Effects of Aerobic Exercise Training on Serum Sex Hormone Binding Globulin,Body Fat Index,and Metabolic Syndrome Factors in Obese Postmenopausal Women

Abstract

Background:

The percentage of obese postmenopausal women with metabolic syndrome is rising, and physical factors associated with the metabolic syndrome prevalence or incidence are also rising, including high body mass index (BMI), visceral fat area (VFA), low plasma sex hormone-binding globulin (SHBG) levels, and low cardiorespiratory fitness. Therefore, we investigated the influence of aerobic exercise on SHBG, body fat index (BFI), and metabolic syndrome factors in obese postmenopausal Korean women.

Methods:

Thirty healthy postmenopausal, women aged 53.46±2.4 years and with over 32% body fat, were randomly assigned to an aerobic exercise group (EX; n=15) or to a “nonexercise” control (Con; n=15) group. The primary outcome measurements were serum SHBG, lipid profiles, insulin levels, and metabolic syndrome factors. Secondary outcome measurements were body composition, VFA, blood pressure (BP), and homeostasis model assessment of insulin resistance (HOMA-IR).

Results:

Posttraining body weight and BFI (P<0.05), total cholesterol, glucose, and insulin levels (P<0.01), BP, and HOMA-IR (P<0.001) decreased, whereas SHBG (P<0.001) and metabolic syndrome factors (P<0.01) improved in the exercise group but not in the control group. SHBG levels also showed a significant positive correlation with high-density lipoprotein cholesterol (HDL-C) and significant negative correlations withglucose, diastolic blood pressure, fat mass, BMI, and percent body fat (P<0.05).

Conclusions:

Our findings indicate that aerobic exercise improves body composition, SHBG, insulin levels, and metabolic syndrome factors. These findings suggest that in obesepostmenopausal Korean women, 16 weeks of aerobic exercise is effective for preventing the metabolic syndrome caused by obesity.

Introduction

O verweight and obesity are conditions that are reaching epidemic proportions in both the developed and the developing worlds, although the tracking of this phenomenon is somewhat complicated by variability in the definitions for overweight and obesity. In the Korea, 35.6% of men and 26.5% of women are classified as overweight. About 80% of obese adults are afflicted with at least one disease, and 40% have two or more of the diseases associated with obesity, such as hypertension, cancers, gallbladder disease, type 2 diabetes, and cardiovascular disease.¹

Sex hormone-binding globulin (SHBG) is the main transport protein for testosterone and estradiol in plasma and regulates the bioavailability of sex steroids to target cells.² It is mainly synthesized in the liver³ and binds testosterone with high affinity and estradiol with somewhat lower affinity. Hyperandrogenemia in women is associated with visceral obesity, insulin resistance, low high-density lipoprotein cholesterol (HDL-C), and increased plasminogen activator inhibitor-1 (PAI-1) and triglycerides.⁴ In postmenopausal women, it has been shown that SHBG also correlated positively with HDL-C⁵ and inversely with body mass index (BMI), the amount of body fat, and body composition.^6,7 Several studies show a relationship between low levels of SHBG and central obesity, hyperglycemia, hyperinsulinemia, and lipid profiles.^8
–10 In addition, SHBG is associated with insulin resistance and metabolic syndrome.^11,12 Therefore, it is known that low SHBG levels could be predictive for metabolic syndrome incidence and could be a marker for insulin resistance.^11,13

Numerous research studies have investigated the beneficial effects of physical activity on the measures of obesity and cardiometabolic risk factors as well as increasing insulin sensitivity and improving metabolism.^14

–17 However, to our knowledge, the relationship of SHBG, body fat index (BFI), and metabolic syndrome factors has not been investigated in obese postmenopausal women. The fact that the percentage of obese postmenopausal women with metabolic syndrome is rising and physical factors associated with the metabolic syndrome prevalence or incidence, including high BMI, visceral fat area (VFA), body composition, low plasma SHBG levels,⁶ and low cardiorespiratory fitness, are also rising.¹⁸ Moreover, little is known about the role of SHBG in regard to BFI and metabolic syndrome risk factors in the Korean population. Thus, the purpose of this study was to investigate the effects of aerobic exercise on serum SHBG, BFI, and metabolic syndrome factors in obese postmenopausal Korean women.

Materials and Methods

Participants

Thirty healthy, obese [percentage of body fat (%BF), >32%] postmenopausal women of similar age (54.53±2.82 years) from the Busan metropolitan area provided an informed written consent to participate in this study. The participants were considered postmenopausal if they had not menstruated for at least 1 year and their plasma follicle-stimulating hormone (FSH) levels were higher than 30 mIU/mL. All women were sedentary, did not regularly participate in physical activity (defined as <20 min of exercise twice a week), had no history of drug or alcohol abuse or cardiovascular disease, had stable weight (±2 kg weight change in 3 months), and were not taking hormones or other medications known to influence serum lipid levels or body composition. The women were categorized as nonsmokers. The health of the participants was determined by a health questionnaire, physical examination, and laboratory tests. All participants gave a written informed consent form approved by the Institutional Human Research Committee.

Study design

The nature and goals of the study were thoroughly explained to the women, and they provided written informed consent before participating in the study. The participants were tested in the morning, at the same time of day, to avoid diurnal variation of temperature. Participants were asked to refrain from exercise for 24 h before testing and from caffeine ingestion on testing days. Upon arrival, a 12-h fasting blood sample was obtained, and measurements of anthropometry, resting blood pressure, and body composition were performed. After this first visit, women were randomized to an aerobic exercise group (n=15) or to a “nonexercise” control group (n=15) for 16 weeks.

Body composition and anthropometric assessment

Blood pressure (BP) was measured twice in the right arm after 15 min of rest in the supine position in a quiet environment, and the mean of the two recordings was calculated. Height was measured to the nearest 0.1 cm using a stadiometer with the subject barefoot, and weight was recorded to the nearest 0.1 kg using a standardized electronic digital scale with light clothes. From these measurements, body mass index (BMI) was calculated as weight in kilograms divided by the square of height in meters (kg/m²). Waist circumference (WC) was measured to the nearest 0.1 cm at the narrowest point between the lowest rib margin and the iliac crest, and hip circumference was measured in a horizontal plane at the maximal circumference of the hips or buttocks region, whichever is above the gluteal fold. BF, lean body mass (LBM), fat mass (FM), and VFA were measured at the beginning and end of each phase using bioelectrical impedance analysis method (InBody 720; Biospace, Seoul, Korea) following the procedures recommended by the American College of Sports Medicine.¹⁹

Blood sampling

Venous blood samples were drawn between 8 and 10 a.m. after a 12-h overnight fast, and the serum was separated and stored at −70°C. Glucose concentrations in fasting serum, total cholesterol (TC), triglycerides (TG), HDL-C, and low-density lipoprotein cholesterol (LDL-C) were measured using a Toshiba TBA 200FR NEO analyzer (Diamond Diagnostics, Inc., Holliston, MA). Serum insulin concentration was measured by immunoradiometric assay using an insulin kit (Coat-A-count Insulin, DPC, USA) and γ-counter (COBRA 5010 Quantum, PACKARD, USA). The index of insulin resistance was estimated using the homoeostasis model of assessment of insulin resistance (HOMA-IR), as HOMA-IR=[fasting insulin (μU/mL)×fasting glucose (mmol/L)]/22.5.²⁰ Serum SHBG was measured using an Immunoradiometric Assay (IRMA) kit (BIOCODE S.A., Liege, Belgium), sensitivity 3 nmol/L, intraassay CV 2.1 ∼4.5% and interassay CV 4.7 ∼12.2%.

Aerobic exercise program

The exercise intervention line dance was taught and practiced three times a week for 60 min per session on nonconsecutive days by the aerobic exercise group, at a specified intensity based on age-predicted maximal heart rate (HRmax) for 16 weeks. The intensity of exercise was initially set at 55%–65% of the age-predicted HRmax and was gradually increased by 5% every 4 weeks until 70%–80% of the age-predicted HRmax was reached (stage 1=55%–65%; stage 2=60%–70%; stage 3=65%–75%; stage 4=70%–80%). All aerobic exercise sessions were verified by direct supervision and/or the use of a heart rate monitor (Polar Electro Inc.) that was recording. All exercise sessions took place at a research fitness center under the supervision of a certified exercise specialist. The line dance exercise program required participants to step and/or balance in one of many combinations; they could move forward, backward, left, right or on the spot, with turns of either 90 or 180°.

The line dance exercise program offers the greatest health benefits by enabling each participant to develop their muscle strength, aligned postures, lung capacity, and maintaining the body while lowering their risk for heart disease.

Statistical analysis

All data were expressed as mean±standard deviation (SD), and all statistical analyses were performed using the Statistical Package for Social Sciences (SPSS) version 17.0 software (SPSS Inc., Chicago, IL). Alpha levels were set at P<0.05. This intervention trial was designed to compare pre- and postexercise intervention variables. Changes from baseline to the end of the intervention were determined by a paired t-test and independent t-test. In multiple linear regression analysis, WC, TG, HDL-C, systolic blood pressure (SBP), diastolic blood pressure (DBP), and glucose were assessed as the independent variables and serum SHBG change as the dependent variable in the exercise group.

Results

Participant characteristics and body composition

The variables of body composition, lipid profiles, metabolic syndrome factors, insulin, and HOMA-IR were measured in all women before the start of the exercise training and after the end of the 16-week exercise training. There were no significant differences in baseline demographic characteristics between the study groups (results not shown).

The exercise group and control group at baseline were similar in age, height, body weight, %BF, LBM, BMI, WC, and VFA. However, after the line dance exercise training, the exercise group had a lower body weight, %BF, BMI, WC, and VFA compared with the control group (P<0.05). Also, it has noted that LBM was slightly lower in exercise group than in control group, but the difference was not statistically significant (Table 1).

Table 1.

Changes in Body Composition and VFA After 16-Week Line Dance Exercise

	Control (n=15)		Aerobic exercise (n=15)
	Before	After	Before	After
%BF (%)	36.58±1.66	37.52±2.36^a	35.95±2.98	33.46±3.30^b,c
Weight (kg)	61.62±3.88	63.15±4.32^b	60.94±4.04	58.69±3.79^b,c
LBM (kg)	39.00±3.27	39.51±3.96	39.06±3.28	39.09±3.75
BMI (kg·m⁻²)	25.12±1.49	25.94±1.35^b	25.03±1.33	24.21±1.22^b,c
WC (cm)	85.92±1.71	86.77±1.73^a	86.15±1.46	85.00±1.41^b,c
VFA (cm²)	100.54±8.40	105.69±8.57^b	103.53±10.09	98.23±7.72^b,c

Values are presented as mean±standard deviation (SD).

P<0.05 vs. before.

P<0.01 vs. before.

P<0.001 vs. control.

VFA, visceral fat area; %BF, percentage of body fat; LBM, lean body mass; BMI, body mass index; WC, waist circumference.

SHBG and metabolic syndrome factors

Table 2 shows that baseline values between groups were comparable for the SHBG, lipid profiles, resting SBP and DBP, as well as insulin and HOMA-IR. The exercise intervention resulted in significant increase in SHBG (P<0.001) and improvements in metabolic syndrome factors (P<0.05). The exercise group decreased significantly more in TC, glucose and insulin levels (P<0.01), BP, and HOMA-IR (P<0.001) than the control group. No changes in TG, HDL-C, and LDL-C were observed between the line dance exercise group and control group after the training.

Table 2.

Changes in SHBG, Metabolic Syndrome Factors, and Energy Metabolism

	Control (n=15)		Aerobic exercise (n=15)
	Before (26.6%)	After (33.3%)	Before (20%)	After (6.6%)
SHBG (μg/mL)	44.24±8.09	42.20±8.79^a	43.30±9.20	45.99±10.01^b,e
TC (mg/dL)	204.23±16.14	213.77±12.90^c	214.77±21.85	197.85±16.30^c,d
TG (mg/dL)	111.46±22.77	120.92±26.27^c	109.92±24.62	105.54±22.71^c
HDL-C (mg/dL)	50.00±10.54	47.62±8.96^b	46.92±10.32	50.08±10.42^c
LDL-C (mg/dL)	153.00±24.76	163.69±21.52^c	157.92±22.99	149.38±20.72^c
SBP (mmHg)	131.62±3.71	133.77±3.17^b	133.23±5.05	124.62±4.65^c,e
DBP (mmHg)	86.92±2.90	88.69±3.22^c	86.08±6.60	78.54±3.86^c,e
Insulin (μU/mL)	8.05±1.23	8.42±1.20^c	8.16±1.04	7.27±1.02^c,d
Glucose (mmol/L)	100.46±11.03	106.38±11.08^c	101.38±8.41	95.00±10.38^c,d
HOMA-IR	2.16±0.18	2.25±1.10^b	2.14±0.18	2.07±0.14^b,e

Metabolic syndrome was defined following the criteria provided by the National Cholesterol Education Program Adult Treatment Panel III (NCEP ATP III) and Korean Society for the Study of Obesity (KSSO); % is frequency of subjects with the metabolic syndrome factors.

Values are presented as mean±standard deviation (SD).

P<0.05 vs. before.

P<0.01 vs. before.

P<0.001 vs. before.

P<0.01 vs. control.

P<0.001 vs. control.

SHBG, sex hormone-binding globulin; TC, total cholesterol; TG, triglyceride; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; SBP, systolic blood pressure; DBP, diastolic blood pressure; HOMA-IR, homeostasis model assessment of insulin resistance.

In the postmenopausal obese women exercise group, using multiple linear regression analysis (Table 3), SHBG concentrations were correlated significantly with HDL-C, DBP, and glucose in the aerobic exercise group after training. It was observed that DBP and glucose were significantly decreased with exercise, highlighting an improvement in SHBG and increased HDL-C. However, WC, TG, and SBP were not correlated with SHBG. In the control group, SHBG was significantly and positively correlated with TG, DBP, and glucose (Table 4).

Table 3.

Regression Analysis of SHBG and Metabolic Syndrome Factors in the Line Dance Exercise Group After Training

Independentvariables	B	SE B	Beta	t-value	F	R ²
Constant	422.081	178.907		2.359	97.817	0.990
WC (cm)	−1.341	2.288	−0.190	−0.586
TG (mg/dL)	−0.073	0.037	−0165	−1.949
HDL-C (mg/dL)	−1.124	0.137	−1.171	−8.197^a
SBP (mmHg)	−0.773	0.402	−0.359	−1.925
DBP (mmHg)	−0.386	0.133	−0.149	−2.903^a
Glucose (m mol/L)	−0.753	0.322	−0.781	−2.334^a

P<0.05.

SHBG, sex hormone-binding globulin; SE, standard error; WC, waist circumference; TG, triglyceride; HDL-C, high-density lipoprotein cholesterol; SBP, systolic blood pressure; DBP, diastolic blood pressure.

Table 4.

Regression Analysis of SHBG and Metabolic Syndrome Factors in the Control Group After Training

Independent variables	B	SE B	Beta	t-value	F	R ²
Constant	514.754	94.121		5.469	11.137	0.918
WC (cm)	−1.699	0.780	−0.334	−2.178
TG (mg/dL)	−0.403	0.088	−1.204	−4.586 ^a
HDL-C (mg/dL)	−0.133	0.228	−0.135	−0.583
SBP (mmHg)	−1.455	0.623	−0.524	−2.336
DBP (mmHg)	−1.732	0.55	−0.635	−3.147 ^a
Glucose (m mol/L)	0.734	0.194	0.925	3.786 ^a

p<0.05.

SHGB, sex hormone-binding globulin; SE, standard error; WC, waist circumference; TG, triglyceride; HDL-C, high-density lipoprotein cholesterol; SBP, systolic blood pressure; DBP, diastolic blood pressure.

Discussion

Postmenopausal women who engage in regular and continuous physical activity have improved serum SHBG,²¹ body composition, lipid profiles, adipose tissue, and metabolic syndrome factors²² because such physical activity significantly improves and reduces body weight, BMI, FM, BP, lipid profiles, glucose, and energy metabolism.

The primary purpose of this study was to investigate the effects of aerobic exercise on serum SHBG, BFI, and metabolic syndrome factors in obese postmenopausal Korean women. The major findings of this study were the significant effects on body composition, metabolic syndrome factors, insulin, HOMA-IR, and SHBG in the line dance exercise group (but not in the control group). No difference was observed for LBM, although exercise intensity was gradually increased by 5% every 4 weeks in exercise group.

In the present study, SHBG concentrations were demonstrated in obese postmenopausal Korean women, and the relationships between SHBG concentrations and characteristics of metabolic syndrome factors and BFI were assessed. Interestingly, our study results shows strong relationships between SHBG and HDL-C, DBP, glucose, FM, BMI, and %BF in obese postmenopausal women with exercise training group but not in the nonexercise training group.

In this study, we found that aerobic exercise induced a decrease of body composition and improvement of SHBG, metabolic syndrome factors, and energy metabolism. In particular, we found that the exercise group had significantly higher SHBG and lower TC, BP, glucose, insulin, and HOMA-IR compared to the control group; however, no significant differences in TG, HDL-C, and LDL-C were found between the exercise group and control group after the 16-week exercise training. The women in the exercise group did not have significant changes in TG, HDL-C, and LDL-C, but had much better levels than the nonexercise group before and after the intervention. Our results are in agreement with a recent study by Halverstadt et al.²³ and Christopher et al.,²⁴ who reported that body weight, FM, TC, TG, LDL-C, insulin, and HOMA-IR were decreased significantly after exercise training. Similar data were observed in that serum TC, TG, LDL-C, and glucose were significantly decreased, and HDL-C and health-related fitness increased in obese middle-aged women after exercise training.²⁵ The results of this study and previous studies indicate that aerobic exercise may prevent lifestyle disease by reducing fat mass and WC, especially the highly metabolic abdominal fat mass and insulin levels. Our findings support the line dance exercise to improve SHBG, BFI, and metabolic syndrome factors in obese postmenopausal women following the minimal exercise recommendations from the American College of Sports Medicine and the American Heart Association in adults.²⁶

Menopausal status is a time of significant changes in sex hormone levels, the most important of which are testosterone and estradiol.² Menopause causes dramatic changes in the levels of hormones in the body, and such changes in hormones have been linked to increased hyperinsulinemia-related cardiovascular risk and metabolic syndrome.

Low plasma SHBG levels and high free androgen index (FAI) have been associated with all the individual components of metabolic syndrome in both men and women.^5,27 Metabolic syndrome affects 20%–30% of middle-aged women and has been linked to the growth of diabetes and cardiovascular disease.²⁸ Moreover, low plasma SHBG levels were associated with an increased number of characteristics of the metabolic syndrome, especially in men and premenopausal women.¹¹

In the present study, we found a positive correlation between BMI, insulin, and HOMA-IR changes after the line dance exercise training. BMI and insulin levels are inversely correlated with SHBG in obese postmenopausal women, and insulin prevents SHBG production.^29,30 Therefore, the present study demonstrates that reductions in body weight, insulin levels, or HOMA-IR may result in the increase of SHBG found in these obese postmenopausal Korean women. In our exercise group, BMI, insulin, and HOMA-IR were strongly associated with serum SHBG concentrations, suggesting that the severity of insulin level is a determinant factor in SHBG level. These findings are in agreement with a previous study that SHBG is a more sensitive marker of the pathogenetic contribution of insulin resistance to the pathogenesis of atherosclerosis than insulin itself.³¹

SHBG levels also showed a significant positive correlation with HDL-C and significant negative correlations with glucose, DBP, FM, BMI, and %BF. Multiple linear regression analysis was used to analyze the relationships between SHBG and metabolic syndrome factors after the line dance exercise training. We observed that high SHBG concentrations were associated with some of the individual components of the metabolic syndrome factors such as high HDL-C level and reduced DBP and glucose. This strong relation between SHBG and metabolic syndrome factors was explained mostly by increased insulin levels. Our study results suggest that serum SHBG could represent a marker of metabolic syndrome. However, TG and SBP were not associated with SHBG concentrations in obese postmenopausal Korean women. The current study's data are in agreement with previous studies^11,12,32 showing significantly positive relationships between SHBG and metabolic syndrome. These studies reported that plasma SHBG levels may represent a significant predictor of the metabolic syndrome in men and obese postmenopausal women. This study also found that the results show strong relationships between SHBG and BFI in obese postmenopausal women with exercise (results not shown). Similar findings were reported by Akin et al.,³³ who aimed to determine SHBG concentrations in premenopausal obese women and features of the metabolic syndrome. Their low SHBG group was significantly heavier and had higher BMI values with higher WC than the high SHBG group. Our findings support the notion that aerobic exercise such as line dancing can be used to lower and manage BFI, blood lipids, energy metabolism, and metabolic syndrome factors in obese postmenopausal Korean women.

Several limitations of the present study should be acknowledged. We did not measure the maximal or submaximal test performed before and after the exercise training program to evaluate fitness of subjects. Although only SHBG was measured, we were unable to investigate whether other endogenous sex hormones (such as estradiol and testosterone) were associated with the metabolic syndrome factors.

Future research should address the following recommendations for further studies. Additional studies are needed to confirm the results of this study, compare the effects of the line dance exercise on the variables of obese and nonobese or premenopausal and postmenopausal women by age or exercise type, and to develop effective line dance exercise programs with different age groups.

Conclusions

Our findings indicate that regular and continuous aerobic exercise training is effective in improving body composition, serum SHBG concentrations, serum lipids, insulin levels, and metabolic syndrome factors in obese postmenopausal Korean women. The present study suggests that reductions in body weight, insulin levels, or HOMA-IR may result in the increases in SHBG found in these obese postmenopausal Korean women. Our results support the notion that aerobic exercise training works for the prevention of cardiovascular disease and metabolic syndrome in postmenopausal women.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

References

Saad

, Gooren

. The role of testosterone in the metabolic syndrome: A review. J Steroid Biochem Mol Biol, 2009; 114:40–43.

Rosner

. Sex steroid transport: Binding proteins. Adashi

. Rock

. Rosenwaks

. Reproductive Endocrinology, Surgery, and Technology. Philadelphia, New York: Lippincott-Raven Publishers, 1996; 606–626.

Hautanen

. Synthesis and regulation of sex hormone-binding globulin in obesity. Int J Obes Relat Metab Disord, 2000; 24:S64–S70.

, von Eckardstein

. Androgens and coronary artery disease. Endocr Rev, 2003; 24:183–217.

Tchernof

, Despres

. Sex steroid hormones, sex hormone-binding globulin, and obesity in men and women. Horm Metab Res, 2000; 32:526–536.

Haffner

. Sex hormones, obesity, fat distribution, type 2 diabetes and insulin resistance: epidemiological and clinical correlation. Int J Obes Relat Metab Disord, 2000; 24:S64–S70.

Maggio

, Lauretani

, Basaria

et al. Sex hormone binding globulin levels across the adult lifespan in women-the role of body mass index and fasting insulin. J Endocrinol Invest, 2008; 31:597–601.

Evans

, Hoffmann

, Kalkhoff

et al. Relationship of androgenic activity to body fat topography, fat cell morphology, and metabolic aberrations in premenopausal women. J Clin Endocrinol Metab, 1983; 57:304–310.

Ivandic

, Prpic-Krizevac

, Sucic

et al. Hyperinsulinemia and sex hormones in healthy premenopausal women: relative contribution of obesity, obesity type and duration of obesity. Metabolism, 1998; 47:13–19.

10.

Bataille

, Perret

, Evans

et al. Sex hormone binding globulin is a major determinant of the lipid profile: The RPIME study. Atherosclerosis, 2005; 179:369–373.

11.

Hajamor

, Despres

, Couillard

et al. Relationship between sex hormone-binding globulin levels and features of the metabolic syndrome. Metabolism, 2003; 52:724–730.

12.

Weinberg

, Manson

, Buring

et al. Low sex hormone-binding globulin is associated with the metabolic syndrome in postmenopausal women. Metabolism, 2006; 55:1473–1480.

13.

Kalme

, Seppala

, Qiao

et al. Sex hormone-binding globulin and insulin-like growth factor-binding protein-1 as indicators of metabolic syndrome, cardiovascular risk, and mortality in elderly men. J Clin Endocrinol Metab, 2005; 90:1550–1556.

14.

Katzmarzyk

, Leon

, Wilmore

et al. Targeting the metabolic syndrome with exercise: Evidence from the heritage family study. Med Sci Sports Exerc, 2003; 35:1703–1709.

15.

Lakka

, Laaksonen

. Physical activity in prevention and treatment of metabolic syndrome. Appl Physiol Nutr Metab, 2007; 32:76–88.

16.

Johnson

, Slentz

, Houmard

et al.

Exercise training amount and intensity effects on metabolic syndrome(from studies of a targeted risk reduction intervention through defined exercise)

Am J Cardiol, 2007; 100:1759–1766.

17.

Derouich

, Boutayeb

. The effect of physical exercise on the dynamics of glucose and insulin. J Biochem, 2002; 35:911–917.

18.

LaMonte

, Barlow

, Jurca

et al. Cardiorespiratory fitness is inversely associated with the incidence of metabolic syndrome: A prospective study of men and women. Circulation, 2005; 112:505–512.

19.

American College of Sports Medicine. ACSM's Guidelines for Exercise Testing and Prescription, 7 ^th. Philadelphia, PA: Lippinocott Williams & Wilkins Publishers, 2006.

20.

Matthews

, Hosker

, Rudenski

et al. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia, 1985; 28:412–419.

21.

McTiernan

, Tworoger

, Ulrich

et al. Effect of exercise on serum estrogens in postmenopausal women: A 12-month randomized clinical trial. Cancer Res, 2004; 64:2923–2928.

22.

Lee

, Kim

. Effects of hatha yoga exercise on serum leptin and metabolic syndrome factors in menopause obese middle-aged women. Korean J Life Science, 2010; 20:1100–1106.

23.

Halverstadt

, Phares

, Wilund

et al. Endurance exercise training raises high-density lipoprotein cholesterol and lowers small low-density lipoprotein and very low-density lipoprotein independent of body fat phenotypes in older men and women. Metabolism, 2007; 56:444–450.

24.

Yumchuk

, Tessler

, Barnard

. Changes in sex hormone-binding globulin, insulin, and serum lipids in postmenopausal women on a low-fat, high-fiber diet combined with exercise. Nutr Cancer, 2000; 38:158–162.

25.

Kim

, Lee

, Yang

. Effects of hatha yoga exercise on body composition, serum lipids, and health- obese middle-aged women. Korean J Life Science, 2011; 21:521–528.

26.

Nelson

, Rejeski

, Blair

et al. Physical activity and public health in older adults: Recommendation from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc, 2007; 39:1436–1445.

27.

Weinberg

, Manson

, Buring

et al. Low sex hormone-binding globulin is associated with the metabolic syndrome in postmenopausal women. Metabolism, 2006; 55:1473–1480.

28.

Janssen

, Powell

, Crawford

et al. Menopause and the metabolic syndrome: The study of women's health across the nation. Arch Intern Med, 2008; 168:1568–1575.

29.

Plymate

, Hoop

, Jones

et al. Regulation of sex hormone-binding globulin production by growth factors. Metabolism, 1990; 39:967–970.

30.

Svendsen

, Hassager

, Christiansen

. The response to treatment of overweight in postmenopausal women is not related to fat distribution. Int J Obes Relat Metab Disord, 1995; 19:496–502.

31.

Reinecke

, Boqdanski

, Woltering

et al. Relation of serum levels of sex hormone binding globulin to coronary heart disease in postmenopausal women. Am J Cardiol, 2002; 90:364–368.

32.

Akin

, Bastemir

, Alkis

et al. SHBG levels correlate with insulin resistance in postmenopausal women. Eur J Intern Med, 2009; 20:162–167.

33.

Akin

, Bastemir

, Alkis

et al. Associations between sex hormone binding globulin and metabolic syndrome parameters in premenopausal obese women. Indian J Med Sci, 2008; 62:407–415.