Get - Wiley Online Library

ORIGINAL
PAPER
Long-Term Effects of Aerobic Plus Resistance Training on the
Metabolic Syndrome and Adiponectinemia in Obese Adolescents
Marco Túlio de Mello, PhD;1 Aline de Piano, MSc;2 June Carnier, MSc;2 Priscila de Lima Sanches, MSc;2 Fabı́ola Alvise Corrêa,
MSc;2 Lian Tock, MD;2 Regina M. Y. Ernandes, MD;3 Sérgio Tufik, MD, PhD;1,3 Ana R. Dâmaso, PhD2,4
From the Department of Psychobiology,1 Post-Graduate Program of Nutrition,2 Funding Research to Psychopharmacology,3 and Biosciences
Department,4 Paulista Medicine School, Federal University of São Paulo, UNIFESP-EPM, São Paulo, Brazil
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 immunosor-
bent 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.
Address for correspondence: Ana R. Dâmaso, PhD, CEPE ⁄ GEO, Rua:
Prof. Francisco de Castro, 93, Vila Clementino, 04020-060 São
Paulo ⁄ SP, Brazil
E-mail: [email protected]
METHODS
Manuscript received: May 20, 2010; Revised: August 18, 2010;
Accepted: September 10, 2010
DOI: 10.1111/j.1751-7176.2010.00388.x
Official Journal of the American Society of Hypertension, Inc.
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
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
343
Aerobic Plus Resistance Training on Metabolic Syndrome
|
de Mello et al.
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 (16.711.47 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.
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 )70C 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.
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
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.
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
344
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
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.
Exercise Protocol.
AT Plus RT: The AT+RT regimen 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
Official Journal of the American Society of Hypertension, Inc.
Aerobic Plus Resistance Training on Metabolic Syndrome
(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
|
de Mello et al.
mation on the food pyramid, diet record assessment,
weight loss and miracle diets, food labels, dietetics, fatfree 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 a
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
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 inforOfficial Journal of the American Society of Hypertension, Inc.
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
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
345
346
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
Abbreviations: D, 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.
3.682.28c
12.91 (8.43–16.13)b,c,d
10.82 (6.82–14.71)a,c
9.18 (6.12–13.86)c
4.24 (3.02–10.69)
5.01 (3.20–10.21)
Adiponectin, lg ⁄ mL
6.66 (2.78–10.19)a
0.772.49
)19.8423.28c
)18.6317.50
149.3834.80b
90.5328.57b
135.5825.66a
77.7724.84a
173.4633.42
112.7330.11
4.5321.81
5.5315.14
167.6944.68
100.7633.09
159.0633.85
95.8625.68
162.4747.86
95.2037.40
Total cholesterol, mg ⁄ dL
LDL-C, mg ⁄ dL
)2.020.66
)0.780.62
2.410.83b,d
2.790.83b
4.791.37
3.470.53
3.851.38b
2.970.89b
Visceral, cm
Subcutaneous fat, cm
5.431.85
3.340.65
4.731.19a
3.170.88
)1.721.57
)0.390.79
2.730.94a
2.590.66a
)17.346.50c
2.315.22c
31.0013.73b,d
60.808.86
48.2312.13
59.998.59
34.6210.61b
62.219.40
40.028.66
64.1310.32
Fat mass, kg
Lean mass, kg
35.558.92a
60.867.30a
)5.678.05
)2.294.01
35.6613.37a
56.329.39
)15.456.95c
)5.542.41c
)11.426.10c
31.635.06b,d
33.2812.00b,d
91.3911.12
37.235.19
44.168.08
97.2111.26
108.2212.27
)2.622.38
)2.876.01
96.889.88
96.529.86
34.074.79b
35.559.04b
36.634.14
38.396.75
104.1511.92
BMI, wt ⁄ ht2
Fat mass, %
Body mass, wt
34.044.21a
36.607.12
)7.917.48
30.555.02a
30.0910.77a
b
1y
a
6 mo
Baseline
6 mo
a
1y
b
D at 1 y
Baseline
Aerobic Plus Resistance Training
Aerobic Training
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).
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).
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).
D at 1 y
de Mello et al.
Syndrome Before and After Intervention for Weight Loss With Different Kinds of Exercise
|
TABLE I. Body Composition, Subcutaneous and Visceral Adipose Tissues, and Biochemical Parameters in Obese Adolescents With the Metabolic
Aerobic Plus Resistance Training on Metabolic Syndrome
Official Journal of the American Society of Hypertension, Inc.
|
de Mello et al.
4
2
0
Changes in HOMA-IR
39.695.83
41.936.68
40.737.40
3.316.94
42.0710.84
42.407.63
40.407.35
Official Journal of the American Society of Hypertension, Inc.
6
Abbreviations: D, 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.
b
Baseline vs 1 year of intervention P.05. cBaseline vs 6 months P.05. d6 months vs 1 year of intervention P.05.
0.105.30
r=0.47 P =.02
HDL-C, mg ⁄ dL
)2.261.33
)17.0611.38a
)6.732.55
92.7612.70b
77 (58–198)
1.61 (0.58–3.87)a,b,d
3.10 (1.04–4.38)a,c
95.348.03c
71 (54–167)
3.67 (1.86–7.05)
110.3912.31
102 (43–206)
99.309.24b
91 (27–241)b
)5.706.37
)22.0029.61
3.36 (1.30–10.46)
104.477.87
108 (47–250)
Waist circumference, cm
Triglycerides, mg ⁄ dL
98.609.72c
94 (46–178)c
3.51 (1.98–14.40)
HOMA-IR
3.51 (1.98–14.40)
)1.163.88
)6.386.80a
)9.745.67
83.464.07a,b,d
7.70 (2.90–18.90)a,b,d
90.265.24
13.40 (5.00–19.30)a,c
90.006.10
17.30 (8.30–30.20)
1.616.77
)5.8117.70
93.767.87
13.70 (6.70–43.30)
94.466.99c
17.60 (5.30–51.80)
91.734.93
16.00 (8.40–63.2)
Glucose, mg ⁄ dL
Insulin, lU ⁄ mL
D at 1 y
16.2519.90
)8.335.77
1y
6 mo
118.373.47
77.294.89
Baseline
134.3316.35a
83.334.87
7.1412.66
)3.4611.43
D at 1 y
1y
115.715.13
76.535.54
117.134.10
78.565.24
6 mo
Baseline
122.6612.22
81.339.90
SBP, mm Hg
DBP, mm Hg
Aerobic Plus Resistance Training
Aerobic Training
TABLE II. Metabolic Syndrome Parameters in Obese Adolescents Before and After Intervention for Weight Loss
115.837.92b
74.165.14
Aerobic Plus Resistance Training on Metabolic Syndrome
-2
-4
-6
-8
-10
-12
-14
-6
-5
-4
-3
-2
-1
Changes in Visceral Fat
0
1
2
3
95% confidence
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.
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
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
347
Aerobic Plus Resistance Training on Metabolic Syndrome
|
de Mello et al.
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 HOMAIR 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
TABLE III. Frequency of Altered Metabolic
Syndrome Components at Baseline and After 1 Year
of Intervention in Obese Adolescents
Aerobic Plus
Resistance
Training
Aerobic
Training
Baseline
1y
Baseline
1y
MS (IDF, 2005)
(n=15)
(n=15)
(n=15)
(n=15)
Three or more
15
3a
15
0a
8
0
10
1a
4
1
a
0
0a
7
1
0a
0a
Waist circumference, cm
TG, mg ⁄ dL
15
5
12a
2a
15
3
7a
1a
HDL, mg ⁄ dL
11
6
11
9
Predictors of
components of MS
SBP, mm Hg
DBP, mm Hg
Glucose, mg ⁄ dL
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.
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
TABLE IV. Characteristics of Food Intake in Obese Adolescents With the Metabolic Syndrome Before and After
Intervention for Weight Loss
Aerobic Training
Variables
Energy intake, kcal
Baseline
6 mo
Aerobic Plus Resistance Training
1y
Baseline
2391.67907.94
1707.04462.13
1595.50409.26
Carbohydrate, g
Carbohydrate, %
302.70102.99
50.378.68
b
a
Protein, g
Protein, %
115.9264.89
18.425.16
88.2948.69b
20.655.72
85.5333.83
31.174.59
53.4519.59b
27.605.60
Lipid, g
Lipid, %
210.1949.60
51.737.92
a
2065.50582.38
6 mo
1y
1282.15369.85
b
1205.33384.88a,c
241.6292.38
49.307.41
b
182.1330.69
57.9210.75b
162.9248.33a
54.467.90
76.8823.23a
19.314.89
99.3446.03
18.405.21
58.4632.53b
16.995.53
53.7915.23a
18.494.08
46.7117.19a
26.807.24
75.1827.47
32.304.15
36.9720.20b
24.147.31
37.7322.23a
25.708.86
215.6472.60
53.819.74
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.
348
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
Official Journal of the American Society of Hypertension, Inc.
Aerobic Plus Resistance Training on Metabolic Syndrome
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 jB 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 longterm 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 ⁄ 530690, 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.
References
1. Pietiläinen KH, Kaprio J, Borg P, et al. Physical inactivity and obesity: a vicious circle. Obesity (Silver Spring). 2008;16:409–414.
2. Kim Y, Lee S. Physical activity and abdominal obesity in youth.
Appl Physiol Nutr Metab. 2009;34:571–581.
3. Brown T, Avenell A, Edmunds LD, et al. Systemic review of longterm lifestyle interventions to prevent weight gain and morbity in
adults. Obes Rev. 2009;10:627–638.
4. Caranti DA, Tock L, Prado WL, et al. Long-term multidisciplinary
therapy decreases predictors and prevalence of metabolic syndrome
in obese adolescents. Nutr Metab Cardiovasc Dis. 2007;17:e11–
e13.
5. American College of Sports Medicine. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2002;
34:364–380.
6. Barbeau P, Johnson MH, Howe CA, et al. Ten months of exercise
improves general and visceral adiposity, bone, and fitness in black
girls. Obesity (Silver Spring). 2007;15:2077–2085.
Official Journal of the American Society of Hypertension, Inc.
|
de Mello et al.
7. Eliakim A, Makowski GS, Brasel JA, et al. Adiposity, lipid levels,
and brief endrance training in nonobese adolescent males. Int J
Sports Med. 2000;21:332–337.
8. Gutin B, Barbeau P, Owens S, et al. Effects of exercise intensity on
cardiovascular fitness, total body composition, and visceral adiposity
of obese adolescents. Am J Clin Nutr. 2002;75:818–826.
9. Coppen AM, Risser JA, Vash PD. Metabolic syndrome resolution in
children and adolescents after 10 weeks of weight loss. J Cardiometab Syndr. 2008;3:205–210.
10. Dâmaso AR, do Prado WL, de Piano A, et al. Relationship between
nonalcoholic fatty liver disease prevalence and visceral fat in obese
adolescents. Dig Liver Dis. 2008;40:132–139.
11. McCall A, Raj R. Exercise for prevention of obesity and diabetes in
children and adolescents. Clin Sports Med. 2009;28:393–421.
12. Wickham EP, Stern M, Evans RK, et al. Prevalence of the metabolic
syndrome among obese adolescents enrolled in a multidisciplinary
weight management program: clinical correlates and response to
treatment. Metab Syndr Relat Disord. 2009;7:179–186.
13. Katsuki A, Sumida Y, Gabazza EC, et al. Plasma levels of agoutirelated protein are increased in obese men. J Clin Endocrinol Metab.
2001;86:1921–1924.
14. Kotronen A, Seppälä-Lindroos A, Bergholm R, et al. Tissue specificity of insulin resistance in humans: fat in the liver rather than muscle is associated with features of the metabolic syndrome.
Diabetologia. 2008;51:130–138.
15. Niklas B, You T, Pahor M. Behavioural treatments for chronic systemic inflammation: effects of dietary weight loss and exercise training. CMAJ. 2005;172:1199–1209.
16. Tanner JM, Whitehouse RH. Clinical longitudinal standards for
height, weight velocity and stages of puberty. Arch Dis Child.
1976;51:170–179.
17. Centers for Disease Control and Prevention. Prevalence of overweight among children and adolescents: United States, 1999–2000.
http://www.cdc.gov/nchs/products/pubs/pubd/hestats/overwght99.htm.
Accessed 28 June 2010.
18. Fields DA, Goran MI. Body composition techniques and the fourcompartment model in children. J Appl Physiol. 2000;89:613–620.
19. Ribeiro-Filho FF, Faria AN, Azjen S, et al. Methods of estimation of
visceral fat: advantages of ultrasonography. Obes Res. 2003;11:
1488–1494.
20. Zimmet P, Alberti KGMM, Kaufman F, et al. for the IDF Consensus Group. The metabolic syndrome in children and adolescents –
an IDF consensus report. Pediatr Diabetes. 2007;8:299–306.
21. World Health Organization (WHO). Report of a WHO consultation. In: Alwan A, King H, eds. Definition, Diagnosis and Classification of Diabetes Mellitus and Its Complications. Part 1: Diagnosis
and Classification of Diabetes Mellitus. Geneva: Department of
Noncommunicable Disease Surveillance, World Healthy Organization; 1999:1–59.
22. Foschini D, Araújo RC, Bacurau RF, et al. Treatment of obese adolescents: the influence of periodization models and ACE genotype.
Obesity (Silver Spring). 2010;18: 766–772.
23. Lofrano-Prado MC, Antunes HK, do Prado WL, et al. Quality of
life in Brazilian obese adolescents: effects of a long-term multidisciplinary lifestyle therapy. Health Qual Life Outcomes. 2009;7:61.
24. NRC (National Academic Press). Dietary Reference Intake: Applications in Dietary Assessment. Washington DC: National Academic
Press; 2001.
25. Hill RJ, Davies PS. The validity of self-reported energy intake as
determined using the doubly labeled water technique. Br J Nutr.
2001;85:415–430.
26. Stanton RA. Nutrition problems in an obesogenic environment. Med
J Aust. 2006;184:76–79.
27. Antić S, Lazarević G, Velojić M, et al. Exercise as a therapeutic
option in cardiometabolic risk reduction. Med Pregl. 2009;62(suppl
3):59–65.
28. Shaibi GQ, Cruz ML, Ball GD, et al. Effects of resistance training
on insulin sensitivity in overweight Latino adolescent males. Med
Sci Sports Exerc. 2006;38:1208–1215.
29. Davis JN, Kelly LA, Lane CJ, et al. Randomized control trial to
improve adiposity and insulin resistance in overweight Latino adolescents. Obesity (Silver Spring). 2009;17:1542–1548.
30. Balducci S, Zanuso S, Nicolucci A, et al. Anti-inflammatory effect
of exercise training in subjects with type 2 diabetes and the
metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis. 2010;20:
608–617.
31. Elloumi M, Ben Ounis O, Makni E, et al. Effect of individualized
weight-loss programmes on adiponectin, leptin and resistin levels in
obese adolescent boys. Acta Paediatr. 2009;98:1487–1493.
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
349
Aerobic Plus Resistance Training on Metabolic Syndrome
|
de Mello et al.
32. Christian AH, Mochari H, Mosca LJ. Waist circumference, body
mass index, and their association with cardiometabolic and global
risk. J Cardiometab Syndr. 2009;4:12–19.
33. Manigrasso MR, Ferroni P, Santilli F, et al. Association between circulating adiponectin and interleukin-10 levels in android obesity:
effects of weight loss. J Clin Endocrinol Metab. 2005;90:5876–
5879.
350
The Journal of Clinical Hypertension
Vol 13 | No 5 | May 2011
34. Wang Y, Zhou M, Lam KSL, et al. Protective roles of adiponectin
in obesity related fatty liver diseases: mechanisms and therapeutic
implications. Arq Bras Endocrinol Metabol. 2009;53:201–212.
35. de Piano A, Tock L, Carnier J, et al. Negative correlation between
NPY ⁄ AgRP concentration and adiponectinemia in Nonalcoholic
Fatty Liver Disease obese adolescents submitted to a long-term interdisciplinary therapy. Metabolism. 2010;59:613–619.
Official Journal of the American Society of Hypertension, Inc.