Core body temperature, energy expenditure, and epinephrine during fasting, eucaloric feeding, and overfeeding in healthy adult men: evidence for a ceiling effect for human thermogenic response to diet

Abstract

Background: In homeothermic animals, approximately 50% of daily energy expenditure (EE) is spent to maintain a consistent core body temperature (CBT). In humans, little is known about CBT responses to feeding and overfeeding and their relationship to diet-related changes in EE.

Objective: To study the effects of feeding and overfeeding on CBT and its association with diet-induced thermogenesis (DIT).

Design: Fifty-three healthy men with normal glucose regulation and a wide range of body composition (mean ± SD, body fat: 25 ± 8%, range: 7-43%) had 24-h EE assessed during fasting in a whole-room indirect calorimeter with concomitant CBT measurement by ingestible capsules and 24-h urinary collection for catecholamine measurements. Changes in 24-h EE (DIT) and CBT compared to fasting were assessed during three normal-protein (20%) diets using a cross-over design: one eucaloric diet (EBL, 50% carbohydrate, n = 37) and two overfeeding diets with 200% energy requirements: a high-fat (FNP, 60% fat, n = 25) and a high-carbohydrate (CNP; 75% carbohydrate, n = 24) diet.

Results: The average 24-h CBT (avgCBT) during fasting was 36.81 ± 0.14 °C (inter-individual CV = 0.4%) and positively correlated with 24-h urinary epinephrine (r = 0.61, p < 0.001), but not with body composition measures (p > 0.05). AvgCBT increased during EBL (Δ = 0.06 ± 0.11 °C, p = 0.002), FNP (Δ = 0.13 ± 0.14 °C, p < 0.001), and CNP (Δ = 0.19 ± 0.13 °C, p < 0.001) and associated with increased DIT during EBL (r = 0.43, p = 0.01, β = 31 kcal/day/0.1 °C) and FNP (r = 0.60, p = 0.002, β = 43 kcal/day/0.1 °C), but not CNP (p = 0.47). A ceiling effect for the increase in CBT, but not in DIT, was observed during feeding and, particularly, overfeeding.

Conclusions: CBT increases with feeding and is moderately associated with DIT to a different degree depending on the macronutrient composition of the overfeeding diet. There is a ceiling effect such that individuals with a higher CBT during fasting have limited capacity to increase CBT with feeding. Because of body thermoregulatory mechanisms that maintain a constant CBT, these results indicate that CBT has a limited role in the inter-individual variability in DIT.

Trial registration: ClinicalTrials.gov NCT00523627.

Keywords: Core body temperature; Diet-induced thermogenesis; Fasting, energy balance; Overfeeding.

Copyright © 2019 Elsevier Inc. All rights reserved.

Figures

Figure 1.. Twenty-four-hour time courses of CBT and EE during fasting, eucaloric feeding, and two different overfeeding diets.

Averaged 24-hour time courses of the minute-by-minute trajectory of core body temperature (CBT) (A) and energy expenditure (EE) (B) measured during the four dietary interventions. All the diets have different trajectories for CBT (p

Figure 2.. Determinants of CBT.

The mean 24-h core body temperature (avgCBT) was negatively associated with age (Panel A) but did not correlate with percentage body fat (Panel B). The avgCBT during fasting (FST) was positively correlated with urinary epinephrine, shown in log10-scale on the x-axis (Panel C), but not with urinary norepinephrine (Panel D).

Figure 3.. Ceiling effect of CBT changes during feeding and overfeeding.

The graphs in the first column depict the mean 24-h core body temperature (avgCBT) during fasting (FST) on the x-axis versus the avgCBT during eucaloric feeding (EBL, panel A), high-fat overfeeding (FNP, panel D), and high-carbohydrate overfeeding (CNP, panel G) on the y-axis. In each graph, the solid regression line between avgCBT during fasting and the avgCBT during each diet was statistically compared to the dashed identity line to test the ceiling effect on CBT during eucaloric feeding and overfeeding. The vertical dashed lines represent the upper CBT value during each diet above which CBT did not increase with feeding or overfeeding, which was mathematically calculated as the point where the regression line intersected the identity line. During EBL, the upper CBT limit was 36.99 °C, 36.98 °C during FNP, and was the highest during the CNP diet at 37.13 °C, where there was no increase in CBT despite feeding and overfeeding. To further demonstrate the ceiling effects, the five subjects with the highest avgCBT during 24-h fasting (in red) had smaller changes in CBT from fasting compared to the subjects with the lowest CBT during 24-h FST (in blue) during EBL (panel B), FNP (panel E), and CNP (panel H), despite no differences in the concomitant change in EE during these diets (panels C, F, and I). Analyses between groups (lowest vs. highest mean CBT during 24-h fasting) were carried out using Student’s unpaired t-test.

Figure 4.. Relationships between CBT and 24-h EE with feeding and overfeeding with respect to their fasting values.

Positive relationships between the mean 24-h core body temperature (avgCBT, Panel A) and 24-h energy expenditure (EE, Panel B) during fasting (FST, x-axis) vs. eucaloric feeding (EBL), 200% high-fat (FNP) and high-carbohydrate (CNP) overfeeding. Solid lines represent best-fit lines in each condition. Strong ceiling effects for the diet-related increases from fasting were observed for avgCBT but not for 24-h EE.

Figure 5.. Relationships between changes in CBT, DIT, and urinary epinephrine concentration feeding and overfeeding.

Relationships between the change in mean 24-h core body temperature from fasting (ΔavgCBT) and the diet induced thermogenesis (DIT, graphs in the first column) and the thermic effect of food (TEF, graphs in the middle column) during eucaloric feeding (EBL, Panels A and B), during high-fat overfeeding (FNP, Panels D and E), but not during high-carbohydrate overfeeding (CNP, Panels G and H). Relationships between the change in urinary epinephrine from fasting expressed as fold change on a log10 scale (y-axis) and change in avgCBT during FNP (Panel F) but during eucaloric feeding (Panel C) or high-carbohydrate overfeeding (Panel I). After removal of four volunteers with the highest change in CBT (>0.2°C), the relationship was no longer significant (p=0.28). Diet composition: Eucaloric diet (EBL) with 50% carbohydrate, 30% fat, and 20% protein; high-carbohydrate overfeeding diet (CNP) with 75% carbohydrate, 5% fat, and 20% protein; and high-fat overfeeding diet (FNP) with 20% carbohydrate, 60% fat, and 20% protein. The total energy intake of overfeeding diets was twice the 24-h EE measured during the eucaloric diet (EBL). The DIT was calculated as: 24hEEDiet −24hEEFST; the TEF was calculated by: DITDiet/Energy IntakeDiet ×100.