Bifidogenic effect of a wheat arabinoxylan (MC-AX) is observed across two animal models, a simulated human intestine model (SHIME®) and a clinical study

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Flore DEPEINT Jean-Michel LECERF Philippe R POUILLART Yves BECKERS Hafida KHORSI-CAUET

Abstract

Dietary fibres consist of carbohydrate polymers of plant origin and are neither digested nor absorbed in the small intestine. They have at least one functional property linked to stools production, colonic fermentation, cholesterol, glucose or insulin levels. Different models are available to investigate the prebiotic potential of such a molecule. The aim of this study was to compare our clinical data with three previously unpublished preclinical studies, all looking for prebiotic activity of a medium-chain arabinoxylan (MC-AX) extracted from wheat endosperm. MC-AX was tested in an in vitro multicompartment digestive system (SHIME®), piglet and rat models as well as a clinical study, at doses ranging from 1 to 10g/day and exposed for 2 to 4 weeks. Selected bacterial counts and metabolites were measured at different time points. MC-AX induced an increase in Bifidobacterium in treated groups compared to placebo of at least one log unit in all models. This could be measured as early as 7 days (SHIME®) with the strongest variation observed in piglets (2 logs) at day 14. We observed a significant decrease in acetate production, balanced by an increase in both propionate and butyrate in the rodent and human studies. While there are some quantitative differences between the models, partially due to dose or species specificities, there is a clear and consistent overall pattern. Data were also compared to published clinical trials on dietary fibres to explain some structure-activity relationships relative to their physicochemical properties.

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How to Cite
DEPEINT, Flore et al. Bifidogenic effect of a wheat arabinoxylan (MC-AX) is observed across two animal models, a simulated human intestine model (SHIME®) and a clinical study. Medical Research Archives, [S.l.], v. 5, n. 4, apr. 2017. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/938>. Date accessed: 17 apr. 2024.
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Research Articles

References

Alander, M., J. Mättö, W. Kneifel, M. Johansson, B. Kögler, R. Crittenden, T. Mattila-Sandholm, and M. Saarela. 2001. “Effect of Galacto-Oligosaccharide Supplementation on Human Faecal Microflora and on Survival and Persistence of Bifidobacterium Lactis Bb-12 in the Gastrointestinal Tract.” International Dairy Journal 11 (10): 817–25. doi:10.1016/S0958-6946(01)00100-5.
Aleixandre, Amaya, and Marta Miguel. 2008. “Dietary Fiber in the Prevention and Treatment of Metabolic Syndrome: A Review.” Critical Reviews in Food Science and Nutrition 48 (10): 905–12. doi:10.1080/10408390701761886.
Andrewartha, Kathryn A., Don R. Phillips, and Bruce A. Stone. 1979. “Solution Properties of Wheat-Flour Arabinoxylans and Enzymically Modified Arabinoxylans.” Carbohydrate Research 77 (1): 191–204. doi:10.1016/S0008-6215(00)83805-7.
Belenguer, Alvaro, Sylvia H. Duncan, Grietje Holtrop, Susan E. Anderson, Gerald E. Lobley, and Harry J. Flint. 2007. “Impact of pH on Lactate Formation and Utilization by Human Fecal Microbial Communities.” Applied and Environmental Microbiology 73 (20): 6526–33. doi:10.1128/AEM.00508-07.
Bouhnik, Yoram, Laurent Raskine, Guy Simoneau, Eric Vicaut, Christel Neut, Bernard Flourié, Fred Brouns, and Francis R. Bornet. 2004. “The Capacity of Nondigestible Carbohydrates to Stimulate Fecal Bifidobacteria in Healthy Humans: A Double-Blind, Randomized, Placebo-Controlled, Parallel-Group, Dose-Response Relation Study.” The American Journal of Clinical Nutrition 80 (6): 1658–64.
Broekaert, Willem F., Christophe M. Courtin, Kristin Verbeke, Tom Van de Wiele, Willy Verstraete, and Jan A. Delcour. 2011. “Prebiotic and Other Health-Related Effects of Cereal-Derived Arabinoxylans, Arabinoxylan-Oligosaccharides, and Xylooligosaccharides.” Critical Reviews in Food Science and Nutrition 51 (2): 178–94. doi:10.1080/10408390903044768.
Chassard, Christophe, Eve Delmas, Paul A. Lawson, and Annick Bernalier-Donadille. 2008. “Bacteroides Xylanisolvens Sp. Nov., a Xylan-Degrading Bacterium Isolated from Human Faeces.” International Journal of Systematic and Evolutionary Microbiology 58 (4): 1008–13. doi:10.1099/ijs.0.65504-0.
Chassard, Christophe, Vanessa Goumy, Marion Leclerc, Christophe Del’homme, and Annick Bernalier-Donadille. 2007. “Characterization of the Xylan-Degrading Microbial Community from Human Faeces.” FEMS Microbiology Ecology 61 (1): 121–31. doi:10.1111/j.1574-6941.2007.00314.x.
Childs, Caroline E., Henna Röytiö, Esa Alhoniemi, Agnes A. Fekete, Sofia D. Forssten, Natasa Hudjec, Ying Ni Lim, et al. 2014. “Xylo-Oligosaccharides Alone or in Synbiotic Combination with Bifidobacterium Animalis Subsp. lactis Induce Bifidogenesis and Modulate Markers of Immune Function in Healthy Adults: A Double-Blind, Placebo-Controlled, Randomised, Factorial Cross-over Study.” British Journal of Nutrition 111 (11): 1945–56. doi:10.1017/S0007114513004261.
Christensen, Ellen Gerd, Tine Rask Licht, Thomas Dyrmann Leser, and Martin Iain Bahl. 2014. “Dietary Xylo-Oligosaccharide Stimulates Intestinal Bifidobacteria and Lactobacilli but Has Limited Effect on Intestinal Integrity in Rats.” BMC Research Notes 7: 660. doi:10.1186/1756-0500-7-660.
Cleemput, G., S. P. Roels, M. van Oort, P. J. Grobet, and J. A. Delcour. 1993. “Heterogeneity in the Structure of Water-Soluble Arabinoxylans in European Wheat Flours of Variable Bread-Making Quality.” Cereal Chemistry (USA). http://agris.fao.org/agris-search/search.do?recordID=US9421086.
Cloetens, Lieselotte, Willem F. Broekaert, Yasmine Delaedt, Frans Ollevier, Christophe M. Courtin, Jan A. Delcour, Paul Rutgeerts, and Kristin Verbeke. 2010. “Tolerance of Arabinoxylan-Oligosaccharides and Their Prebiotic Activity in Healthy Subjects: A Randomised, Placebo-Controlled Cross-over Study.” British Journal of Nutrition 103 (5): 703–13. doi:10.1017/S0007114509992248.
Courtin, C. M., and J. A. Delcour. 2002. “Arabinoxylans and Endoxylanases in Wheat Flour Bread-Making.” Journal of Cereal Science 35 (3): 225–43. doi:10.1006/jcrs.2001.0433.
Courtin, Christophe M., Willem F. Broekaert, Katrien Swennen, G. Aerts, V. Van Craeyveld, and Jan A. Delcour. 2009. “Occurence of Arabinoxylo-Oligosaccharides and Arabinogalactan Peptides in Beer.” Journal of the American Society of Brewing Chemists 67 (2): 112–17.
Damen, Bram, Lieselotte Cloetens, Willem F. Broekaert, Isabelle François, Olivier Lescroart, Isabel Trogh, Filip Arnaut, et al. 2012. “Consumption of Breads Containing In Situ–Produced Arabinoxylan Oligosaccharides Alters Gastrointestinal Effects in Healthy Volunteers.” The Journal of Nutrition 142 (3): 470–77. doi:10.3945/jn.111.146464.
Damen, Bram, Joran Verspreet, Annick Pollet, Willem F. Broekaert, Jan A. Delcour, and Christophe M. Courtin. 2011. “Prebiotic Effects and Intestinal Fermentation of Cereal Arabinoxylans and Arabinoxylan Oligosaccharides in Rats Depend Strongly on Their Structural Properties and Joint Presence.” Molecular Nutrition & Food Research 55 (12): 1862–74. doi:10.1002/mnfr.201100377.
Davis, L. M. G., I. Martínez, J. Walter, and R. Hutkins. 2010. “A Dose Dependent Impact of Prebiotic Galactooligosaccharides on the Intestinal Microbiota of Healthy Adults.” International Journal of Food Microbiology 144 (2): 285–92. doi:10.1016/j.ijfoodmicro.2010.10.007.
Depeint, Flore, George Tzortzis, Jelena Vulevic, Kerry I’Anson, and Glenn R. Gibson. 2008. “Prebiotic Evaluation of a Novel Galactooligosaccharide Mixture Produced by the Enzymatic Activity of Bifidobacterium Bifidum NCIMB 41171, in Healthy Humans: A Randomized, Double-Blind, Crossover, Placebo-Controlled Intervention Study.” The American Journal of Clinical Nutrition 87 (3): 785–791.
Duncan, Sylvia H, Georgina L Hold, Adela Barcenilla, Colin S Stewart, and Harry J. Flint. 2002. “Roseburia Intestinalis Sp. Nov., a Novel Saccharolytic, Butyrate-Producing Bacterium from Human Faeces.” International Journal of Systematic and Evolutionary Microbiology 52 (5): 1615–20. doi:10.1099/00207713-52-5-1615.
Ebringerova, A., and T. Heinze. 2000. “Xylan and Xylan Derivatives - Biopolymers with Valuable Properties, 1. Naturally Occuring Xylans Structures, Isolation Procedures and Properties.” Macromolecular Rapid Communications 21: 542–56.
Elleuch, Mohamed, Dorothea Bedigian, Olivier Roiseux, Souhail Besbes, Christophe Blecker, and Hamadi Attia. 2011. “Dietary Fibre and Fibre-Rich by-Products of Food Processing: Characterisation, Technological Functionality and Commercial Applications: A Review.” Food Chemistry 124 (2): 411–21. doi:10.1016/j.foodchem.2010.06.077.
Finegold, Sydney M., Zhaoping Li, Paula H. Summanen, Julia Downes, Gail Thames, Karen Corbett, Scot Dowd, Michael Krak, and David Heber. 2014. “Xylooligosaccharide Increases Bifidobacteria but Not Lactobacilli in Human Gut Microbiota” 5 (3): 436–45. doi:10.1039/C3FO60348B.
François, Isabelle E. J. A., Olivier Lescroart, Wim S. Veraverbeke, Massimo Marzorati, Sam Possemiers, Henrike Hamer, Karen Windey, et al. 2014. “Effects of Wheat Bran Extract Containing Arabinoxylan Oligosaccharides on Gastrointestinal Parameters in Healthy Preadolescent Children.” Journal of Pediatric Gastroenterology and Nutrition 58 (5): 647–53. doi:10.1097/MPG.0000000000000285.
Gibson, G. R., and M. B. Roberfroid. 1995. “Dietary Modulation of the Human Colonic Microbiota: Introducing the Concept of Prebiotics.” The Journal of Nutrition 125 (6): 1401–12.
Gibson, Glenn R., Hollie M. Probert, Jan Van Loo, Robert A. Rastall, and Marcel B. Roberfroid. 2004. “Dietary Modulation of the Human Colonic Microbiota: Updating the Concept of Prebiotics.” Nutrition Research Reviews 17 (2): 259–75. doi:10.1079/NRR200479.
Grootaert, Charlotte, Jan A. Delcour, Christophe M. Courtin, Willem F. Broekaert, Willy Verstraete, and Tom Van de Wiele. 2007. “Microbial Metabolism and Prebiotic Potency of Arabinoxylan Oligosaccharides in the Human Intestine.” Trends in Food Science & Technology 18 (2): 64–71. doi:10.1016/j.tifs.2006.08.004.
Grootaert, Charlotte, Pieter Van den Abbeele, Massimo Marzorati, Willem F. Broekaert, Christophe M. Courtin, Jan A. Delcour, Willy Verstraete, and Tom Van de Wiele. 2009. “Comparison of Prebiotic Effects of Arabinoxylan Oligosaccharides and Inulin in a Simulator of the Human Intestinal Microbial Ecosystem.” FEMS Microbiology Ecology 69 (2): 231–42. doi:10.1111/j.1574-6941.2009.00712.x.
Hallfrisch, Judith, and Kay M. Behall. 2000. “Mechanisms of the Effects of Grains on Insulin and Glucose Responses.” Journal of the American College of Nutrition 19 (sup3): 320S–325S. doi:10.1080/07315724.2000.10718967.
Harvey, R. F., E. W. Pomare, and K. W. Heaton. 1973. “EFFECTS OF INCREASED DIETARY FIBRE ON INTESTINAL TRANSIT.” The Lancet, Originally published as Volume 1, Issue 7815, 301 (7815): 1278–80. doi:10.1016/S0140-6736(73)91294-4.
Hopkins, Mark J., Hans N. Englyst, Sandra Macfarlane, Elizabeth Furrie, George T. Macfarlane, and Andrew J. McBain. 2003. “Degradation of Cross-Linked and Non-Cross-Linked Arabinoxylans by the Intestinal Microbiota in Children.” Applied and Environmental Microbiology 69 (11): 6354–60. doi:10.1128/AEM.69.11.6354-6360.2003.
Hsu, Cheng-Kuang, Jiunn-Wang Liao, Yun-Chin Chung, Chia-Pei Hsieh, and Yin-Ching Chan. 2004. “Xylooligosaccharides and Fructooligosaccharides Affect the Intestinal Microbiota and Precancerous Colonic Lesion Development in Rats.” The Journal of Nutrition 134 (6): 1523–28.
Hughes, S. A., P. R. Shewry, L. Li, G. R. Gibson, M. L. Sanz, and R. A. Rastall. 2007. “In Vitro Fermentation by Human Fecal Microflora of Wheat Arabinoxylans.” Journal of Agricultural and Food Chemistry 55 (11): 4589–95. doi:10.1021/jf070293g.
Izydorczyk, Marta S., and Costas G. Biliaderis. 1995. “Cereal Arabinoxylans: Advances in Structure and Physicochemical Properties.” Carbohydrate Polymers, Frontiers in Carbohydrate Research-4, 28 (1): 33–48. doi:10.1016/0144-8617(95)00077-1.
Joly, Claire, Jérôme Gay-Quéheillard, André Léké, Karen Chardon, Stéphane Delanaud, Véronique Bach, and Hafida Khorsi-Cauet. 2013. “Impact of Chronic Exposure to Low Doses of Chlorpyrifos on the Intestinal Microbiota in the Simulator of the Human Intestinal Microbial Ecosystem (SHIME®) and in the Rat.” Environmental Science and Pollution Research 20 (5): 2726–34. doi:10.1007/s11356-012-1283-4.
Koecher, Katie J., Jackie A. Noack, Derek A. Timm, Abby S. Klosterbuer, William Thomas, and Joanne L. Slavin. 2014. “Estimation and Interpretation of Fermentation in the Gut: Coupling Results from a 24 H Batch in Vitro System with Fecal Measurements from a Human Intervention Feeding Study Using Fructo-Oligosaccharides, Inulin, Gum Acacia, and Pea Fiber.” Journal of Agricultural and Food Chemistry 62 (6): 1332–37. doi:10.1021/jf404688n.
Kontula, P., M. -L. Suihko, T. Suortti, M. Tenkanen, T. Mattila-Sandholm, and A. von Wright. 2000. “The Isolation of Lactic Acid Bacteria from Human Colonic Biopsies after Enrichment on Lactose Derivatives and Rye Arabinoxylo-Oligosaccharides.” Food Microbiology 17 (1): 13–22. doi:10.1006/fmic.1999.0268.
Kurasawa, Shin’ichi, Valerie S. Haack, and Judith A. Marlett. 2000. “Plant Residue and Bacteria as Bases for Increased Stool Weight Accompanying Consumption of Higher Dietary Fiber Diets.” Journal of the American College of Nutrition 19 (4): 426–33. doi:10.1080/07315724.2000.10718942.
Lecerf, Jean-Michel, Flore Dépeint, Elise Clerc, Yann Dugenet, Claude N. Niamba, Larbi Rhazi, Amélie Cayzeele, et al. 2012. “Xylo-Oligosaccharide (XOS) in Combination with Inulin Modulates Both the Intestinal Environment and Immune Status in Healthy Subjects, While XOS Alone Only Shows Prebiotic Properties.” British Journal of Nutrition 108 (10): 1847–1858.
Lee, Sc., and L. Prosky. 1994. “International Survey on Dietary Fiber: Definition, Analysis, and Reference Materials.” Journal of AOAC International 78 (1): 22–36.
Lu, Z. X., K. Z. Walker, J. G. Muir, and K. O’Dea. 2004. “Arabinoxylan Fibre Improves Metabolic Control in People with Type II Diabetes.” European Journal of Clinical Nutrition 58 (4): 621–28. doi:10.1038/sj.ejcn.1601857.
Lu, Zhong X., Peter R. Gibson, Jane G. Muir, Marisa Fielding, and Kerin O’Dea. 2000. “Arabinoxylan Fiber from a By-Product of Wheat Flour Processing Behaves Physiologically like a Soluble, Fermentable Fiber in the Large Bowel of Rats.” The Journal of Nutrition 130 (8): 1984–90.
Lunn, J., and J. L. Buttriss. 2007. “Carbohydrates and Dietary Fibre.” Nutrition Bulletin 32 (1): 21–64. doi:10.1111/j.1467-3010.2007.00616.x.
Maes, C., and J. A. Delcour. 2002. “Structural Characterisation of Water-Extractable and Water-Unextractable Arabinoxylans in Wheat Bran.” Journal of Cereal Science 35 (3): 315–26. doi:10.1006/jcrs.2001.0439.
Mäkeläinen, H., S. Forssten, M. Saarinen, J. Stowell, N. Rautonen, and A. Ouwehand. 2009. “Xylo-Oligosaccharides Enhance the Growth of Bifidobacteria and Bifidobacterium Lactis in a Simulated Colon Model.” Beneficial Microbes 1 (1): 81–91. doi:10.3920/BM2009.0025.
Maki, Kevin C., Glenn R. Gibson, Robin S. Dickmann, Cyril W. C. Kendall, C. -Y. Oliver Chen, Adele Costabile, Elena M. Comelli, et al. 2012. “Digestive and Physiologic Effects of a Wheat Bran Extract, Arabino-Xylan-Oligosaccharide, in Breakfast Cereal.” Nutrition 28 (11–12): 1115–21. doi:10.1016/j.nut.2012.02.010.
Marlett, Judith A. 1997. “Sites and Mechanisms for the Hypocholesterolemic Actions of Soluble Dietary Fiber Sources.” In Dietary Fiber in Health and Disease, edited by David Kritchevsky and Charles Bonfield, 109–21. Advances in Experimental Medicine and Biology 427. Springer US. http://link.springer.com/chapter/10.1007/978-1-4615-5967-2_13.
Matteuzzi, D., E. Swennen, M. Rossi, T. Hartman, and V. Lebet. 2004. “Prebiotic Effects of a Wheat Germ Preparation in Human Healthy Subjects.” Food Microbiology 21 (1): 119–24. doi:10.1016/S0740-0020(03)00009-1.
Mitsou, Evdokia K., Niki Panopoulou, Katja Turunen, Vasilis Spiliotis, and Adamantini Kyriacou. 2010. “Prebiotic Potential of Barley Derived β-Glucan at Low Intake Levels: A Randomised, Double-Blinded, Placebo-Controlled Clinical Study.” Food Research International 43 (4): 1086–92. doi:10.1016/j.foodres.2010.01.020.
Molly, K., M. van de Woestyne, and W. Verstraete. 1993. “Development of a 5-Step Multi-Chamber Reactor as a Simulation of the Human Intestinal Microbial Ecosystem.” Applied Microbiology and Biotechnology 39 (2): 254–58. doi:10.1007/BF00228615.
Neyrinck, Audrey M., Sam Possemiers, Céline Druart, Tom Van de Wiele, Fabienne De Backer, Patrice D. Cani, Yvan Larondelle, and Nathalie M. Delzenne. 2011. “Prebiotic Effects of Wheat Arabinoxylan Related to the Increase in Bifidobacteria, Roseburia and Bacteroides/Prevotella in Diet-Induced Obese Mice.” PLOS ONE 6 (6): e20944. doi:10.1371/journal.pone.0020944.
Nitrayova, S., M. Brestensky, J. Heger, and P. Patras. 2013. “The Pig as a Valuable Model for Monitoring Digestion and the Ecosystem of the Digestive Tract.” Microbial Ecology in Health & Disease 24: 13–14.
Pereira, Dora I. A., and Glenn R. Gibson. 2002. “Cholesterol Assimilation by Lactic Acid Bacteria and Bifidobacteria Isolated from the Human Gut.” Applied and Environmental Microbiology 68 (9): 4689–93. doi:10.1128/AEM.68.9.4689-4693.2002.
Phillips, Glyn O., and Steve W. Cui. 2011. “An Introduction: Evolution and Finalisation of the Regulatory Definition of Dietary Fibre.” Food Hydrocolloids, Dietary Fibre and Bioactive Polysaccharides, 25 (2): 139–43. doi:10.1016/j.foodhyd.2010.04.011.
Possemiers, Sam, Kristof Verthé, Sofie Uyttendaele, and Willy Verstraete. 2004. “PCR-DGGE-Based Quantification of Stability of the Microbial Community in a Simulator of the Human Intestinal Microbial Ecosystem.” FEMS Microbiology Ecology 49 (3): 495–507. doi:10.1016/j.femsec.2004.05.002.
Pouillart, Philippe R., Flore Dépeint, Afif Abdelnour, Laetitia Deremaux, Odile Vincent, Jean-Claude Mazière, Jean-Yves Madec, et al. 2010. “Nutriose, a Prebiotic Low-Digestible Carbohydrate, Stimulates Gut Mucosal Immunity and Prevents TNBS-Induced Colitis in Piglets.” Inflammatory Bowel Diseases 16 (5): 783–794.
Reygner, Julie, Claire Joly Condette, Aurélia Bruneau, Stéphane Delanaud, Larbi Rhazi, Flore Depeint, Latifa Abdennebi-Najar, Veronique Bach, Camille Mayeur, and Hafida Khorsi-Cauet. 2016. “Changes in Composition and Function of Human Intestinal Microbiota Exposed to Chlorpyrifos in Oil as Assessed by the SHIME® Model.” International Journal of Environmental Research and Public Health 13 (11): 1088. doi:10.3390/ijerph13111088.
Rowan, Angela M., P. J. Moughan, M. N. Wilson, K. Maher, and C. Tasman-Jones. 1994. “Comparison of the Ileal and Faecal Digestibility of Dietary Amino Acids in Adult Humans and Evaluation of the Pig as a Model Animal for Digestion Studies in Man.” British Journal of Nutrition 71 (1): 29–42. doi:10.1079/BJN19940108.
Rycroft, C. E., M. R. Jones, G. R. Gibson, and R. A. Rastall. 2001. “A Comparative in Vitro Evaluation of the Fermentation Properties of Prebiotic Oligosaccharides.” Journal of Applied Microbiology 91 (5): 878–87.
Sanchez, J. I., M. Marzorati, C. Grootaert, M. Baran, V. Van Craeyveld, C. M. Courtin, W. F. Broekaert, J. A. Delcour, W. Verstraete, and T. Van de Wiele. 2009. “Arabinoxylan-Oligosaccharides (AXOS) Affect the Protein/carbohydrate Fermentation Balance and Microbial Population Dynamics of the Simulator of Human Intestinal Microbial Ecosystem.” Microbial Biotechnology 2 (1): 101–13. doi:10.1111/j.1751-7915.2008.00064.x.
Santos, A., M. San Mauro, and D. Marquina Díaz. 2006. “Prebiotics and Their Long-Term Influence on the Microbial Populations of the Mouse Bowel.” Food Microbiology 23 (5): 498–503. doi:10.1016/j.fm.2005.07.004.
Scheppach, W. M., C. E. Fabian, and H. W. Kasper. 1987. “Fecal Short-Chain Fatty Acid (SCFA) Analysis by Capillary Gas-Liquid Chromatography.” The American Journal of Clinical Nutrition 46 (4): 641–46.
Talasniemi, J. Petteri, Sirpa Pennanen, Heikki Savolainen, Leo Niskanen, and Jyrki Liesivuori. 2008. “Analytical Investigation: Assay of D-Lactate in Diabetic Plasma and Urine.” Clinical Biochemistry 41 (13): 1099–1103. doi:10.1016/j.clinbiochem.2008.06.011.
Van Craeyveld, V., Katrien Swennen, Emmie Dornez, Tom Van de Wiele, Massimo Marzorati, Willy Verstraete, Yasmine Delaedt, et al. 2008. “Structurally Different Wheat-Derived Arabinoxylooligosaccharides Have Different Prebiotic and Fermentation Properties in Rats.” The Journal of Nutrition 138 (12): 2348–55. doi:10.3945/jn.108.094367.
Van den Abbeele, Pieter, Philippe Gérard, Sylvie Rabot, Aurélia Bruneau, Sahar El Aidy, Muriel Derrien, Michiel Kleerebezem, et al. 2011. “Arabinoxylans and Inulin Differentially Modulate the Mucosal and Luminal Gut Microbiota and Mucin-Degradation in Humanized Rats.” Environmental Microbiology 13 (10): 2667–80. doi:10.1111/j.1462-2920.2011.02533.x.
Van den Abbeele, Pieter, Charlotte Grootaert, Sam Possemiers, Willy Verstraete, Kim Verbeken, and Tom Van de Wiele. 2009. “In Vitro Model to Study the Modulation of the Mucin-Adhered Bacterial Community.” Applied Microbiology and Biotechnology 83 (2): 349–59. doi:10.1007/s00253-009-1947-2.
Van den Abbeele, Pieter, Koen Venema, Tom Van de Wiele, Willy Verstraete, and Sam Possemiers. 2013. “Different Human Gut Models Reveal the Distinct Fermentation Patterns of Arabinoxylan versus Inulin.” Journal of Agricultural and Food Chemistry 61 (41): 9819–27. doi:10.1021/jf4021784.
Vardakou, Maria, Carmen Nueno Palop, Michael Gasson, Arjan Narbad, and Paul Christakopoulos. 2007. “In Vitro Three-Stage Continuous Fermentation of Wheat Arabinoxylan Fractions and Induction of Hydrolase Activity by the Gut Microflora.” International Journal of Biological Macromolecules 41 (5): 584–89. doi:10.1016/j.ijbiomac.2007.07.017.
Walton, Gemma E., Congyi Lu, Isabel Trogh, Filip Arnaut, and Glenn R. Gibson. 2012. “A Randomised, Double-Blind, Placebo Controlled Cross-over Study to Determine the Gastrointestinal Effects of Consumption of Arabinoxylan-Oligosaccharides Enriched Bread in Healthy Volunteers.” Nutrition Journal 11: 36. doi:10.1186/1475-2891-11-36.
Wang, J. F., Y. H. Zhu, D. F. Li, Z. Wang, and B. B. Jensen. 2004. “In Vitro Fermentation of Various Fiber and Starch Sources by Pig Fecal Inocula.” Journal of Animal Science 82 (9): 2615–22. doi:10.2527/2004.8292615x.
Williams, Barbara A., Deirdre Mikkelsen, Laure le Paih, and Michael J. Gidley. 2011. “In Vitro Fermentation Kinetics and End-Products of Cereal Arabinoxylans and (1,3;1,4)-β-Glucans by Porcine Faeces.” Journal of Cereal Science 53 (1): 53–58. doi:10.1016/j.jcs.2010.09.003.
Windey, Karen, Isabelle François, Willem Broekaert, Vicky De Preter, Jan A. Delcour, Thierry Louat, Jean Herman, and Kristin Verbeke. 2014. “High Dose of Prebiotics Reduces Fecal Water Cytotoxicity in Healthy Subjects.” Molecular Nutrition & Food Research 58 (11): 2206–18. doi:10.1002/mnfr.201400298.