Long-Term Effects of Aerobic Plus Resistance Training on the Metabolic Syndrome and Adiponectinemia in Obese Adolescents

Authors


Ana R. Dâmaso, PhD, CEPE/GEO, Rua: Prof. Francisco de Castro, 93, Vila Clementino, 04020-060 São Paulo/SP, Brazil
E-mail: ana.damaso@unifesp.br

Abstract

The metabolic syndrome is an emerging clinical problem and different kinds of interventions have emphasized that healthy eating and exercise are crucial to its control. The aim of this study was to identify whether aerobic training plus resistance training (AT+RT) is more effective than AT on improving features of the metabolic syndrome and adiponectinemia in obese adolescents. A total of 30 adolescents (aged 15–19 years, body mass index ≥95 percentile) were enrolled in the program. All patients were diagnosed with the metabolic syndrome and submitted to 1 year of interdisciplinary intervention. They were divided into two groups: AT (n=15) and AT+RT (n=15). Blood samples were collected to analyze glycemia and lipid profiles. Adiponectin was measured by enzyme-linked immunosorbent assay, and insulin resistance was measured by homeostasis model assessment of insulin resistance index. After short- and long-term intervention, both groups presented a significant reduction in body mass, body mass index, fat mass, and visceral fat. Indeed, the AT+RT group had significantly higher changes throughout the intervention in body composition, total cholesterol, waist circumference, glucose, and adiponectin. Although important clinical parameters were ameliorated with AT, the AT+RT group showed more effective improvements in metabolic profiles and adiponectinemia. These findings suggest a clinical role of AT+RT in the control of metabolic syndrome in pediatric populations. J Clin Hypertens (Greenwich). 2011;13:343–350. ©2010 Wiley Periodicals, Inc.

Physical inactivity in adolescence strongly and independently predicts obesity and favors the development of a self-perpetuating vicious cycle of obesity and a sedentary lifestyle. Not surprisingly, physical activity should be a major target of obesity prevention in the young.1

Childhood obesity has continued to escalate despite considerable efforts to reverse the current trends. Childhood obesity represents a public health concern because overweight-obese youth experience comorbidities such as type 2 diabetes mellitus, nonalcoholic fatty liver disease (NAFLD), metabolic syndrome, and cardiovascular disease, which are conditions that were once considered to be limited to adults.2–4

Although mounting evidence in adults has demonstrated the benefits of regular physical activity as a treatment strategy for abdominal obesity and cardiovascular risk, the specific role of aerobics combined with resistance training (RT) is unclear in adolescents with the metabolic syndrome.2,5

Several randomized controlled studies have suggested that aerobic training (AT) is a better therapeutic coadjuvant to treat youth obesity and metabolic syndrome than RT alone.6–8 However, evidence regarding the effects of AT+RT on the control of metabolic syndrome is lacking and demands further investigation.

Recently, studies have demonstrated that the metabolic syndrome represented a constellation of metabolically altered parameters that could lead to a chronic inflammatory process during adolescence and adulthood.4,9–12 Interestingly, adiponectin, the most abundant hormone secreted by adipose tissue, has potent anti-inflammatory effects that have been shown to be inversely correlated with insulin resistance (IR). In addition, obesity (mainly visceral adiposity) has been shown to reduce adiponectin.13,14

AT and nutritional interventions have been proven to be good strategies to control inflammatory processes from visceral and hepatic risk factors, including an increase in adiponectin and a reduction in C-reactive protein in adults.15 However, the role of AT+RT on adiponectin levels in obese adolescents with the metabolic syndrome has not been clearly elucidated.

Thus, the aim of the present study was to investigate whether AT+RT was more effective than AT alone at improving the metabolic profile and adiponectinemia in obese adolescents with the metabolic syndrome submitted to a long-term interdisciplinary intervention. We hypothesized that AT+RT would provide the greatest improvement on the parameters of metabolic syndrome as well as the inflammatory processes mediated by adiponectin.

Methods

Study Participants

A total of 43 obese adolescents were enrolled in the program. However, only 30 patients completed the year of therapy. The 30 postpuberty16 obese adolescents (body mass index [BMI] >95th percentile of the Centers for Disease Control and Prevention reference growth charts),17 who were between 15 and 19 years of age (16.71±1.47 years), included 10 girls and 20 boys who were recruited for a long-term (1 year) weight-loss intervention study. The inclusion criteria for the postpubertal stage were based on the Tanner scale (stage 5) for boys and girls.16 The noninclusion criteria were endocrine diseases, chronic alcohol consumption, pregnancy, and previous use of drugs (eg, anabolic-androgenic steroids or psychotropics) that could affect appetite regulation. We obtained parental informed consent as well as consent from the adolescents to participate as volunteers in an interdisciplinary weight-loss program. This study was conducted in accordance with the principles of the Declaration of Helsinki and was formally approved by the ethics committee of the Federal University of São Paulo – Paulista Medicine School (number 0135/04).

Participants were divided into two groups: (1) 1 year of AT plus RT (AT+RT: n=15) or (2) 1 year of AT (AT: n=15). Before the study began, both groups performed 2 weeks of similar training for adaptation. All patients reported that they had no experience with RT prior to the study. Evaluations were made at baseline, after 6 months (short-term), and after 1 year (long-term) of interdisciplinary therapy. All participants were completely familiarized with all testing procedures before the experiment to reduce the influence of any learning effects.

Anthropometric Measurements and Body Composition

Barefooted participants wearing light clothing were weighed to the nearest 0.1 kg. Stature was measured to the nearest 0.5 cm with a wall-mounted stadiometer. BMI was calculated as body weight divided by height squared (wt/ht2), and body composition was measured by plethysmography in the BOD POD body composition system (version 1.69; Life Measurement Instruments, Concord, CA).18

Measurements of Visceral and Subcutaneous Fat

All abdominal ultrasonography procedures and measurements of visceral and subcutaneous fat were performed double-blinded by the same physician, who specialized in diagnostic imaging, using a 3.5-MHz multifrequency transducer. This procedure allowed for a reduction in the risk margin for misclassification. The intra-examination coefficient of variation for ultrasonography was 0.8%. Ultrasonography measurements were taken for intra-abdominal (visceral) and subcutaneous fat. Ultrasonography-determined subcutaneous fat was defined as the distance between the skin and the external face of the rectus abdominis muscle, and visceral fat was defined as the distance between the internal face of the same muscle and the anterior wall of the aorta.19

Serum Analysis

Blood samples were collected in the outpatient clinic around 8 am after an overnight fast. After collection, the blood was centrifuged for 10 minutes at 5000 rpm and stored at −70°C for future analyses. The materials used for collection were disposable and adequately labeled. Blood was collected by a skilled and qualified technician, and lipid profiles were measured. Insulin resistance was assessed by the homeostasis model assessment of insulin resistance index (HOMA-IR). The HOMA-IR was calculated by the product of blood glucose (fasting blood glucose) and immunoreactive insulin (I): (fasting blood glucose [mg/dL]×I [mU/L])/405. All variables were analyzed using commercial kits. The adiponectin concentration was measured using a commercially available enzyme-linked immunosorbent assay kit.

Metabolic Syndrome Diagnosis

Using modified adult criteria, the new 2005 International Diabetes Federation (IDF) definition for metabolic syndrome in children and adolescents built on previous studies of the prevalence of the syndrome in children and adolescents.20 Due to developmental challenges presented by age-related differences in children and adolescents, the new IDF definition includes 6 to 9 years, 10 to 15 years, and 16 years and older. Individuals 16 years and older used existing IDF criteria for adults. In all 3 groups, abdominal obesity was the essential condition for diagnosis of metabolic syndrome.

Research Design

The interdisciplinary obesity intervention consisted of AT+RT along with clinical, nutritional, and psychological therapy. This group was compared with a control group, which performed AT alone. The use of interdisciplinary therapy as a criterion has been suggested by the World Health Organization.21 All measurements were performed at baseline, after 6 months (short-term), and after 1 year (long-term) of therapy.

Exercise Protocol.

AT Plus RT:  The AT+RT regi-men was performed 3 times per week for 1 year. This training included 30 minutes of AT plus 30 minutes of RT per session. The volunteers were oriented to invert the order of the exercises at each training session: in one session, the adolescent started the training session with aerobic exercises, and in the subsequent session, the same adolescent started with the RT. The AT mode consisted of running on a motor-driven treadmill at the cardiac frequency intensity of the ventilatory threshold I (±4 bpm), which was determined by the results of an initial oxygen uptake test for aerobic exercises (cycle-ergometer and treadmill). The physiologists controlled the cardiac frequency, which was measured with a cardiometer at intervals of 5 minutes during all training sessions. The exercise program was based on the American College of Sports Medicine (ACSM) recommendations (2002).5 We used exercises for the main muscle groups (bench press, leg press, sit-ups, lat pull-down, hamstring curls, lower back, military press, calf raises, arm curls, and triceps pushdown), and the order of the exercises was strictly followed by the group.

The first 2 weeks of the RT were for adaptation to training and learning of the movements (3 sets of 15–20 maximal repetitions [MRs]). Following this adaptation period, the training load was adjusted by increasing the weight and intensity and decreasing the number of repetitions to between 6 and 20 for each of the 3 sets. The following rest intervals were allowed between series and exercises: 15 to 20 MR=45 seconds, 10 to 12 MR=1 minute, and 6 to 8 MR=1.5 minutes. The training loads were adjusted in each training session and evaluated according to the increases in the strength of the participants. Therefore, the training was conducted with MRs.

Aerobic Training:  During the year of therapy, obese adolescents followed a personalized AT program that included 60-minute sessions 3 times a week (180 min/wk) under the supervision of a sports physiologist. Each program was developed according to the results of an initial oxygen uptake test for aerobic exercises (cycle-ergometer and treadmill). The intensity was set at a workload corresponding to the ventilatory threshold I (50%–70% of oxygen uptake test). At the end of 6 weeks, aerobic tests were individually performed to assess physical capacities and adjust physical training intensities. During the aerobic sessions, heart rates of the adolescents were monitored. The exercise program was based on the recommendations of the ACSM (2002)5 and adapted by Foschini and colleagues (2009).22

Psychological Therapy.  Psychological therapy was established by validated questionnaires, which took into account some of the psychological problems caused by obesity, such as depression, eating disorders, anxiety, decreased self-esteem, and body image disorders. During the interdisciplinary therapy, adolescents received psychological orientation for 1 hour in a weekly group session. The psychologist discussed body image and eating disorders, such as bulimia and anorexia nervosa, as well as binge eating disorders and their signs, symptoms, and health consequences. The psychologist also discussed the relationship between feelings and food as well as familial problems, such as alcoholism. Individualized psychological therapy was recommended when weight problems or poor dietary habits were found.23

Nutritional Therapy.  Energy intake was set at the levels recommended by the dietary reference for patients with a low level of physical activity (of the same age and sex as our study patients) following a balanced diet.24 No drugs or antioxidants were recommended. Once a week, adolescents had a dietetics lesson, which provided information on the food pyramid, diet record assessment, weight loss and miracle diets, food labels, dietetics, fat-free and low-calorie foods, fats, and other nutritional themes. All patients received individual nutritional consultation during the intervention program.

A 3-day dietary record was collected at the beginning of the study, 6 months into the study, and 12 months into the study. Because most obese people under-report their food consumption, adolescents were asked to record their diet with the help of their parents.25 Although the degree of under-reporting may be substantial, this is a validated method to assess dietary consumption.26 Portions were measured in terms of familiar volumes and sizes. The dietician taught the parents and the adolescents how to record food consumption. These dietary data were transferred to a computer by the same dietician, and the nutrient composition was analyzed by a PC program developed at the Federal University of São Paulo – Paulista Medicine School, which used data from Western and local food tables. In addition, the parents were encouraged to call the dietitian if they needed extra information.

Clinical Therapy.  To accomplish health and clinical parameters, obese adolescents of both groups visited the endocrinologist once a month. Medical follow-ups and treatment were based on initial patient and familial histories, physical examination, and intervention for unhealthy problems that developed during the therapy.

Statistical Analysis

Statistical analyses were performed using STATISTICA (version 7.0 for Windows; StatSoft, Tulsa, OK). An α of 0.05 was used as the sample size calculation. We verified Gaussian distribution of variables with a Kolmogorov–Smirnov test, and the parametric variables with skewed distribution are expressed as mean ± standard deviation. For the nonparametric variables (insulin, HOMA-IR, and triglycerides), the median, along with the minimum and maximum values, is expressed in the descriptive tables. The comparisons between the measurements of the parametric parameters before and 6 months and 1 year after intervention were determined by repeated-measures analysis of variance. The Wilcoxon signed rank and Mann–Whitney U tests were used to analyze the nonparametric variables. Pearson’s correlation coefficients were used to assess potential relationships between variables, and chi-square tests were performed to analyze the frequencies of metabolic syndrome components in the different kinds of training.

Results

Although 43 obese adolescents were enrolled in the program, only 30 patients completed more than 75% of the treatment sessions during the 1-year study. Of the 13 patients who did not finish the study, 7 were from the AT group and 6 were from the AT+RT group. It is important to note that there were no differences in patient adherence to any of the variables of the program (ie, training, clinical, nutritional, and psychological). In addition, no sex differences were observed in adherence rates. The main reasons for dropping out of the study were financial and family problems, school, and job opportunities.

At baseline conditions, the aerobic capacity analyzed by VO2 maximum did not show a significant difference between AT and AT+RT groups. An improvement in this variable was demonstrated only in the AT group (data not shown). The AT+RT group showed higher values of adiponectin and systolic blood pressure (BP) compared with the AT group. After 6 months, both the AT and AT+RT groups presented a significant reduction in body mass, BMI, fat mass, visceral fat, and waist circumference. In addition, both groups showed significant increases in lean mass and adiponectinemia. After short-term intervention, the AT+RT group showed significant reductions in subcutaneous fat, total cholesterol, and low-density lipoprotein cholesterol (LDL-C), whereas the AT group showed reductions in glucose and triglycerides.

One year of intervention promoted significant reductions in body mass, BMI, fat mass, visceral fat, subcutaneous fat, and waist circumference in both groups. Interestingly, the AT group had a significant reduction in total cholesterol, LDL-C, glucose, insulin, and HOMA-IR, whereas the AT+RT group showed decreases in triglyceride levels and increases in adiponectinemia (Table I and Table II). A comparison of the short- and long-term effects revealed that AT+RT improved body mass, BMI, fat mass, visceral fat, insulin, and adiponectinemia, while the AT only group showed an improvement in visceral fat. We also observed a positive correlation across time between the changes of visceral fat and HOMA-IR (r=0.47, P=.02) (Figure).

Table I.   Body Composition, Subcutaneous and Visceral Adipose Tissues, and Biochemical Parameters in Obese Adolescents With the Metabolic Syndrome Before and After Intervention for Weight Loss With Different Kinds of Exercise
 Aerobic TrainingAerobic Plus Resistance Training
Baseline6 mo1 yΔ at 1 yBaseline6 mo1 yΔ at 1 y
  1. Abbreviations: Δ, change; BMI, body mass index; LDL-C, low-density lipoprotein cholesterol. Values are expressed as mean ± standard deviation or median (minimum – maximum). aBaseline vs 6 months P≤.05. bBaseline vs 1 year of intervention P≤.05. cGroup aerobic training vs group aerobic plus resistance training for the same time P≤.05. d6 months vs 1 year of intervention P≤.05.

Body mass, wt104.15±11.9296.52±9.86a96.88±9.88b−7.91±7.48108.22±12.2797.21±11.26a91.39±11.12b−15.45±6.95c
BMI, wt/ht236.63±4.1434.04±4.21a34.07±4.79b−2.62±2.3837.23±5.1930.55±5.02a31.63±5.06b,d−5.54±2.41c
Fat mass, %38.39±6.7536.60±7.1235.55±9.04b−2.87±6.0144.16±8.0830.09±10.77a33.28±12.00b,d−11.42±6.10c
Fat mass, kg40.02±8.6635.55±8.92a34.62±10.61b−5.67±8.0548.23±12.1335.66±13.37a31.00±13.73b,d−17.34±6.50c
Lean mass, kg64.13±10.3260.86±7.30a62.21±9.40−2.29±4.0159.99±8.5956.32±9.3960.80±8.862.31±5.22c
Visceral, cm5.43±1.854.73±1.19a3.85±1.38b−1.72±1.574.79±1.372.73±0.94a2.41±0.83b,d−2.02±0.66
Subcutaneous fat, cm3.34±0.653.17±0.882.97±0.89b−0.39±0.793.47±0.532.59±0.66a2.79±0.83b−0.78±0.62
Total cholesterol, mg/dL162.47±47.86159.06±33.85167.69±44.684.53±21.81173.46±33.42135.58±25.66a149.38±34.80b−19.84±23.28c
LDL-C, mg/dL95.20±37.4095.86±25.68100.76±33.095.53±15.14112.73±30.1177.77±24.84a90.53±28.57b−18.63±17.50
Adiponectin, μg/mL5.01 (3.20–10.21)6.66 (2.78–10.19)a4.24 (3.02–10.69)0.77±2.499.18 (6.12–13.86)c10.82 (6.82–14.71)a,c12.91 (8.43–16.13)b,c,d3.68±2.28c
Table II.   Metabolic Syndrome Parameters in Obese Adolescents Before and After Intervention for Weight Loss
 Aerobic TrainingAerobic Plus Resistance Training
Baseline6 mo1 yΔ at 1 yBaseline6 mo1 yΔ at 1 y
  1. Abbreviations: Δ, change; DBP, diastolic blood pressure; HDL, high-density lipoprotein cholesterol; HOMA-IR, homeostasis model assessment insulin resistance index; SBP, systolic blood pressure. Values are expressed as mean ± standard deviation or median (minimum – maximum). aGroup aerobic training vs group aerobic plus resistance training for the same time P≤.05. bBaseline vs 1 year of intervention P≤.05. cBaseline vs 6 months P≤.05. d6 months vs 1 year of intervention P≤.05.

SBP, mm Hg122.66±12.22117.13±4.10115.71±5.137.14±12.66134.33±16.35a118.37±3.47115.83±7.92b16.25±19.90
DBP, mm Hg81.33±9.9078.56±5.2476.53±5.54−3.46±11.4383.33±4.8777.29±4.8974.16±5.14−8.33±5.77
Glucose, mg/dL91.73±4.9394.46±6.99c93.76±7.871.61±6.7790.00±6.1090.26±5.2483.46±4.07a,b,d−6.38±6.80a
Insulin, μU/mL16.00 (8.40–63.2)17.60 (5.30–51.80)13.70 (6.70–43.30) −5.81±17.7017.30 (8.30–30.20)13.40 (5.00–19.30)a,c7.70 (2.90–18.90)a,b,d−9.74±5.67
HOMA-IR3.51 (1.98–14.40)3.51 (1.98–14.40)3.36 (1.30–10.46)−1.16±3.883.67 (1.86–7.05)3.10 (1.04–4.38)a,c1.61 (0.58–3.87)a,b,d−2.26±1.33
Waist circumference, cm104.47±7.8798.60±9.72c99.30±9.24b−5.70±6.37110.39±12.3195.34±8.03c92.76±12.70b−17.06±11.38a
Triglycerides, mg/dL108 (47–250)94 (46–178)c91 (27–241)b−22.00±29.61102 (43–206)71 (54–167)77 (58–198) −6.7±32.55
HDL-C, mg/dL40.40±7.3542.40±7.6342.07±10.843.31±6.9440.73±7.4041.93±6.6839.69±5.830.10±5.30
Figure FIG.

 Positive correlation between changes in visceral fat and changes in homeostasis model assessment insulin resistance index (HOMA-IR) in obese adolescents with the metabolic syndrome.

Indeed, a comparison of the AT+RT group with the AT group demonstrated that there were significant changes along the intervention in body mass, BMI, fat mass (percentage and kg), lean mass (kg), total cholesterol, glucose, waist circumference, and adiponectinemia (Table I and Table II).

After long-term intervention, the prevalence of the metabolic syndrome was significantly decreased from 15 patients to 3 patients in the AT group and 15 patients to 0 patients in the AT+RT group. A comparison of the baseline measures and the results at the end of the therapy showed that the frequency of altered diastolic BP, glucose, waist circumference, and triglycerides significantly decreased in both groups (Table III).

Table III.   Frequency of Altered Metabolic Syndrome Components at Baseline and After 1 Year of Intervention in Obese Adolescents
Predictors of MS (IDF, 2005)Aerobic TrainingAerobic Plus Resistance Training
Baseline (n=15)1 y (n=15)Baseline (n=15)1 y (n=15)
  1. Abbreviations: DBP, diastolic blood pressure; HDL, high-density lipoprotein; HOMA-IR, homeostasis model assessment insulin resistance index; IDF, International Diabetes Federation; MS, metabolic syndrome; SBP, systolic blood pressure; TG, triglycerides. aChi-square test, P<.05.

Three or more components of MS153a150a
SBP, mm Hg80101a
DBP, mm Hg40a70a
Glucose, mg/dL10a10a
Waist circumference, cm1512a157a
TG, mg/dL52a31a
HDL, mg/dL116119

An analysis of the food intake in both groups showed that there was a significant reduction in energy intake and macronutrients. After the 1-year intervention, the AT+RT group showed a lower energy intake compared with the AT group (Table IV).

Table IV.   Characteristics of Food Intake in Obese Adolescents With the Metabolic Syndrome Before and After Intervention for Weight Loss
VariablesAerobic TrainingAerobic Plus Resistance Training
Baseline6 mo1 yBaseline6 mo1 y
  1. Values are expressed as mean ± standard deviation. aBaseline vs 1 year of intervention P≤.05. b6 months vs 1 year of intervention P≤.05. cGroup aerobic training vs group aerobic plus resistance training for the same time P≤.05.

Energy intake, kcal2391.67±907.941707.04±462.131595.50±409.26a2065.50±582.381282.15±369.85b1205.33±384.88a,c
Carbohydrate, g302.70±102.99210.19±49.60b215.64±72.60a241.62±92.38182.13±30.69b162.92±48.33a
Carbohydrate, %50.37±8.6851.73±7.9253.81±9.7449.30±7.4157.92±10.75b54.46±7.90
Protein, g115.92±64.8988.29±48.69b76.88±23.23a99.34±46.0358.46±32.53b53.79±15.23a
Protein, %18.42±5.1620.65±5.7219.31±4.8918.40±5.2116.99±5.5318.49±4.08
Lipid, g85.53±33.8353.45±19.59b46.71±17.19a75.18±27.4736.97±20.20b37.73±22.23a
Lipid, %31.17±4.5927.60±5.6026.80±7.2432.30±4.1524.14±7.3125.70±8.86

Discussion

Regular physical activity is one of the most important nonpharmacologic tools in reducing overall cardiometabolic risk because it significantly improves quality of life and regulates body weight, BP, blood glucose, and the lipid profile.27 Our results support the idea that physical activity can reduce cardiometabolic risk and is effective in reducing metabolic syndrome prevalence (Table III).

The results of the present study demonstrated that AT+RT was more effective than AT alone in controlling the metabolic syndrome in obese adolescents after long-term intervention. Indeed, AT+RT provided a continuous improvement of several parameters from 6 months to 1 year of intervention, including BMI, fat mass, visceral fat, glucose, insulin, HOMA-IR, and adiponectinemia (Table I, Table II, and Table III).

A systematic review of long-term lifestyle interventions to prevent weight gain and morbidity in adults demonstrated that dieting with exercise and behavior therapy resulted in a significant reduction in hypertension and a decreased risk of metabolic syndrome,3 which was similar to our results. It is important to note that both of the groups in the present study showed an improvement in food intake, including a significant reduction in macronutrient ingestion. However, the AT+RT group had a lower energy intake compared with the AT group after 1 year of intervention (Table III and Table IV). Taken together, these findings reinforce the impact of the association between nutrition and exercise for effective control of metabolic syndrome components.4,28,29

After long-term therapy, AT+RT was more effective than AT alone in improving glucose, insulinemia, insulin resistance, waist circumference, and LDL-C, which suggested important effects on metabolic and hormonal adjustments.30 Moreover, the reduction of body fat was likely the major contributing factor to the improvements in insulin resistance, lipids, and adiponectin. Indeed, the AT+RT group demonstrated greater changes in body fat compared with the AT group. These results should be confirmed in a large cohort study because there are controversies in the literature about the effects of RT alone on metabolic syndrome–related outcomes in obese adolescents.28,29

A recent investigation suggested that AT+RT may lead to improvement in metabolic rate, which would induce an increase in lipid oxidation and a reduction of body and fat mass.31 It is important to note that AT+RT resulted in a greater body mass reduction than AT alone (15 kg vs 8 kg). Moreover, AT+RT promoted a greater change in BMI, fat mass (percentage and kg), lean mass (kg), total cholesterol, glucose, waist circumference, and adiponectinemia compared with the AT group. These variables are relevant to the metabolic syndrome, and improving these factors can reduce cardiometabolic risk. Indeed, BMI and waist circumference have been reported to be predictors of cardiovascular risk.32

In obese adolescents, the expansion of visceral adipose tissue is an independent risk factor for NAFLD development, which is a new component of the metabolic syndrome.10 Indeed, a visceral adiposity diagnosis >4.50 cm for girls and >5.53 cm for boys was shown to be predictive of NAFLD, and each centimeter of expansion in visceral adipose tissue was correlated with a 2-fold increase in NAFLD development.10 The reduction in visceral adipose tissue observed in the present investigation suggested that AT+RT more effectively reduced the inflammatory process commonly associated with obesity-related metabolic syndrome and NAFLD. Although both kinds of exercise training were effective in controlling visceral fat, only AT+RT resulted in a significant reduction of fat mass percentage and increased lean body mass.

The ability of both kinds of exercise to reduce visceral fat in the present study may be essential for the control of the metabolic syndrome because visceral fat is associated with metabolic syndrome components, such as insulin and HOMA-IR. Indeed, we found a positive correlation between visceral fat and HOMA-IR changes during our therapy (Figure).

We also observed that the AT+RT group had a significantly higher adiponectin concentration and reduced insulin resistance by the end of the therapy. Although the AT+RT group showed higher adiponectin levels at baseline, we observed a continuous increase in adiponectin levels at both 6 and 12 months. Interestingly, we did not observe the same effect in the AT group (Table I and Table II).

Similar to our results, Balducci and colleagues30 found that AT+RT promoted a significant increase in adiponectin. Therefore, this kind of training in obese adolescents with the metabolic syndrome appears to be associated with a significant reduction of proinflammatory processes, which could partially be mediated by adiponectin actions. Indeed, the effects of AT+RT on adiponectin could also affect insulin and improve metabolic syndrome and the cardiovascular risk factors at young ages.

Adiponectin is an insulin-sensitizing adipokine that possesses multiple beneficial effects on obesity-related medical complications.33 It may also have antiatherogenic and anti-inflammatory properties, and high circulating levels of adiponectin have been related to a lower risk of coronary heart disease.34 It is likely that the impaired actions of adiponectin are clinically important in obese patients because adiponectin is the most abundant adipocyte-derived hormone with established anti-inflammatory and insulin-sensitizing effects. Indeed, adiponectin has many important actions in obesity-related pathologies, including regulating hepatic mitochondrial functions, which decreases the levels of mitochondrial lipid peroxidation products, and attenuating the translocation of nuclear factor κB to the nucleus, which inhibits the production of proinflammatory cytokines.35

The key observation of our study was that AT+RT resulted in a greater improvement of metabolic syndrome parameters than AT alone, which confirmed the important role of this kind of exercise therapy in the control of the metabolic syndrome.

Conclusions

Although important clinical parameters were ameliorated with AT in a pediatric population, AT+RT more effectively improved the metabolic profile and reduction of proinflammatory processes, which could partially be mediated by adiponectin action, commonly associated with the metabolic syndrome in this long-term interdisciplinary obesity intervention. These findings emphasized the potential therapeutic implications of AT+RT and suggested that new strategies for lifestyle changes may be necessary to improve metabolic syndrome risk factors in obese adolescents.

Acknowledgments and disclosures:  We would like to thank the patients that participated in the study and the sources of funding: FAPESP 2008/53069-0, AFIP, FAPESP 2006/00684-3, FAPESP (CEPID/Sleep #9814303-3 S.T) CNPq, CAPES, CENESP, and UNIFESP-EPM supported the CEPE-GEO Interdisciplinary Obesity Intervention Program.

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