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Energy Metabolism During Cold Exposure A. L. Vallerand and I. Jacobs Environmental Physiology Section, Division of Biosciences, Defence and Civil Institute of Environmental Medicine, North York, Ontario, Canada

Introduction

Abstract A. L. Vallerand and I. Jacobs, Energy Metabolism During Cold Exposure. Tnt J Sports Med, Vol 13, Suppl 1,Sl91 —S193, —S193, 1992. Suppl 1,S191

Recent advances on the influence of cold exposure on energy metabolism in animals and humans are summarized. Although the cold-induced enhancements in carbohydrate metabolism have been the focus of numerous

view of the interaction between cold and exercise, the reader is referred to Dr. Therminarias' paper in this Symposium).

Animal Experiments

studies, it was only recently that pieces of evidence from animal studies have suggested that cold exposure exerts an insulin-like effect on peripheral tissue glucose uptake, which appears appears to proceed primarily via insulin-independent insulin-independent pathpathways. Interestingly, this phenomenon was observed in insulin-sensitive tissues of warm- as well as cold-adapted rats. Whereas previous human studies have concentrated on the cold-induced changes in basal levels of hormones and metabolic substrates, recent work from our laboratory has demonstrated that exposure exposure to to cold cold at at rest rest shifts shifts substrate substrateutilutilization from mainly lipids at thermal neutrality to carbohy-

Animal experiments have revealed that cold exposure greatly increases lipolysis, plasma free fatty acids (FFA), glycerol and catecholamines levels, lipid oxidation as well as FFA turnover (3, 8, 10). Much more attention, however, has been devoted to to carbohydrate carbohydrate metabolism. metabolism. ItIt isiswell well established that cold exposure greatly enhances plasma plasma gluglucose turnover, tolerance, oxidation and uptake (2, 7, 11, 12). It was even suggested that acute cold (48 h at 5 °C) exerts an "insulin-like" effect on glucose uptake in insulin-sensitive tissues such as skeletal and heart muscles as well as white and brown

drates, representing the main fuel for shivering thermo-

adipose tissues (12). Another experiment in which animals had barely detectable insulin levels provided further evidence that cold exposure stimulates peripheral tissue glucose uptake

genesis. Further investigation has revealed that the marked

increment in carbohydrate oxidation in cold-exposed humans is derived from a greater utilization of both circulating glucose and intramuscular glycogen. With respect to lipid metabolism, recent studies have shown that the coldinduced increase in lipid oxidation in man is fuelled primarily by the fatty acids released from white adipose tissue

primarily via insulin-independent pathways (9), possibly similar to the well-known "insulin-like" effect of exercise (see 12). Interestingly, about the same cold-induced increase in skeletal muscle glucose uptake was observed in both warm- and coldadapted adapted rats rats (16). (16). Although Although shivering shivering thermogenesis thermogenesis could could be be implicated in warm-adapted animals, such is not the case in the cold-adapted ones since they do not shiver (16), suggesting the

triglycerides (TG) and possibly intramuscular TG, not plasma TG. One practical application of this work on energy metabolism in the the cold cold resides resides in in the the pharmacologipharmacological approach to improve cold tolerance, where pharmacological agents that alter energy metabolism and substrate

possibility of a norepinephrine activation of nonshivering thermogenesis of muscular (16) or vascular origin (1).

utilization could be used to enhance cold thermogenesis

Human Experiments Experiments

and produce warmer body temperatures.

In contrast to these animal studies, little is

words Key words

Animals, carbohydrate, humans, lipid, substrate strate utilization

I

known about fuel metabolism in humans. Although it has been reported in humans that cold exposure increased basal levels of plasma FFA, glycerol, catecholamines and that it decreases

plasma glucose and insulin (for a review see 14, 17), these changes did not reveal any information with respect respect to to subsubstrate utilization. Using the well-known indirect calorimetry and nonprotein respiratory exchange ratio technique, we have recently demonstrated that that the the cold-induced cold-induced increase increase in in heat heat production (fasting semi-nude subjects at rest for 2 h at 10 °C, was m s1 wind) wasassociated associatedwith withaa58% 58%and and63% 63% increase increase in 11 ms'wind)

carbohydrate and lipid oxidation, respectively, and an un13(l992)S191 —Sl93 lnt.J.SportsMed. 13(1992)S191—S193 lnt.J.SportsMed. Georg Thieme Verlag Verlag Stuttgart New York GeorgThieme York

changed protein oxidation (14; Fig. 1). The proportion of sub-

strate utilization was also dramatically altered. At thermal

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When the thermal insulation provided by the microclimate and by peripheral vasoconstriction have been optimized, and body heat losses remain too high, cold-exposed mammals at rest must rely on their capacity to increase heat production through the oxidation of additional metabolic lie substrates to avoid or delay hypothermia (14, 18; for a re-

S192 mt.J.J.Sports S192 mt. Sports Med. Med. 13 (1992) (1992) +58B% +588%

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ni 60 j6O a, 0,

50 gg 50 50 a Ct :2 2 40 40 'C 0 'Cta30 30 0 20 V 20

Fig. 1 Rates of

acids for oxidation during prolonged exercise, it was hypothe-

carbohydrate, lipid arid protein oxidaand tion in fasting seminude subjects exposed to either thermal neutrality

sized that the same concept could apply to the cold. cold. UnforUnfortunately, plasma TG clearance was found unaffected unaffected by by the the cold (17). It remains to be determined whether intramuscular TG (the only other source of fatty acids) represents a key source of readily available fatty acids for oxidation in in the the

(29 °C) or cold

shivering muscles (17).

(10 °C (10 C 11 ms1 wind) for 2 h at rest (Redrawn from ref.

10

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14).

cold

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Conclusions

Recent animal and human studies have thus permitted a better understanding of the influence of cold on energy metabolism and substrate utilization. So what? Why should this be so important? One practical application of this work is that if ifwe weunderstand understandenergy energymetabolism metabolismslightly slightlybetter better

in the cold, perhaps we will be able to enhance heat production, provide warmer body temperatures and improve cold tolerance. After having demonstrated that a key limiting factor in the cold was substrate mobilisation and/or utilization, and not the 02/CO 2 carrying capacity or the mitochondrial oxidative capacity, it was found that pharmacological agents, like theophylline, that altered fuel metabolism in the cold were also effective in retarding the onset of hypothermia in both animals and humans (for a review see 18). Another good example is the ingestion of a mixture of ephedrine/caffeine in cold-ex-

posed subjects. It enhanced energy expenditure through a greater carbohydrate oxidation and consequently produced

0

C

warmer body temperatures (15). Since these drugs are thermogenic at thermal neutrality, it was not clear whether they would act through shivering and/or nonshivering mechanisms (15). Finally, very little information is currently available in humans on the turnover and futile cycling of metabolic substrates, on the insulininsulin- and and non-insulin-mediated non-insulin-mediated glucose glucose uptake uptake as as well well the as on the mechanisms through which shivering or nonshiver-

a C) 0

ing thermogenic processes can be enhanced, and future stu-

a 0.

dies dealing with these concepts are badly needed.

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References References

neutrality, the greatest proportion of the energy expenditure was derived from lipids (59%), but in the cold, there was a marked shift to carbohydrates carbohydrates (51 (51% % of the total energy expenditure; 14). The next logical step was to attempt to determine the origin or the source of substrates thus oxidized.

Confirming previous animal work, we have been able to show that the utilization of circulating carbohydrates (13) is accelerated in the cold even in the presence of a reduced insulinemia (13). In addition, cold exposure increases intramuscular glycogen gycogen (4) the utilization of intramuscular (4) which which can be a limiting factor in the cold since low levels prior to cold water immersion (90 mm in 18 °C water) significantly accelerated body cooling (5).

Coiquhoun E. Q., Clarq M. G.: Colquhoun 0.: Open Openquestion: question:Has Hasthermogenethermogenesis in muscle been overlooked and misinterpreted? News in Physiol 2

Sci6:256—259, 1991. Depocas F., Masironi R.: Body glucose as fuel for thermogenesis Depocas

in the white rat exposed exposed to to cold. cold. Am Am JJPhysio/ Physiol 199: 1051—1055, 1960. 1960.

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Himms-Hagen J.: Lipid metabolism during cold exposure and cold acclimation. Lipids 7:310—320, 1972. coldacclimation.Lipids7: 310—320,1972. Martineau L., Jacobs Jacobs1.:I.:Muscle Muscleglycogen glycogen utilization during shiverutilization during shivering thermogenesis in in humans. humans. JApplPhysiolS6: JApplPhysiol56: 2046—2050, 2046—2050,1988. 1988. Martineau L., Jacobs I.: Muscle glycogen availability and temperature regulation in humans. JApplPhysioló6: JAppIP/iysiol66: 72— JApplPhysiol66: 72— 78, 78, 11 989a. 989a. Martineau L., Jacobs I.: Free fatty acids availability and temperature regulation in cold water. JAppiPhysiol JApplPhysiol67: 67:2466—2472, 2466—2472, 1 989b.

Minaire Y., Forichon J., J., Dallevet Dallevet G., 0., Jomain M. J.: Combined effects of cold and somatostatin on glucose kinetics in dogs. Eur J ApplPhysiol46:249—259, 249—259, 1981. 1981. 8 ApplPhysiol46: Paul P., Holmes W. L.: Free fatty acid metabolism during stress: exercise, acute cold exposure and anaphylactic shock. Lipids 8:

It was also of interest to ascertain ascertain the the origin origin of of the fatty acids oxidized in the cold. Using nicotinic acid to

142— 150,1973 142—150,1973 Shibata H., Perusse F., Vallerand A. L., Bukowiecki L. J.: Cold ex-

block white adipose tissue lipolysis, and thus markedly

posure reverses the inhibitory effects of fasting posure fasting on on peripheral peripheral gluglucose uptake in rats. Am 257 (Reg. Tnt. Comp. Physiol. 26): Am JPhysiol JPhysiol257 R96— RIO RI 01,1989. 1,1989. R96—Rl01,1989. 0. E.: Physio'ogical efect RobertE.: Physioiogical Physiological efect of of cold exposure, in RobertThompson G. shaw, D. (ed): International Review of Physiology II, vol 15, Baltimore MD, UnviersityPress, 1977, pp 29—69. timoreMD,TlnviersityPress, timoreMD,TJnviersityPress, l977,pp29—69.

decrease plasma glycerol and FFA, Martineau and Jacobs (6) showed that it did not alter metabolic rate, lipid oxidation or body cooling, suggesting that the body oxidized fatty acids from another source. Since plasma triglycerides (TG) were already known to represent another important source of fatty

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A. L. Vallerand and I. Jacobs

Energy Metabolism during Cold Exposure Vallerand A. L., Lupien J., Bukowiecki L. J.: Interactions of cold

exposure and starvation on glucose tolerance and insulin re-

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sponse. AmJPhysiol245 (Endo Metab 80): E575 —E58 1, 1983. Vallerand A. L., Perusse F., Bukowiecki L. J.: Cold exposure potentiates the effect of insulin on in vivo glucose uptake. Am J Phyisol253 (EndoMetab 16): El79—186, 1987. Vallerand A. L., Frim J., Kavanagh M. F.: Plasma glucose and in-

sulin responses to oral and intravenous glucose in cold-exposed humans.JApplPhysiol65: 2395—2399, 1988. Vallerand A, L., Jacobs I.: Rates of energy substrates utilization during human cold exposure. JAppiPhysiol 58: 873— 878, 1989. Vallerand A. L., Jacobs I., Kavanagh M. F.: Mechanism of en-

hanced cold tolerance by an ephedrine/caffeine mixture in humans.JApplPhysiol67: 438—444,1989. Vallerand A. L., Perusse F., Bukowiecki L. J.: Stimulatory effects of cold exposure and cold acclimation on glucose uptake in rat peripheral tissues. Am J Physiol 259 (Regul Tnt Comp Physiol 28):

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mt. J. Sports Med. 13 (1992) S193

Vallerand A. L., Jacobs I.: Influence of cold exposure on plasma TG clearance in humans. Metabolism 39: 1211—1218, 1990. Wang L. C. H., Man S. F. P., Belcastro A. N.: Metabolic and hor-

monal responses in theophylline-increased cold resistance in males.JApplPhysiol63: 589—596, 1987.

Dr. A. L. Vallerand Environmental Physiology Section Division of Biosciences Defence and Civil Institute of Environmental Medicine 1133 SheppardAve.W. P. 0. Box 2000 North York, Ontario M3M 3B9

Canada

R1043— R1049, 1990.

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Energy metabolism during cold exposure.

Recent advances on the influence of cold exposure on energy metabolism in animals and humans are summarized. Although the cold-induced enhancements in...
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