, T, Hernandez, A, Mansfield, J, Kim, JC, Mullan, BP, Hampson, DJ, Pluske, JR 2010. Diets containing inulin but not lupins help to prevent swine dysentery in experimentally challenged pigs. Journal of Animal Science 88, 33273336.CrossRefGoogle Scholar
Hansen, LL, Mejer, H, Thamsborg, SM, Byrne, DV, Roepstorff, A, Karlsson, AH, Hansen-Møller, J, Jensen, MT, Tuomola, M 2006. Influence of chicory roots (Cichorium intybus L) on boar taint in entire male and female pigs. Animal Science 82, 359368.CrossRefGoogle Scholar
Hansen-Møller, J 1994. Rapid high-performance liquid chromatographic method for simultaneous determination of androstenone, skatole and indole in back fat from pigs. Journal of Chromatography B 661, 219230.CrossRefGoogle Scholar
Hass, R, Busche, R, Luciano, L, Reale, E, Engelhardt, WV 1997. Lack of butyrate is associated with induction of Bax and subsequent apoptosis in the proximal colon of guinea pig. Gastroenterology 112, 875881.CrossRefGoogle ScholarPubMed
Jensen, MT, Jensen, BB 1994. Gas chromatographic determination of indole and 3-methylindole (skatole) in bacterial culture media, intestinal contents and faeces. Journal of Chromatography B 655, 275280.CrossRefGoogle ScholarPubMed
Jensen, MT, Hansen, LL 2006. Feeding with chicory roots reduces the amount of odorous compounds in colon and rectal contents of pigs. Animal Science 82, 369376.CrossRefGoogle Scholar
Jensen, MT, Cox, RP, Jensen, BB 1995a. Microbial production of skatole in the hind gut of pigs given different diets and its relation to skatole deposition in backfat. Animal Science 61, 293304.CrossRefGoogle Scholar
Jensen, MT, Cox, RP, Jensen, BB 1995b. 3-Methylindole (Skatole) and Indole production by mixed populations of pig fecal bacteria. Applied and Environmental Microbiology 61, 31803184.CrossRefGoogle ScholarPubMed
Jensen, AN, Mejer, H, Mølbak, L, Langkjær, M, Jensen, TK, Angen, Ø, Martinussen, T, Klitgaard, K, Baggesen, DL, Thamsborg, SM, Roepstorff, A 2011. The effect of a diet with fructan-rich chicory roots on intestinal helminths and microbiota with special focus on Bifidobacteria and Campylobacter in piglets around weaning. Animal 5, 851860.CrossRefGoogle ScholarPubMed
Kleessen, B, Schwarz, S, Boehm, A, Fuhrmann, H, Richter, A, Henle, T, Krueger, M 2007. Jerusalem artichoke and chicory inulin in bakery products affect faecal microbiota of healthy volunteers. British Journal of Nutrition 98, 540549.CrossRefGoogle ScholarPubMed
Knarreborg, A, Beck, J, Jensen, MT, Laue, A, Agergaard, N, Jensen, BB 2002. Effect of non-starch polysaccharides on production and absorption of indolic compounds in entire male pigs. Animal Science 74, 445453.CrossRefGoogle Scholar
Kolida, S, Gibson, G 2007. Prebiotic capacity of inulin-type fructans. The Journal of Nutrition 137 (suppl. 11), 2503S2506S.CrossRefGoogle ScholarPubMed
Mentschel, J, Claus, R 2003. Increased butyrate formation in the pig colon by feeding raw potato starch leads to a reduction of colonocyte apoptosis and a shift to the stem cell compartment. Metabolism 52, 14001405.CrossRefGoogle Scholar
Norwegian Ministry of Agriculture and Food 2008. Dyr: Forbudet mot kastrering av gris er utsatt. Retrieved August 9, 2011 from http://www.regjeringen.no/en/dep/lmd/aktuelt/nyheter/2008/nov-08/dyr-forbudet-mot-kastrering-av-gris-er-u.html?id=536264Google Scholar
National Research Council (NRC) 1998. Nutrient Requirements of Swine, 10th revised edition (ed. Sine nomine), pp. 117122. National Academy Press, Washington, DC, USA.Google Scholar
Øverland, M, Kjos, NP, Fauske, AK, Teige, J, Sørum, H 2011. Easily fermentable carbohydrates reduce skatole formation in the distal intestine of entire male pigs. Livestock Science 140, 206217.CrossRefGoogle Scholar
Øverland, M, Granli, T, Kjos, NP, Fjetland, O, Stokstad, M, Steien, SH 2000. Effect of dietary formates on growth performance, carcass traits, sensory quality, intestinal microflora and stomach alteration in growth-finishing pigs. Journal of Animal Science 78, 18751884.CrossRefGoogle Scholar
Pauly, C, Spring, P, O'Doherty, JV, Ampuero Kragten, S, Bee, G 2008. Performances, meat quality and boar taint of castrates and entire male pigs fed a standard and a raw potato starch-enriched diet. Animal 2, 17071715.CrossRefGoogle Scholar
Ramnani, P, Gaudier, E, Bingham, M, van Bruggen, P, Tuohy, KM, Gibson, GR 2010. Prebiotic effect of fruit and vegetable shots containing Jerusalem artichoke inulin: a human intervention study. British Journal of Nutrition 104, 233240.CrossRefGoogle ScholarPubMed
Roberfroid, MB 2005. Introducing inulin-type fructans. British Journal of Nutrition 93, S13S25.CrossRefGoogle ScholarPubMed
Roberfroid, MB 2007. Inulin-type fructans: functional food ingredients. The Journal of Nutrition 137 (suppl. 11), 2493S2502S.CrossRefGoogle ScholarPubMed
SAS Institute 1990. SAS Users Guide. SAS Institute Inc., Cary, NC, USA.Google Scholar
Slimestad, R, Seljaasen, R, Meijer, K, Skar, SL 2010. Norwegian-grown Jerusalem artichoke (Helianthus tuberosus L.): morphology and content of sugars and fructo-oligosaccharides in stems and tubers. Journal of the Science of Food and Agriculture 90, 956964.CrossRefGoogle ScholarPubMed
Swanson, KMJ, Busta, FF, Peterson, EH, Johnson, MG 1992. Colony count methods. In Compendium of methods for the microbiological examination of foods, (ed. C Vanderzant and DF Splittstoesser), pp. 7595. American Public Health Association, Washington, DC, USA.Google Scholar
Tuomola, M, Harpio, R, Knuuttila, P, Mikola, H, Lövgren, T 1997. Time-resolved fluoroimmunoassay for the measurement of androstenone in porcine serum and fat samples. Journal of Agricultural and Food Chemistry 45, 35293534.CrossRefGoogle Scholar
Whittington, FM, Nute, GR, Hughes, SI, McGivan, JD, Lean, IJ, Wood, JD, Doran, E 2004. Relationships between skatole and androstenone accumulation, and cytochrome P4502E1 expression in Meishan × Large White pigs. Meat Science 67, 569576.CrossRefGoogle Scholar
Xu, ZR, Hu, CH, Wang, MQ 2002. Effects of fructooligosaccharide on conversion of l-tryptophan to skatole and indole by mixed populations of pig fecal bacteria. Journal of General and Applied Microbiology 48, 8389.CrossRefGoogle ScholarPubMed
Yokoyama, MT, Carlson, JR, Holdeman, LV 1977. Isolation and characteristics of a skatole-producing Lactobacillius sp. from the bovine rumen. Applied and Environmental Microbiology 34, 837842.CrossRefGoogle Scholar
Zamaratskaia, G 2004. Factors involved in the development of boar taint. Influence of breed, age, diet and raising conditions. PhD, Swedish University of Agricultural Sciences, Uppsala, Sweden.Google Scholar
Zamaratskaia, G, Babol, J, Andersson, HK, Andersson, K, Lundström, K 2004a. 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 93, 235243.CrossRefGoogle Scholar
Zamaratskaia, G, Babol, J, Andersson, H, Lundström, K 2004b. 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, 9198.CrossRefGoogle Scholar