Whole body adaptation to cold may occur in humans, but the mechanisms that lead to this adaptation are not clearly understood (16,17,26). In women, the responses to cold water have been explored (22,27), but the thermoregulatory adjustments in women acutely exposed to cold air have historically received scant research attention (14,28,29,33,34). The paucity of information related to the metabolic adjustments to repeated cold air exposure in women reveals a similar response to that observed in men (32). Men and women repeatedly exposed to cold air appear to show a significant attenuation in resting metabolic rate (RMR) during acute cold exposure (16,32). However, the hormonal and metabolic responses of exercise trained and untrained women to repeated acute cold air exposure have not been reported.
Acute exposure to very cold air (≤ 5°C) in nude man evokes frank shivering, bradycardia, elevated stroke volume, peripheral vasoconstriction caused by large increases in plasma norepinephrine (NE), and an elevated RMR as the body defends core body temperature (12,13,16,30,31,36,37). Women, like men, also exhibit frank shivering when exposed to the similar cold air temperatures; however, unlike men, they experience lower skin temperatures, no bradycardia, and no increase in stroke volume (12,13,33,40). Notably, there are no reports of plasma NE changes in women during such exposures. However, in light of the findings of Wagner (40) who reported that blood flow in the forearm and finger were not affected by gender, plasma NE concentrations may be similar in men and women during cold.
Immunoreactive beta-endorphin (IBE) has been implicated in thermoregulation in animals (5) and humans (8,9,21,39). Plasma IBE is elevated during exposure to sauna heating (23,24) and during intense exercise (10), but the relationship between plasma IBE and the thermoregulatory responses to cold stress remains unclear (8,9,39).
Leaner men with high aerobic fitness exhibit increased mean skin temperature and metabolic heat production during cold air exposure compared with less fit men, which may result from a decreased thickness of insulating subcutaneous adipose tissue (1,3,7,20,25). There are no reports of similar comparisons between exercise trained and untrained women.
The purpose of this investigation was to measure resting metabolic rate, plasma norepinephrine, and plasma immunoreactive beta endorphin during serial 45-min exposures to 4°C air during two consecutive 5-d periods, separated by 2 weekend days, in two groups of women differing in aerobic fitness. We hypothesized that HFW would exhibit an elevated RMR, NE, and IBE compared with LFW during exposure to cold air.
Ten Caucasian, eumenorrhoeic women were recruited to this study. Each subject provided voluntary informed consent before entry into the study. The research protocol employing human subjects in this study has been reviewed and approved by the Naval Medical Research Institute's Committee for the Protection of Human Subjects. Subject characteristics are found in Table 1. Peak oxygen consumption (V˙O2peak) was obtained during a progressive cycle ergometer test. After a 5-min warm-up at 50 W the resistance of the ergometer was increased by 25 W every 2 min until the subject reached volitional exhaustion. Tests for V˙O2peak were successful if the subject reached her predicted maximal heart rate (220-age), the respiratory quotient exceeded 1.2, she could not maintain 50 rpm with encouragement, and oxygen consumption peaked and then plateaued or declined as the workload increased. V˙O2peak was determined by averaging the values recorded during the final minute of the test. Expired gases were collected and analyzed by a metabolic cart (Sensormedics 2900, Anaheim, CA) calibrated to known gases. Subjects were specifically instructed to maintain their normal dietary and exercise habits during the 2-wk duration of the study.
Five subjects with no history of endurance training and a peak oxygen consumption less than 40 mL O2·kg−1·min−1 (35 ± 1.3; mean ± SEM) were assigned to the less fit (LFW) group. Five subjects with a history of endurance training and a peak oxygen consumption greater than 50 mL O2·kg−1·min−1 (56.7 ± 3.8) were assigned to the highly fit (HFW) group.
Subjects reported to the lab after an overnight fast at the same time each morning, Monday through Friday during a 2-wk period. Subjects did not report to the lab on Saturday or Sunday because it was closed. Each subject entered into the study on a Monday within 3 d of beginning menstruation and finished on a Friday 12 d later (4,34). Each day subjects reported to the laboratory, they were weighed nude and then dressed in a cotton, short sleeved T-shirt (without brazier), nylon athletic shorts, and cotton socks. Temperature probes (Type EU surface probe, Science Electronics, Dayton, OH) were placed on the left medial ankle beneath the sock, left pectoral muscle, and left upper back beneath the shirt and bare left index finger. Temperatures were recorded each minute by an electronic data logger (Squirrel 1200 series, Science Electronics). To document the application of cold stress, mean skin temperature was calculated as the arithmetic mean of the recorded temperatures of the left medial ankle, left pectoral muscle, and left upper back. Rectal temperature was not measured because no change in core body temperature was expected as a result of the short exposures to cold air (16,30-32,37).
Subjects were seated and rested quietly for 45 min in a thermal neutral (22°-24°C) room, covered by a light cotton blanket, before entering an environmental chamber maintained at 3.5 ± 0.6°C for 45 min. Inside the chamber subjects sat on an open-backed chair with their legs separated and hands resting on a small table. Air flow within the chamber was maintained at 2 m·s−1.
Each Monday and Friday (days 1, 5, 8, and 12) of the study, an antecubital vein was cannulated to obtain blood samples. Whole blood was collected into prechilled vacutainer tubes containing ethylene diamine tetra-acetic acid (EDTA), 10 min after insertion of the cannula, at the end of the thermal neutral period, and at the end of cold exposure. Plasma samples were analyzed as described previously for catecholamines by high performance liquid chromatography (HPLC) (30,31,37) and for immunoreactive beta-endorphin (IBE) by radioimmunoassay (19). On these days oxygen consumption was continuously measured using a flow through ventilation system on a metabolic cart (Sensormedics 2900) calibrated to known gases. Subjects were familiarized with all procedures during two practice sessions in 24°C air before beginning the study. Subjects were paid a nominal sum at the completion of their portion of the study.
Descriptive data (Table 1) were analyzed by one-way ANOVA. Metabolic and endocrine data were analyzed by repeated measures ANOVA using SAS 6.06 in a Group by Day by Temperature by Time design (SAS Institute, Cary, NC). Significant interactions or main effects are reported. Values are reported as mean ± SEM. Significance was set at P < 0.05.
The two groups were not different for age (YR), height (HT), and lean body mass (LBM). Groups differed significantly in mass (WT) P < 0.01, body fat percentage (BF) P < 0.001, body surface area (BSA) P < 0.05 and V˙O2peak P < 0.001 (Table 1).
Mean skin and finger temperatures during warm and cold air exposure were not significantly different between groups and the pattern of response to cold exposure did not change during the course of the study. Mean skin temperature was 32.8 ± 0.02°C during warm rest and fell rapidly during cold air exposure to 27.1 ± 0.2°C (P < 0.001). Mean finger temperature was 28.1 ± 0.2°C during warm exposure and fell to 12.4 ± 0.4° by the end of 45 min of cold exposure (P < 0.001).
Plasma NE concentrations were not different between groups on any day at the end of 45 min in the warm environment (1.72 ± 1.1 nmol·L−1). By the end of 45 min of cold exposure NE in the HFW group (10.88 ± 1.2 nmol·L−1) was more than twice the concentration found in the LFW group (4.95 ± 1.0 nmol·L−1) (P < 0.001). The NE response to the cold challenge was not different on subsequent test days.
Plasma IBE was higher in HFW (15.4 ± 1.53 pmol·L−1) than LFW (9.34 ± 1.95 pmol·L−1) (P < 0.02) and not affected by exposure to cold on any test day. During 45 min in a thermally neutral (22°C) environment RMR did not change within or between groups over the study period. During warm exposure, RMR was about 9% of V˙O2peak (242 ± 17 mL O2·min−1) each day.
There were clear differences in the RMR responses during the first 15 min, expressed as a percent of V˙O2peak, between LFW (Fig. 1) and HFW (Fig. 2) subjects to repeated cold air exposure at rest (P < 0.01). During the first 10 min of exposure to cold air on day 1, the metabolic response increased to 30.5 ± 4.8% of V˙O2peak (659 ± 106 mL O2·min−1) in the LFW group compared to 13.0 ± 1.1% (352 ± 65 mL O2·min−1) in the HFW group. By the 10th min the LFW group metabolic response was reduced to 20.9 ± 2.6% (421 ± 55 mL O2·min−1), while HFW fell to 9.4 + 1.2% (252.8 ± 63 mL O2·min−1) before slowly rising to 13.6 ± 1.2% by 45 min.
The maximal response to cold on day 5 was attenuated in the LFW group to 25.4 ± 3.8% of V˙O2peak (569.3 ± 106 mL O2·min−1) and the maximal response to cold remained at 24 ± 4.2% on days 8 and 12. The response to cold air by the HFW group increased significantly (P < 0.05) to 14.1% (471 ± 108 mL O2·min−1) by day 5 and remained steady through 45 min of cold exposure. However, there were no further differences in the response to cold air on days 8 and 12 in the HFW group. By day 5 there were no differences in absolute oxygen consumption between the groups after the initial 10 min of exposure to cold air.
This study investigated the effect of repeated daily cold air exposures during two consecutive 5-d periods separated by two weekend days on resting metabolic rate (RMR), plasma norepinephrine (NE), and immunoreactive beta-endorphin (IBE) in two groups of women differing in aerobic fitness. A significant finding of this investigation is the unique pattern of oxygen consumption in the LFW during the first 10 min of cold exposure. This characteristic metabolic response pattern is suggestive of a hyperventilation response (15). We were limited by the technology we used (i.e., flow through ventilation system) and cannot confirm that our subjects experienced large increases in minute ventilation on exposure to cold air; however, it is unlikely that the differences in metabolic rate between the groups could be explained on the basis of increased minute ventilation. The increase in oxygen consumption is likely a result of the increase in muscular activation as a response to the cold exposure and the increase in plasma NE (16,36,41).
Consistent with another study we find that RMR during warm air exposure is independent of training or physical fitness (2). However, acute exposure to 3.5°C appears to be more stressful to less aerobically fit individuals than to individuals possessing high aerobic fitness. Women with lower aerobic fitness used a significantly larger percentage of their aerobic capacity than women of higher fitness. This observation may indicate a physiological response which would allow HFW to remain exposed to cold air for a longer period of time than LFW (1). By conserving body heat or producing metabolic heat more efficiently may provide highly fit women an advantage on exposure to cold air.
Each group exhibited a distinctly characteristic metabolic response pattern to acute cold exposure that remained relatively unchanged during the study period (Figs. 1 and 2). Peak oxygen consumption during acute cold exposure was modestly attenuated after four cold air exposures in the LFW group, but the pattern of response remained the same. The HFW group did not demonstrate the same response pattern as the LFW group. Following the initial 10 min of cold air exposure, the metabolic rate increased significantly by 4% during cold exposure in the HFW group by day 5 when exposed to cold. This rise in oxygen consumption by the HFW group is 80 mL O2·min−1 higher than on day 1. Unlike the study by Silami-Garcia and Haymes (32) which showed a reduction in oxygen consumption of approximately 60 mL O2·min−1, oxygen consumption was not decreased in either LFW or HFW after 10 exposures to cold air.
Compared with male subjects exposed to 4°C air, the plasma concentration of NE by the LFW group was nearly the same as untrained men; however, the response by the HFW group was about 4 nmol·L−1 higher (16,30,31,37). The large differences in plasma NE between the two groups was an unexpected finding which may be a result of endurance training by HFW. Exercise acutely increases catecholamines possibly resulting in the down regulation of NE receptors (4,35). Additionally, the reduction in insulation because of a thinner subcutaneous fat layer in the HFW may have contributed to the elevated NE levels we observed by altering the physiological responses to the sensation of cold in the HFW group (1). Thus the differences in the metabolic response may be a result, in part, to the differences in peripheral vasoconstriction in the two groups. LFW may have experienced a lower degree of vasoconstriction leading to increased blood flow and larger heat losses in the periphery which resulted in an increased drive to shiver, when compared with the HFW. Early onset of violent shivering would lead to large increases in oxygen consumption until the subject adjusted to the cold sensation or the reduction in heat flow to the environment caused by vasoconstriction reduced the drive to shiver. Peripheral blood flow, cardiac output, and heat flux in the periphery are areas for future research in women differing in aerobic fitness exposed to extreme cold.
The significant (4%) rise in metabolic rate by day 5 in the HFW appears to be an unexplained physiological adjustment to extreme cold. This adjustment in metabolic rate does not appear to be related to NE or IBE because the plasma concentrations were not different between sampling days within HFW. Further, there were no significant differences between test days for mean skin temperature or finger temperature in the HFW.
We found differences in plasma concentration of IBE between HFW and LFW at rest in a warm room. This finding is surprising in that other investigators have not shown a difference in plasma IBE at rest in two groups of men differing in training status (11). Further, training does not alter the IBE response to acute high intensity exercise (18). The differences in IBE shown in the present study may be because our subjects maintained their current activity and training regimens as instructed. We may have observed a "training" effect on plasma IBE that may partially explain the differences between the two groups.
Plasma IBE was unchanged in either LFW or HFW following an acute exposure to cold air, which differs from the findings reported by Gerra (8), although we speculated that IBE may have been elevated by peripheral nerve stimulation because of shivering (38). On the basis of exercise data, we would not expect plasma IBE to be affected by cold exposure because an exercise intensity of 70% of V˙O2peak for at least 20 min is required to elevate plasma IBE in men (10,39). Clearly the subjects in this study did not approach the relative aerobic intensity by shivering required to elicit a change in plasma IBE.
We conclude that repeated exposure to 3.5°C air may not result in significant acclimation to cold in women regardless of aerobic fitness. Plasma norepinephrine and IBE were unchanged within groups over the study period. Cold exposure requires a larger portion of the aerobic potential in women of lower aerobic fitness than in women of high aerobic fitness. Acute exposure to cold air appears to be physiologically more stressful for less aerobically fit women. The metabolic and hormonal responses to acute cold air exposure in groups of women differing in aerobic fitness warrants further investigation into the mechanism of the physiological response to repeated cold air exposure in women. In agreement with other studies, our findings suggest the existence of a temperature threshold for acclimation to cold air that is warmer than the temperature used in this study (32,39).
1. Bittel, J. H. M., C. Nonotte-Varly, G. H. Livecchi-Gonnot, G. L. M. J. Savourey, and A. M. Hanniquet. Physical fitness and thermoregulatory reactions in a cold
environment in men. J. Appl. Physiol.
2. Broeder, C. E., K. A. Burrhus, L. S. Svanevik, and J. H. Wilmore. The effects of aerobic fitness on resting metabolic rate. Am. J. Clin. Nutr.
3. Budd, G. M., J. R. Brotherhood, A. L. Hendrie, and S. E. Jeffery. Effects of fitness, fatness and age on men's responses to whole body cooling in air. J. Appl. Physiol.
4. Bullen, B. A., G. S. Skriner, I. Z. Beitins, et al. Endurance training effects on plasma hormonal responsiveness and sex hormone excretion. J. Appl. Physiol.
5. Clark, W. G. Effects of opioid peptides on thermoregulation. Fed. Proc.
6. Cunningham, D. J., J. A. J. Stolwijk, and C. B. Wenger. Comparitive thermoregulatory responses of resting men and women
. J. Appl. Physiol.
7. Falk, B., O. Bar-Or, J. Smolander, and G. Frost. Response to rest and exercise
in the cold
: effects of age and aerobic fitness. J. Appl. Physiol.
8. Gerra, G., R. Volpi, R. Delsignore, et al. Sex-related responses of beta-endorphin
, ACTH, GH and PRL to cold
exposure in humans. Acta Endocrinol.
9. Glickman-Weiss, E. L., A. G. Nelson, C. M. Hearon, F. L. Goss, and R. J. Robertson. Are beta-endorphins and thermoregulation during cold
-water immersion related? Undersea Hyperb. Med.
10. Goldfarb, A. H., B. D. Hatfield, D. Armstrong, and J. Potts. Plasma beta-endorphin
concentration: response to intensity and duration of exercise
. Med. Sci. Sports Exerc.
11. Goldfarb, A. H., B. D. Hatfield, J. Potts, and D. Armstrong. Beta-endorphin
time course response to intensity of exercise
: effect of training status. Int. J. Sports Med.
12. Graham, T. E. Thermal, metabolic, and cardiovascular changes in men and women
stress. Med. Sci. Sports Exerc.
13. Graham, T. E., M. Vishwanathan, J. P. Van Dijk, A. Bonen, and J. C. George. Thermal and metabolic responses to cold
by men and by eumenorrheic and amenorrheic women
. J. Appl. Physiol.
14. Hardy, J. D. and E. F. Dubois. Differences between men and women
in their response to heat and cold
. Proc. Natl. Acad. Sci. USA
15. Hayward, J. S. and C. D. French. Hyperventilation response to cold
water immersion: reduction by staged entry. Aviat. Space Environ. Med.
16. Hesslink, R., M. D'Alesandro, D. W. Armstrong III, and H. L. Reed. Human cold
air habituation is independent of thyroxine and thyrotropin. J. Appl. Physiol.
17. Horvath, S. M., A. Freedman, and H. Golden. Acclimatization to extreme cold
. Am. J. Physiol.
18. Howlett, T. A., S. Tomlin, L. Ngahfoong, et al. Release of B-endorphin
and met-enkephalin during exercise
in normal women
: response to training. Br. Med. J.
19. Iranamesh, A., G. Lizarralde, M. L. Johnson, and J. D. Veldhuis. Circadian, ultradian, and episodic release of B-endorphin
in men and its temporal coupling with cortisol. J. Clin. Endocrinol. Metab.
20. Jacobs, I., T. Romet, J. Frim, and A. Hynes. Effects of endurance fitness on responses to cold
water immersion. Aviat. Space Environ. Med.
21. Kelso, T. B., W. G. Herbert, F. C Gwazdaukas, F. L. Goss, and J. L. Hess. Exercise
-thermoregulatory stress and increased plasma β-endorphin
/β-lipotropin in humans. J. Appl. Physiol.
22. Kollias, J., L. Barlett, V. Bergsteinova, J. S. Skinner, E. R. Buskirk, and W. C. Nicholas. Metabolic and thermal responses of women
during cooling in water. J. Appl. Physiol.
23. Kukkonen-Harjula, K., P. Oja, K. Laustiola, et al. Haemodynamic and hormonal responses to heat exposure in a Finnish sauna bath. Eur. J. Appl. Physiol.
24. Laatikainen, T., K. Salminen, A. Kohvakka, and J. Petterson. Response of plasma endorphins, prolactin and catecholamines in women
to intense heat in a sauna. Eur. J. Appl. Physiol.
25. Leblanc, J., J. Cote, S. Dulac, and F. Dulong-Turcot. Effects of age, sex and physical fitness on responses to local cooling. J. Appl. Physiol.
26. Leblanc, J. Factors affecting cold
acclimation and thermogenesis in man. Med. Sci. Sports Exerc.
27. McArdle, W. D., J. R. Magel, T. J. Gergley, R. J. Spina, and M. M. Toner. Thermal adjustment to cold
-water exposure in resting men and women
. J. Appl. Physiol.
28. Murray, S. J., R. J. Shephard, and M. W. M. Radomski. Physiological changes in women
environments. Int. J. Biometeorol.
29. Nunnely, S. H. Physiological responses of women
to thermal stress: a review. Med. Sci. Sports
30. Reed, H. L., S. Pepper, D. Armstrong, Von Tersch, and S. Lewis. Oxygen saturation of brachial venous blood correlates with fingertip tempeature between 11°C and 29°C. Aviat. Space Environ. Med.
31. Reed, H. L., K. R. Kowalski, M. M. D'Alesandro, R. Robertson, and S. B. Lewis. Propanolol fails to lower the increased blood pressure caused by cold
air exposure. Aviat. Space Environ. Med.
32. Silami-Garcia E. and E. M. Haymes. Effects of repeated short-term cold
exposures on cold
-induced thermogenesis of women
. Int. J. Biometeorol.
33. Stevens, G. H. J., T. E. Graham, and B. A. Wilson. Gender differences in cardiovascular and metabolic responses to cold
. Can. J. Physiol. Pharmacol.
34. Stevenson, L. A. and M. A. Kolka. Thermoregulation in women
. Exerc. Sport Sci. Rev.
35. Taylor, J. A., G. A. Hand, D. G. Johnson, and D. R. Seals. Augmented forearm vasoconstriction during dynamic exercise
in healthy older men. Circulation
36. Therminarias, A., P. Flore, M. F. Oddou-Chirpaz, C. Gharib, and G. Gauquelin. Hormonal responses to exercise
during moderate cold
exposure in young vs. middle-aged subjects. J. Appl. Physiol.
37. Thomas J. R., S. Ahlers, J. House, et al. Adrenergic responses to cognitive activity in a cold
environment. J. Appl. Physiol.
38. Thoren P., J. Floras, P. Hoffman, and D. Seals. Endorphins and exercise
: physiological mechanisms and clinical implications. Med. Sci. Sports Exerc.
39. Vishwanathan, M., J. P. Van Dijk, T. E. Graham, A. Bonen, and J. C. George. Exercise
-induced changes in plasma beta-endorphin
and beta-lipotropin in men and women
. J. Appl. Physiol.
40. Wagner, J. A. and S. M. Horvath. Cardiovascular reactions to cold
exposures differ with age and gender. J. Appl. Physiol.
41. Wilkerson, J. E., P. B. Raven, N. W. Bolduan, and S. M. Horvath. Adaptations in man's adrenal function in response to acute cold
stress. J. Appl. Physiol.
Keywords:© Williams & Wilkins 1998. All Rights Reserved.
EXERCISE; WOMEN; COLD; ENDORPHIN; CATECHOLAMINE; METABOLISM