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Appetite
journal homepage: www.elsevier.com/locate/appet
Research report
a r t i c l e
i n f o
Article history:
Received 26 September 2012
Received in revised form 25 May 2013
Accepted 27 May 2013
Available online 10 June 2013
Keywords:
Aerobic training
Resistance training
Neuropeptides
Obesity
a b s t r a c t
Background: The regulation of energy balance is inuenced by physical exercise. Although some studies
show a stimulation of hormones related to food intake, others show that exercise provides satiety. Aim:
The aim of this study was to compare the effects of aerobic training (AT) and aerobic plus resistance training (AT + RT) on anorexigenic and orexigenic factors in obese adolescents undergoing interdisciplinary
weight loss therapy. Methods: A total of 26 obese adolescents, aged 1519 years with BMI P P95 were
submitted to 12 months of interdisciplinary intervention (clinical support, nutrition, psychology and
physical exercise) and divided into two groups, aerobic training (AT) (n = 13) or aerobic plus resistance
training (AT + RT) (n = 13), which were matched according to gender and body mass. Blood samples were
collected to analyze orexigenic factors (AgRP, NPY, MCH) and the anorexigenic factor alpha-MSH. Results:
The AT and AT + RT groups signicantly reduced body mass, body mass index and body fat mass (kg) during the therapy. The AT group showed no signicant changes in body lean mass (kg), whereas the AT + RT
group showed an increase in body lean mass (kg) during the interdisciplinary intervention. There was an
increase in AgRP levels (ng/ml) only in the AT + RT group after 6 months of interdisciplinary intervention
compared with baseline condition. Conversely, a-MSH levels (ng/ml) increased only in the AT group after
12 months of interdisciplinary intervention compared with baseline condition. Conclusion: Aerobic training (AT) as part of an interdisciplinary therapy is more effective than aerobic plus resistance training
(AT + RT) to improve secretion of anorexigenic/orexigenic factors in obese adolescents.
2013 Elsevier Ltd. All rights reserved.
Introduction
An interdisciplinary intervention, incorporating both psychological and physiological components, is important to promote
the reduction of body mass, blood pressure and coronary diseases
(Carnier et al., 2010; Sanches et al., 2012). Thus, physical exercise
has an important role in helping with weight loss, as well as main-
q
Acknowledgments: We would like to thank AFIP, CAPES (AUX-PE-PNPD 2566/
2011), CNPq, CEMSA, UNIFESP, FAPESP (CEPID/Sono no. 9814302-3), FAPESP (2006/
00684-3; 2008/53069-0; 2011/50356-0; 2011/50414-0) and the patients. Conicts
of interest: The authors have nothing to disclose.
Corresponding authors.
E-mail addresses: junecarnier@gmail.com (J. Carnier), ana.damaso@unifesp.br
(A.R. Dmaso).
0195-6663/$ - see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.appet.2013.05.018
169
Methods
Study population
A total of 134 adolescents were selected to participate of the
present study. They were selected from GEO (Interdisciplinary
Obesity Program) of Universidade Federal de So Paulo UNIFESP
in 2010.
Of these 134 participants, we excluded 74 (36 from the AT
group and 38 from the AT + RT group) because they did not complete the therapy for reasons such as starting a professional job,
changes in school schedule, lack of motivation and lack of money
for transportation. Additionally, participants who did not perform
all necessary examinations in the three stages of evaluation and
who did not complete 75% of all therapies were also excluded.
Forty-seven of the remaining 60 obese adolescents were initially
included in the AT + RT group and 13 were in the AT group. To evaluate the same number of volunteers in each group, the 13 patients
of the AT group were matched according to gender and body mass
with volunteers from the AT + RT group. Thus, a total of 26 obese
adolescents were evaluated in this study (13 adolescents performed the AT exercises and 13 adolescents performed the AT + RT
exercises). There were ve boys and eight girls in each group (AT
and AT + RT group) (Fig. 1).
The inclusion criteria for participating in this program for weight
loss were as follows: post-pubertal adolescents presenting with
obesity who were healthy enough to perform physical activity and
available to participate in the program for 1 year. All adolescents
were aged from 15 to 19 years, presented with obesity (BMI > 95th
percentile, according to the Center for Disease Control and Prevention) and were considered post-pubertal (Tanner Stage = 5). An
endocrinologist assessed the Tanner stage, appointing the value that
best identied the stage of sexual maturation for each adolescent
(Tanner & Whithouse, 1976). All adolescents completed the effort
electrocardiogram maximum test until exhaustion to verify whether
they could safely perform physical exercise. The non-inclusion criteria were limitations such as an identied genetic disease (e.g. Down
syndrome), metabolic or endocrine diseases, chronic alcohol consumption or previous use of drugs such as glucocorticoids and psychotropics or pregnancy (Fig. 2).
170
Clinical therapy
All obese adolescents were evaluated by the endocrinologist in
the presence of their parents once each month. The doctor monitored and evaluated all clinical exams of adolescents and treated
any health problems during therapy. The medical follow-up included the initial medical history as well as a physical examination
of blood pressure, heart rate and body weight; additionally, patients were checked for their adherence to all interdisciplinary
therapies. At all of these appointments with the doctor, the entire
GEO team was also present. The team discussed with the patients
and their parents some possible changes in lifestyle to promote
their health status.
Psychological therapy
All adolescents participated in weekly psychological orientation
group sessions (15 people per session) based on the psychodynamic approach with one trained psychologist. At these sessions,
body image, low self-esteem, family problems, and eating disorders such as bulimia, anorexia nervosa, and binge eating, including
their signals, symptoms and consequences for health were discussed, in addition to other topics. Individual psychological therapy was recommended when behavioral alterations were found
to be necessary.
171
Nutritional therapy
The adolescents participated in group and individual interventions. The themes of group interventions were weight loss diets,
the food pyramid, dietary analysis, diet and light concepts, fat
and cholesterol, eating disorders, fast foods, nutrition labeling,
how to prepare a healthy snack and nutrition tips for special events
(parties, barbecues, etc.). The lessons were taught by trained nutritionists to encourage the adolescents to follow healthy eating habits. Furthermore, all adolescents were interviewed individually
twice a month. Energy intake was set at the levels recommended
by the dietary reference intake for subjects with low levels of physical activity of the same age and gender (National Research Council
& Food & Nutrition Board, 1989).
Physiotherapy
The adolescents participated both in group and individual interventions with two physical therapists once a week. Individual consultations were also performed if the patient had any injuries. The
themes of group interventions were postural orientation, diaphragmatic breathing, hydrotherapy, RPG, isostretching, balance and
stretching.
Statistical analyses
Distributional assumptions were veried by the Kolmogorov
Smirnov test. An analysis of variance for repeated measures (ANOVA) was used to compare both groups at the same time and each
group during the therapy. For conrmation Tukeys post hoc test
was used. Data were analyzed by means of STATISTICA version
7.0 for Windows, with signicance set at p < 0.05 and expressed
as the mean S.D.
Results
It was found that the AT group signicantly (p < 0.05) reduced
body mass and BMI after 1 year of therapy. For this group, the body
fat mass (kg) was reduced signicantly (p < 0.05) after both
6 months and after 1 year of therapy. The AT group showed no signicant changes in body lean mass (kg), NPY or MCH levels during
the interdisciplinary intervention (Table 1).
Analyzing the AT + RT group, the results show that this group
signicantly (p < 0.05) reduced body mass, BMI and body fat mass
(kg) after both 6 months and after 1 year of therapy when compared with the baseline conditions. In addition, the body lean mass
(kg) increased signicantly (p < 0.05) after 1 year of therapy when
compared with baseline conditions. There was no signicant
change in NPY or MCH concentrations in either group during the
interdisciplinary intervention (Table 1).
In Fig. 3, the results show that the AT group exhibited signicantly (p < 0.05) increased values of a-MSH after 1 year of interdisciplinary therapy. Furthermore, the a-MSH levels were
signicantly (p < 0.05) higher after 1 year compared with after
6 months of therapy. However, the levels of AgRP did not change
signicantly during the therapy. For the AT + RT group, it was observed that the levels of AgRP increased signicantly (p < 0.05)
after 6 months of therapy and then reduced (p < 0.05) after 1 year
of therapy. Additionally, the levels of serum a-MSH after 6 months
and 1 year of therapy were different (p < 0.05) when compared between groups (Fig. 3).
In relation to the diet, both groups signicantly (p < 0.05) reduced similarly their total energy intake after 6 months and 1 year
of therapy. The AT + RT group signicantly (p < 0.05) reduced their
intake of lipids and protein after 6 months and after 1 year of interdisciplinary therapy. The AT group showed a signicant (p < 0.05)
reduction in carbohydrate intake after 6 months and after 1 year
(Table 2).
Discussion
One of the most interesting results in the present study was the
increase of AgRP concentrations in the AT + RT group after
6 months of intervention, followed by a reduction in AgRP levels
after 1 year of therapy. This result demonstrates that this group
had greater difculty in controlling their food intake at 6 months
of therapy due to increased secretion of the orexigenic factor AgRP,
which is involved with hunger signals at the hypothalamic arcuate
nucleus, but this effect was reversed by the end of the therapy (Andrews, 2011). Despite this difculty of the AT + RT group in controlling hunger, based on the concentrations of AgRP, this group
showed a reduction in total energy intake, lipids and protein after
6 months and after 1 year of interdisciplinary therapy. Few studies
have been conducted to correlate types of exercise with anorexigenic and orexigenic factors. An experimental study found that
6 weeks of aerobic exercise promoted a decrease in plasma ghrelin
and increase of AgRP (Ghanbari-Niaki, Abednazari, Tayebi, Hossaini-Kakhak, & Kraemer, 2009). These results do not totally agree
with the results found in the present study, as we found an increase of AgRP in the AT + RT group, but not in the AT group. The
difference between these results may be due to the type of treatment provided in the two studies. Although the study of NiakiGhanbari et al. evaluated the effect of isolated aerobic exercise in
mice, the present study evaluated the effect of an interdisciplinary
intervention in obese adolescents. Thus, other factors such as diet
and psychological factors may also inuence the results shown in
this paper. Conversely, corroborating our ndings, a study showed
that circuit-resistance exercise was able to increase plasma AgRP
levels, suggesting that this type of physical activity induces hyper-
Table 1
Anthropometric, body composition and neuropeptides values of aerobic training (AT) and aerobic training (AT) + resistance training (RT) groups at baseline and after 6 and
12 months of therapy.
Aerobic training (AT)
Baseline
Body mass (kg)
BMI (kg/m2)
Body fat mass (kg)
Body lean mass (kg)
NPY (ng/ml)
MCH (ng/ml)
93.92 14.06
35.36 3.95
39.57 9.47
54.21 13.31
1.08 1.29
8.11 4.41
1 year
Baseline
b
85.30 12.84
32.21 4.52b
31.46 12.69b
53.93 11.74
2.20 2.54
7.18 4.22
94.62 13.86
34.41 3.53
42.30 8.16
52.31 7.46
2.22 3.99
4.79 2.12
6 months
86.36 14.03
31.33 3.88a
32.63 8.32a
53.72 8.52
4.58 7.35
3.39 0.73
1 year
a
83.94 12.64b
30.35 4.29b
28.28 9.93b
55.67 7.28b
2.75 5.10
5.10 1.99
172
Fig. 3. AgRP (ng/ml) and a-MSH (ng/ml) values of aerobic training (AT) and aerobic training (AT) + resistance training (RT) groups at baseline and after 6 and 12 months of
therapy.
Table 2
Food intake values of aerobic training (AT) and aerobic training (AT) + resistance training (RT) groups at baseline and after 6 months and 1 year of therapy.
Aerobic training (AT)
Energy (kcal)
Protein (g)
Carbohydrate (g)
Lipids (g)
Baseline
6 months
1 year
Baseline
6 months
1 year
1857.01 357.61
95.10 21.39
248.57 49.40
49.41 19.99
1251.11 89.11a
72.54 9.32
168.31 18.75a
34.56 4.20
1318.14 203.25b
86.86 23.68
158.58 30.88b
37.22 10.78
1902.67 508.68
66.80 43.67
182.13 105.28
50.50 28.33
1141.08 402.74a
47.60 14.28a
162.22 56.92
33.91 14.86a
1310.79 330.69b
58.29 20.02b
197.49 48.02
33.48 11.51b
173
Cook, C. M., & Schoeller, D. A. (2011). Physical activity and weight control.
Conicting ndings. Current Opinion in Clinical Nutrition and Metabolic Care,
14(5), 419424.
Dmaso, A., de Piano, A., Tock, L., & Srirajaskanthan, R. (2009). Nutritional and
clinical strategies on prevention and treatment of NAFLD and metabolic
syndrome. In R. Lakshman, V. R. Preedy, R. R. Watson, & R. Srirajaskanthan
(Eds.), Nutrition (1st ed.. Diet therapy and the liver. Nutritional and clinical
strategies on the prevention and treatment of NAFLD and metabolic syndrome (1st
ed.), pp. 113130). London: Taylor & Francis LDT.
de Mello, M. T., de Piano, A., Carnier, J., Sanches Pde, L., Corra, F. A., Tock, L., et al.
(2011). Long-term effects of aerobic plus resistance training on the metabolic
syndrome and adiponectinemia in obese adolescents. The Journal of Clinical
Hypertension (Greenwich), 13(5), 343350.
Diguez, C., Vazquez, M. J., Romero, A., Lpez, M., & Nogueiras, R. (2011).
Hypothalamic control of lipid metabolism. Focus on leptin, ghrelin and
melanocortins. Neuroendocrinology, 94(1), 111.
Dietary reference intake for energy, carbohydrate, ber, fat, fatty acids, cholesterol,
protein, and amino acids (2002/2005). The report may be acessed via
www.nap.edu.
Fields, D. A., Hunter, G. R., & Goran, M. I. (2000). Validation of the BOD POD with
hydrostatic weighing. Inuence of body clothing. International Journal of Obesity,
24, 200205.
Foschini, D., Arajo, R. C., Bacurau, R. F., De Piano, A., De Almeida, S. S., Carnier, J.,
et al. (2010). Treatment of obese adolescents. The inuence of periodization
models and ACE genotype. Obesity (Silver Spring), 18(4), 766772.
Ghanbari-Niaki, A., Abednazari, H., Tayebi, S. M., Hossaini-Kakhak, A., & Kraemer, R.
R. (2009). Treadmill training enhances rat agouti-related protein in plasma and
reduces ghrelin levels in plasma and soleus muscle. Metabolism, 58(12),
17471752.
Ghanbari-Niaki, A., Nabatchian, S., & Hedayati, M. (2007). Plasma agouti-related
protein (AgRP), growth hormone, insulin responses to a single circuit-resistance
exercise in male college students. Peptides, 28(5), 10351039.
Hansen, M. J., Schith, H. B., & Morris, M. J. (2005). Feeding responses to a
melanocortin agonist and antagonist in obesity induced by a palatable high-fat
diet. Brain Research, 1039(12), 137145.
Kirk, E. P., Donnelly, J. E., Smith, B. K., Honas, J., Lecheminant, J. D., Bailey, B. W., et al.
(2009). Minimal resistance training improves daily energy expenditure and fat
oxidation. Medicine and Science in Sports and Exercise, 41(5), 11221129.
Lus Griera, J., Mara Manzanares, J., Barbany, M., Contreras, J., Amig, P., & SalasSalvad, J. (2007). Physical activity, energy balance and obesity. Public Health
Nutrition, 10(10A), 11941199.
Martins, C., Kulseng, B., King, N. A., Holst, J. J., & Blundell, J. E. (2010). The effects of
exercise-induced weight loss on appetite-related peptides and motivation to
eat. Journal of Clinical Endocrinology and Metabolism, 95(4), 16091616.
Misra, M., Tsai, P. M., Mendes, N., Miller, K. K., & Klibanski, A. (2009). Increased
carbohydrate induced ghrelin secretion in obese vs. normal-weight adolescent
girls. Obesity (Silver Spring), 17(9), 16891695.
National Research Council, Food and Nutrition Board (1989). Recommended Dietary
Allowances (10th ed.). Washington, DC: National Academy Press.
Prince, A. C., Brooks, S. J., Stahl, D., & Treasure, J. (2009). Systematic review and
meta-analysis of the baseline concentrations and physiologic responses of gut
hormones to food in eating disorders. American Journal of Clinical Nutrition,
89(3), 755765.
Sanches, P. D., Mello, M. T., Fonseca, F. A., Elias, N., Piano, A. D., Carnier, J., et al.
(2012). Insulin resistance can impair reduction on carotid intima-media
thickness in obese adolescents. Arquivos Brasileiros de Cardiologia, 99, 892899.
Stensel, D. (2010). Exercise, appetite and appetite-regulating hormones.
Implications for food intake and weight control. Annals of Nutrition and
Metabolism, 57(Suppl. 2), 3642.
Tanner, J. M., & Whithouse, R. H. (1976). Clinical longitudinal standards for height,
weight, weight velocity and stages of puberty. Archives of Disease in Childhood,
51, 170179.
Tian, D. R., Li, X. D., Shi, Y. S., Wan, Y., Wang, X. M., Chang, J. K., et al. (2004). Changes
of hypothalamic alpha-MSH and CART peptide expression in diet-induced obese
rats. Peptides, 25(12), 21472153.
Tock, L., Dmaso, A. R., de Piano, A., Carnier, J., Sanches, P. L., Lederman, H. M., et al.
(2010). Long-term effects of metformin and lifestyle modication on
nonalcoholic fatty liver disease obese adolescents. Journal of Obesity, pii:
831901.