Influence of different inclusion levels and chain length of inulin on microbial ecology and the state of mucosal protective barrier in the large intestine of young pigs
M. Barszcz A B , M. Taciak A and J. Skomiał A
+ Author Affiliations
- Author Affiliations
A The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, 05-110 Jabłonna, Poland.
B Corresponding author. Email: m.barszcz@ifzz.pl
Animal Production Science 58(6) 1109-1118 https://doi.org/10.1071/AN16014
Submitted: 7 January 2016 Accepted: 16 November 2016 Published: 30 January 2017
Abstract
The objective of the study was to examine the effect of inulin level, in regard to its degree of polymerisation (DP), on microbial activity and mucosal immune system of the large intestine of pigs. A total of 56 castrated male piglets (PIC × Penarlan P76) were allocated to seven groups and fed from the 10th day of life cereal-based diets without the addition of inulin or with 1%, 2% or 3% of inulin with an average DP of 10 (IN10) or 23 (IN23). Pigs were sacrificed at the age of 50 days. Feeding IN10 diets increased fructan concentration in the large intestine compared with IN23 diets, but did not affect microbial activity, except for digesta pH and mucinase activity in the middle colon, which were greater at the 1% level compared with the control group and other IN10 diets, respectively. The concentration of secretory immunoglobulin A in the caecum and middle colon was reduced by the 1% IN10 diet compared with the control group. Pigs fed the 2% IN23 diet had a higher butyric acid concentration in the caecum and proximal colon and greater isoacid concentrations in the middle and distal colon in comparison to the control. Dietary level of IN23 did not affect secretory immunoglobulin A concentration but the count of caecal intraepithelial lymphocytes was higher in pigs on the 1% IN23 diet than on the control diet. Neither IN10 nor IN23 diets affected populations of Bifidobacterium or Lactobacillus spp. In conclusion, the effects of inulin in the large intestine of pigs depended on dietary level and DP. IN23 increased short-chain fatty acid production at the 2% level and slightly activated mucosal immune status at the 1% level.
Additional keywords: fermentation, fructans, intraepithelial lymphocytes, microbiota, secretory immunoglobulin A.
References
Almagro-Moreno S, Pruss K, Taylor RK (2015) Intestinal colonization dynamics of Vibrio cholerae. PLoS Pathogens 11, e1004787| Intestinal colonization dynamics of Vibrio cholerae.Crossref | GoogleScholarGoogle Scholar |
Amit-Romach E, Sklan D, Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poultry Science 83, 1093–1098.
| Microflora ecology of the chicken intestine using 16S ribosomal DNA primers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Oktr0%3D&md5=1386642f64cc98edc1c59afb9cb82dc8CAS |
Apolinário AC, de Lima Damasceno BPG, de Macêdo Beltrão NE, Pessoa A, Converti A, da Silva JA (2014) Inulin-type fructans: a review on different aspects of biochemical and pharmaceutical technology. Carbohydrate Polymers 101, 368–378.
| Inulin-type fructans: a review on different aspects of biochemical and pharmaceutical technology.Crossref | GoogleScholarGoogle Scholar |
Association of Official Analytical Chemists (AOAC) (2000) ‘Methods of analysis of AOAC International.’ 17th edn. (AOAC, Arlington, VA)
Barszcz M, Taciak M, Skomiał J (2011) A dose-response effects of tannic acid and protein on growth performance, caecal fermentation, colon morphology, and β-glucuronidase activity of rats. Journal of Animal and Feed Sciences 20, 613–625.
| A dose-response effects of tannic acid and protein on growth performance, caecal fermentation, colon morphology, and β-glucuronidase activity of rats.Crossref | GoogleScholarGoogle Scholar |
Barszcz M, Taciak M, Skomiał J (2016) 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 70, 278–292.
| 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.Crossref | GoogleScholarGoogle Scholar |
Bauer E, Williams BA, Smidt H, Verstegen MWA, Mosenthin R (2006) Influence of the gastrointestinal microbiota on development of the immune system in young animals. Current Issues in Intestinal Microbiology 7, 35–52.
Blachier F, Mariotti F, Huneau JF, Tomé D (2007) Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33, 547–562.
| Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSlsrnO&md5=8cd78078da8edd76a4dc1d1a69f4b68eCAS |
Desrouillères K, Millette M, Vu KD, Touja R, Lacroix M (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. Journal of Functional Foods 17, 816–827.
| 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.Crossref | GoogleScholarGoogle Scholar |
Eberhard M, Henning U, Kuhla S, Brunner RM, Kleessen B, Metges CC (2007) Effect of inulin supplementation on selected gastric, duodenal, and caecal microbiota and short chain fatty acid pattern in growing piglets. Archives of Animal Nutrition 61, 235–246.
| Effect of inulin supplementation on selected gastric, duodenal, and caecal microbiota and short chain fatty acid pattern in growing piglets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsVyrtLk%3D&md5=d9d16d1a76bb421be7f0a3ffec72e80aCAS |
Gibson GR (1999) Dietary modulation of the human gut microflora using prebiotics oligofructose and inulin. The Journal of Nutrition 129, 1438S–1441S.
Gibson GR, Beatty ER, Wang X, Cummings JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982.
| Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt1emt7g%3D&md5=f93b2bec17695bbbf66fc7a30d2998b8CAS |
Gu X, Li D (2004) Effect of dietary crude protein level on villous morphology, immune status and histochemistry parameters of digestive tract in weaning piglets. Animal Feed Science and Technology 114, 113–126.
| Effect of dietary crude protein level on villous morphology, immune status and histochemistry parameters of digestive tract in weaning piglets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFamsr4%3D&md5=b59894c9b16ce7786f5fb739192ff7efCAS |
Halas D, Hansen CF, Hampson DJ, Mullan BP, Kim JC, Wilson RH, Pluske JR (2010) Dietary supplementation with benzoic acid improves apparent ileal digestibility of total nitrogen and increases villous height and caecal microbial diversity in weaner pigs. Animal Feed Science and Technology 160, 137–147.
| Dietary supplementation with benzoic acid improves apparent ileal digestibility of total nitrogen and increases villous height and caecal microbial diversity in weaner pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFCrt7rP&md5=348b791d742b2215178a1315b7637ce9CAS |
Herosimczyk A, Lepczyński A, Ożgo M, Skomiał J, Dratwa-Chałupnik A, Tuśnio A, Taciak M, Barszcz M (2015) Differentially expressed proteins in the blood serum of piglets in response to a diet supplemented with inulin. Polish Journal of Veterinary Sciences 18, 541–548.
| Differentially expressed proteins in the blood serum of piglets in response to a diet supplemented with inulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvF2lu73I&md5=fc431d29c12f073f6d1083d1b1cdc77aCAS |
Ito H, Wada T, Ohguchi M, Sugiyama K, Kiriyama S, Morita T (2008) The degree of polymerization of inulin-like fructans affects cecal mucin and immunoglobulin A in rats. Journal of Food Science 73, H36–H41.
| The degree of polymerization of inulin-like fructans affects cecal mucin and immunoglobulin A in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslSjsbk%3D&md5=d4d03e2aa7ced34eefe9e4f812a5841eCAS |
Jaskiewicz J, Zhao Y, Hawes JW, Shimomura Y, Crabb DW, Harris RA (1996) Catabolism of isobutyrate by colonocytes. Archives of Biochemistry and Biophysics 327, 265–270.
| Catabolism of isobutyrate by colonocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhs1ajsb4%3D&md5=d4e26c3edc1485cc25840e3b8edf0f32CAS |
Kaplan H, Hutkins RW (2000) Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria. Applied and Environmental Microbiology 66, 2682–2684.
| Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvFWntr8%3D&md5=ba5fb7c9551898097da5307a1260ade9CAS |
Kastner S, Perreten V, Bleuler H, Hugenschmidt G, Lacroix C, Meile L (2006) Antibiotic susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food. Systematic and Applied Microbiology 29, 145–155.
| Antibiotic susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVyiur4%3D&md5=5dfd4f55853a549e10ff65224ec0ac6eCAS |
Kaufmann P, Pfefferkorn A, Teuber M, Meile L (1997) Identification and quantification of Bifidobacterium species isolated from food with genus-specific 16S rRNA-targeted probes by colony hybridization and PCR. Applied and Environmental Microbiology 63, 1268–1273.
Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S, Tu ZJ, Isaacson RE (2011) Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Veterinary Microbiology 153, 124–133.
| Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs.Crossref | GoogleScholarGoogle Scholar |
Kleessen B, Hartmann L, Blaut M (2001) Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. British Journal of Nutrition 86, 291–300.
| Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmt12rtLY%3D&md5=1397dbb8fac25c0c7bc542b1414914ebCAS |
Kleessen B, Hartmann L, Blaut M (2003) Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. British Journal of Nutrition 89, 597–606.
| Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOqsbg%3D&md5=c442cabaeb94c55ac1ecd5ab51672b08CAS |
Kunisawa J, Takahashi I, Kiyono H (2007) Intraepithelial lymphocytes: their shared and divergent immunological behaviors in the small and large intestine. Immunological Reviews 215, 136–153.
| Intraepithelial lymphocytes: their shared and divergent immunological behaviors in the small and large intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVKrt74%3D&md5=83edc83e7f1bd4f9a4023a373700108fCAS |
Lepczynski A, Herosimczyk A, Ozgo M, Skomial J, Taciak M, Barszcz M, Berezecka N (2015) Dietary supplementation with dried chicory root triggers changes in the blood serum proteins engaged in the clotting process and the innate immune response in growing pigs. Journal of Physiology and Pharmacology 66, 47–55.
Loh G, Eberhard M, Brunner RM, Hennig U, Kuhla S, Kleessen B, Metges CC (2006) Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. The Journal of Nutrition 136, 1198–1202.
Menne E, Guggenbuhl N, Roberfroid M (2000) Fn-type chicory inulin hydrolysate has a prebiotic effect in humans. The Journal of Nutrition 130, 1197–1199.
Mikkelsen LL, Jensen BB (2004) Effect of fructo-oligosaccharides and transgalacto-oligosaccharides on microbial populations and microbial activity in the gastrointestinal tract of piglets post-weaning. Animal Feed Science and Technology 117, 107–119.
| Effect of fructo-oligosaccharides and transgalacto-oligosaccharides on microbial populations and microbial activity in the gastrointestinal tract of piglets post-weaning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotlajtr0%3D&md5=593a7ec477cc3c03ce2e96a12cd5207eCAS |
Mitsuoka T, Hidaka H, Eida T (1987) Effect of fructo-oligosaccharides on intestinal microflora. Die Nahrung 31, 427–436.
| Effect of fructo-oligosaccharides on intestinal microflora.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c%2FhsVWiuw%3D%3D&md5=a1ccb396e3ca4dbfec7d217b0212d34aCAS |
Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, Yajima T, Takenouchi-Ohkubo N (2004) Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clinical and Experimental Immunology 137, 52–58.
| Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVSht7Y%3D&md5=20a91e300fb6d88b15d1babc9eeec43aCAS |
Niness KR (1999) Inulin and oligofructose: what are they? The Journal of Nutrition 129, 1402S–1406S.
Paßlack N, Al-samman M, Vahjen W, Männer K, Zentek J (2012) Chain length of inulin affects its degradation and the microbiota in the gastrointestinal tract of weaned piglets after a short-term dietary application. Livestock Science 149, 128–136.
| Chain length of inulin affects its degradation and the microbiota in the gastrointestinal tract of weaned piglets after a short-term dietary application.Crossref | GoogleScholarGoogle Scholar |
Roberfroid MB, Van Loo JAE, Gibson GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. The Journal of Nutrition 128, 11–19.
Rothkötter HJ, Möllhoff S, Pabst R (1999) The influence of age and breeding conditions on the number and proliferation of intraepithelial lymphocytes in pigs. Scandinavian Journal of Immunology 50, 31–38.
| The influence of age and breeding conditions on the number and proliferation of intraepithelial lymphocytes in pigs.Crossref | GoogleScholarGoogle Scholar |
Sansonetti PJ (2004) War and peace at mucosal surfaces. Nature Reviews. Immunology 4, 953–964.
| War and peace at mucosal surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVarsb7I&md5=a1910646c3970bbb9b7293922186e51dCAS |
Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiological Reviews 90, 859–904.
| Gut microbiota in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyku7rM&md5=9d575024e79b8c93a3f11c7f783e3ca9CAS |
Snoeck V, Peters IR, Cox E (2006) The IgA system: a comparison of structure and function in different species. Veterinary Research 37, 455–467.
| The IgA system: a comparison of structure and function in different species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xls1Srtrk%3D&md5=54e25fe2f985a6701e62409502d8e181CAS |
Tako E, Glahn RP, Welch RM, Lei X, Yasuda K, Miller DD (2008) Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. British Journal of Nutrition 99, 472–480.
| Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFektLc%3D&md5=8f8bd2685b276825cb45355f0c41556cCAS |
Tang M, Laarveld B, Van Kessel AG, Hamilton DL, Estrada A, Patience JF (1999) Effect of segregated early weaning on postweaning small intestinal development in pigs. Journal of Animal Science 77, 3191–3200.
| Effect of segregated early weaning on postweaning small intestinal development in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFeitQ%3D%3D&md5=798ad07dc421c828b7b458376ad2859fCAS |
Tsen HY, Lin CK, Chi WR (1998) Development and use of 16S rRNA gene targeted PCR primers for the identification of Escherichia coli cells in water. Journal of Applied Microbiology 85, 554–560.
| Development and use of 16S rRNA gene targeted PCR primers for the identification of Escherichia coli cells in water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmtlOqs7Y%3D&md5=3f495485eccd24ef6840e9d988c2669aCAS |
Valeri M, Rossi Paccani S, Kasendra M, Nesta B, Serino L, Pizza M, Soriani M (2015) Pathogenic E. coli exploits SsIE mucinase activity to translocate through the mucosal barrier and get access to host cells. PLoS One 10, e0117486
| Pathogenic E. coli exploits SsIE mucinase activity to translocate through the mucosal barrier and get access to host cells.Crossref | GoogleScholarGoogle Scholar |
Wang RF, Cao WW, Cerniglia CE (1996) PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Applied and Environmental Microbiology 62, 1242–1247.
Wellock IJ, Fortomaris PD, Houdijk JGM, Wiseman J, Kyriazakis I (2008) The consequences of non-starch polysaccharide solubility and inclusion level on the health and performance of weaned pigs challenged with enterotoxigenic Escherichia coli. British Journal of Nutrition 99, 520–530.
| The consequences of non-starch polysaccharide solubility and inclusion level on the health and performance of weaned pigs challenged with enterotoxigenic Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFektbs%3D&md5=b30318826e9d9a2b15cdb4146d00e5e1CAS |
Windey K, De Preter V, Verbeke K (2012) Relevance of protein fermentation to gut health. Molecular Nutrition & Food Research 56, 184–196.
| Relevance of protein fermentation to gut health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFaru7zI&md5=767486b8ed4a7777ee17e961d9f5c660CAS |
Yamamoto M, Fujihashi K, Kawabata K, McGhee JR, Kiyono H (1998) A mucosal intranet: intestinal epithelial cells down-regulate intraepithelial, but not peripheral, T lymphocytes. Journal of Immunology (Baltimore, Md.: 1950) 160, 2188–2196.
Zhu XY, Zhong T, Pandya Y, Joerger RD (2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Applied and Environmental Microbiology 68, 124–137.
| 16S rRNA-based analysis of microbiota from the cecum of broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1WgsQ%3D%3D&md5=e85cf32f23751c1d4a8c2a5a94f33af1CAS |
