Adults with metabolically healthy overweight or obesity present more brown adipose tissue and higher thermogenesis than their metabolically unhealthy counterparts

Abstract

Background: There is a subset of individuals with overweight/obesity characterized by a lower risk of cardiometabolic complications, the so-called metabolically healthy overweight/obesity (MHOO) phenotype. Despite the relatively higher levels of subcutaneous adipose tissue and lower visceral adipose tissue observed in individuals with MHOO than individuals with metabolically unhealthy overweight/obesity (MUOO), little is known about the differences in brown adipose tissue (BAT).

Methods: This study included 53 young adults (28 women) with a body mass index (BMI) ≥25 kg/m² which were classified as MHOO (n = 34) or MUOO (n = 19). BAT was assessed through a static ¹⁸F-FDG positron emission tomography/computed tomography scan after a 2-h personalized cooling protocol. Energy expenditure, skin temperature, and thermal perception were assessed during a standardized mixed meal test (3.5 h) and a 1-h personalized cold exposure. Body composition was assessed by dual-energy x-ray absorptiometry, energy intake was determined during an ad libitum meal test and dietary recalls, and physical activity levels were determined by a wrist-worn accelerometer.

Findings: Participants with MHOO presented higher BAT volume (+124%, P = 0.008), SUVmean (+63%, P = 0.001), and SUVpeak (+133%, P = 0.003) than MUOO, despite having similar BAT mean radiodensity (P = 0.354). In addition, individuals with MHOO exhibited marginally higher meal-induced thermogenesis (P = 0.096) and cold-induced thermogenesis (+158%, P = 0.050). Moreover, MHOO participants showed higher supraclavicular skin temperature than MUOO during the first hour of the postprandial period and during the cold exposure, while no statistically significant differences were observed in other skin temperature parameters. We observed no statistically significant differences between MHOO and MUOO in thermal perception, body composition, outdoor ambient temperature exposure, resting metabolic rate, energy intake, or physical activity levels.

Interpretation: Adults with MHOO present higher BAT volume and activity than MUOO. The higher meal- and cold-induced thermogenesis and cold-induced supraclavicular skin temperature are compatible with a higher BAT activity. Overall, these results suggest that BAT presence and activity might be linked to a healthier phenotype in young adults with overweight or obesity.

Funding: See acknowledgments section.

Keywords: Adaptive thermogenesis; Brown fat; Cardiometabolic health; Metabolism; Thermoregulation.

Fig. 1

Images of two representative individuals, one with metabolically healthyandobesity (MHO) and another one with metabolically unhealthy and obesity (MUO). Blue dots indicate brown adipose tissue volume and red dots indicate maximal brown adipose tissue activity (maximal standardized uptake value).

Fig. 2

Differences between adults with metabolically healthy overweight/obesity (MHOO) and metabolically unhealthy overweight/obesity (MUOO) in brown adipose tissue volume,¹⁸F-FDG uptake and mean radiodensity after a personalized cold exposure. a) BAT volume; b) BAT mean radiodensity (MHOO, n = 27; MUOO, n = 9); c) BAT SUVmean; and d) BAT SUVpeak. SUV values are shown relative to lean mass. Data represent mean and 95% confidence interval. P values obtained from analysis of covariance adjusting for sex. Abbreviations: BAT: brown adipose tissue; HU: Hounsfield Unit; SUV: Standardized uptake value.

Fig. 3

Differences between adults with metabolically healthy overweight/obesity (MHOO) and metabolically unhealthy overweight/obesity (MUOO) in the temperature of the water irrigating the cooling vest before the brown adipose tissue assessment (a), thermal perception during the previous month (b), thermal perception during the warm period before the personalized cold exposure before the PET-CT scan (c; MHOO, n = 19 and MUOO, n = 13), and thermal perception during the cold period of the personalized cold exposure before the PET-CT scan (d; MHOO, n = 28 and MUOO, n = 15). Panels b, c, and d, the greater the value the greater the cold perception. Data represent mean and 95% confidence interval. P values obtained from analysis of covariance adjusting for sex.

Fig. 4

Differences between adults with metabolically healthy overweight/obesity (MHOO) and metabolically unhealthy overweight/obesity (MUOO) in meal- (a, b) and cold-induced thermogenesis (c, d). Data represent mean and 95% confidence interval. Panels a and c: P values for time, group, and Time × Group interaction effects obtained from two-way repeated-measures analysis of covariance (ANCOVA) adjusting for sex (Huynh-Feldt correction). Timepoint 0 represents the resting metabolic rate value. Panels b and d: P values obtained from analysis of covariance adjusting for sex. Abbreviations: EE: Energy expenditure; EI: Energy intake; min: minutes; RMR: Resting metabolic rate.

Fig. 5

Differences between adults with metabolically healthy overweight/obesity (MHOO) and metabolically unhealthy overweight/obesity (MUOO) in meal- (a, c, e, g, i) and cold-induced (b, d, f, h, j) changes in mean, proximal, distal, peripheral gradient, and supraclavicular skin temperatures. In meal-induced changes in temperature (a, c, e, g, i), negative values in the X axes represent the resting metabolic rate period, whereas in cold changes in temperature (b, d, f, h, j) represent the warm room period. Data represent mean and 95% confidence interval. In meal-induced changes (a, c, e, g, i), time point 0 represents the start of the meal intake, whereas in cold-induced changes (b, d, f, h, j) represents the start of the cold exposure. P values for time, group, and Time × Group interaction effects obtained from a two-way repeated-measures analysis of covariance (ANCOVA) adjusting for sex (Huynh-Feldt correction).