Muscle Metabolism and Shivering During Cold Stress1
Two English explorers recently completed an unsupported coast-to-coast crossing of the Antarctic by foot, dragging a few hundred pounds with them on sleds for 95 days; they experienced temperatures as low as -85°C (-121°F) (Stroud, 1993). A small group of Norwegians completed a similar unsupported 1,400-km trek in the Arctic lasting 100 days, with temperatures down to -54°C (-65°F) (Gautvik et al., 1993). These expeditions demonstrated that it is possible to perform hard physical work for months on end in cold environments, provided adequate planning enables appropriate preparation of food rations and protective clothing and equipment. These expeditions and others suggest there are probably no particular nutritional considerations specific to long-term operations in the cold other than the requirement for sufficient energy consumption to balance energy expenditure.
Contrasting with such situations, the premise directing the research interests of this laboratory is the possibility that emergency survival situations can arise when military personnel cannot be adequately protected from the cold by available clothing and/or shelter. The Canadian Forces recently experienced just such an event when a C130 aircraft crashed north of the magnetic North Pole in October 1991 (de Groot, 1993). Weather complicated rescue attempts until 32 hours after the crash. During this time the survivors had to deal with temperatures ranging from -20° to -60°C (-4° to -76°F) considering the windchill factor. In such situations, hypothermia is delayed in direct proportion to the capacity for, and intensity of, metabolic heat production (i.e., shivering).
By measuring the electrical activity of many muscle groups simultaneously during cold-induced shivering, it is now known that several large muscle groups are recruited and contract at relatively low intensities that are less than 20 percent of their maximum force-generating capabilities (Bell et al., 1992). Because so many muscle groups are involved in shivering, the sum total of their contractile activities can result in a four- or fivefold increase in metabolic rate and in heat production. Much of the attention of Jacobs and coworkers has been directed toward the substrates that are used by skeletal muscle to increase heat production during shivering. Until about a decade ago there was very little empirically based information available in this regard for human subjects. Therefore, some fundamental experiments were carried out in an attempt to fill this knowledge gap. (The reader is referred to Jacobs et al.  for a more detailed review of thermoregulatory thermogenesis during cold stress.)
For example, Vallerand et al. (1988) administered a clinical glucose tolerance test to subjects who were sitting in either cold air or at a comfortable temperature for 2 hours. These data were the first to show in humans that glucose is eliminated more rapidly from the circulation during cold exposure, presumably to provide more available substrate to fuel the increase in metabolic rate. It is also noteworthy that this more rapid uptake of glucose during cold exposure occurs with lower insulin levels in the cold compared to warm temperatures.
Subsequently attempts were made to quantify the rates of substrate oxidation of fat, carbohydrate, and protein in humans during cold exposure with indirect calorimetric techniques. As one might presume, the increase in metabolic rate during shivering is caused by increases in oxidation of both fat and carbohydrate, but the relative increase in the rate of substrate oxidation caused by shivering is greatest for carbohydrates (Vallerand and Jacobs, 1989). In resting subjects exposed to either cold air or cold water, carbohydrates and fat contribute approximately equally to heat production (Martineau and Jacobs, 1989a, b; Vallerand and Jacobs, 1989). From a strategic point of view, this finding seems unfortunate because the body's availability of carbohydrates is quite limited compared to the abundant fat and protein stores. Aware of the well-established positive relationship between muscle glycogen concentration and endurance exercise performance of skeletal muscle, this research group
speculated that there may be a similar detrimental effect caused by muscle glycogen depletion on another form of muscle contraction, that is, shivering and the associated heat production.
CARBOHYDRATE AVAILABILITY AND COLD TOLERANCE
This laboratory has used the needle biopsy technique to measure muscle glycogen changes in the cold. This technique is relatively innocuous and enables biochemical quantification of metabolic events within the muscle cell. Cold-water immersion at 18°C (64°F) was used for experiments because it is a way to very rapidly overwhelm the body's ability to compensate for heat loss by increasing metabolism. Subjects were removed from the water when their rectal temperature reached 35.5°C (95.9°F). Biopsies were taken from the thigh muscle under local anesthetic before and after the immersion to evaluate the changes in glycogen as a result of the water immersion (Martineau and Jacobs, 1988). A series of studies were also carried out in which the muscle glycogen concentrations were manipulated prior to water immersion by appropriate dietary and exercise protocols (Martineau and Jacobs, 1989a); the purpose of these studies was to evaluate the effects of very low and very high glycogen levels on metabolic heat production during the water immersion.
Metabolic rate during cold-water immersion, expressed as oxygen consumption, increases to values that are usually around four or five times the normal resting metabolic rate. Infrequently scientists in this laboratory have observed individuals who exhibit somewhat higher values, six or seven times the resting values. Initial studies suggested that part of this increase in metabolic rate is fueled by muscle glycogen, as all of the subjects demonstrated a decrease in leg glycogen concentration after the water immersion (Martineau and Jacobs, 1988). The second objective of these experiments was to evaluate the effects of manipulating the preimmersion glycogen levels on heat production during cold-water immersion. The manipulations did result in the subjects entering the water during one trial with muscle glycogen levels that were only about 50 percent of normal and during another trial when they were about 150 percent of normal (Martineau and Jacobs, 1989a). Oxygen consumption during the water immersion was about the same on each trial. The respiratory exchange ratio (RER), which is the ratio of carbon dioxide produced divided by the oxygen consumption, differed between trials as expected. An increase in the RER is interpreted as reflecting an increase in the proportion of energy that is transduced from the oxidation of carbohydrates; a decrease in the RER reflects an increase in the proportion of energy transduced from fat oxidation. Metabolic heat production is calculated based on the combination of RER and oxygen consumption. Significantly less metabolic heat production per unit time was observed when the body's carbohydrate stores were depleted compared to the other trials (Martineau and
Jacobs, 1989a). There was also a significantly more rapid body cooling rate, as reflected by the changes in rectal temperature, when the body had little glycogen stored in its muscles and presumably also in the liver (Martineau and Jacobs, 1989a). If one were to take these observations on body temperature cooling rate and try to translate the effects into how long a downed pilot, for example, would last in cold water before becoming severely hypothermic, the results suggest that in the glycogen-depleted state, the individual would cool to a potentially critical temperature significantly more rapidly. Based on the efficiency with which search and rescue activities are coordinated today with the aid of the Search and Rescue Satellite, this time interval is indeed significant.
These initial studies were conducted with subjects resting in cold air or cold water. Based on these results, this research group hypothesized that the requirement to do physical work superimposed on the experimental cold stress might induce a more rapid breakdown of muscle glycogen than if the same work were done at a comfortable temperature. Therefore subjects were asked to perform either light or heavy exercise, once at 9°C (48°F) air temperature and again on a separate day at 21°C (70°F) (Jacobs et al., 1985). Lean subjects were intentionally recruited so that they would begin shivering quickly during their cold-air exposure. Results showed that significantly more glycogen was in fact utilized to do the light exercise in the cold compared to doing the same work at 21°C (70°F). There was no difference in glycogen depletion rates, however, for the higher exercise intensities. This result is consistent with earlier observations that the heat production associated with hard exercise is sufficient to offset heat loss to the environment, thus obviating the need for shivering.
FAT UTILIZATION AND SHIVERING
Investigations also have been conducted on the effects of manipulating the body's circulating fat pools on heat production during cold-water immersion. Vallerand and Jacobs (1990) reported that triglycerides infused into a vein were not eliminated more rapidly from the circulation during cold-air exposure than during warm-air exposure, contrasting with the results for glucose infusion (Vallerand et al., 1988). In another series of experiments, the circulating free-fatty-acid concentration was manipulated by having subjects ingest nicotinic acid in the form of niacin pills prior to and during the water immersion (Martineau and Jacobs, 1989b). Nicotinic acid blocks lipolysis. This effect was demonstrated by the dramatic reduction in plasma free fatty acids and glycerol levels prior to and during the water immersion. Again contrasting with the effects of manipulating the carbohydrate stores, metabolic heat production was virtually unaffected; the proportion of total heat production that
could be attributed to fat oxidation was significantly reduced, but there was compensation by simply increasing carbohydrate oxidation.
THE PREFERRED FUEL
For reasons that are still unclear, carbohydrates seem to be a somewhat preferred substrate during shivering thermogenesis. The effect of hard physical exertion is somewhat similar to shivering thermogenesis in that the body is not able to maintain the same intensity of exertion when carbohydrate stores are depleted, that is, a shift to a greater reliance on fat oxidation to fuel muscle contraction is not sufficient for the musculature to be able to maintain a high level of exertion, just as body temperature could not be maintained as well when carbohydrate stores were depleted (Martineau and Jacobs, 1989a). Interestingly, similar experiments were carried out at the U.S. Army Research Institute of Environmental Medicine (USARIEM), and they did not detect any significant muscle glycogen utilization during cold-water immersion (Young et al., 1989). Discrepancies between USARIEM's studies and those from this laboratory cannot be explained other than to suggest that subjects in this laboratory's experiments were much leaner than those of Young et al. (1989).
AUTHOR'S CONCLUSIONS AND RECOMMENDATIONS
The above brief summary of some of the recent work from this laboratory describes fundamental research that was required to understand how skeletal muscle fuels shivering. Only after such an understanding is achieved can one then consider the development of a substance or procedure that could be applied in an acute survival situation, that is, to enhance thermogenesis during shivering and, by doing so, delay the time to onset of life-threatening hypothermia. Such applications have in fact been developed and are described in the chapter by Andre L. Vallerand (see Chapter 15 in this volume).
- Aside from increased energy demands, does a cold environment elicit an increased demand or requirement for specific nutrients? This author's opinion is that the primary requirement is to balance the increased energy expenditure associated with shivering and exercising in the cold, with a commensurate increase in energy consumption.
- Can performance be enhanced in a cold environment by providing increased amounts of specific nutrients? Studies from this lab suggest that depletion of the body's carbohydrate reserves impairs metabolic heat production during shivering and may thus accelerate the onset of hypothermia. The well-established relationship between aerobic exercise performance and
- carbohydrate availability is therefore much more important in a cold environment.
- Field studies are required to evaluate the effects of nutritional energy deficits on body temperature regulation and work capacity under simulated survival conditions.
Bell, D., P. Tikuisis, and I. Jacobs 1992 Relative intensity of muscular contraction during shivering. J. Appl. Physiol. 72:2336–2342.
de Groot, W.H. 1993 Survival from a C130 accident in the Canadian high Arctic. Pp. K1.1–K1.5 in The Support of Air Operations under Extreme Hot and Cold Weather Conditions. Advisory Group for Aerospace Research and Development (AGARD) Conference Proceedings 540. Neuilly-sur-Seine, France: North Atlantic Treaty Organization.
Gautvik, W., J.O. Owe, and T.A. Oftedal 1993 Evaluation of life support equipment during an unsupported North Pole expedition. Pp. 2.1–2.6 in The Support of Air Operations under Extreme Hot and Cold Weather Conditions. Advisory Group for Aerospace Research and Development (AGARD) Conference Proceedings 540. Neuilly-sur-Seine, France: North Atlantic Treaty Organization.
Jacobs, I. 1993 Fuelling shivering in humans during cold water immersion. Pp. 6.1–6.3 in The Support of Air Operations under Extreme Hot and Cold Weather Conditions. Advisory Group for Aerospace Research and Development (AGARD) Conference Proceedings 450. Neuilly-sur-Seine, France: North Atlantic Treaty Organization.
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1989b Free fatty acid availability and temperature regulation in cold water. J. Appl. Physiol. 67:2466–2472.
Stroud, M. 1993 Shadows on the Wasteland. London: Jonathan Cape.
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Vallerand, A.L., J. Frim, and M.F. Kavanagh 1988 Plasma glucose and insulin responses to oral i.v. glucose in cold-exposed humans. J. Appl. Physiol. 65:2395–2399.
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