Clin Physiol Funct Imaging (2015)
doi: 10.1111/cpf.12252
The effects of exercise training under mild hypoxic conditions on body composition and circulating adiponectin in postmenopausal women Masato Nishiwaki1, Ryoko Kawakami2, Kazuto Saito3, Hiroyuki Tamaki4 and Futoshi Ogita3 1
Faculty of Engineering, Osaka Institute of Technology, Osaka, 2Department of Health Promotion and Exercise, National Institute of Health and Nutrition, Tokyo, 3Department of Sports and Life Sciences, National Institute of Fitness and Sports in Kanoya, Kanoya, and 4Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Niigata, Japan
Summary Correspondence Futoshi Ogita, Department of Sports and Life Sciences, National Institute of Fitness and Sports in Kanoya, 1 Shiromizu-cho, Kanoya, Kagoshima 891-2393, Japan E-mail: [email protected]
Accepted for publication Received 4 October 2014; accepted 17 March 2015
Key words adipokines; body fat; exercise; hypoxia; prescription; training
Purpose: This study aimed to examine the effects of exercise training under mild hypoxic conditions on body composition and circulating adiponectin levels in postmenopausal women. Methods: Fourteen postmenopausal women (56 1 years) were assigned to a normoxic (N group) or hypoxic (H group) exercise group. Aquatic exercise training was performed at an intensity of 50% peak oxygen uptake level for 30 min per training session, 4 days per week, for 8 weeks. The H group performed the exercise under hypobaric hypoxic conditions, which corresponds to 2000 m above sea level, and each participant was exposed to these conditions for 2 h per session. Results: After the training, no significant changes were observed in any of the measured values for the N group. Conversely, body mass (573 25 to 545 23 kg), body mass index (246 08 to 234 07 kg m 2), body fat (307 19 to 281 16%) and preperitoneal fat thickness as an index of visceral fat accumulation (103 17 to 64 10 mm) significantly reduced only in the H group. Circulating adiponectin levels significantly increased (95 18 to 114 20 lg ml 1), and the changes in adiponectin were significantly correlated with those in body mass (r = 081) and body mass index (r = 085). Conclusions: These results suggest that exercise training under mild hypoxic conditions could more effectively reduce body fat and increase adiponectin levels in postmenopausal women in a shorter period, than exercise training in normoxia.
Introduction Recent studies have shown that adiponectin, which is an adipose tissue-specific plasma protein, has anti-atherogenic, anti-inflammatory and insulin-sensitizing effects (Goldstein & Scalia, 2004; Berggren et al., 2005; Whitehead et al., 2006). Circulating adiponectin levels were lower in patients with type 2 diabetes, obesity and cardiovascular disease than healthy subjects (Goldstein & Scalia, 2004; Berggren et al., 2005; Whitehead et al., 2006). Furthermore, an increase in adiponectin levels occurs as a result of a marked reduction of body mass and/or fat following intervention or treatment (Yang et al., 2001; Hara et al., 2005; Bluher et al., 2006; Simpson & Singh, 2008; Yoshida et al., 2010; Moghadasi et al., 2011). Previous studies have also demonstrated changes in adiponectin levels associated with body mass reduction (Yang et al.,
2001; Balagopal et al., 2005; Giannopoulou et al., 2005; Hara et al., 2005). These results thus indicate that large losses of body mass and/or fat associated with exercise training result in an increase in adiponectin levels. Regular physical activity in hypoxia has been recently known to induce several beneficial adaptations (Bailey et al., 2000; Schobersberger et al., 2003; Haufe et al., 2008; Netzer et al., 2008; Wiesner et al., 2010; Nishiwaki et al., 2011; Morishima et al., 2013; Ogita et al., 2014; Shi et al., 2014). In particular, several reports have demonstrated that exercise training under mild-to-moderate hypoxic conditions (i.e. approximately 2000–2700 m above sea level, 3–4 days week 1, for 4–8 weeks) induces a reduction of body mass and fat and an increase in insulin sensitivity (Haufe et al., 2008; Netzer et al., 2008; Wiesner et al., 2010; Shi et al., 2014). We have also provided evidence that aquatic exercise
© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd
1
2 Hypoxic training and adiponectin, M. Nishiwaki et al.
_ 2 ) for 30 min per training [i.e. 50% peak oxygen uptake (VO training session] under mild hypoxic conditions induces a decrease in arterial stiffness in postmenopausal women (Nishiwaki et al., 2011). Although chronic hypoxia (approximately 4500–5000 m above sea level) elicits a significant increase in blood pressure (BP) even in healthy humans (Calbet, 2003; Lundby et al., 2008), such physiological responses are altered by the level of hypoxia, duration of exposure, and the intensity or type of physical activity (Gallagher & Hackett, 2004; Muza, 2007). In fact, several previous studies have shown that BP does not increase significantly after exercise in mild hypoxia or during intermittent hypoxic exposure at 4300 m above sea level (Schobersberger et al., 2003; Beidleman et al., 2004; Wiesner et al., 2010; Nishiwaki et al., 2011; Shi et al., 2014). Therefore, exercise training under mild hypoxic conditions can more effectively reduce cardiovascular and metabolic risk factors, than exercise training in normoxia. Previous studies have generally reported that postmenopausal women have an increase in cardiovascular and metabolic risk factors, such as high BP, dyslipidemia and high central adiposity, because estrogen levels, which is a female hormone, are dramatically reduced after menopause (BarrettConnor & Bush, 1991). Therefore, to reduce cardiovascular and metabolic diseases in aged women, the prevention and treatment of an increase in such risk factors found in postmenopausal women are of primary importance. Based on these previous findings, the aim of the present study was to examine the effects of exercise training under mild hypoxic conditions on body composition and circulating adiponectin levels in postmenopausal women. Our hypothesis was that exercise training in mild hypoxia would result in a reduction of body mass and fat even in postmenopausal women than exercise performed under normoxic conditions. Because hypoxic training was likely to induce a marked reduction of body mass and fat, we further hypothesized that these changes in body composition associated with hypoxic training would elicit an increase in circulating adiponectin levels in a shorter period, compared to exercise performed in normoxia.
Methods Subjects The subjects were 14 Japanese postmenopausal women. The mean values and standard error of the mean (SEM) for age, height and body mass were 56 1 years, 1525 12 cm and 561 17 kg, respectively. All participants were at least a few years past menopause, and the mean duration since menopause was 6 1 years. None of the women were receiving hormone replacement therapy, had a history of smoking or took any medication during the experimental period. Participants were divided into two groups matched for their physical fitness level and then randomized to either a normobaric normoxic (N group, n = 7) or hypobaric hypoxic (H group, n = 7) exercise group. All subjects were informed
about the procedures and risks of the study before providing written informed consent to participate. All study protocols were approved by the Ethics Committee for Human and Animal Experiments of the National Institute of Fitness and Sports (approval number: 16-39). The study was performed in accordance with the guidelines of the Declaration of Helsinki. Experimental procedures Each group was studied twice (i.e. before and after the training). All subjects were instructed to stop oral intake, with the exception of water, overnight 12 h before the tests. To avoid the acute effects of exercise or hypobaric hypoxia, participants were studied ≥24 h after their last exercise training session. All tests were conducted in a quiet air-conditioned room (22–24°C) under normobaric normoxic conditions. Exercise training Exercise training was conducted in a specific swimming pool located in a chamber in which atmospheric pressure could be regulated (Ogita & Tabata, 1992). As buoyancy effect reduces weight-bearing force on the skeletal joints, aquatic exercise is often used as a safer and easier type of exercise for the elderly and obese individuals, and thus aquatic exercise was chosen from exercise type in the present study (Nishiwaki et al., 2011). Aquatic exercise was performed for 30 min per training session, 4 days per week, for 8 weeks. The aquatic exercise programe was done with expert instructors who demonstrated this programme for the participants throughout the exercise period. The heart rate (HR) was measured continuously using a wireless HR monitor (Acculex Plus; Polar, New Hyde Park, NY, USA) in all training sessions. The receiver of HR monitor was fixed on the edge of pool, and HR during exercise was visually displayed to both subjects and instructors. The subjects were required to perform exercise maintaining approximately the target HR, which was predetermined from a cycling exercise (pretest), at _ 2 peak. To achieve the target HR, instrucan intensity of 50%VO tors also gave movement instructions to individual participants. Water level was set at around the xiphisternal level (water temperature 27–29°C). The N group performed exercise training under normobaric normoxic conditions (7493–7500 mmHg). On the other hand, the H group performed exercise training under hypobaric hypoxic conditions corresponding to 2000 m above sea level (6001–6038 mmHg). Because a previous study has demonstrated that hypoxic stimulus influences the changes in circulating metabolites and hormones in terms of substrate metabolism during exercise and the recovery over the total 2 h (Katayama et al., 2010), the subjects in H group were exposed to these conditions for 2 h per session. That is, the subjects in the H group performed 05 h of exercise and then had a rest for 15 h in the sitting position under hypobaric hypoxic conditions. Participants in both groups were instructed to maintain their normal diet and to refrain from any other specific exercise training throughout the study period.
© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd
4 Hypoxic training and adiponectin, M. Nishiwaki et al.
between both groups. Changes in parameters were analysed by two-way repeated-measures ANOVA (group 9 period) followed by the Tukey method for post hoc multiple comparisons. Student’s unpaired t-test and ANCOVA were conducted to remove the influences of initial levels of body composition and adiponectin levels from the training effects (Sugawara et al., 2004; Davis et al., 2009). To determine the relationship between changes in adiponectin and changes in body composition, adiponectin levels were log-transformed, as previously described (Ryan et al., 2003). Correlations were then analysed by Spearman’s correlation coefficient because of small number of
Body mass (kg)
80
N
80
70
70
60
60
50
50
40
40
30
pre
post
30
H
Results Baseline Before exercise training, there were no significant differences in any parameters between groups. Furthermore, no significant difference was observed in the target HR for exercise training between the N (88 3 beats min 1) and H (95 4 beats min 1) groups. (b)
*
BMI (kg/m2)
(a)
subjects (H group, n = 7). Results were regarded as statistically significant if P
doi: 10.1111/cpf.12252
The effects of exercise training under mild hypoxic conditions on body composition and circulating adiponectin in postmenopausal women Masato Nishiwaki1, Ryoko Kawakami2, Kazuto Saito3, Hiroyuki Tamaki4 and Futoshi Ogita3 1
Faculty of Engineering, Osaka Institute of Technology, Osaka, 2Department of Health Promotion and Exercise, National Institute of Health and Nutrition, Tokyo, 3Department of Sports and Life Sciences, National Institute of Fitness and Sports in Kanoya, Kanoya, and 4Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, Niigata, Japan
Summary Correspondence Futoshi Ogita, Department of Sports and Life Sciences, National Institute of Fitness and Sports in Kanoya, 1 Shiromizu-cho, Kanoya, Kagoshima 891-2393, Japan E-mail: [email protected]
Accepted for publication Received 4 October 2014; accepted 17 March 2015
Key words adipokines; body fat; exercise; hypoxia; prescription; training
Purpose: This study aimed to examine the effects of exercise training under mild hypoxic conditions on body composition and circulating adiponectin levels in postmenopausal women. Methods: Fourteen postmenopausal women (56 1 years) were assigned to a normoxic (N group) or hypoxic (H group) exercise group. Aquatic exercise training was performed at an intensity of 50% peak oxygen uptake level for 30 min per training session, 4 days per week, for 8 weeks. The H group performed the exercise under hypobaric hypoxic conditions, which corresponds to 2000 m above sea level, and each participant was exposed to these conditions for 2 h per session. Results: After the training, no significant changes were observed in any of the measured values for the N group. Conversely, body mass (573 25 to 545 23 kg), body mass index (246 08 to 234 07 kg m 2), body fat (307 19 to 281 16%) and preperitoneal fat thickness as an index of visceral fat accumulation (103 17 to 64 10 mm) significantly reduced only in the H group. Circulating adiponectin levels significantly increased (95 18 to 114 20 lg ml 1), and the changes in adiponectin were significantly correlated with those in body mass (r = 081) and body mass index (r = 085). Conclusions: These results suggest that exercise training under mild hypoxic conditions could more effectively reduce body fat and increase adiponectin levels in postmenopausal women in a shorter period, than exercise training in normoxia.
Introduction Recent studies have shown that adiponectin, which is an adipose tissue-specific plasma protein, has anti-atherogenic, anti-inflammatory and insulin-sensitizing effects (Goldstein & Scalia, 2004; Berggren et al., 2005; Whitehead et al., 2006). Circulating adiponectin levels were lower in patients with type 2 diabetes, obesity and cardiovascular disease than healthy subjects (Goldstein & Scalia, 2004; Berggren et al., 2005; Whitehead et al., 2006). Furthermore, an increase in adiponectin levels occurs as a result of a marked reduction of body mass and/or fat following intervention or treatment (Yang et al., 2001; Hara et al., 2005; Bluher et al., 2006; Simpson & Singh, 2008; Yoshida et al., 2010; Moghadasi et al., 2011). Previous studies have also demonstrated changes in adiponectin levels associated with body mass reduction (Yang et al.,
2001; Balagopal et al., 2005; Giannopoulou et al., 2005; Hara et al., 2005). These results thus indicate that large losses of body mass and/or fat associated with exercise training result in an increase in adiponectin levels. Regular physical activity in hypoxia has been recently known to induce several beneficial adaptations (Bailey et al., 2000; Schobersberger et al., 2003; Haufe et al., 2008; Netzer et al., 2008; Wiesner et al., 2010; Nishiwaki et al., 2011; Morishima et al., 2013; Ogita et al., 2014; Shi et al., 2014). In particular, several reports have demonstrated that exercise training under mild-to-moderate hypoxic conditions (i.e. approximately 2000–2700 m above sea level, 3–4 days week 1, for 4–8 weeks) induces a reduction of body mass and fat and an increase in insulin sensitivity (Haufe et al., 2008; Netzer et al., 2008; Wiesner et al., 2010; Shi et al., 2014). We have also provided evidence that aquatic exercise
© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd
1
2 Hypoxic training and adiponectin, M. Nishiwaki et al.
_ 2 ) for 30 min per training [i.e. 50% peak oxygen uptake (VO training session] under mild hypoxic conditions induces a decrease in arterial stiffness in postmenopausal women (Nishiwaki et al., 2011). Although chronic hypoxia (approximately 4500–5000 m above sea level) elicits a significant increase in blood pressure (BP) even in healthy humans (Calbet, 2003; Lundby et al., 2008), such physiological responses are altered by the level of hypoxia, duration of exposure, and the intensity or type of physical activity (Gallagher & Hackett, 2004; Muza, 2007). In fact, several previous studies have shown that BP does not increase significantly after exercise in mild hypoxia or during intermittent hypoxic exposure at 4300 m above sea level (Schobersberger et al., 2003; Beidleman et al., 2004; Wiesner et al., 2010; Nishiwaki et al., 2011; Shi et al., 2014). Therefore, exercise training under mild hypoxic conditions can more effectively reduce cardiovascular and metabolic risk factors, than exercise training in normoxia. Previous studies have generally reported that postmenopausal women have an increase in cardiovascular and metabolic risk factors, such as high BP, dyslipidemia and high central adiposity, because estrogen levels, which is a female hormone, are dramatically reduced after menopause (BarrettConnor & Bush, 1991). Therefore, to reduce cardiovascular and metabolic diseases in aged women, the prevention and treatment of an increase in such risk factors found in postmenopausal women are of primary importance. Based on these previous findings, the aim of the present study was to examine the effects of exercise training under mild hypoxic conditions on body composition and circulating adiponectin levels in postmenopausal women. Our hypothesis was that exercise training in mild hypoxia would result in a reduction of body mass and fat even in postmenopausal women than exercise performed under normoxic conditions. Because hypoxic training was likely to induce a marked reduction of body mass and fat, we further hypothesized that these changes in body composition associated with hypoxic training would elicit an increase in circulating adiponectin levels in a shorter period, compared to exercise performed in normoxia.
Methods Subjects The subjects were 14 Japanese postmenopausal women. The mean values and standard error of the mean (SEM) for age, height and body mass were 56 1 years, 1525 12 cm and 561 17 kg, respectively. All participants were at least a few years past menopause, and the mean duration since menopause was 6 1 years. None of the women were receiving hormone replacement therapy, had a history of smoking or took any medication during the experimental period. Participants were divided into two groups matched for their physical fitness level and then randomized to either a normobaric normoxic (N group, n = 7) or hypobaric hypoxic (H group, n = 7) exercise group. All subjects were informed
about the procedures and risks of the study before providing written informed consent to participate. All study protocols were approved by the Ethics Committee for Human and Animal Experiments of the National Institute of Fitness and Sports (approval number: 16-39). The study was performed in accordance with the guidelines of the Declaration of Helsinki. Experimental procedures Each group was studied twice (i.e. before and after the training). All subjects were instructed to stop oral intake, with the exception of water, overnight 12 h before the tests. To avoid the acute effects of exercise or hypobaric hypoxia, participants were studied ≥24 h after their last exercise training session. All tests were conducted in a quiet air-conditioned room (22–24°C) under normobaric normoxic conditions. Exercise training Exercise training was conducted in a specific swimming pool located in a chamber in which atmospheric pressure could be regulated (Ogita & Tabata, 1992). As buoyancy effect reduces weight-bearing force on the skeletal joints, aquatic exercise is often used as a safer and easier type of exercise for the elderly and obese individuals, and thus aquatic exercise was chosen from exercise type in the present study (Nishiwaki et al., 2011). Aquatic exercise was performed for 30 min per training session, 4 days per week, for 8 weeks. The aquatic exercise programe was done with expert instructors who demonstrated this programme for the participants throughout the exercise period. The heart rate (HR) was measured continuously using a wireless HR monitor (Acculex Plus; Polar, New Hyde Park, NY, USA) in all training sessions. The receiver of HR monitor was fixed on the edge of pool, and HR during exercise was visually displayed to both subjects and instructors. The subjects were required to perform exercise maintaining approximately the target HR, which was predetermined from a cycling exercise (pretest), at _ 2 peak. To achieve the target HR, instrucan intensity of 50%VO tors also gave movement instructions to individual participants. Water level was set at around the xiphisternal level (water temperature 27–29°C). The N group performed exercise training under normobaric normoxic conditions (7493–7500 mmHg). On the other hand, the H group performed exercise training under hypobaric hypoxic conditions corresponding to 2000 m above sea level (6001–6038 mmHg). Because a previous study has demonstrated that hypoxic stimulus influences the changes in circulating metabolites and hormones in terms of substrate metabolism during exercise and the recovery over the total 2 h (Katayama et al., 2010), the subjects in H group were exposed to these conditions for 2 h per session. That is, the subjects in the H group performed 05 h of exercise and then had a rest for 15 h in the sitting position under hypobaric hypoxic conditions. Participants in both groups were instructed to maintain their normal diet and to refrain from any other specific exercise training throughout the study period.
© 2015 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd
4 Hypoxic training and adiponectin, M. Nishiwaki et al.
between both groups. Changes in parameters were analysed by two-way repeated-measures ANOVA (group 9 period) followed by the Tukey method for post hoc multiple comparisons. Student’s unpaired t-test and ANCOVA were conducted to remove the influences of initial levels of body composition and adiponectin levels from the training effects (Sugawara et al., 2004; Davis et al., 2009). To determine the relationship between changes in adiponectin and changes in body composition, adiponectin levels were log-transformed, as previously described (Ryan et al., 2003). Correlations were then analysed by Spearman’s correlation coefficient because of small number of
Body mass (kg)
80
N
80
70
70
60
60
50
50
40
40
30
pre
post
30
H
Results Baseline Before exercise training, there were no significant differences in any parameters between groups. Furthermore, no significant difference was observed in the target HR for exercise training between the N (88 3 beats min 1) and H (95 4 beats min 1) groups. (b)
*
BMI (kg/m2)
(a)
subjects (H group, n = 7). Results were regarded as statistically significant if P
