Original article

Z. CHECINSKA-MACIEJEWSKA1, E. MILLER-KASPRZAK1, A. CHECINSKA1, E. KOREK1,
M. GIBAS-DORNA1, A. ADAMCZAK-RATAJCZAK1, P. BOGDANSKI2, H. KRAUSS1

GENDER-RELATED EFFECT OF COLD WATER SWIMMING ON THE SEASONAL CHANGES IN LIPID PROFILE, ApoB/ApoA-I RATIO, AND HOMOCYSTEINE CONCENTRATION IN COLD WATER SWIMMERS

1Department of Physiology, Poznan University of Medical Sciences, Poznan, Poland; 2Department of Education and Obesity Treatment and Metabolic Disorders, Poznan University of Medical Sciences, Poznan, Poland
It has been proposed that regular cold swimming is associated with health benefits. However, the effect of cold adaptation on particular cardiovascular risk factors, within a single swimming season, remains unknown. Our aim was to evaluate the impact of cold water swimming on the seasonal changes in lipid profile and on apolipoprotein and homocysteine concentration in 34 cold water swimmers (CWS) aged 48 – 68 years. Blood samples were collected at the beginning (October), the middle (January), and the end (April) of the swimming season. Body mass (BM), total cholesterol (TC), high-density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides (TG), ApoB/ApoA-I ratio, and homocysteine concentrations were evaluated. In October, female CWS showed lower BM (P = 0.01), TG concentrations (P = 0.03), and ApoB/ApoA-I ratios (P = 0.008), and higher HDL (P = 0.01) than in men. Similar trends in BM (P = 0.002), HDL (P = 0.0006), and ApoB/ApoA-I ratio (P = 0.01) were seen in January, and for BM (P = 0.002), TG (P = 0.005), HDL (P = 0.003), and ApoB/ApoA-I (P = 0.01) in April. A decrease in TG concentration between January and April (P = 0.05), lower homocysteine concentration between October and January (P = 0.01), and between October and April (P = 0.001) were documented in CWS. A strong drop in homocysteine concentration was observed in female versus male CWS (P = 0.001 versus P = 0.032), particularly between October and April in women (P = 0.001) and October and January in men (P = 0.05). The ApoB/ApoA-I ratio in female CWS decreased over the season (P = 0.02), particularly between October and January (P = 0.05), and a trend toward the TG concentration to reduce over the swimming season was also observed in female CWS. No beneficial changes were noticed in the control group over the season. Our results suggest that the favorable effect of cold swimming on the cardiovascular risk factors may be gender-dependent; further studies are thus needed to draw a precise conclusion.
Key words:
cold water swimmers, cholesterol, high-density lipoprotein, low-density lipoprotein, triglycerides, homocysteine, apolipoproteins, cardiovascular risk

INTRODUCTION

Swimming in ice-cold natural water is an extreme activity that is practiced in many regions around the world, among them Scandinavia, Poland, Canada, Russia, and China. The healing properties of low temperature are also the basis of cold-air whole-body cryotherapy, which is used to treat arthritic diseases, muscle soreness, and sports injuries (1, 2). Regular cold swims are believed to improve the general well-being, as well several parameters associated with oxidative stress, immunology response, and the rheological, morphological, and biochemical blood profiles (3-5). On the other hand, an unhealthy effect of longtime regular winter swimming on cardiac and cerebrovascular risk has also been reported recently (6). Increased mortality associated with cardiovascular disease (CVD) implications is more frequently observed in the winter season (7). This data makes the influence of winter swimming on cardiovascular risk interesting to explore. The process of cold adaptation during repeated cold swims differs in nature from the initial cold water immersion, which induces a reaction known as cold shock (8, 9). Repeated cold exposure brings lower discomfort, in a process of habituation (9). CWS have been reported to possess better ability to cope with oxidative stress as a result of repeated exposure to cold and subsequent cold adaptation (7). To maintain core body temperature during cold exposure, both shivering and nonshivering components of thermogenesis are required (7, 10-13). Vybiral et al. observed the later onset of the shivering process in winter swimmers than in control subjects, and suggested nonshivering thermogenesis to be a significant part of the cold response in CWS (10-12). The involvement of brown adipose tissue (BAT) in the response to cold has been demonstrated in animal and human studies (14-16). Sympathetic activity due to cold exposure is involved in lipolysis and carbohydrate metabolism. Components of the lipid profile, as well as apolipoproteins B (ApoB) and AI (ApoA-I) involved in lipid transport, are proposed to be markers closely related to cardiovascular risk (17). Similarly, an increased concentration of a nonprotein amino acid, homocysteine, has been established as an independent risk factor for CVD (18-20). Recently, it has been demonstrated that male CWS are characterized by healthier lipid profile, lower ApoB/ApoA-I ratios, and lower homocysteine levels than moderately active men who had never participated in cold adaptation (7). Since it is well known that regularity of physical exercises is important for achieving health advantages, the influence of regular cold water swimming on the health of participants remains a promising, but still uncertain issue. The approach used to evaluate seasonal changes in the studied parameters in CWS seems to be helpful in explaining this phenomenon. Similarly, limited data is available on the differences between women and men in their reaction to seasonal cold swimming activity. Our recent studies suggest that gender response to repeated cold exposure might be dissimilar, and may be accompanied by increased insulin sensitivity, lower body mass index (BMI), and diminished fat free mass in female CWS than in men (21, 22). This raises the question of the potential effect of regular cold baths on the seasonal variability of other cardiovascular risk related parameters in female and male CWS.

The aim of the present study was thus to examine the effect of cold swimming on seasonal changes in lipid profile, the apolipoprotein B/A-I ratio, and homocysteine concentration in women and men adapted to cold water swimming.

MATERIALS AND METHODS

Study population

A total of 54 CWS were recruited to the study from the Kolobrzeg Walrus Club (KWC). Briefly, healthy volunteers who regularly swim outdoors in the winter season responded to an announcement posted on the KWC website and underwent a medical examination and an assessment of their general health condition. The exclusion criteria were diabetes, hypertension, dyslipidemia, acute chronic inflammatory diseases (such as rheumatoid arthritis and inflammatory conditions of the gastrointestinal tract), malignancy, and any pharmacotherapy. The control group consisted of 23 age-matched healthy individuals who performed moderate physical activity instead of cold water swimming during the study. All individuals gave their written consent to participate in the study. Participants who did not turn up for any one of the measurement checkpoints, because of reasons such as illness, noncompliance with the study rules, or withdrawn of consent, were excluded from further analysis. Of the 54 participants (22 women and 32 men) enrolled into the study, a total of 34 (16 women and 18 men) completed the swimming season.

The study was performed in accordance with the Declaration of Helsinki. The Ethical Committee of Poznan University of Medical Sciences approved the study (No. 1006/13).

The swimming season

CWS were exposed twice a week to the cold water of the Baltic Sea without protection during the six-month time window from October to April. The average seawater temperature was 9.5°C in October, 1.0°C in January, and 4.4°C in April. The exposure involved rapid entrance into the Baltic Sea after 15 min warm-up, and swimming comparable to recreational swimming between 3 – 6 metabolic equivalents (METS). The total cold water exposure lasted 5 – 10 min, and never exceeded 15 min. The control group involved age-matched healthy volunteers who performed walking for 45 min twice a week during the study. All participants were asked to maintain their normal diet and physical activity habits during the experiment. Individuals were asked to complete a food diary and to avoid using supplements. At three points in time, dietary data and a physical activity questionnaire were assessed to monitor conditions during the study. Living habits, additional exercise activity, and nutritional behavior were constant and comparable among individuals. To examine both the short and long impact of the cold water swimming on the participants’ parameters, we assessed anthropometric and biochemical measurements in the three checkpoints of October, January, and April.

Anthropometric and biochemical measurements

Body mass (BM) and BMI were measured in participants using a Tanita BC-418 MA 3 bioelectrical impedance analyzer. Peripheral venous blood samples were taken after an overnight fast from each participant, following 30 min of supine rest. Plasma total cholesterol (TC), low-density lipoprotein cholesterol (LDL), high-density lipoprotein cholesterol (HDL), and triglycerides (TG) were evaluated using a Dimension EXL with LM Integrated Chemistry System Analyzer (Siemens, Newark, NJ, US). Values for LDL cholesterol were estimated using the Friedewald formula. The intra-assay and interassay coefficients of variation were 1.3% and 0.8% for TC, 0.5% and 1% for TG, and 2.3% and 2.4% for HDL cholesterol, respectively. Plasma total homocysteine concentration was determined by immunoassay using an IMX analyzer (Abbott Laboratories, Princeton, US). ApoA-I and ApoB were assessed using the nephelometric method (23).

Statistical analysis

Statistical analysis was performed using Statistica for Windows 10.0 (StatSoft, Poland). The results were expressed as arithmetic means with standard errors or medians with a range. Student’s t-test was used to compare quantitative variables with normal distribution between groups. Variables that were not normally distributed were compared between groups by using the Mann-Whitney test. Repeated measure analysis of variance (ANOVA) with the appropriate Tukey’s HSD post-hoc test was applied for variables with normal distribution, in order to compare measurements at the three time points in the study. For data not following a normal distribution, a nonparametric Friedman ANOVA with Dunn’s post-hoc test was used to determine the seasonal changes in the variables. The effect sizes for the repeated measure ANOVA and Friedman ANOVA were reported as partial eta squared or Kendall’s W concordance values, respectively.

A P-value of less than 0.05 was considered significant.

RESULTS

The baseline characteristics of male and female CWS at the beginning of the swimming season in October, along with a comparison between groups, are shown in Table 1. The significant differences between groups involved lower BM (P = 0.01), TG concentration (P = 0.03), and ApoB/ApoA-I ratio (P = 0.008), and a higher HDL level (P = 0.01) in CWS women than in men. At the middle of the swimming season, in January, similar significant differences in the BM value (P = 0.002), HDL level (P = 0.0006), and ApoB/ApoA-I ratio (P = 0.01) were observed, while no changes were seen in TG concentration, between the CWS groups. At the end of the swimming season in April, the BM value and TG concentration was significantly higher in the CWS male group (P = 0.005), and there was a trend toward higher LDL concentrations (P = 0.06) in the male group, compared to the female group. In April, the women were characterized by decreased ApoB/ApoA-I ratios (P = 0.01) and increased HDL (P = 0.003), compared with the men. Detailed data are given in Table 2.

Table 1. Baseline characteristics of female and male cold water swimmers (CWS) at the beginning of the swimming season.
Table 1
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or median ranges; BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; TG, triglycerides; ApoB, apolipoprotein B; ApoA-I, apolipoprotein A-I; Ts, Student’s t-test; MW, Mann-Whitney test.
Table 2. Changes between female and male cold water swimmers (CWS) at the middle and end of the swimming season.
Table 2
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or median ranges; BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; TG, triglycerides; ApoB, apolipoprotein B; ApoA-I, apolipoprotein A-I; Ts, Student’s t-test; MW, Mann-Whitney test.

There were no statistically significant differences between CWS and the control group in terms of the evaluated parameters, except in the case of homocysteine. Compared to controls, CWS demonstrated significantly elevated homocysteine concentrations (P = 0.001). The baseline characteristics of the groups are given in Table 3. Analysis of the parameters between the three measurement points (October, January, and April) showed a statistically significant decrease in the concentration of TG over the course of the season (P = 0.04), particularly between its middle and end (P = 0.05). A statistically significant diminished level of homocysteine was observed in the CWS group (P = 0.0001) during the season, particularly with respect to the beginning and middle (P = 0.01) and the beginning and endpoint of the study (P = 0.001), as summarized in Table 4. The control group demonstrated a statistically significant increase in the seasonal TG concentration (P = 0.01) and the ApoB/ApoA-I ratio (P = 0.05) between October and January, and in TC (P = 0.05) between October and April (Table 5).

Table 3. Characteristic of cold water swimmers (CWS) and control volunteers.
Table 3
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or median ranges; BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; TG, triglycerides; ApoB, apolipoprotein B; ApoA-I, apolipoprotein A-I; Ts, Student’s t-test; MW, Mann-Whitney test.
Table 4. Seasonal changes in the parameters in cold water swimmers (CWS) group.
Table 4
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or median ranges; BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein; TC, cholesterol; TG, triglycerides; ApoB, apolipoprotein B; ApoA-I, apolipoprotein A-I; An, ANOVA; Fri, Friedman test (nonparametric repeated measures ANOVA); Dunn’s, Dunn’s multiple comparisons test; Tuk, Tukey’s Test; #, effect size (Kendall’s W concordance).
Table 5. Seasonal changes in the parameters in the control group.
Table 5
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or median ranges;
BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; TG, triglycerides; ApoB: apolipoprotein B; ApoA-I, apolipoprotein A-I; An, ANOVA; Tuk, Tukey’s test; *, effect size (partial eta squared).

A marked statistically significant drop in homocysteine concentrations over the swimming season was observed in the female CWS (P = 0.001), particularly between the beginning and the end of the season (P = 0.001). The ratio of ApoB to ApoA-I in females decreased significantly over the season (P = 0.02), reaching statistical significance between the beginning and the middle point (P = 0.05). A trend toward a reduction in TG concentration (P = 0.06) over the swimming season was observed in CWS women, but the difference was not quite significant. Detailed data are presented in Table 6. No statistically significant changes in the parameters were found in female controls over the season (Table 7). A statistically significant decreased level of homocysteine concentration (P = 0.05) was found in the CWS men between October and January (Table 6). A significant seasonal rise in the TG concentration and the ApoB/ApoA-I ratio between October and January (P = 0.05) was observed in the male controls (Table 7).

Table 6. Seasonal changes in the parameters in female and male cold water swimmers (CWS).
Table 6
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or medians with ranges; BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; TG, triglycerides; ApoB, apolipoprotein B; ApoA-I, apolipoprotein A-I; An, ANOVA; Fri, Friedman test (nonparametric repeated measures ANOVA) Dunn’s, Dunn’s multiple comparisons test; Tuk, Tukey’s test; #, effect size (Kendall’s W concordance).
Table 7. Seasonal changes in the parameters in female and male controls.
Table 7
Bold values indicate significant differences at P < 0.05. Data are presented as arithmetic means ± SDs or median ranges; BM, body mass; BMI, body mass index; TC, total cholesterol; LDL, low-density lipoprotein cholesterol; HDL, high-density lipoprotein cholesterol; TG, triglycerides; ApoB, apolipoprotein B; ApoA-I, apolipoprotein A-I; An, ANOVA; Fri, Friedman test (nonparametric repeated measures ANOVA); Dunn’s, Dunn’s multiple comparisons test; Tuk, Tukey’s test; *, effect size (partial eta squared).

DISCUSSION

Our study has demonstrated for the first time significant gender differences in cardiovascular risk parameters including homocysteine concentration, lipid profile, and ApoB/ApoA-I ratio in response to cold water swimming over a single season. No beneficial seasonal changes in the parameters we evaluated were found in age-matched controls, who had never participated in any type of voluntary cold exposure. We show that, although significant, favorable antiatherogenic changes in TG and homocysteine concentration are visible in the entire CWS population, more pronounced benefits were observed in the female swimmers, who showed a decrease in homocysteine concentration, ApoB/ApoA-I ratio, and a trend toward decreased TG; CWS men, in contrast, showed only reduced homocysteine levels over the swimming season.

The role of homocysteine in the development of atherosclerosis and cardiovascular risk has been a subject of several studies (18, 19, 24, 25). It has been demonstrated that gender differences do exist in plasma total homocysteine concentration and that male homocysteine levels are often higher than those of women; this is explained by the difference in fat free masses and estradiol concentrations between genders (24, 26). The CWS women in our study had similar concentrations of homocysteine to the CWS men, but were of perimenopausal or postmenopausal age. In the perimenopausal period, the level of sex hormones, including estradiol, may fluctuate greatly (27), and a relationship between serum homocysteine levels and endogenous estrogens has also been reported for postmenopausal women (26); taken together, these might explain our findings. It is noteworthy that, in our study, the mean homocysteine concentration in all CWS at the beginning of the season was slightly over 15 µmol/L - the limit considered safe for cardiovascular risk. This was a puzzling finding. It has been shown that plasma homocysteine concentration negatively correlates with BMI in healthy women (28). In our study, CWS women presented normal BMI, while the CWS men were overweight, but both groups showed similar homocysteine concentrations at the beginning of the swimming season. Plasma levels of homocysteine often increase after menopause, and this seemed to be in line with our results (29); however, in the age-matched controls, we did not observe the homocysteine levels that we found in the CWS. It may be the case that cold-adapted individuals are typically characterized by elevated homocysteine concentrations. This hypothesis could be supported by the study of Borione et al., who documented a prevalence of hyperhomocysteinemia in elite winter sport athletes, compared to control subjects (30). They demonstrated that 32% of winter athletes, as compared to 7.1% of control individuals, had homocysteine levels above the normal 15 µmol/l range (30).

In our study, homocysteine concentration significantly decreased during cold water adaptation in the entire CWS group, in contrast to the unchanged homocysteine level observed over the season in the control individuals. Male CWS exhibited a statistically significant drop in homocysteine concentration between October and January. Recently, Kralova Lesna et al. (7) examined the concentration of homocysteine in cold-adapted male swimmers at the end of the swimming season, and showed a significantly decreased concentration of homocysteine in this group, as compared to healthy, non-cold-adapted controls. Our six-month study provides a seasonal, repeated observation of homocysteine concentration in each individual, and additionally includes a female group. Interestingly, in our study, the more evident decreases in homocysteine concentration over the swimming season were observed for the CWS women, while no such seasonal changes were found in women from the control group. Our previous data showed that CWS women respond differently to repeated cold by changes in body composition parameters, including lower BMI and diminished fat-free mass (21). Recently, we have also demonstrated increased insulin sensitivity in female CWS, as compared to healthy women who did not participate in any cold swimming activity (22). The diminished levels of homocysteine observed in CWS over the swimming season may be explained by the involvement of oxidative stress associated with the cold adaptation process. Homocysteine can be converted in two main ways, one of which is through the transsulfuration pathway leading to glutathione synthesis from cysteine (20). The flux of homocysteine in the transsulfuration pathway under oxidative stress conditions was examined in hepatoma cell lines by Mosharov et al. (25), who confirmed that the pathway is regulated under oxidative conditions and that almost half of the intracellular glutathione pool in human liver cells derived from homocysteine (25). Sakr et al. have found that chronic exhaustive swimming in 26°C water, similarly to hypoxia, can induce oxidative stress in Sprague-Dawley rats (31). Swimming is also the basis of a forced swim test commonly used as an animal model for depressive-like behavior to test the action of antidepressants in animals (32). Kumral et al. have demonstrated that regular swimming exercise in lukewarm water, beneficially influences oxidative injury and modulates oxidative-antioxidative balance in Wistar albino rats after renovascular hypertension surgery (33). Recently, some studies have confirmed that cold stress adaptation during five months of winter swimming leads to adaptive changes in the oxidant-antioxidant status in humans (5, 34).

Statistically significant beneficial changes in TG concentration were observed in the CWS group over the swimming season, while control subjects demonstrated increased TG levels between October and January. The data on typical seasonal variation in TG level remain contradictory, and include variable TG concentrations from summer to winter (35-37). An in vitro study performed to estimate the effect of severe cold temperature on the cellular level demonstrated that cells secrete vehicle-like structures containing lipids in response to severe cold stress (38). Recently, Nie et al. performed an animal study to investigate the effect of cold exposure on the serum lipid profile (39), showing that cold exposure decreases TG concentration in C57BL/6 mice compared to controls. Activation of the sympathetic nervous system is a crucial part of cold adaptation, and is associated with nonshivering thermogenesis (12, 22). The activation of nonshivering thermogenesis by BAT is thought to explain cold adaptation (10, 12, 21). It has been suggested that BAT responds to cold by utilizing fatty acids derived from triglyceride lipolysis to produce heat; this activity has been suggested as a therapeutic approach to obesity (14). Although the BAT content of CWS participants was not examined in our study, we demonstrated that, during the cold adaptation process, TG concentrations significantly dropped in the entire CWS group between the middle and end of the swimming season, compared to the seasonal increase in TG concentration observed in the controls. A new finding is that, having examined the male and female CWS separately, only the latter showed a trend toward decreasing TG concentrations over the swimming season. Saito et al. studied seasonal BAT metabolic activation through the 2-[18F] fluoro-2-deoxyglucose (FDG) uptake associated with cold exposure in healthy individuals, finding that FDG uptake was more prominent in winter and decreased with increasing adiposity, as measured by BMI (15). The mean BM value of female CWS observed in our study was significantly lower than in CWS men, which may provide an explanation of the results. Because no such changes were noticed in the BM-matched female controls, the involvement of cold water swimming in the observed TG variation may serve as an explanation. Ockne et al. demonstrated that the amplitude of the seasonal variability in lipid profile is greater in women than in men (35). Together with our results, this may suggest that women are more predisposed to seasonal modifications of lipid profile by additional factors such as cold water exposure.

Over the course of the swimming season, the trend toward decreasing LDL concentration was found exclusively in CWS women, accompanied by stable seasonal LDL levels in the controls. Higher circulating VLDL-triglycerides in men compared to age-matched women have been reported (13). It has been found that fat oxidation during exercise is lower in men than in women (13). The effect of cold temperature on the lipid profile, including LDL concentration, has previously been demonstrated by Ziemman et al. in healthy men after sessions of whole body cryostimulation (40), and by Lubkowska et al. (41). Ziemman et al. also demonstrated a decrease in TC concentration after cryostimulation. CWS in our study did not show any significant changes in TC concentrations. Conversely, a seasonal increase in TC was found in the control group. The pattern of seasonal increase in TC during wintertime has previously been reported by others (35-37). Compared to the statistically significant result obtained for the controls, our finding seems to indicate the preventive potential of cold adaptation to influence the lipid profile in CWS.

Cold exposure leads to BAT activation and subsequent arteriosclerosis protection in an animal model of human-like metabolism of lipoproteins (16, 42). The antiatherogenic action of activated BAT depends on the clearance of lipoproteins enriched for ApoE via the LDL receptor (LDLR) pathway (16). Berbee et al. performed a study on hyperlipidemic APOE*3-Leiden.CETP mice that express LDLR and ApoE, confirming that BAT activation was involved in the decrease in TG, TC, and LDL cholesterol (16). Conversely, cold exposure promoted atherosclerotic changes in cold-acclimated ApoE –/– and LDRL–/– mice via deposition of lipids due to abrogated induction of lipolysis by cold (43). Prolonged exposure to cold in wild mice revealed decreased levels of both TC and TG. To confirm the clinical significance of these results, the authors recruited individuals with high baseline LDL levels to the study. After exposure for two days to cold (16°C), the individuals showed significant elevation of their LDL levels (43). Our results, obtained from CWS exposed to cold over one swimming season, do not support this observation. No significant seasonal changes in LDL concentration were observed in individuals characterized by elevated LDL level at baseline (data not shown). Female CWS demonstrated a trend toward decreasing LDL, while no such changes were found in female controls over the season. The discrepancy between results may be explained by the short time of cold exposure and the mild cold temperature applied by the authors, which suggest that both experimental factors are relevant to the careful investigation of cold adaptation benefits in humans. The intensity of cold stress may differentially influence that physiological response, as has been recently presented in a hypogonadal rat model by Islam et al. (44). It has been suggested that the short and long-term effects of cold exposure are dissimilar (6). Chondronikola et al. demonstrated, that the exact effect of nonshivering cold exposure on the modulation of lipid level may be delayed in humans (45).

The ApoB/ApoA-I ratio is a more informative and useful indicator of CVD risk than apolipoprotein concentrations considered separately, or with the traditional lipid profile (17). The large AMORIS study found that women were characterized by lower ApoB/ApoA-I ratios than men (17), similarly to the results observed in our CWS groups. Recently, Anagnostis et al. demonstrated that, in younger women, ApoB concentrations are lower than in men, but in the 50 – 55 age range, their values become similar to the concentrations found in men (46). This is, however, not very relevant for ApoB/ApoA-I, since the concentrations of ApoA-I remain elevated in postmenopausal women, compared to men (46). Nevertheless, in our study, the female CWS group was the one that was characterized by a statistically significant decrease in ApoB/ApoA-I ratio over the swimming season. This may suggest that winter swimming has, in this respect, more benefits for women than for men. This observation is confirmed by the absence of differences in ApoB/ApoA-I ratio in the female control group. Since ApoB is an integral LDL apoprotein, the fact that the trend toward lower seasonal LDL concentrations was observed exclusively in the female CWS group seems to be consistent. A transcriptome analysis performed by Shore et al. in female C57BL6 mice exposed to 24 h of cold temperature showed that, in response to cold, the liver expression of genes encoding ApoA-I and ApoB was downregulated (47). The impact of cold on the function of apolipoproteins thus needs to be elucidated in further studies.

Generally, cold water swimming is believed to act favorably on the health of swimmers. This been confirmed in our study and in those of others who have documented its positive effect on oxidative stress capacity, blood parameter patterns, insulin sensitivity, and even mood and memory of CWS (3, 4, 5, 21). There is, however, some data that disagrees with these conclusions. Gao et al., in a survey of 894 individuals enrolled in the Winter Swimming Organization in China for about 20 years, demonstrated a higher incidence of heart attack and cerebral vascular diseases in CWS than in the control group. The authors hypothesized that, while the short-term effects of cold water swimming may be beneficial to health, the long-term effects may be harmful (6). However, Gao et al. did not provide detailed data on the study population, including age, gender, length of active membership in the winter swimming organization, frequency of swimming, or the existence of any diseases, including heart disorders or other concomitant factors in winter swimmers. Cardiac arrhythmias are reported to be a consequence of cold water immersion and can be explained by autonomic conflict, a state when both limbs of the autonomic nervous system undergo simultaneous activation (48). In ischemic heart disease, the autonomic conflict may be more severe and proarrhythmic, due to oxygen consumption caused by tachycardia accompanied in patients by atherosclerosis and altered vessel dilatation (48). Knowledge of any such predisposing factors in these swimmers would thus seem to be important when drawing further conclusions regarding the results. Moreover, in the light of published data, differential conditions applied in the CWS studies, regarding the temperature of water or the duration of exposure, make the results difficult to compare, and they need to be carefully analyzed to establish the exact role of cold water swimming in the maintenance of well-being.

In our study, repeated cold water swims during the season were associated with plausible seasonal changes in lipid profile, apolipoprotein ratios, and homocysteine levels in winter swimmers, particularly in female CWS; these seem to be very promising results and to indicate the preventive and therapeutic potential of this extreme physical activity, which is worth exploring in further research.

Conflict of interests: None declared.

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R e c e i v e d : August 25, 2017
A c c e p t e d : December 27, 2017
Author’s address: Dr. Zuzanna Checinska-Maciejewska, Department of Physiology, Poznan University of Medical Sciences, 6 Swiecickiego Street, 60-781 Poznan, Poland. e-mail: zuchecinska@gmail.com