Winter Swimming: Body Hardening and Cardiorespiratory Protection Via Sustainable Acclimation : Current Sports Medicine Reports

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Winter Swimming: Body Hardening and Cardiorespiratory Protection Via Sustainable Acclimation

Manolis, Antonis S. MD1; Manolis, Stavros A. MSc2; Manolis, Antonis A. DPT, MS3; Manolis, Theodora A. MD4; Apostolaki, Naomi PhD5; Melita, Helen MD6

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Current Sports Medicine Reports 18(11):p 401-415, November 2019. | DOI: 10.1249/JSR.0000000000000653
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Abstract

Introduction

Winter swimming is a stressful condition of whole-body exposure to cold water (1). However, certain individuals who regularly practice this sport activity, winter swimmers, have achieved variable degrees of acclimatization to cold. The question arises whether this extreme sport activity has any health benefits or whether it may confer potentially harmful effects. As a form of exercise, winter swimming entails aerobic activity; however, this becomes more laborious and strenuous when performed in cold water environments. When practiced by individuals who are in good general health adopting a regular, progressive, and adaptive mode, winter swimming appears to confer cardiovascular (CV) and other health benefits (2–4). On the other hand, unaccustomed individuals, when acutely exposed to cold water, depending on the degree of coldness, are at risk of death either from the initial neurogenic cold-shock response, or from progressive decrease of swimming efficiency or from hypothermia (5–7). Furthermore, as with any intense and strenuous exercise (8), individuals with evident or occult underlying CV conditions may be more susceptible to adverse effects with provocation and exacerbation of arrhythmias and CV events that may pose a significant health risk (6).

The guidelines of the governing body for aquatics, Federation Internationale de Natation (FINA), suggest that open-water swimmers should only compete when the water temperature is ≥16°C or <31°C (measured 1 m below the surface) to minimize the risk of severe hypothermia or hyperthermia, respectively; if water temperature is beyond these limits, the event is canceled (9). It is obvious therefore that swimming in colder than 16°C water puts the individual at risk of hypothermia, depending on the severity of cold and the duration of exposure. However, following an appropriate progressive acclimation procedure, this risk is minimized or eliminated for individuals engaged in recreational winter swimming. Even better, adaptation to cold water and regular practice of this activity has been deemed beneficial to health and well-being. Winter swimmers claim to be more energetic, active, and brisk than the controls, achieving greater vigor-activity scores (4). Swimmers afflicted by arthritis, fibromyalgia, or asthma report that winter swimming offers good relief from pains and other physical symptoms together with decreased tension and fatigue and improved mood and memory (4).

Body hardening or sturdiness has been perceived as exposure to a natural stimulus (e.g., cold) that results in increased resistance to stress and diseases, such as acute cardiorespiratory diseases (10). Acute oxidative loading due to cold exposure may ultimately lead to long-term antioxidative adaptation which may serve as a potential molecular mechanism resulting in body hardening (11). Certain immune-system components (leukocytes, monocytes, interleukin[IL]-6) have been shown to be increased in winter swimmers implying readiness to combat infection (12).

Cold exposure triggers thermoregulatory responses. The skin is the first organ exposed to cold water and responds with vasoconstriction which shunts the blood away from the skin surface through the deeper veins in an initial attempt to conserve heat (Fig. 1) (13). This results in widening of the gradient between core and peripheral temperature. Vasoconstriction occurs via sympathetic activation and is conveyed primarily via stimulation of α-noradrenergic receptors in blood vessels. Vasoconstriction may be enhanced via other sympathetically released cotransmitters, such as adenosine triphosphate (ATP) and neuropeptide Y (14–17). Piloerection also may have some, albeit small, contribution in heat conservation by trapping air among hairs and thus increasing the body insulating layer (13). Following vasoconstriction to conserve heat, the mechanisms of thermogenesis are activated (Fig. 1). Shivering may produce thermogenesis; a peak shivering metabolic rate of fivefold the resting metabolic rate has been reported (18). Shivering is triggered by a drop in core temperature and is initiated by the hypothalamic preoptic area (POA) but mediated by the somatic motor cortex in response to signals from cold receptors particularly situated in the skin (19). Another mechanism of thermogenesis involves brown adipose tissue (BAT); sympathetic nervous system activity, in response to inputs from peripheral and central thermoreceptors, can stimulate nonshivering thermogenesis from BAT (20–22).

F1
Figure 1:
The schema illustrates the body's reaction to acute cold-water immersion when several mechanisms are activated (quadrants), depending on the degree of coldness, leading to neurogenic, cardiac, respiratory and other reactions and consequences (rectangles) that may have deleterious health effects in the unaccustomed individual. See text for discussion. AF, atrial fibrillation; CO, cardiac output; HR, heart rate; Insp., inspiratory; NE, norepinephrine; NS, nonshivering; SNS, sympathetic nervous system; VF, ventricular fibrillation.

Thus, a decrease in skin temperature during cold exposure is the initial stimulus for an increased vasoconstrictor response to cold (23). The ensuing decrease in core temperature during repeat exposure to cold appears to be the necessary stimulus for the development of the increased sympathetic response to cold that plays an important role for adaptation. The duration of the reduction in core temperature may be an important factor for inducing insulative acclimation. Some investigators have provided evidence that these thermoregulatory responses are governed by the central nervous system rather than peripheral mechanisms mediating responses to cold exposure (24).

For the compilation of the presented data, an extensive literature review of the topics of swimming, open water swimming, winter swimming/swimmers, cold (water) exposure/tolerance, cold (water) acclimatization/acclimation/adaptation/habituation, cold water immersion, exercise and cold, hypothermia, thermogenesis, thermoregulation, with emphasis on CV/respiratory responses to cold water was conducted in PubMed, Scopus, and Google Scholar. Furthermore, one of the authors (A.S.M.) has a first-hand experience in this topic as he himself is practicing the sport of winter swimming and has compiled the tips included in Tables 1 and 2.

T1
Table 1:
Tips to avoid adverse and ill effects from cold exposure as a winter swimmer.
T2
Table 2:
How to adapt in cold water swimming/additional tips.

Cold Water Classification

As mentioned, FINA has set the 16°C water temperature limit (measured 1 m below the surface) as the lower cutoff for open-water swimming competition, indicating that swimming in colder than 16°C water puts the individual at risk of hypothermia, depending on the severity of cold and the duration of exposure (9). It should be noted that the official water temperature required for Olympic swimming competition is 25°C to 28°C (77°F–82°F). The International Winter Swimming Association has introduced three categories for their events based on water temperature, classifying water as cold water (+5.1°C up to +9.0°C), freezing water (+2.1°C up to +5.0°C), and ice water (−2.0°C up to +2.0°C) (https://iwsa.world/water-classification) (29). The respective maximal swimming distance is limited to 1000 m for cold water, 450 m for freezing water, and 200 m for ice water. However, most of the recreational winter swimming takes place at much higher open-water temperatures, commonly between 10°C and 16°C. Importantly, the subjective feeling and perception of cold is commensurate with the air temperature; when the air temperature is very low (e.g., 3°C), then a 16°C water temperature feels much colder than when the air temperature is 15°C.

CV System Responses

Unaccustomed individuals exposed to cold water rapidly develop heart rate acceleration by ≥20 bpm, increased cardiac output, peripheral vasoconstriction, increased systolic and diastolic blood pressure (BP), and potentially malignant ventricular arrhythmias (Fig. 1) (6). These CV responses to cold-water immersion represent only a slight risk for healthy individuals, but an inordinate risk for persons with hypertension, coronary artery disease (CAD), or other structural heart disease.

A study examined the CV responses to cold in a group of 28 subjects swimming in ice-cold water in winter (30). Systolic BP increased significantly while the subjects were waiting undressed in cold air in the cabin by the pond. Neither immersion nor swimming in the ice-cold water caused further increase in systolic BP, while diastolic BP showed only a modest rise. Blood pressure had returned to control values at 4 min later. Electrocardiographic signs remained unchanged. Although very high pressures were recorded in several subjects, no signs of left ventricular hypertrophy or other CV or cerebrovascular effects could be detected.

Modifications of the activity of β-adrenoceptors play an important role in mechanisms responsible for adaptation of humans to cold. Catecholamine-induced increase in metabolic rate, mediated by β1 and β2 receptors, appears to be attenuated after cold adaptation, indicating downregulation of β1 and β2 adrenoceptors (31).

A study examined the impact of repeated exposure to cold and cold adaptation on CV risk factors, thyroid hormones and the capacity to reset the damaging effect of oxidative stress in 10 well cold-adapted winter swimmers and 16 nonadapted controls (2). A decreased apolipoprotein B/apolipoprotein A1 (ApoB/ApoA1) ratio was found in the winter swimmer group (P < 0.05), but other lipoprotein parameters, including cholesterol efflux capacity, did not differ significantly. Plasma homocysteine was lower in winter swimmers in comparison with controls (P < 0.05). Higher triiodothyronine (T3) values were observed in the winter swimmers compared with the controls (P < 0.05), but thyrotropin (TSH) and other thyroid hormones did not differ between both groups. Winter swimmers had lower activity of glutathione peroxidase 1 (antioxidant defense marker) (P < 0.05), lower concentrations of conjugated dienes (oxidative stress marker) (P < 0.05) and increased activities of paraoxonase 1 (protector against lipid oxidation) (P < 0.001) compared with control subjects. A trend for decreased activity of catalase (antioxidative enzyme) (P = 0.06) in winter swimmers compared with the control group also was observed, but glutathione (antioxidant) levels did not differ significantly. Zinc concentration was higher in the winter swimmer group than in the control group (P < 0.001). The authors concluded that human cold adaptation can influence oxidative stress markers. Trends toward an improvement of CV risk factors in cold-adapted subjects also indicate the positive effect of cold adaptation on cardioprotective mechanisms.

A survey about the long-term effects of winter swimming in cold seawater on “heart attack” and cerebral vascular diseases was carried out in 894 Chinese winter swimmers (32). However, the authors provided very limited information reporting 53 deaths over 30 years versus an expected number of 48.6 deaths (mortality ratio, 1.09).

In summary, acute exposure of unaccustomed individuals to cold water immersion represents a strong CV stress stimulus and poses a great risk for death, particularly for those with occult or underlying structural heart disease. On the other hand, for winter swimmers who have achieved an adequate degree of acclimation to cold water exposure and have built a cold-protective mechanism, this sport activity may contribute to and enhance CV health by various adaptive mechanisms.

Humoral Response and Metabolic Changes

Protection from cold is affected via a decrease of heat loss and an increase of heat production. However, with cold-water exposure of the whole body, heat loss is unavoidable, although it can be minimized by cutaneous vasoconstriction (see discussion below on adaptation). Heat production occurs by muscular activity and by chemical reactions. Oxidative phosphorylation of body fuels, such as carbohydrates and fats, provides the organism with energy-rich phosphate compounds, while releasing heat for bodily uses (33). Thyroid and adrenal hormones and the sympathetic nervous system maintain and regulate the oxidative phosphorylation that occurs primarily in the mitochondria of brown and white fat and skeletal muscle tissues. It is noteworthy that animals from which thyroid or adrenal glands have been removed do not tolerate cold. The efficacy of oxidative phosphorylation has been shown to be regulated by uncoupling proteins, of which at least five species are known at the moment (34).

Adrenal medullary and thyroid hormones and sympathetic stimulation lead to increased activity of uncoupling proteins that reduce the oxidative phosphorylation, by this way increasing heat production (35). Studies have demonstrated the existence of adrenergic thermogenesis and the role of the sympathetic nervous system in controlling metabolic rate, heart rate, and vasomotion in humans exposed to cold (31,36,37). In addition to the increased metabolism, driven by thyroid and adrenal hormones, many changes in CV functions, such as vasoconstriction and raised BP, occur in response to cold. Other humoral and metabolic changes are described below.

A study examined the role of adrenoceptors in mediating adrenergic functions after adaptation of humans to cold, and the effect of increasing doses of β1 (dobutamine) and β2 (terbutaline) sympathomimetics on resting metabolic rate, heart rate, systolic BP, rectal, and skin temperatures of seven controls and of seven cold-adapted winter swimmers (31). Increase in metabolic rate, mediated by β1 and β2 sympathomimetics, was attenuated after cold adaptation, indicating downregulation of β1 and β2 adrenoceptors. Since cold adapted humans have greater capacity of nonshivering thermogenesis than that mediated by both β1 and β2 adrenoceptors, the role of other subtypes of adrenoceptors in mediating nonshivering thermogenesis is postulated. Heart rate increased after administration of the β2 agonist, but not by the β1 agonist. The significance of β2 adrenoceptors in mediating heart rate was depressed after cold adaptation. The authors concluded that modifications in the activity of β adrenoceptors play a crucial role in mechanisms responsible for adaptation of humans to cold.

As mentioned, thyroid hormones and catecholamines have an important role in thermogenesis. The acute hormonal and metabolic effects of long-distance swimming in cold (18.5°C) water were evaluated in 22 long-distance swimmers (38). A positive correlation was obtained between percent body fat and rectal temperature measured at the end of the competition. After the competition, an increase in plasma catecholamines (epinephrine, norepinephrine), cortisol, thyroxine, free fatty acids, and lactate, a decrease in glucose and insulin, and no change in growth hormone, T3, triglycerides, and cholesterol concentrations were noted. The increase in plasma thyroxine was more pronounced in the slower swimmers; the change in blood cortisol concentrations was higher in those with the most acute decrease in body temperature.

A study examined the influence of long-term regular exposure to acute cold temperature on humoral factors (39). Two types of exposure (three times a week) were studied in 10 healthy females, winter swimming in ice-cold water (water 0-2°C for 20 s) and whole-body cryotherapy (air, –110°C for 2 min in a special chamber) over the course of 12 wk. Plasma adrenocorticotropin (ACTH) and cortisol in weeks 4 to 12 on time-points 35 min were significantly lower than in week 1, probably due to habituation, suggesting that neither winter swimming nor whole-body cryotherapy stimulated the pituitary-adrenal cortex axis. Plasma epinephrine was unchanged during both experiments, but norepinephrine showed significant twofold to threefold increases each time for 12 wk after both cold exposures. Plasma IL-1-beta, IL-6 or tumor necrosis factor (TNF) alpha did not show any changes after cold exposure. The authors concluded that the main finding of this study was a sustained cold-induced stimulation of norepinephrine, which was remarkably similar between exposures (39). Other investigators considered hormonal variations in winter swimmers as seasonal rather than an effect of winter swimming (40).

A study examined whether cold water swimming for seven consecutive months changes basal leptin and insulin concentrations and insulin sensitivity in 17 healthy recreational female regular swimmers aged 45 ± 8.7 years, exposed to cold water at least twice a week for 5 to 10 min (mean water temperature, 9.5°C in October, 1.0°C in January, and 4.4°C at the end of April) (41). Winter swimming significantly increased insulin sensitivity and decreased insulin and leptin concentrations (P = 0.006, P = 0.032, P = 0.042, respectively). Leptin concentration positively correlated with body mass index (BMI) and insulin level (r = 0.412, r = 0.868, respectively). Insulin level inversely correlated with insulin sensitivity and positively with glucose (r = −0.893, r = 0.166, respectively). No associations between leptin and insulin sensitivity were found. The authors concluded that regular cold-water swimming may stimulate metabolic changes suggesting that leptin and insulin participate in adaptive metabolic mechanisms triggered by repeated cold exposure accompanied by mild exercise in healthy nonobese women.

A study of acute and chronic effects of winter swimming (n = 11) on several hormones indicated an initial increase of TSH levels within the normal range both in the untrained and in the cold-trained persons, with a subsequent decrease (42). Similar changes occurred in cortisol serum concentrations, though psychological stress seemed to interfere with cold stress. There were mild decreases in prolactin serum levels after cold stress, whereas follicle-stimulating hormone, luteinizing hormone, and growth hormone remained unaltered. There was a mild initial elevation of serum glucose after cold stress which disappeared after training. There were long-term training effects on basal prolactin levels which increased by almost twofold, and on insulin serum levels which dropped by almost 50%; after 2.5 months of training, there was a significant 50% inhibition of insulin release after the cold-water immersion.

A study investigated BP and hormonal changes during one winter swimming season in winter swimmers and nonswimmer controls on three occasions (autumn, winter, and spring) (40). Mean systolic BP of the winter swimmers fell from 134 ± 12 mm Hg to 128 ± 12 mm Hg (P < 0.05) during the winter, and a slight but nonsignificant drop also was seen in the controls. Mean plasma noradrenaline levels diminished significantly from autumn to spring, and more so in the winter swimmer group, but no statistically significant difference was observed between the groups. Adrenaline levels also showed a decreasing trend. Plasma homovanillic acid and beta-endorphin values were on the same level in all seasonal samples in both groups. Plasma serotonin levels decreased in both groups by about 50% by spring, but 5-hydroxyindoleacetic acid (the primary metabolite of serotonin) did not change significantly. The authors concluded that BP and plasma catecholamine levels decreased during winter swimming practice over one winter, but similar, albeit to a lesser degree, changes also were observed in the control persons; whether these humoral changes reflect adaptation to cold or seasonal variation was not clear (40). Another study indicated that cold adaptation induced by winter swimming attenuates the catecholamine responses to cold water (43).

A study carried out in 12 male winter swimmers showed positive effects of winter swimming on the rheological properties of blood, manifested by an increase in erythrocyte deformability without accompanying changes in erythrocyte aggregation (44). In another study, red blood cell, white blood cell, and platelet counts increased significantly (4.7%, P = 0.005; 40.6%, P < 0.001; and 25.0%, P < 0.001, respectively) after swimming in cold water (6°C) (45). According to the authors, the increase in the total number of white blood cells indicates a cold stress-induced generalized reactive leukocytosis, while the increase in red blood cell count with parallel increase in hemoglobin and hematocrit was due to winter swimming-induced hemoconcentration produced by plasma volume changes from the shift of plasma water from the intravascular to the extravascular compartments, due to the sympathetic nervous system activation and the consequent reactive vasoconstriction.

Studies indicate positive adaptive changes in the antioxidant system of healthy winter swimmers. These changes seem to increase the capacity and efficiency of the antioxidant system, increase the resistance and tolerance, and improve the readiness and defensive reaction of the human body to stress factors (1).

Hormonal and metabolic changes occurring during prolonged cold-water immersion in individuals wearing thermal protection gear and performing intermittent exercise affording slow rate of body cooling are similar in direction and magnitude to those occurring in persons submitted to short-duration unprotected exposures (46). These changes included diurnal variations of cortisol and ACTH levels, with larger increases occurring after evening immersions, a greater than threefold increase in norepinephrine, significant increases in T3 uptake and epinephrine, free fatty acid levels and lactate, and a decline of glucose levels. Only changes in norepinephrine correlated significantly with changes in rectal temperature.

Human thermoregulatory and vascular fluid responses to cold stress were studied in seven men subjected to cold stress in a standardized cold-air and cold-water exposure before and after a cold acclimation program consisted of daily immersion (90 min) in cold water (18°C) repeated five times per week for five consecutive weeks (47,48). Preacclimation and postacclimation, metabolism increased (P < 0.01) by 85% during the first 10 min of cold air exposure and thereafter rose slowly. After acclimation, rectal temperature was lower (P < 0.01) before and during cold air exposure. Mean weighted skin temperature was lower (P < 0.01) following acclimation than before. Plasma norepinephrine increased during both cold air exposures (P < 0.002), but the increase was larger (P < 0.004) following acclimation (47). The percent reduction in plasma volume was larger (P < 0.01) in cold water (−17%) than in cold air (−12%). Cold water immersion resulted in greater (P < 0.01) diuresis than cold air exposure. Plasma K+ concentration increased (P < 0.01) during cold (both air and water) exposure, whereas plasma Na+ concentration was unchanged. Calculated renal clearance and urinary excretion rate of both Na+ and K+ increased during cold (both air and water) exposure. Also, although BP increased during the first cold-water exposure, a smaller BP increment was observed after acclimation, while cardiac output responses to cold remained unaffected (49). The authors concluded that repeated cold-water immersion stimulated development of true cold acclimation of the insulative type and did not influence vascular fluid responses to cold stress, while vascular fluid shifts, body cooling, and diuresis were all greater in cold water than in air (47,48).

The classical notion of cold-induced plasma volume reduction attributed to increased cold-induced diuresis generated by an inhibition of antidiuretic hormone (ADH) release (50,51) has been challenged by the fact that most of the hemoconcentration appears to be reversible during rewarming. Experimental data have indicated that the reduction of plasma volume noted during cold stress could be mainly attributed to a transient shift of plasma volume from vascular to interstitial spaces, due to an increase of BP, rather than solely explained by cold-induced diuresis (52).

Beyond recreational winter swimming, an extreme sport of ice swimming has emerged since 2009, which entails swimming 1 mile in water ≤5°C (53). The development of metabolic acidosis, increased blood glucose, creatine kinase, and cortisol levels have been documented after swimming 1 “ice mile” in an experienced ice swimmer who completed six consecutive “ice miles” within 2 d (53). The rise in cortisol and the drop in core body temperature were associated with increased acidosis. The rise in glucose and cortisol was attributed to the high level of physical stress; similarly, the rise in creatine kinase is attributable to increased exercise-induced physiological stress and/or suggests skeletal muscle damages due to shivering. Skin body temperature dropped, while core body temperature initially increased during the first few minutes after the start (an effect known as “anticipatory thermogenesis”) subsequently dropping by 1°C to 2.5°C, reaching a nadir at ~30 min after finish of the “ice miles.” The initial increase in core body temperature might be due to peripheral vasoconstriction and the exercise-induced increase in metabolic heat production (54). The intense muscular contractions in the first minutes to adapt to cold exposure may generate heat and contribute to the phenomenon of “anticipatory thermogenesis.” Another way to increase core body temperature in the first minutes in the cold water is to engage in preswim warming exercise. Nevertheless, the swimmer suffered an after-drop in temperature postswim resulting in hypothermia (<36°C) despite his high BMI and long experience in cold-water swimming. It should be pointed out that hypothermia is the most prevalent medical risk in open-water swimming as suggested by other investigators (55); this risk is apparently accentuated for cold-water swimmers. Other investigators have indicated a positive correlation between rectal temperature and body fat observed at the end of a long-distance (32 km) swimming event (38).

In summary, heat preservation during cold exposure is attained via a decrease of heat loss and an increase of heat production. However, with cold-water exposure of the whole body, heat loss is unavoidable; it can be minimized by cutaneous vasoconstriction. Heat production occurs by muscular activity (shivering) and by chemical reactions (nonshivering thermogenesis; see discussion below). A cascade of humoral and hormonal changes takes place to preserve body heat. Sympathetic stimulation produces vasoconstriction, which, together with the thermogenic mechanisms, may lead to an initial increase in core body temperature. Adrenal medullary and thyroid hormones and sympathetic stimulation augment the activity of uncoupling proteins that reduce the oxidative phosphorylation leading to heat production. However, continued and/or extended cold exposure, especially in very cold water, may result in hypothermia (<36°C) which is the most prevalent medical risk in open-water swimming. Cold adaptation induced by winter swimming attenuates the catecholamine responses to cold water and augments the body's capacity to preserve heat. Furthermore, winter swimming with repeated cold-water immersion stimulates the development of cold acclimation, may increase insulin sensitivity, and produce positive adaptive changes in the antioxidant system of healthy winter swimmers, thus improving the readiness of the human body to stress factors. Finally, vascular fluid shifts and increased diuresis occur with cold water exposure leading to a reduction of plasma volume, which could also be attributed to a transient shift of plasma volume from vascular to interstitial spaces, due to an increase of BP, rather than solely explained by cold-induced diuresis.

Respiratory System Responses

For the healthy unaccustomed individual, the neurogenically induced cold-shock respiratory responses represent the greatest threat to survival occurring during cold-water immersion which produces an “inspiratory gasp” followed by uncontrollable hyperventilation, leading to respiratory alkalosis and hypocapnia (Fig. 1) (6,56,57). Large falls in the arterial tension of carbon dioxide have been associated with ventricular fibrillation in dogs and men (6,58). Such falls also can result in cerebral hypoxia caused by reductions in cerebral blood flow and a shift to the left in the hemoglobin dissociation curve, accounting for the tetany, disorientation, and clouding of sensorium demonstrated by subjects during the first minutes of cold-water immersion (6,59). The cold-shock-induced reduction in breath-hold time significantly increases the risk of an immersion victim aspirating water.

Respiratory responses to cold stress were studied in seven men before and after a cold acclimation program of daily 90-min cold-water (18°C) immersions repeated five times a week for five consecutive weeks (49). In cold air (5°C) following cold acclimation, the oxygen consumption (V˙O2) at 10 min was lower (P < 0.02) postacclimation than preacclimation; however, no differences were found in cold water (18°C). The minute ventilation (VE) increased (P < 0.01) during cold (air and water) stress tests as a function of carbon dioxide production (V˙CO2). Acclimation did not affect the VE-V˙CO2 relationship or the pattern of breathing during exposure to cold air or water. The acclimation had no effect on cardiac output or arteriovenous O2 difference, which both increased (P < 0.01) during the first 45 min of cold stress test, and then remained stable. The authors concluded that cold acclimation attenuated the onset of metabolic heat production during exposure to cold air but did not alter its ultimate magnitude or the relationships between the cardiorespiratory variables and metabolic requirements.

A case-control study examined the influence of physical and mental skills training on the response to sudden cold-water immersion and on controlling hyperventilation upon immersion in six inexperienced swimmers who received 1 wk of cold-water head-out immersions (10 × 3 min at 15°C) in comparison with six inexperienced control swimmers who received immersions in temperate water (27°C) (60). There were significant improvements in the intervention group's ability to suppress rapid increases in respiratory frequency from 62 ± 24 breaths per minute to 33 ± 12 breaths per minute. A smaller and more transient drop in brain blood flow was noted than that previously reported due to the hypertensive response associated with treading water. The authors concluded that cold-water habituation, combined with mental skills training, could improve voluntary control over the respiratory portion of the cold-shock response, enhancing survival prospects in a real-life emergency scenario, such as an overturned boat.

Although swimming is generally beneficial to one's overall health, recent data suggest that it also may have detrimental effects on the respiratory system, especially when practiced in pools or in polluted recreational water (61,62). Chemicals used in pools resulting from the interaction between chlorine and organic matter may be irritating to the respiratory tract and induce upper and lower respiratory symptoms, particularly in children, lifeguards, and high-level swimmers. The prevalence of atopy, rhinitis, asthma, and airway hyper-responsiveness is increased in elite swimmers compared with the general population (61,63). This may be related to the airway epithelial damage and increased nasal and lung permeability caused by the exposure to chlorine subproducts in indoor swimming pools, in association with airway inflammatory and remodeling processes. Furthermore, waterborne viral and other diseases have been associated with swimming pools (64). Toxicological studies have shown that swimming pool water and many disinfection byproducts can be mutagenic, genotoxic, and carcinogenic; epidemiologic studies have shown that exposure to disinfection byproducts increases the risk of respiratory adverse effects and bladder cancer (65).

On the other hand, winter swimming in open seawater avoids these potential ailments of indoor pool-water swimming, unless this recreational activity is performed in polluted marine waters (62,66). Importantly, epidemiological data have shown a decrease in respiratory infections by ~40% in acclimated winter swimmers (11,67).

An interesting issue concerning upper respiratory infections in swimmer athletes is the association of a deficient or insufficient vitamin D status with a propensity to respiratory infections (68). An Israeli study of 98 young athletes (including 12 swimmers) and dancers (age, 14.7 ± 3.0 years), found that 73% of participants were vitamin D insufficient, defined as serum 25(OH)D concentration < 30 ng·mL−1 (mean serum 25(OH)D concentration 25.3 ± 8.3 ng·mL−1) (69). The authors concluded that among young athletes and dancers from various disciplines in a sunny country, a high prevalence of vitamin D insufficiency was identified. A higher rate of vitamin D insufficiency was found among participants who practice indoors, during the winter months, and in the presence of iron depletion. Another study examined if vitamin D3 supplementation reduces upper respiratory infection burden in 55 vitamin D-insufficient swimmers, randomized to receive vitamin D3 or placebo for 12 winter weeks (70). There were no between-group differences in the frequency, severity, or duration of respiratory infections. Exploratory analyses revealed that in the placebo group only, the change in 25(OH)D concentrations during the trial was highly associated with the duration of respiratory infections (r = −0.90, P < 0.001), and moderately associated with the severity of respiratory infections (r = −0.65, P = 0.043). The between-group differences for duration were highly significant. Vitamin D3 supplementation in swimmers with vitamin D insufficiency did not reduce respiratory infection burden. However, larger decreases in serum 25(OH)D concentrations were associated with significantly longer and more severe respiratory infection episodes.

In summary, for the unaccustomed individual, the neurogenically induced cold-shock respiratory responses represent the greatest threat to survival. However, cold-water acclimation may ameliorate these responses. Although swimming is generally beneficial to one's overall health, recent data suggest that it also may have detrimental effects on the respiratory system, especially when practiced in pools attributed to chemicals (chlorine) which may be irritating to the respiratory tract, and/or viral or bacterial pollutants. Furthermore, a high rate of vitamin D insufficiency was found among indoor swimmers associated with significantly longer and more severe respiratory infection episodes; vitamin D3 supplementation does not appear to reduce respiratory infection burden. All these adverse effects of pool swimming are avoided by individuals practicing winter swimming in open sea water, and when acclimation has been achieved, the respiratory infection rate may be reduced.

Adaptative Responses to Winter Swimming

Thermoregulation

The thermoregulatory system comprises two essential components, the thermosensory neurons that monitor local temperature from the skin and from deep structures (viscera, spinal cord, and hypothalamus), and a control circuit in the POA of the hypothalamus which triggers thermoeffector responses to keep temperature constant (71). Cold responses, in general, are more sensitive to skin temperature, potentially reflecting the preponderance of cold receptors, whereas hot responses are more sensitive to core temperature, where warm receptors prevail (72).

As mentioned, exposure to cold initially activates heat-saving mechanisms, which include cutaneous vasoconstriction and piloerection, followed by recruitment of thermogenic mechanisms (Fig. 1). Initially, skeletal muscle shivering takes place that leads to ATP hydrolysis generating heat; and when cold exposure is sustained, nonshivering thermogenesis of BAT, also referred to as adaptive thermogenesis, develops over longer-term.

Thermogenic mechanisms aiming at counteracting temperature changes and maintaining temperature within a very narrow range are strongly controlled by endocrine regulators, including several hormones like leptin, glucocorticoids, or insulin and, principally, by thyroid hormones (37,71). The POA in the hypothalamus constitutes the central thermoregulatory center, which receives thermal information from the skin, viscera, and other internal organs, and sends signals evoking autonomic, somatic, hormonal, and behavioral responses. This hypothalamic center monitors local brain temperature and thus controls thermoregulation. Thermosensitive (warm- and cold-sensitive) neurons have been described in the POA that respond to local hypothalamic temperature (73).

Peripheral thermosensation is affected via several nonselective cation channels of the transient receptor potential (TRP) family which serve as molecular thermal sensors in sensory neurons and other cells activated by changes in temperature and also contribute, directly or indirectly, to thermoregulation (71,74,75). Cation channels activated by cold temperatures include TRP melastastin 8 (TRPM8) (76), TRP ankyrin subtype 1 protein (TRPA1) (77), and TRP cation channel, subfamily C member 5 (TRPC5) (78). TRPM8 is the only TRP channel for which there is general agreement about its principal role in detection of cold temperature (79). It also is expressed in a small subset of primary sensory neurons of the dorsal root and trigeminal ganglia (80). TRPM8 channels are promptly activated by cold, with detectable currents below 26°C to 28°C, likely mediating innocuous cold sensation (79). TRPA1 is a polymodal ion channel expressed in nociceptors, originally proposed to be a noxious cold receptor (81), activated at temperatures below 17°C, thus contributing to noxious cold sensation, although this role remains controversial (77).

The molecular mechanisms responsible for central thermoregulation in the hypothalamus are largely unknown (82). With regard to neurons in the POA of hypothalamus, pacemaker current channels, potassium leak channels, and TRP channel TRPV4 seem to be involved in temperature sensing (83,84). In the spinal cord, thermal sensation may reflect the activation of TRP channels in the central end of sensory neurons located in the spinal dorsal horn (85). In the viscera, temperature thermosensitivity mechanisms for receptive neurons also are less well elucidated; animal studies have shown that several TRP channels, similar to the skin afferent nerves, are expressed in gastrointestinal vagal afferent nerves (86).

A hypothermic type of adaptation may develop in individuals subjected to repeated cold-water immersion. According to a study, repeated exposures of young sportsmen to cold water (head out, 14°C, 1 h, three times per week for 4–6 wk) induced changes in regulation of thermal homeostasis (87). Central and peripheral body temperatures at rest and during cold immersion were lowered. A downward shift of shivering threshold was observed. “Cold acclimated” subjects also showed a lowered cold sensation. A trend toward a small increase in the body fat content also was observed. Cold adaptation and body insulation are further conferred by increased vasoconstriction, as evidenced by the lowered skin temperature. However, the changes induced by cold acclimation were transient, disappearing within 2 wk after termination of the adaptation procedure. More frequent and/or longer-lasting cold exposures may lead to persistent or permanent changes in thermogenesis and body insulation.

A study examined subjects undertaking repeated cold-water (10°C) immersions over 3 d and compared them with subjects who had only two half-body immersions (88). Repeated immersions reduced the heart rate, respiratory frequency, and volume responses (P < 0.01), despite identical skin temperature profiles in both groups. The authors concluded that the mechanisms involved in producing habituation of the initial responses are located more centrally than the peripheral receptors. Another study showed that very short (20 s) ice-cold water exposure repeated three times per week for 3 months in healthy women led to habituation of thermal sensation and comfort (89).

Sympathetic Nervous System Activation

Hypothermic stress of immersion in cold water stimulates release of norepinephrine from the sympathetic nervous system (46,89). In six men, after immersion in 10°C water for 2 min, the mean norepinephrine concentration was increased from 359 ± 32 (basal) to 642 ± 138 pg·mL−1 and rose gradually to a maximum of 1.171 ± 226 pg·mL−1 after 45 min of immersion (90). Metabolic rate increased approximately threefold during the immersion period. After rewarming in warm water (40°C), the subjects showed a transient peak in plasma norepinephrine followed by a rapid decrease to basal levels after 30 min. The fall in plasma norepinephrine after approximately 8 min of rewarming occurred despite persistent depression of the core temperature and coincided with a sudden decrease in metabolic rate and cessation of body shivering. The authors concluded that the sympathetic nervous system response to cold can be activated or suppressed very quickly and is dependent on the skin temperature.

When the temperature in the distal extremities (fingers and toes) gets quite low while the core temperature is still warm, paradoxical cold-induced vasodilation may occur, attributable to opening of arteriovenous anastomoses (91). This mechanism may protect against cold injuries. However, vasodilation is almost absent during hypothermia for reasons of survival.

Oxidative Stress

Whole-body cold exposure has been shown to induce oxidative stress of mild degree (10). This type of repeated mild oxidative stress leads to adaptation via preconditioning which confers improved antioxidative protection. Such an adaptive mechanism of the antioxidant system developed by regular cold-water exposure could provide a tentative explanation of body hardening and enhanced body readiness to stress factors related to an increase in the protection against oxidative stress (1,92).

A study investigated the effects of severe cold stress on total peroxyl radical-trapping antioxidant capacity of plasma (TRAP) in two groups of healthy women, a whole-body cryotherapy group (n = 10) exposed to −110°C for 2 min and a winter swimming group (n = 10) exposed for 20 s in ice-cold water three times per week for 12 wk (93). Although there was a marked heterogeneity among subjects, during the first 4 wk, the mean TRAP value significantly increased at 2 min after cold exposure in the cryotherapy group, returning to baseline 35 min after the exposure; similar changes were observed in the winter swimming group. However, all changes due to cold were relatively mild (<5%). After 4 wk, no changes in TRAP values after the cold exposures were noticed and no long-term changes in basal TRAP values were observed. The authors concluded that regular cryotherapy and winter swimming do not seem to be harmful with regard to antioxidative capacity.

Another study examined the effect of one session of swimming in ice-cold water and one hot sauna session (performed a few months later) on oxidant-antioxidant balance in 21 experienced winter swimmers and 19 first-time winter swimmers (94). There were no differences in initial values of antioxidant enzymes activity and lipid peroxidation products level between the two groups. Significant changes were observed after sauna in catalase activity, which is the crucial antioxidant enzyme that neutralizes reactive oxygen species generated as a result of thermal stress. Increased level of thiobarbituric acid reactive substance was observed in the novice group as a result of sauna bath, indicating that exposure to high ambient temperature is a source of oxidative stress; however, such a stress was not noticed in regular winter swimmers. The authors concluded that regular baths in cold water combined with sauna probably lead to adaptive changes that protect the organism against harmful effects of thermal stress.

Another study evaluated 10 healthy winter swimmers before and after winter swimming (92). A drastic decrease in plasma uric acid concentration was observed during and following the exposure to the cold-water stimulus. The authors postulated that the uric acid decrease might be caused by its consumption after formation of oxygen radicals; a hypothesis that they felt was supported by the observation that the erythrocytic level of oxidized glutathione and the ratio of oxidized glutathione/total glutathione also increased after cold exposure. On the other hand, the baseline concentration of reduced glutathione was increased, and the concentration of oxidized glutathione was decreased in the erythrocytes of winter swimmers as compared with those of nonwinter swimmers. The authors interpreted these findings as an adaptation to repeated oxidative stress leading to body hardening (increased tolerance to stress and diseases) (92). Importantly, it should be noted that glutathione, a powerful antioxidant, is crucial in the removal and detoxification of carcinogens, albeit glutathione also may make tumors less sensitive to chemotherapy (95).

Immune System

The cytokine response after thermal stress consisting of sauna followed by swimming in ice-cold water was investigated in habitual and inexperienced winter swimmers (12). In regular winter swimmers, the concentrations of plasma IL-6, leukocytes, and monocytes at rest were significantly higher than in inexperienced subjects. In experienced female winter swimmers, the plasma concentration of the soluble receptor for IL-6 was significantly lower than that in inexperienced female swimmers. In both groups, granulocytosis, hemoconcentration, and significant increases in the concentrations of ADH, cortisol, and IL-6 were observed after the stimuli. However, the changes in the cortisol concentration were dramatically larger in habitual winter swimmers. The authors concluded that thermal stress with sauna followed by swimming in ice-cold water appeared to stimulate both the neuroendocrine and the immune systems, and the results indicate that adaptive mechanisms occur in habitual winter swimmers. The basal levels of several immune response components (leukocytes, monocytes, IL-6) were higher in winter swimmers than in controls, indicating that the immune system is mildly stimulated and probably more prepared to react to an infection (12).

Similar findings had been shown by an earlier study which examined the effect of cold-water immersion (14°C for 1 h) on the immune system of athletic young men (96). With repeated cold-water immersions (three times a week for 6 wk), a small, but significant, increase in the proportions of monocytes, lymphocytes with expressed IL2 receptors (CD25) and in plasma TNF alpha content was induced. An increase in the plasma concentrations of some acute phase proteins, such as haptoglobin and hemopexin, also was observed. After 6 wk of repeated immersions, a trend toward an increase in the plasma concentrations of IL6 and the amount of total T lymphocytes (CD3), T helper cells (CD4), T suppressor cells (CD8), activated T and B lymphocytes (HLA-DR), and a decrease in the plasma concentration of alpha 1-antitrypsin was observed. The authors concluded that repeated cold-water immersions mildly activated the immune system.

Another study examined the immunological responses to cold-water (18°C) exposure together with the effects of pretreatment with either passive heating or exercise in seven healthy men (mean age, 24.0 ± 1.9 years) (97). Core temperature rose by 1°C during passive heating and during exercise in 35°C water and remained stable during exercise in 18°C water. Subsequent cold exposure induced leukocytosis and granulocytosis, an increase in natural killer cell count and activity, and a rise in circulating levels of IL-6. Pretreatment with exercise in 18°C water augmented the leukocyte, granulocyte, and monocyte response. The authors concluded that acute cold exposure has immunostimulating effects and that pretreatment with physical exercise can enhance this response.

Types of Adaptation

Four types of cold adaptation have been described, metabolic, insulative, hypothermic, and insulative hypothermic (Fig. 2) (98–100); other investigators have suggested only metabolic and insulative adaptation (101). The term “habituation” also has been suggested to denote blunted shivering and/or cutaneous vasoconstrictor response, resulting from periodic short-term cold exposures (101,102). Metabolic adaptation involves enhanced thermogenesis developing after cold exposures that are more intense, but not severe enough to induce a significant drop in core temperature. Insulative adaptation is characterized by a lower skin temperature upon cold exposure with unchanged metabolic rates and is affected via enhanced vasoconstriction and redistribution of body heat toward the shell that develops from repeated cold exposures which induce a considerable drop in core temperature. Hypothermic adaptation denotes increased tolerance to cold without corresponding physiological changes.

F2
Figure 2:
Four adaptive (acclimation/acclimatization) mechanisms to winter swimming (WS) have been proposed, metabolic, insulative, hypothermic or mixed, all aiming at enhanced preservation of heat via decreased heat loss and increased heat production of variable degrees. In hypothermic cold adaptation, the core temperature is allowed to decrease more via enhanced vasoconstriction (with ensuing considerable decrease in skin temperature) and/or lower metabolic heat production compared with nonacclimatized people before heat production responses are initiated. The metabolic type of cold acclimatization is characterized by increased (shivering/nonshivering) thermogenesis while exposed to cold. Longer periods of winter swimming (better habituation) elicit a hypothermic response (lowered threshold) and delayed onset of shivering, while adrenergic and/or BAT (nonshivering) thermogenesis is operative at a lesser degree as an insulative response proves quite effective in preserving heat (insulative hypothermic adaptation).

The different types of cold adaptation responses and acclimation patterns are dependent on the degree and frequency of whole-body cooling during repeated cold-water immersion, the exposure duration, and length of acclimation period. Brief immersions induce habituation, even when only a few immersions are completed. Metabolic adaptation occurs when it can compensate increased heat loss; when not, insulative mechanisms tend to prevail. Interindividual differences exist in the relative contribution of metabolic and insulative adaptations to cold (103), related to the cold stress intensity and to individual factors, such as diet, the level of physical fitness and body fat content; increased metabolism tends to prevail in lean subjects and insulative responses in obese subjects (98). The blunted shivering and vasoconstrictor responses that develop with habituation might lead to a greater fall in core temperature during cold exposure (hypothermic adaptation). However, not all cold-adapted individuals manifest hypothermic habituation. Hypothermic habituation diminishes the sympathetic response to cold. When the duration of immersion is prolonged and the immersions are repeated over a longer acclimation period, the acclimation patterns beyond habituation are induced, such as metabolic and insulative adaptation, enabling better heat conservation by improved insulation at the body surface, while perfusion of the subcutaneous tissue is more efficiently maintained than before acclimation (102).

A study examined thermoregulation in cold-adapted winter swimmers and in control subjects during 1 h of cold-water immersion (13°C) (36). The thermoregulatory functions of winter swimmers differed from those of non-cold-adapted subjects, wherein the magnitude of cold thermogenesis in winter swimmers was solely related to changes in rectal temperature, while in controls, a significant part of cold thermogenesis during the early phase of cooling was induced by changes in skin temperature input, and only in the late phase of cooling it was the central temperature input which was mainly involved in induction of cold thermogenesis. Shivering was induced later during cooling (after 40 min) in winter swimmers than in controls, which suggests an important participation of nonshivering thermogenesis in the early thermogenic response. Winter swimmers also showed bradycardia and a greater reduction in plasma volume during cooling, indicating restriction of heat loss from the body. Only a nonsignificant increase in quantity of subcutaneous fat was observed in winter swimmers. Thus, winter swimmers were able to withstand a significantly greater temperature gradient between body and environment than non-cold-adapted subjects by modifying the sensory functions of hypothalamic thermoregulatory centers to lower heat loss and produce less heat during cold exposure. Furthermore, increased nonshivering heat production played a greater role in total cold thermogenesis. Heat produced due to thermogenic action of adrenaline may represent more than a quarter of the total cold thermogenesis. The authors concluded that winter swimmers exhibit metabolic, hypothermic and insulative types of cold adaptation.

A recent study investigated the effects of long-term repeated diving in cold sea water on physiological responses to cold exposure (sitting position for 1 h at air temperature 12°C and relative humidity 45%), in 10 older (mean age, 70 years) Korean female divers (haenyeos), who had been exposed to cold water through breath-hold diving since their teens and compared them with those of 10 young (mean age, 23 years) and 6 older (mean age, 73 years) female controls (104). The changes in core temperature showed no significant differences among the groups. The decreases in mean skin temperature were greater for older haenyeos than the other two groups (P < 0.01). Older haenyeos had significantly lower-energy expenditure during cold exposure when compared with older nondiving females (P < 0.05). Heart rate was significantly lower in older haenyeos than that of young nondiving females (P < 0.05). Older haenyeos felt cooler at the face with lower face temperature when compared with older nondiving females. The authors concluded that older haenyeos respond to cold by reducing heat loss from the skin (insulative adaptation) rather than increasing metabolic rate.

Other studies have suggested that decreased skin temperature alone during acclimation sessions suffices for increased vasoconstrictor responses to cold; however, core temperature reductions during acclimation are needed to enhance sympathetic activation responses to cold, while the duration (>60 min) of the core temperature reduction is important for inducing insulative acclimation (23).

Nonshivering Thermogenesis

A study in six nonacclimated men examined whether 4 wk of cold exposure to 10°C for 2 h daily for 4 wk (5 d·wk−1), using a liquid-conditioned suit, could increase both the volume of metabolically active BAT and its oxidative capacity (105). Testing was performed using electromyography combined with positron emission tomography with 11C-acetate and 18F-fluorodeoxyglucose. The 4-wk acclimation protocol elicited a 45% increase in BAT volume of activity and a 2.2-fold increase in cold-induced total BAT oxidative metabolism (P < 0.05). There was no significant change in shivering intensity. Fractional glucose uptake in BAT increased after acclimation. The authors concluded that daily cold exposure not only increases the volume of metabolically active BAT but also increases its oxidative capacity and thus its contribution to cold-induced thermogenesis.

Nonshivering thermogenesis involves beta-adrenergic receptors of the heart, blood vessels, adipocytes, and muscles (37). During the early phase of cold exposure (first 20 min), the thermogenesis mediated by beta adrenergic receptors may cover ~80% of the total metabolic increase induced by cold (105). After ~30 min of cooling the relative proportion of beta-adrenergic thermogenesis starts to decline, reaching 20% of the total cold thermogenesis at the end of cooling. It seems that human adrenergic thermogenesis is mostly produced outside of the BAT. According to experiments with infusion of adrenaline, skeletal muscle contributes ~40% and adipose tissue ~5% of the whole-body adrenaline-induced thermogenesis (107).

With regard to the body habitus of winter swimmers, their BMI has been reported lower or equal to age- and gender-matched controls, suggesting that it is not the large BMI that might have a protective effect against heat loss during swims in cold water without wetsuits (108). Rather, successful recreational swimming in cold water is influenced by factors other than body habitus, such as acclimatization, heat production while swimming, and adjusting immersion time. On the other hand, the relatively low prevalence of obesity in winter swimmers suggests that cold-water swimming could contribute to a healthy lifestyle (108).

In summary, brief, intermittent cold exposures induce adaptation by heat-saving mechanisms, which include cutaneous vasoconstriction and piloerection, followed by activation of thermogenic mechanisms, initially via shivering, even when only very limited areas of the body surface are exposed and whole-body heat losses are probably minute (Fig. 1). More pronounced physiological adjustments occur only when repeated cold-exposure leads to significant body heat loss. Insulative adjustments appear to develop when repeated cold exposures are too severe for body heat loss to be offset by increased metabolic heat production with the attendant risk of significant core temperature decline and development of hypothermia. However, it also is possible that an enhanced nonshivering thermogenic capability involving beta-adrenergic receptors and/or BAT can develop in humans in response to chronic cold exposure to counteract and balance the heat loss. Other data (98) suggest that body composition and physical fitness may determine the acclimation type, with lean, fit individuals developing metabolic adjustments and fat, less fit individuals developing insulative adjustments. Other investigators have suggested the progressive development of different stages in the cold-adaptation process (109) with an initial response to whole-body cold exposure by shivering, later replaced by insulative adaptations developed to help restrict body heat loss. Finally, behavioral acclimatization also is important as it avoids prolonged potentially harmful cold exposures (101).

The acquired acclimation to cold water exposure may be gradually lost when cold exposures are discontinued. Thus, a regular sustainable activity is required to maintain adaptation, and when cold-water swimming is interrupted for a given time, cold water showering may be helpful, while at reinitiation of the activity, a progressive and escalating strategy with a staged protocol needs to be followed (Tables 1 and 2).

Potential Benefits vs Health Risks

Swimming is a popular sport worldwide among people of all ages favored by many individuals over land exercises including patients with rheumatic diseases, who tolerate swimming better as a form of aerobic exercises, as they attain lower oxygen consumption and similar CV benefits characterized by lower heart rate and greater stroke volume (110). Swimming appears comparable to land exercises in its effect on CV risk factors, including BP reduction, and is well tolerated by patients with stable CAD and/or heart failure, with adequate safety, especially when practiced in moderation and under the supervision of health care providers. However, in patients with a history of congenital long QT syndrome (LQTS), swimming should be avoided because of the increased risk of a cardiac arrhythmic event and drowning (110).

On the other hand, winter swimming with cold-water exposure is a stressful condition, and as such, it may pose certain health risks. Swimming in cold water by unaccustomed persons may have detrimental effects (Fig. 1), whereas adaptive physiologic mechanisms increase tolerance to cold water in experienced swimmers (Fig. 2). The impact of acute exposure of the novice to cold water immersion and the ensuing voluntary apnea (cold-shock response) could result in parasympathetic and sympathetic activity resulting in life-threatening cardiac arrhythmias, pulmonary edema, and potential death (5–7).

Underlying Structural or Electrical Heart Disease

Patients with underlying heart disease may develop untoward effects upon exposure to cold water. Although patients with compensated chronic heart failure have been reported to tolerate water immersion and swimming in moderately cold (22°C) water well, the observed increase in ventricular extrasystoles raises concerns about the potential danger of high-grade ventricular arrhythmias in this patient group (111). Exposure to water of lower temperature seems prohibitive in this group of patients. In patients with CAD, cold-induced ischemia and provocation of angina are well-known and attributed to an increase in BP with an associated increase in myocardial oxygen demand (112,113); furthermore, the documented increase in norepinephrine upon exposure to cold water (89) poses significant potential risk of ischemia and arrhythmias, while this risk may be accentuated by possible cold-induced vasospasm (114); the associated initial hyperventilation occurring upon initial cold-water exposure (6,56) may further contribute to coronary vasospasm (115). Winter swimming also is prohibited in patients with LQTS who are susceptible to potentially malignant ventricular arrhythmias even during regular swimming; one can only imagine a much higher risk incurred by cold water exposure in these patients leading to greater catecholamine release, a most potent arrhythmogenic trigger. Just face, let alone whole body, immersion in cold water can prolong the QT interval, and trigger bradycardic responses, which lead to arrhythmic events with polymorphic ventricular tachycardia in the form of torsade de pointes that may degenerate into ventricular fibrillation (110).

Acclimation tips

As with any type of exercise, one needs to gradually build this experience and provide adequate time and techniques to progressively adapt and acclimatize oneself to cold-water exposure (Tables 1 and 2). Furthermore, the acquired acclimation needs to be sustained via a regular and adjustable exposure program. An effective way to initiate this experience is to continue regular swimming activity beyond the end of summer into the fall (mild cold) and gradually into the winter months (severe cold), choosing to avoid extreme cold conditions at least during the first 1 to 2 years of such an activity (Table 1). An optimal approach would be for the swimmer to engage in some exercise activity before swimming, such as jogging, playing racket ball, or volley ball on the beach, and most importantly, when exiting the water to promptly remove the wet swimwear and again engage in postswimming warming exercise activities. These latter activities are crucial to restore body temperature and preserve the feeling of wellness under ambient temperature; otherwise one has to clothe in and transfer oneself into a warm environment in order again to restore normal body temperature, especially when the ambient temperature is very low. At the end of a cold-water swim and for a period after it, the deep body temperature of a swimmer may continue to fall due to thermal gradients established during the swim (Table 2) (116,117).

Health Benefits

As mentioned, the repeated mild oxidative stress induced by regular whole-body cold-water exposure leads to adaptation and preconditioning that finally confer improved antioxidative protection further contributing to body hardening (Fig. 3) (10).

F3
Figure 3:
Winter swimming (WS) acclimation leads to body hardening/sturdiness with increased resistance to respiratory infections, improved cardiovascular risk profile, enhanced antioxidative protection and readiness of the immune system. When the health benefits of swimming exercise are added, and when extreme practices that may potentiate adverse effects of cold exposure are avoided, enhanced performance and ability to withstand other kinds of stress with improved general well-being may be expected. LP, lipoprotein; RF, risk factors.

A study examined the effect of cold adaptation on CV risk factors, thyroid hormones, and the capacity of humans to reset the damaging effect of oxidative stress in 10 winter swimmers and 16 nonadapted controls (2). A lower apolipoprotein B/apolipoprotein A1 (ApoB/ApoA1) ratio and plasma homocysteine were found in winter swimmers (P < 0.05). Higher T3 values, but no differences in TSH and other thyroid hormones were noted. Favorable changes in the antioxidant system also were observed in winter swimmers. The authors concluded that trends toward improved CV risk factors with a shift toward a “healthier” lipoprotein profile in winter swimmers indicate the positive effect of cold adaptation on cardioprotective mechanisms, while adaptive responses have led to an increase in antioxidative capacity. Other studies have shown similar results with positive adaptive changes in the antioxidant system of healthy winter-swimmers (1). These changes seem to increase body hardening and readiness to stress factors.

As also mentioned, swimming in cold water appears to stimulate both the neuroendocrine and the immune systems and the data indicate that adaptive mechanisms occur in habitual winter swimmers. The basal levels of several immune response components (leukocytes, lymphocytes, monocytes, IL-6, TNF, acute phase proteins) have been reported to be higher in winter swimmers than in controls, indicating that the immune system is mildly activated and probably more prepared to combat infection (12,96). In keeping with these findings, epidemiological data have shown a decrease in respiratory tract infections by 40% in acclimated winter swimmers (11,67).

Winter swimming is not merely cold adaptation, as it combines exercise with cold exposure. Therefore, one should consider possible synergism of cold exposure and physical activity. Regarding the antioxidant effect of exercise, according to a systematic review and meta-analysis of 30 controlled trials (1346 participants) included in a qualitative analysis with 19 of them included in the meta-analysis, regardless of intensity, volume, type of exercise, and studied population, the antioxidant capacity tended to increase (mean difference 1.45, P < 0.001) and prooxidant parameters tended to decrease (mean difference −1.08, P < 0.001) after physical training (117). Thus, exercise training seems to induce an antioxidant effect. The authors concluded that people, regardless of their health status, should practice some kind of exercise to balance the redox state and to improve health-related outcomes.

Other Risks and Benefits

Neuromuscular cooling and swim failure rather than general hypothermia may be more hazardous during ice swimming (53). Of course, the risk of hypothermia cannot be overlooked as it has been reported to be a common condition affecting mass-participation long-distance open-water swimmers, with prolonged duration of the swim predicting an increased risk of hypothermia (119). One can imagine that this risk is multifold higher when the swim is prolonged in cold water, albeit dependent on the severity of cold and the degree of acclimation.

Winter swimming, except perhaps for the “ice-mile” swimming, is a recreational activity and as such is not subject to potential risks of training-related risks of professional swimmers, where respiratory and other infections and muscular injuries prevail, especially during periods of intensive training (120). Susceptibility to pulmonary and other infections has been attributed to the negative effects of swimming pool chlorine on general health and performance (121), or to the negative impact of intense training on innate immunity (122).

Winter swimming in open-sea-water venues avoids all these potential risks, while acclimation appears to lead to body hardening with increased immune defense, rather than the weakening of the immune system incurred by the overtraining of professional swimmers (117,118). As mentioned, winter swimmers feel more energetic, active, and brisk compared with controls; those afflicted by rheumatic disease, fibromyalgia, or asthma report significant symptomatic improvement (4). Also, epidemiological data report a decrease in respiratory tract infections in acclimated winter swimmers (11). In addition, improvement of CV risk factors in cold-adapted subjects has been reported, indicating the positive effect of cold adaptation on cardioprotective mechanisms (2).

Guidelines

There are no guidelines specifically addressing winter swimming. However, there are guidelines issued for open-sea-water swimming (World Health Organization [WHO]) (25), as well as guidance for enabling people exercising in the cold to avoid cold-weather injuries (American College of Sports Medicine) (26), which should be followed. An important example includes avoidance of alcohol, as alcohol consumption is one of the most frequently reported contributory factors associated with drownings for adults (25). Furthermore, alcohol significantly contributes to hypothermia. Sudden immersion cooling also may be a significant contributory factor to drowning and death. Regarding relevant sports-related injuries, the majority of spinal cord injuries appear to be associated with diving. The WHO indicates that prevention is the best way to reduce the incidence of injury and death related to the aquatic environment, and the majority of injuries can be prevented by appropriate measures at a local level (25). One should keep in mind several conditions predisposing to hypothermia, including factors associated with decreased heat production (e.g., inactivity, fatigue, lack of sleep, endocrine dysfunction), increased heat loss (e.g., immersion, wind, wet clothing, skin disorders), or impaired thermoregulation (e.g., neural disorders, stroke, drugs, alcohol) (26). Older (>60 years) individuals and children are at increased risk of hypothermia. The risk of cold injuries, like frostbite, is minimal for winter swimmers, less than 5% when the ambient temperature is above −15°C (5°F), but increased safety surveillance of swimmers is warranted when the wind chill temperature falls below −27°C (−18°F) since, in those conditions, frostbite can occur in ≤30 min in exposed skin (12). However, one also should watch out for nonfreezing cold injuries, like chilblains, that may occur after 1 to 5 h in cold wet conditions, at temperatures below 16°C. Finally, one should keep in mind other cold-related conditions, such as cold urticaria and cold- and/or exercise-induced asthma (26).

In Tables 1 and 2, we provide some flexible/generalized training tips that may enable the inexperienced cold-water swimmer to progress to the level of an experienced/seasoned cold-water swimmer based on personal experience and a summation of the evidence to date. A winter swimmer candidate should not decide to initiate the activity in winter, but, as suggested in Table 1, one should continue summer swimming activities in a regular pattern (e.g., two to three times per week) throughout the autumn into the winter, as this greatly helps acclimation. Fortunately, when winter arrives, there is a significant time-lag in sea-water temperature drop compared with ambient temperature and this again facilitates adaptation. For the first 2 to 3 years of the activity, one should practice the sport in beach areas with relatively calm sea and water temperatures known to range between 10°C and 16°C and for short swims (5–15 min or shorter if shivering). Around December, sea-water temperature may drop significantly and care should be taken to avoid days of extremely cold or generally bad (windy) weather and big waves. Of course, things may be different in areas with early snowing, where water temperature lowers faster and earlier. One should observe one's own reactions and tolerance and not cross one's own limits, even if enthused with one's own endurance. One should keep in mind that staying in cold water for longer than 30 min increases risk of hypothermia; hypothermia ensues faster in severely cold water (freezing or ice water). Engaging in warm-up exercise/activity before and after swimming is helpful. Most importantly, after exiting cold water, one should promptly warm up (e.g., with dry clothing and a hot drink) and maintain warmth for a few hours afterward. Maintenance of acclimation is important with regular (at least once weekly) sessions; ending regular hot-water showers with cold water showering at home may add to sustainability of acclimation. With long breaks, risks are lurking, and one should restart progressive cold-water exposure training.

Conclusions

Acute exposure to cold water can be detrimental for the unaccustomed individual, commensurate with the degree of coldness, as it may produce an initial, neurogenically mediated cold shock response with inspiratory gasp, hyperventilation and hypocapnia followed by cerebral anoxia and/or cardiorespiratory arrest. Other acute adverse effects may include progressive decrease of swimming efficiency and/or hypothermia, all contributing to risk of drowning and death. Winter swimmers have been able to surpass these hurdles by adopting a habituation strategy to achieve acclimation and what is perceived as body hardening with increased body tolerance to stressors. Furthermore, they seem to enjoy some other potential health benefits, which, in addition to a well-accepted sense of well-being and vigor, may possibly comprise a healthier CV risk profile, enhanced antioxidative protection, increased immune system readiness and a reduced incidence of respiratory infections.

Nevertheless, the field is currently lacking, and thus in dire need of, prospective studies and epidemiological data regarding the potential risks or merits of this important sport activity. In this work, in addition to reviewing existing data regarding the health consequences of winter swimming, an attempt has been made to provide those practicing winter swimming or intending to embark on such an activity with some essential tips to avoid adverse and ill effects from cold exposure (Tables 1 and 2). In addition, the gist of this presentation is illustrated in Figures 1 to 3 which depict the mechanisms and consequences of the body's reaction to acute cold-water immersion of the unaccustomed individual, the types of adaptive mechanisms to winter swimming, and the potential health benefits (body hardening) of acclimation to winter swimming.

The authors declare no conflict of interest and do not have any financial disclosures.

References

1. Lubkowska A, Dolegowska B, Szygula Z, et al. Winter-swimming as a building-up body resistance factor inducing adaptive changes in the oxidant/antioxidant status. Scand. J. Clin. Lab. Invest. 2013; 73:315–25.
2. Kralova Lesna I, Rychlikova J, Vavrova L, Vybiral S. Could human cold adaptation decrease the risk of cardiovascular disease? J. Therm. Biol. 2015; 52:192–8.
3. Kolettis TM, Kolettis MT. Winter swimming: healthy or hazardous? Evidence and hypotheses. Med. Hypotheses. 2003; 61:654–6.
4. Huttunen P, Kokko L, Ylijukuri V. Winter swimming improves general well-being. Int. J. Circumpolar Health. 2004; 63:140–4.
5. Keatinge WR, Prys-Roberts C, Cooper KE, et al. Sudden failure of swimming in cold water. Br. Med. J. 1969; 1:480–3.
6. Tipton MJ. The initial responses to cold-water immersion in man. Clin. Sci. (Lond.). 1989; 77:581–8.
7. Tipton M, Eglin C, Gennser M, Golden F. Immersion deaths and deterioration in swimming performance in cold water. Lancet. 1999; 354:626–9.
8. Manolis AS, Manolis AA. Exercise and arrhythmias: a double-edged sword. Pacing Clin. Electrophysiol. 2016; 39:748–62.
9. Bergeron MF, Bahr R, Bartsch P, et al. International Olympic Committee consensus statement on thermoregulatory and altitude challenges for high-level athletes. Br. J. Sports Med. 2012; 46:770–9.
10. Siems WG, Brenke R, Sommerburg O, Grune T. Improved antioxidative protection in winter swimmers. QJM. 1999; 92:193–8.
11. Brenke R. Winter-swimming: an extreme form of body hardening. Therapeutikon. 1990; 4:466–72.
12. Dugue B, Leppanen E. Adaptation related to cytokines in man: effects of regular swimming in ice-cold water. Clin. Physiol. 2000; 20:114–21.
13. Tansey EA, Johnson CD. Recent advances in thermoregulation. Adv. Physiol. Educ. 2015; 39:139–48.
14. Bradley E, Law A, Bell D, Johnson CD. Effects of varying impulse number on cotransmitter contributions to sympathetic vasoconstriction in rat tail artery. Am. J. Physiol. Heart Circ. Physiol. 2003; 284:H2007–14.
15. Burnstock G. Cotransmission in the autonomic nervous system. Handb. Clin. Neurol. 2013; 117:23–35.
16. Stephens DP, Aoki K, Kosiba WA, Johnson JM. Nonnoradrenergic mechanism of reflex cutaneous vasoconstriction in men. Am. J. Physiol. Heart Circ. Physiol. 2001; 280:H1496–504.
17. Stephens DP, Saad AR, Bennett LA, et al. Neuropeptide Y antagonism reduces reflex cutaneous vasoconstriction in humans. Am. J. Physiol. Heart Circ. Physiol. 2004; 287:H1404–9.
18. Eyolfson DA, Tikuisis P, Xu X, et al. Measurement and prediction of peak shivering intensity in humans. Eur. J. Appl. Physiol. 2001; 84:100–6.
19. Nakamura K. Afferent pathways for autonomic and shivering thermoeffectors. Handb. Clin. Neurol. 2018; 156:263–79.
20. Saito M, Okamatsu-Ogura Y, Matsushita M, et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009; 58:1526–31.
21. Klingenspor M. Cold-induced recruitment of brown adipose tissue thermogenesis. Exp. Physiol. 2003; 88:141–8.
22. van der Lans AA, Wierts R, Vosselman MJ, et al. Cold-activated brown adipose tissue in human adults: methodological issues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2014; 307:R103–13.
23. O'Brien C, Young AJ, Lee DT, et al. Role of core temperature as a stimulus for cold acclimation during repeated immersion in 20 degrees C water. J. Appl. Physiol. (1985). 2000; 89:242–50.
24. Muzik O, Reilly KT, Diwadkar VA. “Brain over body”—a study on the willful regulation of autonomic function during cold exposure. Neuroimage. 2018; 172:632–41.
25. WHO. Guidelines for safe recreational water environments. Volume 1, coastal and fresh waters. WHO Library Cataloguing-in-Publication Data. 2003; 1–219.
26. Castellani JW, Young AJ, Ducharme MB, et al. American College of Sports Medicine position stand: prevention of cold injuries during exercise. Med. Sci. Sports Exerc. 2006; 38:2012–29.
27. Hayward JS, Eckerson JD, Collis ML. Thermal balance and survival time prediction of man in cold water. Can. J. Physiol. Pharmacol. 1975; 53:21–32.
    28. Kaciuba-Uscilko H, Greenleaf JE. Acclimatization to cold in humans. NASA Technical Memorandum 101012, April 1989. https://ntrs.nasa.gov/search.jsp?R=19890013690. 1989.
      29. IWSA. Water classification—International Winter Swimming Association. [cited 2019 September 12]. 2019. https://iwsa.world/water-classification.
      30. Zenner RJ, De Decker DE, Clement DL. Blood-pressure response to swimming in ice-cold water. Lancet. 1980; 1:120–1.
      31. Jansky L, Vybiral S, Trubacova M, Okrouhlik J. Modulation of adrenergic receptors and adrenergic functions in cold adapted humans. Eur. J. Appl. Physiol. 2008; 104:131–5.
      32. Gao HM, Gao X, Ma BX, Zhang H. Long-term risks of cardiac and cerebral vascular diseases increased following winter swimming in the cold seawater. Int. J. Cardiol. 2014; 177:701–2.
      33. Paakkonen T, Leppaluoto J. Cold exposure and hormonal secretion: a review. Int. J. Circumpolar Health. 2002; 61:265–76.
      34. Bouillaud F, Alves-Guerra MC, Ricquier D. UCPs, at the interface between bioenergetics and metabolism. Biochim. Biophys. Acta. 2016; 1863:2443–56.
      35. Solmonson A, Mills EM. Uncoupling proteins and the molecular mechanisms of thyroid thermogenesis. Endocrinology. 2016; 157:455–62.
      36. Vybiral S, Lesna I, Jansky L, Zeman V. Thermoregulation in winter swimmers and physiological significance of human catecholamine thermogenesis. Exp. Physiol. 2000; 85:321–6.
      37. Jansky L. Humoral thermogenesis and its role in maintaining energy balance. Physiol. Rev. 1995; 75:237–59.
      38. Dulac S, Quirion A, DeCarufel D, et al. Metabolic and hormonal responses to long-distance swimming in cold water. Int. J. Sports Med. 1987; 8:352–6.
      39. Leppaluoto J, Westerlund T, Huttunen P, et al. Effects of long-term whole-body cold exposures on plasma concentrations of ACTH, beta-endorphin, cortisol, catecholamines and cytokines in healthy females. Scand. J. Clin. Lab. Invest. 2008; 68:145–53.
      40. Hirvonen J, Lindeman S, Matti J, Huttunen P. Plasma catecholamines, serotonin and their metabolites and beta-endorphin of winter swimmers during one winter. Possible correlations to psychological traits. Int. J. Circumpolar Health. 2002; 61:363–72.
      41. Gibas-Dorna M, Checinska Z, Korek E, et al. Variations in leptin and insulin levels within one swimming season in non-obese female cold water swimmers. Scand. J. Clin. Lab. Invest. 2016; 76:486–91.
      42. Hermanussen M, Jensen F, Hirsch N, et al. Acute and chronic effects of winter swimming on LH, FSH, prolactin, growth hormone, TSH, cortisol, serum glucose and insulin. Arctic Med. Res. 1995; 54:45–51.
      43. Huttunen P, Rintamaki H, Hirvonen J. Effect of regular winter swimming on the activity of the sympathoadrenal system before and after a single cold water immersion. Int. J. Circumpolar Health. 2001; 60:400–6.
      44. Teleglow A, Dabrowski Z, Marchewka A, et al. The influence of winter swimming on the rheological properties of blood. Clin. Hemorheol. Microcirc. 2014; 57:119–27.
      45. Lombardi G, Ricci C, Banfi G. Effect of winter swimming on haematological parameters. Biochem Med (Zagreb). 2011; 21:71–8.
      46. Smith DJ, Deuster PA, Ryan CJ, Doubt TJ. Prolonged whole body immersion in cold water: hormonal and metabolic changes. Undersea Biomed. Res. 1990; 17:139–47.
      47. Young AJ, Muza SR, Sawka MN, et al. Human thermoregulatory responses to cold air are altered by repeated cold water immersion. J. Appl. Physiol. (1985). 1986; 60:1542–8.
      48. Young AJ, Muza SR, Sawka MN, Pandolf KB. Human vascular fluid responses to cold stress are not altered by cold acclimation. Undersea Biomed. Res. 1987; 14:215–28.
      49. Muza SR, Young AJ, Sawka MN, et al. Respiratory and cardiovascular responses to cold stress following repeated cold water immersion. Undersea Biomed. Res. 1988; 15:165–78.
      50. Morgan ML, Anderson RJ, Ellis MA, Berl T. Mechanism of cold diuresis in the rat. Am. J. Physiol. 1983; 244:F210–6.
      51. Wittert GA, Or HK, Livesey JH, et al. Vasopressin, corticotrophin-releasing factor, and pituitary adrenal responses to acute cold stress in normal humans. J. Clin. Endocrinol. Metab. 1992; 75:750–5.
      52. Vogelaere P, Savourey G, Deklunder G, et al. Reversal of cold induced haemoconcentration. Eur. J. Appl. Physiol. Occup. Physiol. 1992; 64:244–9.
      53. Knechtle B, Stjepanovic M, Knechtle C, et al. Physiological responses to swimming repetitive “ice miles”. J. Strength Cond. Res. 2018. doi:10.1519/JSC.0000000000002690. [Epub ahead of print].
      54. Maeda T. Relationship between maximum oxygen uptake and peripheral vasoconstriction in a cold environment. J. Physiol. Anthropol. 2017; 36:42.
      55. Macaluso F, Barone R, Isaacs AW, et al. Heat stroke risk for open-water swimmers during long-distance events. Wilderness Environ. Med. 2013; 24:362–5.
      56. Cooper KE, Martin S, Riben P. Respiratory and other responses in subjects immersed in cold water. J. Appl. Physiol. 1976; 40:903–10.
      57. Datta A, Tipton M. Respiratory responses to cold water immersion: neural pathways, interactions, and clinical consequences awake and asleep. J. Appl. Physiol. (1985). 2006; 100:2057–64.
      58. Brown EB Jr., Miller F. Ventricular fibrillation following a rapid fall in alveolar carbon dioxide concentration. Am. J. Physiol. 1952; 169:56–60.
      59. Baker S, Atha J. Canoeists' disorientation following cold immersion. Br. J. Sports Med. 1981; 15:111–5.
      60. Croft JL, Button C, Hodge K, et al. Responses to sudden cold-water immersion in inexperienced swimmers following training. Aviat. Space Environ. Med. 2013; 84:850–5.
      61. Bougault V, Boulet LP. Airway dysfunction in swimmers. Br. J. Sports Med. 2012; 46:402–6.
      62. Mannocci A, La Torre G, Spagnoli A, et al. Is swimming in recreational water associated with the occurrence of respiratory illness? A systematic review and meta-analysis. J. Water Health. 2016; 14:590–9.
      63. Bougault V, Turmel J, Levesque B, Boulet LP. The respiratory health of swimmers. Sports Med. 2009; 39:295–312.
      64. Bonadonna L, La Rosa G. A review and update on waterborne viral diseases associated with swimming pools. Int. J. Environ. Res. Public Health. 2019; 16.
      65. Manasfi T, Coulomb B, Boudenne JL. Occurrence, origin, and toxicity of disinfection byproducts in chlorinated swimming pools: an overview. Int. J. Hyg. Environ. Health. 2017; 220:591–603.
      66. Chamberlain M, Marshall AN, Keeler S. Open water swimming: medical and water quality considerations. Curr. Sports Med. Rep. 2019; 18:121–8.
      67. Tipton MJ, Collier N, Massey H, et al. Cold water immersion: kill or cure? Exp. Physiol. 2017; 102:1335–55.
      68. Umarov J, Kerimov F, Toychiev A, et al. Association the 25(OH) vitamin D status with upper respiratory tract infections morbidity in water sports elite athletes. J. Sports Med. Phys. Fitness. 2019. doi:10.23736/S0022-4707.19.09834-7. [Epub ahead of print].
      69. Constantini NW, Arieli R, Chodick G, Dubnov-Raz G. High prevalence of vitamin D insufficiency in athletes and dancers. Clin. J. Sport Med. 2010; 20:368–71.
      70. Dubnov-Raz G, Rinat B, Hemila H, et al. Vitamin D supplementation and upper respiratory tract infections in adolescent swimmers: a randomized controlled trial. Pediatr. Exerc. Sci. 2015; 27:113–9.
      71. Senaris R, Ordas P, Reimundez A, Viana F. Mammalian cold TRP channels: impact on thermoregulation and energy homeostasis. Pflugers Arch. 2018; 470:761–77.
      72. Romanovsky AA. Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007; 292:R37–46.
      73. Nakayama T, Eisenman JS, Hardy JD. Single unit activity of anterior hypothalamus during local heating. Science. 1961; 134:560–1.
      74. Vriens J, Nilius B, Voets T. Peripheral thermosensation in mammals. Nat. Rev. Neurosci. 2014; 15:573–89.
      75. Castillo K, Diaz-Franulic I, Canan J, et al. Thermally activated TRP channels: molecular sensors for temperature detection. Phys. Biol. 2018; 15:021001.
      76. Almaraz L, Manenschijn JA, de la Pena E, Viana F. TRPM8. Handb. Exp. Pharmacol. 2014; 222:547–79.
      77. Zygmunt PM, Hogestatt ED. TRPA1. Handb. Exp. Pharmacol. 2014; 222:583–630.
      78. Zimmermann K, Lennerz JK, Hein A, et al. Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc. Natl. Acad. Sci. U. S. A. 2011; 108:18114–9.
      79. Latorre R, Brauchi S, Madrid R, Orio P. A cool channel in cold transduction. Physiology (Bethesda). 2011; 26:273–85.
      80. Morenilla-Palao C, Luis E, Fernandez-Pena C, et al. Ion channel profile of TRPM8 cold receptors reveals a role of TASK-3 potassium channels in thermosensation. Cell Rep. 2014; 8:1571–82.
      81. Story GM, Peier AM, Reeve AJ, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell. 2003; 112:819–29.
      82. Nakamura K. Central circuitries for body temperature regulation and fever. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011; 301:R1207–28.
      83. Zhao Y, Boulant JA. Temperature effects on neuronal membrane potentials and inward currents in rat hypothalamic tissue slices. J. Physiol. 2005; 564:245–57.
      84. Wechselberger M, Wright CL, Bishop GA, Boulant JA. Ionic channels and conductance-based models for hypothalamic neuronal thermosensitivity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006; 291:R518–29.
      85. Morrison SF, Nakamura K. Central neural pathways for thermoregulation. Front Biosci (Landmark Ed). 2011; 16:74–104.
      86. Zhang L, Jones S, Brody K, et al. Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am. J. Physiol. Gastrointest. Liver Physiol. 2004; 286:G983–91.
      87. Jansky L, Janakova H, Ulicny B, et al. Changes in thermal homeostasis in humans due to repeated cold water immersions. Pflugers Arch. 1996; 432:368–72.
      88. Tipton MJ, Eglin CM, Golden FS. Habituation of the initial responses to cold water immersion in humans: a central or peripheral mechanism? J. Physiol. 1998; 512(Pt 2):621–8.
      89. Smolander J, Mikkelsson M, Oksa J, et al. Thermal sensation and comfort in women exposed repeatedly to whole-body cryotherapy and winter swimming in ice-cold water. Physiol. Behav. 2004; 82:691–5.
      90. Johnson DG, Hayward JS, Jacobs TP, et al. Plasma norepinephrine responses of man in cold water. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 1977; 43:216–20.
      91. Daanen HA. Finger cold-induced vasodilation: a review. Eur. J. Appl. Physiol. 2003; 89:411–26.
      92. Siems WG, van Kuijk FJ, Maass R, Brenke R. Uric acid and glutathione levels during short-term whole body cold exposure. Free Radic. Biol. Med. 1994; 16:299–305.
      93. Dugue B, Smolander J, Westerlund T, et al. Acute and long-term effects of winter swimming and whole-body cryotherapy on plasma antioxidative capacity in healthy women. Scand. J. Clin. Lab. Invest. 2005; 65:395–402.
      94. Mila-Kierzenkowska C, Wozniak A, Boraczynski T, et al. Thermal stress and oxidant–antioxidant balance in experienced and novice winter swimmers. J. Therm. Biol. 2012; 37:595–601.
      95. Bansal A, Simon MC. Glutathione metabolism in cancer progression and treatment resistance. J. Cell Biol. 2018; 217:2291–8.
      96. Jansky L, Pospisilova D, Honzova S, et al. Immune system of cold-exposed and cold-adapted humans. Eur. J. Appl. Physiol. Occup. Physiol. 1996; 72:445–50.
      97. Brenner IK, Castellani JW, Gabaree C, et al. Immune changes in humans during cold exposure: effects of prior heating and exercise. J. Appl. Physiol. (1985). 1999; 87:699–710.
      98. Bittel J. The different types of general cold adaptation in man. Int. J. Sports Med. 1992; 13(Suppl. 1):S172–6.
      99. Launay JC, Savourey G. Cold adaptations. Ind. Health. 2009; 47:221–7.
      100. Daanen HA, Van Marken Lichtenbelt WD. Human whole body cold adaptation. Temperature (Austin). 2016; 3:104–18.
      101. Makinen TM. Different types of cold adaptation in humans. Front. Biosci. (Schol. Ed). 2010; 2:1047–67.
      102. Sawka MN, Castellani JW, Pandolf KB, Young AJ. Human adaptations to heat and cold stress. Dresden, NATO RTO-MP-076 2001:KN4-1-KN4-15.
      103. van Marken Lichtenbelt WD, Schrauwen P, van De Kerckhove S, Westerterp-Plantenga MS. Individual variation in body temperature and energy expenditure in response to mild cold. Am. J. Physiol. Endocrinol. Metab. 2002; 282:E1077–83.
      104. Park J, Kim S, Kim DH, et al. Whole-body cold tolerance in older Korean female divers “haenyeo” during cold air exposure: effects of repetitive cold exposure and aging. Int. J. Biometeorol. 2018; 62:543–51.
      105. Blondin DP, Labbé SM, Tingelstad HC, et al. Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J. Clin. Endocrinol. Metab. 2014; 99:E438–46.
      106. Simeckova M, Jansky L, Lesna II, et al. Role of beta adrenoceptors in metabolic and cardiovascular responses of cold exposed humans. J. Therm. Biol. 2000; 25:437–42.
        107. Simonsen L, Stallknecht B, Bülow J. Contribution of skeletal muscle and adipose tissue to adrenaline-induced thermogenesis in man. Int. J. Obes. Relat. Metab. Disord. 1993; 17(Suppl. 3):S47–51; discussion S68.
        108. Crow BT, Matthay EC, Schatz SP, et al. The body mass index of San Francisco cold-water swimmers: comparisons to U.S. national and local populations, and pool swimmers. Int. J. Exerc. Sci. 2017; 10:1250–62.
        109. Skreslet S, Aarefjord F. Acclimatization to cold in man induced by frequent scuba diving in cold water. J. Appl. Physiol. 1968; 24:177–81.
        110. Lazar JM, Khanna N, Chesler R, Salciccioli L. Swimming and the heart. Int. J. Cardiol. 2013; 168:19–26.
        111. Schmid JP, Morger C, Noveanu M, et al. Haemodynamic and arrhythmic effects of moderately cold (22 degrees C) water immersion and swimming in patients with stable coronary artery disease and heart failure. Eur. J. Heart Fail. 2009; 11:903–9.
        112. Neill WA, Duncan DA, Kloster F, Mahler DJ. Response of coronary circulation to cutaneous cold. Am. J. Med. 1974; 56:471–6.
        113. Marchant B, Donaldson G, Mridha K, et al. Mechanisms of cold intolerance in patients with angina. J. Am. Coll. Cardiol. 1994; 23:630–6.
        114. Stefenelli T, Sinzinger H, Sochor H, et al. Humoral regulation during cold-induced coronary arterial spasm. Int. J. Cardiol. 1989; 25:199–205.
        115. Rasmussen K, Bagger JP, Bottzauw J, Henningsen P. Prevalence of vasospastic ischaemia induced by the cold pressor test or hyperventilation in patients with severe angina. Eur. Heart J. 1984; 5:354–61.
        116. Tipton M, Bradford C. Moving in extreme environments: open water swimming in cold and warm water. Extrem Physiol Med. 2014; 3:12.
        117. Golden FS, Hervey GR, Tipton MJ. Circum-rescue collapse: collapse, sometimes fatal, associated with rescue of immersion victims. J. R. Nav. Med. Serv. 1991; 77:139–49.
        118. de Sousa CV, Sales MM, Rosa TS, et al. The antioxidant effect of exercise: a systematic review and meta-analysis. Sports Med. 2017; 47:277–93.
        119. Brannigan D, Rogers IR, Jacobs I, et al. Hypothermia is a significant medical risk of mass participation long-distance open water swimming. Wilderness Environ. Med. 2009; 20:14–8.
        120. Hellard P, Avalos M, Guimaraes F, et al. Training-related risk of common illnesses in elite swimmers over a 4-yr period. Med. Sci. Sports Exerc. 2015; 47:698–707.
        121. Khodaee M, Edelman GT, Spittler J, et al. Medical Care for Swimmers. Sports Med. Open. 2016; 2:27.
        122. Rama L, Teixeira AM, Matos A, et al. Changes in natural killer cell subpopulations over a winter training season in elite swimmers. Eur. J. Appl. Physiol. 2013; 113:859–68.
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