Military sustained operations (SUSOPS) expose soldiers to extended periods (many days) of multiple stressors. These stressors include exertional fatigue, sleep deprivation, and energy deficits. Recently, our laboratory (18) studied U.S. Army Rangers after completion of a 61-d training period and found that immediately after Ranger School, shivering thermogenesis and peripheral heat retention were blunted, core body temperature was lower, and the risk of hypothermia was increased. However, it is not apparent how these data would translate to a short-term SUSOPS that is operationally more common. For example, the length of Ranger training leads to physiological changes (e.g., 7.4-kg weight loss and 10% subcutaneous fat loss), which affect thermoregulatory responses in the cold, but these changes are not likely to occur during a 3- to 4-d SUSOPS, which induces significant stress but not of the magnitude of Ranger School.
Previously, we have examined some of the individual SUSOPS stressors that could affect thermoregulation in the cold. These studies have generally reported small, but significant, blunting of vasoconstriction and shivering. For example, our laboratory has found that both acute and chronic exercise (1,2) before cold exposure causes core temperature to fall to a greater degree than under control conditions due to greater peripheral heat loss. We have also demonstrated that multiple cold-water exposures over a 10-h period, which can occur during these types of operations, decrease the shivering response (3). These studies, though providing information about individual stressors imbedded within SUSOPS, cannot provide information on the interaction of several factors over a short time period that could increase susceptibility to hypothermia. It is unknown what effect a typical 3- to 4-d SUSOPS in a temperate environment will have on subsequent thermoregulatory responses if a person is exposed to a cold environment.
The purpose of this study was to examine shivering and skin temperature responses during cold-air exposure after an 84-h multi-stressor military exercise and determine whether SUSOPS increases the risk of hypothermia. It was hypothesized that both shivering and vasoconstriction would be blunted after 84 h of SUSOPS, causing a greater fall in core temperature, compared with control conditions where subjects are neither sleep deprived or in negative energy balance.
Ten male soldiers volunteered to participate in this study after giving informed written consent. The appropriate Institutional Review Boards approved the study. Physical characteristics were age, 23.7 ± 1.4 (SE) yr; height, 179 ± 4 cm; mass, 85.9 ± 4.4 kg; body surface area, 2.05 ± 0.07 m2, and percent body fat, 19.0 ± 1.6%. Subjects were engaged in regular physical exercise but were not highly trained.
Height, body mass, and % body fat (dual energy x-ray absorbitometry; Model DPX-L, Lunar Corp., Madison, WI) were obtained before the experiment. Mass and % fat were also obtained after the 84-h sustained operation.
Subjects completed two cold-air tests (CAT), one at the end of a control week of tests and another at the end of an 84-h SUSOPS (see Fig. 1). Cold-air tests were conducted between 1300 and 1630 h, and control and SUSOPS cold-air tests were spaced by 1 wk. During the control week, subjects were not sleep deprived or in a negative energy balance. However, they did perform a variety of physical and cognitive tests before undergoing the CAT (Fig. 1). During the SUSOPS week, subjects performed the same physical and cognitive tests before the CAT, but overlaid on them was a limited amount of sleep and food (see below). The subjects were sitting in nylon-webbed chairs and dressed in only shorts, socks, and woolen glove liners for the CAT. Baseline values for temperature, metabolic heat production, plasma norepinephrine, and thermal sensation were collected during a 20-min period with conditions maintained at an air temperature of 25°C and 50% relative humidity (RH) with a minimal air velocity. After this, ambient temperature (Tamb) was reduced by 0.5°C·min−1 over a 30-min period, after which Tamb was maintained constant at 10°C and 50% RH for an additional 150 min. Oxygen uptake, carbon dioxide output, and minute ventilation were measured by open-circuit spirometry at minutes 30, 60, 90, 120, and 150. Rectal temperature (Tre) and mean skin temperature were obtained every minute. While exposed to the cold, the subjects were not allowed to employ behavioral thermoregulation (no unnecessary physical activity or “huddling”). All subjects consumed the cracker and spread (380 kcal) from an Army Meal-Ready-to-Eat (MRE) ∼105-min before each CAT to ensure that plasma glucose concentrations remained at normal levels throughout CAT.
The experiment consisted of 84 h (from 0600 h on day 1 to 1800 h on day 4) of physical activity with limited time allotted for sleep and energy intake was less than energy expenditure. Forty-nine hours of this time period were spent doing military-relevant field exercises. The timetable of experimental tests and activities during the control and SUSOPS weeks is presented in Fig. 1. Studies were conducted in June (average low temperature, 17°C; average high temperature, 30°C), July (low, 14°C; high, 24°C), and October (low, 7°C; high, 22°C).
Sleep was restricted by scheduling only limited blocks (1 h for each sleep period) and keeping soldiers busy performing mental and physical tasks for the majority of each 24-h day. Sleep patterns were monitored via actigraph activity monitors (Mini Mitter Co., Inc., Bend, OR, and Precision Control Design, Inc., Fort Walton Beach, FL). Sleep time was calculated by adding the time periods where no movement was detected. Actigraphy indicated that subjects slept for a total of 6.2 ± 0.4 h during the 84-h SUSOPS period.
Subjects consumed one U.S. Army MRE (range: 1100–1352 kcal) per day during the SUSOPS week, supplemented with one bagel, juice, and a piece of fruit on the morning of days 1, 3, and 4 and a candy bar on day 2. Thus, the subjects consumed an average of 1653 ± 25 kcal·d−1 (225 ± 6 g carbohydrate, 54 ± 2 g fat, and 69 ± 3 g protein). Subjects had free access to water throughout each week. The estimated mean total daily energy expenditure was ∼4500 kcal·d−1, which was based on body mass and the estimated energy cost of the activities performed.
Physical performance tests before each CAT were the same during the control and SUSOPS weeks. In brief, these tests were an obstacle course (2 runs, ∼35-s duration), two power tests (bench throw and squat jump; each ∼ 30-s duration), and a repetitive box lift (lift 20.5 kg repetitively for 10-min to a height of 1.3 m). These physical performance tasks occurred between 0930 and 1115 h with rest scheduled between tasks. Data from these performance tests will be reported in another publication. After these tests, subjects rested and consumed a portion of an MRE before undertaking the CAT.
Measurements and calculations.
Rectal temperature (Tre) was measured using a thermistor (YSI Model 400, Yellow Springs, OH) inserted 10 cm past the anal sphincter. Skin temperature (Tsk) was measured using thermistor disk sensors (Concept Engineering, Old Saybrook, CT) attached on the skin surface (right side of body) at five sites (calf, medial thigh, tricep, forearm (ventral), and subscapular). Mean weighted skin temperature (Tsk) was calculated (1) as: Tsk = 0.28·Tsubscapular + 0.14·Tforearm + 0.08·Ttriceps + 0.22·Tcalf + 0.28·Tthigh. Mean body temperature (Tb) during cold exposure was calculated (16) as follows: Tb = 0.67·Tre + 0.33·Tsk. Percent oxygen (Model S-3A, Applied Electrochemistry) carbon dioxide (model LB-2, Beckman) and volume (Tissot spirometer, Collins, Braintree, MA) were measured from a 90-s collection of the subjects’ air expired into a 150-L Douglas Bag. Metabolic heat production (, W·m−2) was estimated from V̇O2 and respiratory exchange ratio (RER) using the following equation (5): = (0.23[RER] + 0.77) ·(5.873)(V̇O2)·(60/AD), where AD is body surface area (m2). Body heat storage (⋅) or heat debt (HD) was calculated using two methods (5,16). Partitional calorimetry used the following equation: ±⋅ = − Ẇ − ⋖ − Ė − − ( + Ċ), where is the metabolic rate, Ẇ is work rate (0 in this experiment), ⋖ is the respiratory heat losses by convection and evaporation (0.08; 16), Ė is evaporative heat loss (presumed to be negligible in this experiment and set at 0), represents conductive heat loss (0 in this experiment), and + Ċ (8.3·[Tsk − Tamb];16) represents dry heat loss. Heat debt was also calculated by thermometry using the formula (16) HD = Tb·mass (kg)·specific heat of tissues (3.47 kJ·kg−1·°C−1). Heart rate (HR) was measured from three chest electrodes (CM-5 configuration) and radiotelemetered to an oscilloscope-cardiotachometer (Hewlett-Packard, Andover, MA). Thermal sensation, using a 17-point category scale, was measured before and every 30 min during CAT (6).
Whole blood samples were drawn before cold exposure (minute 0) and at minutes 30 and 175 of cold-air exposure from an indwelling 18-gauge venous catheter placed in a superficial forearm vein. Aliquots were centrifuged at 4°C to separate the plasma. Plasma samples were frozen at −40°C before analysis. Plasma glucose was measured on an auto-analyzer (Model 2300, Yellow Springs Instrument, Inc., Yellow Springs, OH). Plasma norepinephrine (NE) concentrations were determined from mass spectroscopy-gas chromatography (21).
Data were analyzed using a two-factor (experimental trial × time) repeated-measures ANOVA. When significant F-ratios were calculated, paired comparisons were made post hoc using a Newman-Keuls test. The slope and threshold (to determine shivering sensitivity and onset, respectively) of each individual’s Tb versus Δ relationship were determined by least squares linear regression with the threshold (onset of shivering) defined as the Tb at a Δ of 0. Any increase in Δ above 0 denotes shivering thermogenesis. The Tb vs Δ relationship and the body composition variables between control and SUSOPS were analyzed using dependent t-tests. The level of significance for differences reported is P < 0.05. Values are mean ± SE.
Body mass (85.9 ± 4.4 to 82.5 ± 4.2 kg;P < 0.0001), % body fat (19.0 ± 1.6 to 18.0 ± 1.8%;P < 0.03), and fat-free mass (69.3 ± 3.3 to 67.3 ± 3.1 kg;P < 0.001) all declined as a result of SUSOPS.
Temperature regulation responses.
Metabolic heat production, an index of shivering thermogenesis, was significantly lower (P < 0.05) at minute 30 during the SUSOPS trial compared with the control trial (Fig. 2A). Metabolic heat production had a tendency to remain lower, although not statistically, through to minute 90 in SUSOPS. Interestingly, metabolic heat production was significantly higher (P < 0.05) in SUSOPS at minute 150, compared with the control trial. Oxygen consumption had the same pattern of response as metabolic heat production. RER was lower in SUSOPS (0.76 ± 0.04) versus control (0.87 ± 0.06) before the CAT and was generally 0.04–0.08 lower throughout the CAT in SUSOPS versus control. The relationship of the mean body temperature to the change in metabolic heat production is shown graphically in Figure 2B. The onset of shivering occurred at a lower mean body temperature (P < 0.05) in the SUSOPS (34.8 ± 0.2°C) trial compared with the control (35.8 ± 0.2°C) trial. The slope of the Tb-Δ relationship was greater (P < 0.05) in the SUSOPS (−39.7 ± 8.1 W·m−2·°C−1) trial compared with the control (−17.7 ± 2.4 W·m−2·°C−1) trial. These data indicate that shivering started later in SUSOPS, but once initiated, shivering increased to a greater extent per °C fall in mean body temperature in the SUSOPS trial.
Rectal temperatures were similar between SUSOPS (37.25 ± 0.08°C) and control (37.27 ± 0.09°C) trials at minute 0 of the CAT. During the cold-air test, core temperature was significantly lower (P < 0.05) during the last 2 h of cold exposure in SUSOPS compared with the control trial (Fig. 3A). Heat debt, calculated using thermometric methods, was significantly greater in the first 90 min of exposure in SUSOPS (Fig. 3B). However, partitional calorimetry analysis indicated that heat debt was not significantly different (P > 0.05) between SUSOPS and control trials after 150 min of cold exposure. Mean skin temperature responses, an index of vasoconstriction although not as precise as measuring blood flow, were significantly (P < 0.05) lower in the SUSOPS, versus control trial, at minutes 30, 60, and 90, with no differences at any other time period (Fig. 4A). The Tre-Tsk gradient during the CAT is shown in Fig. 4B. During the CAT after SUSOPS, the Tre-Tsk gradient was larger (P < 0.05) than during the control trial after 30, 60, and 90 min. Heart rates ranged from 68 to 74 beats·min−1 throughout the CAT and were not different between trials. Subjects also did not rate their thermal sensations any differently between SUSOPS and control trials.
Plasma concentrations for glucose and norepinephrine are presented in Table 1. There were no significant differences within or between trials for plasma glucose and these remained within normal levels. Plasma norepinephrine concentrations increased as a result of cold exposure in both trials, but there were no significant differences between SUSOPS and control before, at minute 30, or at the end of cold exposure.
This study examined the effects of an 84-h military sustained operations exercise that is operationally realistic, without the comparably large changes in body fat and tissue insulation observed after 61 d of U.S. Army Ranger training (18). The principal finding in this study was the greater fall in core temperature during cold-air exposure after 84 h of SUSOPS, compared with the control trial, although the vasoconstrictor responses were not impaired, as hypothesized, after SUSOPS. Several factors might explain the lower core temperature after SUSOPS. One possibility is a blunted shivering response indicated by the delayed onset of shivering after SUSOPS, compared with rested conditions. Another possibility is that during cold-air exposure after SUSOPS, there was a redistribution of heat from the core to the periphery due to a higher thermal gradient, thereby causing a greater fall in core temperature.
Three primary stressors are present during SUSOPS that may impact shivering thermogenesis. They are sleep deprivation, negative energy balance, and exertional fatigue caused by previous exercise. Prior exercise was ruled out as a mechanism for the delayed shivering response in this study because we have previously demonstrated this stressor does not blunt shivering thermogenesis during subsequent cold exposure (1,2). Furthermore, because the physical performance test battery was the same before each cold test, the effect of acute exercise was the same in both the control and SUSOPS trials. Thus, it is concluded that one of the other scenarios affected shivering after the 84-h SUSOPS: sleep deprivation alone, negative energy balance alone, or the combination of sleep deprivation and negative energy balance.
Volunteers in this study slept for ∼6 h over 3.5 d and thus were sleep deprived. Recent data support the idea that sleep deprivation, in combination with negative energy balance, impairs the shivering response. Young et al. (18) found the shivering response was not initiated until a lower mean body temperature was achieved after enduring a multi-stressor training school before beginning their initial experimental cold exposure. However, it is difficult to attribute the changes in shivering thermogenesis solely to sleep deprivation in that study due to the multiple stressors present. Studies examining sleep deprivation, independently, have generally observed no effect on core temperature responses to cold exposure, but the methodologies and study protocols preclude definitive conclusions. Fiorica et al. (4) observed no effect on shivering and vasoconstriction after 82 h of sleep deprivation. However, subjects did not serve as their own controls, and baseline core temperature in their control group progressively increased over 4 d, despite testing at the same time of day, which confounded data interpretation. Kolka et al. (7) measured thermoregulatory responses during exercise in cold air (0°C) after 50 h of sleep deprivation and observed impairments in heat dissipation mechanisms during exercise that resulted in greater heat storage and elevated core temperatures. Thus, that study (7) did not examine physiological adjustments (shivering, vasoconstriction) needed to prevent a fall in core temperature. Savourey and Bittel (14) utilized a 27-h period of sleep deprivation, which was likely too short a time to cause a treatment effect on core temperature responses. Interestingly, in contrast to our finding of a delayed shivering response, Savourey and Bittel (14) found that sleep deprivation increased the sensitivity of the shivering response, i.e., shivering began earlier. However, that study used a subjective measure of shivering to determine onset as opposed to an objective measure such as changes in metabolic heat production. Finally, Landis et al. (9) found that one night of sleep deprivation lowered forearm blood flow responses to an initial fall of skin temperature from 35°C to 32°C (suggestive of enhanced vasoconstriction), but when skin was heated to 38°C and then cooled to 32°C, esophageal temperature declined more rapidly after sleep deprivation, although forearm blood flow was not altered and could not explain the change in core temperature. Thus, sleep-deprivation effects on thermoregulatory responses to cold are unclear. Sleep deprivation may play a role by changing the set-point temperature at which physiological responses are regulated. After both a multi-stressor scenario (13) and sleep deprivation alone (7), core temperature was lowered ∼0.5°C at rest before beginning exercise, but neither of these studies provides conclusive evidence of a reduced set point.
Volunteers in this study had a 2800 kcal·d−1 caloric deficit. Previous studies suggest that underfeeding, despite normal glucose concentrations, impairs thermoregulatory responses to cold (10,11,18). In one study (18), it is difficult to discern whether underfeeding was responsible for the blunted shivering response because there were large changes in body composition. In the other two studies (10,11) subjects consumed no food for 2 d before testing and changes in the core temperature-metabolic rate relationship were measured after this 48-h fasting period. Unlike the changes seen in the present study (a decrease in the shivering onset, i.e., a temperature threshold change along with an increased gain), Macdonald and colleagues (10) found a reduced gain (sensitivity) in the metabolic rate-core temperature relationship after 2 d of fasting in men. Similarly, a decline in the metabolic rate response to cold after fasting was observed in women after 48-h food deprivation (11). The different shivering responses to the underfeeding stress between these studies and SUSOPS may be due to the type of underfeeding. In SUSOPS, subjects ate (including 2 h before exposure) but were underfed relative to their energy expenditure, whereas in the other two studies, subjects were sedentary and consumed no food at all. One possibility is that the diminished metabolic heat response is due to an elevated basal norepinephrine level that has been observed after either 48 h of fasting (11) or a combination of sleep loss, underfeeding, and exertional fatigue (18), which may lead to a down-regulation of beta-adrenergic receptors (12). However, our SUSOPS scenario did not increase resting plasma norepinephrine values.
Interestingly, SUSOPS appeared to enhance the vasoconstrictor response (based on lower Tsk values, not on direct measurement of blood flow and qualitatively higher plasma norepinephrine values) to cold exposure at the same time it caused lower core temperatures and a delayed shivering response. This pattern of response is similar to the insulative acclimation that occurs after multiple cold-water immersions (17). The increased gradient between the core and skin in SUSOPS would favor heat transfer/heat redistribution from the core to the subcutaneous muscle shell and maintain muscle blood flow to the periphery (19), but with an insulative acclimation, not as much heat would be lost to the environment. This hypothesis is also supported by the result that heat debt, determined by partitional calorimetry, was not different between the SUSOPS and Control trials. Tikuisis et al. (15) state that cold acclimation can occur but would not be manifested in a change in body heat storage if changes in heat production and heat conservation occur simultaneously as occurred after SUSOPS. In contrast to our finding of a more pronounced vasoconstrictor response, previous studies have shown that the vasoconstrictor response to cold is attenuated after either Ranger School (18), 48 h of fasting (10,11) and 27 h of sleep deprivation (14). Another potential reason for our findings is that the subjects “trained” while they performed 21–22 h of physical work per day. Young et al. (20) have shown the vasoconstrictor response to cold is enhanced after endurance training. Furthermore, Kollias and Buskirk (8) also reported that aerobic training enhanced the vasoconstrictor response to cold air. Those studies trained their subjects for 8–9 wk with 35–51 actual training hours completed. Perhaps the continuous physical activity of this SUSOPS scenario mediated an enhanced vasoconstriction in the same manner because the numbers of hours that the subjects were actually doing physical exercise approached that in these training studies and our subjects were not highly trained athletes upon initiation of the study. In Ranger School, the long period of exertional fatigue likely did not lead to a training effect per se, but more likely, overtraining. In addition, Army Rangers lost a substantial amount of subcutaneous fat, which would cause skin temperatures to be elevated upon cold exposure.
In summary, this study was the first to demonstrate that short-term (3.5 d) sustained activity with sleep loss and negative energy balance shifts the mean body temperature threshold for the onset of shivering thermogenesis. However, once body temperature began to fall after the SUSOPS trial, shivering was vigorously activated to defend against large declining rectal temperature. Lower core temperatures after SUSOPS were also associated with an enhanced vasoconstrictor response and no change in heat debt, suggesting SUSOPS induces physiological changes that may cause a pattern of response similar to insulative acclimation. The results of this short-term SUSOPS differed from that observed after 61 d of Ranger School in that the difference in core temperature between the control and SUSOPS trials at the end of cold exposure was less than that observed after Ranger School (1.0°C) and Ranger students had blunted vasoconstrictor responses. Future studies need to further define the relative roles of sleep deprivation and negative energy balance on thermoregulatory responses to cold exposure.
We would like to thank the volunteers who endured all the stresses of this experiment. Your dedication to this study was outstanding and we appreciate all that you did.
Special thanks to the following individuals for their technical support: Janet Staab, Scott Robinson, Chris Kesick, Dan Ditzler, Leslie Levine, Catherine O’Brien, Sam Cheuvront, Chris Donajkowski, Katherine Blais, Frank Chivera, Christopher Houck, John Kremer, Joshua Morgan, James Moulton, Anthony Rogers, Thad Ross, Matthew Stamm, Ronald Ulrigg, and Kevin Warren. Thanks also to Dr. Michael Sawka and Dr. Andrew Young for their helpful comments.
The views, opinions, and/or findings in this report are those of the authors and should not be construed as official Department of the Army position, policy, or decision unless so designated by other official designation. Human subjects participated in these studies after giving their free and informed voluntary consent. Investigators adhered to AR 70-25 and USMRDC Regulation 70-25 on Use of Volunteers in Research.
1. Castellani, J. W., A. J. Young, D. W. Degroot, et al. Thermoregulation during cold exposure after several days of exhaustive exercise. J. Appl. Physiol. 90: 939–946, 2001.
2. Castellani, J. W., A. J. Young, J. E. Kain, A. Rouse, and M. N. Sawka. Thermoregulation during cold exposure: effects of prior exercise. J. Appl. Physiol. 87: 247–252, 1999.
3. Castellani, J. W., A. J. Young, M. N. Sawka, and K. B. Pandolf. Human thermoregulatory responses during serial cold-water immersions. J. Appl. Physiol. 85: 204–209, 1998.
4. Fiorica V., E. A. Higgins, P. F. Iampietro, M. T. Lategola, and A. W. Davis. Physiological responses of men during sleep deprivation
. J. Appl. Physiol. 24: 167–176, 1968.
5. Gagge, A. P., and R. R. Gonzalez. Mechanisms of heat exchange: biophysics and physiology. In: Handbook of Physiology, Section 4, Environmental Physiology, M. J. Fregly and C. M. Blatteis (Eds.). New York: Oxford University Press, 1996, pp. 45–84.
6. Gagge, A. P., J. A. J. Stolwijk, and J. D. Hardy. Comfort and thermal sensations and associated physiological responses at various ambient temperatures. Environ. Res. 1: 1–20, 1967.
7. Kolka, M. A., B. J. Martin, and R. S. Elizondo. Exercise in a cold environment after sleep deprivation
. Eur. J. Appl. Physiol. 53: 282–285, 1984.
8. Kollias, J., R. Boileau, and E. R. Buskirk. Effects of physical condition in man on thermal responses to cold air. Int. J. Biometeorol. 16: 389–402, 1972.
9. Landis, C. A., M. V. Savage, M. J. Lentz, and G. L. Brengelmann. Sleep deprivation
alters body temperature dynamics to mild cooling and heating not sweating threshold in women. Sleep 21: 101–108, 1998.
10. Macdonald, I. A., T. Bennett, and R. Sainsbury. The effect of a 48 h fast on the thermoregulatory responses to graded cooling in man. Clin. Sci. 67: 445–452, 1984.
11. Mansell, P. I., and I. A. Macdonald. Effects of underfeeding and of starvation on thermoregulatory responses to cooling in women. Clin. Sci. 77: 245–252, 1989.
12. Opstad, P. K. Adrenergic desensitization and alterations in free and conjugated catecholamines during prolonged physical strain and energy deficiency. Biog. Amines 7: 625–639, 1990.
13. Opstad, P. K., and R. Bahr. Reduced set-point temperature in young men after prolonged strenuous exercise combined with sleep and energy deficiency. Arct. Med. Res. 50: 122–126–, 1991.
14. Savourey, G., and J. Bittel. Cold thermoregulatory changes induced by sleep deprivation
in men. Eur. J. Appl. Physiol. 69: 216–220, 1994.
15. Tikuisis, P., D. H. Mccracken, and M. W. Radomski. Heat debt during cold air exposure before and after cold water immersions. J. Appl. Physiol. 71: 60–68, 1991.
16. Vallerand, A. L., G. Savourey, and J. H. M. Bittel. Determination of heat debt in the cold: partitional calorimetry vs. conventional methods. J. Appl. Physiol. 72: 1380–1385, 1992.
17. Young, A. J. Homeostatic responses to prolonged cold exposure: human cold acclimatization. In: Handbook of Physiology, Section 4, Environmental Physiology, M. J. Fregly and C. M. Blatteis (Eds.). New York: Oxford University Press, 1996, pp. 419–438.
18. Young, A. J., J. W. Castellani, C. O’Brien, et al. Exertional fatigue
, sleep loss, and negative energy balance
increase susceptibility to hypothermia. J. Appl. Physiol. 85: 1210–1217, 1998.
19. Young, A. J., S. R. Muza, M. N. Sawka, R. R. Gonzalez, and K. B. Pandolf. Human thermoregulatory responses to cold air are altered by repeated cold water immersion. J. Appl. Physiol. 60: 1542–1548, 1986.
20. Young, A. J., M. N. Sawka, L. Levine, et al. Metabolic and thermal adaptations from endurance training in hot or cold water. J. Appl. Physiol. 78: 793–801, 1995.
21. Zamecnik, J. Quantitation of epinephrine, norepinephrine
, dopamine, metanephrine, and normetanephrine in human plasma using negative ion chemical ionization GC-MS. Int. J. Spectroscopy Soc. Can. 42: 106–112, 1997.
Keywords:©2003The American College of Sports Medicine
FATIGUE; NEGATIVE ENERGY BALANCE; NOREPINEPHRINE; SHIVERING; SLEEP DEPRIVATION