Extent and determinants of thermogenic responses to 24 hours of fasting, energy balance, and five different overfeeding diets in humans

Abstract

Context: Individual variation in the ability to convert excess calories to heat and the effects of dietary macronutrient composition are unclear.

Objective: Stability and determinants of the energy expenditure (EE) response to overconsumption were assessed.

Design, setting, and participants: Twenty subjects (75% male) with normal glucose regulation were evaluated during 24 hours each of energy balance, fasting, and 5 different diets with 200% energy requirements in a clinical research unit.

Interventions: Five 1-day overfeeding diets were given in random order: high carbohydrate (75%) and low protein (3%); high carbohydrate and normal protein (20%); high fat (46%) and low protein; high fat (60%) and normal protein; and balanced (50% carbohydrates, 20% protein).

Main outcome measures: The 24-hour EE, sleeping EE, and thermic effect of food (TEF) during each diet were measured with a metabolic chamber. Appetitive hormones were measured before and after the diets.

Results: The EE response to overfeeding exhibited good intraindividual reproducibility. Similar increases above eucaloric feeding in 24-hour EE (mean 10.7 ± 5.7%, P < .001; range 2.9-18.8%) and sleeping EE (14.4 ± 11.3%, P < .001; range 1.0-45.1%) occurred when overfeeding diets containing 20% protein, despite differences in fat and carbohydrate content, but the EE response during overfeeding diets containing 3% protein was attenuated. The percent body fat negatively correlated with TEF during normal protein overfeeding (r = -0.53, P < .01). Fasting peptide YY negatively correlated with TEF (r = -0.56, P < .01) and the increase in sleeping EE (r = -0.54, P < .01) during overfeeding.

Conclusions: There is an intrinsic EE response to overfeeding that negatively associates with adiposity, although it represents a small percentage of consumed calories.

Trial registration: ClinicalTrials.gov NCT00523627.

Figures

Figure 1.

EE per minute over 23.25 hours during all dietary interventions and compared with eucaloric feeding (shown in purple on every graph). The EE per minute during overfeeding is shown with the balanced overfeeding diet (BOF) (n = 20) with 50% carbohydrates (C), 30% fat (F), and 20% protein (P) in dark blue in (panel A); with the high carbohydrate, normal-protein diet (CNP) (n = 20) with 75% C, 5% F, 20% P in light blue (panel B); with the high-fat, normal-protein diet (FNP) (n = 19) with 20% C, 60% F, 20% P in blue (panel C); with the high-carbohydrate, low-protein diet (CLP) (n = 20) with 75% C, 22% F, 3% P in green (panel D); and with the low-protein diet (LPF) (n = 20) with 51% C, 46% F, 3% P in light green (panel E). The EE per minute during fasting (FST) (n = 20) is shown in red (panel F). The 0:00 time period indicates entry into the respiratory chamber (1 hour after consuming breakfast); lunch was given at the 3-hour mark, dinner at the 8-hour mark, and snack at the 11-hour mark. Participants were asked to be in bed from the 15-hour mark to at least the 21-hour mark in the chamber and to limit unnecessary activity throughout the 24-hour period. The trajectories were significantly different from eucaloric feeding (P < .001) during fasting and overfeeding with the BOF, CNP, and FNP diets.

Figure 2.

Relationship between DIT and dietary intake. DIT was calculated as the difference between the 24h-EE during each feeding intervention and the fasting assessment [n = 20 individuals represented 6 times each (1 individual is represented only 5 times)]. Solid squares indicate feeding during energy balance and open squares indicate normal protein overfeeding. Solid diamonds indicate low-protein overfeeding. The gray line indicates the expected dose-response curve, assuming a strictly linear relationship, between DIT and intake based on feeding studies from D'Alessio et al. (7).

Figure 3.

Correlation between mean thermic effect of food (TEF%) (Pearson r = −0.56, P < .01) (A) and percent change in sleeping EE (r = −0.54, P < .01) (B) during normal protein overfeeding (mean from 3 normal protein overfeeding diets) and mean fasting PYY in the 20 participants. PYY was drawn prior to beginning the overfeeding diets.