TY - JOUR
T1 - Effects of high-fiber diets enriched with carbohydrate, protein, or unsaturated fat on circulating short chain fatty acids
T2 - Results from the OmniHeart randomized trial
AU - Mueller, Noel T.
AU - Zhang, Mingyu
AU - Juraschek, Stephen P.
AU - Miller, Edgar R.
AU - Appel, Lawrence J.
N1 - Funding Information:
Supported by National Heart, Lung, and Blood Institute of the NIHgrants K01HL141589 (to NTM) and K23HL135273 (to SPJ). Supplemental Figure 1 and Supplemental Tables 1–3 are available from the “Supplementary data” link in the online posting of the article and from the same link in the online table of contents at https://academic.oup.com/ajcn/. Data described in the article, code book, and analytic code will be made available upon request pending application and approval. Address correspondence to NTM (e-mail: noeltmueller@jhu.edu). Abbreviations used: Carb diet, carbohydrate-rich diet; DBP, diastolic blood pressure; GEE, generalized estimating equation; OmniHeart, Optimal Macronutrient Intake Trial to Prevent Heart Disease; Prot diet, protein-rich diet; SBP, systolic blood pressure; SCFA, short-chain fatty acids; Unsat diet, unsaturated fat–rich diet. Received August 28, 2019. Accepted for publication December 3, 2019. First published online January 11, 2020; doi: https://doi.org/10.1093/ ajcn/nqz322.
Publisher Copyright:
Copyright © 2020 The Author(s).
PY - 2020/3/1
Y1 - 2020/3/1
N2 - Background: Short chain fatty acids (SCFAs; e.g., acetate, propionate, and butyrate) are produced by microbial fermentation of fiber in the colon. Evidence is lacking on how high-fiber diets that differ in macronutrient composition affect circulating SCFAs. Objectives: We aimed to compare the effects of 3 high-fiber isocaloric diets differing in %kcal of carbohydrate, protein, or unsaturated fat on circulating SCFAs. Based on previous literature, we hypothesized that serum acetate, the main SCFA in circulation, increases on all high-fiber diets, but differently by macronutrient composition of the diet. Methods: OmniHeart is a randomized crossover trial of 164 men and women (≥30 y old); 163 participants with SCFA data were included in this analysis. We provided participants 3 isocaloric high-fiber (∼30 g/2100 kcal) diets, each for 6 wk, in random order: a carbohydrate-rich (Carb) diet, a protein-rich (Prot) diet (protein predominantly from plant sources), and an unsaturated fat-rich (Unsat) diet. We used LC-MS to quantify SCFA concentrations in fasting serum, collected at baseline and the end of each diet period. We fitted linear regression models with generalized estimating equations to examine change in ln-transformed SCFAs from baseline to the end of each diet; differences between diets; and associations of changes in SCFAs with cardiometabolic parameters. Results: From baseline, serum acetate concentrations were increased by the Prot (β: 0.24; 95% CI: 0.12, 0.35), Unsat (β: 0.21; 95% CI: 0.10, 0.33), and Carb (β: 0.12; 95% CI: 0.01, 0.24) diets; between diets, only Prot compared with Carb was significant (P = 0.02). Propionate was decreased by the Carb (β:-0.10; 95% CI:-0.16,-0.03) and Unsat (β:-0.10; 95% CI:-0.16,-0.04) diets, not the Prot diet; between diet comparisons of Carb vs. Prot (P = 0.006) and Unsat vs. Prot (P = 0.002) were significant. The Prot diet increased butyrate (β: 0.05; 95% CI: 0.00, 0.09) compared with baseline, but not compared with the other diets. Increases in acetate were associated with decreases in insulin and glucose; increases in propionate with increases in leptin, LDL cholesterol, and blood pressure; and increases in butyrate with increases in insulin and glucose, and decreases in HDL cholesterol and ghrelin (Ps < 0.05). Conclusions: Macronutrient composition of high-fiber diets affects circulating SCFAs, which are associated with measures of appetite and cardiometabolic health. This trial was registered at clinicaltrials.gov as NCT00051350.
AB - Background: Short chain fatty acids (SCFAs; e.g., acetate, propionate, and butyrate) are produced by microbial fermentation of fiber in the colon. Evidence is lacking on how high-fiber diets that differ in macronutrient composition affect circulating SCFAs. Objectives: We aimed to compare the effects of 3 high-fiber isocaloric diets differing in %kcal of carbohydrate, protein, or unsaturated fat on circulating SCFAs. Based on previous literature, we hypothesized that serum acetate, the main SCFA in circulation, increases on all high-fiber diets, but differently by macronutrient composition of the diet. Methods: OmniHeart is a randomized crossover trial of 164 men and women (≥30 y old); 163 participants with SCFA data were included in this analysis. We provided participants 3 isocaloric high-fiber (∼30 g/2100 kcal) diets, each for 6 wk, in random order: a carbohydrate-rich (Carb) diet, a protein-rich (Prot) diet (protein predominantly from plant sources), and an unsaturated fat-rich (Unsat) diet. We used LC-MS to quantify SCFA concentrations in fasting serum, collected at baseline and the end of each diet period. We fitted linear regression models with generalized estimating equations to examine change in ln-transformed SCFAs from baseline to the end of each diet; differences between diets; and associations of changes in SCFAs with cardiometabolic parameters. Results: From baseline, serum acetate concentrations were increased by the Prot (β: 0.24; 95% CI: 0.12, 0.35), Unsat (β: 0.21; 95% CI: 0.10, 0.33), and Carb (β: 0.12; 95% CI: 0.01, 0.24) diets; between diets, only Prot compared with Carb was significant (P = 0.02). Propionate was decreased by the Carb (β:-0.10; 95% CI:-0.16,-0.03) and Unsat (β:-0.10; 95% CI:-0.16,-0.04) diets, not the Prot diet; between diet comparisons of Carb vs. Prot (P = 0.006) and Unsat vs. Prot (P = 0.002) were significant. The Prot diet increased butyrate (β: 0.05; 95% CI: 0.00, 0.09) compared with baseline, but not compared with the other diets. Increases in acetate were associated with decreases in insulin and glucose; increases in propionate with increases in leptin, LDL cholesterol, and blood pressure; and increases in butyrate with increases in insulin and glucose, and decreases in HDL cholesterol and ghrelin (Ps < 0.05). Conclusions: Macronutrient composition of high-fiber diets affects circulating SCFAs, which are associated with measures of appetite and cardiometabolic health. This trial was registered at clinicaltrials.gov as NCT00051350.
KW - acetate
KW - butyrate
KW - diet
KW - fiber
KW - macronutrient
KW - microbiome
KW - propionate
KW - protein
KW - short-chain fatty acids
KW - unsaturated fat
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U2 - 10.1093/ajcn/nqz322
DO - 10.1093/ajcn/nqz322
M3 - Article
C2 - 31927581
AN - SCOPUS:85081073669
SN - 0002-9165
VL - 111
SP - 545
EP - 554
JO - American Journal of Clinical Nutrition
JF - American Journal of Clinical Nutrition
IS - 3
ER -