Effect of inulin-type fructans on blood lipid profile and glucose level: A systematic review and meta-analysis of randomized controlled trials

European Journal of Clinical Nutrition

Volumn 71, Issue 1, 2017, Pages 9-20

  Liu, F ^a   Prabhakar, M ^a   Ju, J ^b   Long, H ^a   Zhou, H W ^a,c  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b SHANDONG UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTAN; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INULIN; INULIN TYPE FRUCTAN; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; UNCLASSIFIED DRUG; HIGH DENSITY LIPOPROTEIN; INSULIN; LOW DENSITY LIPOPROTEIN;

DIET RESTRICTION; DIET SUPPLEMENTATION; DYSLIPIDEMIA; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HUMAN; LIPID BLOOD LEVEL; META ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PUBLISHING; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SYSTEMATIC REVIEW; ADULT; ANALYSIS; BLOOD; DIETARY SUPPLEMENT; FEMALE; MALE;

ADULT; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; DIETARY SUPPLEMENTS; DYSLIPIDEMIAS; FASTING; FEMALE; FRUCTANS; HUMANS; INSULIN; INULIN; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MALE; OVERWEIGHT; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 84987623393     PISSN: 09543007     EISSN: 14765640     Source Type: Journal    
DOI: 10.1038/ejcn.2016.156     Document Type: Review

References (79)

1. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 1995; 125: 1401-1412
2. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I et al. Prebiotic effects: metabolic and health benefits. Br J Nutr 2010; 104(Suppl 2): S1-S63
3. Kelly G. Inulin-type prebiotics-A review: part 1. Altern Med Rev 2008; 13: 315-329
4. Delzenne NM, Neyrinck AM, Backhed F, Cani PD. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 2011; 7: 639-646
5. Delzenne NM, Neyrinck AM, Cani PD. Modulation of the gut microbiota by nutrients with prebiotic properties: consequences for host health in the context of obesity and metabolic syndrome. Microb Cell Fact 2011; 10(Suppl 1): S10
6. Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, Louis P. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 2009; 101: 541-550
7. Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, Le Chatelier E et al. Dietary intervention impact on gut microbial gene richness. Nature 2013; 500: 585-588
8. 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: 541-546
9. Karlsson FH, Tremaroli V, Nookaew I, Bergström G, Behre CJ, Fagerberg B et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature 2013; 498: 99-103
10. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490: 55-60
11. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008; 57: 1470-1481
12. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 2011; 472: 57-63
13. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK et al. Gut microbiota in human adults with type 2 diabetes differs from nondiabetic adults. PLoS One 2010; 5: e9085
14. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE et al. A core gut microbiome in obese and lean twins. Nature 2009; 457: 480-484
15. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesityassociated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027-1031
16. Cani PD, Delzenne NM. Gut microflora as a target for energy and metabolic homeostasis. Curr Opin Clin Nutr Metab Care 2007; 10: 729-734
17. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101: 15718-15723
18. Ranganath LR, Beety JM, Morgan LM, Wright JW, Howland R, Marks V. Attenuated GLP-1 secretion in obesity: cause or consequence? Gut 1996; 38: 916-919
19. Bonsu NK, Johnson CS, McLeod KM. Can dietary fructans lower serum glucose? J Diabetes 2011; 3: 58-66
20. Wu T, Yang Y, Zhang L, Han J. Systematic review of the effects of inulin-type fructans on blood lipid profiles: a meta-analysis. Journal of Hygiene Research 2010; 39: 172-176
21. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006-1012
22. Higgins J, Green S. Cochrane handbook for systematic reviews of interventions. Cochrane collaboration. 2011. Available at: www.cochranehandbook.org
23. Laird NM, Mosteller F. Some statistical methods for combining experimental results. International J Technol Assess Health Care 1990; 6: 5-30
24. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560
25. Sterne JA, Sutton AJ, Ioannidis JP, Terrin N, Jones DR, Lau J et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 2011; 343: d4002
26. Dehghan P, Gargari BP, Jafar-Abadi MA, Aliasgharzadeh A. Inulin controls inflammation and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized-controlled clinical trial. Int J Food Sci and Nutr 2014; 65: 117-123
27. Dehghan P, Pourghassem GB, Asgharijafarabadi M. Effects of high performance inulin supplementation on glycemic status and lipid profile in women with type 2 diabetes: a randomized, placebo-controlled clinical trial. Health Promot Perspect 2013; 3: 55-63
28. Van Dokkum W, Wezendonk B, Srikumar TS, Van Den Heuvel EG. Effect of nondigestible oligosaccharides on large-bowel functions, blood lipid concentrations and glucose absorption in young healthy male subjects. Eur J Clin Nutr 1999; 53: 1-7
29. Forcheron F, Beylot M. Long-term administration of inulin-type fructans has no significant lipid-lowering effect in normolipidemic humans. Metabol-Clin and Experim 2007; 56: 1093-1098
30. Letexier D, Diraison F, Beylot M. Addition of inulin to a moderately highcarbohydrate diet reduces hepatic lipogenesis and plasma triacylglycerol concentrations in humans. American J Clin Nutr 2003; 77: 559-564
31. Luo J, Van Yperselle M, Rizkalla SW, Rossi F, Bornet FR, Slama G. Chronic consumption of short-chain fructooligosaccharides does not affect basal hepatic glucose production or insulin resistance in type 2 diabetics. J Nutr 2000; 130: 1572-1577
32. Pedersen A, Sandstrom B, Van Amelsvoort JM. The effect of ingestion of inulin on blood lipids and gastrointestinal symptoms in healthy females. Br J Nutr 1997; 78: 215-222
33. Russo F, Chimienti G, Riezzo G, Pepe G, Petrosillo G, Chiloiro M et al. Inulinenriched pasta affects lipid profile and Lp(a) concentrations in Italian young healthy male volunteers. Eur J Nutr 2008; 47: 453-459
34. Scheid MM, Genaro PS, Moreno YM, Pastore GM. Freeze-dried powdered yacon: effects of FOS on serum glucose, lipids and intestinal transit in the elderly. Eur J Clin Nutr 2014; 53: 1457-1464
35. Causey JL, Feirtag JM, Gallaher DD. Effects of dietary inulin on serum lipids, blood glucose and the gastrointestinal environment in hypercholesterolemic men. Nutr Res 2000; 20: 191-201
36. Davidson MH, Maki KC. Effects of dietary inulin on serum lipids. J Nutr 1999; 129: 1474S-1477S
37. Giacco R, Clemente G, Luongo D, Lasorella G, Fiume I, Brouns F et al. Effects of short-chain fructo-oligosaccharides on glucose and lipid metabolism in mild hypercholesterolaemic individuals. Clin Nutr 2004; 23: 331-340
38. Jackson KG, Taylor GR, Clohessy AM, Williams CM. The effect of the daily intake of inulin on fasting lipid, insulin and glucose concentrations in middle-aged men and women. Br J Nutr 1999; 82: 23-30
39. Daud NM, Ismail NA, Thomas EL, Fitzpatrick JA, Bell JD, Swann JR et al. The impact of oligofructose on stimulation of gut hormones, appetite regulation and adiposity. Obesity (Silver Spring) 2014; 22: 1430-1438
40. Luis DA, Fuente B, Izaola O, Aller R, Gutierrez S, Morillo M. Double blind randomized clinical trial controlled by placebo with a fos enriched cookie on saciety and cardiovascular risk factors in obese patients. Nutr Hosp 2013; 28: 78-85
41. Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PG, Neyrinck AM et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 2013; 62: 1112-1121
42. Genta S, Cabrera W, Habib N, Pons J, Carillo IM, Grau A et al. Yacon syrup: beneficial effects on obesity and insulin resistance in humans. Clin Nutr 2009; 28: 182-187
43. Parnell JA, Reimer RA. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr 2009; 89: 1751-1759
44. Tovar AR, Caamano MC, Garcia-Padilla S, Garcia OP, Duarte MA, Rosado JL. The inclusion of a partial meal replacement with or without inulin to a calorie restricted diet contributes to reach recommended intakes of micronutrients and decrease plasma triglycerides: a randomized clinical trial in obese Mexican women. Nutr J 2012; 11: 44
45. Alles MS, Roos NM, Bakx JC, van Lisdonk E, Zock PL, Hautvast GA. Consumption of fructooligosaccharides does not favorably affect blood glucose and serum lipid concentrations in patients with type 2 diabetes. Am J Clin Nuti 1999; 69: 64-69
46. Wu X, Ma C, Han L, Nawaz M, Gao F, Zhang X et al. Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr Microbiol 2010; 61: 69-78
47. Beserra BT, Fernandes R, Do RV, Mocellin MC, Kuntz MG, Trindade EB. A systematic review and meta-analysis of the prebiotics and synbiotics effects on glycaemia, insulin concentrations and lipid parameters in adult patients with overweight or obesity. Clin Nutr 2015; 34: 845-858
48. Brighenti F. Dietary fructans and serum triacylglycerols: a meta-analysis of randomized controlled trials. J Nutr 2007; 137: 2552S-2556S
49. Roberfroid MB, Delzenne NM. Dietary fructans. Annu Rev Nutr 1998; 18: 117-143
50. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I et al. Prebiotic effects: metabolic and health benefits. Br J Nutr 2010; 104(Suppl 2): S1-S63
51. Liu TW, Cephas KD, Holscher HD, Kerr KR, Mangian HF, Tappenden KA et al. Nondigestible fructans alter gastrointestinal barrier function, gene expression, histomorphology, and the microbiota profiles of diet-induced obese C57BL/ 6 J mice. J Nutr 2016; 146: 949-956
52. Holme I. An analysis of randomized trials evaluating the effect of cholesterol reduction on total mortality and coronary heart disease incidence. Circulation 1990; 82: 1916-1924
53. National Heart Foundation clinical guidelines for the assessment and management of dyslipidaemia. Dyslipidaemia Advisory Group on behalf of the scientific committee of the National Heart Foundation of New Zealand. N Z Med J 1996; 109: 224-231
54. Jenkins DJ, Jones PJ, Lamarche B, Kendall CW, Faulkner D, Cermakova L et al. Effect of a dietary portfolio of cholesterol-lowering foods given at 2 levels of intensity of dietary advice on serum lipids in hyperlipidemia: a randomized controlled trial. JAMA 2011; 306: 831-839
55. Ooi LG, Liong MT. Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int J Mol Sci 2010; 11: 2499-2522
56. Dikeman CL, Murphy MR, Fahey GJ. Dietary fibers affect viscosity of solutions and simulated human gastric and small intestinal digesta. J Nutr 2006; 136: 913-919
57. Levrat MA, Remesy C, Demigne C. High propionic acid fermentations and mineral accumulation in the cecum of rats adapted to different levels of inulin. J Nutr 1991; 121: 1730-1737
58. Delzenne NM, Daubioul C, Neyrinck A, Lasa M, Taper HS. Inulin and oligofructose modulate lipid metabolism in animals: review of biochemical events and future prospects. Br J Nutr 2002; 87(Suppl 2): S255-S259
59. Wolever TM, Brighenti F, Royall D, Jenkins AL, Jenkins DJ. Effect of rectal infusion of short chain fatty acids in human subjects. Am J Gastroenterology 1989; 84: 1027-1033
60. Kimura I, Inoue D, Maeda T, Hara T, Ichimura A, Miyauchi S et al. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G proteincoupled receptor 41 (GPR41). Proc Natl Acad Sci USA 2011; 108: 8030-8035
61. Mithieux G, Gautier-Stein A. Intestinal glucose metabolism revisited. Diabetes Res Clin Pract 2014; 105: 295-301
62. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A et al. Microbiota-generated metabolites promote metabolic benefits via gutbrain neural circuits. Cell 2014; 156: 84-96
63. Rossi M, Corradini C, Amaretti A, Nicolini M, Pompei A, Zanoni S et al. Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study of pure and fecal cultures. Appl Environ Microbiol 2005; 71: 6150-6158
64. Trautwein EA, Rieckhoff D, Erbersdobler HF. Dietary inulin lowers plasma cholesterol and triacylglycerol and alters biliary bile acid profile in hamsters. J Nutr 1998; 128: 1937-1943
65. Creely SJ, McTernan PG, Kusminski CM, Fisher F, Da SN, Khanolkar M et al. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab 2007; 292: E740-E747
66. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761-1772
67. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. American J Clin Nutr 2008; 87: 534-538
68. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 2010; 18: 190-195
69. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 2007; 50: 2374-2383
70. Kolida S, Meyer D, Gibson GR. A double-blind placebo-controlled study to establish the bifidogenic dose of inulin in healthy humans. European J Clin Nutr 2007; 61: 1189-1195
71. Meyer D, Stasse-Wolthuis M. The bifidogenic effect of inulin and oligofructose and its consequences for gut health. Eur J Clin Nutr 2009; 63: 1277-1289
72. Cani PD, Daubioul CA, Reusens B, Remacle C, Catillon G, Delzenne NM. Involvement of endogenous glucagon-like peptide-1(7-36) amide on glycaemia-lowering effect of oligofructose in streptozotocin-treated rats. J Endocrinol 2005; 185: 457-465
73. Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R. Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes 2006; 55: 1484-1490
74. Delmee E, Cani PD, Gual G, Knauf C, Burcelin R, Maton N et al. Relation between colonic proglucagon expression and metabolic response to oligofructose in high fat diet-fed mice. Life Sci 2006; 79: 1007-1013
75. Urias-Silvas JE, Cani PD, Delmee E, Neyrinck A, Lopez MG, Delzenne NM. Physiological effects of dietary fructans extracted from Agave tequilana Gto. and Dasylirion spp. Br J Nutr 2008; 99: 254-261
76. Delzenne NM, Cani PD, Daubioul C, Neyrinck AM. Impact of inulin and oligofructose on gastrointestinal peptides. Br J Nutr 2005; 93(Suppl 1): S157-S161
77. Tarini J, Wolever TM. The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects. Appl Physiol Nutr Metab 2010; 35: 9-16
78. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E et al. Shortchain fatty acids stimulate glucagon-like peptide-1 secretion via the G-proteincoupled receptor FFAR2. Diabetes 2012; 61: 364-371
79. Drucker DJ. The biology of incretin hormones. Cell Metab 2006; 3: 153-165