Effects of arabinoxylan and resistant starch on intestinal microbiota and short-chain fatty acids in subjects with metabolic syndrome: A randomised crossover study

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Hald, Stine ^a   Schioldan, Anne Grethe ^a   Moore, Mary E ^b   Dige, Anders ^a   Lærke, Helle Nygaard ^c   Agnholt, Jørgen ^a   Knudsen, Knud Erik Bach ^c   Hermansen, Kjeld ^a   Marco, Maria L ^b   Gregersen, Søren ^a   Dahlerup, Jens F ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIHYPERTENSIVE AGENT; ARABINOXYLAN; BENZOIC ACID; BUTYRIC ACID; CARBOHYDRATE; FORMIC ACID; HEXANOIC ACID; HIPPURIC ACID; HYPOCHOLESTEROLEMIC AGENT; ISOVALERIC ACID; LACTIC ACID; LIGNIN; MEBENDAZOLE; RNA 16S; SHORT CHAIN FATTY ACID; SORBIC ACID; STARCH; SUCCINIC ACID; VALERIC ACID; VOLATILE FATTY ACID; XYLAN;

ABDOMINAL DISCOMFORT; ABDOMINAL PAIN; ADULT; AGED; ALCOHOL CONSUMPTION; ANTHROPOMETRY; ARTICLE; BACTEROIDETES; BIFIDOBACTERIUM; BLOATING; BODY FAT DISTRIBUTION; BODY MASS; BODY WEIGHT; CALORIC INTAKE; CEREAL; CLINICAL ARTICLE; CONSTIPATION; CONTROLLED STUDY; CROSSOVER PROCEDURE; DESULFOVIBRIONACEAE; DIET SUPPLEMENTATION; DIETARY FIBER; DIETARY INTAKE; DNA EXTRACTION; ENTEROBIASIS; FECES ANALYSIS; FEMALE; FIRMICUTES; FLATULENCE; FOOD COMPOSITION; GASTROINTESTINAL SYMPTOM; GENE AMPLIFICATION; GENE SEQUENCE; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; INTERVENTION STUDY; INTESTINE FLORA; LIFESTYLE; MALE; METABOLIC SYNDROME X; NAUSEA; PARABACTEROIDES; PHYSICAL ACTIVITY; QUESTIONNAIRE; RANDOMIZED CONTROLLED TRIAL; RATING SCALE; SCORING SYSTEM; SMOKING HABIT; WAIST CIRCUMFERENCE; WESTERN DIET; ADMINISTRATION AND DOSAGE; DIET THERAPY; DRUG EFFECTS; ENERGY METABOLISM; FECES; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MICROFLORA; MIDDLE AGED;

AGED; BIFIDOBACTERIUM; CROSS-OVER STUDIES; DIETARY FIBER; ENERGY METABOLISM; FATTY ACIDS, VOLATILE; FECES; FEMALE; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; MALE; METABOLIC SYNDROME X; MICROBIOTA; MIDDLE AGED; RNA, RIBOSOMAL, 16S; STARCH; XYLANS;

EID: 84979289595     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0159223     Document Type: Article

References (71)

1. Hartvigsen ML, Gregersen S, Laerke HN, Holst JJ, Bach Knudsen KE, Hermansen K. Effects of concentrated arabinoxylan and beta-glucan compared with refined wheat and whole grain rye on glucose and appetite in subjects with the metabolic syndrome: a randomized study. European journal of clinical nutrition. 2014; 68(1):84-90. doi: 10.1038/ejcn.2013.236 PMID: 24253758
2. Kovatcheva-Datchary P, Arora T. Nutrition, the gut microbiome and the metabolic syndrome. Best practice & researchClinical gastroenterology. 2013; 27(1):59-72. doi: 10.1016/j.bpg.2013.03.017
3. McIntosh GH, Noakes M, Royle PJ, Foster PR. Whole-grain rye and wheat foods and markers of bowel health in overweight middle-aged men. The American Journal of Clinical Nutrition. 2003; 77(4):967-74. PMID: 12663299
4. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature. 2013; 500(7464):541-6. doi: 10.1038/nature12506 PMID: 23985870
5. Haenen D, Zhang J, da Silva CS, Bosch G, van der Meer IM, van Arkel J, et al. A Diet High in Resistant Starch Modulates Microbiota Composition, SCFA Concentrations, and Gene Expression in Pig Intestine. The Journal of nutrition. 2013. doi: 10.3945/jn.112.169672
6. Yamashita H, Fujisawa K, Ito E, Idei S, Kawaguchi N, Kimoto M, et al. Improvement of obesity and glucose tolerance by acetate in Type 2 diabetic Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Bioscience, biotechnology, and biochemistry. 2007; 71(5):1236-43. JST.JSTAGE/bbb/60668 [pii]. PMID: 17485860
7. Lin HV, Frassetto A, Kowalik EJ Jr., Nawrocki AR, Lu MM, Kosinski JR, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PloS one. 2012; 7(4):e35240. doi: 10.1371/journal.pone.0035240 PMID: 22506074
8. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009; 58(7):1509-17. doi: 10.2337/db08-1637 PMID: 19366864
9. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacological research. 2013; 69(1):52-60. Epub 2012/11/14. doi: 10.1016/j.phrs.2012.10.020 PMID: 23147033.
10. Lattimer JM, Haub MD. Effects of dietary fiber and its components on metabolic health. Nutrients. 2010; 2(12):1266-89. 10.3390/nu2121266; doi: 10.3390/nu2121266 PMID: 22254008
11. Starch Resistant. Proceedings for the 2nd plenary meeting of EURESTA: European FLAIR Concerted Action No. 11 on physiological implications of the consumption of resistant starch in man. Crete, 29 May-2 June 1991. European journal of clinical nutrition. 1992; 46 Suppl 2:S1-148.
12. Weaver GA, Krause JA, Miller TL, Wolin MJ. Cornstarch fermentation by the colonic microbial community yields more butyrate than does cabbage fiber fermentation; cornstarch fermentation rates correlate negatively with methanogenesis. The American Journal of Clinical Nutrition. 1992; 55(1):70-7. PMID:1309475
13. van Munster IP, Tangerman A, Nagengast FM. Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Digestive diseases and sciences. 1994; 39(4):834-42. PMID: 8149850
14. Martinez I, Kim J, Duffy PR, Schlegel VL, Walter J. Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PloS one. 2010; 5(11):e15046. doi: 10.1371/journal.pone.0015046 PMID: 21151493
15. Nielsen TS, Laerke HN, Theil PK, Sorensen JF, Saarinen M, Forssten S, et al. Diets high in resistant starch and arabinoxylan modulate digestion processes and SCFA pool size in the large intestine and faecal microbial composition in pigs. The British journal of nutrition. 2014:1-13. S000711451400302X [pii].
16. Tachon S, Zhou J, Keenan M, Martin R, Marco ML. The intestinal microbiota in aged mice is modulated by dietary resistant starch and correlated with improvements in host responses. FEMS microbiology ecology. 2013; 83(2):299-309. doi: 10.1111/j.1574-6941.2012.01475.x PMID: 22909308
17. Abell GC, Cooke CM, Bennett CN, Conlon MA, McOrist AL. Phylotypes related to Ruminococcus bromii are abundant in the large bowel of humans and increase in response to a diet high in resistant starch. FEMS microbiology ecology. 2008; 66(3):505-15. doi: 10.1111/j.1574-6941.2008.00527.x PMID: 18616586
18. Ze X, Duncan SH, Louis P, Flint HJ. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. The ISME journal. 2012; 6(8):1535-43. doi: 10.1038/ismej.2012.4 PMID: 22343308
19. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. Isme j. 2011; 5(2):220-30. Epub 2010/08/06. doi: 10.1038/ismej.2010.118 PMID: 20686513; PubMed Central PMCID: PMCPmc3105703.
20. Saulnier L, Sada P-E, Branlard G, Charmet G, Guillon F. Wheat arabinoxylans: Exploiting variation in amount and composition to develop enhanced varieties. Journal of Cereal Science. 2007; 46(3):261-81.
21. Bach Knudsen KE, Serena A, Kjaer AK, Jorgensen H, Engberg R. Rye bread enhances the production and plasma concentration of butyrate but not the plasma concentrations of glucose and insulin in pigs. The Journal of nutrition. 2005; 135(7):1696-704. 135/7/1696 [pii]. PMID: 15987852
22. Neyrinck AM, Possemiers S, Druart C, Van de Wiele T, De Backer F, Cani PD, et al. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, Roseburia and Bacteroides/Prevotella in diet-induced obese mice. PloS one. 2011; 6(6):e20944. doi: 10.1371/journal.pone.0020944 PMID: 21695273
23. Lappi J, Salojarvi J, Kolehmainen M, Mykkanen H, Poutanen K, de Vos WM, et al. Intake of whole-grain and fiber-rich rye bread versus refined wheat bread does not differentiate intestinal microbiota composition in Finnish adults with metabolic syndrome. The Journal of nutrition. 2013; 143(5):648-55. doi: 10.3945/jn.112.172668 PMID: 23514765
24. Garcia AL, Steiniger J, Reich SC, Weickert MO, Harsch I, Machowetz A, et al. Arabinoxylan fibre consumption improved glucose metabolism, but did not affect serum adipokines in subjects with impaired glucose tolerance. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme. 2006; 38(11):761-6. doi: 10.1055/s-2006-955089 PMID: 17111305
25. Garcia AL, Otto B, Reich SC, Weickert MO, Steiniger J, Machowetz A, et al. Arabinoxylan consumption decreases postprandial serum glucose, serum insulin and plasma total ghrelin response in subjects with impaired glucose tolerance. European journal of clinical nutrition. 2007; 61(3):334-41. doi: 10.1038/sj.ejcn.1602525 PMID: 16988651
26. Lu ZX, Walker KZ, Muir JG, O'Dea K. Arabinoxylan fibre improves metabolic control in people with Type II diabetes. European journal of clinical nutrition. 2004; 58(4):621-8. doi: 10.1038/sj.ejcn.1601857 PMID: 15042130
27. Alberti KG, Zimmet P, Shaw J, Group IDFETFC. The metabolic syndrome - a new worldwide definition. Lancet. 2005; 366(9491):1059-62. S0140-6736(05)67402-8 [pii]. PMID: 16182882
28. Englyst HN, Kingman SM, Cummings JH. Classification and measurement of nutritionally important starch fractions. European journal of clinical nutrition. 1992; 46 Suppl 2:S33-50. PMID: 1330528
29. Suresh K. An overview of randomization techniques: An unbiased assessment of outcome in clinical research. Journal of human reproductive sciences. 2011; 4(1):8-11. doi: 10.4103/0974-1208.82352 PMID: 21772732
30. Ingerslev AK, Theil PK, Hedemann MS, Laerke HN, Bach Knudsen KE. Resistant starch and arabinoxylan augment SCFA absorption, but affect postprandial glucose and insulin responses differently. The British journal of nutrition. 2014; 111(9):1564-76. doi: 10.1017/S0007114513004066 PMID: 24507768
31. Francis CY, Morris J, Whorwell PJ. The irritable bowel severity scoring system: a simple method of monitoring irritable bowel syndrome and its progress. Alimentary Pharmacology & Therapeutics. 1997; 11(2):395-402.
32. Svedlund J, Sjodin I, Dotevall G. GSRS - a clinical rating scale for gastrointestinal symptoms in patients with irritable bowel syndrome and peptic ulcer disease. Digestive diseases and sciences. 1988; 33(2):129-34. PMID: 3123181
33. Lewis SJ, Heaton KW. Stool form scale as a useful guide to intestinal transit time. Scandinavian Journal of Gastroenterology. 1997; 32(9):920-4. doi: 10.3109/00365529709011203 PMID: 9299672
34. Stjernman H, Granno C, Jarnerot G, Ockander L, Tysk C, Blomberg B, et al. Short health scale: a valid, reliable, and responsive instrument for subjective health assessment in Crohn's disease. Inflammatory bowel diseases. 2008; 14(1):47-52. doi: 10.1002/ibd.20255 PMID: 17828783
35. McCleary BV, Monaghan DA. Measurement of resistant starch. Journal of AOAC International. 2002; 85(3):665-75. PMID: 12083259
36. Bach Knudsen KE. Carbohydrate and lignin contents of plant materials used in animal feeding. Anim Feed Sci Tecnol. 1997; 67(4):319-38. doi: 10.1016/S0377-8401(97)00009-6
37. Englyst HN, Cummings JH. Simplified method for the determination of total non-starch polysaccharides by gas-liquid chromatography of constituent sugars as alditol acetates. Analyst. 1984; 109(7):937-42. doi: 10.1039/AN9840900937
38. Jensen MT, Cox RP, Jensen BB. Microbial production of skatole in the hind gut of pigs given different diets and its relation to skatole deposition in backfat. Animal Science. 1995; 61(02):293-304. doi: 10.1017/S1357729800013837
39. Bokulich NA, Joseph CM, Allen G, Benson AK, Mills DA. Next-generation sequencing reveals significant bacterial diversity of botrytized wine. PloS one. 2012; 7(5):e36357. doi: 10.1371/journal.pone.0036357 PMID: 22563494
40. McInnis EA, Kalanetra KM, Mills DA, Maga EA. Analysis of raw goat milk microbiota: impact of stage of lactation and lysozyme on microbial diversity. Food Microbiology. 2015; 46:121-31. doi: 10.1016/j.fm.2014.07.021 PMID: 25475275
41. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature methods. 2010; 7(5):335-6. doi: 10.1038/nmeth.f.303 PMID: 20383131
42. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology. 2006; 72(7):5069-72. 72/7/5069 [pii]. PMID: 16820507
43. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England). 2010; 26(19):2460-1. doi: 10.1093/bioinformatics/btq461
44. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature methods. 2013; 10(1):57-9. doi: 10.1038/nmeth.2276 PMID: 23202435
45. Faith DP. Conservation evaluation and phylogenetic diversity. Biological Conservation. 1992; 61(1):1-10. http://dx.doi.org/10.1016/0006-3207(92)91201-3.
46. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology. 2005; 71(12):8228-35. 71/12/8228 [pii]. PMID: 16332807
47. Nordgaard I, Hove H, Clausen MR, Mortensen PB. Colonic production of butyrate in patients with previous colonic cancer during long-term treatment with dietary fibre (Plantago ovata seeds). Scandinavian Journal of Gastroenterology. 1996; 31(10):1011-20. PMID: 8898423
48. Schoenfeld DA. Statistical considerations for clinical trials and scintific experiments http://hedwig.mgh.harvard.edu/sample-size/size.html - cross2010 [cited 2015].
49. Julious SA, Campbell MJ, Altman DG. Estimating sample sizes for continuous, binary, and ordinal outcomes in paired comparisons: practical hints. Journal of biopharmaceutical statistics. 1999; 9(2):241-51. Epub 1999/06/24. doi: 10.1081/bip-100101174 PMID: 10379691.
50. Bland M. Cross-over trials https://www-users.york.ac.uk/~mb55/msc/trials/cross.htm2010 [cited 2015].
51. Team RC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013.
52. Salonen A, Lahti L, Salojarvi J, Holtrop G, Korpela K, Duncan SH, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. The ISME journal. 2014; 8(11):2218-30. doi: 10.1038/ismej.2014.63 PMID: 24763370
53. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science (New York, NY). 2011; 334(6052):105-8. doi: 10.1126/science.1208344
54. Tojo R, Suarez A, Clemente MG, de los Reyes-Gavilan CG, Margolles A, Gueimonde M, et al. Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J Gastroenterol. 2014; 20(41):15163-76. Epub 2014/11/12. doi: 10.3748/wjg.v20.i41.15163 PMID: 25386066; PubMed Central PMCID: PMCPmc4223251.
55. Yang J, Keshavarzian A, Rose DJ. Impact of dietary fiber fermentation from cereal grains on metabolite production by the fecal microbiota from normal weight and obese individuals. Journal of medicinal food. 2013; 16(9):862-7. doi: 10.1089/jmf.2012.0292 PMID: 24044495
56. Macfarlane GT, Englyst HN. Starch utilization by the human large intestinal microflora. The Journal of applied bacteriology. 1986; 60(3):195-201. PMID: 2423494
57. Margolles A, Sanchez B. Selection of a Bifidobacterium animalis subsp. lactis strain with a decreased ability to produce acetic acid. Applied and Environmental Microbiology. 2012; 78(9):3338-42. doi: 10.1128/AEM.00129-12 PMID: 22389372
58. Fukuda S, Toh H, Taylor TD, Ohno H, Hattori M. Acetate-producing bifidobacteria protect the host from enteropathogenic infection via carbohydrate transporters. Gut microbes. 2012; 3(5):449-54. 21214 [pii]. PMID: 22825494
59. Tanner SA, Chassard C, Zihler Berner A, Lacroix C. Synergistic effects of Bifidobacterium thermophilum RBL67 and selected prebiotics on inhibition of Salmonella colonization in the swine proximal colon PolyFermS model. Gut pathogens. 2014; 6(1):44-014-0044-y. eCollection 2014. doi: 10.1186/s13099-014-0044-y
60. Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, et al. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Applied and Environmental Microbiology. 2006; 72(5):3593-9. 72/5/3593 [pii]. PMID: 16672507
61. Rios-Covian D, Gueimonde M, Duncan SH, Flint HJ, de Los Reyes-Gavilan CG. Enhanced butyrate formation by cross-feeding between Faecalibacterium prausnitzii and Bifidobacterium adolescentis. FEMS microbiology letters. 2015. Epub 2015/10/01. doi: 10.1093/femsle/fnv176 PMID: 26420851.
62. Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. The British journal of nutrition. 2004; 91(6):915-23. doi: 10.1079/BJN20041150 PMID: 15182395
63. Bourriaud C, Robins RJ, Martin L, Kozlowski F, Tenailleau E, Cherbut C, et al. Lactate is mainly fermented to butyrate by human intestinal microfloras but inter-individual variation is evident. Journal of applied microbiology. 2005; 99(1):201-12. Epub 2005/06/18. doi: 10.1111/j.1365-2672.2005.02605.x PMID: 15960680.
64. Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. The American Journal of Gastroenterology. 2010; 105(11):2420-8. doi: 10.1038/ajg.2010.281 PMID: 20648002
65. Belobrajdic DP, Bird AR, Conlon MA, Williams BA, Kang S, McSweeney CS, et al. An arabinoxylan-rich fraction from wheat enhances caecal fermentation and protects colonocyte DNA against diet-induced damage in pigs. The British journal of nutrition. 2012; 107(9):1274-82. doi: 10.1017/S0007114511004338 PMID: 22115395
66. Poslusna K, Ruprich J, de Vries JH, Jakubikova M, van't Veer P. Misreporting of energy and micronutrient intake estimated by food records and 24 hour recalls, control and adjustment methods in practice. The British journal of nutrition. 2009; 101 Suppl 2:S73-85. doi: 10.1017/S0007114509990602 PMID: 19594967
67. Jonsdottir SE, Brader L, Gunnarsdottir I, Kally Magnusdottir O, Schwab U, Kolehmainen M, et al. Adherence to the Nordic Nutrition Recommendations in a Nordic population with metabolic syndrome: high salt consumption and low dietary fibre intake (The SYSDIET study). Food & nutrition research. 2013; 57: doi: 10.3402/fnr.v57i0.21391
68. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Alimentary Pharmacology & Therapeutics. 2008; 27(2):104-19. doi: 10.1111/j.1365-2036.2007.03562.x
69. Rigottier-Gois L, Bourhis AG, Gramet G, Rochet V, Dore J. Fluorescent hybridisation combined with flow cytometry and hybridisation of total RNA to analyse the composition of microbial communities in human faeces using 16S rRNA probes. FEMS microbiology ecology. 2003; 43(2):237-45. doi: 10.1111/j.1574-6941.2003.tb01063.x PMID: 19719684
70. Kaneda T. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiological reviews. 1991; 55(2):288-302. PMID: 1886522
71. Cummings JH, Beatty ER, Kingman SM, Bingham SA, Englyst HN. Digestion and physiological properties of resistant starch in the human large bowel. The British journal of nutrition. 1996; 75(5):733-47. PMID: 8695600