2 & PRIME;-fucosyllactose alone or combined with resistant starch increases circulating short-chain fatty acids in lean men and men with prediabetes and obesity

Emanuel E. Canfora; Lars M. M. Vliex; Taojun Wang; Arjen Nauta; Freek G. Bouwman; Jens J. Holst; Koen Venema; Erwin G. Zoetendal; Ellen E. Blaak

doi:10.3389/fnut.2023.1200645

2 & PRIME;-fucosyllactose alone or combined with resistant starch increases circulating short-chain fatty acids in lean men and men with prediabetes and obesity

Emanuel E. Canfora^*, Lars M. M. Vliex, Taojun Wang, Arjen Nauta, Freek G. Bouwman, Jens J. Holst, Koen Venema, Erwin G. Zoetendal, Ellen E. Blaak

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

BackgroundInfusion of short-chain fatty acids (SCFA) to the distal colon beneficially affects human substrate and energy metabolism. Here, we hypothesized that the combination of 2 & PRIME;-fucosyllactose (2 & PRIME;-FL) with resistant starch (RS) increases distal colonic SCFA production and improves metabolic parameters. MethodsIn this randomized, crossover study, 10 lean (BMI 20-24.9 kg/m(2)) and nine men with prediabetes and overweight/obesity (BMI 25-35 kg/m(2)) were supplemented with either 2 & PRIME;-FL, 2 & PRIME;-FL+RS, or placebo one day before a clinical investigation day (CID). During the CID, blood samples were collected after a overnight fast and after intake of a liquid high-fat mixed meal to determine plasma SCFA (primary outcomes). Secondary outcomes were fasting and postprandial plasma insulin, glucose, free fatty acid (FFA), glucagon-like peptide-1, and peptide YY concentrations. In addition, fecal SCFA and microbiota composition, energy expenditure and substrate oxidation (indirect calorimetry), and breath hydrogen excretion were determined. ResultsIn lean men, supplementation with 2 & PRIME;-FL increased postprandial plasma acetate (P = 0.017) and fasting H-2 excretion (P = 0.041) compared to placebo. Postprandial plasma butyrate concentration increased after 2 & PRIME;-FL and 2 & PRIME;-FL+RS as compared to placebo (P < 0.05) in lean men and men with prediabetes and overweight/obesity. Additionally, 2 & PRIME;-FL+RS decreased fasting and postprandial plasma FFA concentrations compared to placebo (P < 0.05) in lean men. ConclusionSupplementation of 2 & PRIME;-FL with/without RS the day before investigation increased systemic butyrate concentrations in lean men as well as in men with prediabetes and obesity, while acetate only increased in lean men. The combination of 2 & PRIME;-FL with RS showed a putatively beneficial metabolic effect by lowering plasma FFA in lean men, indicating a phenotype-specific effect.

Original language	English
Article number	1200645
Number of pages	13
Journal	Frontiers in nutrition
Volume	10
Issue number	1
DOIs	https://doi.org/10.3389/fnut.2023.1200645
Publication status	Published - 17 Jul 2023

Keywords

short-chain fatty acids
human milk oligosaccharides
obesity
prediabetes
substrate metabolism
LARGE-INTESTINE
GUT MICROBIOTA
DEGRADATION
OXIDATION
TISSUE

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10.3389/fnut.2023.1200645Licence: CC BY

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Canfora, E. E., Vliex, L. M. M., Wang, T., Nauta, A., Bouwman, F. G., Holst, J. J., Venema, K., Zoetendal, E. G., & Blaak, E. E. (2023). 2 & PRIME;-fucosyllactose alone or combined with resistant starch increases circulating short-chain fatty acids in lean men and men with prediabetes and obesity. Frontiers in nutrition, 10(1), Article 1200645. https://doi.org/10.3389/fnut.2023.1200645

@article{fa91662fd0ef475384d2f2d81b1273da,

title = "2 & PRIME;-fucosyllactose alone or combined with resistant starch increases circulating short-chain fatty acids in lean men and men with prediabetes and obesity",

abstract = "BackgroundInfusion of short-chain fatty acids (SCFA) to the distal colon beneficially affects human substrate and energy metabolism. Here, we hypothesized that the combination of 2 & PRIME;-fucosyllactose (2 & PRIME;-FL) with resistant starch (RS) increases distal colonic SCFA production and improves metabolic parameters. MethodsIn this randomized, crossover study, 10 lean (BMI 20-24.9 kg/m(2)) and nine men with prediabetes and overweight/obesity (BMI 25-35 kg/m(2)) were supplemented with either 2 & PRIME;-FL, 2 & PRIME;-FL+RS, or placebo one day before a clinical investigation day (CID). During the CID, blood samples were collected after a overnight fast and after intake of a liquid high-fat mixed meal to determine plasma SCFA (primary outcomes). Secondary outcomes were fasting and postprandial plasma insulin, glucose, free fatty acid (FFA), glucagon-like peptide-1, and peptide YY concentrations. In addition, fecal SCFA and microbiota composition, energy expenditure and substrate oxidation (indirect calorimetry), and breath hydrogen excretion were determined. ResultsIn lean men, supplementation with 2 & PRIME;-FL increased postprandial plasma acetate (P = 0.017) and fasting H-2 excretion (P = 0.041) compared to placebo. Postprandial plasma butyrate concentration increased after 2 & PRIME;-FL and 2 & PRIME;-FL+RS as compared to placebo (P < 0.05) in lean men and men with prediabetes and overweight/obesity. Additionally, 2 & PRIME;-FL+RS decreased fasting and postprandial plasma FFA concentrations compared to placebo (P < 0.05) in lean men. ConclusionSupplementation of 2 & PRIME;-FL with/without RS the day before investigation increased systemic butyrate concentrations in lean men as well as in men with prediabetes and obesity, while acetate only increased in lean men. The combination of 2 & PRIME;-FL with RS showed a putatively beneficial metabolic effect by lowering plasma FFA in lean men, indicating a phenotype-specific effect.",

keywords = "short-chain fatty acids, human milk oligosaccharides, obesity, prediabetes, substrate metabolism, LARGE-INTESTINE, GUT MICROBIOTA, DEGRADATION, OXIDATION, TISSUE",

author = "Canfora, {Emanuel E.} and Vliex, {Lars M. M.} and Taojun Wang and Arjen Nauta and Bouwman, {Freek G.} and Holst, {Jens J.} and Koen Venema and Zoetendal, {Erwin G.} and Blaak, {Ellen E.}",

year = "2023",

month = jul,

day = "17",

doi = "10.3389/fnut.2023.1200645",

language = "English",

volume = "10",

journal = "Frontiers in nutrition",

issn = "2296-861X",

publisher = "Frontiers Media S.A.",

number = "1",

}

TY - JOUR

T1 - 2 & PRIME;-fucosyllactose alone or combined with resistant starch increases circulating short-chain fatty acids in lean men and men with prediabetes and obesity

AU - Canfora, Emanuel E.

AU - Vliex, Lars M. M.

AU - Wang, Taojun

AU - Nauta, Arjen

AU - Bouwman, Freek G.

AU - Holst, Jens J.

AU - Venema, Koen

AU - Zoetendal, Erwin G.

AU - Blaak, Ellen E.

PY - 2023/7/17

Y1 - 2023/7/17

N2 - BackgroundInfusion of short-chain fatty acids (SCFA) to the distal colon beneficially affects human substrate and energy metabolism. Here, we hypothesized that the combination of 2 & PRIME;-fucosyllactose (2 & PRIME;-FL) with resistant starch (RS) increases distal colonic SCFA production and improves metabolic parameters. MethodsIn this randomized, crossover study, 10 lean (BMI 20-24.9 kg/m(2)) and nine men with prediabetes and overweight/obesity (BMI 25-35 kg/m(2)) were supplemented with either 2 & PRIME;-FL, 2 & PRIME;-FL+RS, or placebo one day before a clinical investigation day (CID). During the CID, blood samples were collected after a overnight fast and after intake of a liquid high-fat mixed meal to determine plasma SCFA (primary outcomes). Secondary outcomes were fasting and postprandial plasma insulin, glucose, free fatty acid (FFA), glucagon-like peptide-1, and peptide YY concentrations. In addition, fecal SCFA and microbiota composition, energy expenditure and substrate oxidation (indirect calorimetry), and breath hydrogen excretion were determined. ResultsIn lean men, supplementation with 2 & PRIME;-FL increased postprandial plasma acetate (P = 0.017) and fasting H-2 excretion (P = 0.041) compared to placebo. Postprandial plasma butyrate concentration increased after 2 & PRIME;-FL and 2 & PRIME;-FL+RS as compared to placebo (P < 0.05) in lean men and men with prediabetes and overweight/obesity. Additionally, 2 & PRIME;-FL+RS decreased fasting and postprandial plasma FFA concentrations compared to placebo (P < 0.05) in lean men. ConclusionSupplementation of 2 & PRIME;-FL with/without RS the day before investigation increased systemic butyrate concentrations in lean men as well as in men with prediabetes and obesity, while acetate only increased in lean men. The combination of 2 & PRIME;-FL with RS showed a putatively beneficial metabolic effect by lowering plasma FFA in lean men, indicating a phenotype-specific effect.

AB - BackgroundInfusion of short-chain fatty acids (SCFA) to the distal colon beneficially affects human substrate and energy metabolism. Here, we hypothesized that the combination of 2 & PRIME;-fucosyllactose (2 & PRIME;-FL) with resistant starch (RS) increases distal colonic SCFA production and improves metabolic parameters. MethodsIn this randomized, crossover study, 10 lean (BMI 20-24.9 kg/m(2)) and nine men with prediabetes and overweight/obesity (BMI 25-35 kg/m(2)) were supplemented with either 2 & PRIME;-FL, 2 & PRIME;-FL+RS, or placebo one day before a clinical investigation day (CID). During the CID, blood samples were collected after a overnight fast and after intake of a liquid high-fat mixed meal to determine plasma SCFA (primary outcomes). Secondary outcomes were fasting and postprandial plasma insulin, glucose, free fatty acid (FFA), glucagon-like peptide-1, and peptide YY concentrations. In addition, fecal SCFA and microbiota composition, energy expenditure and substrate oxidation (indirect calorimetry), and breath hydrogen excretion were determined. ResultsIn lean men, supplementation with 2 & PRIME;-FL increased postprandial plasma acetate (P = 0.017) and fasting H-2 excretion (P = 0.041) compared to placebo. Postprandial plasma butyrate concentration increased after 2 & PRIME;-FL and 2 & PRIME;-FL+RS as compared to placebo (P < 0.05) in lean men and men with prediabetes and overweight/obesity. Additionally, 2 & PRIME;-FL+RS decreased fasting and postprandial plasma FFA concentrations compared to placebo (P < 0.05) in lean men. ConclusionSupplementation of 2 & PRIME;-FL with/without RS the day before investigation increased systemic butyrate concentrations in lean men as well as in men with prediabetes and obesity, while acetate only increased in lean men. The combination of 2 & PRIME;-FL with RS showed a putatively beneficial metabolic effect by lowering plasma FFA in lean men, indicating a phenotype-specific effect.

KW - short-chain fatty acids

KW - human milk oligosaccharides

KW - obesity

KW - prediabetes

KW - substrate metabolism

KW - LARGE-INTESTINE

KW - GUT MICROBIOTA

KW - DEGRADATION

KW - OXIDATION

KW - TISSUE

U2 - 10.3389/fnut.2023.1200645

DO - 10.3389/fnut.2023.1200645

M3 - Article

C2 - 37529001

SN - 2296-861X

VL - 10

JO - Frontiers in nutrition

JF - Frontiers in nutrition

IS - 1

M1 - 1200645

ER -