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Carbohydrates, glycemic index and diabetes mellitus

The acute effects of inulin and resistant starch on postprandial serum short-chain fatty acids and second-meal glycemic response in lean and overweight humans

Abstract

Background/Objectives:

Colonic fermentation of dietary fiber to short-chain fatty acids (SCFA) may protect against obesity and diabetes, but excess production of colonic SCFA has been implicated in the promotion of obesity. We aimed to compare the effects of two fermentable fibers on postprandial SCFA and second-meal glycemic response in healthy overweight or obese (OWO) vs lean (LN) participants.

Subjects/Methods:

Using a randomized crossover design, 13 OWO and 12 LN overnight fasted participants were studied for 6 h on three separate days after consuming 300 ml water containing 75 g glucose (GLU) as control or with 24 g inulin (IN) or 28 g resistant starch (RS). A standard lunch was served 4 h after the test drink.

Results:

Within the entire group, compared with control, IN significantly increased serum SCFA (P<0.001) but had no effect on free-fatty acids (FFA) or second-meal glucose and insulin responses. In contrast, RS had no significant effect on SCFA but reduced FFA rebound (P<0.001) and second-meal glucose (P=0.002) and insulin responses (P=0.024). OWO had similar postprandial serum SCFA and glucose concentrations but significantly greater insulin and FFA than LN. However, the effects of IN and RS on SCFA, glucose, insulin and FFA responses were similar in LN and OWO.

Conclusions:

RS has favorable second-meal effects, likely related to changes in FFA rather than SCFA concentrations. However, a longer study may be needed to demonstrate an effect of RS on SCFA. We found no evidence that acute increases in SCFA after IN reduce glycemic responses in humans, and we were unable to detect a significant difference in SCFA responses between OWO vs LN subjects.

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References

  1. Weickert MO, Pfeiffer AFH . Metabolic effects of dietary fiber consumption and prevention of diabetes. J Nutr 2008; 138: 439–442.

    Article  CAS  Google Scholar 

  2. Nilsson A, Granfeldt Y, Östman E, Preston T, Björck I . Effects of GI and content of indigestible carbohydrates of cereal-based evening meals on glucose tolerance at a subsequent standardised breakfast. Eur J Clin Nutr 2006; 60: 1092–1099.

    Article  CAS  Google Scholar 

  3. Wolever TMS, Bentum-Williams A, Jenkins DJA . Physiological modulation of plasma free fatty acid concentrations by diet: metabolic implications in nondiabetic subjects. Diabetes Care 1995; 18: 962–970.

    Article  CAS  Google Scholar 

  4. Nilsson A, Östman E, Preston T, Björck I . Effects of GI vs content of cereal fibre of the evening meal on glucose tolerance at a subsequent standardized breakfast. Eur J Clin Nutr 2008; 62: 712–720.

    Article  CAS  Google Scholar 

  5. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL et al. Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids. Endocrinology 2008; 149: 4519–4526.

    Article  CAS  Google Scholar 

  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. Biosci Biotechnol Biochem 2007; 71: 1236–1243.

    Article  CAS  Google Scholar 

  7. Crouse JR, Gerson CD, DeCarli LM, Lieber CS . Role of acetate in the reduction of plasma free fatty acids produced by ethanol in man. J Lipid Res 1968; 9: 509–512.

    CAS  PubMed  Google Scholar 

  8. Wolever TMS, Brighenti F, Royall D, Jenkins AL, Jenkins DJA . Effect of rectal infusion of short chain fatty acids in human subjects. Am J Gastroenterol 1989; 84: 1027–1033.

    CAS  PubMed  Google Scholar 

  9. Brighenti F, Benini L, Del Rio D, Casiraghi C, Pellegrini N, Scazzina F et al. Colonic fermentation of indigestible carbohydrates contributes to the second-meal effect. Am J Clin Nutr 2006; 83: 817–822.

    Article  CAS  Google Scholar 

  10. Tarini J, Wolever TMS . 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.

    Article  CAS  Google Scholar 

  11. Slavin J, Stewart M, Timm D, Grabitske H, Hospattankar A Fermentation patterns and short chain fatty acid profiles of wheat dextrin and other functional fibres. In: Dietary Fibre: New Frontiers for Food and Health, 2010, pp 177–191..

  12. Jenkins DJA, Vuksan V, Kendall CWC, Würsch P, Jeffcoat R, Waring S et al. Physiological effects of resistant starches on fecal bulk, short chain fatty acids, blood lipids and glycemic index. J Am Coll Nutr 1998; 17: 609–616.

    Article  CAS  Google Scholar 

  13. Johnston KL, Thomas EL, Bell JD, Frost GS, Robertson MD . Resistant starch improves insulin sensitivity in metabolic syndrome. Diabetic Med 2010; 27: 391–397.

    Article  CAS  Google Scholar 

  14. Robertson MD, Bickerton AS, Dennis AL, Vidal H, Frayn KN . Insulin-sensitizing effects of dietary resistant starch and effects on skeletal muscle and adipose tissue metabolism. Am J Clin Nutr 2005; 82: 559–567.

    Article  CAS  Google Scholar 

  15. Robertson MD, Currie JM, Morgan LM, Jewell DP, Frayn KN . Prior short-term consumption of resistant starch enhances postprandial insulin sensitivity in healthy subjects. Diabetologia 2003; 46: 659–665.

    Article  CAS  Google Scholar 

  16. Robertson MD, Wright JW, Loizon E, Debard C, Vidal H, Shojaee-Moradie F et al. Insulin-sensitizing effects on muscle and adipose tissue after dietary fiber intake in men and women with metabolic syndrome. J Clin Endocrinol Metab 2012; 97: 3326–3332.

    Article  CAS  Google Scholar 

  17. Diez M, Hornick JL, Baldwin P, Istasse L . Influence of a blend of fructo-oligosaccharides and sugar beet fiber on nutrient digestibility and plasma metabolite concentrations in healthy Beagles. Am J Vet Res 1997; 58: 1238–1242.

    CAS  PubMed  Google Scholar 

  18. Rozan P, Nejdi A, Hidalgo S, Bisson JF, Desor D, Messaoudi M . Effects of lifelong intervention with an oligofructose-enriched inulin in rats on general health and lifespan. Br J Nutr 2008; 100: 1192–1199.

    Article  CAS  Google Scholar 

  19. Diez M, Hornick JL, Baldwin P, Van Eenaeme C, Istasse L . The influence of sugar-beet fibre, guar gum and inulin on nutrient digestibility, water consumption and plasma metabolites in healthy Beagle dogs. Res Vet Sci 1998; 64: 91–96.

    Article  CAS  Google Scholar 

  20. Beylot M . Effects of inulin-type fructans on lipid metabolism in man and in animal models. Br J Nutr 2005; 93 (Suppl), S163–S168.

    Article  CAS  Google Scholar 

  21. Bonsu NK, Johnson CS, Mcleod KM . Can dietary fructans lower serum glucose? J Diabetes 2011; 3: 58–66.

    Article  CAS  Google Scholar 

  22. Raninen K, Lappi J, Mykkänen H, Poutanen K . Dietary fiber type reflects physiological functionality: comparison of grain fiber, inulin, and polydextrose. Nutr Rev 2011; 69: 9–21.

    Article  Google Scholar 

  23. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI . Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005; 102: 11070–11075.

    Article  CAS  Google Scholar 

  24. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI . An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444: 1027–1031.

    Article  Google Scholar 

  25. Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity 2010; 18: 190–195.

    Article  Google Scholar 

  26. Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TMS, Comelli EM . Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes 2014; 4: e121.

    Article  CAS  Google Scholar 

  27. Teixeira TFS, Grześkowiak L, Franceschini SCC, Bressan J, Ferreira CLLF, Peluzio MCG . Higher level of faecal SCFA in women correlates with metabolic syndrome risk factors. Br J Nutr 2013; 109: 914–919.

    Article  CAS  Google Scholar 

  28. Murugesan S, Ulloa-Martínez M, Martínez-Rojano H, Galván-Rodríguez FM, Miranda-Brito C, Romano MC et al. Study of the diversity and short-chain fatty acids production by the bacterial community in overweight and obese Mexican children. Eur J Clin Microbiol Infect Dis 2015; 34: 1337–1346.

    Article  CAS  Google Scholar 

  29. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D . Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS One 2009; 4: e7125.

    Article  Google Scholar 

  30. Santacruz A, Collado MC, García-Valdés L, Segura MT, Marítn-Lagos JA, Anjos T et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 2010; 104: 83–92.

    Article  CAS  Google Scholar 

  31. Furet J-, Kong L-, Tap J, Poitou C, Basdevant A, Bouillot J et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 2010; 59: 3049–3057.

    Article  CAS  Google Scholar 

  32. Ainsworth BE, Haskell WL, Leon AS, Jacobs Jr DR, Montoye HJ, Sallis JF et al. Compendium of physical activities: classification of energy costs of human physical activities. Med Sci Sports Exerc 1993; 25: 71–80.

    Article  CAS  Google Scholar 

  33. Pereira MA, FitzerGerald SJ, Gregg EW, Joswiak ML, Ryan WJ, Suminski RR et al. A Collection of Physical Activity Questionnaires for Health-Related Research. Modifiable Activity Questionnaire. Med Sci Sports Exerc 1997; 29 (Suppl), S73–S78.

    Google Scholar 

  34. Rahat-Rozenbloom S, Fernandes J, Gloor GB, Wolever TMS . Evidence for greater production of colonic short-chain fatty acids in overweight than lean humans. Int J Obes 2014; 38: 1525–1531.

    Article  CAS  Google Scholar 

  35. Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome 2013; 1: 3.

    Article  Google Scholar 

  36. Gloor GB, Reid G . Compositional analysis: a valid approach to analyze microbiome high-throughput sequencing data. Can J Microbiol 2016; 62: 692–703.

    Article  CAS  Google Scholar 

  37. Fernandes J, Vogt J, Wolever TMS . Inulin increases short-term markers for colonic fermentation similarly in healthy and hyperinsulinaemic humans. Eur J Clin Nutr 2011; 65: 1279–1286.

    Article  CAS  Google Scholar 

  38. Freeland KR, Wilson C, Wolever TMS . Adaptation of colonic fermentation and glucagon-like peptide-1 secretion with increased wheat fibre intake for 1 year in hyperinsulinaemic human subjects. Br J Nutr 2010; 103: 82–90.

    Article  CAS  Google Scholar 

  39. James SL, Muir JG, Curtis SL, Gibson PR . Dietary fibre: a roughage guide. Intern Med J 2003; 33: 291–296.

    Article  CAS  Google Scholar 

  40. Yang J, Martínez I, Walter J, Keshavarzian A, Rose DJ . Invitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production. Anaerobe 2013; 23: 74–81.

    Article  CAS  Google Scholar 

  41. Bodinham CL, Smith L, Thomas EL, Bell JD, Swann JR, Costabile A et al. Efficacy of increased resistant starch consumption in human type 2 diabetes. Endocr Connect 2014; 3: 75–84.

    Article  CAS  Google Scholar 

  42. Klosterbuer AS, Thomas W, Slavin JL . Resistant starch and pullulan reduce postprandial glucose, insulin, and GLP-1, but have no effect on satiety in healthy humans. J Agric Food Chem 2012; 60: 11928–11934.

    Article  CAS  Google Scholar 

  43. Jenkins DJA, Wolever TMS, Ocana AM, Vuksan V, Cunnane SC, Jenkins M et al. Metabolic effects of reducing rate of glucose ingestion by single bolus versus continuous sipping. Diabetes 1990; 39: 775–781.

    Article  CAS  Google Scholar 

  44. Christensen NJ, Ørskov H, Hansen AP . Significance of glucose load in oral glucose tolerance tests. Acta Med Scand 1972; 192: 337–342.

    Article  CAS  Google Scholar 

  45. Bodinham CL, Al-Mana NM, Smith L, Robertson MD . Endogenous plasma glucagon-like peptide-1 following acute dietary fibre consumption. Br J Nutr 2013; 110: 1429–1433.

    Article  CAS  Google Scholar 

  46. Fernandes J, Vogt J, Wolever TMS . Intravenous acetate elicits a greater free fatty acid rebound in normal than hyperinsulinaemic humans. Eur J Clin Nutr 2012; 66: 1029–1034.

    Article  CAS  Google Scholar 

  47. De Vadder F, Kovatcheva-Datchary P, Goncalves D, Vinera J, Zitoun C, Duchampt A et al. Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits. Cell 2014; 156: 84–96.

    Article  CAS  Google Scholar 

  48. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R et al. Human genetics shape the gut microbiome. Cell 2014; 159: 789–799.

    Article  CAS  Google Scholar 

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Acknowledgements

We are thankful to Kervan Rivera-Rufner for analyzing serum and fecal SCFA. Supported by grant no. 486906 from the Canadian Institutes of Health Research (CIHR), Institute of Nutrition, Metabolism and Diabetes. Clinical Trials registration number (at www.ClinicalTrials.gov): NCT02562014.

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Correspondence to T M S Wolever.

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Rahat-Rozenbloom, S., Fernandes, J., Cheng, J. et al. The acute effects of inulin and resistant starch on postprandial serum short-chain fatty acids and second-meal glycemic response in lean and overweight humans. Eur J Clin Nutr 71, 227–233 (2017). https://doi.org/10.1038/ejcn.2016.248

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