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Diabetes & Metabolism 34 (2008) 595–600

Original article

Effects of two-month physical-endurance and diet-restriction programmes
on lipid profiles and insulin resistance in obese adolescent boys
O. Ben Ounis a,∗ , M. Elloumi a , I. Ben Chiekh a , A. Zbidi a , M. Amri c , G. Lac b , Z. Tabka a
a

Laboratory of Cardio-Circulatory, Respiratory, Metabolic and Hormonal Adaptations to the Muscular Exercise,
Faculty of Medicine Ibn El Jazzar, 4002 Sousse, Tunisia
b Department of biology, University Blaise-Pascal, 63177 Aubière, France
c Department of biology, University El Manar, 1002 Tunis, Tunisia
Received 6 January 2008; received in revised form 23 May 2008; accepted 30 May 2008
Available online 18 October 2008

Abstract
Aim. – The aim of this study was to assess the impact of a two-month programme of physical endurance and dietary restriction, alone and
combined, on plasma lipids and insulin resistance in obese adolescents.
Methods. – A total of 24 obese adolescent boys participated in programmes of either dietary restriction (R), physical endurance at the point
of maximum lipid oxidation (LIPOXmax ) (E) or diet combined with training (R + E). Anthropometric characteristics, metabolic measures and
biochemical analyses were performed in all subjects before and after the interventions. An estimated insulin resistance was calculated using the
homoeostasis model assessment (HOMA-IR) index.
Results. – At the end of the two-month programmes, adolescents in the R + E group showed greater reductions in body mass index
(−3.9 ± 0.7 kg/m2 ) and waist circumference (−12.3 ± 4.8 cm) (P < 0.001) than either the R or E group. A significant decrease (P < 0.01) in
HOMA-IR index (−2.13 ± 0.11), plasma triglycerides, LDL and total cholesterol was also seen in the R + E group. Moreover, at the end of the
programme, the ratio of HDL cholesterol to triglycerides was significantly increased from baseline in the R + E group (0.93 ± 0.09 vs. 0.68 ± 0.11;
P < 0.01).
Conclusion. – Compared with either moderate physical endurance or dietary restriction, a combination of both resulted in a significant decrease
in cardiovascular risk factors and HOMA-IR index in obese adolescent boys.
© 2008 Elsevier Masson SAS. All rights reserved.
Résumé
Effet sur le profil lipidique et la résistance à l’insuline d’un programme comportant un entraînement en endurance, combiné ou non à un régime
alimentaire, pendant deux mois chez des adolescents obèses.
Objet. – Évaluer les effets d’un régime alimentaire et d’un programme d’entraînement en endurance de deux mois sur la résistance à l’insuline
et les lipides plasmatiques, indépendamment et combinés chez des adolescents obèses.
Méthodes. – Vingt-quatre garc¸ons adolescents obèses ont participé au programme comparant les effets d’un régime alimentaire (R), d’un
entraînement en endurance au point d’oxydation maximal des lipides (LIPOXmax ) (E) et d’un régime associé à l’entraînement (R + E). Les
caractéristiques anthropométriques, les mesures métaboliques et les analyses biochimiques ont été enregistrées chez tous les sujets avant et après
les programmes. L’estimation de la résistance à l’insuline a été calculée par l’index HOMA-R.
Résultats. – À l’issue de ce programme, R + E a montré une diminution plus importante de l’indice de masse corporelle (−3,9 ± 0,7 kg/m2 ) et du
tour de taille (−12,3 ± 4,8 cm) (P < 0,001) que R et E. Une diminution significative (P < 0,01) du HOMA-R (−2,13 ± 0,11), des triglycérides, du
LDL cholestérol et du cholestérol total a été observée chez R + E. Par ailleurs, le rapport du HDL cholestérol)/triglycérides était significativement
augmenté chez R + E (0,93 ± 0,09 vs 0,68 ± 0,11 ; P < 0,01).



Corresponding author.
E-mail address: omar oda@yahoo.fr (O. Ben Ounis).

1262-3636/$ – see front matter © 2008 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.diabet.2008.05.011

596

O. Ben Ounis et al. / Diabetes & Metabolism 34 (2008) 595–600

Conclusion. – Comparée au régime alimentaire seul ou à l’entraînement en endurance seul, la combinaison des deux programmes induit une
réduction plus importante du niveau des facteurs de risque cardiovasculaire et de l’index HOMA-R.
© 2008 Elsevier Masson SAS. All rights reserved.
Keywords: Obese adolescents; Lipid; Insulin resistance; Physical exercise; Training programme; Low-calorie diet
Mots clés : Adolescents obèses ; Lipides ; Résistance à l’insuline ; Exercice physique ; Programme d’entraînement ; Régime hypocalorique

Abbreviations
R
E
R+E
LIPOXmax
LIPOXmax (mg/min)
COP
Wmax
VO2 max
HR
WC
BF%
FM
FFM
PS
VCO2

Diet restriction
Exercise training
Diet restriction combined with exercise
training
point Maximal lipid oxidation point
Maximal rate of lipid oxidation
Crossover point
Maximum aerobic power
Maximum oxygen uptake rate
Heart rate
Waist circumference
Body fat in percentage
Fat mass
Fat free mass
Pubertal status
Dioxide of carbon rejected rate

1. Introduction
There is a global epidemic of obesity in children and adolescents in most of the developed countries today. This epidemic
has been accompanied by a marked increase in the frequency
of cardiovascular risk factors such as high blood pressure, dyslipidaemia and insulin resistance [1], the main component of
the metabolic syndrome seen in a large number of overweight
adolescents [2].
Waist circumference has been considered an acceptable surrogate marker of abdominal fat mass in adolescents [3], an
increase in which is also associated with increased levels of
cardiovascular risk factors [4]. An unbalanced diet and a lack
of physical activity have been suggested to promote the development of excess fat storage in adipose tissue, which is an
endocrine organ producing a variety of factors that can regulate
energy metabolism and insulin sensitivity [5].
Skeletal muscle is the most important regulator of fat oxidation and can have a positive impact on fat-mass balance. Defects
in muscle lipid metabolism have been observed in obese individuals both at rest and during exercise [6]. It is well accepted
that prolonged aerobic exercise has beneficial effects on tissue
sensitivity to insulin [7] and on the transport of blood lipids
[8].
Weight loss has been shown to favourably affect several
indicators of cardiovascular risk such as plasma lipids [9]. However, high-density lipoprotein cholesterol (HDL-C) levels are
generally not improved [10]. As a low HDL-C is associated
with increased cardiovascular risk [11], this may minimize the
overall impact of diet on the risk of cardiovascular disease.
On the other hand, exercise is associated with an increase
in HDL-C [12]. For this reason, a combination of diet and

exercise may be the optimal approach to controlling dyslipidaemia.
Brandou et al. [13] developed a model of maximum fat oxidation (LIPOXmax ) based on the ‘crossover concept’ [14]. We
used these two parameters to prescribe individualized exercise
training for each of our study subjects.
The present study investigated the effects of diet and
endurance training—alone or combined—on weight loss,
insulin resistance and blood-lipid parameters in obese adolescent boys over a two-month period. We hypothesized that the
combined diet and exercise regime would bring about improvements in insulin resistance and serum lipid profile via its effects
on lipid oxidation during exercise.
2. Materials and methods
2.1. Subjects
We selected 24 obese adolescent boys, aged 12–14 years,
whose body mass index (BMI) was greater than 97th percentile,
as defined by French population curves [15]. None of the subjects were using drugs or other therapy for obesity, and none
had prior histories of disease or injury that would prevent daily
exercise. Consent to participate in the rehabilitation programme
was obtained from each boy and his parents, and the project was
approved by the Research Ethics Committee of the Faculty of
Medicine, University of Sousse, in Tunisia.
The subjects were randomly assigned to one of three programme groups:
• diet (R);
• physical training at LIPOXmax (E);
• and diet plus training (R + E).
2.2. Anthropometry
Height, weight, and hip and waist circumferences were
recorded. BMI was calculated as weight in kilograms divided
by height in meters squared (kg/m2 ).
In all subjects, two skin-fold thicknesses (triceps and subscapular) were measured in triplicate by the same trained
observer. Measurements were made on the right-hand side of
the body using a Harpenden calliper.
Body-fat percentage (BF%) was calculated using the
equations of Slaughter et al. [16] for boys with triceps
and subscapular skin folds less than 35 mm as follows:
BF% = 1.21 × (Σ) – 0.008 × (Σ) 2 −1.7, where Σ is the sum
of two skin folds (triceps and subscapular) in millimetre.

O. Ben Ounis et al. / Diabetes & Metabolism 34 (2008) 595–600

Pubertal stage was evaluated according to the Tanner classification [17] by a trained paediatrician:
• prepubertal children were those in Tanner stage I;
• pubertal children were in Tanner stages II–III;
• and post-pubertal children were in Tanner stages IV–V.
2.3. Biochemical analysis
Total cholesterol (TC), triglycerides (TG), HDL-C and glucose levels were measured in all subjects before and after the
interventional programmes using standardized techniques, as
described by Wegge et al. [18]. LDL-C was calculated using the
Friedewald formula [19], and plasma insulin was assayed using
the IRMA kit (Immunotech, France). An estimate of insulin
resistance was calculated by the homoeostasis model assessment (HOMA-IR) index as: [fasting insulin (␮U/mL) × fasting
glucose (mmol/L)]/22.5.
To distinguish normal from impaired insulin sensitivity,
HOMA-IR greater than 2.5 and greater than 4.0 were the cut-off
points used in children and adolescents, respectively [20]. We
adapted guidelines from the World Health Organization (WHO)
[21] to define the metabolic syndrome:
• raised arterial blood pressure defined as systolic blood pressure greater or equal to 140 mmHg and/or diastolic blood
pressure greater or equal to 90 mmHg;
• raised plasma triglycerides greater or equal to 1.7 mmol/L
and/or HDL cholesterol less than 0.9 mmol/L;
• waist-to-hip ratio greater than 0.9 and/or BMI greater
than 30 kg/m2 .

597

VCO2 were determined as the means of measurements taken during the fifth and sixth minutes of each state, according to MacRae
et al. [24].
In addition, after smoothing the curves, we calculated two
parameters to represent the balance between fat and CHO utilization induced by increasing exercise intensity:
• the crossover point (COP) of substrate utilization;
• and the maximum fat-oxidation (LIPOXmax ) point, as previously described [14,13].
2.5. Dietary programme
The subjects in the R and R + E groups recorded (four
times/week), in a specially designed notebook, the quantity of
and time at which food was eaten. A dietician then prescribed
each individualized diet, including the quantity and type of foods
recommended, after an initial dietary assessment to determine
the total amount of calories to be consumed per day. The diet
was set at 500 kcal per day below the initial dietary records, and
comprised 15% proteins, 55% carbohydrates and 30% lipids.
The foods were selected according to the subjects’ usual eating
habits.
2.6. Training programme
Physical training (E and R + E) was carried out four days a
week (90 min per day) for two months at a HR corresponding to
LIPOXmax , in a gymnasium supervised by physical-education
professors. Exercises included a warm-up, running, jumping
and playing with a ball. During each exercise session, HR was
continuously monitored (Polar Electro, Kempele, Finland).

2.4. Exercise testing
2.7. Statistical analysis
The subjects performed an exercise test on an electromagnetically braked cycle ergometer (Ergoline, Bitz, Germany)
according to the protocol described by Brandou et al. [13]. Gas
exchange was monitored on a breath-by-breath basis, using a
metabolic cart (ZAN 600, ZAN Messgeräte, Oberthulba, Germany).
The maximum oxygen-uptake rate (VO2 max ) and maximum
aerobic power (Wmax ) was calculated according to Wasserman’s
equation for obese boys [22]:
VO2max = (28.5 × weight) + 288.1.
The following equation was used to calculate Wmax [22]:


Wmax = VO2 max –10 (× weight) /10.3.
The test consisted of five consecutive six-minute steady-state
workloads at 20, 30, 40, 50 and 60% of Wmax . Heart rate
(HR) was monitored by electrocardiography during the exercise testing (ZAN ECG 800, ZAN Messgeräte).Calculation
of cholesterol (CHO) and lipid-oxidation rates were assessed
from gas-exchange measurements according to the non-protein
respiratory quotient (R) technique [23] where: CHO (mg/
min) = 4.585 VCO2 – 3.2255 VO2 ; lipids (mg/min) = 1.7012
VCO2 + 1.6946 VO2 (with VO2 and VCO2 in mL/min). VO2 and

Data are presented as means plus or minus standard deviations (S.D.). Paired Student’s t test was used for comparisons
among the three groups (R, E and R + E), and unpaired Student’s
t test for group comparisons. Repeated-measures ANOVA compared the responses of each group at different times during the
test, and before and after the interventions.
Tukey’s post-hoc test was used to compare means and, to evaluate the relationships between various parameters, Spearman’s
correlation analysis was performed. P < 0.05 was considered
statistically significant.
3. Results
3.1. Anthropometric characteristics
Anthropometric characteristics are summarized in Table 1.
The three groups were closely matched by age, adiposity and
pubertal stage (Table 1). Daily energy intake was significantly
reduced during the two-month intervention in the R and R + E
groups (P < 0.01), and did not differ between the two groups.
The HR corresponding to LIPOXmax used to set the intensity
of the training programme did not vary between individ-

598

O. Ben Ounis et al. / Diabetes & Metabolism 34 (2008) 595–600

Table 1
Anthropometric characteristics and metabolic parameters of adolescents before and after the two-month dietary-restriction (R), exercise-training (E) and diet-plustraining (R + E) programmes.
R group (n = 8)
Before
Age (years)
PS (I/II–III/IV–V)
Weight (kg)
Height (cm)
BMI (kg/m2 )
FM (kg)
FFM (kg)
Waist (cm)
Hip (cm)
Glucose (mmol/L)
Insulin (␮U/mL)
HOMA-IR
TG (mmol/L)
TC (mmol/L)
HDL-C (mmol/L)
LDL-C (mmol/L)
LDL-C/HDL-C ratio
TC/HDL-C ratio
HDL-C/TG ratio

81.4
163.3
30.7
34.8
46.6
97.3
107.1
4.61
22.6
4.63
1.41
4.24
1.02
2.57
2.52
4.16
0.72

±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±

E group (n = 8)
After

13.7
4.1
2.6
5.3
6.2
8.2
7.2
0.13
6.2
1.7
0.16
0.31
0.08
0.19
0.29
0.25
0.07

13.1 ± 0.7
2/3/3
74.6
163.3
27.8
29.2
45.4
91.1
101.2
4.53
21.8
4.39
1.39
3.93
0.99
2.30
2.32
3.97
0.71

Before

±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±

12.8**
5.1
2.6**
6.2**
4.3*
9.7**
5.5*
0.18
4.3
1.8
0.18
0.63*
0.11
0.26*
0.31
0.32
0.14

80.1
163.8
30.2
34.3
45.8
96.4
100.5
4.58
21.2
4.32
1.40
4.22
1.03
2.55
2.48
4.10
0.74

±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±

R + E group (n = 8)
After

15.8
2.9
4.2
7.2
5.7
11.2
8.8
0.27
5.7
1.3
0.12
0.27
0.06
0.11
0.18
0.28
0.06

13.2 ± 0.1
3/3/2
78.2
163.9
29.4
32.6
45.6
94.6
99.9
4.56
16.1
3.26
1.27
4.01
1.09
2.34
2.15
3.68
0.86

Before

±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±

15.3
3.1
4.9
6.3
4.8
10.2
8.2
0.17
3.6*
1.1*
0.11*
0.42
0.1*
0.34
0.16*
0.31*
0.15*

84.5
164.2
31.3
35.4
49.1
98.6
107.6
4.64
23.2
4.78
1.45
4.29
0.98
2.64
2.69
4.38
0.68

±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±
±

After

13.5
2.6
4.0
5.7
3.4
6.7
9.1
0.15
4.6
1.2
0.21
0.58
0.08
0.13
0.22
0.19
0.11

13.3 ± 0.7
2/3/3
73.0 ±
164.7 ±
27.4 ±
24.2 ±
48.8 ±
86.3 ±
98.7 ±
4.32 ±
13.8 ±
2.65 ±
1.21 ±
3.78 ±
1.13 ±
2.09 ±
1.85 ±
3.35 ±
0.93 ±

14.1***
1.3
4.4***
6.3***
6.2
8.2***
8.6***
0.22**
3.3**
1.5**
0.19**
0.52**
0.14**
0.21**
0.13**
0.20**
0.09**

Data are means ± S.D.
PS: pubertal status; BMI: body mass index; FM: fat mass; FFM: fat-free mass; HOMA-IR: homoeostasis model assessment index for insulin resistance; TG:
triglycerides; TC: total cholesterol; HDL-C: high-density lipoprotein cholesterol; LDL-C: low-density lipoprotein cholesterol.
* P < 0.05, ** P < 0.01, *** P < 0.001.

uals in the E (HR = 127.2 ± 4.1 bpm; P < 0.05) and R + E
(HR = 124.5 ± 3.6 bpm; P < 0.05) groups.
After the two-month programme, BMI, waist circumference and fat mass decreased significantly in both the R
(−2.9 ± 0.2 kg/m2 , −6.2 ± 2.4 cm and −5.6 ± 0.8 kg, respectively; P < 0.01) and R + E (−3.9 ± 0.7 kg/m2 , −12.3 ± 4.8 cm
and −11.2 ± 3.7 kg, respectively; P < 0.001) groups (Table 1).
There were no significant changes in these parameters in the E
group.
3.2. Substrate oxidation
Parameters of substrate utilization changed (Fig. 1), with
increases in COP and LIPOXmax points in the E (+12.8% ± 3.2
of Wmax and +66.0 ± 12.3 mg/min, respectively; P < 0.05)
and R + E (+20.4% ± 4.6 of Wmax and +108.4 ± 23.6 mg/min,
respectively; P < 0.001) groups. No changes were observed in
the R group (Fig. 1).
3.3. Biochemical analysis
Neither the plasma concentrations of glucose and insulin nor
the lipid profile differed across the three groups before the programme (Table 1). However, after the two-month intervention,
fasting insulin levels decreased significantly in the E and R + E
groups: −5.1 ± 1.3 ␮U/mL (P < 0.05) and −9.4 ± 3.6 ␮U/mL
(P < 0.01), respectively. In addition, the post-interventional
HOMA-IR (insulin resistance) was significantly improved in the
E (P < 0.05) and R + E (P < 0.01) groups, whereas the R group
showed no significant reduction. The R + E group also showed

Fig. 1. Delta comparison before and after intervention of the parameters
of substrate utilization. A. Crossover point (COP) expressed as the percent
of maximum working capacity (%Wmax ). B. Maximum rate of fat oxidation (LIPOXmax ) expressed in mg/min. Values are expressed as means ± S.D.
* P < 0.05; *** P < 0.001.

O. Ben Ounis et al. / Diabetes & Metabolism 34 (2008) 595–600

significant decreases in plasma TG, LDL-C and TC concentrations, and in LDL-C/HDL-C and TC/HDL-C ratios (P < 0.01),
while the R group achieved significant decreases in plasma TC
and LDL-C (P < 0.05) (Table 1).
However, in the E group, reductions were less marked for all
measures (P < 0.05), with no changes in either TC or LDL-C.
Also, after the intervention, the E group’s HDL-C/TG ratio was
higher (0.86 ± 0.15 vs. 0.74 ± 0.06; P < 0.05), as was that of the
R + E group (0.93 ± 0.09 vs. 0.68 ± 0.11; P < 0.01). No changes
were observed in the R group in HDL-C/TG ratio (Table 1).
3.4. Correlations among improvements due to the three
programmes
Waist circumference and the HOMA-IR (r = 0.69; P < 0.01)
were significantly correlated in the R + E subjects. In those in
the E and R + E groups, significant correlations were observed
between changes in LIPOXmax and LDL-C/HDL-C ratio
(r = −0.32; P < 0.05 and r = −0.53; P < 0.01, respectively), and
between changes in LIPOXmax and TC/HDL-C ratio (r = −0.37;
P < 0.05 and r = −0.62; P < 0.01, respectively).
4. Discussion
The present study compared the effects of physical-endurance
training and dietary restriction, alone and combined, on insulin
resistance and lipid profile in obese Tunisian boys. We found
that dietary intervention on its own promoted fat loss, and
improved TC and LDL-C levels, whereas training intervention
alone increased lipid oxidation during exercise, improved the
usual index of insulin resistance and plasma triglycerides, and
increased HDL-C. The combined diet plus training resulted in
further improvements in body composition, insulin resistance
and serum lipid profile, and also offered further benefits to
HDL-C, HDL-C/TG ratio and measures of LIPOXmax .
Obesity is a major independent risk factor for cardiovascular
disease [1]. In humans, a higher risk of atherosclerosis has been
found with high concentrations of TC and LDL-C, and low concentrations of HDL-C [25]. Moreover, low HDL-C levels are
often a reflection of insulin resistance [26].
In addition, it has been suggested that ratios of TC/HDL
and LDL/HDL are better predictors of cardiovascular disease
(CVD) risk reduction than HDL, LDL or TC values on their
own [27]. Evidence to support this idea comes from the reduced
cardiovascular disease risk in subjects after following the R + E
programme. In the present study, TC and LDL-C, along with
the ratios of TC/HDL-C and LDL-C/HDL-C, were significantly
reduced after a programme of diet combined with physical training.
Although exercise alone did not change TC or LDL-C, it had
a positive influence on HDL-C and the TC/HDL-C ratio. Dietary
restriction has led to either a decrease or no change in HDL-C
[10]. In the present study, exercise significantly increased HDLC (P < 0.05 and P < 0.01 with E and R + E, respectively), whereas
the diet group experienced a decline in HDL-C (P = 0.8).
These findings are in agreement with a previous study showing that eight weeks of endurance exercise three times a week

599

increased HDL-C by approximately 10% [28]. Thus, adding
exercise training at LIPOXmax to a restricted diet appears to be
an important factor in improving blood-lipid profiles in obese
adolescents.
As for insulin sensitivity, we observed a small reduction
in fasting glucose accompanied by a much larger decrease in
insulin after the diet plus exercise intervention. Nevertheless,
HOMA-IR decreased significantly (P < 0.01) with R + E, suggesting a decrease in insulin resistance.
In this study, insulin resistance status was assessed by the
HOMA-IR index. However, in children, the validity of this surrogate has been challenged. Indeed, Brandou et al. have reported
a poor correlation between insulin sensitivity and HOMA-IR
index in children aged six to 18 years, suggesting a limited accuracy of this surrogate as a predictor of insulin sensitivity in this
population [29].
Previous studies in overweight children after regular exercise programmes have reported improvements in fasting insulin
[7], whereas diet plus aerobic exercise (three days per week)
improved HOMA-IR in overweight subjects [30]. Exercise
is known to increase insulin-receptor autophosphorylation,
GLUT4 expression and glucose transport [31]. In addition, a
third major cause of insulin resistance is a sedentary lifestyle.
An immediate effect of exercise is an increase in glucose transporters in muscle, which secondarily improves insulin-mediated
glucose disposal [32].
In the present study, changes in body composition did not
correlate significantly with metabolic changes after a two-month
dietary programme. However, the reduced risk of cardiovascular
disease was associated with an increase in fat oxidation in the E
and R + E subjects.
Our study further demonstrates that low-intensity (at
LIPOXmax ) training should be routinely recommended for obese
adolescents. Indeed, it is useful to propose to such a population several options of exercise of variable intensity, according
to their level of sedentarity, to optimize lipid utilization during
exercise [33].
5. Conclusion
The main findings of this study are that two months of
individualized exercise training at LIPOXmax combined with a
restricted diet can result in improvements in plasma lipoproteins, lipid profile and insulin resistance. In addition, such
an intervention can reduce fat mass, waist circumference
and improve ‘fat-burning’ during submaximum exercise. For
this reason, this intervention may be the optimal approach
for the prevention and management of adolescent obesity
and the cardiovascular risk factors present in this population.
Acknowledgements
This study was supported by the Ministry of Higher
Education, Scientific Research and Technology of
Tunisia.

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©Journal of Sports Science and Medicine (2008) 7, 437-445
http://www.jssm.org

Research article

Impact of diet, exercise and diet combined with exercise programs on plasma
lipoprotein and adiponectin levels in obese girls
Omar Ben Ounis 1 , Mohamed Elloumi 1, Mohamed Amri 3, Abdelkarim Zbidi 1, Zouhair Tabka 1
and Gerard Lac 2
1

Laboratory of Physiology, Faculty of Medicine, Sousse, Tunisia, 2 Laboratory of Exercise Biology, University Blaise
Pascal, Clermont-Ferrand, France, 3 Laboratory of Physiology, Faculty of Sciences, Tunis, Tunisia.

Abstract
We studied the effect of three programs, diet restriction (D),
individualized exercise training (E) at the maximal lipid oxidation point (LIPOXmax) and diet combined with exercise (D+E),
on body mass, plasma lipoprotein and adiponectin levels in
obese girls. Eighteen obese adolescents girls aged 12-14 years
were studied. A longitudinal intervention was carried out, consisting of a two-month diet (D; –500 kcal·day-1), of individualized exercise (E; 4 days/week, 90 min·day-1) and of diet combined with exercise (D+E). Body mass, body mass index (BMI),
body fat mass, waist circumference, substrate crossover point,
LIPOXmax point, homeostasis model assessment (HOMA-IR)
index, fasting levels of lipids and circulatory adiponectin, were
measured in all subjects before and after the program. In subjects of the D+E group, body mass, BMI, body fat mass, waist
circumference, HOMA-IR, low-density lipoprotein cholesterol
(LDL-C) and total cholesterol / high-density lipoprotein cholesterol (TC/HDL-C) ratio were significantly lower, and HDL-C
and adiponectin were higher after the program than that of subjects in the D or E groups. Diet/exercise improved the ability to
oxidize lipids during exercise (crossover point: + 18.5 ± 3.4 of
% Wmax; p < 0.01 and fat oxidation rate at LIPOXmax: + 89.7
± 19.7 mg·min-1; p < 0.01). In the D+E group, significant correlations were found between changes in body mass and adiponectin and between changes in the TC/HDL-C ratio and LIPOXmax. These findings show that the combined program of
diet restriction and individualized exercise training at the LIPOXmax point is necessary to simultaneously improve body
mass loss, adiponectin levels, as well as metabolic parameters,
in obese girls.
Key words: Obese girls, lipoprotein, adiponectin, exercise
training, diet restriction.

Introduction
Obesity is a major independent risk factor for cardiovascular disease (Scaglione et al., 2004). Skeletal muscle is
largely involved in the development of obesity (PerezMartin et al., 2001). Moreover, muscular abnormalities
alter the balance of substrate utilization, thus facilitating
fat accumulation in adipose tissue. In contrast, regular
exercise training, generally recommended for obese people, induces muscular metabolic changes, which can reverse these defects (Dumortier et al., 2003).
However, it is now well accepted that adipose tissue is a major endocrine organ producing a variety of
factors that regulate energy metabolism and insulin sensi-

tivity (Kershaw and Flier, 2004). An increased adipose
tissue mass is associated with insulin resistance, hyperglycemia, hypertension and other components of the
metabolic syndrome (Després, 2006).
Adiponectin levels decrease with obesity (Ariata et
al., 1999), and low adiponectin concentration is associated
with insulin resistance (Hotta et al., 2000). Body mass
reduction is followed by an increase in plasma adiponectin concentration (Esposito et al., 2003) and a lowering of several indicators of cardiovascular risk, such as
plasma lipids (Gerhard et al., 2004).
Obesity is characterized by three primary lipoprotein abnormalities: increased triglyceride-rich lipoproteins, increased small low-density lipoprotein (LDL)
particles, and reduced levels of high-density lipoprotein
(HDL) (Grundy, 1998). Moreover, HDL-C concentrations
are commonly a reflection of insulin resistance (Karhapaa
et al., 1994).
Several studies have shown that endurance exercise training has a beneficial effect on conventional
plasma lipoprotein lipids and on circulatory adiponectin
levels (Kraus et al., 2002; Kriketos et al., 2004). Indeed,
Kang et al. (2002) demonstrated that physical activity had
a beneficial effect on LDL particle diameters in obese
adolescents. A recent meta-analysis reported that diet
combined with exercise favours the reduction in LDL-C
and triglycerides but lessens the increase in HDL-C, when
compared with exercise alone (Leon and Sanchez, 2001).
In addition, Kriketos et al. (2004) reported that fasting
adiponectin levels increased by 260% above baseline
values after 2-3 bouts of low to moderate intensity exercise.
Recently, exercise calorimetry has been developed
by several teams in order to target more closely training
protocols for both adults (Dumortier et al., 2003; PerezMartin et al., 2001) and adolescents (Brandou et al., 2003)
suffering from obesity. Consequently, it becomes important to know how diet combined with exercise modifies
the balance of substrates as assessed with this technique
in obese adolescents.
Therefore, in this study we investigated separately
the effects of two-month diet, individualized exercise
training at the point where fat oxidation was maximal
(LIPOXmax) and diet combined with exercise on the
body composition, plasma lipoprotein, metabolic parameters and circulatory levels of adiponectin in obese girls.
Our working hypothesis was that exercise training

Received: 12 May 2008 / Accepted: 04 July 2008 / Published (online): 01 December 2008

438

combined with diet restriction would decrease body fat
mass, insulin resistance and LDL-C and increase adiponectin and HDL-C via its effect on fat oxidation during
exercise.

Methods
Subjects
We examined eighteen obese adolescent girls from two
colleges in the centre of Tunisia. Obesity was defined as a
body mass index (BMI; kg·m-2) greater than the 97th percentile defined by Cole et al. (2000). The pubertal stage
was evaluated according to the Tanner classification
(Tanner et al., 1966) by a trained paediatrician. Prepubertal adolescents comprised those subjects who where
in Tanner stage I, pubertal adolescents those in Tanner
stage II-III and post-pubertal adolescents in Tanner stage
IV-V.
Criteria for participation in the present study included: no past history of cardiovascular disease, no history of smoking, no history of prescribed medicine, and
no regular exercise. This study was approved by the Research Ethics Committee of the Faculty of Medicine,
University of Sousse, Tunisia. The subjects were randomly assigned in 3 evenly divided program groups of 6
subjects: diet restriction (D), individualized exercise training (E) and diet/exercise (D+E). The adolescents and their
parents gave a written informed consent for the experimental protocol.
Anthropometric measurements
Height was measured to the nearest 0.1 cm, waist circumference on the skin at the level of the navel to the nearest
0.2 cm, and total body mass to the nearest 0.1 kg on a
digital scale (OHAUS, Florhman Park, NJ). Participants
were nude or wearing only underwear for measurements
of body mass. Body mass index (BMI) was calculated
using the standard formula: body mass in kilograms divided by height in meters squared (kg·m-2).
The body fat percentage (BF%) was calculated by
using the equation of Slaughter et al. (1988) for children
with triceps and subscapular skinfolds < 35 mm: Girls =
1.33 (sum of 2 skinfolds) – 0.013 (sum of 2 skinfolds2) –
2.5. BF% for children with triceps and subscapular skinfolds > 35 mm: Girls = 0.546 (sum of 2 skinfolds) + 9.7
Two skinfold thicknesses (triceps and subscapular) were measured in the subjects of the three
groups, by the same trained observer to the nearest
0.1mm. Measurements were made on the right hand side
of the body using a Harpenden calliper. Three measurements were taken at each site and the closest two measurements were averaged for use in the analysis. The testretest data were then used to calculate the precision of all
body composition measurements. Each anthropometric
measurement was performed by the same technician for
all participants before and after the two-month intervention.
Biochemical measurements
Fasting adiponectin and insulin were measured before and
after the two-month intervention program. Plasma adiponectin was determined using an ELISA kit (B-Bridge

Adiponectin / lipoprotein in obese girls

international, inc). Insulin was assayed using an IRMA
Insulin kit (Immunotech, France). Assays were carried out
following the manufacturer’s instructions.
Total cholesterol (TC), triglycerides (TG), highdensity lipoprotein cholesterol (HDL-C) and glucose
levels were measured in all subjects before and after the
programs following 12 hours fasting using standardized
techniques described by Wegge et al. (2004). Low-density
lipoprotein cholesterol (LDL-C) was calculated as described by the Friedewald formula (Friedewald et al.,
1972).
Homeostasis model assessment (HOMA-IR) was
used to estimate the degree of insulin resistance, and
calculated using the formula: HOMA-IR = [insulin
(mU·liter-1) × glucose (mmol·liter-1)] / 22.5
To distinguish normal from impaired insulin sensitivity, HOMA-IR > 4.0 was the cut-off level employed for
adolescents, according to the normal values provided by a
previous study (Annunzio et al., 2004). Definition of the
metabolic syndrome in adolescents was made according
to the World Health Organization criteria (Alberti and
Zimmet, 1998).
Exercise testing
The subjects performed an exercise test on an electromagnetically braked cycle ergometer (Ergo-line, Bitz,
Germany) connected to a breath by breath device (ZAN
600, Meβgeräte, Germany) for gas exchange measurements (VO2 and VCO2). The conditions and requirements
of the exercise testing were explained to each subject
before the test. The laboratory temperature and relative
humidity were between 22-24°C and 76% respectively
during the test period.
Maximum oxygen consumption (VO2max) and
theoretical maximal working capacity (Wmax) were calculated for each subject before exercise testing using the
predictive equations of Wasserman et al. (1986) for obese
children. These equations take into account sex and anthropometric characteristics: Girl: VO2max = (52.8 × M)
– 303.4. Wmax = (VO2max – 10 (×M)) × (10.3)-1. M is
the body mass of the subject in kg.
The test consisted of a progressive increase in
workload every 6 min with 5 steady-state workloads corresponding to 20, 30, 40, 50, and 60 % of Wmax. Heart
rate was monitored electrocardiographically throughout
the test (ZAN ECG 800, Meβgeräte, Germany). The subjects underwent a test with the same relative incremental
workload and were compared at the same percentage of
their Wmax. The results of this test were used to determine the exercise training intensity.
Carbohydrate (CHO) and fat oxidation rates were
calculated from the gas exchange measurements according to the non-protein respiratory quotient (R) technique
(Peronnet and Massicote, 1991): CHO oxidation rate
(mg·min-1) = 4.585VCO2 – 3.2255VO2. Fat oxidation rate
(mg·min-1) = 1.6946 VO2 – 1.7012 VCO2.
VO2 and VCO2 were determined as the means of
measurements during the fourth and sixth minutes of each
work load, according to MacRae et al. (1995). This technique provided CHO and lipid oxidation rates at different
levels of exercise.
The percentage of CHO and fat oxidation were

Ounis et al.

439

Table 1. Subjects characteristics before and after the two-month program. Data are means (± SD).
Diet (n = 6)
Exercise (n = 6)
Diet/Exercise (n = 6)
Before
After
Before
After
Before
After
Age (years)
13.4 (.2)
13.1 (.1)
13.0 (.4)
PS (I / II-III / IV-V)
1/2/3
0/3/3
0/2/4
Weight (kg)
79.8 (11.2)
75.6 (10.5) *
81.7 (12.2)
80.3 (12.9)
78.9 (9.2)
73.1 (8.6) **
BMI (kg·m-2)
30.5 (2.2)
28.6 (2.1) *
30.6 (2.3)
29.5 (1.8)
30.0 (2.2)
27.7 (1.5) **
Body fat (kg)
32.4 (4.7)
28.3 (5.1) *
32.5 (4.4)
30.8 (4.5)
33.7 (5.4)
27.1 (3.4) **
WC (cm)
98.2 (7.4)
95.3 (8.5) *
103.4 (8.4)
101.7 (7.4)
96.8 (6.0)
91.1 (6.7) **
Glucose (mmol·l-1)
4.52 (0.13)
4.46 (.17)
4.47 (.16)
4.41 (.10)
4.55 (.13)
4.19 (.16) **
Insulin (µU·ml-1)
20.8 (5.3)
19.6 (4.7)
20.4 (5.1)
16.5 (4.4) *
22.3 (5.1)
13.4 (4.8) **
HOMA-IR
4.18 (1.8)
3.89 (1.3)
4.05 (1.4)
3.23 (1.6) *
4.51 (1.2)
2.50 (1.7) **
Adiponectin (µg·ml-1)
2.13 (.7)
2.62 (1.1) *
1.97 (0.5)
2.73 (0.9) *
2.21 (1.1)
3.35 (1.0) **
TG (mmol·l-1)
1.33 (.11)
1.27 (.13)
1.36 (.17)
1.15 (.12) *
1.41 (.19)
1.13 (.15) **
TC (mmol·l-1)
4.42 (.36)
3.99 (.57) *
4.28 (.32)
4.12 (.44)
4.48 (.49)
3.82 (.56) **
HDL-C (mmol·l-1)
1.12 (.10)
1.10 (.13)
1.08 (.08)
1.16 (.11) *
1.04 (.09)
1.19 (.16) **
LDL-C (mmol·l-1)
2.69 (.21)
2.31 (.23) *
2.58 (.15)
2.43 (.26)
2.79 (.22)
2.11 (.23) **
TC/HDL-C
3.95 (.62)
3.63 (.41) *
3.96 (.23)
3.55 (.36) *
4.31 (.42)
3.21 (.19) **
PS: Pubertal status, BMI: body mass index, WC: waist circumference, HOMA-IR: homeostasis model assessment index for insulin
resistance, TG: triglycerides, TC: total cholesterol, HDL-C: high-density lipoprotein cholesterol, LDL-C: low-density lipoproteincholesterol. * p < 0.05 and ** p < 0.01 before versus after program.

calculated by using the following equations (McGilvery
and Goldstein, 1983): % CHO = ((R – 0.71) / 0.29) × 100.
% Fat = ((1 – R) / 0.29) × 100, in which R is the
respiratory quotient VCO2/VO2. These equations are
based on the assumption that protein breakdown
contributes little to energy metabolism during exercise
(MacArdle et al., 1986).
We determined two parameters representative of
the balance between fat and CHO utilization (PerezMartin et al., 2001): i) crossover point of substrate
oxidation expressed as a percentage of the Wmax. This
point corresponds to the power at which energy from
CHO derived fuels predominates over energy from lipids.
This power intensity is thus employed here as a
standardized index of substrate balance during exercise.
ii) maximal fat oxidation point (LIPOXmax), also
expressed as a percentage of the theoretical maximal
working capacity, and corresponding to the exercise
intensity at which the highest rate of fat oxidation was
observed. This power was used to set the intensity of the
training program.
Dietary program
A balanced and personalized dietary restriction program
was established by a dietician after an initial dietary
assessment in order to define the total amount of calories
consumed per day. In this objective, subjects of the D and
D+E groups recorded the times and amounts of food and
fluid intake for a week before the beginning of the
program.
The dietary program was set at – 500 kcal/day
below the initial dietary records. It was composed of 15%
proteins, 55% carbohydrates and 30% lipids. Adolescents
recorded, in a specifically designed notebook, the quantity
of food and the time at which it was eaten (4 times a
week). The foods were selected according to the subjects’
dietary habits. PowerPoint presentations, videos, games
and role-play scripts were designed for trainers to use
during the educational program.
Each individual’s diet was designed using a Bilnut

4 software package (SCDA Nutrisoft, Cerelles, France), a
computerized database that calculates the food intake and
composition from The National Institute of Statistics of
Tunis 1978. The body mass was measured every week to
assess the immediate effect of the nutritional
modifications.
Exercise training program
The exercise training program was performed in a
gymnasium and supervised by a teacher of physical
education. Subjects of the E and D+E groups trained for
two-months, completing four sessions of 90 min per
week. The intensity of the exercise was fixed at a heart
rate that corresponded to the LIPOXmax point assessed at
the first visit, and it was controlled by monitoring the
heart rate with a Sport-tester device (Vantage NV, Polar
Electro, Kempele, Finland).
In order to enhance the adolescents’ motivation,
the prescribed exercises were varied and included
warming-up, running, jumping and playing with a ball.
However, the intensity at LIPOXmax was maintained
within a narrow range despite these diverse physical
activities.
Statistical analyses
All analyses were performed with SPSS for Windows.
Results are expressed as mean ± standard deviation (SD).
Paired Student’s t-test was used for comparison within the
three groups (D, E and D+E). Repeated-measure ANOVA
was used to compare the responses of different groups, at
different times of the test, before and after the program.
The Tukey post-hoc test was used to compare means. In
order to evaluate the relationship among various
parameters, a Spearman correlation analysis was carried
out. Intraclass correlation coefficients (ICC) were
calculated to evaluate the reliability of all body
composition measurements and the statistics for minimum
difference (MD) needed to be considered real as
calculated by Weir et al. (2005). A value of p < 0.05 was
considered to be statistically significant.

Adiponectin / lipoprotein in obese girls

440

∆ Change (%)
Body Fat

WC

0


-5

∗∗

-10
-15



D

-20

E
∗∗

-25

D+E

Figure 1. Percentage change in body fat mass and waist circumference (WC) from pre to post-program.
* p < 0.05 and ** p < 0.01 between pre- and post-program. D : diet, E : exercise, D+E : diet+exercise.

Table 1 summarizes the anthropometric characteristics and the metabolic parameters of the three groups at
the beginning and at the end of the program. There were
no significant differences among groups for age, body
mass, body fat mass, BMI and pubertal stage before the
study. Main baseline BMI of 30.4 ± 2.2 kg·m-2 indicates
that, on average, these girls were obese at the beginning
of the program.
After the two-month program, body mass, BMI,
waist circumference and body fat mass show a significant
reduction in the D group (-4.2 ± 1.1 kg, -1.9 ± 0.3 kg·m-2,

Results
The reliability for body composition data was as follows:
body mass (ICC = 0.98), height (ICC = 0.99), BMI (ICC
= 0.98), body fat mass (ICC = 0.98), waist circumference
(ICC=0.98) and skinfold thickness (ICC = 0.97).
In addition, the statistics of minimum difference
(MD) for all body composition measurements were 0.33
kg, 0.31 kg·m-2, 0.01m, 0.18 kg, 0.26 cm and 1.1 mm
respectively for body mass, BMI, height, body fat mass,
waist circumference and skinfold thickness.

A
25

∆ Crossover point

∗∗

(% Wmax)


20
15
10
5
0

E

D

D+E

B
120

∆ LIPOXmax

100

(mg·min )
-1

∗∗


80
60
40
20
0

D

E

D+E

Figure 2. Delta comparison (difference pre- and post- program) in obese girls: (A) The crossover point (%
Wmax). (B) Fat oxidation at LIPOXmax (mg·min-1). * p < 0.05 and ** p < 0.01; difference between pre- and
post- program.

Ounis et al.

441

D

60
45
30
15

E

D+E

∆ Change (%)



∗∗

LDL-C

TC/HDL-C

HOMA-IR

0
-15
-30

HDL-C







∗∗

∗∗

-45



-60

∗∗

Figure 3. Percentage changes of plasma HDL-C, LDL-C, TC/HDL-C ratio and HOMA-IR in the three groups
after the program. * p < 0.05 and ** p < 0.01; difference between pre- and post- program.

-2.9 ± 0.6 cm and -4.1 ± 1.4 kg; p < 0.05, respectively)
and the D+E group (-5.8 ± 1.3 kg, -2.3 ± 0.4 kg·m-2, -5.7
± 1.6 cm and -6.6 ± 2.2 kg; p < 0.01, respectively). No
significant change was observed for the E group. The
percentage change of body fat mass and waist circumference are presented in Figure 1.
Substrate utilization was modified by the exercise
training, as well as the diet/exercise programs (Figure 2).
The crossover of substrate utilization increased significantly in the E and D+E groups after the two-month program (15.2 ± 4.6%; p < 0.05 and 18.5 ± 3.4%; p < 0.01 of
Wmax, respectively) (Figure 2 A).
The fat oxidation rate obtained at the LIPOXmax
point increased significantly in the E, and D+E groups
after the program (77.4 ± 10.4 mg·min-1; p < 0.05 and
89.7 ± 19.7 mg·min-1; P < 0.01, respectively). In the diet
group there was no significant change in the crossover
and LIPOXmax points (Figure 2).
Plasma glucose and insulin concentrations and
lipid profile did not differ between the three groups before
the program. After the program, the fasting insulin level
decreased significantly in the E (-3.9 ± .8 µU·ml-1; p <
0.05) and D+E (-8.9 ± 3.2 µU·ml-1; p < 0.01) groups (Table 1). Plasma insulin and glucose concentrations did not
change after the two-month diet program (Table 1).
The usual index of insulin resistance changed significantly after exercise alone and exercise combined with
diet. HOMA-IR decreased significantly in the E and D+E
groups (-20.2 ± 6.7%; p < 0.05, and -44.6 ± 12.4%; p <
0.01, respectively). No change was found in the D group
(Figure 3).
The lipid profile improved significantly after the
two-month diet combined with exercise program.
Diet/exercise increased HDL-C by 14.4%, and decreased
LDL-C and TC/HDL-C by 24.4% and 25.5% respectively
(Figure 3).
Adiponectin levels increased significantly in the D
(p < 0.05), E (p < 0.05) and D+E groups (p < 0.01) (Figure 4).
In the subjects of the D+E group, adiponectin levels exhibited a significant negative correlation with body
mass (r = -0.41; p < 0.01) and HOMA-IR (r = -0.59; p <

0.01). In addition, the TC/HDL-C ratio was positively
correlated to HOMA-IR (r = 0.46; p < 0.01), body mass (r
= 0.35; p < 0.01) and negatively correlated to LIPOXmax
(r = -0.52; p < 0.01).

Adiponectin
(µg·ml-1)
5

before




4

after
∗∗

3
2
1
0

D

E

D+E

Figure 4. Adiponectin levels (before and after programs) in
obese girls. p < 0.05 and ** p < 0.01 compared with the concentrations before the program.

In the E group, adiponectin levels were negatively
correlated to HOMA-IR (r = -0.33; p < 0.05) and the
TC/HDL-C ratio was positively correlated to HOMA-IR
(r = 0.28; p < 0.05) and negatively correlated to LIPOXmax (r = -0.30; p < 0.05).
In the D group, significant correlations were observed between adiponectin levels and body mass (r = 0.31; p < 0.05) and between the TC/HDL-C ratio and
body mass (r = 0.26; p < 0.05).

Discussion
This study shows that the two-month program of diet
restriction combined with exercise training at a working
intensity corresponding to the LIPOXmax leads to greater
improvements in obese girls than diet or exercise alone.
Combined diet and exercise induce a substantial
body fat mass loss (19.6% of initial body fat mass), a
decrease in waist circumference and an increased ability

442

to oxidize lipids during exercise (LIPOXmax increased
from 0.13 to 0.22 g·min-1). The levels of plasma adiponectin and HDL-C were higher and those of LDL-C,
and the TC/HDL-C ratio were lower at the end of the twomonth diet/exercise program.
In this study, we were interested in providing relative reliability estimates of body composition measurements (Weir et al., 2005), and we found excellent testretest reliability for all the tests examined. Skinfold thickness and circumference measurements showed excellent
test-retest reliability, with the ICC estimates exceeding
0.95. Our study has produced excellent reliability of each
participant during anthropometry testing. Moreover, all
body composition measurements reached the minimum
difference needed to be considered real.
Our investigations are based on the technique of
indirect calorimetry, which appears to be valid for measurements of substrate oxidation during sub-maximal
steady-state exercise bouts. Such measurements have
shown that obese people oxidize fewer lipids during exercise than lean matched controls (Perez-Martin et al.,
2001) and that low intensity exercise training markedly
reverses this defect in both adult and adolescent obese
subjects (Brandou et al., 2003; Dumortier et al., 2003).
In the obese population, low-intensity exercise
training may be preferable to high-intensity because of the
lower risk of musculoskeletal injuries and better adherence to the training schedule (Bouchard et al., 1993). In
addition, obesity is characterised by an impaired ability
for fat mobilisation and utilisation, so training at LIPOXmax is able to counteract this metabolic dysfunction and
prevent the decline in fat oxidation induced by body mass
loss in the post-diet period. This effect may be mediated
by maintenance of sympathetic nervous system sensitivity, which tends to be reduced after body mass loss alone
(Van Aggel-Leijssen et al., 2001).
Obesity is considered as a major independent risk
factor for cardiovascular disease (Scaglione et al., 2004).
The National Cholesterol Education Program (NCEP) has
demonstrated that diet alone reduces serum TC and LDLC in normal people. However, a drop in the HDL-C levels
is also often reported (Hellenius et al., 1997; Yancy et al.,
2004). The results of the present study demonstrate that
the diet restriction alone induced an improvement in
LDL-C but without any effect on HDL-C. Reduced HDLC concentrations are an established risk factor for coronary heart disease, and it has been estimated that a 1
mg.dl-1 increase in HDL-C reduces heart disease risk by
4% (Gordon et al., 1986).
HDL-C levels are higher in well-trained endurance athletes (Thompson et al., 1991) and increase in
sedentary subjects after exercise training (Thompson et
al., 1997).
The present study shows that changes in HDL-C
(14.4%) and LDL-C (-24.4%) in the diet/exercise group
are considerably greater than those of the diet or exercise
group alone suggesting a decrease in heart disease risk in
the subjects of the D+E group. Accordingly, Wood et al.
(1991) have shown that a one year combined program
was more effective in improving the lipoprotein profile
than exercise or diet alone and was associated with a rise
in HDL-C and a drop in LDL-C.

Adiponectin / lipoprotein in obese girls

In addition, it has been evidenced that the ratio of
TC/HDL-C is a better predictor of cardiovascular disease
(CVD) risk reduction than HDL-C, LDL-C, or the TC
value alone (Natarajan et al., 2003). Our results show that
exercise does not influence TC or LDL-C. However,
exercise favourably influences HDL-C (7.4% and 14.4%
in the E and D+E groups, respectively) and the TC/HDLC ratio (-10.6% and -25.5% in the E and D+E groups,
respectively). These results agree with the findings of
Varady et al. (2007) who showed that eight weeks of
endurance exercise three times a week increased HDL-C
by approximately 10%. It appears that exercise only,
although not affecting changes in TC and LDL-C, has a
beneficial effect on the TC/HDL-C ratio. Moreover, the
current study demonstrates that combined diet with training improves the lipid profile (TC, LDL-C, HDL-C and
TC/HDL-C) in obese girls.
In the present study, we noted a small decline in
fasting glucose (7.9%) accompanied by a much larger
decrease in insulin (39.9%) after the diet/exercise program. Kang et al. (2002) reported an improvement in
fasting insulin in overweight children after a combined
exercise/diet program. In the same way, three days/week
of aerobic exercise improved HOMA-IR in overweight
subjects (Balagopal et al., 2005).
In this study, HOMA-IR increased by 20.2% and
44.6% respectively in girls undertaking exercise and
diet/exercise programs. The decreased risk of cardiovascular disease is associated with an increase in fat oxidation in the subjects of the E and D+E groups. Indeed, the
TC/HDL-C ratio is significantly negatively correlated to
LIPOXmax after a two-month program of exercise only (r
= -0.30) or combined with diet (r = -0.52).
This study confirms that physical activity associated with reduced food intake improves insulin sensitivity
more than exercise alone or controlled diet alone. An
immediate effect of exercise is an increase in muscle
glucose transporters, which secondarily improves insulinmediated glucose disposal. Presumably, increased oxidation of fatty acids reduces lipid overload, which also increases insulin sensitivity (Goodyear and Kahn, 1998).
The marked improvement observed in serum TG is
primarily due to the combination of the diet restriction
and the exercise training at LIPOXmax. Because the consumption of processed carbohydrates is generally higher
in obese children (St-Onge et al., 2003), the transition to a
diet largely devoid of refined carbohydrates, along with a
daily exercise regimen (Oscai et al., 1972) facilitated
reduction of TG. In addition, the decrease in serum insulin may also play a role in reducing TG.
Obesity is the final consequence of a chronic positive energy balance, regulated by a complex network
between endocrine tissue and the central nervous system
(Cummings and Schwartz, 2003). Fat tissue is increasingly viewed as an active endocrine organ with a high
metabolic activity. Adipocytes produce and secrete several proteins that act as real hormones, responsible for the
regulation of energy intake and expenditure (Mora and
Pessin, 2002).
Adiponectin may act as anti-atherosclerotic factor
not only through direct effects on vascular endothelial
cells, but also through improving insulin resistance and

Ounis et al.

lipid metabolism (Yamamoto et al., 2002). It has been
reported that adiponectin levels lower in young and adolescent subjects who are obese (Zou et al., 2005). Seven
months of moderate intensity exercise training increased
adiponectin levels by 42.8% in obese young women
(Kondo et al., 2006), and in the same way, a significant
body mass loss was associated with a significant increase
in adiponectin levels in 16 obese children after a one-year
Obeldicks intervention program (Reinehr et al., 2004).
Our present study demonstrated that circulatory adiponectin levels are significantly increased in the obese
girls after the two-month intervention program; this increase is more pronounced in the D+E (51.6%) than the E
(38.5%) or D (23%) groups.
Matsubara et al. (2002) have reported significant
correlations between adiponectin levels and insulin resistance. Accordingly, a significant correlation was observed
in our subjects between adiponectin levels and HOMA-IR
after the two-month exercise alone or exercise combined
with diet control, suggesting that adiponectin could be
considered as an important determinant of insulin resistance.
Adiponectin is the first known adipocytokine that
is down-regulated in obesity. The mechanism of this
negative regulation remains unclear, because adiponectin
is secreted exclusively by fat cells (Beltowski, 2003).
Adiponectin secretion decreased when visceral adipose
tissue was isolated and cultured in vitro (Beltowski,
2003). This effect was reduced by decreasing the amount
of tissue cultured per dish. In addition, the effect was
prevented by inhibitors of transcription and translation.
Probably, the increasing mass of white adipose tissue in
obesity reduces adiponectin protein synthesis by a feedback inhibition (Diez and Igleasis, 2003).
Furthermore, adiponectin secretion in vitro is
lower in visceral as opposed to peripheral adipocytes in
children (Sabin et al., 2003), pointing to an influence of
body fat distribution. Because adiponectin is stimulated
by insulin and inhibited by TNF-α, insulin resistance and
enhanced TNF-α expression may contribute to hypoadiponectinemia (Beltowski, 2003). Glucocorticoids are also
reported to inhibit adiponectin gene expression and secretion (Diez and Igleasis, 2003), suggesting that decreased
adiponectin production could play a role in glucocorticoid-induced insulin resistance.

Conclusion
The results from the present study complement the previous findings by showing that the addition of a diet restriction to endurance exercise training significantly improves
body composition, HDL-C, TC/HDL-C ratio, and insulin
resistance. Diet combined with an exercise program is
typically recommended for decreasing body mass, insulin
resistance and LDL-C and increasing fat oxidation, HDLC and adiponectin levels in obese girls.
Acknowledgements
The current study was supported by the Minister of Higher Education,
Scientific Research and Technology of Tunisia. We also thank the
Physical Education teachers Emna Makni and Imen Ben Chiekh.

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Key points
• Diet combined with exercise training improved body
composition, adiponectin levels and metabolic parameters in obese girls.
• Diet only decreases body mass and LDL-C without
improving fat oxidation and HDL- C.
• Individualized exercise training at LIPOXmax point
improved the HDL-C and the circulatory adiponectin
levels with any change of LDL-C and body composition.

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Original article

Impact of training and hypocaloric diet on fat oxidation and body
composition in obese adolescents
Effet de l’entraînement et du régime hypocalorique sur l’oxydation des
lipides et la composition corporelle chez des adolescents obèses
O. Ben Ounis a,∗,b , M. Elloumi a,b,c , M. Amri b , Y. Trabelsi a , G. Lac c , Z. Tabka a
a

Laboratoire des adaptations cardio-circulatoires, respiratoires, métaboliques et hormonales à l’exercice musculaire,
faculté de médecine Ibn El Jazzar, 4002 Sousse, Tunisia
b Département de biologie, faculté de science, université el Manar, 1002 Tunis, Tunisia
c Laboratoire de biologie des activités physiques et sportives (Baps), université Blaise-Pascal,
Clermont-Ferrand, 63172 Aubière cedex, France
Received 20 April 2008; accepted 16 October 2008

Abstract
Objective. – We undertook to evaluate the effects of training and hypocaloric diet on fat oxidation and weight loss in obese adolescents within a
two-month program.
Methods. – The longitudinal intervention of a two-month program was performed in 54 adolescents, whose body mass index was 30.3 ± 4.0 kg/m2 .
They were divided into three groups: hypocaloric diet program (D), individualized training program at the level of maximal lipid oxidation Lipoxmax
(T) and hypocaloric diet combined with training program (D + T). The body composition, the substrate “crossover” point and the Lipoxmax point
were determined before and after each protocol.
Results. – The decreases in body weight and fat mass were more significant in the D + T group (p < 0.01) than in the D (p < 0.05) or T (p = 0.07)
groups. In the D + T group, the crossover point was observed at a higher intensity at the end of the program (+ 19.7% ± 2.4 of Wmax ; p < 0.001),
and the fat oxidation at Lipoxmax has increased by 83.2 ± 15.3 mg/min (p < 0.01). A significant correlation between Lipoxmax and weight was also
observed after the program in D + T subject.
© 2008 Elsevier Masson SAS. All rights reserved.
Résumé
Objectifs. – Évaluer l’effet d’un programme d’entraînement et de régime hypocalorique de deux mois sur l’oxydation des lipides et la perte de
poids chez des adolescents obèses.
Méthodes. – L’intervention longitudinale de deux mois est effectuée chez 54 adolescents, dont l’indice de masse corporelle est de 30,3 ± 4,0 kg/m2 .
Ils ont été répartis en trois groupes : régime hypocalorique (D), programme d’entraînement individualisé au point d’oxydation maximal des lipides
(Lipoxmax ) (T) et l’association des deux (D + T). La composition corporelle, le point de croisement crossover et le point qui correspond au Lipoxmax
sont déterminés avant et après le programme.
Résultats. – La diminution du poids et de la masse grasse est plus significative chez le groupe D + T (p < 0,01) par rapport aux groupes D (p < 0,05)
et T (p = 0,07). Dans le groupe D + T, le point de crossover est observé à des intensités supérieures à la fin du programme (+ 19,7 % ± 2,4 du Wmax ;
p < 0,001) et l’oxydation des lipides au point de Lipoxmax augmente de 83,2 ± 15,3 mg/min (p < 0,01). On a également observé une corrélation
significative entre Lipoxmax et la masse corporelle après le programme chez les sujets du groupe D + T.
© 2008 Elsevier Masson SAS. Tous droits réservés.
Keywords: Obese adolescents; Indirect calorimetry; Fat oxidation; Training; Hypocaloric diet
Mots clés : Adolescents obèses ; Calorimétrie indirecte ; Oxydation des lipides ; Entraînement ; Régime hypocalorique


Corresponding author.
E-mail address: omar oda@yahoo.fr (O. Ben Ounis).

0765-1597/$ – see front matter © 2008 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.scispo.2008.10.002

Please cite this article in press as: Ben Ounis O, et al. Impact of training and hypocaloric diet on fat oxidation and body composition in obese
adolescents. Sci sports (2008), doi:10.1016/j.scispo.2008.10.002

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1. Introduction
The prevalence of childhood and adolescence obesity is rising alarmingly in both industrialized and developing countries
[23,29]. This disease involves several health factors, originating
from biological, behavioral, and environmental sources. Presumably, genetic propriety [30], progressive reduction in daily
physical activities [12] and changes in nutrition habits favoring
consumption of energy-dense foods [13] have been described
as major factors involved in the rise of obesity in children and
adolescents.
Obesity was associated to the development of excessive fat
storage in adipose tissue. This major endocrine organ produces
a variety of factors that regulate the metabolic energy and the
sensitivity of insulin [18] as well as leptin which is an adipokin
that controls food intake. Moreover, childhood and adolescence
are key periods in human lives during which the prevention of
obesity should be carried out because, the adipose tissue growth
is phasic, in that replicative bursts occur during early childhood,
at puberty and in adolescence [27].
In addition, an increase in the mass of adipose tissue is associated with insulin resistance, hyperglycemia, hypertension and
other components of the metabolic syndrome such as type 2
diabetes [31]. Skeletal muscle is largely involved in the development of obesity [25]. More precisely, muscular abnormalities
could alter the balance of substrate utilization, thus facilitating
fat accumulation in adipose tissue. In contrast, regular exercise training, generally recommended in obese people, induces
muscular metabolic changes, which can reverse these defects
[11].
Diet restriction is the most common form of treatment for the
obese subjects.
However, hypocaloric diet alone leads to a decrease in fat
mass with a parallel decrease in fat-free mass. The decrease
in muscle density can be prevented by adding exercise training to the diet [2] as suggested by Maffeis and Castellani
[21] who have recently underlined the importance of physical
activities in the control of body weight in children and adolescents.
Although several surveys have shown that exercise has
increased the oxidation of fat in healthy [14] and obese adults
[32], data in children and/or adolescents is lacking [5]. It has
been shown that the intensity of exercise is one of the major
determinants of substrate utilization. For instance, carbohydrate oxidation increases proportionally with the exercise load,
whereas the rate of fat oxidation initially increases, but then
decreases at high exercise intensity [7].
Brandou et al. [5], based on the crossover concept, [7] have
shown that teenagers who had performed regular moderate exercise for a two-month period (two weeks in a specialized institute
and six weeks at home), exhibited an increase in their ability to oxidize lipids at submaximal exercise. They suggested
that low-intensity exercise training combined with diet program
may prop up an increase in fat oxidation in obese adolescents
[6].
We hypothesize that exercise training at the level of the
Lipoxmax (power intensity at which lipid oxidation is maximum)

combined with hypocaloric diet program would improve the regulation of energy balance and lipid metabolism; it would also
shift the substrate balance towards a higher use of lipids with
weight loss. Therefore, we undertook to evaluate the impacts
of a two-month effect of three programs on substrate oxidation
and body composition in obese adolescents: namely, hypocaloric
diet (D), individualized training (T) and synergistic benefits of
the two protocols (D + T).
2. Subjects and methods
2.1. Subject recruitment
The present study was conducted with the agreement of
the Ministry of Education and the Ethics Committee of Farhat
Hached Hospital, Sousse, Tunisia. Fifty-four Tunisian obese
adolescent students (27 boys and 27 girls) participated in this
study. None of the subjects had a history of chronic disease or
endocrine disorder.
After receiving a comprehensive oral description of the protocol along with the risks and benefits of the study, parents and
children signed a written consent. The subjects were divided
in three groups of 18 subjects of equal gender (nine boys and
nine girls): hypocaloric diet program (D), individualized training program at the maximal lipid oxidation point (Lipoxmax ) (T)
and diet associated to training program (D + T).
2.2. Protocol
The objective of the investigation was to compare the
outcome of the three programs over a two-month period,
using anthropometric and metabolic parameters. All tests were
conducted at the same hour (around 8:30 am) to avoid chronobiological effects. Subjects were asked to fast for 12 hours before
performing the metabolic tests. These tests were performed in a
room with its air conditioned at 24 ◦ C and 76% humidity, during
the months of June and July.
2.3. Anthropometric measurements
Body weight, height, waist and hips measurements were
taken with a variability of 0.1 kg and 0.2 cm. The skinfolds
thickness (in mm) was measured three times with a Harpenden caliper, and the mean value was determined from two sites:
triceps and subscapular.
The body fat in percentage (BF%) was calculated using the
equation of Slaughter et al. [28] for children with triceps and
subscapular skinfolds less than 35 mm:
Boys: BF% = 1.21 (sum of 2 skinfolds) – 0.008 (sum of 2
skinfolds2 ) – 1.7
Girls: BF% = 1.33 (sum of 2 skinfolds) – 0.013 (sum of 2
skinfolds2 ) – 2.5
And for children with triceps and subscapular skinfolds
greater than 35 mm:

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Boys:BF% = 0.783 (sum of 2 skinfolds) – 1.7
Girls:BF% = 0.546 (sum of 2 skinfolds) + 9.7
Fat Free Mass = Body weight – (Body weight × (body fat
%/100))

VCO2 ) were recorded throughout the testing and over the last
3 min of each step [20].
Calculation of CHO and lipid oxidation rates was assessed
from gas exchange measurements, according to the non-protein
respiratory quotient (R) technique [24]:

The body mass index (BMI) was also calculated as
weight/height2 .
An adolescent was then considered obese when his/her BMI
was greater than the 97th percentile [9].

CHO (mg/min) = 4.585 V CO2 − 3.2255 V O2

2.4. Dietary program
A personalized hypocaloric diet program (group D and D + T)
was established by a dietitian after an initial dietary assessment in order to define the total amount of calories consumed
per day. The diet program was set at −500 kcal/day below the
initial dietary records. It was composed of 15% proteins, 55%
carbohydrates and 30% lipids. Foods were selected according
to the subject’s dietary habits. Lecture using PowerPoint® presentations, videos, games, and role-play scripts were designed
for trainers to use during the education program. Each adolescent recorded the quantity of food and the time when it was
eaten (four times a week). Each individual’s diet was designed
using a Bilnut 4 software package (SCDA Nutrisoft, Cerelles,
France), a computerized database that calculates the food intake
and composition from National Institute of Statistics in Tunis
1978.
2.5. Exercise testing
Participants underwent a testing exercise on an
electromagnetically-braked cycle ergometer (Ergoline, Bitz,
Germany) according to the protocol described by Brandou et
al. [5].
Gas exchange was monitored on a breath-by-breath basis,
using a metabolic cart (ZAN 600, Me␤geräte, Germany). The
maximum oxygen uptake rate (VO2 max) and the maximum aerobic power (Wmax ) were calculated using the anthropometric
prediction equations of Wasserman et al. [35] for obese children.
These equations take into account the gender and anthropometric
characteristics:
Girl: VO2 max = (52.8 × M) − 303.4
Boy: VO2 max = (28.5 × M) + 288.1
The following equation was used to calculate Wmax [35]:
Wmax =

(VO2 max −10(×M))
10.3

M is the body mass of the subject in kg.
The heart rate was monitored electrocardiographically during
exercise testing (ZAN ECG 800, Me␤geräte, Germany). A 3 min
rest period was followed by a five-stage progressive submaximal
exercise test (20, 30, 40, 50, and 60% of Wmax ) with 6 min of
exercise at each work rate. The test finished with a 5 min active
recovery period at 20% of Wmax . Ventilatory parameters (VO2 ,

Lipids (mg/ min) = −1.7012 V CO2 + 1.6946 V O2
Proportion of CHO and lipids used from the respiratory quotient (R = VCO2 /VO2 ) were determined, it is a function of the
balance of substrates oxidized by the body.
When the R is 0.7, 100% of energy is derived from lipid
oxidation, and when the R is 1.0, CHO represents 100% of the
oxidized fuels. The percentage of CHO and fat oxidation were
calculated by using the following equation [22]:
% CHO = ((R − 0.71)/0.29) × 100
% Lipid = ((1 − R)/0.29) × 100
We also used the R values to assess the “crossover” point
for substrate utilization and the maximal fat oxidation point
Lipoxmax . The “crossover” point is defined as the power output beyond which CHO usage becomes predominant (i.e., when
approximately 70% of energy is derived from CHO and 30%
from lipids [7]).
The Lipoxmax point is the power at which the increase in
lipid oxidation induced by the increasing workload reaches a
maximum, which will then be followed by a decrease as CHO
becomes the predominant fuel [7]. This point was previously
described in children [5]. We used this intensity to individualize
training.
2.6. Training program
The training program (group T and D + T) was performed in
a gymnasium and supervised by a physical education teacher.
Subjects trained during two months, four sessions per week,
lasting 90 min.
The intensity of the exercise was controlled by monitoring the
heart rate with a Sport-tester device (Vantage NV, Polar Electro,
Kempele, Finland). The exercise load was fixed at a heart rate
that corresponds to Lipoxmax determined during the first visit. In
order to enhance children’s motivation, the prescribed exercises
were varied and included warming-up, running, jumping and
playing with a balloon.
2.7. Statistical analysis
Data were expressed as mean ± S.D. Paired t-test was used
to compare means observed in the same group. Unpaired t-test
was used to compare between groups and gender.
ANOVA for repeated measurements was used to compare the
responses of the different groups, at different exercise intensities before and after the completion of the program. A Tukey
post-hoc analysis was done to compare the means. Correlation
between Lipoxmax and weight was determined by Pearson’s correlation. A 0.05 probability level was used for all statistical

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Table 1
Anthropometric characteristics in the 54 subjects: hypocaloric diet (D), training (T) and diet associated with training (D + T) (mean ± S.D.).
D (n = 18)
Before
Gender (girls/boys)
Age (years)
Height (cm)
Weight (kg)
BMI (kg/m2 )
FM (kg)
FFM (kg)
Waist (cm)
Hips (cm)
Energy (kcal/j)

9/9
13.3 ±
162.3 ±
80.7 ±
30.6 ±
33.7 ±
47.0 ±
97.9 ±
106.5 ±
3239 ±

0.6
4.1
13.2
3.0
6.7
6.7
9.3
7.2
247

T (n = 18)
After

Before



162.3 ±
75.7 ±
28.6 ±
28.8 ±
47.0 ±
94.8 ±
102.7 ±
2741 ±

9/9
13.1 ±
163.4 ±
81.1 ±
30.3 ±
33.8 ±
47.3 ±
101.3 ±
108.8 ±
3257 ±

5.1
11.1*
2.8*
5.1*
6.3
8.3
5.5*
32**

1.0
3.9
13.7
4.6
6.7
7.5
11.2
8.8
298

D + T (n = 18)
After

Before



163.5 ±
79.1 ±
29.4 ±
31.8 ±
47.3 ±
98.4 ±
105.9 ±
3268 ±

9/9
13.1 ±
162.8 ±
80.3 ±
30.3 ±
34.0 ±
46.4 ±
97.5 ±
108.1 ±
3328 ±

3.1
13.7
4.6
7.3
6.9
10.2
8.2
130

After
0.9
2.4
14.5
4.3
7.4
7.5
11.1
9.1
165



162.9 ±
74.1 ±
27.7 ±
27.0 ±
47.1 ±
90,6 ±
101.4 ±
2821 ±

4.3
13.3**
3.9*
7.0**
7.3
12.1*
8.6*
81**

BMI: body mass index; FM: fat mass; FFM: fat-free mass.
* p < 0.05.
** p < 0.01; difference between before and after program.

significance. Statistical analyses were performed using SPSS
software.
3. Results
3.1. Characteristics of study population
The anthropometric data of the subjects within each group,
at the beginning and at the end of the program, are shown in
Table 1.
There is no significant difference between both genders
before and after the program for anthropometric and metabolic
parameters. For this reason, the values of these parameters have
been regrouped.
During the weekly meetings with dietitian/nutritionist,
compliance with the energy-reduced diet (−500 kcal/day) was
reported to be adequate, as demonstrated by proper use of the
checklist exchange system. The daily energy intake was significantly reduced during the two-month diet program in the D and
D + T groups (p < 0.01). The reductions of total energy intake
were not different between the two groups.
Table 1 showed that the adolescents of D + T group have
noticed a more significant reduction in their body weight and
fat mass in comparison to the other groups. Anthropometric
parameters show a significant reduction in the D + T and D
group.
For D + T group, weight loss and fat mass loss were –
6.3 ± 1.9 kg (p < 0.01) and – 7.0 ± 1.9 kg (p < 0.01) respectively.
There was a non significant tendency towards increase in fat free
mass in D + T group (+ 0.7 ± 1.5 kg; p = 0.08).
For the D group, weight loss was – 4.9 ± 3.0 kg (p < 0.05),
fat mass loss was – 4.9 ± 2.5 kg (p < 0.05) and fat free mass was
unchanged.
Two months of exercise training targeted at the Lipoxmax did
not significantly alter weight, fat mass or fat free mass.
3.2. Metabolic data
Fig. 1a–c show the percentage of fat and CHO oxidation at
each workload of exercise in D, T and D + T groups between

before and after the program. In the D group, both fat and CHO
oxidation are unchanged after program (Fig. 1a). Fig. 1b and
c shows that after training, the T and D + T groups oxidizes a
lower percentage of CHO and a higher percentage of fat during
exercise.
The crossover point was shifted to a significantly higher
power output in the T and D + T groups (+ 15.6 ± 3.1%, p < 0.01
and + 19.7 ± 2.4%, p < 0.001 of Wmax , respectively), but this
increase was not significant in the D group (+ 5.7 ± 1.2% of
Wmax , p = 0.08).
Fig. 2 displays the change in fat oxidation rates at each work
load for the three groups. In the D group, there was no significant change in the metabolic process after two months of diet
program. However, the increase of fat oxidation at 20, 30, 40%
of Wmax , was more pronounced in D + T group (p < 0.01) than
T group (p < 0.05). In contrast, at 50% of Wmax , fat oxidation
increased similarly in the two groups (p < 0.05).
For the same power output, the maximal rate of lipid oxidation (Lipoxmax ) was significantly higher at the end of program
in T and D + T groups. Indeed, fat oxidation at Lipoxmax values were + 19.8 ± 8.7 mg/min; p = 0.7, + 76.5 ± 16.4 mg/min;
p < 0.05 and + 83.2 ± 15.3 mg/min; p < 0.01 in D, T and
D + T respectively (Fig. 3). When expressed in mg/(watt.min),
these values were 0.4 ± 0.05, 1.7 ± 0.07 and 1.9 ± 0.03
respectively.
Lipoxmax was significantly negatively correlated to weight
(r = 0.36; p = 0.03) in the subjects of D + T group. No significant
correlation was found between Lipoxmax and weight in D and T
groups (r = −0.17; p = 0.14 and r = 0.12; p = 0.21).
4. Discussion
The purpose of this study was to identify the effect of training
and hypocaloric diet on fat oxidation and weight loss in obese
adolescents within a two-month program.
The results showed that our subjects benefited more from
the combined program (D + T) than from the hypocaloric diet
(D) alone or the coached physical activity (T) alone, by better
managing their body mass composition and by enhancing their
fat oxidation.

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Fig. 1. Fat and CHO oxidation rate, expressed as percentage, as the function of the exercise intensity expressed as relative power output in the D (a), T (b) and D + T
(c) groups. * p < 0.05, ** p < 0.01, *** p < 0.001; significant difference in fat and CHO oxidation between before and after the program.

The results of the current study indicate that a substantial
amount of weight loss, namely a loss of 7.8% of initial body
weight, ensuing from a diet combined with exercise training,
has increased the ability to oxidize lipid during exercise at a rate
of 53.8% at the end of the program.
In addition, the major finding of the current intervention is the
increase of maximal rate of lipid oxidation (Lipoxmax ) correlated
with the decrease in body weight after the combined program of
diet and training.

Our metabolic inferences are based on the technique of indirect calorimetry, often used to assess the relative usage of fat and
carbohydrates from the early days of biochemistry; this approach
has previously been applied to both low [5] and high intensity exercises [25]. Potential sources of error in this approach
are little, at least during moderate intensity effort. The intensities of effort were set using Wasserman’s equations [35]; these
approximate values of VO2 max and Wmax could be over- or
underestimated in some subjects, and this would modify the

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Fig. 2. Change in lipid oxidation rate (mg/min), during exercise in the three
groups; D, T and D + T between before and after the program (* p < 0.05 and **
p < 0.01).

crossover points as reported in our survey. However, this methodological problem is minimized because values for the three
observation periods are compared for one given subject.
In addition, the narrow range of the ages of our adolescent
subjects (12–14 years), as well as their matched weight, height
and degree of adiposity are all factors that could contribute to
the accuracy of our estimated metabolic parameters.
Our study showed that exercise training associated with diet
restriction decreased the BMI by – 2.6 kg/m2 and increased the
oxidation of lipid during exercise, which was reflected by the
decline of RER values (from 0.93 to 0.89) and the increase of
crossover point (from 7.8 to 27.5% of Wmax ) and Lipoxmax (from
0.13 to 0.22 g/min).
Brandou et al. [5] also found an increased fat utilization
during submaximal exercises in seven obese adolescents after
a two-week protocol of controlled training in a rehabilitation
institute and a six-week follow-up at home combined to diet
restriction (−300 kcal/day). Similarly, Rodriguez and Moreno
[26] reported that a combined physical activity and a nutritional
intervention contributed to an effective prevention of childhood
and adolescence obesity, because this strategy increased fat oxidation during exercise.
In this study, relative fat oxidation has increased significantly
in our subjects after performing the low intensity exercise training with or without hypocaloric diet. The percentage of total
energy expenditure coming from fat oxidation during exercise
increased from 23.4 to 34.9% (p < 0.05) in T group, and from
22.5 to 38.2% (p < 0.05) in the D + T group.

Fig. 3. Change in fat oxidation rate at Lipoxmax (mg/min), during exercise in the
three groups between before and after the program (* p < 0.05 and ** p < 0.01).

Many studies have shown that exercise with moderate intensity allows high oxidation of lipids in lean [14] and obese
subjects [5]. In the obese population, low-intensity exercise
training may be preferable to high-intensity because of the lower
risk of muscular-skeletal injuries and better adherence [4]. In
addition, obesity is characterised by an impaired ability for fat
mobilisation and utilisation; so training at Lipoxmax is able to
counteract this metabolic dysfunction and prevent the decline in
fat oxidation induced by body weight loss in the postdiet period.
This effect might be mediated by maintenance of sympathetic nervous system sensitivity, which tends to be reduced after
weight loss alone [33]. Nevertheless, it is well established that
mitochondria are adaptable organelles directly involved in substrate oxidation, and skeletal muscle can manifest considerable
plasticity of mitochondrial activity in response to training in
insulin-resistant states, in obese individuals [8]. Interestingly,
the defect in lipid oxidation found in both obese and insulinresistant patients is also highly sensitive to training and, thus, is
rapidly corrected by endurance training targeted at the Lipoxmax
[5,11].
Zachwieja [36] showed that the oxidation of lipids during
submaximal exercise is high following the physical endurance
because lipid utilization spares glycogen stores. Indeed, RER
data indicate that the adolescents were able to oxidize more
lipids after the training program (from 0.93 to 0.90), with the
increase of Lipoxmax of 76.5 mg/min. This improvement in the
ability of oxidizing high level lipids may be beneficial for the
management of obesity, as already postulated by several authors
[21].
In contrast with the endurance training, the diet restriction
alone did not significantly modify either the percentage of fat
oxidation (26.2 versus 27.3%, p = 0.3) or the percentage of
CHO oxidation (73.8% versus 72.7%; p = 0.2). Indeed, it is
recognized that caloric restriction decreases adipocyte lipolytic responsiveness due to reduced expression and activation
of hormone sensitive lipase (HSL), the rate-limiting enzyme
for lypolysis [19]. However, exercise increases adipose tissue
lipolytic responsiveness by enhancing the expression and activation of HSL [10], thereby preventing the decline of fat oxidation
induced by diet restriction [33].
Previous reports have indicated that the intramyocellular lipid
(IMCL) levels have decreased by means of remarkable weight
reduction after gastric surgery in nondiabetic obese subjects
[16]. It is clear that endurance training can induce adaptations
in substrate oxidation characterized by an increase in fat oxidation showed in the present study at 20, 30, 40 and 50% of
Wmax .
One of the key adaptations that takes place in skeletal muscle
after physical training is an increase in mitochondrial protein,
activities of the triacarbxylic acid (TCA) cycle enzymes and
oxidative phosphorylation [1].
Exercise training and regular physical activity have proved
to increase fatty acid turnover [14] and fat oxidation in obese
populations [32]. This improvement of fat oxidation during submaximal exercise observed in our study, especially in T and
D + T groups could be explained by an increase in fatty acid
turnover (FAT). Therefore, the contribution of different sources

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of FA utilized during exercise depends on whether it is originated from adipose tissue, circulating lipoproteins or muscle
triacylglycerol [17].
An overweight profile during childhood and adolescence is
significantly associated with insulin resistance, abnormal lipids
and high blood pressure [31]. However, enhanced oxidation of
fat through physical activity was associated with improvement of
insulin sensitivity in obese subjects [15]. Virkamaki et al. [34]
suggested that IMCL itself or related intracellular substances,
such as diacylglycerol or protein kinase C (PKC), are important regulators of insulin sensitivity in skeletal muscle. A higher
level of fasting lipid oxidation is associated with a normal IMCL
content and insulin sensitivity in obese subjects [15].
Boben and Shulman [3] also suggested that an elevated
plasma level of free fatty acid (FFA) is a key factor linking
obesity with insulin resistance.
In conclusion, the findings of this study have demonstrated
that a two-month individualized exercise training at Lipoxmax ,
combined with caloric restriction program have reduced fat mass
while maintaining fat free mass, and improved the use of the
lipids during submaximal exercise. This intervention represents
a good strategy for an effective prevention and management of
childhood and adolescence obesity.
Acknowledgements
The authors thank the professor of physical education
E. Makni and I. Ben Cheikh.
This study was supported by the Tunisian Ministry of Higher
Education, Scientific Research and Technology.
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Metabolism). Circulation 2003;107:1448–53.
[32] Van Aggel-Leijssen DP, Saris WH, Hul GB, Van Baak MA. Long-term
effects of low-intensity exercise training on fat metabolism in weightreduced obese men. Metabolism 2002;51:1003–10.

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adolescents. Sci sports (2008), doi:10.1016/j.scispo.2008.10.002

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[33] Van Aggel-Leijssen DP, Saris WH, Hul GB, Van Baak MA. Short-term
effects of weight loss with or without low-intensity exercise training on fat
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[34] Virkamaki A, Korsheninnikova E, Seppala-Lindroos A, Vehkavaara S,
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insulin signaling pathways in human skeletal muscle. Diabetes 2001;50:
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[35] Wasserman K, Hansen J, Whipp BJ. Principles of exercise testing and
interpretation. Philadelphia: Lea & Febiger; 1986.
[36] Zachwieja JJ. Exercise as treatment for obesity. Endocrinol Metab Clin
North Am 1996;25:965–88.

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adolescents. Sci sports (2008), doi:10.1016/j.scispo.2008.10.002

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Original article

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Two-month effects of individualized exercise training with or without
caloric restriction on plasma adipocytokine levels in obese
female adolescents

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Effets d’un programme de deux mois d’entraînement individualisé associé ou non à un régime
hypocalorique sur les niveaux plasmatiques des adipocytokines chez des adolescentes obèses

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a

Q1

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DP

Laboratoire des adaptations cardiocirculatoires, respiratoires, métaboliques et hormonales à l’exercice musculaire,
faculté de médecine Ibn El Jazzar, 4002 Sousse, Tunisie
b Biologie des activités physiques et sportives (BAPS), laboratoire biologie B, Les Cézeaux, 63177 Aubière cedex, France
c Laboratoire de physiologie, faculté des sciences de Tunis, Tunisie
d Laboratoire mouvement sport santé (M2S), UFR APS, université de Rennes 2, campus la Harpe, 35044 Rennes, cedex France

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O. Ben Ounis a,c,∗ , M. Elloumi a,b , G. Lac b , E. Makni a , E. Van Praagh b , H. Zouhal d ,
Z. Tabka a , M. Amri c

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Résumé

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Objectifs. – Étudier les effets d’un programme d’entraînement individualisé associé à un régime hypocalorique sur les concentrations plasmatiques
des adipocytokines chez des adolescentes obèses. Matériels et méthodes. – Vingt-sept adolescentes obèses ont été réparties (ordre randomisé) en
trois groupes avec trois interventions différentes sur deux mois : (1) régime hypocalorique (n = 9), (2) entraînement individualisé au niveau du
Lipoxmax (puissance pour laquelle le taux d’oxydation des lipides est maximal) (n = 9) et (3) programme combiné régime/entraînement (n = 9).
La masse corporelle (MC), l’indice de masse corporelle (IMC), le pourcentage de masse grasse (%MG), l’estimation de la résistance à l’insuline
par le modèle d’évaluation homéostasique (HOMA-IR) et les niveaux plasmatiques à jeun des adipocytokines ont été évalués avant et après
les deux mois d’intervention. Résultats. – Le programme régime/entraînement a induit un décalage du niveau de Lipoxmax vers une intensité
supérieure (+27,8 ± 5,1W ; p < 0,01) et une augmentation de l’oxydation des lipides à Lipoxmax (+96,8 ± 16,2 mg/min ; p < 0,01). L’augmentation
de l’oxydation des lipides a été corrélé significativement (p < 0,01) avec les améliorations induites par le programme régime/entraînement sur le
%MG (r = −0,47), le HOMA-IR (r = (0,66), la leptine (r = (0,41), le TNF-␣ (r = (0,48), l’Il-6 (r = (0,38), l’adiponectine (r = 0,43) et la résistine
(r = 0,51). Conclusion. – L’entraînement au niveau du Lipoxmax combiné avec un programme de régime hypocalorique a amélioré la capacité à
oxyder les lipides pendant l’exercice, et cette amélioration a été associée aux améliorations des niveaux plasmatiques des adipocytokines chez des
adolescentes obèses.
© 2009 Publi´e par Elsevier Masson SAS.

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Mots clés : Adolescentes obèses ; Adipocytokines ; Activité physique ; Restriction calorique

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Abstract

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Objectives. – To examine if, in young obese patients, an individualized training programme in association with a caloric restriction programme
which had an effect on whole-body lipid oxidation, was able to induce changes on plasma adipocytokine concentrations. Materials and methods. –
Twenty-seven obese female adolescents participated in the study. Whole-body lipid oxidation during exercise was assessed by indirect calorimetry
during a graded cycle ergometer test. Body mass (BM), body mass index (BMI), percentage of body fat (%BF), insulin homeostasis model
assessment (HOMA-IR) and fasting levels of circulating adipocytokines were assessed prior and after a two-month diet programme, individualized
training programme targeted at Lipoxmax corresponded to the power at which the highest rate of lipids was oxidized and combined diet/training
programme.

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Corresponding author.
E-mail address: omar oda@yahoo.fr (O. Ben Ounis).

0003-4266/$ – see front matter © 2009 Published by Elsevier Masson SAS.
doi:10.1016/j.ando.2009.03.003

Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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Results. – The diet/training programme induced both a shift to a higher-power intensity of Lipoxmax (+27.8 ± 5.1 W; p < 0.01) and an increase of
lipid oxidation at Lipoxmax (+96.8 ± 16.2 mg/min; p < 0.01). The enhancement in lipid oxidation was significantly (p < 0.01) correlated with the
diet/training-induced improvement in %BF (r = −0.47), HOMA-IR (r = (0.66), leptin (r = (0.41), TNF-␣ (r = (0.48), IL-6 (r = (0.38), adiponectin
(r = 0.43) and resistin (r = 0.51). Conclusion. – This study showed that in obese female adolescents a moderate training protocol targeted at Lipoxmax
and combined with a diet programme improved their ability to oxidize lipids during exercise, and that this improvement was associated with changes
in plasma adipocytokine concentrations.
© 2009 Published by Elsevier Masson SAS.

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Keywords: Adolescence obesity; Adipocytokines; Physical activity; Caloric restriction

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The prevalence of obesity continues to rise, and a sedentary lifestyle is recognized as a key-risk factor. Adipose tissue
is not merely a fat storage deposit, but has been recognized
as an endocrine organ able to produce biologically active proteins termed “adipocytokines”. These adipocytokines include
leptin, adiponectin, resistin, tumor necrosis factor-␣ (TNF␣) and interleukin-6 (IL-6) which may be related to the
increase of obesity-mediated adverse effects on glucose and lipid
metabolisms [1,2].
Adiponectin levels decrease with obesity [3] and low
adiponectin concentration is associated with insulin resistance
[4]. TNF-␣ is elevated in obesity and contributes to insulin
resistance, possibly through down-regulation of GLUT-4 and
inhibition of insulin receptor function and signaling [5]. IL6 secreted by fat cells induces hepatic synthesis of C-reactive
protein (CRP), and both molecules are associated with obesity
and cardiovascular disease [6]. Leptin plasma concentration is
directly related to the severity of obesity, as an increase of fat
mass is associated with an increase of leptin [7]. Kondo et al.
[8] showed that changes in circulating adipocytokine levels, due
to increased exercise, were involved in the improvement of a
negative energy balance. Moreover, caloric restriction increases
adiponectin levels and decreases insulin resistance in obese children [9]. Many of the controlled intervention studies have shown
that exercise improves adipocytokine levels, with a concomitant
improvement in BM and/or body composition [10].
Regular endurance training has been shown to favourably
modify the balance of substrate oxidation, especially in patients
with metabolic defects such as obesity [11] and type 2 diabetes [12]. Indeed, exercise training helps to restore fat oxidation
capacity [13], which can be linked to improvement in insulin sensitivity [12]. Given its advantages, indirect calorimetry remains
the most commonly used technique for assessing the balance between fat and carbohydrate (CHO) oxidation during
exercise.
During progressive exercise, it provides a simple index: the
maximum fat oxidation rate point (Lipoxmax ) [14]. This index
can be obtained from gas exchange during submaximum graded
exercise up to 60% of the theoretical maximum aerobic power
[13], and are useful for prescribing an individualized exercise
programme [15] in those with metabolic diseases such as obesity
and type 2 diabetes.
Thus, the aim of our study was to investigate in obese
female adolescents, the effects of a two-month diet programme,

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individualized training programme, carried out at the level
of the Lipoxmax (power intensity at which lipid oxidation
is maximum), and combined programme (diet/training) on
whole-body lipid oxidation and plasma cytokine concentrations. We hypothesized that an increase in lipid oxidation and
an improvement in plasma adipocytokine concentrations in
obese girls well be better after a mixed two-month diet/training
programme than after separate diet or training programmes.

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1. Introduction

2. Patients

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The Research Ethics Committee of the Faculty of Medicine,
Sousse, Tunisia approved this study. Each participant and parents signed an informed consent form before actively engaging
in the study. Twenty-seven 13-year-old obese female adolescents participated in the study. Obesity was defined as body
mass index (BMI) greater than the 97th percentile according to
the French references [16]. None of the children was involved
for more than three hours per week in structured programme
of physical activity or sports training. No patients had diabetesrelated complications, and no medications were administered.
Non-compliant participants were not included. Individuals were
excluded if they had ischemic heart disease or other medical
conditions for which the prescribed exercise might be contraindicated. Each individual came to the laboratory for a medical
examination and anthropometric measurements performed by
a paediatrician.
The adolescents were randomly assigned to one of the
three programme groups: diet group, individualized training at
Lipoxmax group and training combined with diet group.

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3. Methods

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3.1. Anthropometric measures

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Height was measured with a standing stadiometer and
recorded with a precision of 1 mm. Body mass (BM) was
measured to the nearest 0.1 kg with a digital scale (OHAUS,
Florhman Park, NJ). Body mass index (BMI) was calculated as
BM in kilograms divided by height in squared meters (kg/m2 ).
Two skinfold thicknesses (triceps and subscapular) were measured by the same trained technician (Harpenden caliper).
The percentage of body fat (%BF) was calculated using the
equations of Slaughter et al. for girls [17]: with triceps and
subscapular skinfolds less than 35 mm and more than 35 mm

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Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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%BF =1.33(sum of 2 skin folds)−0.013(sum of 2 skin folds)2
− 2.5
%BF = 0.546(sum of 2 skin folds) + 9.7
The test-retest data were then used to calculate the precision
of all body composition measurements. Pubertal stage was evaluated according to the Tanner classification [18] by a trained
paediatrician: pre pubertal children comprised children who
were in stage I, pubertal children in stage II-III, post pubertal
children in stage IV-V.
3.2. Exercise testing

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For the second visit children came to the laboratory between
08:00 and 09:00 a.m. after an overnight fast to perform a cycling
exercise. Children performed a five six-minutes stage exercise at
20, 30, 40, 50, and 60% of their maximum theoretical workload
(Wmax ) using the protocol described previously [19].
We calculated the following theoretical value before exercise testing for each adolescent using the predictive equations
of Wasserman for obese girls [20]:
Maximum oxygen consumption (VO2max ) and Wmax :

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VO2 max = (52.8 × M) − 303.4
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Wmax = (VO2 max −10(×M)) × (10.3)−1 (M : body mass in kg).

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Lipid oxidation(mg/ min) = 1.6946 VO2

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− 1.7012 VCO2 (with VO2 and VCO2 expressed in ml/ min).

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Tests were all performed on an electromagnetically braked
cycle ergometer (Ergoline, Bitz, Germany). VO2 and VCO2 were
measured breath-by-breath through a mask connected to an O2
and CO2 analyzers (ZAN 600, Me␤geräte, Germany). Ventilatory parameters were averaged every 30 s during submaximal
exercise testing. ECG was monitored for the duration of tests.
As previously described [19], we calculated a parameter
representative of the whole-body lipid oxidation during exercise, which is the maximum lipid-oxidation point (Lipoxmax ),
expressed in watts (W) which corresponds to the exercise intensity at which the highest rate of lipid oxidation is achieved
(lipid oxidation at Lipoxmax , expressed in mg/min), according
the following equation:

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3.4. Biochemical analysis

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Blood samples were obtained between 7:00 AM and 8:00 AM
after an overnight fast. Samples were collected in EDTA containing tubes and immediately centrifuged at 4 ◦ C. Plasma samples
were kept on dry ice during transportation from the testing sites
and were stored at −80 ◦ C until analyzed. Plasma glucose concentrations were measured using an automated device (AU2700,
Olympus, France). The interassay coefficient of variability (CV)
was 1.7%. Plasma insulin was assayed by an IRMA Insulin
kit (Immunotech, France). The intra- and interassay CVs were,
respectively, 3.3–4% and 3.7–4.8%. Plasma adiponectin and leptin were determined using an ELISA kit (B-Bridge international,
inc). The intra- and interassays CVs were, respectively, 4.1 and
4.7% for adiponectin and 3 and 3.2% for leptin.
Resistin was measured by an enzyme-linked immunoassay
kit obtained from Biovendor Laboratory Medicine Inc (Brno,
Czech Republic). The intra- and interassay CVs were, respectively, 4.5 and 7.8%. Plasma levels of IL-6 and TNF-α were
measured with saline using quantikine ELISA-kits from R&D
systems (cat. nos. HS600 and HSTA00C, respectively). The
intra-assay CV for TNF-␣ and IL-6 assays was less than 10%.
The interassay CV was 12.2% for TNF-␣ and 18.2% for IL6.
Insulin resistance was assessed using the homeostatic
model assessment for insulin resistance (HOMA-IR). The
HOMA-IR has been validated in children and adolescents
[21] and was computed as follows: HOMA-IR = [insulinemia
(␮U/ml) × glycemia (mmol/l)]/22.5.

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week at two local schools in the community where the participants lived. Lectures using Powerpoint® presentations, videos,
games, and role-play scripts were designed for trainers to use
during the education programme.
Subjects of training and diet/training groups received a twopage summary of information about exercise prepared by an
exercise physiologist. It included a list of the general health
benefits of regular exercise as well as various recommendations
and precautions about exercise. An exercise prescription specifying the duration, frequency, and intensity of exercise based on
the participant’s heart rate corresponding to Lipoxmax assessed
at the first visit, was also provided. The training programme
consisted of 90 minutes of supervised activity per day at a heart
rate that corresponded to Lipoxmax , less than four days per week
during eight weeks.

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respectively:

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3.3. Intervention programmes

3.5. Statistical analyses

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Based in the identified risk factors for the participants, the
intervention focused on changes in diet and physical activity to
reduce the cardiovascular disease risk by encouraging the participants (diet and diet/training groups) to decrease saturated
fat and cholesterol intake, increase consumption of a variety
of fruits and vegetables, increase the consumption of dietary
fiber and limit salt. The diet programme consisted of a 500 kcal
daily caloric reduction below the actual energy requirement. The
nutritional education programme was conducted four days per

All values are expressed as mean ± S.D. Paired Student’s
t-test was used for comparison within the three groups and
unpaired Student’s t-test was used for group’s comparisons.
Repeated-measure ANOVAs were used to compare the
responses of different groups, at different times of the test, preand postprogram. Interclass correlation coefficients (ICC) were
calculated to evaluate the reliability of all body composition
measurements [22]. Correlation between Lipoxmax and other
parameters was determined by Pearson’s correlation. All

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Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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Table 1
Subject characteristics pre- and postintervention programme in the diet group (n = 9), the training group (n = 9) and the diet/training group (n = 9).
Les caractéristiques des sujets avant et après le programme chez le groupe diet (n = 9), le groupe exercice (n = 9) et le groupe diet/exercice (n = 9).
Training

Age (years)
PS (I/II-III/IV-V)
BM (kg)
BMI (kg/m2 )
BF%
Energy intake (kcal/day)
Glucose (mmol/l)
Insulin (␮U/ml)
HOMA-IR
Resistin (ng/ml)
Adiponectin (␮g/ml)
Leptin (ng/ml)
TNF-␣ (pg/ml)
IL-6 (pg/ml)

13.2 ±
2/3/4
80.2 ±
30.5 ±
38.2 ±
3144 ±
4.42 ±
21.3 ±
4.18 ±
7.4 ±
4.2 ±
19.8 ±
7.4 ±
4.7 ±

0.3
10.1
2.2
4.9
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0.11
4.2
1.3
1.3
0.4
5.2
2.4
1.1

Post

Pre


2/3/4
75.3 ±
28.5 ±
35.4 ±
2629 ±
4.37 ±
20.6 ±
4.00 ±
8.9 ±
4.7 ±
16.2 ±
5.6 ±
4.4 ±

13.1 ±
1/3/5
80.5 ±
30.4 ±
39.3 ±
3208 ±
4.51 ±
21.6 ±
4.33 ±
6.2 ±
4.4 ±
20.1 ±
7.1 ±
5.5 ±

9.8*
1.3*
5.3*
92**
0.14
4.6
1.6
1.4*
0.6
5.3*
2.9*
1.3

0.9
11.4
1.8
4.2
228
0.14
5.3
1.7
2.4
0.5
6.1
3.7
1.6

Post

Pre


1/3/5
79.3 ±
29.8 ±
37.9 ±
3226 ±
4.44 ±
17.8 ±
3.51 ±
7.8 ±
5.2 ±
16.2 ±
5.3 ±
4.7 ±

13.1 ±
2/3/4
82.3 ±
31.2 ±
39.1 ±
3242 ±
4.62 ±
22.7 ±
4.66 ±
7.6 ±
4.1 ±
19.5 ±
8.6 ±
5.8 ±

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Pre

Diet/training

10.8
1.7
6.1
119
0.16
3.1*
1.4
1.1*
0.6*
5.3*
3.1*
1.2*

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Post
0.8
8.7
2.1
5.0
123
0.12
4.2
1.5
2.4
0.3
6.4
2.1
2.1


2/3/4
72.8 ±
27.6 ±
33.2 ±
2734 ±
4.26 ±
14.3 ±
2.71 ±
9.9 ±
5.8 ±
13.9 ±
5.2 ±
4.3 ±

9.4**
1.2**
4.3**
97**
0.15**
3.4**
0.9**
1.2*
0.5**
3.3**
1.4**
1.2**

Numbers are mean ± S.D. *: p < 0.05 and **: p < 0.01 post- versus preprogram in the three groups.
BF%: percentage of body fat; BM: body mass; BMI: body mass index; HOMA-IR: homeostasis model assessment index for insulin resistance; HR: heart rate;
Lipoxmax : the power at which the highest rate of lipids is oxidized; IL-6: interleukin-6; PS: puberty stage; TNF-␣: tumor necrosis factor-alpha.

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statistical analyses were performed using SPSS version 8.0.
P < 0.05 was considered statistically significant.
4. Results

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Anthropometric, physical fitness, and related biochemical
characteristics before and after the intervention programmes are
shown in Table 1.
For all body composition measurements, the reliability was
excellent; ICC > 95%. Comparisons of the three groups before
the intervention showed that they were matched for anthropometric parameters, age, and pubertal stage.
Before the programme, plasma adiponectin and leptin levels
were similar in all subjects. However, the plasma resistin, IL-6
and TNF-␣ level were significantly different between the three
groups in the preprogramme. Indeed, IL-6 and TNF-␣ level were
higher in the diet/training subjects than in the diet or training
subjects.
After the eight-week intervention programme, BMI
decreased by 6.1, 1.5, 11.5%, and %BF by 7.3, 3.6, 15.1% in
diet, training and diet/training groups respectively (Table 1).
At the end of the programme, diet/training group had a significant decrease in leptin, TNF-␣ and IL-6, and a significant
increase in adiponectin and resistin at the end of the programme.
These changes were more pronounced in the diet/training
group compared to the others groups (Fig. 1).
Exercise training had, however, marked effects on wholebody lipid oxidation. After subsequent training, the Lipoxmax
was raised to a higher power (+19.3 ± 3.4 W; p < 0.05
and + 27.8 ± 5.1 W; p < 0.01) in the training and diet/training
groups, respectively (Fig. 2A).
Fig. 2B shows that the post-training lipid oxidation at
Lipoxmax was significantly increased compared with pretraining
values (+61.7 ± 9.6 mg/min; p < 0.05 and + 96.8 ± 16.2 mg/min;
p < 0.01) in the training and diet/training groups, respectively.

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There was no significant change for this parameter in the diet
group (Lipoxmax : +6.1 ± 2.4 W; p = 0.7 and lipid oxidation at
Lipoxmax : +23.2. ± 6.6 mg/min; p = 0.4).
The postprogram usual index of insulin resistance (HOMAIR) was significantly improved in training (p < 0.05) and
diet/training (p < 0.01) groups. Diet group did not present a
significant reduction in HOMA-IR (Fig. 3).
In the diet/training group, Lipoxmax exhibited a significant (p < 0.01) negative correlation with BMI (r = (0.31),
BF% (r = (0.47), leptin (r = (0.49), TNF-␣ (r = (0.48), IL-6
(r = (0.38), HOMA-IR (r = (0.66) and a significant (p < 0.01)
positive correlation with adiponectin (r = 0.43), resistin
(r = 0.51).
In the training group, Lipoxmax exhibited a significant
(p < 0.05) negative correlation with leptin (r = (0.36), TNF-␣
(r = (0.41), IL-6 (r = (0.30), HOMA-IR (r = (0.44) and a significant (p < 0.05) positive correlation with adiponectin (r = 0.31),
resistin (r = 0.39). No significant correlations between Lipoxmax
and other parameters were observed in the diet group (Table 2).

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Fig. 1. Percentage changes of plasma adipocytokine levels in the three groups
after the two-month programme. * p < 0.05 and ** p < 0.01; difference between
after and before the programme.
Changements en pourcentage des niveaux plasmatiques des adipocytokines
après le programme chez les filles obèses. * p < 0,05 et ** p < 0,01.

Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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The present study showed that, in obese female adolescents, moderate training over two-month targeted at the level
of Lipoxmax increases their ability to oxidize lipids during exercise, and that this increase is correlated with an improvement
in both insulin sensitivity and plasma adipocytokine concentrations. Moreover, the group who performed the diet/training
programme for two-month exhibited a significant correlation
between lipid oxidation and body composition changes.
The first and most obvious effect of these interventions on
food intake and exercise is the body weight loss and the improvement of the body image. This was evident in the diet group with a
significant weight loss, but not in the training group for whom the
weight-loss was rather slight. The combination of the two treatments, diet-training group, resulted in the best reduction of body
weight, in account probably with a greater negative energetic
balance. When examining more deeply the body composition, it
appeared that the reduction in body fat mass was quite two-folds
higher in the diet/training group than in the diet group, which is
the expected effect of a slimming intervention.
Less visible are the changes in the glucose metabolism; in
these adolescents, glucose levels were still in the normal range
and did not change after the intervention. However, there was
a tendency to insulin resistance (high insulin and HOMA-IR)
which was reduced after the two-month of training with or
without diet. Oppositely to the weight loss, the major effect
was attributable to the exercise program, and one more time,
the combination of the diet plus training was the more effective.
Skeletal muscle is largely involved in the development of
obesity [15]. Moreover, muscular abnormalities alter the balance of substrate utilization, thus facilitating fat accumulation
in adipose tissue. In contrast, regular exercise training, generally recommended for obese people, induces muscular metabolic
changes, which can reverse these defects [19].
Obesity is characterised by an impaired ability for fat mobilisation and utilisation, so training at Lipoxmax is able to
counteract this metabolic dysfunction and prevent the decline
in fat oxidation induced by BM loss in the postdiet period. This
effect may be mediated by maintenance of sympathetic nervous
system sensitivity, which tends to be reduced after BM loss alone
[23]. Recently, exercise calorimetry has been developed by several teams in order to target more closely training protocols for
both adults [15] and adolescents [24] suffering from obesity.
Consequently, it becomes important to know how diet combined
with exercise modifies the balance of substrates as assessed with
this technique in obese adolescent boys [19].
Leptin is thought to provide information about nutritional status and fat mass to neural centres regulating feeding behaviour,
appetite and energy expenditure [7]. The most important variable that determines circulating leptin concentrations is body fat
mass [25]. The obese adolescents of the present study showed
significantly higher levels of leptin. However, leptin was significantly lower after the two-month programme in all subjects,
but this decrease was more significant in diet/training group
and was associated with a decrease in body fat and an increase

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5. Discussion

EC

TE

DP

Fig. 2. Maximal lipid oxidation (Lipoxmax ) during exercise: A: Lipoxmax
expressed in watts. B: Rate of fat oxidation at Lipoxmax , expressed in mg/min.
* p < 0.05 and ** p < 0.01 between before and after the programme.
Changement du point d’oxydation maximale des lipides (Lipoxmax ) entre avant
et après le programme : * p < 0,05 et ** p < 0,01. A : Lipoxmax exprimé en watts.
B : Taux de l’oxydation des lipides au niveau du Lipoxmax , exprimé en mg/min.

RR

Fig. 3. Percentage changes of HOMA-IR in the three groups after the programme. * p < 0.05 and ** p < 0.01; difference between after and before the
programme.
Changement en pourcentage de l’index usuel de la résistance à l’insuline ;
HOMA-IR après le programme. * p < 0,05 et ** p < 0,01.

CO

Table 2
Correlation between Lipoxmax and others parameters over the 2-month programme.
Coefficients de corrélation entre Lipoxmax et les autres paramètres après le
programme de deux mois.
Diet

Training

Diet/training

BMI (kg/m2 )
BF%
Leptin (ng/mL)
TNF-␣ (pg/mL)
HOMA-IR
Adiponectin (ng/mL)
Resistin (ng/mL)
IL-6 (pg/mL)

0.17
−0.15
0.14
0.14
0.11
0.19
0.13
0.16

−0.12
0.16
−0.36*
−0.41*
−0.44*
0.31*
0.39*
−0.30*

−0.31**
−0.47**
−0.49**
−0.48**
−0.66**
0.43**
0.51**
−0.38**

UN

Lipoxmax

BF%: percentage of body fat; BMI: body mass index; GH: growth hormone;
HOMA-IR: homeostasis model assessment index for insulin resistance; IL6: interleukine-6; Lipoxmax : maximum rate of lipid oxidation; TNF-␣: tumor
necrosis factor-alpha.
* p < 0.05.
** p < 0.01.

5

Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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6. Conclusion

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Our results show that in female obese adolescents an
increase in fat oxidation during exercise resulted obviously in an
improvement in body composition, but essentially in circulating
adipocytokine levels and the insulin resistance state by the combination of diet and individualized exercise training targeted at
Lipoxmax .

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Acknowledgements

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This study was supported by the Ministry of Higher Education, Scientific Research and Technology of Tunisia.

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TNF-␣ produced by white adipose tissue is markedly upregulated in obesity and contributes to insulin resistance by
interfering with insulin receptor signaling [36]. This adipocytokine inhibits adiponectin production in adipose tissue. Rubin
et al. [37] suggested that increased levels of adiposity, resulting
in decreased adiponectin and in increased TNF-␣ concentration, may link being overweight with insulin resistance during
adolescence. Our results show that the diet/training programme
decreases significantly the plasma levels of TNF-␣ in obese
girls and this increase is associated with the improvement in
the insulin sensitivity.
In the present study we showed that the diet program did
not improve IL-6 concentrations. However, the improved body
composition induced by diet combined with training is associated with decreased serum concentrations of the IL-6 in obese
girls.
This finding was also reported in obese adolescents after
a three-week weight reduction programme including physical activities [38]. Although being significantly higher in
diet/training than in diet and training before the intervention,
TNF-␣ and IL-6 were decreased to the same level after the
intervention, showing the preponderant effect of training in this
improvement.
Resistin is a recently discovered adipocyte-released hormone
that has been positively correlated with several features of body
composition and insulin resistance [39]. Nevertheless, the physiological role of resistin on obesity and insulin resistance is
unclear, with some studies reporting a significant association
between resistin levels, obesity, and insulin resistance [40],
whereas other studies were not able to show any significant
associations [41].
In addition, plasma levels of this protein have been scarcely
reported, and there is little information about its possible
variations after weight loss. In the present study, changes of
resistin level observed in the training and diet/training groups
were significantly correlated with Lipoxmax and Lipoxmax
was significantly correlated with changes in insulin sensitivity presented in this study by HOMA-IR. Therefore,
our data support the hypothesis that resistin antagonizes
insulin action, suggesting that the decrease of this hormone
is associated with the improvement of insulin sensitivity.

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in Lipoxmax . The administration of leptin reduces hepatic fat
mass and improves insulin sensitivity in humans suffering from
this condition [26]. Suppression of the fatty-acid-synthesizing
enzyme stearyl-CoA desaturase-1 can correct the hypometabolic
phenotype of leptin deficiency, implying that leptin not only
works via central anorectic effects but also by increasing hepatic
fatty acid oxidation [27].
Our results showed that the decrease in plasma leptin levels
was associated in the decrease in HOMA-IR values in the training and diet/training groups after the two-month programme,
suggesting the improvement of insulin sensitivity in the subjects
of they groups. A negative correlation between obesity and circulating adiponectin has been well established, and adiponectin
concentrations increase concomitantly with weight loss [28].
In the present study, adiponectin was significantly higher
for training and diet/training groups after the programme; this
increase was associated with the decrease in BMI and the surrogate of insulin resistance (HOMA-IR) in the diet/training group.
The mechanism underlying the role of adiponectin in lipid
oxidation may involve the regulation of production or activity
of proteins associated with triglyceride metabolism, including CD36, acyl CoA oxidase, 5’-activated protein kinase, and
peroxisome proliferator-activated receptor ␥ (PPAR␥) [29].
In our study we observed a significant positive correlation
between Lipoxmax and adiponectin in subjects of training and
diet/training groups.
Adiponectin decreases lipid synthesis and glucose production in the liver and causes decreases in glucose and free fatty
acid concentrations in the blood. In addition, triglyceride production is decreased and fat oxidation and energy dissipation
in the muscle are increased. Our results showed that in the
diet/training group the improvement in whole-body lipid oxidation, and particularly the lipid oxidation rate at Lipoxmax during
exercise was significantly positively correlated with the increase
in plasma adiponectin concentrations. Adiponectin intracellular
signalling is connected with activation of adenosine monophosphate kinase [30], which has been previously shown to attenuate
b-adrenergic stimulation of lipolysis in fat tissue and muscle
[31].
It has been suggested that the strength of the association
between adipocytokines and insulin resistance is higher in
overweight- compared with normal-weight children. Similarly,
decreased physical activity levels have been associated with
increased insulin resistance [32].
Levels of these adipocytokines appear to respond favourably
to sustained physical activity [33] in children. It has been speculated that increased but not decreased physical activity or aerobic
power, an indicator of cardiovascular fitness, might attenuate, if
existent, the relationship between insulin resistance and resistin,
TNF-␣, and IL-6.
Aerobic training is considered to be a key-factor in the
treatment of obesity, and numerous studies have shown an
improvement in the metabolic as well the cardiovascular status
of obese individuals after a regular aerobic training programme.
Contradictory findings exist in the literature describing reduction [34] as well as no change [35] of plasma TNF-␣ induced
by diet or physical activity.

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O. Ben Ounis et al. / Annales d’Endocrinologie xxx (2009) xxx–xxx

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Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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References

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Please cite this article in press as: Ben Ounis O, et al. Two-month effects of individualized exercise training with or without caloric restriction
on plasma adipocytokine levels in obese female adolescents. Ann Endocrinol (Paris) (2009), doi:10.1016/j.ando.2009.03.003

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