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Impaired Metabolic Flexibility to High-Fat Overfeeding Predicts Future Weight Gain in Healthy Adults.

ABSTRACT: The ability to switch fuels for oxidation in response to changes in macronutrient composition of diet (metabolic flexibility) may be informative of individuals' susceptibility to weight gain. Seventy-nine healthy, weight-stable participants underwent 24-h assessments of energy expenditure and respiratory quotient (RQ) in a whole-room calorimeter during energy balance (EBL) (50% carbohydrate, 30% fat) and then during 24-h fasting and three 200% overfeeding diets in a crossover design. Metabolic flexibility was defined as the change in 24-h RQ from EBL during fasting and standard overfeeding (STOF) (50% carbohydrate, 30% fat), high-fat overfeeding (HFOF) (60% fat, 20% carbohydrate), and high-carbohydrate overfeeding (HCOF) (75% carbohydrate, 5% fat) diets. Free-living weight change was assessed after 6 and 12 months. Compared with EBL, RQ decreased on average by 9% during fasting and by 4% during HFOF but increased by 4% during STOF and by 8% during HCOF. A smaller decrease in RQ, reflecting a smaller increase in lipid oxidation rate, during HFOF but not during the other diets predicted greater weight gain at both 6 and 12 months. An impaired metabolic flexibility to acute HFOF can identify individuals prone to weight gain, indicating that an individual's capacity to oxidize dietary fat is a metabolic determinant of weight change.

SUBMITTER: Begaye B

PROVIDER: S-EPMC6971489 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Impaired Metabolic Flexibility to High-Fat Overfeeding Predicts Future Weight Gain in Healthy Adults.

Begaye Brittany B Vinales Karyne L KL Hollstein Tim T Ando Takafumi T Walter Mary M Bogardus Clifton C Krakoff Jonathan J Piaggi Paolo P

Diabetes 20191111 2

The ability to switch fuels for oxidation in response to changes in macronutrient composition of diet (metabolic flexibility) may be informative of individuals' susceptibility to weight gain. Seventy-nine healthy, weight-stable participants underwent 24-h assessments of energy expenditure and respiratory quotient (RQ) in a whole-room calorimeter during energy balance (EBL) (50% carbohydrate, 30% fat) and then during 24-h fasting and three 200% overfeeding diets in a crossover design. Metabolic f ...[more]

PMID: 31712321

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Project description:BackgroundGreater increase in 24-h energy expenditure (24EE) during overfeeding and smaller decrease in 24EE during fasting ("spendthrift" metabolic phenotype) are associated with more weight loss during sustained caloric restriction in overweight subjects.ObjectivesThe aim of this study was to investigate whether these acute metabolic responses can also predict weight gain during sustained overfeeding in lean individuals.MethodsSeven lean men participated in this study. Prior to overfeeding, 24EE responses to fasting and 200% normal-protein overfeeding were measured in a whole-room indirect calorimeter. Volunteers underwent 6 wk of 150% low-protein (2%) overfeeding followed by another wk of weight-maintaining diet, during which 24EE was revaluated. Body composition, 24EE, and various hormone concentrations, including fibroblast growth factor 21 (FGF21), were assessed at baseline, at wk 1, 3, and 6 of the overfeeding period, and 1 wk following overfeeding through the use of dual-energy X-ray absorptiometry, indirect calorimetry, and ELISA. Cumulative energy surplus was calculated from 24EE, daily physical activity, and direct measurements of calories of nutrient intake, feces, and urine by bomb calorimetry.ResultsThe average weight gain during 6 wk of low-protein overfeeding was 3.8 kg (6.1%, min: +2.5%, max: +8.0%). During 24-h fasting at baseline, 24EE decreased on average (mean ± SD) by 158 ± 81 kcal/d (P = 0.007). Subjects with less 24EE decrease during fasting (more metabolically spendthrift individuals) gained less weight (r = -0.84, P = 0.03), less fat mass (r = -0.81, P = 0.049), and stored less calories (r = -0.91, P = 0.03) during overfeeding. Following overfeeding, increased 24EE above requirements for achieved body size was associated with less weight and fat mass gain (r = -0.78, P = 0.04) and with the increase in 24EE during 200% normal-protein overfeeding measured at baseline (r = 0.91, P = 0.005). Serum FGF21 concentrations increased up to 44-fold during overfeeding (P < 0.0001).ConclusionsLow-protein overfeeding may be an important tool to identify metabolic phenotypes (spendthrift compared with thrifty) that characterize susceptibility to weight gain. This trial was registered at clinicaltrials.gov as NCT00687115.

Project description:Previous cross-sectional studies showed that immigrants from low-income to high-income countries have higher risk of cardiovascular disease and type 2 diabetes mellitus. We investigated the association between weight gain during the resettlement in South Korea and risk of metabolic syndrome (MetS) among North Korean refugees (NKRs) in this cross-sectional study. In total, 932 NKRs aged 20-80 years in South Korea voluntarily underwent health examination from 2008 to 2017. We compared the risk of MetS and its components between the weight gain group (gained ≥5 kg) and the non-weight gain group (gained <5 kg, maintained or lost body weight) during resettlement in South Korea after defection from North Korea. Multiple logistic regression analysis predicted odds ratio of MetS on the basis of weight change, adjusting for covariates and current body mass index (BMI). We also evaluated the difference in body composition of NKRs between two groups. The prevalence of MetS in the weight gain group was 26%, compared to 10% in the non-weight gain group (p-value < 0.001). The weight gain group had a two-fold higher risk of MetS than the non-weight gain group after adjusting for current BMI (odds ratio 1.875, p-value = 0.045). The prevalence of central obesity, impaired fasting glucose, elevated blood pressure, and hypertriglyceridemia were higher in the weight gain group than the non-weight gain group (36% vs. 12%, p-value < 0.001; 32% vs. 19%, p-value < 0.001; 34 vs. 25%, p-value = 0.008; 19% vs. 13%, p-value = 0.025, respectively). The analysis of body composition showed that the percentage of body fat in the weight gain group was higher than in the non-weight gain group, indicating increased fat mass rather than muscle mass in the weight gain group as their body weight increased during resettlement (33.4 ± 6.53% vs. 28.88 ± 7.40%, p < 0.005). Excess weight gain after defection from North Korea increased the risk of MetS among NKRs in South Korea. It is necessary to monitor weight change among NKRs and their effect on their metabolic health in the long term.

Project description:Because no large prospective study has investigated neural vulnerability factors that predict future weight gain, we tested whether neural response to receipt and anticipated receipt of palatable food and monetary reward predicted body fat gain over a 3-year follow-up in healthy-weight adolescent humans and whether the TaqIA polymorphism moderates these relations. A total of 153 adolescents completed fMRI paradigms assessing response to these events; body fat was assessed annually over follow-up. Elevated orbitofrontal cortex response to cues signaling impending milkshake receipt predicted future body fat gain (r = 0.32), which is a novel finding that provides support for the incentive sensitization theory of obesity. Neural response to receipt and anticipated receipt of monetary reward did not predict body fat gain, which has not been tested previously. Replicating an earlier finding (Stice et al., 2008a), elevated caudate response to milkshake receipt predicted body fat gain for adolescents with a genetic propensity for greater dopamine signaling by virtue of possessing the TaqIA A2/A2 allele, but lower caudate response predicted body fat gain for adolescents with a genetic propensity for less dopamine signaling by virtue of possessing a TaqIA A1 allele, though this interaction was only marginal [p-value <0.05 corrected using voxel-level familywise error rate (pFWE) = 0.06]. Parental obesity, which correlated with TaqIA allele status (odds ratio = 2.7), similarly moderated the relation of caudate response to milkshake receipt to future body fat gain, which is another novel finding. The former interaction implies that too much or too little dopamine signaling and reward region responsivity increases risk for overeating, suggesting qualitatively distinct reward surfeit and reward deficit pathways to obesity.Significance statementBecause no large prospective study has investigated neural vulnerability factors that predict future weight gain we tested whether neural response to receipt and anticipated receipt of palatable food and monetary reward predicted body fat gain over 3-year follow-up in healthy-weight adolescent humans and whether the TaqIA polymorphism moderates these relations. Elevated reward activation in response to food cues predicted future body fat gain. Elevated reward response to food receipt predicted body fat gain for adolescents with a TaqIA A2/A2 allele and lower reward response predicted body fat gain for those with a TaqIA A1 allele. Results imply that too much or too little dopamine signaling and reward region responsivity increases risk for overeating.

Dataset Information

Impaired Metabolic Flexibility to High-Fat Overfeeding Predicts Future Weight Gain in Healthy Adults.

Publications

Impaired Metabolic Flexibility to High-Fat Overfeeding Predicts Future Weight Gain in Healthy Adults.

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