In vitro prebiotic potential of agricultural by-products on intestinal fermentation, gut barrier and inflammatory status of piglets

Uerlings, Julie; Schroyen, Martine; Bautil, An; Courtin, Christophe; Richel, Aurore; Arevalo Sureda, Ester; Bruggeman, Geert; Tanghe, Sofie; Willems, Els; Bindelle, Jérôme; Everaert, Nadia

doi:10.1017/S0007114519002873

Article (Scientific journals)

In vitro prebiotic potential of agricultural by-products on intestinal fermentation, gut barrier and inflammatory status of piglets

Uerlings, Julie; Schroyen, Martine; Bautil, An et al.

2020 • In British Journal of Nutrition, 123 (3), p. 293-307

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/241245

DOI
10.1017/S0007114519002873

PubMed
31699173

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Uerlingsetal2020.pdf

Publisher postprint (1.12 MB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

By-products; In vitro fermentation; Intestinal porcine epithelial cells; Microbiota; SCFA; Article; Clostridium

Abstract :

[en] The inclusion of fibre-rich ingredients in diets is one possible strategy to enhance intestinal fermentation and positively impact gut ecology, barrier and immunity. Nowadays, inulin-type fructans are used as prebiotics in the feed of piglets to manipulate gut ecology for health purposes. Likewise, some by-products could be considered as sustainable and inexpensive ingredients to reduce gut disorders at weaning. In the present study, chicory root and pulp, citrus pulp, rye bran and soya hulls were tested in a three-step in vitro model of the piglet's gastro-intestinal tract combining a pepsin-pancreatin hydrolysis (digestion), a dialysis step using cellulose membranes (absorption) and a colonic batch fermentation (fermentation). The fermentation kinetics, SCFA and microbiota profiles in the fermentation broth were assessed as indicators of prebiotic activity and compared with the ones of inulin. The immunomodulatory effects of fermentation supernatant (FS) were investigated in cultured intestinal porcine epithelial cells (IPEC-J2) by high-throughput quantitative PCR. Chicory root displayed a rapid and extensive fermentation and induced the second highest butyrate ratio after inulin. Citrus pulp demonstrated high acetate ratios and induced elevated Clostridium clusters IV and XIVa levels. Chicory root and pulp FS promoted the intestinal barrier integrity with up-regulated tight and adherens junction gene expressions in comparison with inulin FS. Chicory pulp FS exerted anti-inflammatory effects in cultured IPEC-J2. The novel approach combining an in vitro fermentation model with IPEC-J2 cells highlighted that both chicory root and pulp appear to be promising ingredients and should be considered to promote intestinal health at weaning. © The Authors 2019.

Disciplines :

Agriculture & agronomy
Animal production & animal husbandry

Author, co-author :

Uerlings, Julie ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition

Schroyen, Martine ; Université de Liège - ULiège > Département GxABT > Département GxABT

Bautil, An; Laboratory of Food Chemistry and Biochemistry, Department of Microbial and Molecular Systems (MS), KU Leuven, Leuven, 3001, Belgium

Courtin, Christophe; Laboratory of Food Chemistry and Biochemistry, Department of Microbial and Molecular Systems (MS), KU Leuven, Leuven, 3001, Belgium

Richel, Aurore ; Université de Liège - ULiège > Département GxABT > SMARTECH

Arevalo Sureda, Ester ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition

Bruggeman, Geert; Royal Agrifirm Group, AW Apeldoorn, 7325, Netherlands

Tanghe, Sofie; Royal Agrifirm Group, AW Apeldoorn, 7325, Netherlands

Willems, Els; Royal Agrifirm Group, AW Apeldoorn, 7325, Netherlands

Bindelle, Jérôme ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition

Everaert, Nadia ; Université de Liège - ULiège > Département GxABT > Ingénierie des productions animales et nutrition

Language :

English

Title :

In vitro prebiotic potential of agricultural by-products on intestinal fermentation, gut barrier and inflammatory status of piglets

Publication date :

2020

Journal title :

British Journal of Nutrition

ISSN :

0007-1145

eISSN :

1475-2662

Publisher :

Cambridge University Press, United Kingdom

Volume :

123

Issue :

Pages :

293-307

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

ID33848511

Available on ORBi :

since 13 November 2019

Statistics

Number of views

166 (57 by ULiège)

Number of downloads

10 (10 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Gibson GR &Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125, 1401-1412.
Metzler B, Bauer E &Mosenthin R (2005) Microflora management in the gastrointestinal tract of piglets. Asian Australas J Anim Sci 18, 1353-1362.
Van der Waaij D, Berghuis-de Vries JM &Lekkerkerk-van der Wees JEC (1971) Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. Epidemiol Infect 69, 405-411.
Knudsen KEB, Serena A, Canibe N, et al. (2003) New insight into butyrate metabolism. Proc Nutr Soc 62, 81-86.
Roediger WEW (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424-429.
Peng L, Li Z-R, Green RS, et al. (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 139, 1619-1625.
Louis P, Duncan SH, McCrae SI, et al. (2004) Restricted distribution of the butyrate kinase pathway among butyrateproducing bacteria from the human colon. J Bacteriol 186, 2099-2106.
Lopetuso LR, Scaldaferri F, Petito V, et al. (2013) Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog 5, 23.
Pohl CS, Medland JE &Moeser AJ (2015) Early-life stress origins of gastrointestinal disease: animal models, intestinal pathophysiology, and translational implications. Am J Physiol Liver Physiol 309, G927-G941.
Dong GZ &Pluske JR (2007) The low feed intake in newly-weaned pigs: problems and possible solutions. Asian-Australas J Anim Sci 20, 440-452.
Lallès J-P, Bosi P, Smidt H, et al. (2007) Weaning-A challenge to gut physiologists. Livest Sci 108, 82-93.
Pluske JR, Turpin DL &Kim J-C (2018) Gastrointestinal tract (gut) health in the young pig. Anim Nutr 4, 187-196.
Veereman G (2007) Pediatric applications of inulin and oligofructose. J Nutr 137, 2585S-2589S.
Samanta AK, Jayapal N, Senani S, et al. (2013) Prebiotic inulin: useful dietary adjuncts to manipulate the livestock gut microflora. Braz J Microbiol 44, 1-14.
Van Waes C, Baert J, Carlier L, et al. (1998) A rapid determination of the total sugar content and the average inulin chain length in roots of chicory (Cichorium intybus L). J Sci Food Agric 76, 107-110.
Wang X, Chen Q &Lü X (2014) Pectin extracted from apple pomace and citrus peel by subcritical water. Food Hydrocoll 38, 129-137.
Hata Y, Yamamoto M &Nakajima K (1991) Effects of soybean oligosaccharides on human digestive organs. J Clin Biochem Nutr 10, 135-144.
Ortega-González M, Oćon B, Romero-Calvo I, et al. (2014) Nondigestible oligosaccharides exert nonprebiotic effects on intestinal epithelial cells enhancing the immune response via activation of TLR4-NFκB. Mol Nutr Food Res 58, 384-393.
Capitán-Canadas F, Ortega-González M, Guadix E, et al. (2014) Prebiotic oligosaccharides directly modulate proinflammatory cytokine production in monocytes via activation of TLR4. Mol Nutr Food Res 58, 1098-1110.
Zenhom M, Hyder A, Heller KJ, et al. (2011) Prebiotic oligosaccharides reduce proinflammatory cytokines in intestinal Caco-2 cells via activation of PPARγ and peptidoglycan recognition protein 3. J Nutr 141, 971-977.
Dimitrov Z, Gotova I &Chorbadjiyska E (2014) In vitro characterization of the adhesive factors of selected probiotics to Caco-2 epithelium cell line. Biotechnol Biotechnol Equip 28, 1079-1083.
Mangell P, Nejdfors P, Wang M, et al. (2002) Lactobacillus plantarum 299v inhibits Escherichia coli-induced intestinal permeability. Dig Dis Sci 47, 511-516.
Cilla A, Alegría A, Barberá R, et al. (2013) Foods or bioactive constituents of foods as chemopreventives in cell lines after simulated gastrointestinal digestion: a review. In Oxidative Stress and Chronic Degenerative Diseases-A Role for Antioxidants [JA Morales-González, editor]. IntechOpen. https://www.intechopen.com/books/oxidative-stress-and-chronicdegenerative-diseases-A-role-for-antioxidants/foods-or-bioactiveconstituents-of-foods-as-chemopreventives-in-cell-lines-aftersimulated-gastroint (accessed December 2019).
Williams BA, Voigt C &Verstegen MWA (1998) The faecal microbial population can be representative of large intestinal microfloral activity. Proc Br Soc Anim Sci, 165 Abstract.
Bauer E, Williams BA, Bosch MW, et al. (2004) Differences in microbial activity of digesta from three sections of the porcine large intestine according to in vitro fermentation of carbohydrate-rich substrates. J Sci Food Agric 84, 2097-2104.
Brosnahan AJ &Brown DR (2012) Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations. Vet Microbiol 156, 229-237.
Pearce SC, Coia HG, Karl JP, et al. (2018) Intestinal in vitro and ex vivo models to study host-microbiome interactions and acute stressors. Front Physiol 9, 1584.
Borowicki A, Stein K, Scharlau D, et al. (2010) Fermented wheat aleurone inhibits growth and induces apoptosis in human HT29 colon adenocarcinoma cells. Br J Nutr 103, 360-369.
Munjal U, Glei M, Pool-Zobel BL, et al. (2009) Fermentation products of inulin-type fructans reduce proliferation and induce apoptosis in human colon tumour cells of different stages of carcinogenesis. Br J Nutr 102, 663-671.
Uerlings J, Bindelle J, Schroyen M, et al. (2019) Fermentation capacities of fructan and pectin-rich by-products and purified fractions via an in vitro piglet's fecal model. J Sci Food Agric 99, 5720-5733.
Van Soest PJ, Robertson JB &Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74, 3583-3597.
Englyst HN &Cummings JH (1984) Simplified method for the measurement of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst 109, 937-942.
Aguedo M, Fougnies C, Dermience M, et al. (2014) Extraction by three processes of arabinoxylans from wheat bran and characterization of the fractions obtained. Carbohydr Polym 105, 317-324.
Gebruers K, Courtin CM &Delcour JA (2010) Quantification of arabinoxylans and their degree of branching using gas chromatography. In Analysis of Bioactive Components in Small Grain Cereals (Healthgrain Methods), pp. 177-189 [PR Shewry and JL Ward, editors]. St Paul, MN: American Association of Cereal Chemists, Inc.
Bindelle J, Buldgen A, Boudry C, et al. (2007) Effect of inoculum and pepsin-pancreatin hydrolysis on fibre fermentation measured by the gas production technique in pigs. Anim Feed Sci Technol 132, 111-122.
Boisen S &Fernández J (1997) Prediction of the total tract digestibility of energy in substrates and pigs diets by in vitro analyses. Anim Feed Sci Technol 68, 228-277.
Kalala G, Kambashi B, Everaert N, et al. (2018) Effect of a diet rich in prebiotic fibers of inulin type and behavior on intestinal health in obese patients in an human in vitro fermentation patterns. In 23rd National Symposium for Applied Biological Sciences. Brussels, Belgium.
Menke K &Steingass H (1988) Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim Res Dev 28, 7-55.
Tran THT, Boudry C, Everaert N, et al. (2016) Adding mucins to an in vitro batch fermentation model of the large intestine induces changes in microbial population isolated from porcine feces depending on the substrate. FEMS Microbiol Ecol 92, fiv165.
Wilfart A, Montagne L, Simmins H, et al. (2007) Digesta transit in different segments of the gastrointestinal tract of pigs as affected by insoluble fibre supplied by wheat bran. Br J Nutr 98, 54-62.
Groot JCJ, Cone JW, Williams BA, et al. (1996) Multiphasic analysis of gas production kinetics on in vitro ruminal fermentation. Anim Feed Sci Technol 64, 77-89.
Amit-Romach E, Sklan D &Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci 83, 1093-1098.
Livak KJ &Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 25, 402-408.
Wang RF, Cao WW &Cerniglia CE (1996) PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Appl Environ Microbiol 62, 1242-1247.
Langendijk PS, Schut F, Jansen GJ, et al. (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 3069-3075.
Matsuki T, Watanabe K, Fujimoto J, et al. (2004) Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 70, 7220-7228.
Matsuki T, Watanabe K, Fujimoto J, et al. (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68, 5445-5451.
Schierack P, Nordhoff M, Pollmann M, et al. (2006) Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem Cell Biol 125, 293-305.
Stoy A-CF, Heegaard PMH, Sangild PT, et al. (2013) Gene expression analysis of the IPEC-J2 cell line: a simple model for the inflammation-sensitive preterm intestine. ISRN Genomics 2013, 7.
Andersen CL, Jensen JL &Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64, 5245-5250.
Tran THT, Boudry C, Everaert N, et al. (2016) Prebiotic potential of novel carbohydrates in an in vitro co-inoculation fermentation model of the bacteria isolated from pig intestine and Salmonella. J Anim Sci 94, 58-61.
Boudry C, Poelaert C, Portetelle D, et al. (2012) Discrepancies in microbiota composition along the pig gastrointestinal tract between in vivo observations and an in vitro batch fermentation model1. J Anim Sci 90, 393-396.
Marcináková M, Klingberg TD, Lauková A, et al. (2010) The effect of pH, bile and calcium on the adhesion ability of probiotic enterococci of animal origin to the porcine jejunal epithelial cell line IPEC-J2. Anaerobe 16, 120-124.
Lee SI &Kang KS (2019) N-acetylcysteine modulates lipopolysaccharide-induced intestinal dysfunction. Sci Rep 9, 1004.
Jha R, Fouhse JM, Tiwari UP, et al. (2019) Dietary fiber and intestinal health of monogastric animals. Front Vet Sci 6, 48.
Shim SB, Verdonk JMAJ, Pellikaan WF, et al. (2007) Differences in microbial activities of faeces from weaned and unweaned pigs in relation to in vitro fermentation of different sources of inulin-type oligofructose and pig feed ingredients. Asian-Australas J Anim Sci 20, 1444-1452.
Pellikaan WF, Verdonk JMAJ, Shim SB, et al. (2007) Adaptive capacity of faecal microbiota from piglets receiving diets with different types of inulin-type fructans. Livest Sci 108, 178-181.
Tamaki Y, Konishi T &Tako M (2008) Isolation and characterization of pectin from peel of Citrus tankan. Biosci Biotechnol Biochem 72, 896-899. https://www.intechopen.com/books/oxidative-stress-and-chronicdegenerative-diseases-A-role-for-antioxidants/foods-or-bioactiveconstituents-of-foods-as-chemopreventives-in-cell-lines-aftersimulated-gastroint (accessed December 2019).
Williams BA, Voigt C &Verstegen MWA (1998) The faecal microbial population can be representative of large intestinal microfloral activity. Proc Br Soc Anim Sci, 165 Abstract.
Bauer E, Williams BA, Bosch MW, et al. (2004) Differences in microbial activity of digesta from three sections of the porcine large intestine according to in vitro fermentation of carbohydrate-rich substrates. J Sci Food Agric 84, 2097-2104.
Brosnahan AJ &Brown DR (2012) Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations. Vet Microbiol 156, 229-237.
Pearce SC, Coia HG, Karl JP, et al. (2018) Intestinal in vitro and ex vivo models to study host-microbiome interactions and acute stressors. Front Physiol 9, 1584.
Borowicki A, Stein K, Scharlau D, et al. (2010) Fermented wheat aleurone inhibits growth and induces apoptosis in human HT29 colon adenocarcinoma cells. Br J Nutr 103, 360-369.
Munjal U, Glei M, Pool-Zobel BL, et al. (2009) Fermentation products of inulin-type fructans reduce proliferation and induce apoptosis in human colon tumour cells of different stages of carcinogenesis. Br J Nutr 102, 663-671.
Uerlings J, Bindelle J, Schroyen M, et al. (2019) Fermentation capacities of fructan and pectin-rich by-products and purified fractions via an in vitro piglet's fecal model. J Sci Food Agric 99, 5720-5733.
Van Soest PJ, Robertson JB &Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74, 3583-3597.
Englyst HN &Cummings JH (1984) Simplified method for the measurement of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst 109, 937-942.
Aguedo M, Fougnies C, Dermience M, et al. (2014) Extraction by three processes of arabinoxylans from wheat bran and characterization of the fractions obtained. Carbohydr Polym 105, 317-324.
Gebruers K, Courtin CM &Delcour JA (2010) Quantification of arabinoxylans and their degree of branching using gas chromatography. In Analysis of Bioactive Components in Small Grain Cereals (Healthgrain Methods), pp. 177-189 [PR Shewry and JL Ward, editors]. St Paul, MN: American Association of Cereal Chemists, Inc.
Bindelle J, Buldgen A, Boudry C, et al. (2007) Effect of inoculum and pepsin-pancreatin hydrolysis on fibre fermentation measured by the gas production technique in pigs. Anim Feed Sci Technol 132, 111-122.
Boisen S &Fernández J (1997) Prediction of the total tract digestibility of energy in substrates and pigs diets by in vitro analyses. Anim Feed Sci Technol 68, 228-277.
Kalala G, Kambashi B, Everaert N, et al. (2018) Effect of a diet rich in prebiotic fibers of inulin type and behavior on intestinal health in obese patients in an human in vitro fermentation patterns. In 23rd National Symposium for Applied Biological Sciences. Brussels, Belgium.
Menke K &Steingass H (1988) Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim Res Dev 28, 7-55.
Tran THT, Boudry C, Everaert N, et al. (2016) Adding mucins to an in vitro batch fermentation model of the large intestine induces changes in microbial population isolated from porcine feces depending on the substrate. FEMS Microbiol Ecol 92, fiv165.
Wilfart A, Montagne L, Simmins H, et al. (2007) Digesta transit in different segments of the gastrointestinal tract of pigs as affected by insoluble fibre supplied by wheat bran. Br J Nutr 98, 54-62.
Groot JCJ, Cone JW, Williams BA, et al. (1996) Multiphasic analysis of gas production kinetics on in vitro ruminal fermentation. Anim Feed Sci Technol 64, 77-89.
Amit-Romach E, Sklan D &Uni Z (2004) Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poult Sci 83, 1093-1098.
Livak KJ &Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 25, 402-408.
Wang RF, Cao WW &Cerniglia CE (1996) PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples. Appl Environ Microbiol 62, 1242-1247.
Langendijk PS, Schut F, Jansen GJ, et al. (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61, 3069-3075.
Matsuki T, Watanabe K, Fujimoto J, et al. (2004) Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 70, 7220-7228.
Matsuki T, Watanabe K, Fujimoto J, et al. (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68, 5445-5451.
Schierack P, Nordhoff M, Pollmann M, et al. (2006) Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem Cell Biol 125, 293-305.
Stoy A-CF, Heegaard PMH, Sangild PT, et al. (2013) Gene expression analysis of the IPEC-J2 cell line: a simple model for the inflammation-sensitive preterm intestine. ISRN Genomics 2013, 7.
Andersen CL, Jensen JL &Orntoft TF (2004) Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64, 5245-5250.
Tran THT, Boudry C, Everaert N, et al. (2016) Prebiotic potential of novel carbohydrates in an in vitro co-inoculation fermentation model of the bacteria isolated from pig intestine and Salmonella. J Anim Sci 94, 58-61.
Boudry C, Poelaert C, Portetelle D, et al. (2012) Discrepancies in microbiota composition along the pig gastrointestinal tract between in vivo observations and an in vitro batch fermentation model1. J Anim Sci 90, 393-396.
Marcináková M, Klingberg TD, Lauková A, et al. (2010) The effect of pH, bile and calcium on the adhesion ability of probiotic enterococci of animal origin to the porcine jejunal epithelial cell line IPEC-J2. Anaerobe 16, 120-124.
Lee SI &Kang KS (2019) N-acetylcysteine modulates lipopolysaccharide-induced intestinal dysfunction. Sci Rep 9, 1004.
Jha R, Fouhse JM, Tiwari UP, et al. (2019) Dietary fiber and intestinal health of monogastric animals. Front Vet Sci 6, 48.
Shim SB, Verdonk JMAJ, Pellikaan WF, et al. (2007) Differences in microbial activities of faeces from weaned and unweaned pigs in relation to in vitro fermentation of different sources of inulin-type oligofructose and pig feed ingredients. Asian-Australas J Anim Sci 20, 1444-1452.
Pellikaan WF, Verdonk JMAJ, Shim SB, et al. (2007) Adaptive capacity of faecal microbiota from piglets receiving diets with different types of inulin-type fructans. Livest Sci 108, 178-181.
Tamaki Y, Konishi T &Tako M (2008) Isolation and characterization of pectin from peel of Citrus tankan. Biosci Biotechnol Biochem 72, 896-899.
Van Craeyveld V, Swennen K, Dornez E, et al. (2008) Structurally different wheat-derived arabinoxylooligosaccharides have different prebiotic and fermentation properties in rats. J Nutr 138, 2348-2355.
Loh G, Eberhard M, Brunner RM, et al. (2006) Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. J Nutr 136, 1198-1202.
Roberfroid MB, Van Loo JAE &Gibson GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. J Nutr 128, 11-19.
Howard MD, Gordon DT, Pace LW, et al. (1995) Effects of dietary supplementation with fructooligosaccharides on colonic microbiota populations and epithelial cell proliferation in neonatal pigs. J Pediatr Gastroenterol Nutr 21, 297-303.
Arrigoni E, Jörger F, Kollöffel B, et al. (2002) In vitro fermentability of a commercial wheat germ preparation and its impact on the growth of bifidobacteria. Food Res Int 35, 475-481.
Crittenden R, Karppinen S, Ojanen S, et al. (2002) In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J Sci Food Agric 82, 781-789.
Hughes SA, Shewry PR, Li L, et al. (2007) In vitro fermentation by human fecal microflora of wheat arabinoxylans. J Agric Food Chem 55, 4589-4595.
Allsopp P, Possemiers S, Campbell D, et al. (2013) An exploratory study into the putative prebiotic activity of fructans isolated from Agave angustifolia and the associated anticancer activity. Anaerobe 22, 38-44.
Pham VT, Seifert N, Richard N, et al. (2018) The effects of fermentation products of prebiotic fibres on gut barrier and immune functions in vitro. PeerJ 6, 5288-5291.
McGuire VA &Arthur JSC (2015) Subverting toll-like receptor signaling by bacterial pathogens. Front Immunol 6, 607.
Caruso R, Warner N, Inohara N, et al. (2014) NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41, 898-908.
Jiang C, Ting AT &Seed B (1998) PPAR-γ agonists inhibit production of monocyte inflammatory cytokines. Nature 391, 82.
Ricote M, Li AC, Willson TM, et al. (1998) The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391, 79.
Luo J-L, Kamata H &Karin M (2005) IKK/NF-kappaB signaling: balancing life and death-A new approach to cancer therapy. J Clin Invest 115, 2625-2632.
Zhang HM, Rao JN, Guo X, et al. (2004) Akt kinase activation blocks apoptosis in intestinal epithelial cells by inhibiting caspase-3 afterpolyamine depletion.JBiolChem279, 22539-22547.
Chi H, Barry SP, Roth RJ, et al. (2006) Dynamic regulation of pro-and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc Natl Acad Sci 103, 2274-2279.
Hommes DW Peppelenbosch MP &van Deventer SJH (2003) Mitogen activated protein (MAP) kinase signal transduction pathways andnovel anti-inflammatory targets. Gut52, 144-151.
Le Sciellour M, Labussière E, Zemb O, et al. (2018) Effect of dietary fiber content on nutrient digestibility and fecal microbiota composition in growing-finishing pigs. PLOS ONE 13, e0206159.