INTRODUCTION
Human adaptation to thermal stress is a significant issue affecting physical performance and human health, particularly influencing mortality and morbidity [1]. Cold adaptation, which can occur through acclimation or acclimatization, could modify thermoregulatory responses, including physiological, behavioral, and perceptual responses to a cold stimulus, in three main ways: habituation, insulative, and metabolic adaptation [2]. These physiological adaptations could enable individuals to defend against cold injuries by reducing strain or enhancing strain endurance in a cold environment [3]. Due to the importance of cold adaptation, several previous efforts have been made to determine the characteristics and modifiers of cold adaptations, such as the required severity and duration of cold exposure, fitness level, altitude, and psychological factors [2,4-6]. However, the features of cold adaptations are less clear compared to those of heat adaptations.
In particular, physical activity could modify thermoregulatory responses to cold stress and a degree of cold adaptation [7]. However, there is a lack of studies investigating the effects of exercise during repeated cold exposures on cold adaptation and the previous results are controversial. Specifically, some studies have reported that exercise during cold exposure may prevent general cold adaptation because increased thermogenesis during exercise could compensate for cold stress [8]. In contrast, others have suggested that the increased heat loss from sweat evaporation and convection of perfused muscle shells during exercise could lead to greater cold stress and, consequently, greater cold adaptation [9].
For instance, Launay et al. [8] did not find any alteration in thermoregulatory responses in participants who performed training in the cold while cold adaptation response (e.g., hypothermic response) was significant in participants who did not engage in exercise training in the cold, suggesting that exercise could prevent general cold adaptation. In contrast, Geurts et al. [10] observed a cold habituation response, such as an increased skin temperature of the fingers and improved thermal ratings during cold immersion, even after repeated cold exposures with an elevated core temperature due to exercise. Additionally, there are debates regarding the effect of cold adaptations on cold-induced vasodilation (CIVD) response, which was first reported by Lewis [11]. CIVD has been presumed to play a protective role against impairment of manual dexterity and/or peripheral cold injury in the cold [12].
Given the growing significance of cold adaptation in recreational and occupational activities involving high physical exertion in cold environments [13], it is important to assess the influence of exercise on cold adaptation. The present study aimed to determine whether exercise during repeated cold exposures affects thermoregulatory adaptations to cold stimuli. To achieve this objective, we investigated thermoregulatory responses to cold in two groups, comparing cold athletes accustomed to outdoor exercise during the winter season (CA) with non-athletic individuals exposed to cold (CON) before and after the winter seasons.
METHODS
1. Participants
A total of 40 participants were recruited with the following demo-graphic characteristics: age: 21±2 years, height: 176.4±5.7 cm, and weight: 74.6±8.4 kg. Among them, twenty participants were CA who engaged in exercise training outdoors for at least 10 hours per week (e.g., soccer and rugby). The remaining participants were in the CON group and self-reported that they did not regularly engage in outdoor exercise; therefore, they were likely passively exposed to cold during the winter season. However, due to the participant's dropout (e.g., seven CA and one CON participant), a total of 32 participants completed the present experiment. All participants were physically active, non-smokers, and they were excluded if they exhibited any signs or symptoms related to cardiovascular and neurological diseases or had a history of cold allergy. Before the study, written informed consent was obtained from all participants after providing full information about the purpose, procedures, and potential risks of the study. This study was reviewed and approved by the Institutional Review Board (KHGIRB-21-171).
2. Protocol
The study consisted of three laboratory visits, including one familiarization and two experimental sessions. Each experimental session was carried out before (November) and after the winter season (March). During the familiarization, participants were provided with an explanation of the experimental procedure, signed informed consent, and underwent anthropometric measurements. Then, they were familiarized with the measurement instruments and cold-water immersion test. Subsequently, participants practiced the fine dexterity test until they reached a performance plateau, defined as achieving a score within ±5% of their previous score [10].
For the second session (experimental session before the winter), participants arrived at the laboratory after refraining from strenuous exercise, alcohol, and caffeine consumption for at least 12 hours before the scheduled test. Upon their arrival, participants wore cotton scrubs and rested quietly while measurement sensors were instrumented. After 15 minutes of rest on a chair, the experiment commenced with the baseline measurements of cardiovascular parameters, body temperature, and cutaneous cold sensitivity. Then, participants immersed their dominant hand up to the wrist in ice water (4-5°C) for 16 minutes. Throughout the immersion, cardiovascular responses, body temperature, cold pain scores, and thermal sensation scores were recorded. Participants also completed the fine dexterity test three times (i.e., before the cold immersion, after the cold immersion, and after a 5-minute recovery period). The third session (experimental session after the winter) followed the same experimental protocol as described above (Fig. 1). All experiments were conducted in a controlled thermoneutral indoor environment with an ambient temperature of 22-25°C and a relative humidity of 30-35%.
3. Measurements
1) Body temperature
Skin temperature was measured continuously by a data logger (NT Logger N543, Nikkiso-Therm Co., Tokyo, Japan) attached to the following locations: shoulder, chest, thigh, and calf. Consequently, the mean skin temperature (Tsk) was calculated by the following formula:
Core temperature (Tc) was measured from the tympanic membrane at rest, during cold immersion, and the recovery period using an infrared thermometer (IRT6030, BRAUN Co., Kronberg, Germany). The measurement was duplicated, and the average value was used for the data analysis. The mean body temperature (Tb) was calculated using the following formula:
2) Cold pressor response & Cold-induced vasodilation
Participants immersed their dominant hand up to the wrist in ice water (4-5°C) for sixteen minutes while seated on a chair. To examine sympathetic responses to cold, systolic and diastolic blood pressure (SBP and DBP; mmHg), stroke volume (SV; mL), and cardiac output (Q; L/min) were measured at rest, during the first minute, and the last minute of the recovery phase. These measurements were continuously obtained using a non-invasive finger plethysmography (Finometer PRO, Finapres Medical Systems B.V. Co., Amsterdam, Netherlands).
CIVD response was evaluated by continuously monitoring finger skin temperature. This was achieved by utilizing a data logger (NT Logger N543, Nikkiso-Therm Co., Tokyo, Japan) attached to the nail bed of the fourth finger, an area known to have abundant arteriovenous anastomoses [14]. The CIVD responses were quantified using the following terminology as described by Daanen [14]: The lowest finger skin temperature after cold immersion was defined as the minimum temperature (Tmin). The highest finger skin temperature during cold immersion was referred to as the maximum temperature (Tmax). The mean finger skin temperature (Tmean) represented the average finger skin temperature over the immersion period, excluding the first 5 minutes. The amplitude was determined as the difference between Tmin and Tmax. The peak time (tpeak) was determined as the time interval between Tmin and Tmax.
3) Perceived variables (Cold pain & Thermal sensation)
During the cold immersion, the participants were asked to rate their cold pain and thermal sensation scores at the first minute of the cold exposure. The perceived pain was measured using a visual analog scale ranging from 0 (indicating no pain) to 10 (representing the worst pain) and the thermal sensation was measured using a thermal sensation scale ranging from −4 (very cold) to 4 (very hot) [15].
4) Cutaneous cold sensitivity
Cutaneous cold sensitivity was assessed on the back of the non-dominant hand using the method of the limit with a thermal stimulator (Intercross-210, Intercross Co., Tokyo, Japan). Initially, the thermal stimulator probe (25×25 mm) was placed on the skin and adjusted to match the skin temperature. Measurement began when the heat flux between the probe and the skin site was stabilized within a range of ±75 W/m2. Subsequently, the probe temperature was gradually decreased at a constant rate of 0.3°C/sec. Participants were instructed to press a switch with their non-dominant hand when they detected a temperature change, signaling the end of the measurement. Cold sensitivity was determined by calcu-lating the difference between the absolute values of heat flux at the start and end of the measurement. In this study, a lower heat flux value indicated a greater degree of cold sensitivity. The measurements were performed in triplicated and the average value was used for data analysis.
5) Manual dexterity
Manual dexterity was assessed using the O’ Connor finger dexterity test. Participants were seated comfortably on a chair in front of a table and instructed to pick up and placing of as many pins as possible in a board composed of 100 holes in ten rows of ten holes each. This test was carried out for one minute; therefore, a greater number of filled holes indicated higher dexterity levels.
4. Statistical analysis
Parametric data, including sympathetic responses, cold sensitivity, and CIVD parameters, were analyzed using SPSS (Ver. 26, IBM, Somers, WI, USA). Sympathetic responses to cold (BP, SV, Q) and cold sensitivity were analyzed using a three-way mixed ANOVA with repeated measures, with the group serving as a between-subject factor. CIVD parameters were analyzed using a three-way mixed ANOVA with repeated measures and paired t-tests to compare the two seasons. For nonpara-metric data concerning the perceived variables (cold pain and thermal sensation), a Friedman test was performed using the R package (ver. 4.2.1, R Foundation, Vienna, Austria). The significance level for all statistical analyses was set at α=0.05.
RESULTS
1. Cold pressor response
No three-way interaction was observed in the cardiovascular variables (BP, SV, Q). However, a significant season*time interaction was found in SBP (F=3.398, p =.044), SV (F=11.338, p <.001), and Q (F=17.372, p <.001). Specifically, SBP in the post-season tended to be lower than in the pre-season at 1 minute during cold immersion (p =.055). SV in the post-season was significantly lower than in the pre-season at rest (p =.024), at 1 minute during cold immersion (p <.001), and during the recovery phase (p <.001). Similarly, Q in the post-season was significantly lower at 1 minute during cold immersion (p <.001) and during the recovery phase (p =.027) compared to the pre-season (Fig. 2). These results suggest that sympathetic reactivity to acute cold exposure was attenuated in both groups after the winter season, without a significant difference between the groups.
2. Perceived variables
No three-way interaction was observed for the cold pain score. However, a significant season*group interaction was found (F=4.375, p =.036), indicating a difference in cold pain scores between groups before and after the winter season. Therefore, the Friedman test was conducted separately for each group. The results showed a significant main effect of the season in the CON group (F=9.930, p =.002), with a significant decrease in cold pain scores after the winter season. In contrast, the CA group showed no significant change in cold pain scores (Table 1).
Table 1.
Comparison of cold-induced vasodilation and subjective parameters before and after the winter season
Regarding thermal sensation scores, no significant three-way or two-way interactions were observed. However, there was a significant main effect of the season (F=4.359, p =.037), suggesting that thermal sensation scores generally increased in both groups after the winter season (Table 1). Additionally, cutaneous cold sensitivity significantly decreased in both groups after the winter season (F=4.973, p =.034) (Fig. 3A).
3. Body temperature & Cold-induced vasodilation
After the winter season, both groups exhibited an increase in body temperature and an improved CIVD response. While no significant interactions between season, time, and group were found, there was a significant main effect of the season for the mean body temperature (F=3.837, p =.005). This suggests that mean body temperature increased significantly in both groups following the winter season, with no notable difference between the groups (Fig. 3B). Similarly, CIVD response was significantly improved in both groups (F=6.864, p =.034) particularly in the temperature domain (Tmax, Tmin, and Tmean) after the winter season without a group difference (Table 1).
4. Manual dexterity
Despite slightly improved manual dexterity after the winter season in both groups, no significant interactions were found in manual dexterity for season, time, and group (F=0.041, p =.841) (Table 2). Similarly, in terms of change rate of dexterity, the impairment and recovery rates after the cold water immersion were significantly improved after the winter season, the results indicate that factors like season and groups may not significantly influence dexterity in the measured context.
Table 2.
Comparison of manual dexterity parameters before and after the winter season
DISCUSSION
This study aimed to investigate the effects of exercise during repeated cold exposures on thermoregulatory adaptation. The results provide several implications for understanding seasonal cold acclimatization and directions for future research. Firstly, both groups exhibited features of cold habituation in physiological variables after the winter season, such as higher body temperature and blunted sympathetic response to local cold stress. Secondly, both groups also showed improved thermal perception and reduced cold sensitivity with no significant difference between the groups. However, a significant difference was observed in cold pain scores. Finally, CIVD responses were enhanced in both groups; however, this did not result in an improvement in fine manual dexterity following cold exposure. Contrary to previous findings [8], which indicated that cold exposure combined with exercise in a controlled environment does not lead to general thermoregulatory cold adaptation, the present results demonstrate that repeated exercise during the winter season does not hinder cold adaptation. In fact it produces a similar pattern of cold acclimatization compared to the control group, suggesting increased body temperature due to exercise is unlikely to diminish climatic cold stimulus to the body.
1. Effects of exercise on physiological adaptation
After the winter season, we observed an increase in mean body temperature and attenuated cardiovascular responses (SBP, SV, and Q) during acute local cold exposure in both groups. These results were representative characteristics of cold habituation and were thought to be due to the reduction of sympathetic activation responding to cold stress. Espe-cially, norepinephrine is the primary neurotransmitter that accounts for the cold-induced vasoconstriction of peripheral blood vessels [16]. It is generally understood that cold exposure on the skin triggers a receptor-mediated neural signaling pathway that traverses through the dorsal horn of the spinal cord to the preoptic area of the hypothalamus, consequently activating sympathetic nerves innervating cutaneous blood vessels and releasing norepinephrine [17]. This pathway could be the “ first line of defense” in a cold environment that effectively increases the insulation of the body's shell by decreasing the temperature gradient between the body and the environment [16,17]. However, when humans are chronically exposed to cold stimuli, the physiological response to cold becomes less pronounced. This cold habituation is accompanied by reduced sympathetic nervous activation during cold exposure. For example, Makinen et al. [18] and Leppäluoto et al. [19] demonstrated that sympathetic response to cold stress was reduced by from 20 to 24% after 10 days of cold exposure (2 hr/day at 10°C). Furthermore, Hesslink et al. [20] demonstrated that a habituated response to cold depends on the change in plasma norepinephrine rather than the change in thyroid-stimulating hormone or thyroxine. Therefore, our results indicated that a decrease in sympathetic activation by habituation results in a blunted cardiovascular response to cold (decreased systolic blood pressure, stroke volume, and cardiac output) and higher body temperature by attenuating cutaneous vasoconstriction after the winter season.
In addition, our results showed a change in the response pattern of SV and Q to cold stimuli after the winter season. Before the winter season, SV and Q either remained stable or slightly increased in response to cold water immersion. However, after the winter season, SV and Q during cold water immersion were lower than baseline even though being exposed to cold stimuli. These results could also support that norepinephrine release decreased after the winter season. Specifically, during cold water immersion, heart contractile, heart rate, and peripheral vasoconstriction increase due to elevated epinephrine or norepinephrine. Cardiac preload also could increase due to enhanced venous return by the peripheral vasoconstriction, leading to increased stroke volume [21]. Therefore, the decreased SV and Q during cold water immersion indicated a smaller release of norepinephrine in response to acute cold stimuli. Furthermore, Monahan et al. [22] found that coronary artery vasodilation occurred during cold water immersion in young males, and this vasodilation response could be disrupted through α- and β-adrenergic block-ade. These blockades interfere with nitric oxide synthesis via α2-adrenergic receptors located on coronary artery endothelial cells and the activation of β2-adrenergic receptors located on coronary vascular smooth muscle cells respectively. Therefore, cold habituation decreased the release of epinephrine and norepinephrine, leading to attenuated coronary artery vasodilation during cold water immersion. The attenuated vasodilation, in turn, could result in increased afterload for our participants aged between 20 and 29. Consequently, the increased afterload could lower SV and Q during the cold water immersion than baseline.
2. Effects of exercise on perceived adaptation
After the winter season, both groups showed a pattern of habituation in cutaneous cold sensitivity and thermal sensation of the hand in the absence of a significant group difference. However, a significant group difference was observed in the cold pain score. Specifically, the cold pain score in CON was significantly lower in the post-season compared to the pre-season, while the cold pain score in CA remained similar. The cause of this group difference is unclear, but it could be related to exercise-induced thermogenesis (EIT) and exercise-induced analgesia (EIA).
EIT may prevent the habituation of cold pain. For example, Launay et al. [8] found that a near-zero thermal load in the cold (i.e., a positive thermal load due to training and a negative thermal load due to cold exposures) could impede cold adaptation. Additionally, individuals who engage in training in the cold may generate sufficient metabolic heat to raise their body temperature above the thermal activation threshold of TRPA1, which is activated by cold stimuli (17°C), lower than that of TRPM8 (∼25-28°C). This could potentially reduce the amount of cold pain stress experienced by participants [23].
EIA may also impede the habituation of cold pain. Several studies have observed an increase in pain thresholds following exercise and have suggested that lower pain ratings could be a result of EIA [24-26]. This decreased pain sensitivity due to EIA is thought to be primarily induced by two mechanisms: neural and hormonal. In neural mechanisms, exercise itself may decrease the perception of various stimuli, particularly pain stimuli, allowing the central nervous system to focus on movement control during exercise by reducing the sensory information flow to the hypothalamus and somatosensory cortex [25,26]. In hormonal mechanisms, the endogenous opioid peptides such as enkephalin and β-endorphin release during exercise [27]. When the opioid peptide binds their specific receptors, it initiates a cascade of processes that ultimately lead to hyperpolarization and prevent the generation of action potential generation. These events could lead to reduced somatic sensitivity [28,29]. Consequently, the thermal load offsetting due to EIT and the increased pain threshold due to EIA could decrease the total amount of pain stress experienced by the participants in the CA group. Therefore, these factors may attenuate the habituation of cold pain. However, further research is necessary to clarify the effects of exercise on cold pain habituation.
3. Effects of exercise on manual performance in the cold
The CIVD response was enhanced in both groups after repeated cold exposures during the winter season, as evidenced by higher temperature parameters of the fingers (Tmax, Tmean, Tmin), which is consistent with previous research showing that the increasing core temperature due to exercise does not deteriorate a local cold acclimation or manual function [10]. The improved CIVD response probably resulted from the reduced sympathetic activation, which is considered to play a major role in the control of CIVD [14]. However, despite the improved CIVD response, both groups did not show improved manual dexterity immediately after cold water immersion and a 5-minute recovery, contrary to what previous studies speculated [30,31]. There could be two main reasons for this result.
Firstly, the enhanced CIVD response may not have been sufficient to offset the impairment in dexterity [32], considering that fine manual dexterity can be severely affected at a finger temperature of 15-16°C [33]. The Tmax reached only about 10°C in the post-season, even though the overall finger temperature was higher in the post-season. Moreover, the nail bed of the finger, where we placed the thermal logger, has a higher density of arteriovenous anastomoses and typically exhibits a more pronounced CIVD response than other areas of the finger [34]. Therefore, the actual temperature difference across the entire fingers during the CIVD response between seasons might be less significant. Furthermore, dexterity impairment rarely occurs at finger skin temperatures above 20°C [33]. In our study, the finger skin temperature of our participants returned to above 20°C after a 5-minute recovery phase, even in the pre-season. Thus, the enhanced CIVD response could not induce a significant preventing effect in manual dexterity impairment after cold water immersion.
Secondly, the CIVD response might be a localized phenomenon isolated to the distal portions of the fingers. Geurts et al. [35] observed an increase in index finger temperature but not in the first dorsal interosseous (FDI) muscle, which is primarily responsible for the abduction of the index finger, at the apex of CIVD. Accordingly, CIVD could be improved by repeated cold exposure, but this improvement may not have a direct positive effect on fine manual dexterity after cold water immersion.
CONCLUSION
The present investigation showed that exercise training during the winter season does not prevent the body from acclimatizing to cold stress. Both the exercise and non-exercise groups exhibited characteristics of cold habituation after the winter season, including elevated body temperature, diminished sympathetic response to acute cold immersion, and decreased perceptual sensitivity to cold stimuli. These adaptations occurred regardless of routine outdoor exercise during cold conditions. However, in terms of cold pain scores, the CA group demonstrated less habituation compared to the CON group, despite engaging in more outdoor activities (including training sessions, matches, and daily routines). This significant group difference suggests a new direction for further research into the effects of exercise on cold acclimatization.
Furthermore, the present results demonstrated that seasonal cold exposure improved the response of CIVD; however, such enhancement did not lead to a favorable outcome in fine manual dexterity after cold water immersion. These findings challenge the assumed biological benefits of CIVD, which was previously believed to protect against the impairment of manual dexterity. Therefore, further research is needed to explore the advantages of CIVD in cold environments.
Several limitations were identified in the present study. First, participants in the CA group likely could not exercise consistently during all instances of cold exposure, leading to situations where they were exposed to cold without engaging in exercise. Similarly, general physical activity in the CON group, with or without cold exposure during the winter season, was neither controlled nor quantified; therefore, their cold responses measured in this study should not be interpreted as a pattern of cold acclimatization in the absence of exercise or physical activity. Second, precise matching of cold exposure levels between the two groups was not possible due to variations in physical activity levels, clothing conditions, and exposure duration, which could fluctuate daily, even within the same group. These factors may have affected the accurate determination of the specific effects of exercise on cold acclimatization during the winter season. Further, caution is needed in interpreting the present data. The lack of group differences in the variables related to cold acclimatization does not necessarily indicate the both groups exhibited a similar degree of a seasonal cold acclimatization. At the same time, the findings suggest the impact of exercise on cold adaptation may differ between acclimation and acclimatization, as shown by the present and previous studies.
Despite these limitations, the present study demonstrates that routine exercise training in cold outdoor conditions does not prevent the body from acclimatizing to seasonal cold. This contributes to our understanding of cold adaptation in humans and provides valuable insights for future research in this field.
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