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J Appl Physiol 94: 1039-1044, 2003. First published November 8, 2002; doi:10.1152/japplphysiol.00720.2002
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Vol. 94, Issue 3, 1039-1044, March 2003

Metabolic, thermoregulatory, and perceptual responses during exercise after lower vs. whole body precooling

Andrea T. White1, Scott L. Davis1, and Thad E. Wilson2

1 Department of Exercise and Sport Science, University of Utah, Salt Lake City, Utah 84112; and 2 Department of Biomedical Sciences, Southwest Missouri State University, Springfield, Missouri 65804


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The purpose of this investigation was to compare the thermoregulatory, metabolic, and perceptual effects of lower body (LBI) and whole body (WBI) immersion precooling techniques during submaximal exercise. Eleven healthy men completed two 30-min cycling bouts at 60% of maximal O2 uptake preceded by immersion to the suprailiac crest (LBI) or clavicle (WBI) in 20°C water. WBI produced significantly lower rectal temperature (Tre) during minutes 24-30 of immersion and lower Tre, mean skin temperature, and mean body temperature for the first 24, 14, and 16 min of exercise, respectively. Body heat storage rates differed significantly for LBI and WBI during immersion and exercise, although no net differences were observed between conditions. For WBI, metabolic heat production and heart rate were significantly higher during immersion but not during exercise. Thermal sensation was significantly lower (felt colder) and thermal discomfort was significantly higher (less comfortable) for WBI during immersion and exercise. In conclusion, WBI and LBI attenuated Tre increases during submaximal exercise and produced similar net heat storage over the protocol. LBI minimized metabolic increases and negative perceptual effects associated with WBI.

body temperature; water immersion; metabolic heat production; body heat storage


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

EXERCISE-INDUCED INCREASES in metabolic heat load considerably challenge temperature homeostasis and may ultimately impair physical work performance (20). Precooling is a strategy used to decrease the temperature of a large tissue mass, thereby creating a "heat sink" before exercise and/or environmentally induced thermal exposure. The beneficial effects of precooling include thermoregulatory, circulatory, and performance benefits (4, 12, 16, 21). By creating a greater body heat storage (S) capacity, precooling delays the onset of heat dissipation mechanisms by lengthening the time required to reach sweat threshold (21). In effect, precooling increases the reserve for heat storage, allowing more work to be accomplished before a given increase in core temperature (Tc) is reached (25, 26). As a consequence of reducing or delaying the need to dissipate heat, precooling may result in less competition for blood flow between the skin and working muscles during exercise in the heat, thus resulting in less cardiovascular strain.

Several investigators have demonstrated clear benefits of precooling as a means to improve exercise performance in healthy individuals (4, 12, 16, 21), whereas other investigators have reported that precooling had no effect or actually decreased performance (2, 3, 7, 15). Lower body cool water immersion before physical activity has also been helpful in minimizing heat-related decrements in physical function and fatigue in heat-sensitive individuals with multiple sclerosis (MS) (25). Discrepancies in the precooling literature are likely due to varying cooling methods and experimental ambient conditions and to differing exercise loads and population characteristics.

The most effective precooling strategy would maximize the physiological benefits of decreased body temperature (Tb) (creation of a heat sink, delay of heat dissipation mechanisms) while minimizing the disadvantages of an "adverse" environment [increased metabolic heat production (M), physical discomfort]. The purpose of this investigation was to compare the effects of two water immersion precooling techniques on thermoregulatory and metabolic responses during exercise-induced heat stress. We hypothesized that lower body immersion (LBI), a treatment that our laboratory has shown to be well tolerated, would be as effective a precooling treatment as whole body immersion (WBI) by delaying the time until a given temperature increase is reached during subsequent submaximal exercise (25). Although there have been several studies that have examined thermoregulatory responses to whole body precooling as well as physiological responses to maximal exercise after precooling, we are aware of no direct comparisons of WBI and LBI precooling techniques on thermoregulatory and metabolic responses during a constant submaximal work rate. A submaximal work rate may more practically represent daily activities for average individuals, as opposed to maximal trials performed on highly fit individuals in stressful environments. Furthermore, LBI represents a more practical and accessible method of precooling for individuals with mobility constraints and very little tolerance for increases in Tc, such as many MS patients.


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Subjects

Eleven healthy men (subject characteristics in Table 1) volunteered to participate. Data were collected in a dry temperate climate (~22°C, ~20% relative humidity, and elevation ~1,300 m). The protocol was approved by the University of Utah Human Subjects Review Board, and all subjects provided written, informed consent.

                              
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Table 1.   Subject characteristics

Measurements

Temperature. Skin temperature (Tsk) was measured by attaching banjo-type surface temperature probes (Yellow Springs Instruments) to the calf, thigh, chest, and arm. Rectal temperature (Tre) was measured via general use thermistor (Yellow Springs Instruments) inserted 10 cm past the anal sphincter. All temperature probes were connected to a digital thermistor readout unit (Digitec).

Metabolic and cardiovascular. Heart rate was monitored continuously by using a heart rate monitor (Polar). Oxygen consumption (VO2) was measured by using indirect calorimetry via an automated metabolic cart (ParvoMedics).

Participant perception. The Borg 6-20 point scale of rating of perceived exertion (RPE) was used to determine the participants' perception of exercise intensity. Nine-point thermal sensation (0 = very cold to 8 = very hot), five-point thermal discomfort (1 = comfortable to 5 = intolerable), and five-point sweating sensation scales (1 = not at all to 5 = maximally) were used to determine the participants' thermal comfort during the protocol (8).

Calculations

Temperature calculations. Four Tsk sites were used and weighted according to the following equation: mean Tsk = 0.3(Tsk chest + Tsk arm) + 0.2(Tsk thigh + Tsk calf) (23). Mean Tb was calculated via the following weighting system: mean Tb = (0.65 · Tc) + (0.35 · meanTsk), where Tc is indexed by Tre (5).

S. S was estimated via the following formula: S = 0.97 · mass · (Delta Tb/Delta t)/AD, where Delta Tb is the change in mean body temperature, /Delta t is the change in time, and AD is body surface area (in m2) (13).

M. M was calculated according to the following formula (10): M = [0.23(R) + 0.77] · (5.873/VO2) · (60/AD), where R is respiratory exchange ratio.

Protocol

Each participant reported to the laboratory three times over the course of the experiment: for a pretest session and for two randomly ordered precooling trials of either LBI or WBI. Each session was separated by 1 wk and was performed at the same time of day. During the pretest session, physical characteristics were measured and subjects performed a maximal graded exercise test on a Monarch cycle ergometer to determine maximal O2 uptake (VO2 max). The work rate corresponding to 60% VO2 max was calculated and used for the subsequent submaximal exercise trials described below.

Each precooling trial consisted of four 30-min phases: baseline, immersion, exercise, and recovery. Each phase was separated by 10 min for subject and instrument transition. During the baseline period, each subject, dressed in shorts and shoes, rested on a reclining chair in a thermoneutral environment (22°C, 20% relative humidity). During WBI and LBI, subjects were seated in cool water (20°C), immersed to the level of the clavicle and iliac crest, respectively. The exercise phase consisted of cycling at a work rate corresponding to 60% VO2 max in an environmental chamber at 30.3 ± 0.2°C and 31.9 ± 0.7% relative humidity. After exercise, subjects rested in a semireclined position in a thermoneutral environment throughout the recovery phase.

Statistics

Descriptive statistics (means ± SE) are reported for dependent variables. Two-way (treatment vs. time) ANOVAs with repeated measures were used to evaluate thermoregulatory responses during each experimental phase. When significant main effects were observed, post hoc Tukey's analyses were performed to determine where treatment and/or time differences existed.


    RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Thermoregulatory Responses

During immersion, significant time and time × treatment (LBI vs WBI) effects were observed for Tre (P < 0.001). Post hoc analysis indicated that, during WBI, Tre was significantly lower than baseline at minutes 24-30 (Fig. 1).


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Fig. 1.   Rectal temperature (Tre) during lower body (LBI) and head-out whole body (WBI) immersion in 20°C water. Bracket indicates significant differences between conditions.

During the exercise phase, Tre, mean Tsk, and mean Tb increased significantly (P < 0.001) over time for both LBI and WBI conditions. Significant treatment differences were also observed for Tre (P < 0.002), mean Tsk (P < 0.034), and mean Tb (P < 0.009) throughout exercise. After WBI, Tre was significantly lower than LBI for the first 24 min of exercise (P < 0.05, post hoc Tukey's test). Mean Tsk and mean Tb were also lower during exercise after WBI compared with LBI, but the treatment differences were no longer significant after 14 min (mean Tsk) and 16 min (mean Tb) of exercise. S rates were significantly different between WBI and LBI during immersion (P < 0.002) and exercise (P < 0.003) phases (Fig. 2). However, net changes in S over the entire experimental protocol did not differ significantly between conditions.


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Fig. 2.   Body heat storage during immersion, exercise, and net protocol (combined immersion and exercise phases) for LBI and WBI precooling treatments. NS, not significant.

Metabolic Responses

There were no significant differences in M or heart rate between LBI and WBI during baseline or recovery phases. However, during immersion, M was nearly twice as high for WBI compared with LBI (132 ± 15 vs. 71 ± 5 W/m2, respectively, at minute 30; P < 0.01) (Table 2). Heart rate was also significantly higher during WBI compared with LBI (P < 0.05) (Table 2). No significant treatment (WBI vs. LBI) differences were observed for M or heart rate during exercise (Table 3).

                              
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Table 2.   Effect of lower body and head-out whole body cold-water immersion on core body temperature, heart rate, metabolic heat production, thermal sensation, and thermal discomfort at 10, 20, and 30 min of immersion


                              
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Table 3.   Effect of lower body and head-out whole body precooling on heart rate, rating of perceived exertion, metabolic heat production, sweat sensation, thermal sensation, and thermal discomfort during submaximal exercise at a workload corresponding to 60% VO2max

Subjective Responses

There were no differences between treatments for sweat sensation, thermal sensation, or thermal discomfort during baseline and recovery phases. Thermal sensation throughout immersion was significantly lower (felt colder) during WBI compared with LBI (P < 0.05). Similarly, thermal discomfort was significantly higher (less comfortable) for WBI throughout immersion (P < 0.005) (Table 2).

During the exercise phase, sweat sensation scores increased significantly after both treatments. After WBI, sweat sensation scores were significantly lower than those after LBI through 20 min of exercise (P < 0.05). Treatment differences were no longer apparent at 30 min for sweat sensation (Table 3).

There were no significant treatment differences in RPE scores during exercise. However, RPE scores increased significantly (P < 0.05) during exercise after both precooling treatments.


    DISCUSSION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Our laboratory has previously demonstrated, in a small number of MS patients, that LBI precooling is tolerable, effective, and practical for use (25). Because many MS patients experience symptom worsening with small (0.5°C) increases in internal temperature, an effective precooling technique could have profound effects on preserving physical function during conditions that increase internal temperature. In turn, precooling could facilitate greater participation in health-enhancing activities such as exercise and rehabilitation programs (1, 22).

To date, the relative effectiveness of WBI and LBI precooling on thermoregulatory and metabolic responses during submaximal exercise has not been investigated. A direct comparison of the effects of these two immersion techniques during subsequent submaximal exercise performance was necessary to prescribe appropriate precooling recommendations for clinical populations.

The present study demonstrated that LBI and WBI precooling techniques 1) prevented excessive Tre increases during subsequent submaximal exercise by lowering initial Tc and 2) resulted in similar net S changes over the experimental protocol. WBI produced a greater cooling effect compared with LBI, as demonstrated by significantly lower Tre during the first 24 min of exercise. However, this larger cooling effect was accompanied by higher M and less thermal comfort during cooling. LBI also produces significant physiological benefits but minimizes the metabolic and perceptual effects resulting from WBI.

During 30 min of cool-water immersion, heat in the body core was presumably conserved by peripheral vasoconstriction in the immersed extremities, reducing the skin-to-water temperature gradient. The magnitude of heat loss during WBI was greater due to the larger skin surface area exposed to cooling, as well as greater heat flow from the trunk areas (14). This was demonstrated by a significant reduction in Tre compared with baseline during the last 6 min of immersion. By themselves, these observations would appear to suggest that WBI is a superior precooling method. However, the effectiveness of both precooling techniques became more evident during subsequent exercise when blood circulating through the cooled areas produced significant initial reductions in Tre.

During WBI, M increased significantly to a value nearly twice that achieved during LBI (Table 2). This corresponds well to the afferent stimulation provided by the two immersion techniques (11), with WBI exposing approximately twice as much skin surface area. In cold air, increasing M may preserve core temperature but cannot offset heat loss in cool or cold water (6, 17). M during LBI was somewhat higher than reported during thermoneutral conditions (~73 W/m2 during LBI compared with ~40-49 W/m2) (19). Using the Weir (24) equation, Lee et al. (17) reported slightly lower M during resting immersion to the hip and neck in 15 and 25°C than was observed in the present study. The differences between hip- and neck-level immersion at 15 and 25°C were ~140 and ~40 W/m2, respectively (17). At 15°C, increased M during neck-level immersion was likely due to greater thermal afferent input and shivering induced by larger decreases in Tc. In the present study, a difference of ~60 W/m2 between WBI and LBI was observed, which is consistent with the findings of Lee et al. for the 25°C immersion condition.

Smaller increases in M during LBI may be beneficial for some clinical populations. For example, MS patients have limited physical capacity for work due to accumulated disability and abnormal fatigue, which is worsened by increased Tb. The increase in M induced by WBI is somewhat counterproductive to the purpose of precooling for individuals with MS, which is to facilitate achievement of physical activities.

Differential responses in temperature and metabolism between LBI and WBI resulted in significant differences in S rates over the course of the experiment. WBI resulted in a significantly greater rate of heat loss during immersion and a significantly greater positive S rate during exercise compared with LBI (Fig. 2). However, the net effect of both immersion techniques was essentially the same when the negative and positive changes were balanced for the entire experiment. This is in contrast to our laboratory's previous work using the same exercise protocol preceded by either LBI precooling or no cooling (25). Although precooling resulted in greater rates of negative and positive S during immersion and exercise, respectively, net S over the course of the experiment was significantly greater for the no-cooling condition (25). This higher heat gain corresponded to significantly higher Tre in the noncooled condition for the duration of exercise.

LBI and WBI produced different thermoregulatory responses during water immersion, but both treatments produced a significant reduction in Tre during the first minutes of exercise, although WBI resulted in a significantly larger reduction in Tre. In practical terms, both WBI and LBI treatments provided an effective heat sink to lengthen the time to reach an increase in Tre of 0.5°C above baseline. During exercise, an overall Tre increase of ~1°C was observed after both WBI and LBI. This magnitude of change in Tre is consistent with other studies that have utilized the same relative workload (25, 26). Because precooling does not appear to alter the slope of temperature increases during 30 min of submaximal exercise (Fig. 3), the reduction in Tre produced by precooling largely determines the net Tre increase above normal baseline temperature. In a study that compared LBI precooling to no cooling in MS patients, LBI produced an afterdrop of 0.8°C (25). As in the present study, 30 min of exercise at 60% VO2 max resulted in overall Tre increases of 0.9°C for LBI and noncooled conditions. During the noncooled trial, a Tre of 0.5°C above baseline was reached at 22 min of exercise. In contrast, LBI produced no net increase in Tre at the end of 30 min of exercise (25).


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Fig. 3.   Tre (top), mean skin temperature (Tsk; middle), and mean body temperature (Tb; bottom) responses during submaximal cycling exercise after LBI and WBI in 20°C water. Brackets indicate significant differences between conditions.

Similarly, in healthy men, LBI precooling produced a reduction in Tre of 1°C, noted by 6-8 min of exercise at 60% VO2 max. The time required to produce a 0.5°C Tre increase was 33 min for the precooled condition compared with 15 min for the noncooled condition (26). In the present study, WBI and LBI produced similar delays in the time to increase Tre by 0.5°C (24 and 28 min of exercise for LBI and WBI, respectively). Variability in the studies cited above was due to differing immersion temperatures (16°C for Ref. 26, and 20°C for the present study) and ambient conditions during exercise (21-23°C for Ref. 26, and 30°C for the present study). Immersion temperature for the present study was based on observations suggesting WBI in 16°C water would not be tolerated well (4, 18).

Throughout WBI, thermal sensation scores were significantly lower (colder) and thermal discomfort scores were significantly higher (more uncomfortable) compared with LBI. Although the differences in thermal comfort and thermal sensation were statistically significant, one might question the practical interpretation of a one-point difference on these perceptual scales. However, this small perceptual benefit combined with the greater accessibility of LBI (which can be accomplished in a regular bath tub by using tap water) may indicate the use of LBI precooling as a practical means to delay heat stress during subsequent physical activity, be it exercise or activities of daily living.

During exercise, subjective measures assessed after WBI and LBI were similar. There were no treatment differences in RPE throughout exercise. This observation is consistent with Booth et al. (4) and Wilson et al. (26), but it differs from that of White et al. (25). This discrepancy is likely due to differing subject populations. The latter study examined MS patients who experienced symptom worsening with increased Tc. Greater difficulty with motor control and other neurological signs may explain the increased perception of effort.

Sweat sensation was significantly lower after WBI through minute 20 of exercise, suggesting that sweat production may have been reduced. This is consistent with our laboratory's previous work that demonstrated that precooling significantly delayed onset of sweating and led to decreased sweat loss during 60 min of submaximal exercise (26).

Limitations

In the present study, mean Tb was estimated by the Burton equation (5), wherein Tre is given the weighting factor of 0.65, and mean Tsk is given the weighting factor of 0.35. The Burton equation was used because of the higher weighting of Tsk, because during a cold stress, especially during water immersion, skin temperature is more important in thermal balance. Although other weighting systems (e.g., 0.8 · Tre and 0.2 · mean Tsk or 0.9 · Tre and 0.1 · mean Tsk) used in the literature slightly alter the calculated mean Tb value, using them would not affect the interpretation of the data comparing the two treatments.

Water immersion to the level of the neck alters body fluid balance and cardiovascular responses while in the water (9). However, we did not observe the characteristic baroreceptor-mediated decrease in heart rate due to increases in central blood volume during water immersion to the level of the neck because of the overriding effect of the 20°C water on increasing M. It is therefore unlikely that differences in depth of water immersion per se had profound effects on the thermal or cardiovascular responses during exercise after water immersion.

Conclusion

In conclusion, WBI and LBI attenuated Tc increases during submaximal exercise by producing a reduction in Tre, with WBI producing a slightly greater cooling effect. Both treatments produced similar net S over the entire protocol. However, LBI minimized metabolic increases and negative perceptual effects associated with WBI. Because of its similar thermal effect, reduced metabolic and perceptual effects, and ease of use, LBI should be the preferred precooling method for patient populations that demonstrate impaired physical function with increased internal temperature.


    ACKNOWLEDGEMENTS

We acknowledge the technical support of Bob Shafer. We also thank all of the study participants for their time and cooperation.


    FOOTNOTES

This study was supported in part by a grant from the National Multiple Sclerosis Society.

Address for reprint requests and other correspondence: A. T. White, Dept. of Exercise and Sport Science, University of Utah, 250 S. 1850 E., Rm. 241, Salt Lake City, UT 84112-0920 (E-mail: andrea.white{at}health.utah.edu).

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.

First published November 8, 2002;10.1152/japplphysiol.00720.2002

Received 5 August 2002; accepted in final form 31 October 2002.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1.   Baker, DG. Multiple sclerosis and thermoregulatory dysfunction. J Appl Physiol 92: 1779-1780, 2002.

2.   Bergh, U, and Ekblom B. Physical performance and peak aerobic power at different body temperatures. J Appl Physiol 46: 885-889, 1979.

3.   Bolster, DR, Trappe SW, Short KR, Scheffield-Moore M, Parcell AC, Schulze KM, and Costill DL. Effects of precooling on thermoregulation during subsequent exercise. Med Sci Sports Exerc 31: 251-257, 1999.

4.   Booth, J, Marino F, and Ward JJ. Improved running performance in hot humid conditions following whole body precooling. Med Sci Sports Exerc 29: 943-949, 1997.

5.   Burton, AC. Human calorimetry. J Nutr 9: 261-280, 1935.

6.   Castellani, JW, Young AJ, Sawka MN, and Pandolf KB. Human thermoregulatory responses during serial cold-water immersions. J Appl Physiol 85: 204-209, 1998.

7.   Drust, B, Cable NT, and Reilly T. Investigation of the effects of the pre-cooling on the physiological responses to soccer-specific intermittent exercise. Eur J Appl Physiol 81: 11-17, 2000.

8.   DuBois, AB, Harb ZF, and Fox SH. Thermal discomfort of respiratory protective devices. Am Ind Hyg Assoc J 51: 550-554, 1990.

9.   Epstein, Y, Shapiro Y, and Brill S. Role of surface area-to-mass ratio and work efficiency in heat intolerance. J Appl Physiol 54: 831-836, 1983.

10.   Gagge, AP, and Gonzalez RR. Mechanisms of heat exchange: biophysics and physiology. In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc, 1996, vol. I, p. 45-84, sect. 4, chapt. 4.

11.   Hensel, H. Thermoreceptors. Annu Rev Physiol 36: 233-249, 1974.

12.   Hessemer, V, Langusch D, Bruck LK, Bodeker RH, and Breidenbach T. Effect of slightly lowered body temperatures on endurance performance in humans. J Appl Physiol 57: 1731-1737, 1984.

13.   Holmer, I. Body cooling with ice for warm-water diving operations. Undersea Biomed Res 16: 471-479, 1989.

14.   Hong, SK, Lee CK, Kim JK, Song SH, and Rennie DW. Peripheral blood flow and heat flux of Korean women divers. Fed Proc 28: 1143-1148, 1969.

15.   Kruk, B, Pekkarinen H, Harri M, Manninen K, and Hanninen O. Thermoregulatory responses to exercise at low ambient temperature performed after precooling or preheating procedures. Eur J Appl Physiol 59: 416-420, 1990.

16.   Lee, DT, and Haymes EM. Exercise duration and thermoregulatory responses after whole body precooling. J Appl Physiol 79: 1971-1976, 1995.

17.   Lee, DT, Toner MM, McArdle WD, Vrabas IS, and Pandolf KB. Thermal and metabolic responses to cold-water immersion at knee, hip, and shoulder levels. J Appl Physiol 82: 1523-1530, 1997.

18.   Martineau, L, and Jacobs I. Muscle glycogen utilization during shivering thermogenesis in humans. J Appl Physiol 65: 2046-2050, 1988.

19.   McArdle, WD, Katch FI, and Katch VL. Exercise Physiology: Energy, Nutrition, and Performance. Baltimore, MD: Williams & Wilkins, 1996.

20.   Nadel, ER. Problems With Temperature Regulation During Exercise. New York: Academic, 1977.

21.   Olschewski, H, and Bruck K. Thermoregulatory, cardiovascular, and muscular factors related to exercise after precooling. J Appl Physiol 64: 803-811, 1988.

22.   Petajan, JH, Gappmaier E, White AT, Spencer MK, Mino L, and Hicks R. Impact of aerobic training on fitness and quality of life of multiple sclerosis patients. Ann Neurol 39: 432-441, 1996.

23.   Ramanathan, NL. A new weighting system for mean surface temperature of the human body. J Appl Physiol 19: 531-533, 1964.

24.   Weir, JBDV New methods for calculating metabolic rate with reference to protein metabolism. J Physiol 109: 1-9, 1949.

25.   White, AT, Wilson TE, Davis SL, and Petajan JH. Effect of precooling on physical performance in multiple sclerosis. Mult Scler 6: 176-180, 2000.

26.   Wilson, TE, Johnson SC, Petajan JH, Davis SL, Gappmaier E, Luetkemeier MJ, and White AT. Thermal regulatory responses to submaximal cycling following partial body precooling. Eur J Appl Physiol 88: 67-75, 2002.


J APPL PHYSIOL 94(3):1039-1044
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