Chinese Journal of Physiology

ORIGINAL ARTICLE
Year
: 2020  |  Volume : 63  |  Issue : 1  |  Page : 21--26

Acute and chronic effects of aerobic exercise on serum irisin, adropin, and cholesterol levels in the winter season: Indoor training versus outdoor training


Serhat Ozbay1, Süleyman Ulupınar2, Engin Şebin3, Konca Altınkaynak4,  
1 Department of Faculty of Sport Sciences, Erzurum Technical University, Erzurum, Turkey
2 Department of Faculty of Sport Sciences, Graduate School of Health Sciences, Hacettepe University, Ankara, Turkey
3 Department of Biochemistry, Erzurum Regional Education and Research Hospital, Erzurum, Turkey
4 Department of Medical Biochemistry, School of Medicine, University of Health Sciences, Istanbul, Turkey

Correspondence Address:
Dr. Süleyman Ulupınar
Faculty of Sport Sciences, Graduate School of Health Sciences, Hacettepe University, Ankara
Turkey

Abstract

The aim of this study is to investigate the acute and chronic effects of aerobic training performed indoors and outdoors on irisin, adropin, and cholesterol levels in winter. Thirty-two healthy males participated in this study. Participants were divided into two groups: outdoor group (n = 16) and indoor group (n = 16). They then performed 40-min aerobic running exercises 4 days/week for 18 weeks. The outdoor group trained at −5°C–5°C environmental temperature, while the indoor group trained at 21°C–25°C. Blood samples were collected before and after the 18-week training period and immediately after the first training. The results showed that single aerobic exercise induced minimal increase in serum irisin concentrations in both groups. In addition, irisin levels did not change in the outdoor group but significantly decreased in the indoor group after the 18-week training period. Aerobic exercise had no acute or chronic effects on serum adropin levels in the indoor group. However, the aerobic training caused a decrease in adropin levels chronically, but there was no acute effect after single aerobic exercise in the outdoor group. Furthermore, there was no acute effect on high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol, and total cholesterol after single aerobic exercise in both groups. However, after the 18-week training period, there was a significant increase in HDL-C levels in both groups. Moreover, the increase in HDL-C in the outdoor group was higher than in the indoor group. Thus, this study provides evidence for the beneficial chronic effects of aerobic exercise and cold on HDL-C levels as well as the beneficial acute effects on irisin concentrations.



How to cite this article:
Ozbay S, Ulupınar S, Şebin E, Altınkaynak K. Acute and chronic effects of aerobic exercise on serum irisin, adropin, and cholesterol levels in the winter season: Indoor training versus outdoor training.Chin J Physiol 2020;63:21-26


How to cite this URL:
Ozbay S, Ulupınar S, Şebin E, Altınkaynak K. Acute and chronic effects of aerobic exercise on serum irisin, adropin, and cholesterol levels in the winter season: Indoor training versus outdoor training. Chin J Physiol [serial online] 2020 [cited 2020 Feb 26 ];63:21-26
Available from: http://www.cjphysiology.org/text.asp?2020/63/1/21/277955


Full Text

 Introduction



Earlier studies have demonstrated numerous benefits of exercise, and current studies have investigated the more specific effects of exercise components, such as the type, duration, intensity, frequency, and resting time.[1],[2] Environmental temperature is one of the factors that may impact the effects of exercise on human metabolism. Evidence that shows cold exposure increases energy expenditure and improves metabolic rate suggests that cold environments have stress effects similar to exercise.[3],[4] People who adapt to cold environments are supposedly more resistant to metabolic disorders, possibly due to maintenance of larger amounts of brown adipose tissue.[5] Moreover, novel studies have investigated whether exercise-induced myokines related to browning of adipose tissue can be alternative solutions for the prevention of metabolic disorders.[6],[7]

Irisin is produced by proteolytic cleavage of fibronectin type III domain-containing protein 5 (FNDC5), and it has been suggested that this myokine induces thermogenesis, reduces body weight, and improves glucose homeostasis.[8] Irisin composed of 112-amino acid glycosylated protein hormone, and irisin amino acid sequences are identical in humans, mice, and rats.[9],[10] Emerging novel findings have suggested that irisin could affect the brown adipose tissue activation and thus could increase energy expenditure.[11] Irisin, induced by submaximal exercise or cold, is believed to be a factor that causes the browning of adipose tissue to compensate for the increased demand for fat or glucose oxidation.[12] The first studies conducted after the discovery of irisin[9] were presented as a hopeful approach in the prevention of health-threatening, major diseases such as obesity and type 2 diabetes. However, many contradictory results have been observed in subsequent studies.[8],[13],[14]

Adropin was first isolated in 2008 by Kumar et al., and it was suggested that it could play an important role in lipid metabolism.[15],[16] Adropin contains 76 amino acids, and human, mouse, and rat adropin amino acid sequences are identical, like irisin.[15],[16] Adropin protects against obesity-associated hyperinsulinemia and hepatosteatosis by maintaining the balance of lipid and glucose metabolism, since peptides secreted by peripheral tissues can regulate lipid metabolism in key insulin-target tissues.[15],[17],[18] Previous studies reported that elevated adropin concentration in circulation reduced insulin resistance and glucose intolerance that occurred in response to metabolic stress.[15],[17],[19] Fujie et al.[20] reported that aerobic exercise intervention significantly elevated serum adropin levels in elderly subjects and suggested that arterial stiffness could be improved by increasing the adropin levels via aerobic exercise interventions.

In addition to available medical treatments, aerobic exercise has been shown to improve the prognosis of cardiovascular diseases, and furthermore, aerobic exercise can be applied without side effects, unlike medications.[21] Previous studies have consistently indicated that increased low-density lipoprotein cholesterol (LDL-C) levels or decreased high-density lipoprotein cholesterol (HDL-C) levels are associated with an increased risk of myocardial infarction and vascular death.[22],[23] Therefore, the basic approach for preventing cardiovascular risk is to increase HDL-C concentrations or to decrease LDL-C concentrations.[21] Studies involving the exercise trial have shown that HDL-C levels are more sensitive to aerobic exercise than LDL-C.[21],[24] Studies investigating the effects of aerobic exercise usually include single acute exercise trials. Furthermore, the combined effects of the cold and aerobic exercise on mediators such as adropin and irisin, or cholesterol levels, are not clear. Therefore, the aim of this study is to investigate the acute and chronic effects of long-term aerobic training performed indoors and outdoors on irisin, adropin, and cholesterol levels in winter.

 Materials and Methods



Participants

Thirty-two healthy males participated in this trial. The inclusion criteria were as follows: At least 18 years of age and no chronic medical condition requiring regular prescription medication. All participants were informed about possible risks related to experimental procedures and gave written informed consent to participate in this study. The research protocol was approved by the Ethics Committee of Erzurum Regional Education and Research Hospital (ERERH-37732058-514.10).

Anthropometric measurements

The participants' height was measured with a portable stadiometer (Holtain Ltd, Crosswell, Crymych, Dyfed, UK). Body weights and body fat percentage were measured using Tanita body composition and weighting scale (BC-310; Tanita Corp., Tokyo, Japan).

Experimental protocols

Participants performed 40 min of long-term, aerobic running exercises 4 days/week for 18 weeks. The outdoor group performed outdoor training at −5°C–5°C environmental temperature, while the indoor group performed indoor training at 21°C–25°C. Participants completed the exercises at a standard velocity of 65%–70% (50%–55% VO2max) of their maximum heart rate (HR). The maximum HR was calculated according to the Karvonen formula (220 − age). To control running speeds, the HR was followed simultaneously with the telemetric HR monitor during the exercise (S610i, Polar Electro Oy, Kempele, Finland). Participants' attendance at training was recorded. The outdoor group had an attendance rate of 97.6%; and the indoor group had an attendance rate of 98.2%. To measure plasma irisin, adropin, and cholesterol levels, 10 mL of venous blood was taken from an antecubital vein before the 18-week training period, immediately after the first training, and 24 h after the 18-week training period. Participants were asked to fast for 3–4 h before participating in trainings, maintain their normal daily meal routines, and not to use any stimulant or supplement during the study period. Environmental temperature was recorded via a digital thermometer. The indoor group dressed as they wished, but the outdoor group wore three layers of clothing: The skin-contact inner layer was lightweight polyester or polypropylene, the middle layer was polyester fleece or wool, and they also wore windproof outer layer.

Biochemical measures

Venous blood samples were withdrawn from the antecubital vein in aprotinin-containing tubes after 3 h of fasting. Serum was separated immediately by centrifuging at 4000 rpm at 4°C for 5 min. The samples were then frozen and stored at −80°C until participants completed all trainings. Irisin and adropin concentrations were measured using a commercially available enzyme immunoassay kit (Human irisin ELISA kit 201-12-5328, SunRed, China; Human adropin ELISA kit 201-12-2015, SunRed, China) with intra- and inter-assay coefficients with a variation of 10.0% and 12.0%, respectively. The blood samples were analyzed in a double-blind fashion.

Statistical analysis

Statistical analysis was performed using SPSS 21.0 version (IBM SPSS Statistics for Windows, Armonk, NY, USA). All data were presented as mean ± standard deviation. A P < 0.05 was accepted as statistically significant. Independent t-test was used to determine the significance between the groups (indoor vs. outdoor). Paired t-test was used to determine the significance between before and after 18 weeks. The effect size (0.2–0.5: small; 0.5–0.8: medium; >0.8: large) was calculated to determine practical importance (Cohen). Repeated-measures two-way ANOVA test was used to determine the significance in the group × time interactions. Bonferroni post hoc test was used to determine the difference among the measurement points in cases F-statistics were significant. Mauchly's test of sphericity was used to control the assumption of sphericity. In cases where the assumption could not be provided, Greenhouse–Geisser correction was applied if the epsilon value (ε) was <0.75, and Huynh–Feldt correction was applied if the ε value was >0.75. In addition, partial eta squared values were calculated to determine the effect size of training interventions on dependent variables.

 Results



There was no significant difference between the groups in the descriptive characteristics and blood parameters at baseline [Table 1].{Table 1}

In both groups, there was no significant difference in body mass before and after the 18-week training period; however, body fat percentage values significantly increased following the 18-week training period in both groups [Table 2].{Table 2}

Serum irisin concentration significantly increased after the first training, whereas it significantly decreased after the 18-week training period compared to baseline in the indoor group. However, irisin concentration significantly increased after the first training but remained unchanged after the 18-week period compared to baseline in the outdoor group [Table 3]. Serum adropin concentration remained unchanged after the first training in both groups; however, it significantly decreased after the 18-week period in the outdoor group but remained unchanged after the 18-week period in the indoor group. HDL-C values remained unchanged after the first training and significantly increased after the 18-week period in both groups. However, the increased amount in the outdoor group after the 18-week period was higher than in the indoor group. LDL-C and total cholesterol values remained unchanged both after the first training and the 18-week period in both groups [Table 3].{Table 3}

 Discussion



This study investigated the acute and chronic effects of long-term aerobic training performed in different environmental temperatures on serum irisin, adropin, and cholesterol levels. In novel studies on obesity, which has increased exponentially in recent years, new strategies that aim to increase metabolic energy expenditure have been investigated. Exercise-induced factors that are secreted from the skeletal muscle have been thought to provide great advantages in the prevention and treatment of many metabolic disorders, particularly obesity.[25] In addition, it was reported that cold exposure activates the sympathetic nervous system in a similar way to exercise, increasing metabolic rate, thus burning triglyceride stores.[26],[27] This study provides evidence for that aerobic exercise induces an acute increase in irisin concentrations, but the data have not shown a chronic increase after the 18-week training period. This study provides evidence for the beneficial acute effects of aerobic exercise on irisin concentrations as well as the beneficial chronic effects on HDL-C levels. In addition, this study has revealed that outdoor aerobic exercise performed in a cold environment caused a higher increase in HDL-C levels than indoor aerobic exercise.

Irisin, induced by submaximal exercise or cold, is a myokine derived from FNDC5 that transforms white fats to brown-fat-like.[3],[9] The first studies conducted after the discovery of irisin[9] investigated an alternative approach to the prevention of major health-threatening diseases such as obesity and type 2 diabetes. However, many contradictory results have been observed in subsequent studies. Current investigations have indicated that acute and transient elevation of irisin level following exercise is the most accepted understanding.[28],[29] For example, a previous study found an increase in irisin level immediately after treadmill exercise in mice.[30] However, another study showed that rats with metabolic syndrome that performed swimming exercise for 30 min/day for 4 weeks had no significant change in irisin levels.[31] On the other hand, Nygaard et al.[29] revealed that irisin levels significantly increased both after 60 min of aerobic training and 60 min of strength training. Löffler et al.[28] reported an increase in serum irisin levels after both 15 min of cycling exercise and 30 min of walking, gymnastics, and sprint exercises. However, they conducted a 6-week regular exercise program in the same study and found no significant change in irisin levels. Similarly, in a previous study, healthy adults underwent a cycling training program for 3 days/week for 12 weeks and no significant changes were found in irisin levels. As in the aforementioned studies, this study revealed that irisin concentration increased following aerobic exercise, but that this increase was not permanent. Furthermore, after the 18-week training period in the winter season, irisin concentration decreased in the indoor group, but there was no change in the irisin levels in the outdoor group. Similar to the present study, Hew-Butler et al.[32] applied a 5-km aerobic running training program for 10 weeks and found that although subjects' aerobic capacity improved, irisin concentrations tended to decrease. In a comprehensive review, it was emphasized that regular exercise was not a major determinant for increasing UCP-1 expression, but this effect could increase if cold and exercise are combined.[33] Coker et al.[4] measured the serum irisin concentrations of eight healthy adults during Yukon Arctic Ultra event (430 miles; the temperature during the event ranged from −45°C to −8°C), which is the longest and coldest ultra-endurance event in the world. They indicated that cold exposure and extreme physical exertion promoted a significant increase in serum irisin level. Hence, this study supported the findings of many studies that have shown that irisin concentrations increased following aerobic exercise, as well as suggesting that this effect could be increased when aerobic exercise was combined with cold.

Adropin has been reported to be effective in preventing adiposity, insulin resistance, and impaired glucose tolerance and could be beneficial for cardiovascular health by regulating blood flow and capillary density.[15],[34] Ganesh-Kumar et al.[19] showed that adropin levels were negatively correlated with age and body mass index, while age-adjusted adropin levels were higher in males than females. On the other hand, there are conflicting findings in several previous studies examining the relationships between aerobic exercise and adropin concentrations. Fujie et al.[20] found that serum adropin levels increased approximately 75% after 8 weeks of regular aerobic exercise. Fujie et al.,[35] in another study, indicated that aging reduced serum adropin levels, whereas aerobic exercise significantly increased adropin levels in mice. On the other hand, in a previous study, rats performed 30 min of swimming exercise per day for 4 weeks and no significant change in adropin levels was observed. Alizadeh et al.[17] investigated the acute effect of 30 min of aerobic exercise on adropin, glucose, insulin level, and insulin resistance in 24 overweight women. They found that aerobic exercise was effective on insulin level and for insulin resistance, but not effective on glucose and adropin. The findings from this study showed that neither environmental temperature nor aerobic exercise had an acute effect on adropin concentrations. However, adropin levels decreased significantly when trainings were held outdoors, whereas adropin levels did not show any significant changes when trainings were held indoors following the 18-week training period, which was performed during winter.

It is known that exercise not only has positive effects on physical fitness, strength, and endurance characteristics but also helps to improve lipids profile.[21] HDL-C is a valid and consistent predictor of cardiovascular events, which has been proven by many different prospective studies.[36] The previous studies investigating the chronic effects of exercise on HDL-C consistently observed that exercise increased HDL-C levels.[37],[38] However, the effect of aerobic exercise on LDL-C and total cholesterol is not clear. LeMura et al.[39] found a decrease in LDL-C and total cholesterol after a 16-week exercise period, while O'Donovan et al.[37] found an increase in LDL-C and total cholesterol after a 24-week exercise period. It was proven that both a cold environment and aerobic exercise could affect the concentration of fatty acids because the concentration of fatty acids is largely unaffected by maximal exercise but increases after submaximal exercises and cold exposure.[3],[26] This study indicated that the 18-week aerobic exercise period significantly increased HDL-C levels, and this amount increased further when aerobic exercises were combined with a cold environment temperature. However, both aerobic exercise and cold exposure had no significant effect on LDL-C and total cholesterol following the 18-week training period.

 Conclusions



Aerobic exercise induced minimal increases in serum irisin concentrations. In addition, it was observed that irisin levels did not change after the 18-week training period when aerobic exercise and cold exposure were combined, but irisin levels decreased significantly when aerobic exercises were performed at normal temperature (21°C–25°C). It was also found that aerobic exercise performed at normal temperature had no acute or chronic effect on adropin levels. However, aerobic exercise performed in a cold environment caused a chronic decrease of adropin but had no acute effect. Furthermore, the findings of this study indicated that aerobic exercise and cold have no acute effect on HDL-C, LDL-C, and total cholesterol. However, aerobic exercise provided a significant chronic increase in HDL-C values. Moreover, the increased amount rose further when aerobic exercises were performed in a cold environment.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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