The effects of inulin, dried Jerusalem artichoke tuber and a multispecies probiotic preparation on microbiota ecology and immune status of the large intestine in young pigs

Archives of Animal Nutrition

Volumn 70, Issue 4, 2016, Pages 278-292

  Barszcz, Marcin ^a   Taciak, Marcin ^a   Skomiał, Jacek ^a  

^a POLISH ACADEMY OF SCIENCES   (Poland)

Author keywords

Fermentation; immunity; intestinal microorganisms; inulin; piglets; prebiotics; probiotics

Indexed keywords

INULIN; PREBIOTIC AGENT; PROBIOTIC AGENT;

ANALYSIS; ANIMAL; ANIMAL FOOD; BACTERIUM; CECUM; CHEMISTRY; COLON; DIET; IMMUNOLOGY; INNATE IMMUNITY; MALE; MICROBIOLOGY; PIG; SUNFLOWER; VETERINARY;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BACTERIA; CECUM; COLON; DIET; HELIANTHUS; IMMUNITY, INNATE; INULIN; MALE; PREBIOTICS; PROBIOTICS; SUS SCROFA;

EID: 84975283379     PISSN: 1745039X     EISSN: 14772817     Source Type: Journal    
DOI: 10.1080/1745039X.2016.1184368     Document Type: Article

References (48)

1. S.Almagro-Moreno, K.Pruss, R.K.Taylor 2015. Intestinal colonization dynamics of Vibrio cholerae. PLoS Pathog. 11:e1004787.
2. E.Amit-Romach, D.Sklan, Z.Uni. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci. 83:1093–1098.
3. [AOAC] Association of Official Analytical Chemists. 2000. Official methods of analysis of AOAC. 17th ed. Washington, DC: Association of Official Analytical Chemists.
4. M.Barszcz, M.Taciak, J.Skomiał. 2011. A dose-response effects of tannic acid and protein on growth performance, caecal fermentation, colon morphology, and β-glucuronidase activity of rats. J Anim Feed Sci. 20:613–625.
5. V.Bontempo, A.Di Giancamillo, G.Savoini, V.Dell’Orto, C.Domeneghini. 2006. Live yeast dietary supplementation acts upon intestinal morpho-functional aspects and growth in weanling piglets. Anim Feed Sci Technol. 129:224–236.
6. M.E.Davis, C.V.Maxwell, G.F.Erf, D.C.Brown, T.J.Wistuba. 2004. Dietary supplementation with phosphorylated mannans improves growth response and modulates immune function of weanling pigs. J Anim Sci. 82:1882–1891.
7. K.Desrouillères, M.Millette, K.D.Vu, R.Touja, M.Lacroix. 2015. Cancer preventive effects of a specific probiotic fermented milk containing Lactobacillus acidophilus CL1285, L. casei LBC80R and L. rhamnosus CLR2 on male F344 rats treated with 1,2-dimethylhydrazine. J Funct Foods. 17:816–827.
8. M.Eberhard, U.Hennig, S.Kuhla, R.M.Brunner, B.Kleessen, C.C.Metges. 2007. Effect of inulin supplementation on selected gastric, duodenal, and caecal microbiota and short chain fatty acid pattern in growing piglets. Arch Anim Nutr. 61:235–246.
9. European Commission. 2003. European Union register of feed additives. Edition 228. Regulation (EC) No 1831/2003. Appendixes 3e, 4 – 18.04.2016. 1–192.
10. E.R.Farnworth, H.W.Modler, D.A.Mackie. 1995. Adding Jerusalem artichoke (Helianthus tuberosus L.) to weanling pig diets and the effect on manure composition and characteristics. Anim Feed Sci Technol. 55:153–160.
11. M.L.Forchielli, W.A.Walker. 2005. The role of gut-associated lymphoid tissue and mucosal defence. Brit J Nutr. 93:S41–S48.
12. D.Halas, C.F.Hansen, D.J.Hampson, B.P.Mullan, J.C.Kim, R.H.Wilson, J.R.Pluske. 2010. Dietary supplementation with benzoic acid improves apparent ileal digestibility of total nitrogen and increases villous height and caecal microbial diversity in weaner pigs. Anim Feed Sci Technol. 160:137–147.
13. K.Hod, Y.Ringel. 2016. Probiotics in functional bowel disorders. Best Pract Res Clin Gastroenterol. 30:89–97.
14. L.V.Hooper, D.R.Littman, A.J.Macpherson. 2012. Interactions between the microbiota and the immune system. Science. 336:1268–1273.
15. Y.Hou, L.Wang, D.Yi, B.Ding, X.Chen, Q.Wang, H.Zhu, Y.Liu, Y.Yin, J.Gong, G.Wu. 2014. Dietary supplementation with tributyrin alleviates intestinal injury in piglets challenged with intrarectal administration of acetic acid. Brit J Nutr. 111:1748–1758.
16. R.Isaacson, H.B.Kim. 2012. The intestinal microbiome of the pig. Anim Health Res Rev. 13:100–109.
17. H.Ito, T.Wada, M.Ohguchi, K.Sugiyama, S.Kiriyama, T.Morita. 2008. The degree of polymerization of inulin-like fructans affects cecal mucin and immunoglobulin A in rats. J Food Sci. 73:H36–H41.
18. J.Juskiewicz, Z.Zdunczyk, M.Wroblewska, J.Oszmianski, T.Hernandez. 2002. The response of rats to feeding with diets containing grapefruit flavonoid extract. Food Res Int. 35:201–205.
19. P.Kaufmann, A.Pfefferkorn, M.Teuber, L.Meile. 1997. Identification and quantification of Bifidobacterium species isolated from food with genus-specific 16S rRNA-targeted probes by colony hybridization and PCR. Appl Environ Microbiol. 63:1268–1273.
20. L.Kocsis, P.Liebhard, W.Praznik. 2007. Effect of seasonal changes on content and profile of soluble carbohydrates in tubers of different varieties of Jerusalem artichoke (Helianthus tuberosus L.). J Agric Food Chem. 55:9401–9408.
21. J.Kunisawa, I.Takahashi, H.Kiyono. 2007. Intraepithelial lymphocytes: their shared and divergent immunological behaviors in the small and large intestine. Immunol Rev. 215:136–153.
22. C.Lauridsen, E.-M.Vestergaard, S.Højsgaard, S.K.Jensen, M.T.Sørensen. 2011. Inoculation of weaned pigs with E. coli reduces depots of vitamin E. Livest Sci. 137:161–167.
23. C.Mair, C.Plitzner, K.J.Domig, K.Schedle, W.Windisch. 2010. Impact of inulin and a multispecies probiotic formulation on performance, microbial ecology and concomitant fermentation patterns in newly weaned piglets. J Anim Physiol Anim Nutr. 94:e164–e177.
24. J.Matías, J.González, L.Royano, R.A.Barrena. 2011. Analysis of sugars by liquid chromatography – mass spectrometry in Jerusalem artichoke tubers for bioethanol production optimization. Biomass Bioenerg. 35:2006–2012.
25. L.Mølbak, L.E.Thomsen, T.K.Jensen, K.E.Bach Knudsen, M.Boye. 2007. Increased amount of Bifidobacterium thermacidophilum and Megasphaera elsdenii in the colonic microbiota of pigs fed a swine dysentery preventive diet containing chicory roots and sweet lupine. J Appl Microbiol. 103:1853–1867.
26. Y.Nakamura, S.Nosaka, M.Suzuki, S.Nagafuchi, T.Takahashi, T.Yajima, N.Takenouchi-Ohkubo, T.Iwase, I.Moro. 2004. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clin Exp Immunol. 137:52–58.
27. I.Nochta, T.Tuboly, L.Babinszky. 2009. Effect of different levels of mannan-oligosaccharide supplementation on some immunological variables in weaned piglets. J Anim Physiol Anim Nutr. 93:496–504.
28. C.L.Ohland, W.K.MacNaughton. 2010. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 298:G807–G819.
29. N.Paßlack, M.Al-samman, W.Vahjen, K.Männer, J.Zentek. 2012. Chain length of inulin affects its degradation and the microbiota in the gastrointestinal tract of weaned piglets after a short-term dietary application. Livest Sci. 149:128–136.
30. H.S.Rasmussen, K.Holtug, P.B.Mortensen. 1988. Degradation of amino acids to short-chain fatty acids in humans: an in vitro study. Scand J Gastroenterol. 23:178–182.
31. W.Saengthongpinit, T.Sajjaanantakul. 2005. Influence of harvest time and storage temperature on characteristics of inulin from Jerusalem artichoke (Helianthus tuberosus L.) tubers. Postharvest Biol Tec. 37:93–100.
32. P.J.Sansonetti. 2004. War and peace at mucosal surfaces. Nat Rev Immunol. 4:953–964.
33. K.M.Schachtschneider, C.J.Yeoman, R.E.Isaacson, B.A.White, L.B.Schook, M.Pieters. 2013. Modulation of systemic immune responses through commensal gastrointestinal microbiota. PLoS One. 8:e53969.
34. S.Seifert, B.Watzl. 2007. Inulin and oligofructose: review of experimental data on immune modulation. J Nutr. 137:2563S–2567S.
35. I.Sekirov, S.L.Russell, L.C.M.Antunes, B.B.Finlay. 2010. Gut microbiota in health and disease. Physiol Rev. 90:859–904.
36. S.Y.Shiau, G.W.Chang. 1983. Effects of dietary fiber on fecal mucinase and β-glucuronidase activity in rats. J Nutr. 113:138–144.
37. E.Tako, R.P.Glahn, R.M.Welch, X.Lei, K.Yasuda, D.D.Miller. 2008. Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. Brit J Nutr. 99:472–480.
38. H.M.Timmerman, C.J.M.Koning, L.Mulder, F.M.Rombouts, A.C.Beynen. 2004. Monostrain, multistrain and multispecies probiotics – a comparison of functionality and efficacy. Int J Food Microbiol. 96:219–233.
39. H.Y.Tsen, C.K.Lin, W.R.Chi. 1998. Development and use of 16S rRNA gene targeted PCR primers for the identification of Escherichia coli cells in water. J Appl Microbiol. 85:554–560.
40. A.Valdovska, A.Jemeljanovs, M.Pilmane, I.Zitare, I.H.Konosonoka, M.Lazdins. 2014. Alternative for improving gut microbiota: use of Jerusalem artichoke and probiotics in diets of weaned piglets. Pol J Vet Sci. 17:61–69.
41. M.Valeri, S.Rossi Paccani, M.Kasendra, B.Nesta, L.Serino, M.Pizza, M.Soriani. 2015. Pathogenic E. coli exploits SslE mucinase activity to translocate through the mucosal barrier and get access to host cells. PLoS One. 10:e0117486.
42. J.M.A.J.Verdonk, S.B.Shim, P.van Leeuwen, M.W.A.Verstegen. 2005. Application of inulin-type fructans in animal feed and pet food. Brit J Nutr. 93:S125–S138.
43. S.G.Vhile, N.P.Kjos, H.Sørum, M.Øverland. 2012. Feeding Jerusalem artichoke reduced skatole level and changed intestinal microbiota in the gut of entire male pigs. Animal. 6:807–814.
44. L.Vogt, D.Meyer, G.Pullens, M.Faas, M.Smelt, K.Venema, U.Ramasamy, H.A.Schols, P.De Vos. 2015. Immunological properties of inulin-type fructans. Crit Rev Food Sci Nutr. 55:414–436.
45. R.F.Wang, W.W.Cao, C.E.Cerniglia. 1996. PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Appl Environ Microbiol. 62:1242–1247.
46. P.J.Weimer, G.N.Moen. 2013. Quantitative analysis of growth and volatile fatty acid production by the anaerobic ruminal bacterium Megasphaera elsdenii T81. Appl Microbiol Biotechnol. 97:4075–4081.
47. K.Windey, V.De Preter, K.Verbeke. 2012. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 56:184–196.
48. X.Y.Zhu, T.Zhong, Y.Pandya, R.D.Joerger. 2002. 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl Environ Microbiol. 68:124–137.