J Appl Physiol 103: 1346-1351, 2007.
First published July 19, 2007; doi:10.1152/japplphysiol.00931.2006
8750-7587/07 $8.00
Fueling shivering thermogenesis during passive hypothermic recovery
François Haman,1
Chris G. Scott,2 and
Glen P. Kenny2
1Faculty of Health Sciences and 2School of Human Kinetics, University of Ottawa, Ottawa, Ontario, Canada
Submitted 22 August 2006
; accepted in final form 6 July 2007
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ABSTRACT
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In humans, the relative importance of oxidative fuels for sustaining shivering during passive hypothermic recovery or rewarming is still unclear. The main goals of this study were 1) to quantify the respective contributions of lipids and carbohydrates (CHO) during passive rewarming and 2) to determine the effects of precooling exercise on the pattern of fuel utilization. With indirect calorimetry methodologies, changes in fuel metabolism were quantified in nonacclimatized adult men shivering to rewarm from moderate hypothermia (core temperature 
34.5°C) not following (Con) or following a precooling exercise at 75% 
O2max for 15 min (Pre-CE). As hypothermic individuals shiver to normothermia, results showed that CHO dominate at all shivering intensities above 50% Shivpeak, while lipids were preferred at lower intensities. This change in the relative importance of CHO and lipids to total heat production was dictated entirely by modulating CHO oxidation rate, which decreased by as much as 10-fold from the beginning to the end of rewarming (from 1,611 ± 396 to 141 ± 361 mg/min for Con and 1,555 ± 230 to 207 ± 261 mg/min for Pre-CE). In contrast, lipid oxidation rate remained constant and low (relatively to maximal rates at exercise) throughout rewarming, averaging 183 ± 141 for Con and 207 ± 118 mg lipids/min for Pre-CE. In addition, this pattern of fuel selection remained the same between treatments. We concluded that fuel selection is regulated entirely by changes in CHO oxidation rate. Further research should focus on establishing the exact regulatory processes involved in achieving this large upregulation of CHO utilization rate following hypothermia.
hypothermia; human survival; heat loss; fuel selection; thermoregulation
IN COLD EXPOSED HUMANS, significant decreases in core temperature or hypothermia occur when increases in heat production are not sufficient to compensate for increases in heat loss. Following a hypothermic episode, shivering thermogenesis (ST) remains the only physiological process available for reestablishing core temperature in nonexercising, nonassisted individuals (15). Most studies during passive hypothermic recovery or passive rewarming focused on the efficiency of external warming methods (for example, warm water immersion, warm air breathing; Ref. 6) and, therefore, little is known about the metabolic requirements of ST following hypothermia. In the only study focusing on the energy demand of ST during passive rewarming, Neufer et al. (15) showed that core warming rate in nonacclimatized hypothermic men remained unaffected by glycogen depletion (0.61 vs. 0.71°C/h for control vs. glycogen depleted). However, the respective importance of CHO and lipids to total heat production (
prod) still remains unknown because rates of oxidation have never been quantified. During sustained low and moderate shivering intensities, recent work has shown that the relative contribution of CHO to total prod increases progressively as shivering intensifies, while that of lipids and proteins decreases progressively (11). Most importantly, these changes in fuel selection occur entirely by upregulating rates of CHO utilization because lipid and protein oxidation rates remain unchanged. Whether this same pattern of fuel selection is found during passive rewarming remains to be established.
Therefore, the main goals of this study were 1) to determine the pattern of fuel selection during rewarming and 2) to investigate the potential effects of high-intensity, short-duration precooling exercise on changes in fuel utilization rates. More specifically, changes in CHO and lipid oxidation rates were quantified in nonacclimatized adult men following moderate hypothermia (core temperature 34.5°C). These experiments were conducted either without performing precooling exercise (Con) or following a precooling exercise bout at 75% O2max for 15 min on a cycle ergometer (Pre-CE). Based on the previously reported fuel selection pattern observed during low- and moderate-intensity shivering (11), we predict that the contribution of CHO to total heat production will be dominant at high shivering intensities, while lipids will be the preferred fuel at lower intensities. Second, assuming that the combination of cycling at 75% O2max for 15 min is sufficient to induce neuromuscular fatigue and a reduction in CHO availability, we anticipate that CHO utilization rate will be decreased during rewarming following precooling exercise due to an overall reduction in the recruitment of type II, fatigable fibers, and/or CHO availability (9, 14, 22).
This study will also address another important issue. Previous shivering work indicates that maximal lipid oxidation rate seems to be already reached at low metabolic rates (135 mg·lipids kg–1·h–1; Ref. 11); a value more than three times lower than the one reported for sustained exercise by Achten et al. (1). Physiological reasons for this limitation are still unknown because subsequent measurements during shivering were only performed at low [2.5x resting metabolic rate (RMR) or 15% O2max] and moderate intensities (3.5x RMR or 20% O2max). In the present study, it is expected that shivering intensities during rewarming will exceed 3.5x RMR and may even reach maximal shivering intensity at 5x RMR (5) due to the severity of the cold stress. Consequently, this study will allow us to determine if higher rates of lipid oxidation can be achieved during shivering.
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METHODS
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Subjects.
Six healthy, physically active men with no history of cardiorespiratory disease or cold injuries volunteered for this study. The subject's characteristics were as follows (mean ± SD): age: 24.4 ± 5.5 yr; height: 1.79 ± 0.06 m; weight: 78.5 ± 11.5 kg; body surface area: 1.98 ± 0.15 m2 (12); percentage body fat: 16.1 ± 5.5% [hydrostatic weighing according to Siri equation; (18)]; O2max: 43.3 ± 6.7 ml·kg–1·min–1 [incremental progressive maximal oxygen consumption test (O2max) on a cycle ergometer (19)]. The study was approved by the Health Sciences Ethics Committee of the University of Ottawa, and written consent was obtained from the participants.
Experimental protocol.
Each subject participated in two experimental trials: 1) rewarming without precooling exercise (Con) and 2) rewarming with precooling exercise (Pre-CE; described in more detail below). These experimental trials were randomized and conducted at the same time of the day after 48 h without heavy physical activity. Subjects were also instructed to abstain from consuming caffeine and alcohol for at least 12 h prior to each trial and to refrain from eating for at least 2 h before each experiment. Care was taken to minimize thermal stimuli between awakening and the start of the experiment (i.e., to avoid exposure to hot or cold temperatures and to avoid physical activity during transit from home to the laboratory). On their arrival in the laboratory, subjects were instrumented with thermal probes and asked to sit quietly for 1 h at 23°C (32% relative humidity). During this baseline period, temperature and indirect calorimetry measurements were collected in the last 30 min. Subjects were then asked to 1) remain resting for an additional 15 min (Con) or 2) perform 15 min of cycling at 75% O2max (Pre-CE). Following the aforementioned treatment, subjects were immersed up to the clavicles in a circulated water bath at 7°C (simulating typical open water temperatures in early spring and late autumn in Canada) until their core temperature reached 34.5°C. Prior to this cold water immersion, subjects were fitted with neoprene mitts and socks to minimize the risk of developing nonfreezing cold injuries at the extremities. During the immersion period, the water temperature was monitored with a thermocouple and adjusted when necessary by the addition of ice. Once core temperature reached 34.5°C, subjects were helped out of the water bath, towel dried, and asked to remain seated in an upright position at room temperature (23°C) until their core temperature had returned to baseline values (prior to cold exposure or precooling exercise). During cooling, time before reaching 34.5°C was not different between Con and Pre-CE averaging, respectively, 56 ± 21 min (ranging from 34 to 92 min depending on the subject) and 53 ± 23 min (ranging from 31 to 94 min). Rewarming time back to baseline values was also the same between treatments, averaging 40.0 ± 4.1 min for Con and 37.5 ± 7.6 min for Pre-CE.
Thermal response.
Whole body heat loss (loss in kj/min) was estimated using the following equation:
 | (1) |
where, 
and 
represent rates of radiative and convective heat loss and resp is the rate of evaporative and convective heat loss by ventilation. and were estimated using heat flux transducers (Concept Engineering, Old Saybrook, CT) placed on the surface of the skin at 11 sites (i.e., forehead, chest, biceps, forearm, abdomen, lower and upper back, front and back calf, quadriceps, hamstrings) and calculated using an area-weighed equation (3). Evaporative heat loss from the skin was assumed to be negligible at 23 and 10°C (16). rsep was estimated using the following equation:
 | (2) |
where, 
is the density of air (kg/m3), E the ventilation (l/min), 
is the latent heat vaporization (m3/s), c is the specific heat (J·kg–1·K–1; subscripts a and v refer to air and vapor, respectively), T is temperature (°C or K) (subscripts e and I refer to the expired and inspired air, respectively), and 
is the humidity ratio.
Total heat production (prod) was calculated by indirect respiratory calorimetry corrected for protein oxidation (see below). Percent of shivering peak was determined by dividing O2 (ml·kg–1·min–1) values measured in the cold by the highest metabolic rate recorded postcooling for Con and Pre-CE. This maximal shivering rate (Shivpeak in ml·kg–1·min–1) was not different from those calculated using the shivering peak estimated for each subject using the equation proposed by Eyolfson et al. (5):
 | (3) |
where, O2max is the maximal oxygen consumption (ml·kg–1·min–1), BMI is the body mass index (kg·m–2), and the age is in years.
Esophageal temperature (Tes) was monitored continuously using a pediatric probe (Mon-a-therm general purpose, Mallinckrodt Medical, St. Louis, MO). Rewarming rate (°C/min) was calculated using Tes values measured at 15-s intervals following cold water immersion. Mean skin temperature (
skin) was averaged from 12 sites (i.e., finger tip plus 11 heat transducer sites mentioned above for heat flux measurements) using an area-weighed equation (3).
Metabolic rate and fuel utilization.
Pulmonary ventilation (E), oxygen consumption (O2), and carbon dioxide production (CO2) were determined using a mouthpiece and a calibrated automated metabolic analyzer (Med-Graphics CPX-D, St. Paul, MN). O2 and CO2 were averaged every 5 min and carbohydrate (CHOox) and lipid (FATox) oxidation rates (in g/min) were calculated using the following equations (2, 13):
 | (4) |
 | (5) |
where CO2 (l/min) and O2 (l/min) were corrected for the volumes of O2 and CO2 corresponding to protein oxidation (1.010 and 0.843 l/g, respectively). Protein oxidation rate was estimated at 66 mg/min based on previously published urinary urea excretion measurements made on 12-h postabsorptive men with normal CHO reserves (8, 10). Energy potentials of 16.3, 40.8, and 19.7 kJ/g were used to calculate the amount of heat produced from glucose, lipid (fatty acids), and protein (amino acids) oxidation, respectively (4, 17).
Statistical analyses.
Changes in Tes, skin, loss, and prod were assessed by two-way ANOVA for repeated measures. Differences in prod, fuel utilization for CHO (CHOox) and lipids (FATox) at baseline (23°C) as well as during exercise (only for the precooling exercise experiment), cooling and rewarming were determined using a one-way ANOVA to verify the main effect of the treatment (Con vs. Pre-CE). Statistical differences were considered significant when P 
0.05. The statistical power of for the two-way ANOVA for repeated measures was calculated for CHOox and FATox and it reached 0.54 and 0.74, respectively. All values presented are means ± SD (n = 6) unless indicated otherwise.
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RESULTS
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Thermal responses.
Changes in skin, Tes, prod, and loss measured prior to cooling, during precooling exercise (Pre-CE only), during cooling and postcooling for Con and Pre-CE are presented in Fig. 1. While postexercise values were significantly higher for Pre-CE, no difference between Con and Pre-CE were observed by the end of cooling and throughout rewarming. By the end of immersion, skin decreased from 31.9 ± 0.6°C at baseline to 12.2 ± 4.7°C prior to rewarming for Con and from 31.7 ± 0.9 to 11.2 ± 3.5°C for Pre-CE (Fig. 1). Tes decreased from 37.1 ± 0.3 to 34.1 ± 0.3°C for Con and from 37.1 ± 0.2°C to 34.5 ± 0.03°C for Pre-CE (Fig. 1). prod increased 3.7-fold for Con from 7.2 ± 1.1 to 26.5 ± 7.5 kJ/min and 3.9-fold for Pre-CE from 6.7 ± 1.2 to 25.1 ± 7.7 kJ/min (Fig. 1). For both Con and Pre-CE, metabolic rates reached by the beginning of rewarming was equivalent to maximal shivering intensity (5). loss increased fourfold for Con from 7.4 ± 0.9 to 29.8 ± 10.3 kJ/min and for Pre-CE from 7.4 ± 1.4 to 29.7 ± 13.8 kJ/min (Fig. 1). By the end of rewarming, skin and Tes increased to 27.5 ± 1.3 and 36.2 ± 0.3°C for Con (27.6 ± 1.0 and 36.2 ± 0.2°C for Pre-CE) while prod and loss increased to 10.8 ± 3.4 and 5.9 ± 1.7 kJ/min for Con (14.5 ± 9.4 and 5.1 ± 1.7°C for Pre-CE).
Changes in rewarming rates and heat balance during rewarming are shown in Fig. 2. Rewarming rate and heat balance during rewarming were not different between Pre-CE and Con. Maximal rewarming rate was measured at 15 min and averaged 0.09 ± 0.05°C/min (Con) and 0.08 ± 0.05°C/min (Pre-CE). In addition, Fig. 3 illustrates changes in shivering intensity (%Shivpeak) as a function of changes in Tes and skin for Con and Pre-CE. Again, no difference was found between Con and Pre-CE.
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Fig. 2. Changes in rewarming rate (top) and heat balance (bottom) in men recovering from moderate hypothermia measured in men recovering from moderate hypothermia not following (Con) and following precooling exercise (Pre-CE). Values are presented for the longest rewarming period common to all subjects for each condition.
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Fuel selection.
Changes in the absolute rates and relative contributions of CHO and lipids to total heat production as a function of percent shivering intensity (%Shivpeak) during rewarming are presented in Fig. 4. From the beginning to the end of rewarming, shivering intensity ranged from 97 ± 4 to 26 ± 5.1%Shivpeak for Con and from 95 ± 3 to 27 ± 7%Shivpeak for Pre-CE. Along this range of shivering intensities, no significant difference in absolutes rates of oxidation and relative contribution to total prod were observed between Con and Pre-CE. Absolute rates of CHO oxidation varied from 1,611 ± 396 to 141 ± 360 mg/min for Con and 1,555 ± 237 to 207 ± 261 mg/min for Pre-Ex. In contrast, absolute rates of lipid oxidation remained constant averaging 183 ± 141 mg/min for Con and 207 ± 118 mg/min for Pre-Ex. Relative contributions of CHO to total 
prod decreased continuously from beginning to the end of rewarming from 79.3 ± 15.6 to 25.5 ± 13.2% prod for Con and from 69.9 ± 9.9 to 37.7 ± 11.8% prod for Pre-CE), whereas that of lipids increased from 16.7 ± 15.7 to 60.9 ± 13.2% prod for Con and from 26.4 ± 10.3 to 48.4 ± 12.4% prod for Pre-CE. The crossover point or point at which CHO and lipid provide equally to total heat production occurred at 50% (Con) and 60%Shivpeak (Pre-CE) and was not different between treatments. Table 1 summarizes total amounts of CHO and lipids used during rewarming in Con and Pre-CE, as well as the relative contributions of these fuels to total prod averaged over the entire rewarming period. Again, no overall differences between Con and Pre-CE were found in the total amount of CHO or of lipid used to sustain shivering and in the relative contributions of these fuels to total prod production when averaged over the entire rewarming period.
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Table 1. Hprod as well as absolute and relative contributions of CHO and lipids to Hprod measured in men recovering from moderate hypothermia not following or following pre-CE
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DISCUSSION
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This study quantifies the contributions of CHO and lipids to total heat production during passive rewarming. It shows that as individuals shiver to normothermia, CHO dominate at all shivering intensities above 50%Shivpeak, while lipids are preferred at lower intensities (Fig. 4). This change in CHO and lipid utilization rate is achieved entirely by a modulation of CHO oxidation rate, which varies by as much as 10-fold from the beginning to the end of rewarming (Fig. 4). In contrast, over the entire range of shivering intensities, lipid oxidation rate remains stable and low (relative to maximal rates during exercise, see Oxidizing lipids). The pattern of fuel selection found here during rewarming is consistent with the one observed previously in men during sustained low- and moderate-intensity shivering (11; Fig. 5). Finally, pre-cooling exercise at 75% O2max for 15 min is insufficient to cause the anticipated decrease in CHO utilization rate during rewarming (P = 0.20; Fig. 4 and Table 1).
Fuel selection during passive hypothermic recovery.
The 7°C water immersion used in this study to induce hypothermia in nonacclimatized men resulted in decreases of 3°C for Tes and 20°C for skin by the end of cold exposure. Together these changes in deep and peripheral temperatures were sufficient to elicit maximal shivering by the beginning of warming [4–5 times resting metabolic rate or 50% O2max; Eyolfson et al. (5)]. As individuals shiver to normothermia, results show that absolute rates of CHO oxidation decrease by as much as 10-fold (from 1,611 ± 396 to 141 ± 361 mg/min for Con and 1,555 ± 230 to 207 ± 261 mg/min for Pre-CE), whereas lipid utilization rate remains constant (discussed later, see Oxidizing lipids; Fig. 4, A and B). In effect, the relative contribution of CHO decreases progressively (from 80 to 25% prod for Con and from 70 to 38% prod for Pre-CE), whereas that of lipids increases from 17 to 61% prod for Con (from 26 to 48% prod for Pre-CE) as shivering lessens in intensity and individuals approach normothermia (Fig. 4, C and D). The crossover point or the shivering intensity at which CHO and lipids contribute equally to total heat production occurs at 50%Shivpeak when precooling exercise is not performed. This pattern of fuel oxidation rate is consistent with the one described recently during sustained shivering in nonhypothermic adult men exposed for 90 min to either 10°C [low-intensity shivering (L); or 5°C (moderate-intensity shivering (M); Ref. 11]. We compared patterns of fuel selection found previously during sustained shivering in nonhypothermic men (11) and during passive rewarming in hypothermic men in the present study. This comparison is summarized in Fig. 5 and reveals that fuel selection patterns are identical between shivering conditions. As observed in the present study, rates of CHO oxidation increase from L to M intensified, whereas that of lipids remains unaffected (Fig. 5, top). In addition, the relative importance of CHO increases progressively as shivering intensifies during sustained shivering in nonhypothermic men while that of lipids decreases. These changes in the relative importance of CHO and lipids to total heat production also reveal the same crossover point found at 50%Shivpeak. With an isotopic tracer method, this previous work has also shown that most of the increase in CHO oxidation rate from L to M is supported by a substantial increase in the mobilization of muscle glycogen reserves. In the present study, it is still unclear whether the 8- to 10-fold increase in CHO oxidation rate found during hypothermic recovery is also sustained primarily by an increase in muscle glycogen utilization rate.
On the basis of previous observations, a number of mechanisms could be responsible for the large increase in CHO oxidation observed here. Fuel selection is modified acutely in three ways: 1) by recruiting different metabolic pathways within the same fibers, 2) by recruiting specific subpopulations of fuel specific fibers within the same muscle, or 3) by recruiting muscles varying in fiber composition (20). In the cold, the first two mechanisms of fuel selection have been identified (7, 8). During low-intensity shivering [2.5 times resting metabolic rate (RMR)], CHO-depleted and CHO-loaded individuals were able to sustain the same rate of heat production by recruiting different metabolic pathways within the same fibers (7). In contrast, during moderate shivering (3.5 times RMR), alterations in fuel selection are achieved by recruiting subpopulations of fuel specific fibers within the same muscle (8). In view of the large range of shivering intensities found here during hypothermic recovery (up to 5 times RMR), we can speculate that the 8- to 10-fold increase in CHO utilization rate is achieved by proportionally increasing the specific recruitment of "CHO specific" fibers (i.e., type II glycolytic fibers) within shivering muscles; assuming that the same muscles were recruited throughout warming). Clearly, however, additional work is needed to identify the exact mechanisms responsible for this regulation in CHO oxidation rate.
Oxidizing lipids.
During hypothermic recovery, the relative importance of lipids increases progressively as shivering intensity declines and individuals approach normothermia. However, this change is not achieved by upregulating lipid oxidation rate as it remains constant, averaging 183 ± 141 for Con and 207 ± 118 mg lipids/min for Pre-CE throughout rewarming (Fig. 4). Similarly, during sustained shivering in the cold, previous work has shown that lipid oxidation rate never exceeds 165 mg lipids/min even when shivering intensity increases from low to moderate (Fig. 5; Ref. 11). Together these findings indicate that maximal rates of lipid oxidation are already achieved at low shivering intensities. Clearly, however, we anticipated that much higher rates could be reached as shivering intensified from 3.5 to 5x RMR. To date, the highest RFox values measured during shivering are still more than three times lower than reported for sustained exercise (1). What limits lipid utilization rate during shivering? Although the exact physiological reasons are unclear at best, we can speculate on a number of possible mechanisms that may limit RFox during shivering. For example, cold exposure is associated with reduced peripheral blood flow, which may lead to impaired fatty acid supply to shivering muscles via the circulation. In addition, as shivering intensity increases, the progressive recruitment of proportionally more type II glycolytic fibers may occur, whereas the recruitment of type I lipolitic fibers remains constant. Finally, one may also consider the influence of cold exposure on other factors responsible for controlling fuel oxidation such as circulating hormones (e.g., catecholamines), trans-membrane transporters (fatty acid transporters), and a series of intracellular metabolites (acetyl-CoA, malonyl-CoA, Ca2+, ADP, AMP, Pi, and AMPK l). Future work in this field of research should attempt to better understand the relative importance of these factors on energy substrate regulation in the cold.
Effect of precooling exercise.
The second objective of this study was to examine whether precooling exercise at 75% O2max for 15 min is sufficient to reduce CHO utilization rate by inducing neuromuscular fatigue and, thus, the recruitment of type II, fatigable muscle fibers. Recent work had shown that the recruitment of type II fatigable fibers was key in dictating fuel selection in the cold by modulating CHO oxidation rate (8). Based on previous observations during rewarming, we also expected that such changes in fuel use could occur without significant alterations in rates of heat production and/or rewarming. For example, during sustained shivering in the cold, a growing body of evidence indicates that heat production rates can be sustained independently of 1) changes in the size of glycogen reserves (or fuel mixtures being used; Refs. 9, 14, 22) or 2) whether exhaustive exercise is performed prior to cold exposure (21). In addition, during passive rewarming in hypothermic men, Neufer et al. (15) showed that rewarming rates remain unimpaired even when the size of muscle glycogen reserves are reduced prior to cooling. However, to date, the effects of precooling exercise on thermal responses and on oxidative fuel selection during rewarming had never been quantified. In the present study, results show that exercising at 75% O2max for 15 min prior to cooling has no significant effect on prod and rewarming rate (Figs. 1 and 2, Table 1). In addition, contrary to what was expected, absolute rates and relative contributions of CHO to total prod remained unchanged between Con and Pre-CE (Fig. 4, Table 1). It is likely that the precooling exercise intensity and duration selected in this study were insufficient to induce the expected neuromuscular fatigue and associated reduction in type II fiber recruitment and/or CHO availability. It still remains unclear whether more intense and longer duration exercise could modify thermal responses and the pattern of fuel selection during passive rewarming.
Conclusion.
This study shows that both CHO and lipids play substantial roles in sustaining heat production during passive hypothermic recovery (CHO above and lipids below 50%Shivpeak); a pattern unaffected by precooling exercise (75% O2max for 15 min). More importantly, it indicates that this regulation in fuel selection is modulated entirely by changes in CHO oxidation rate, which is downregulated by as much as 10-fold from the beginning to the end of rewarming. In contrast, lipid oxidation rate remains unchanged, reaching a maximum rate at very low shivering intensity. Further research should focus on establishing the exact regulatory processes involved in achieving this large upregulation of CHO utilization rate following hypothermia.
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FOOTNOTES
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Address for reprint requests and other correspondence: F. Haman, Faculty of Health Sciences, Univ. of Ottawa, 125 Univ. St, Ottawa, Ontario, Canada K1N 6N5 (e-mail: fhaman{at}uottawa.ca)
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
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Copyright © 2007 by the American Physiological Society.
TOP
ABSTRACT
METHODS
and solid line) and following precooling exercise (Pre-CE; 
and dotted line). %Shivpeak is presented in reverse order to better illustrate the rewarming process.
