TY - JOUR

T1 - Fiber mixture-specific effect on distal colonic fermentation and metabolic health in lean but not in prediabetic men

AU - Canfora, Emanuel E.

AU - Hermes, Gerben D.A.

AU - Müller, Mattea

AU - Bastings, Jacco

AU - Vaughan, Elaine E.

AU - van Den Berg, Marco A.

AU - Holst, Jens J.

AU - Venema, Koen

AU - Zoetendal, Erwin G.

AU - Blaak, Ellen E.

N1 - Funding Information: TResearch of this work was performed in the public–private partnership ‘CarboKinetics’ coordinated by the Carbohydrate Competence Center (CCC, https://www.cccresearch.nl ). CarboKinetics is financed by participating industrial partners Agrifirm Innovation Center B.V., Cooperatie AVEBE U.A., DSM Food Specialties B.V., FrieslandCampina Netherlands B.V., Nutrition Sciences N.V., Sensus B.V., and VanDrie Holding N.V. allowances of The Netherlands Organisation for Scientific Research (NWO).

PY - 2022

Y1 - 2022

N2 - Infusions of the short-chain fatty acid (SCFA) acetate in the distal colon improved metabolic parameters in men. Here, we hypothesized that combining rapidly and slowly fermentable fibers will enhance distal colonic acetate production and improve metabolic health. In vitro cultivation studies in a validated model of the colon were used to identify fiber mixtures that yielded high distal colonic acetate production. Subsequently, in two randomized crossover studies, lean and prediabetic overweight/obese men were included. In one study, participants received supplements of either long-chain inulin+resistant starch (INU+RS), INU or maltodextrin (PLA) the day prior to a clinical investigation day (CID). The second trial studied beta glucan+RS (BG+RS) versus BG and PLA. During each CID, breath hydrogen, indirect calorimetry, plasma metabolites/hormones were assessed during fasting and postprandial conditions. Additionally, fecal microbiota composition and SCFA were determined. In prediabetic men, INU+RS increased plasma acetate compared to INU or PLA (P < .05), but did not affect metabolic parameters. In lean men, INU+RS increased breath hydrogen and fasting plasma butyrate, which was accompanied by increased energy expenditure, carbohydrate oxidation and PYY and decreased postprandial glucose concentrations (all P < .05) compared to PLA. BG+RS increased plasma butyrate compared to PLA (P < .05) in prediabetic individuals, but did not affect other fermentation/metabolic markers in both phenotypes. Fiber-induced shifts in fecal microbiota were individual-specific and more pronounced with INU+RS versus BG+RS. Administration of INU+RS (not BG+RS) the day prior to investigation improved metabolic parameters in lean but not in prediabetic individuals, demonstrating that effects were phenotype- and fiber-specific. Further research should study whether longer-term supplementation periods are required to elicit beneficial metabolic health in prediabetic individuals. Trial registration numbers: Clinical trial No. NCT03711383 (Inulin study) and Clinical trial No. NCT03714646 (Beta glucan study).

AB - Infusions of the short-chain fatty acid (SCFA) acetate in the distal colon improved metabolic parameters in men. Here, we hypothesized that combining rapidly and slowly fermentable fibers will enhance distal colonic acetate production and improve metabolic health. In vitro cultivation studies in a validated model of the colon were used to identify fiber mixtures that yielded high distal colonic acetate production. Subsequently, in two randomized crossover studies, lean and prediabetic overweight/obese men were included. In one study, participants received supplements of either long-chain inulin+resistant starch (INU+RS), INU or maltodextrin (PLA) the day prior to a clinical investigation day (CID). The second trial studied beta glucan+RS (BG+RS) versus BG and PLA. During each CID, breath hydrogen, indirect calorimetry, plasma metabolites/hormones were assessed during fasting and postprandial conditions. Additionally, fecal microbiota composition and SCFA were determined. In prediabetic men, INU+RS increased plasma acetate compared to INU or PLA (P < .05), but did not affect metabolic parameters. In lean men, INU+RS increased breath hydrogen and fasting plasma butyrate, which was accompanied by increased energy expenditure, carbohydrate oxidation and PYY and decreased postprandial glucose concentrations (all P < .05) compared to PLA. BG+RS increased plasma butyrate compared to PLA (P < .05) in prediabetic individuals, but did not affect other fermentation/metabolic markers in both phenotypes. Fiber-induced shifts in fecal microbiota were individual-specific and more pronounced with INU+RS versus BG+RS. Administration of INU+RS (not BG+RS) the day prior to investigation improved metabolic parameters in lean but not in prediabetic individuals, demonstrating that effects were phenotype- and fiber-specific. Further research should study whether longer-term supplementation periods are required to elicit beneficial metabolic health in prediabetic individuals. Trial registration numbers: Clinical trial No. NCT03711383 (Inulin study) and Clinical trial No. NCT03714646 (Beta glucan study).

KW - dietary fibers

KW - gut microbiota

KW - Short-chain fatty acids

KW - substrate metabolism

UR - http://www.scopus.com/inward/record.url?scp=85121623144&partnerID=8YFLogxK

U2 - 10.1080/19490976.2021.2009297

DO - 10.1080/19490976.2021.2009297

M3 - Article

C2 - 34923911

AN - SCOPUS:85121623144

VL - 14

JO - Gut microbes

JF - Gut microbes

SN - 1949-0976

IS - 1

M1 - 2009297

ER -