Outdoor Temperature Influences Cold Induced Thermogenesis in Humans

Jaël R Senn, Claudia I Maushart, Gani Gashi, Regina Michel, Murielle Lalive d'Epinay, Roland Vogt, Anton S Becker, Julian Müller, Miroslav Baláz, Christian Wolfrum, Irene A Burger, Matthias J Betz, Jaël R Senn, Claudia I Maushart, Gani Gashi, Regina Michel, Murielle Lalive d'Epinay, Roland Vogt, Anton S Becker, Julian Müller, Miroslav Baláz, Christian Wolfrum, Irene A Burger, Matthias J Betz

Abstract

Objective: Energy expenditure (EE) increases in response to cold exposure, which is called cold induced thermogenesis (CIT). Brown adipose tissue (BAT) has been shown to contribute significantly to CIT in human adults. BAT activity and CIT are acutely influenced by ambient temperature. In the present study, we investigated the long-term effect of seasonal temperature variation on human CIT. Materials and Methods: We measured CIT in 56 healthy volunteers by indirect calorimetry. CIT was determined as difference between EE during warm conditions (EEwarm) and after a defined cold stimulus (EEcold). We recorded skin temperatures at eleven anatomically predefined locations, including the supraclavicular region, which is adjacent to the main human BAT depot. We analyzed the relation of EE, CIT and skin temperatures to the daily minimum, maximum and mean outdoor temperature averaged over 7 or 30 days, respectively, prior to the corresponding study visit by linear regression. Results: We observed a significant inverse correlation between outdoor temperatures and EEcold and CIT, respectively, while EEwarm was not influenced. The daily maximum temperature averaged over 7 days correlated best with EEcold (R2 = 0.123, p = 0.008) and CIT (R2 = 0.200, p = 0.0005). The mean skin temperatures before and after cold exposure were not related to outdoor temperatures. However, the difference between supraclavicular and parasternal skin temperature after cold exposure was inversely related to the average maximum temperature during the preceding 7 days (R2 = 0.07575, p = 0.0221). Conclusion: CIT is significantly related to outdoor temperatures indicating dynamic adaption of thermogenesis and BAT activity to environmental stimuli in adult humans. Clinical Trial Registration: www.ClinicalTrials.gov, Identifier NCT02682706.

Keywords: brown adipose tissue; cold exposure; cold induced thermogenesis; energy expenditure; outdoor temperature; thermogenesis.

Figures

FIGURE 1
FIGURE 1
Average of maximum daily temperature and date of the respective study visit (marked by blue dots).
FIGURE 2
FIGURE 2
Effect of the average maximum outdoor temperature during the 7 days preceding the study visit on energy expenditure under warm (EEwarm) and cold (EEcold) condition and on cold induced thermogenesis (CIT). (A) Outdoor temperature [°C] and EEwarm [kcal/d] show no significant correlation. p = 0.1771, R2 = 0.033. (B) Inverse correlation between EEcold [kcal/d] and the average maximum temperature during 7 days. (C) CIT [kcal/d] (difference of energy expenditure during warm and cold condition) vs. the average maximum temperature [°C] during 7 days. p = 0.0005, R2 = 0.200.
FIGURE 3
FIGURE 3
The Difference in CIT compared between HighTemp study visit (average daily maximum temperature during the previous 7 days above the median of 19.5°C) and LowTemp study visit (outdoor temperatures below the median) shows a 68% reduction.
FIGURE 4
FIGURE 4
Mean skin temperature [°C] during warm condition (red dots) (p = 0.2562, R2 = 0.024) and in response to the acute cold stimulus (blue squares) (p = 0.674, R2 = 0.003) compared to the average of the daily maximum outdoor temperature over a period of 7 days prior to the corresponding study visit.

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