Diurnal variations of brown fat thermogenesis and fat oxidation in humans

Mami Matsushita,Masayuki Saito,Hitoshi Wakabayashi,Sang-Il Lee,Shinsuke Nirengi,Naoki Sakane,Masayuki Domichi,Masanobu Hibi

doi:10.1038/s41366-021-00927-x

Mami Matsushita, Masayuki Saito + Show 6 more

Open Access

https://doi.org/10.1038/s41366-021-00927-x

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Abstract

Background/objectivesDisturbed circadian rhythm is associated with an increased risk of obesity and metabolic disorders. Brown adipose tissue (BAT) is a site of nonshivering thermogenesis (NST) and plays a role in regulating whole-body energy expenditure (EE), substrate metabolism, and body fatness. In this study, we examined diurnal variations of NST in healthy humans by focusing on their relation to BAT activity.MethodsForty-four healthy men underwent 18F-fluoro-2-deoxy-D-glucose positron emission tomography and were divided into Low-BAT and High-BAT groups. In STUDY 1, EE, diet-induced thermogenesis (DIT), and fat oxidation (FO) were measured using a whole-room indirect calorimeter at 27 °C. In STUDY 2, EE, FO, and skin temperature in the region close to BAT depots (Tscv) and in the control region (Tc) were measured at 27 °C and after 90 min cold exposure at 19 °C in the morning and in the evening.ResultsIn STUDY 1, DIT and FO after breakfast was higher in the High-BAT group than in the Low-BAT group (P < 0.05), whereas those after dinner were comparable in the two groups. FO in the High-BAT group was higher after breakfast than after dinner (P < 0.01). In STUDY 2, cold-induced increases in EE (CIT), FO, and Tscv relative to Tc in the morning were higher in the High-BAT group than in the Low-BAT group (P < 0.05), whereas those after dinner were comparable in the two groups. CIT in the High-BAT group tended to be higher in the morning than in the evening (P = 0.056).ConclusionBAT-associated NST and FO were evident in the morning, but not in the evening, suggesting that the activity of human BAT is higher in the morning than in the evening, and thus may be involved in the association of an eating habit of breakfast skipping with obesity and related metabolic disorders.

Highlights

Whole-body energy expenditure (EE) exhibits diurnal variations, depending largely on the effects of physical activity and food intake
When comparing of the High-Brown adipose tissue (BAT) group with the Low-BAT group, there was no significant difference between the groups in total EE (TEE), SMR, TEE/fat-free mass (FFM), and physical activity levels
We previously measured EE for 24 h with a whole-room indirect calorimeter and found that diet-induced/postprandial thermogenesis (DIT) and fat oxidation are higher in subjects with metabolically active BAT than in those without it, suggesting a significant contribution of BAT to DIT in humans [21]

Summary

Introduction

Whole-body energy expenditure (EE) exhibits diurnal variations, depending largely on the effects of physical activity and food intake. There have been reports that the thermic effect of food intake, the so-called diet-induced/postprandial thermogenesis (DIT), is higher in the morning than in the evening and at night [1,2,3,4,5,6] This may explain the apparent association of meal timing with obesity and related metabolic disorders: for example, habits of breakfast skipping and night eating may lead to increased body fat accumulation probably because of decreased DIT and daily EE [7,8,9,10,11]. The activation of BAT after meal intake is directly confirmed by PET/CT using [15O]O2, [15O]H2O and [18F]fluoro-thiaheptadecanoic acid radiotracers [22] This leads us to hypothesize that BAT may be involved in the diurnal variations of DIT. In a Received: 3 March 2021 Revised: 9 July 2021 Accepted: 23 July 2021 Published online: 2 August 2021

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