Appetite 69 (2013) 168–173

Contents lists available at SciVerse ScienceDirect

Appetite

journal homepage: www.elsevier .com/locate /appet

Research report

Aerobic training (AT) is more effective than aerobic plus resistancetraining (AT + RT) to improve anorexigenic/orexigenic factors in obeseadolescents q

0195-6663/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.appet.2013.05.018

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. Conflictsof interest: The authors have nothing to disclose.⇑ Corresponding authors.

E-mail addresses: junecarnier@gmail.com (J. Carnier), ana.damaso@unifesp.br(A.R. Dâmaso).

June Carnier a,⇑, Marco Túlio de Mello a,b,c, Carolina Ackel-D́Elia a, Flavia Campos Corgosinho a,Raquel Munhoz da Silveira Campos a, Priscila de Lima Sanches a, Deborah Cristina Landi Masquio a,Carlos Roberto Bueno Júnior a, Aline de Piano Ganen a, Aniela C. Martins a, Danielle Arisa Caranti d,e,Lian Tock a, Ana Paula Grotti Clemente a, Sergio Tufik b,c, Ana R. Dâmaso a,d,e,⇑a Programa de Pós-Graduação em Nutrição, Universidade Federal de São Paulo – UNIFESP, Brazilb Departamento de Psicobiologia, Universidade Federal de São Paulo – UNIFESP, São Paulo, Brazilc Associação Fundo de Incentivo à Pesquisa, Universidade Federal de São Paulo – UNIFESP, São Paulo, Brazild Departamento de Biociências, Universidade Federal de São Paulo – UNIFESP, São Paulo, Brazile Programa de Pós-Graduação Interdisciplinar em Ciências da Saúde, Universidade Federal de São Paulo – UNIFESP, São Paulo, Brazil

a r t i c l e i n f o a b s t r a c t

Article history:Received 26 September 2012Received in revised form 25 May 2013Accepted 27 May 2013Available online 10 June 2013

Keywords:Aerobic trainingResistance trainingNeuropeptidesObesity

Background: The regulation of energy balance is influenced by physical exercise. Although some studiesshow 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 train-ing (AT + RT) on anorexigenic and orexigenic factors in obese adolescents undergoing interdisciplinaryweight loss therapy. Methods: A total of 26 obese adolescents, aged 15–19 years with BMI P P95 weresubmitted to 12 months of interdisciplinary intervention (clinical support, nutrition, psychology andphysical exercise) and divided into two groups, aerobic training (AT) (n = 13) or aerobic plus resistancetraining (AT + RT) (n = 13), which were matched according to gender and body mass. Blood samples werecollected to analyze orexigenic factors (AgRP, NPY, MCH) and the anorexigenic factor alpha-MSH. Results:The AT and AT + RT groups significantly reduced body mass, body mass index and body fat mass (kg) dur-ing the therapy. The AT group showed no significant changes in body lean mass (kg), whereas the AT + RTgroup showed an increase in body lean mass (kg) during the interdisciplinary intervention. There was anincrease in AgRP levels (ng/ml) only in the AT + RT group after 6 months of interdisciplinary interventioncompared with baseline condition. Conversely, a-MSH levels (ng/ml) increased only in the AT group after12 months of interdisciplinary intervention compared with baseline condition. Conclusion: Aerobic train-ing (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 taining increased energy expenditure (Foschini et al., 2010; Luís

An interdisciplinary intervention, incorporating both psycho-logical and physiological components, is important to promotethe reduction of body mass, blood pressure and coronary diseases(Carnier et al., 2010; Sanches et al., 2012). Thus, physical exercisehas an important role in helping with weight loss, as well as main-

Griera et al., 2007). However, a deeper understanding of the con-nections between physical activity and appetite is needed to opti-mize treatment of patients with obesity.

There are many factors involved in hunger and satiety signals.Leptin, a key point of this regulation, is secreted by adipose tissueand transported to the brain, where it crosses the blood-brain bar-rier and binds to its specific receptor (OB-R) in two neuronal pop-ulations in the arcuate nucleus (ARC) in the hypothalamus. Theneurons pro-opiomelanocortin (POMC), and cocaine- and amphet-amine-regulated transcript (CART) stimulate the expression of a-melanocyte-stimulating hormone (a-MSH) – secreting neuronsand inhibit the expression of neuropeptide Y/agouti-related pro-tein (NPY/AgRP) (Boguszewski, Paz-Filho, & Velloso, 2010; Diéguez,Vazquez, Romero, López, & Nogueiras, 2011).

J. Carnier et al. / Appetite 69 (2013) 168–173 169

These primary targets of leptin signaling communicate withsecond-order neurons in other hypothalamic nuclei, especially inthe paraventricular nucleus and lateral hypothalamus, to stimulatethe expression of anorexigenic neurotransmitters, including corti-cotropin-releasing hormone (CRH) and thyrotropin-releasing hor-mone (TRH), and to inhibit orexigenic pathways, including orexinand melanin-concentrating hormone (MCH). The final biologicalactions of leptin are inhibition of food intake and stimulation of en-ergy expenditure (Boguszewski et al., 2010; Diéguez et al., 2011).

This complex system of regulation of energy balance is influ-enced by physical exercise. Although some studies show a stimula-tion of hormones related to food intake, others show that exerciseprovides satiety (Cook & Schoeller, 2011). Understanding the en-ergy balance effects of different types of physical exercise couldhelp with the treatment of obese patients.

Aerobic training (AT) and aerobic plus resistance training(AT + RT) are the exercise training programs most studied for thetreatment of obesity. The relationship between the type of exerciseperformed and food intake is not very clear in the literature. Thus,the aim of this study was to compare the effects of both programsas part of an interdisciplinary therapy as measured by AgRP, NPY,MCH and a-MSH levels in obese adolescents. We hypothesizedthat there would be no differences in the energy balance regulationbetween both types of exercise.

Fig. 1. Selection of volunteers for the study.

Methods

Study population

A total of 134 adolescents were selected to participate of thepresent study. They were selected from GEO (InterdisciplinaryObesity Program) of Universidade Federal de São Paulo – UNIFESPin 2010.

Of these 134 participants, we excluded 74 (36 from the ATgroup and 38 from the AT + RT group) because they did not com-plete the therapy for reasons such as starting a professional job,changes in school schedule, lack of motivation and lack of moneyfor transportation. Additionally, participants who did not performall necessary examinations in the three stages of evaluation andwho did not complete 75% of all therapies were also excluded.Forty-seven of the remaining 60 obese adolescents were initiallyincluded in the AT + RT group and 13 were in the AT group. To eval-uate the same number of volunteers in each group, the 13 patientsof the AT group were matched according to gender and body masswith volunteers from the AT + RT group. Thus, a total of 26 obeseadolescents were evaluated in this study (13 adolescents per-formed the AT exercises and 13 adolescents performed the AT + RTexercises). There were five boys and eight girls in each group (ATand AT + RT group) (Fig. 1).

The inclusion criteria for participating in this program for weightloss were as follows: post-pubertal adolescents presenting withobesity who were healthy enough to perform physical activity andavailable to participate in the program for 1 year. All adolescentswere aged from 15 to 19 years, presented with obesity (BMI > 95thpercentile, according to the Center for Disease Control and Preven-tion) and were considered post-pubertal (Tanner Stage = 5). Anendocrinologist assessed the Tanner stage, appointing the value thatbest identified the stage of sexual maturation for each adolescent(Tanner & Whithouse, 1976). All adolescents completed the effortelectrocardiogram maximum test until exhaustion to verify whetherthey could safely perform physical exercise. The non-inclusion crite-ria were limitations such as an identified genetic disease (e.g. Downsyndrome), metabolic or endocrine diseases, chronic alcohol con-sumption or previous use of drugs such as glucocorticoids and psy-chotropics or pregnancy (Fig. 2).

This study was performed in accordance with the principles ofthe declaration of Helsinki and was formally approved by the Eth-ical Committee of the Universidade Federal de São Paulo – UNIFESP(#0135/04). Informed consent was obtained from all subjects and/or their parents. This study was registered at clinicaltrials.gov(NCT01358773).

Research design

The volunteers were submitted to 1 year of interdisciplinaryintervention (clinical support, nutrition, psychology and physicalexercise) and divided into two groups, aerobic training (AT) or aer-obic plus resistance training (AT + RT) (Fig. 2). These aspects oftherapy will be described further below. During the first month,the adolescents were submitted for evaluations. Thereafter, theystarted the interdisciplinary weight loss program. The same evalu-ation procedures were performed after short – (6 months) andlong-term (12 months) therapy (Dâmaso, de Piano, Tock, & Srira-jaskanthan, 2009). All interventions and evaluations were con-ducted in the CEPE (Centro de Estudos em Psicobiologia eExercício) from AFIP, where some research studies of the Universid-ade Federal de São Paulo are conducted.

MeasurementsSubjects were weighed to the nearest 0.1 kg on the Filizola scale

while wearing light weight clothing and no shoes. Height was mea-sured to the nearest 0.5 cm using a wall-mounted stadiometer(Sanny, model ES 2030). Body mass index (BMI) was calculatedas the body weight (wt) divided by height (ht) squared (wt/ht2).Body composition was measured by air-displacement in a BOD

Fig. 2. Diagram of weight loss interdisciplinary therapy.

170 J. Carnier et al. / Appetite 69 (2013) 168–173

POD body composition system (version 1.69, Life MeasurementInstruments, Concord, CA) (Fields, Hunter, & Goran, 2000).

Analyses of food intake were made by 3 days of recordatory in-quiry. With the help of their parents, each adolescent was asked torecord his or her diet over a period of 3 days, including 2 days dur-ing the week and 1 day of the weekend, at the beginning of thestudy and at 6 and 12 months. Portions were measured in termsof familiar volumes and sizes. Dietary data for all individuals weretransferred to a computer by the same nutritionist, and the nutri-ent composition was analyzed by a PC program developed at theUniversidade Federal de São Paulo (Nutwin software, for Windows,1.5 version, 2002).

Blood samples were collected in the outpatient clinic around8:00 a.m. after an overnight fast. Serum AgRP, NPY, MCH anda-MSH concentrations were measured using a commerciallyavailable enzyme-linked immune sorbent assay (ELISA) kit fromPhoenix Pharmaceuticals (Belmont, CA) according to the manufac-turer’s instructions.

Physical therapyAll adolescents performed 1 year of physical exercise three

times a week. All sessions were individually supervised by anexperienced sports physiologist. During the exercise sessions, theadolescents’ heart rates were continuously monitored by cardiom-eter (Polar–Model FS1 dark blue) at intervals of 5 min during alltraining sessions. The exercise program was based on recommen-dations from the ACSM (2009).

Aerobic training: During the year of therapy, the adolescents inthe AT group followed a personalized aerobic training program of60 min duration three times a week under the supervision of asports physiologist. The aerobic exercises were performed at thecardiac frequency intensity of the ventilatory threshold I(±4 bpm) on a motor-driven treadmill (Life Fitness–Model TR9700HR). After every 6 months of training, aerobic tests were per-formed to re-assess physical capacity and to individually adjustphysical training intensity.

Aerobic training plus Resistance training: During the year of ther-apy, the adolescents in the AT + RT group followed a personalized30 min aerobic training program plus 30 min of resistance training

three times a week under the supervision of a sports physiologist.The aerobic exercises were performed as described above. Addi-tionally, the adolescents worked each of the main muscle groupswith resistance training. The exercises performed during the mus-cle training program were the bench press, pulley (lat pull-down),leg-press, curl, ankle extension machine (sitting), curl machine fortriceps, abdominal machine and trunk extensor machine. All ado-lescents had a period of 2 weeks of adaptation to training to learnthe movements, performing three sets of 15–20 RM for each exer-cise. After this adaptation period, the training load was adjustedand every 8 weeks, volume and intensity were adjusted inverselyto decrease the number of repetitions from 15–20 to 10–12 and6–8, respectively, for three sets.

Clinical therapyAll obese adolescents were evaluated by the endocrinologist in

the presence of their parents once each month. The doctor moni-tored and evaluated all clinical exams of adolescents and treatedany health problems during therapy. The medical follow-up in-cluded the initial medical history as well as a physical examinationof blood pressure, heart rate and body weight; additionally, pa-tients were checked for their adherence to all interdisciplinarytherapies. At all of these appointments with the doctor, the entireGEO team was also present. The team discussed with the patientsand their parents some possible changes in lifestyle to promotetheir health status.

Psychological therapyAll adolescents participated in weekly psychological orientation

group sessions (15 people per session) based on the psychody-namic approach with one trained psychologist. At these sessions,body image, low self-esteem, family problems, and eating disor-ders such as bulimia, anorexia nervosa, and binge eating, includingtheir signals, symptoms and consequences for health were dis-cussed, in addition to other topics. Individual psychological ther-apy was recommended when behavioral alterations were foundto be necessary.

J. Carnier et al. / Appetite 69 (2013) 168–173 171

Nutritional therapyThe adolescents participated in group and individual interven-

tions. The themes of group interventions were weight loss diets,the food pyramid, dietary analysis, diet and light concepts, fatand 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 nutri-tionists to encourage the adolescents to follow healthy eating hab-its. Furthermore, all adolescents were interviewed individuallytwice a month. Energy intake was set at the levels recommendedby the dietary reference intake for subjects with low levels of phys-ical activity of the same age and gender (National Research Council& Food & Nutrition Board, 1989).

PhysiotherapyThe adolescents participated both in group and individual inter-

ventions with two physical therapists once a week. Individual con-sultations were also performed if the patient had any injuries. Thethemes of group interventions were postural orientation, diaphrag-matic breathing, hydrotherapy, RPG, isostretching, balance andstretching.

Statistical analyses

Distributional assumptions were verified by the Kolmogorov–Smirnov test. An analysis of variance for repeated measures (ANO-VA) was used to compare both groups at the same time and eachgroup during the therapy. For confirmation Tukey’s post hoc testwas used. Data were analyzed by means of STATISTICA version7.0 for Windows, with significance set at p < 0.05 and expressedas the mean ± S.D.

Results

It was found that the AT group significantly (p < 0.05) reducedbody mass and BMI after 1 year of therapy. For this group, the bodyfat mass (kg) was reduced significantly (p < 0.05) after both6 months and after 1 year of therapy. The AT group showed no sig-nificant changes in body lean mass (kg), NPY or MCH levels duringthe interdisciplinary intervention (Table 1).

Analyzing the AT + RT group, the results show that this groupsignificantly (p < 0.05) reduced body mass, BMI and body fat mass(kg) after both 6 months and after 1 year of therapy when com-pared with the baseline conditions. In addition, the body lean mass(kg) increased significantly (p < 0.05) after 1 year of therapy whencompared with baseline conditions. There was no significantchange in NPY or MCH concentrations in either group during theinterdisciplinary intervention (Table 1).

Table 1Anthropometric, body composition and neuropeptides values of aerobic training (AT) an12 months of therapy.

Aerobic training (AT)

Baseline 6 months 1 year

Body mass (kg) 93.92 ± 14.06 88.36 ± 13.22 85.30 ±BMI (kg/m2) 35.36 ± 3.95 33.24 ± 4.04 32.21 ±Body fat mass (kg) 39.57 ± 9.47 33.01 ± 12.15a 31.46 ±Body lean mass (kg) 54.21 ± 13.31 53.19 ± 11.88 53.93 ±NPY (ng/ml) 1.08 ± 1.29 6.32 ± 6.50 2.20 ±MCH (ng/ml) 8.11 ± 4.41 7.12 ± 2.71 7.18 ±

Data are presented as mean ± SD.a Baseline – 6 months.b Baseline – 1 year.c 6 months – 1 year.

In Fig. 3, the results show that the AT group exhibited signifi-cantly (p < 0.05) increased values of a-MSH after 1 year of interdis-ciplinary therapy. Furthermore, the a-MSH levels weresignificantly (p < 0.05) higher after 1 year compared with after6 months of therapy. However, the levels of AgRP did not changesignificantly during the therapy. For the AT + RT group, it was ob-served that the levels of AgRP increased significantly (p < 0.05)after 6 months of therapy and then reduced (p < 0.05) after 1 yearof therapy. Additionally, the levels of serum a-MSH after 6 monthsand 1 year of therapy were different (p < 0.05) when compared be-tween groups (Fig. 3).

In relation to the diet, both groups significantly (p < 0.05) re-duced similarly their total energy intake after 6 months and 1 yearof therapy. The AT + RT group significantly (p < 0.05) reduced theirintake of lipids and protein after 6 months and after 1 year of inter-disciplinary therapy. The AT group showed a significant (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 theincrease of AgRP concentrations in the AT + RT group after6 months of intervention, followed by a reduction in AgRP levelsafter 1 year of therapy. This result demonstrates that this grouphad greater difficulty in controlling their food intake at 6 monthsof therapy due to increased secretion of the orexigenic factor AgRP,which is involved with hunger signals at the hypothalamic arcuatenucleus, but this effect was reversed by the end of the therapy (An-drews, 2011). Despite this difficulty of the AT + RT group in con-trolling hunger, based on the concentrations of AgRP, this groupshowed a reduction in total energy intake, lipids and protein after6 months and after 1 year of interdisciplinary therapy. Few studieshave been conducted to correlate types of exercise with anorexi-genic and orexigenic factors. An experimental study found that6 weeks of aerobic exercise promoted a decrease in plasma ghrelinand increase of AgRP (Ghanbari-Niaki, Abednazari, Tayebi, Hossa-ini-Kakhak, & Kraemer, 2009). These results do not totally agreewith the results found in the present study, as we found an in-crease of AgRP in the AT + RT group, but not in the AT group. Thedifference between these results may be due to the type of treat-ment provided in the two studies. Although the study of Niaki-Ghanbari et al. evaluated the effect of isolated aerobic exercise inmice, the present study evaluated the effect of an interdisciplinaryintervention in obese adolescents. Thus, other factors such as dietand psychological factors may also influence the results shown inthis paper. Conversely, corroborating our findings, a study showedthat circuit-resistance exercise was able to increase plasma AgRPlevels, suggesting that this type of physical activity induces hyper-

d aerobic training (AT) + resistance training (RT) groups at baseline and after 6 and

Aerobic training (AT) + resistance training (RT)

Baseline 6 months 1 year

12.84b 94.62 ± 13.86 86.36 ± 14.03a 83.94 ± 12.64b

4.52b 34.41 ± 3.53 31.33 ± 3.88a 30.35 ± 4.29b

12.69b 42.30 ± 8.16 32.63 ± 8.32a 28.28 ± 9.93b

11.74 52.31 ± 7.46 53.72 ± 8.52 55.67 ± 7.28b

2.54 2.22 ± 3.99 4.58 ± 7.35 2.75 ± 5.104.22 4.79 ± 2.12 3.39 ± 0.73 5.10 ± 1.99

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 oftherapy.

Table 2Food 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) Aerobic training (AT) + resistance training (RT)

Baseline 6 months 1 year Baseline 6 months 1 year

Energy (kcal) 1857.01 ± 357.61 1251.11 ± 89.11a 1318.14 ± 203.25b 1902.67 ± 508.68 1141.08 ± 402.74a 1310.79 ± 330.69b

Protein (g) 95.10 ± 21.39 72.54 ± 9.32 86.86 ± 23.68 66.80 ± 43.67 47.60 ± 14.28a 58.29 ± 20.02b

Carbohydrate (g) 248.57 ± 49.40 168.31 ± 18.75a 158.58 ± 30.88b 182.13 ± 105.28 162.22 ± 56.92 197.49 ± 48.02Lipids (g) 49.41 ± 19.99 34.56 ± 4.20 37.22 ± 10.78 50.50 ± 28.33 33.91 ± 14.86a 33.48 ± 11.51b

Data are presented as mean ± SD. Significance set at p < 0.05.a Baseline – 6 months.b Baseline – 1 year.c 6 months – 1 year.# Difference between AT and AT + RT groups at the same time.

172 J. Carnier et al. / Appetite 69 (2013) 168–173

phagia to induce fuel recovery after exercise (Ghanbari-Niaki,Nabatchian, & Hedayati, 2007).

It also has been demonstrated that specific types of nutrientscan influence some factors related to energy balance (Misra, Tsai,Mendes, Miller, & Klibanski, 2009). Some authors have shown thatobese rats fed a high-fat diet exhibited a decrease in the number ofneurons carrying a-MSH and CART peptides in the arcuate nucleusof the hypothalamus as well as higher energy intake (Tian et al.,2004). On the contrary, other scientists showed that 2 or 12 weeksof feeding a high-fat diet did not change hypothalamic a-MSH con-tent in rats (Hansen, Schiöth, & Morris, 2005). In the present study,we verified that the AT + RT group significantly reduced the intakeof lipids and did not show significant changes in a-MSH levels after1 year of interdisciplinary therapy, whereas the AT group did notshow changes in lipid intake but exhibited an increase in a-MSHlevels throughout the treatment. It is important to consider thatneither of the two groups consumed macronutrients above the rec-ommended values as determined by the Dietary reference intakefor energy, fiber, fatty acids, and protein (2002/2005). However,this study is limited by the use of the 3-day food record, the instru-ment that assessed the dietary intake of the volunteers in thisstudy. As such, the teenagers in the study may have omitted cer-tain information about their diets, underestimating the amountsof macronutrients consumed.

In addition Prince, Brooks, Stahl, and Treasure (2009) showedthat individuals with eating disorders had higher baseline concen-trations of ghrelin (an appetite stimulant), peptide YY and chole-cystokinin (appetite inhibitors) compared with individualswithout eating disorders. These results suggest that feeding-

related behaviors, such as fasting and purging, can also influencethe levels of orexigenic and anorexigenic factors.

Another interesting result found in the present study was theincrease of a-MSH concentrations after long-term therapy only inobese adolescents who underwent AT. We did not find any studyto compare with our findings that evaluated the effect of exerciseon the concentrations of a-MSH in obese adolescents. However,Alves et al. (2012) verified that healthy elderly male volunteersshowed a reduction of serum a-MSH levels after 3 months of aer-obic training. It is important to consider that this study was con-ducted with older, non-obese people.

These factors could explain the difference in findings betweenthe present study and the study performed by Alves et al. In addi-tion, some studies have shown that the reduction of body mass byphysical training promotes an increase of PYY in obese subjects.PYY is a hormone secreted by the intestine postprandially whichcauses a decrease in appetite and food intake. Studies using ashort-term and long-term intervention found the same result of in-creased satiety after aerobic exercise (Martins, Kulseng, King,Holst, & Blundell, 2010; Stensel, 2010). These studies correlatedwith our results in which we found a reduction of body massaccompanied by an increase in satiety in the AT group.

Although we found that aerobic training (AT) as part of an inter-disciplinary therapy was more effective to improve the energy bal-ance of obese adolescents, the two intervention groups showed nodifference in weight loss at 6 months of treatment and at the end ofthe intervention. It is important to emphasize that we are not eval-uating the effects of exercise as an individual component of thetreatment plan because the volunteers also participated in other

J. Carnier et al. / Appetite 69 (2013) 168–173 173

interventions such as nutrition modification, which helped withweight loss during treatment. Thus, it appears that the stimulationof orexigenic and anorexigenic factors did not effectively contrib-ute to either group exhibiting a worse or better outcome afterinterdisciplinary therapy.

We must also consider that the AT group showed a significantreduction in lean body mass (kg), whereas the AT + RT groupshowed a significant increase in lean body mass (kg) during thetherapy. This factor could partially explain the reason for bothstudied groups exhibiting similar results for weight loss after theintervention, despite the stimulation of anorexigenic factors onlyin the AT + RT group. In accordance with scientific literature, resis-tance training results in increased fat-free mass and therefore en-ergy expenditure, contributing to a positive impact on energybalance and fat oxidation (Kirk et al., 2009).

Because these volunteers had the guidance of and treatment byother health professionals, subjects in the AT + RT group were ableto control hunger and reduce energy intake during the treatmentdespite the unfavorable values of orexigenic and anorexigenic fac-tors for weight loss (Campos et al., 2012; Tock et al., 2010). In addi-tion, previous studies from our group demonstrated that theAT + RT group showed more effective improvements in adiponec-tinemia and metabolic profiles, suggesting that this type of trainingexercise can be important in controlling the metabolic syndrome inadolescents (de Mello et al., 2011).

Although we believe that this study provides relevant findings,the lack of a normal-weight control group and the small number ofvolunteers evaluated at the end of the study (due to the loss of vol-unteers during the long-term intervention of 1 year) are the limita-tions of the study. It is important to highlight that without acontrol group, we cannot know the effects of natural fluctuationsin the analyzed variables.

In conclusion, aerobic training (AT) as part of an interdisciplin-ary therapy is more effective than aerobic plus resistance training(AT + RT) to improve anorexigenic/orexigenic factors in obeseadolescents.

References

ACSM (2009). Position stand on the appropriate intervention strategies for weightloss and prevention of weight regain for adults. Medicine and Science in Sportsand Exercise, 41, 459–471.

Alves, E. S., Souza, H. S., Rosa, J. P., Lira, F. S., Pimentel, G. D., Santos, R. V., et al.(2012). Chronic exercise promotes alterations in the neuroendocrine profile ofelderly people. Hormone and Metabolic Research, 44(13), 975–979.

Andrews, Z. B. (2011). Central mechanisms involved in the orexigenic actions ofghrelin. Peptides, 32(11), 2248–2255.

Boguszewski, C. L., Paz-Filho, G., & Velloso, L. A. (2010). Neuroendocrine bodyweight regulation. Integration between fat tissue, gastrointestinal tract, and thebrain. Endokrynologia Polska, 61(2), 194–206.

Campos, R. M., de Piano, A., da Silva, P. L., Carnier, J., Sanches, P. L., Corgosinho, F. C.,et al. (2012). The role of pro/anti-inflammatory adipokines on bone metabolismin NAFLD obese adolescents. Effects of long-term interdisciplinary therapy.Endocrine.

Carnier, J., de Piano, A., de Lima Sanches, P., Tock, L., do Nascimento, C. M., Oyama, L.M., et al. (2010). The role of orexigenic and anorexigenic factors in aninterdisciplinary weight loss therapy for obese adolescents with symptoms ofeating disorders. International Journal of Clinical Practice, 64(6), 784–790.

Cook, C. M., & Schoeller, D. A. (2011). Physical activity and weight control.Conflicting findings. Current Opinion in Clinical Nutrition and Metabolic Care,14(5), 419–424.

Dâmaso, A., de Piano, A., Tock, L., & Srirajaskanthan, R. (2009). Nutritional andclinical strategies on prevention and treatment of NAFLD and metabolicsyndrome. In R. Lakshman, V. R. Preedy, R. R. Watson, & R. Srirajaskanthan(Eds.), Nutrition (1st ed.. Diet therapy and the liver. Nutritional and clinicalstrategies on the prevention and treatment of NAFLD and metabolic syndrome (1sted.), pp. 113–130). London: Taylor & Francis LDT.

de Mello, M. T., de Piano, A., Carnier, J., Sanches Pde, L., Corrêa, F. A., Tock, L., et al.(2011). Long-term effects of aerobic plus resistance training on the metabolicsyndrome and adiponectinemia in obese adolescents. The Journal of ClinicalHypertension (Greenwich), 13(5), 343–350.

Diéguez, C., Vazquez, M. J., Romero, A., López, M., & Nogueiras, R. (2011).Hypothalamic control of lipid metabolism. Focus on leptin, ghrelin andmelanocortins. Neuroendocrinology, 94(1), 1–11.

Dietary reference intake for energy, carbohydrate, fiber, fat, fatty acids, cholesterol,protein, and amino acids (2002/2005). The report may be acessed viawww.nap.edu.

Fields, D. A., Hunter, G. R., & Goran, M. I. (2000). Validation of the BOD POD withhydrostatic weighing. Influence of body clothing. International Journal of Obesity,24, 200–205.

Foschini, D., Araújo, R. C., Bacurau, R. F., De Piano, A., De Almeida, S. S., Carnier, J.,et al. (2010). Treatment of obese adolescents. The influence of periodizationmodels and ACE genotype. Obesity (Silver Spring), 18(4), 766–772.

Ghanbari-Niaki, A., Abednazari, H., Tayebi, S. M., Hossaini-Kakhak, A., & Kraemer, R.R. (2009). Treadmill training enhances rat agouti-related protein in plasma andreduces ghrelin levels in plasma and soleus muscle. Metabolism, 58(12),1747–1752.

Ghanbari-Niaki, A., Nabatchian, S., & Hedayati, M. (2007). Plasma agouti-relatedprotein (AgRP), growth hormone, insulin responses to a single circuit-resistanceexercise in male college students. Peptides, 28(5), 1035–1039.

Hansen, M. J., Schiöth, H. B., & Morris, M. J. (2005). Feeding responses to amelanocortin agonist and antagonist in obesity induced by a palatable high-fatdiet. Brain Research, 1039(1–2), 137–145.

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 fatoxidation. Medicine and Science in Sports and Exercise, 41(5), 1122–1129.

Luís Griera, J., María Manzanares, J., Barbany, M., Contreras, J., Amigó, P., & Salas-Salvadó, J. (2007). Physical activity, energy balance and obesity. Public HealthNutrition, 10(10A), 1194–1199.

Martins, C., Kulseng, B., King, N. A., Holst, J. J., & Blundell, J. E. (2010). The effects ofexercise-induced weight loss on appetite-related peptides and motivation toeat. Journal of Clinical Endocrinology and Metabolism, 95(4), 1609–1616.

Misra, M., Tsai, P. M., Mendes, N., Miller, K. K., & Klibanski, A. (2009). Increasedcarbohydrate induced ghrelin secretion in obese vs. normal-weight adolescentgirls. Obesity (Silver Spring), 17(9), 1689–1695.

National Research Council, Food and Nutrition Board (1989). Recommended DietaryAllowances (10th ed.). Washington, DC: National Academy Press.

Prince, A. C., Brooks, S. J., Stahl, D., & Treasure, J. (2009). Systematic review andmeta-analysis of the baseline concentrations and physiologic responses of guthormones to food in eating disorders. American Journal of Clinical Nutrition,89(3), 755–765.

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-mediathickness in obese adolescents. Arquivos Brasileiros de Cardiologia, 99, 892–899.

Stensel, D. (2010). Exercise, appetite and appetite-regulating hormones.Implications for food intake and weight control. Annals of Nutrition andMetabolism, 57(Suppl. 2), 36–42.

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, 170–179.

Tian, D. R., Li, X. D., Shi, Y. S., Wan, Y., Wang, X. M., Chang, J. K., et al. (2004). Changesof hypothalamic alpha-MSH and CART peptide expression in diet-induced obeserats. Peptides, 25(12), 2147–2153.

Tock, L., Dâmaso, A. R., de Piano, A., Carnier, J., Sanches, P. L., Lederman, H. M., et al.(2010). Long-term effects of metformin and lifestyle modification onnonalcoholic fatty liver disease obese adolescents. Journal of Obesity, pii:831901.