Shivering thermogenesis in humans: Origin, contribution and metabolic requirement

Abstract

As endotherms, humans exposed to a compensable cold environment rely on an increase in thermogenic rate to counteract heat lost to the environment, thereby maintaining a stable core temperature. This review focuses primarily on the most important contributor of heat production in cold-exposed adult humans, shivering skeletal muscles. Specifically, it presents current understanding on (1) the origins of shivering, (2) the contribution of shivering to total heat production and (3) the metabolic requirements of shivering. Although shivering had commonly been measured as a metabolic outcome measure, considerable research is still needed to clearly identify the neuroanatomical structures and circuits that initiate and modulate shivering and drives the shivering patterns (continuous and burst shivering). One thing is clear, the thermogenic rate in humans can be maintained despite significant inter-individual differences in the thermogenic contribution of shivering, the muscles recruited in shivering, the burst shivering rate and the metabolic substrates used to support shivering. It has also become evident that the variability in burst shivering rate between individuals, despite not influencing heat production, does play a key role in orchestrating metabolic fuel selection in the cold. In addition, advances in our understanding of the thermogenic role of brown adipose tissue have been able to explain, at least in part, the large inter-individual differences in the contribution of shivering to total heat production. Whether these differences in the thermogenic role of shivering have any bearing on cold endurance and survival remains to be established. Despite the available research describing the relative thermogenic importance of shivering skeletal muscles in humans, the advancement in our understanding of how shivering is initiated and modulated is needed. Such research is critical to consider strategies to either reduce its role to improve occupational performance or exploit its metabolic potential for clinical purposes.

Keywords: carbohydrate utilization; electromyography; energy metabolism; fatty acid oxidation; shivering; skeletal muscle; thermogenesis.

Figure 1.

Simplified schematic representation of cold-induced thermogenesis. Afferent input represented by green boxes, efferent output represented by red box, thermoregulatory control center (hypothalamus) and integrated response (core temperature) represented by black boxes. Model adapted from refs. ,,.

Figure 2.

Changes in shivering intensity as a function of changes in mean skin temperature measured under compensable conditions (no change in T_core). Data adapted from refs. , , , , , .

Figure 3.

Changes in thermogenic rate (times resting metabolic rate (xRMR)) as a function of changes in average skin temperature found in various cold exposure studies in lean healthy men. Thermogenic rates are characterized as mild (1–2 xRMR), moderate (2–3 xRMR) and high (>3 xRMR). Points represent data from end of cold exposure for following studies.^,,,,