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Timing of unsaturated fat intake improves insulin sensitivity through gut microbiota-dependent regulation of bile acid metabolism: a randomized controlled trial

ABSTRACT:

The timing of dietary fat intake influences metabolic health. However, the impact of the timing of unsaturated fat (USFA) intake on glycemic control has yet to be explored. This 12-week, double-blind, randomized, controlled, 2 x 2 factorial-designed feeding trial investigated the effects of timing (lunch or dinner) and types of dietary USFA (high monounsaturated fat or polyunsaturated fat diet) intake on glucose metabolism in seventy prediabetes participants (mean age, 57 years, fasting glucose (100-126 mg/dL) or postprandial glucose (140-199 mg/dL)). Sixty participants with completed fecal samples were included in the final analysis (n=15 for each group). Postprandial serum glucose (first primary outcome) and insulin (co-primary outcomes) levels from an oral glucose tolerance test were detected. Insulin sensitivity indices (co-primary outcomes) were calculated. Secondary outcomes were continuous glucose levels, serum fatty acid profile, gut microbiome (metagenomic sequencing) and fecal metabolites. Results showed no significant differences in postprandial glucose between groups. However, USFA intake at lunch (vs dinner) improved insulin sensitivity and reduced postprandial insulin and serum free saturated fatty acid (Ptiming < 0.05, Ptype > 0.05, Pinteraction > 0.05), which was associated with alterations in gut microbiome and bile acid metabolism, regardless of USFA type. Here we show, advancing timing of USFA intake improves insulin sensitivity through the gut microbiome and bile acid metabolism, while the type of USFA does not. A limitation is that sample size calculation and power were based on postprandial glucose changes, whereas other co-primary outcomes were not considered. However, the type I error was controlled (α/4) in their analysis. Trial registration: ChiCTR2100045645.

INSTRUMENT(S): Liquid Chromatography MS - alternating - hilic, Liquid Chromatography MS - alternating - reverse phase, Gas Chromatography MS - positive

PROVIDER: MTBLS12353 | MetaboLights | 2025-04-14

REPOSITORIES: MetaboLights

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			Action	DRS
	MWY-22-1688_120_WH6500-19_T500-Amide-02_V1.0_TY_20221010-MWY221688_R1.mzML	Mzml
	MWY-22-1688_120_WH6500-19_T500-Amide-02_V1.0_TY_20221010-MWY221688_R2.mzML	Mzml
	MWY-22-1688_120_WH6500-19_T500-Amide-02_V1.0_TY_20221010-MWY221688_R3.mzML	Mzml
	MWY-22-1688_120_WH6500-19_T500-Amide-02_V1.0_TY_20221010-T21258303a.mzML	Mzml
	MWY-22-1688_120_WH6500-19_T500-Amide-02_V1.0_TY_20221010-T21258304a.mzML	Mzml

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Project description:The obese, insulin resistant state is characterized by impairments in lipid metabolism. Dietary polyphenols might improve these deteriorations. We have previously shown that 3-days supplementation of combined Epigallocatechin-gallate and Resveratrol (E+R) increased energy expenditure, which was accompanied by improved metabolic flexibility after a high-fat mixed-meal (HFMM) in men. The present study aimed to investigate whether these short-term effects translate into longer-term improvement of insulin sensitivity and lipid metabolism. In this randomized, double-blind study, 42 overweight subjects (21 male, 38Â±2 yrs, BMI 29.7Â±0.5 kg/m2, HOMA-IR 2.1Â±0.2) received either E+R (300 and 80 mg/d, respectively) or placebo (PLA) for 12 weeks (3 months). Before (t0) and after (t3) intervention, tissue-specific insulin sensitivity was assessed by a hyperinsulinemic-euglycemic clamp with stable isotope infusion. Fasting and postprandial (HFMM) lipid metabolism was assessed using indirect calorimetry and blood sampling. Adipose tissue and skeletal muscle lipolysis was measured using microdialysis in men and skeletal muscle biopsies were collected to assess mitochondrial function and gene expression alterations via microarray analysis. E+R supplementation increased fasting (P=0.06) and postprandial (P=0.03) fat oxidation but did not alter energy expenditure compared to PLA. This was accompanied by an E+R-induced increase in oxidative capacity in permeabilized muscle fibers (p<0.05). Moreover, E+R supplementation attenuated the increase in plasma triacylglycerol concentration that was observed in the PLA group (AUC, p<0.05), and tended to decrease visceral fat mass (P=0.09). Finally, insulin-stimulated glucose disposal and suppression of endogenous glucose production were not affected by E+R supplementation. 12 weeks E+R supplementation increased whole-body fat oxidation and skeletal muscle oxidative capacity, but this did not translate into increased tissue-specific insulin sensitivity in overweight and obese subjects. To identify pathways that may underlie the E+R-induced improvement of skeletal muscle mitochondrial capacity, we performed microarray analysis on skeletal muscle biopsies (vastus lateralis muscle), collected before and after 12-weeks E+R or PLA treatment. Gene Set Enrichment Analysis (GSEA) indicated that the most upregulated pathways after E+R supplementation were related to the citric acid cycle and respiratory electron transport chain, while pathways related to carbohydrate metabolism were upregulated in the PLA group. In this randomized, double-blind placebo-controlled, parallel intervention trial, subjects received either a combination of E+R supplements (INTV, 282 mg/d and 80 mg/d, respectively) or placebo (PLA, partly hydrolyzed microcrystalline cellulose-filled capsules) for a period of 12 weeks (3 months) to assess effects of E+R supplementation on tissue-specific insulin sensitivity (primary outcomes) and fasting and postprandial substrate metabolism (secondary outcomes). Skeletal muscle (m. vastus lateralis) biopsies were taken under local anesthesia during fasting conditions before (t0) and after the 12-weeks (t3) intervention period. Extraxted RNA was hybridized on HTA 2.0 Affymetrix arrays and microarray analysis was performed on paired sample sets for 27 subjects (p, PLA n = 14; E+R n = 13).

Project description:The obese, insulin resistant state is characterized by impairments in lipid metabolism. Dietary polyphenols might improve these deteriorations. We have previously shown that 3-days supplementation of combined Epigallocatechin-gallate and Resveratrol (E+R) increased energy expenditure, which was accompanied by improved metabolic flexibility after a high-fat mixed-meal (HFMM) in men. The present study aimed to investigate whether these short-term effects translate into longer-term improvement of insulin sensitivity and lipid metabolism. In this randomized, double-blind study, 42 overweight subjects (21 male, 38±2 yrs, BMI 29.7±0.5 kg/m2, HOMA-IR 2.1±0.2) received either E+R (300 and 80 mg/d, respectively) or placebo (PLA) for 12 weeks (3 months). Before (t0) and after (t3) intervention, tissue-specific insulin sensitivity was assessed by a hyperinsulinemic-euglycemic clamp with stable isotope infusion. Fasting and postprandial (HFMM) lipid metabolism was assessed using indirect calorimetry and blood sampling. Adipose tissue and skeletal muscle lipolysis was measured using microdialysis in men and skeletal muscle biopsies were collected to assess mitochondrial function and gene expression alterations via microarray analysis. E+R supplementation increased fasting (P=0.06) and postprandial (P=0.03) fat oxidation but did not alter energy expenditure compared to PLA. This was accompanied by an E+R-induced increase in oxidative capacity in permeabilized muscle fibers (p<0.05). Moreover, E+R supplementation attenuated the increase in plasma triacylglycerol concentration that was observed in the PLA group (AUC, p<0.05), and tended to decrease visceral fat mass (P=0.09). Finally, insulin-stimulated glucose disposal and suppression of endogenous glucose production were not affected by E+R supplementation. 12 weeks E+R supplementation increased whole-body fat oxidation and skeletal muscle oxidative capacity, but this did not translate into increased tissue-specific insulin sensitivity in overweight and obese subjects. To identify pathways that may underlie the E+R-induced improvement of skeletal muscle mitochondrial capacity, we performed microarray analysis on skeletal muscle biopsies (vastus lateralis muscle), collected before and after 12-weeks E+R or PLA treatment. Gene Set Enrichment Analysis (GSEA) indicated that the most upregulated pathways after E+R supplementation were related to the citric acid cycle and respiratory electron transport chain, while pathways related to carbohydrate metabolism were upregulated in the PLA group.

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Timing of unsaturated fat intake improves insulin sensitivity through gut microbiota-dependent regulation of bile acid metabolism: a randomized controlled trial

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