Effects of a wheat bran extract containing arabinoxylan oligosaccharides on gastrointestinal health parameters in healthy adult human volunteers: A double-blind, randomised, placebo-controlled, cross-over trial

British Journal of Nutrition

Volumn 108, Issue 12, 2012, Pages 2229-2242

  François, Isabelle E J A ^a   Lescroart, Olivier ^a   Veraverbeke, Wim S ^a   Marzorati, Massimo ^b   Possemiers, Sam ^b   Evenepoel, Pieter ^c   Hamer, Henrike ^c   Houben, Els ^c   Windey, Karen ^c   Welling, Gjalt W ^d   Delcour, Jan A ^e   Courtin, Christophe M ^e   Verbeke, Kristin ^c   Broekaert, Willem F ^a  

^a Fugeia NV   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

Author keywords

Colonic SCFA; p Cresol; Prebiotics; Protein fermentation reduction; Wheat bran extract

Indexed keywords

ARABINOXYLAN; CARBOHYDRATE; DRUG METABOLITE; OLIGOSACCHARIDE; PARA CRESOL; PHENOL; PLACEBO; PLANT EXTRACT; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; WHEAT BRAN EXTRACT;

ADULT; ARTICLE; BIFIDOBACTERIUM; BLOOD SAMPLING; CHEMICAL PARAMETERS; CONSTIPATION; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIET RESTRICTION; DIGESTIVE TRACT PARAMETERS; DISEASE SEVERITY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG MEGADOSE; DRUG TOLERABILITY; FECES ANALYSIS; FECES LEVEL; FEMALE; FERMENTATION; FLATULENCE; GASTROINTESTINAL SYMPTOM; HEMATOLOGICAL PARAMETERS; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; INTERVENTION STUDY; LOW DRUG DOSE; MALE; MORBIDITY; NONHUMAN; NORMAL HUMAN; NUTRITIONAL PARAMETERS; PH; QUESTIONNAIRE; RANDOMIZED CONTROLLED TRIAL; SCORING SYSTEM; URINALYSIS; URINARY EXCRETION; VOLUNTEER; WHEAT BRAN;

ADULT; BIFIDOBACTERIUM; CRESOLS; CROSS-OVER STUDIES; DIETARY FIBER; DOUBLE-BLIND METHOD; FATTY ACIDS, VOLATILE; FECES; FEMALE; FERMENTATION; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; HEALTH PROMOTION; HUMANS; HYDROGEN-ION CONCENTRATION; MALE; MIDDLE AGED; OLIGOSACCHARIDES; PLACEBOS; PLANT EXTRACTS; XYLANS;

TRITICUM AESTIVUM;

EID: 84871557038     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114512000372     Document Type: Article

References (83)

1. Swennen K, Courtin CM, Lindemans GCJE, et al. (2006) Large scale production and characterisation of wheat bran arabinoxylooligosaccharides. J Sci Food Agric 86, 1722-1731.
2. Izydorczyk MS & Biliaderis CG (1995) Cereal arabinoxylans: advances in structure and physicochemical properties. Car-bohydr Polym 28, 33-48.
3. Schooneveld-Bergmans MEF, Beldman G & Voragen AGJ (1999) Structural features of glucurono(arabinoxylans) extracted from wheat bran by barium hydroxide. J Cereal Sci 29, 63-75. (Pubitemid 129550018)
4. Andersson R & Aman P. (2008) Cereal arabinoxylan: occurrence, structure and properties. In Advanced Dietary Fibre Technology, pp. 301-314 [BV McCleary and L Prosky, editors]. Oxford: Blackwell Science Ltd.
5. Femia AP, Salvadori M, Broekaert WF, et al. (2010) Arabinox-ylan oligosaccharides (AXOS) reduce preneoplastic lesions in the colon of rats treated with 1, 2-dimethylhydrazine (DMH). Eur J Nutr 49, 127-132.
6. Yamada H, Itoh K, Morishita Y, et al. (1993) Structure and properties of oligosaccharides from wheat bran. Cereal Food World 38, 490-492.
7. Courtin CM, Swennen K, Broekaert WF, et al. (2008) Dietary inclusion of wheat bran arabinoxylooligosaccharides has beneficial nutritional effects on chickens. Cereal Chem 85, 607-613.
8. Courtin CM, Swennen K, Broekaert WF, et al. (2008) Effects of dietary inclusion of xylooligosaccharides, arabinoxylooli-gosaccharides and soluble arabinoxylan on the microbial composition of caecal contents of chickens. J Sci Food Agric 88, 2517-2522.
9. 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.
10. Cloetens L, Broekaert WF, Delaedt Y, et al. (2010) Tolerance of arabinoxylan-oligosaccharides and their prebiotic activity in healthy subjects: a randomised, placebo-controlled cross-over study. Br J Nutr 103, 703-713.
11. Broekaert WF, Courtin CM, Verbeke K, et al. (2011) Prebiotic and other health-related effects of cereal-derived arabinoxylans, arabinoxylan- oligosaccharides and xylo-oligo-saccharides. Crit Rev Food Sci Nutr 51, 178-194.
12. Hamer HM, De Preter V, Cloetens L, et al. (2010) A dietary intervention with arabinoxylan oligosaccharides reduces colonic protein fermenation in heatlhy subjects: results from faecal metabolite fingerprint analysis. Gastroenterology 138, Suppl. 1, 616.
13. Hughes R, Magee EA & Bingham S (2000) Protein degradation in the large intestine: relevance to colorectal cancer. Curr Issues Intest Microbiol 1, 51-58.
14. Bammens B, Evenepoel P, Keuleers H, et al. (2006) Free serum concentrations of the protein-bound retention solute p-cresol predict mortality in hemodialysis patients. Kidney Int 69, 1081-1087. (Pubitemid 43372184)
15. Muir JG, Walker KZ, Kaimakamis MA, et al. (1998) Modulation of fecal markers relevant to colon cancer risk: a high-starch Chinese diet did not generate expected beneficial changes relative to a Western-type diet. Am J Clin Nutr 68, 372-379. (Pubitemid 28355656)
16. Bone E, Tamm A & Hill M (1976) Production of urinary phenols by gut bacteria and their possible role in causation of large bowel cancer. Am J Clin Nutr 29, 1448-1454. (Pubitemid 8007312)
17. De Graaf AA & Venema K (2008) Gaining insight into microbial physiology in the large intestine: a special role for stable isotopes. Adv Microb Physiol 53, 73-168.
18. Meijers B, De Preter V, Verbeke K, et al. (2009) p-Cresyl sulfate serum concentratons in haemodialysis patients are reduced by the prebiotic oligofructose-enriched inulin. Nephrol Dial Transplant 25, 219-224.
19. De Preter V, Falony G, Windey K, et al. (2010) The prebiotic, oligofructose-enriched inulin modulates the faecal metabolite profile: an in vitro analysis. Mol Nutr Food Res 54, 1791-1801.
20. Grootaert C, Delcour JA, Courtin CM, et al. (2007) Microbial metabolism and prebiotic potency of arabinoxylan oligosac-charides in the human intestine. Trends Food Sci Technol 18, 64-71. (Pubitemid 46136903)
21. Sanchez JI, Marzorati M, Grootaert C, et al. (2009) Arabinox-ylan- oligosaccharides (AXOS) affect the protein/carbohydrate fermentation balance and microbial population dynamics of the Simulator of Human Intestinal Microbial Ecosystem. Microb Biotechnol 2, 101-113.
22. Topping DL & Clifton PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and non-starch polysaccharides. Physiol Rev 81, 1031-1064. (Pubitemid 32611227)
23. Hamer HM, Jonkers D, Venema K, et al. (2008) Review Article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27, 104-119. (Pubitemid 350256609)
24. Frankel WL, Zhang W, Singh A, et al. (1994) Mediation of the throphic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology 106, 375-380. (Pubitemid 24041214)
25. Roediger WE (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83, 424-429. (Pubitemid 12078229)
26. Wong JM, de Souza R, Kendall CW, et al. (2006) Colonic health fermentation and short-chain fatty acids. J Clin Gas-troenterol 40, 235-243. (Pubitemid 44309560)
27. Young GP, Hu Y, Le Leu RK, et al. (2005) Dietary fibre and colorectal cancer: a model for environment-gene interactions. Mol Nutr Food Res 49, 571-584. (Pubitemid 40853703)
28. Borowicki A, Stein K, Scharlau K, et al. (2010) Fermented wheat aleurone inhibits growth and induces apoptosis in human HT29 colon adenocarcinoma cells. Br J Nutr 103, 360-369.
29. Robertson DM (2007) Metabolic cross talk between the colon and the periphery: implications for insulin sensitivity. Proc Nutr Soc 66, 351-361.
30. Tazoe H, Otomo Y, Kaji I, et al. (2008) Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. J Physiol Pharmacol 59, Suppl. 2, 251-262.
31. Hu GX, Chen GR, Xu H, et al. (2010) Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. Med Hypotheses 74, 123-126.
32. Winder WW & Hardie DG (1999) AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am J Physiol 277, E1-E10. (Pubitemid 29356721)
33. Zhang BB, Zhou G & Li C (2009) AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metabol 9, 407-416.
34. Grabitske HA & Slavin JL (2009) Gastrointestinal effects of low-digestible carbohydrates. Crit Rev Food Sci Nutr 49, 327-360.
35. Livesey G (2001) Tolerance of low-digestible carbohydrates: a general view. Br J Nutr 85, Suppl. 1, S7-S16. (Pubitemid 32293770)
36. Cloetens L, De Preter V, Swennen K, et al. (2008) Dose-response effect of arabinoxylooligosaccharides on gastrointestinal motility and on colonic bacterial metabolism in healthy volunteers. J Am Coll Nutr 27, 512-518.
37. Knuiman JT, Hautvast JGAG, Van Der Heyden L, et al. (1986) A multi-centre study on completeness of urine collection in 11 European centres. Some problems with the use of creati-nine and 4-aminobenzoic acid as markers of the completeness of collection. Hum Nutr Clin Nutr 50, 229-237. (Pubitemid 16079673)
38. Murakami K, Sasaki S, Takahashi Y, et al. (2008) Sensitivity and specificity of published strategies using urinary creati-nine to identify incomplete 24-h urine collection. Nutr 24, 16-20.
39. Franks AH, Harmsen HJM, Raangs GC, et al. (1998) Variations of bacterial populations in human feces quantified by fluorescent in situ hybridization with group specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Micro-biol 64, 3336-3345. (Pubitemid 28411456)
40. 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.
41. Harmsen HJM, Elfferich P, Schut F, et al. (1999) A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microb Ecol Health Dis 11, 3-12. (Pubitemid 29248950)
42. Suau A, Bonnet R, Stutren M, et al. (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 65, 4799-4807.
43. Aminov R, Walker AW, Duncan SH, et al. (2006) Molecular diversity, cultivation, and improved detection by fluorescent in situ hybridization of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale. Appl Env Microbiol 72, 6371-6376. (Pubitemid 44414672)
44. Harmsen HJM, Raangs GC, He T, et al. (2002) Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 68, 2982-2990. (Pubitemid 34602022)
45. Van de Wiele T, Boon N, Possemiers S, et al. (2004) Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem. FEMS Microbiol Ecol 51, 143-153. (Pubitemid 39647647)
46. Yap WKW, Mohamed S, Jamal MH, et al. (2008) Changes in infants faecal characteristics and microbiota by inulin supplementation. J Clin Biochem Nutr 43, 159-166.
47. Bremner JM & Keeney RD (1965) Steam distillation methods for determination of ammonium, nitrate and nitrite. Anal Chem Acta 32, 485-495.
48. De Loor H, Bammens B, Evenepoel P, et al. (2005) Gas chro-matographic- mass spectrometric analysis for measurement of p-cresol and its conjugated metabolites in uremic and normal serum. Clin Chem 51, 1535-1538. (Pubitemid 41060897)
49. van Munster IP, de Boer HM, Jansen MC, et al. (1994) Effect of resistant starch on breath-hydrogen and methane excretion in healthy volunteers. Am J Clin Nutr 59, 626-630. (Pubitemid 24085099)
50. Riegler G & Esposito I (2001) Bristol scale stool form. A still valid help in medical practice and clinical research. Tech Coloproctol 5, 163-164. (Pubitemid 34151627)
51. Maki KC, Carson ML, Miller MP, et al. (2009) Hydroxypropyl- methylcellulose lowers cholesterol in statin-treated men and women with primary hypercholesterolemia. Eur J Clin Nutr. 63, 1001-1007.
52. Shapiro SS & Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52, 591-611.
53. Conover WJ & Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 35, 124-129.
54. Pinheiro JC & Bates DM. (2004) Mixed-Effects Models in S and S-PLUS. New York: Springer-Verlag.
55. Hothorn T, Bretz F & Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50, 346-363.
56. Sidak Z (1967) Rectangular confidence region for the means of multivariate normal distributions. J Am Stat Ass 62, 626-633.
57. Hopkins MJ, Sharp R & Macfarlane GT (2002) Variation in human intestinal microbiota with age. Dig Liv Dis 34, Suppl. 2, S12-S18.
58. Woodmansey EJ (2007) Intestinal bacteria and ageing. J Appl Microbiol 102, 1178-1186. (Pubitemid 46633436)
59. Roberfroid M (2005) Inulin-Type Fructans. Functional Food Ingredients. Boca Raton, FL: CRC Press.
60. Roberfroid M (2007) Prebiotics: the concept revisited. J Nutr 137, Suppl. 2, 830S-837S. (Pubitemid 46397526)
61. Meyer D & Stasse-Wolthuis M (2009) The bifidogenic effect of inulin and oligofrucotse and its consequences for gut health. Eur J Clin Nutr 63, 1277-1289.
62. Van Dokkum W, Wezendonk B, Srikumar TS, et al. (1999) Effect of nondigestible oligosaccharides on large-bowel functions, blood lipid concentrations and glucose absorption in young healthy male subjects. Eur J Clin Nutr 53, 1-7. (Pubitemid 29041815)
63. Grasten S, Liukkonen K-H, Chrevatidis A, et al. (2003) Effects of wheat pentosan and inulin on the metabolic activity of fecal microbiota and on bowel function in healthy humans. Nutr Res 23, 1503-1514. (Pubitemid 37303888)
64. Causey JL, Feirtag JM, Gallaher DD, et al. (2000) Effects of dietary inulin on serum lipids, blood glucose and the gastrointestinal environment in hypercholesterolemic men. Nutr Res 20, 191-201. (Pubitemid 30084523)
65. Slavin J & Feirtag J (2011) Chicory inulin does not increase stool weight or speed up intestinal transit time in healthy male subjects. Food Funct 2, 72-76.
66. Kleessen B, Sykura B, Zunft HJ, et al. (1997) Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Clin Nutr 65, 1397-1402. (Pubitemid 27187749)
67. Gibson GR, Beatty ER, Wang X, et al. (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975-982.
68. Van Laere K, Hartemink R, Bosveld M, et al. (2000) Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by intestinal bacteria. J Agric Food Chem 48, 1644-1652. (Pubitemid 30331502)
69. Falony G, Vlachou A, Verbrugghe K, et al. (2006) Crossfeeding between Bifidobacterium longum BB536 and acetate-converting butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Mirobiol 72, 7835-7841. (Pubitemid 44927691)
70. Morrison DJ, Mackay WD, Edwards CA, et al. (2006) Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate? Br J Nutr 96, 570-577. (Pubitemid 46470208)
71. Louis P & Flint HJ (2009) Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294, 1-8.
72. Louis P, Young P, Holtrop G, et al. (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 12, 304-314.
73. Topping DL, Fukushima M & Bird AR (2003) Resistant starch as a prebiotic and synbiotic. Proc Nutr Soc 62, 171-176.
74. Zampa A, Silvi S, Fabiani R, et al. (2004) Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10, 19-26. (Pubitemid 38368883)
75. Macfarlane GT, Allison C & Gibson GR (1988) Effect of pH on protease activities in the large intestine. Lett Appl Micro-biol 7, 161-164. (Pubitemid 19043949)
76. Bouhnik Y, Vahedi K, Achour L, et al. (1999) Short-chain fructooligosaccharide administration dose-dependently increases faecal bifidobacteria in healthy humans. J Nutr 129, 113-116. (Pubitemid 29044767)
77. Kruse HP, Kleessen B & Blaut M (1999) Effects of inulin on faecal bifidobacteria in human subjects. Br J Nutr 82, 375-382. (Pubitemid 29531267)
78. Bouhnik Y, Raskine L, Champion K, et al. (2007) Prolonoged administration of low-dose inulin stimulates the growth of bifidobacteria in humans. Nutr Res 27, 187-193. (Pubitemid 46550702)
79. Bonnema AL, Kolberg LW, Thomas W, et al. (2010) Gastrointestinal tolerance of chicory inulin products. J Am Diet Assoc 110, 865-868.
80. Tateyama I, Hashii K, Johno I, et al. (2005) Effect of xylooli-gosaccharide intake on severe constipation in pregnant women. J Nutr Sci Vitaminol 51, 445-448. (Pubitemid 43151733)
81. Den Hond E, Geypens B & Ghoos Y (2000) Effects of high performance chicory inulin on constipation. Nutr Res 20, 731-736. (Pubitemid 30317216)
82. Marteau P, Jacobs H, Cazaubiel M, et al. (2011) Effects of chicory inulin in constipated elderly people: a doubleblind controlled trial. Int J Food Sci Nutr 62, 164-171.
83. François IEJA, Lescroart O, Veraverbeke WS, et al. (2010) Safety assessment of a wheat bran extract containing arabi-noxylan-oligosaccharides: mutagenicity, clastogenicity and 90-day rat-feeding studies. Int J Toxicol 29, 479-495.