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Multiorgan contribution to non-shivering and shivering thermogenesis and vascular responses during gradual cold exposure in humans

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Abstract

Purpose

Human brown adipose tissue (BAT) is known to be a significant thermoeffector in non-shivering thermogenesis (NST), albeit with individual variations in the BAT activity. We hypothesized that humans with less BAT would have more contribution from the skeletal muscle (SM) to NST or earlier shivering onset and greater vasoconstriction to compensate for less BAT-mediated thermogenesis.

Methods

Eighteen males participated in this study. Their BAT activity and detectable volume were investigated. A gradual cold exposure was conducted for inducing NST at 18.6 °C and initiating shivering at 11.6 °C. The energy expenditure, electromyograph of the pectoralis major, skin blood flow, and rectal (Tre) and skin temperatures were evaluated.

Results

BAT volume significantly correlated with the change in metabolic heat production during mild cold phase relative to baseline (NST; r = 0.562, P < 0.05), but not with shivering initiation phase (NST+ ST). SM mass correlated with baseline metabolic heat production (Mbase; r = 0.839, P < 0.01) but not with NST or NST + ST. A positive correlation was noted between BAT volume and Tre at the end of the 18.6 °C exposure period (r = 0.586, P < 0.05), which positively correlated with shivering onset time (r = 0.553, P < 0.05). The skin blood flow, mean skin temperature, and forearm and finger skin temperature difference at the end of the 18.6 °C exposure period did not correlate with NST or BAT volume.

Conclusion

BAT volume positively correlated with NST. Notably, lower Tre in individuals with less BAT volume induced earlier shivering onset for offsetting the less NST. Whereas, no correlation between metabolic and vasomotor responses was observed.

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Abbreviations

BAT:

Brown adipose tissue

CIT:

Cold-induced thermogenesis

EMG:

Electromyography

I tissue :

Tissue insulation

M :

Metabolic heat production

MVC:

Maximal voluntary contraction

NST:

Non-shivering thermogenesis

SkBF:

Skin blood flow

SM:

Skeletal muscle

ST:

Shivering thermogenesis

SUVmean :

Mean standard uptake value

T f–f :

Forearm and finger skin temperature difference

T re :

Rectal temperature

\(\bar{T}_{\text{sk}}\) :

Mean skin temperature

\(\dot{V}{\text{O}}_{2}\) :

Oxygen uptake

References

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Acknowledgements

The authors wish to thank all those who participated in this study.

Funding

This study was supported by a Grant-in-Aid for Scientific Research (No.26291099; 19H03314) from the Japan Society for the Promotion of Science.

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Authors and Affiliations

Authors

Contributions

HW, YK, KM, and TM conceived and designed research. TK, MM, and MS conducted the PET/CT experiments. YK, KM, and TE conducted the gradual cold exposure tests. TK, KM, YK, and HW analyzed data. KM and HW wrote the draft of manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Hitoshi Wakabayashi.

Ethics declarations

Conflict of interests

None declared.

Ethics approval

All experimental protocols in this study were approved by the IRB of the Tenshi College and Hokkaido University.

Additional information

Communicated by George Havenith.

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Wakabayashi, H., Matsumoto, K., Kobori, Y. et al. Multiorgan contribution to non-shivering and shivering thermogenesis and vascular responses during gradual cold exposure in humans. Eur J Appl Physiol 120, 2737–2747 (2020). https://doi.org/10.1007/s00421-020-04496-1

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  • DOI: https://doi.org/10.1007/s00421-020-04496-1

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