Pediatric Exercise Science, 2014, 26, 463-469 http://dx.doi.org/10.1123/pes.2013-0200 © 2014 Human Kinetics, Inc.
Effect of Aerobic Exercise on Hunger Feelings and Satiety Regulating Hormones in Obese Teenage Girls Wagner L. Prado
P. Babu Balagopal
Federal University of São Paulo
Nemours Children’s Clinic
Mara C. Lofrano-Prado
Lila M. Oyama
University of Pernambuco
Federal University of São Paulo
Thiago Ricardo S. Tenório
João Paulo Botero
University of Pernambuco
Federal University of São Paulo
James O. Hill University of Colorado Denver Exercise is implicated in modifying subsequent energy intake (EI) through alterations in hunger and/or satiety hormones. Our aim was to examine the effects of aerobic exercise on hunger, satiety regulatory peptides, and EI in obese adolescents. Nine obese girls (age: 13–18 years old, BMI: 33.74 ± 4.04 kg/m2) participated in this randomized controlled crossover study. Each participant randomly underwent 2 experimental protocols: control (seated for 150 min) and exercise (exercised for 30 min on a treadmill performed at ventilatory threshold [VT] intensity and then remained seated for 120 min). Leptin, peptide YY3–36 (PYY3–36), and subjective hunger were measured at baseline as well as 30 min and 150 min, followed by 24-hr EI measurement. Exercise session resulted in an acute increase in PYY3–36 (p < .01) without changes in leptin and/or hunger scores. The control session increased hunger scores (p < .01) and decreased circulating leptin levels (p = .03). There was a strong effect size for carbohydrate intake (d = 2.14) and a modest effect size for protein intake (d = 0.61) after the exercise compared with the control session. Exercise performed at VT intensity in this study appears to provoke a state of transient anorexia in obese girls. These changes may be linked to an increase in circulating PYY3–36 and maintenance of leptin levels. Keywords: adolescent, obesity, hunger, satiety, exercise, peptide YY Physical activity (PA)/exercise-based lifestyle modification strategies are the cornerstones of obesity treatment. PA creates a net negative energy balance, primarily by increasing energy expenditure (EE; 13). Recently, considerable attention has been focused on the effect of Prado is with the Dept. of Human Movement Sciences, Oyama the Dept. of Physiology, and Botero the Dept. of Human Movement Sciences, Federal University of São Paulo, São Paulo, Brazil. Balagopal is with the Biomedical Research Laboratory, Nemours Children’s Clinic, Jacksonville, FL. Lof rano-Prado is with the University of Pernambuco, Recife, Brazil. Tenório is with the Physical Education Postgraduate Program, University of Pernambuco, Recife, Brazil. Hill is with the Colorado Center for Health & Wellness, University of Colorado, Denver, CO. Address author correspondence to Wagner L. Prado at wagner. [email protected]
exercise on appetite and energy intake (EI; 19). Some, but not all, studies in adults and experimental animals have reported that exercise, mainly high intensity, creates a transient anorexic state as the decrease in hunger after an exercise bout appears to be short lived (26). Exercise is also implicated in modifying subsequent EI through alterations in hunger and/or appetite and regulatory peptides, both at the short- and long-term signaling levels (18). The regulation of energy balance (feeding, EI, and EE) involves an intricate interplay between central nervous system (CNS) and various organs involved in energy homeostasis (32). Several peptides released by peripheral tissues, interact with specific brain areas, stimulating or inhibiting neurons to release anorexigenic or orexigenic neuropeptides that are involved in the control of eating behavior and EE pattern (27). The peripheral signals can be divided in 2 major categories: 1) the adiposity signals,
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such as leptin, which are involved in the long-term regulation of energy balance, acting directly in response to alterations in body fatness, and 2) gut hormones such as peptide YY (PYY), which comprises signals of satiety and hunger and are released between and during meals, involved in the acute control of feeding behavior. The negative energy balance produced by exercise bouts may also stimulate compensatory eating behaviors (eg, hunger, food intake, and appetite; 9), which, in turn, could offset the exercise-induced energy deficit altering its effects on weight loss (16). A few studies have shown that aerobic exercise resulted in no detectable acute increase in EI in obese children (21) and adolescents (5). However, others have shown that high intensity exercise leads to a pronounced reduction in 24-hr EI in obese adolescent boys (31). In normal weight children Bozinovski et al (2) demonstrated that exercise at VT promoted increase in subjective appetite and desire to eat, without changes on EI after exercise sessions. In obese boys, Tamam et al (30) reported an increase in subjective satiety without apparent EI compensation in response to a single bout of exercise at VT intensity. The changes in EI following exercise may be, at least in part, dependent on changes in circulating satietyregulating peptides such as leptin and peptide YY (PYY; 12). However, little is known about the acute effects of exercise at VT intensity on food intake and these appetite regulatory peptides in obese adolescents. The primary aim of this study was to examine the effects of aerobic exercise on subjective hunger feelings, long-term and short-term satiety signals (leptin and PYY3–36), and the 24-hr EI in obese adolescents.
Material and Methods The study protocol was approved by the ethical committee of the University of Pernambuco (#154/09) and informed consent was obtained from all volunteers and/ or their parents. After baseline measurements we implemented a randomized controlled crossover design for the 2 experimental protocols described below. From 15 initially screened for the study, nine tightly controlled obese teenage girls with the following inclusion criteria were recruited through the outpatient clinic of the University of Pernambuco/Brazil for this study: age: 13–18 years, pubertal stage: Tanner 3–4, obesity: BMI > 95th (4) and absence of hypertension and/or other complications (metabolic, respiratory or genetics).
Figure 1 — Experimental design. VAS = visual analog scale.
In this crossover study design, the participants underwent 2 experimental conditions in a randomized order: 1) control (volunteers remained seated for 150 min) and 2) exercise (volunteers exercised on a treadmill for 30 min at a target intensity corresponding to VT and then remained seated for 120 min, after the conclusion of the of exercise session, or150 min from baseline). During the exercise session energy expenditure was measured by indirect calorimetry. During the first visit, anthropometry, body composition, and pubertal stage were measured and the participants underwent a maximal incremental test to determine VT. On the other visits, volunteers arrived at the laboratory around 7 AM after an overnight fast. They were asked to avoid moderate to vigorous PA for 48 hr before the experimental sessions. All participants were given a 350 kcal standard snack (composed of 61.7% carbohydrates, 13.44% proteins and 24.86% lipids), to minimize potential differences in the thermic effect of food (TEF) between participants. At 7:30 AM, participants followed the experimental protocols (control or exercise) in a randomized and counterbalanced order. All experiments were conducted in a temperature-controlled room (21–23 °C) and at the same time of the day. Subjective hunger feelings and the concentration of hormones were assessed at baseline, immediately after the session (30 min) and after 2 hr of passive recovery (150 min). In addition the 24-hr EI was estimated from the 24-hr recordings of food and beverage intake, which began immediately after the completion of the study or the 150 min measurement. Figure 1 depicts the overall experimental protocol. Obese adolescents were weighed wearing light clothing and without shoes on a Filizola scale (Model 160/300, Brazil) to the nearest 0.1 kg. Height was measured to nearest 0.5 cm by using a wall-mounted stadiometer Filizola (Model 160/300, Brazil). Body mass index (BMI) was calculated by dividing body weight (kg) by squared height (m2). Body composition was determined by bioelectrical impedance (Byodinamics A-310 body composition analyzer) under standardized conditions and the participants were asked to avoid consumption of caffeine and other dehydrating agents at least 24 hr before the test and all tests were performed in the fasted condition. Each participant was given drawings of the 5 stages of breast and pubic hair development. In an isolated room, the adolescents were asked to look at the drawings, read the descriptions, think about how they looked in compari-
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son with the drawings, and pick the 1that most closely resembled them; in case of a mismatch, pubic hair was used to determine the pubertal stage (6). Oxygen uptake (VO2) was measured directly in an open circuit respiratory metabolic system (Quark PFT, Cosmed, Italy), during a continuous incremental test on a treadmill (Cosmed T200, Italy). The initial load was set at 3 kph (warm up 3 min) and increased 1km/h each minute until exhaustion, inclination was kept constant at 1% (20). The termination criteria were volitional fatigue, Borg scale and gas exchange ratio higher than 18 and 1.15, respectively (15). The greatest VO2 obtained before test interruption was considered as VO 2peak. Before each test, the instruments were calibrated for gas composition and volume following manufacturers’ recommendations. VT was determined as the point at which there was a systematic increase in VE/VO2 without a corresponding increase in VE/VCO2, by 2 independent researchers. Participants were asked to complete a validated visual analog scale (VAS) to rate hunger (10). The questionnaire consisted of 6 visual analog scales to rate hunger, fullness, desire to eat, how much you can eat now, urge to eat and preoccupation with thoughts of food. The VAS consisted of horizontal lines of 100 mm with defined marks at each extremity that portrayed the expressed desire to eat excessively in the right extremity and the lack the desire to eat or not hungry in the left extremity. VAS was measured by hand, from left (minimum score of 0 cm) to right (maximum score of 10 cm). Each subject recorded all food and beverage consumed for 24 hr from the time when the study was completed (150 min measurement) and they left the laboratory (around 10 AM). A dietitian taught the parents and the adolescents upfront how to record food consumption. They were asked to measure portions in terms of familiar volume and size and by reference to an atlas of local food portions supplied to them. To minimize accuracy bias, the volunteers documented on a sheet what they ate and drank at the time of consumption. All dietary data were transferred to a computer by the same dietitian and EI (Kcal/day) and nutrient intake (carbohydrate, fat and protein) were analyzed using Nutwin software for Windows (Federal University of São Paulo—Paulista Medicine School, 2002) based on Western and local food tables. Blood samples were taken from anticubital vein at baseline, 30 and 150 min. Serum was separated by centrifugation and stored in a deep freezer at –80 °C until analysis. Serum leptin and PYY3–36 were measured by specific enzyme-linked immunosorbent multiplex panel assay kits (Lincoplex-Millipore Corporation, USA; assay sensitivity-leptin [157.2 pg/ml] and PYY [8.4 pg/ml]) using a Luminex system. The multiplex panel kits were developed with polystyrene microspheres with fluorescent dye that acted as both the identifier and the solid surface to build the immunoassay. Data analysis was performed using Statistical and SPSS for Windows. Data are expressed as mean ± SD, and
magnitude of change in percentage (Δ%). Trials (control vs exercise) and time points (basal, 30 min and 150 min) were compared using 2-way ANOVA for repeated measures with Duncan test as post hoc. Difference in 24 hr EI was assessed by paired Students t test. In addition, the effect size was calculated and is displayed when it was moderate (>0.30), as proposed by Cohen (3). Significance was set at p < .05. No order effect was noticed for any of study variables.
3. Results Table 1 summarizes the characteristics of the participants. The intensity of exercise during the session was 68.43 ± 8.31% of the VO2peak and the energy expenditure was 350 ± 15.34 Kcal. Baseline values of hunger scores, EI, leptin, and PYY3–36 were similar between control and exercise conditions (Figure 2 and 3). An interaction effect was observed for hunger (p = .012), indicating that after the control condition the participants’ hunger scores steadily increased from 0.63 ± 0.07 cm to 1.27 ± 0.38 cm at 30 min and 2.30 ± 0.89 cm at 150min, whereas it remained unaltered after the exercise condition (0.90 ± 0.08cm, 1.04 ± 0.08cm, 1.30 ± 0.06cm, for baseline, 30 min and 150 min respectively; Figure 2). In addition, hunger scores at 150 min were significantly higher in the control condition compared with exercise session (p = .01). An interaction effect was observed for leptin (p = .048), indicating that it decreased from 45.8 ± 18.0 ng/ dl to 41.6 ± 16.3 ng/dl at 30 min and 39.4 ± 15.6 ng/dl at 150 min in control condition, whereas it did not change after exercise condition (44.1 ± 15.2 ng/dl, 47.1 ± 20.1 ng/dl and 44.9 ± 17.4 ng/dl, for baseline, 30 min, and 150 min respectively; Figure 3). With respect to PYY3–36, the exercise condition resulted in a significant increase at 30 min (from 54.3 ± 22.9pg/ml to 72.4 ± 20.5pg/ml, which eventually tapered off after 150 min (59.3 ± 15.9 pg/ml; condition effect = 0.019; time effect = 0.031; interaction = 0.0117; Figure 3). However, similar changes were not observed in the Table 1 Participant Characteristics Variables
Mean (SD)
Age (y)
14.90 (1.14)
Body weight (kg)
86.70 (11.10)
BMI (kg/m2)
33.74 (4.03)
BMI percentile
97.78 (0.66)
Fat mass (%)
39.87 (5.40)
VO2peak (ml/kg/min–1) VO2peak at VT
(ml/kg/min–1)
28.25 (1.83) 19.34 (2.80)
Note. BMI= body mass index; VO2peak = peak oxygen uptake represented as ml of oxygen per kg of body mass per min; VT = ventilatory threshold.
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Figure 2 — Effects of exercise at ventilatory threshold on hunger feelings in obese teenage girls. *Denotes significant difference vs. basal; #Denotes significant difference vs. 30 min; ¥Denotes significant difference vs. control.
Figure 3 — Effects of exercise at ventilatory threshold on leptin and PYY3-36 levels in obese teenage girls. *Denotes significant difference vs basal; #Denotes significant difference vs. 30 min.
control condition (63.5 ± 17.3pg/ml, 71.6 ± 16.2 pg/ml, 61.8 ± 8.9 pg/ml, for baseline, 30 min, and 150 min, respectively). The Δ% increase in hunger scores in the control condition was almost 100% and 275% from baseline to 30 min and 150 min respectively. Interestingly, the Δ% increase in hunger scores in the exercise condition was only 13% from baseline to 30 min (nonsignificant; p > .05), but it increased by 139% from baseline to 150 min (p = .01). With regard to the regulatory peptides, the largest Δ% changes were observed after the exercise condition compared with control. The Δ % changes in leptin were 4.33% (p = .05) and 3.36% (p = .01) from baseline to 30 min and 150 min respectively. The corresponding changes for the control condition were –8.43% and –13.45% respectively. In the case of PYY3–36, Δ% increase in the exercise condition by 61% at 30 min (p = .04) and 35.36% at 150 min (p = .15). The corresponding Δ% changes in PYY3–36 for the control condition were 15.94% and 4.28% (both nonsignificant) respectively. The effect of exercise on energy and macronutrient intake is summarized in Table 2. Despite the absence of changes in the 24 hr EI and macronutrient intake between protocols, the results show a high effect size for carbohydrate intake after the exercise bout (d = 2.14); and a modest effect size in protein intake after exercise (d = 0.61) compared with the control session.
Table 2 Effects of Exercise at Ventilatory Threshold on Energy and Macronutrient Intake in Obese Teenage Girls TEI (Kcal/day)
Control
Exercise
p
1526+ 510
1626+ 300
.21
CHO (g/day)
192± 52
346± 108
.47
LIP (g/day)
55± 31
50± 23
.47
Protein (g/day)
80± 30
108± 68
.16
Note. TEI= total energy intake, CHO= carbohydrates, LIP= lipids.
Discussion The present study indicates that exercise performed at VT intensity elicits a transient anorexic effect in obese adolescent girls. Such notion is based on the following findings: (I) an acute increase in PYY3–36, in response to the exercise session and (II) a lack of increase in subjective hunger scores in response to the exercise session. Interestingly, the participants in the control session showed a precipitous increase in subjective hunger scores, but no appreciable change in PYY3–36. Further, the concentration of leptin, remained unaltered by the exercise session. The subjective hunger scores were remarkably lower in the exercise session compared with the control session, both
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Exercise and Satiety Regulating Hormones 467
at 30 min and after 150 min from baseline. The magnitude of changes in PYY3–36 observed in the current study suggests its potential role in the regulation of exercise-induced anorexia in obese adolescent girls, but this observation warrants further exploration in carefully conducted larger studies. It also appears that the anorexic effect was, at least in part, reversed by a compensatory increase in carbohydrate and protein intake over the 24 hr after the completion of the study or the 150 min measurement. The impact of exercise on subsequent EI and satiety signals in obese children and adolescents remains poorly understood, partly because of methodological limitations to address these issues (31). A recent study suggests that high intensity acute exercise reduces the neuronal brain response in food reward regions, potentially leading to decrease food intake (8). Another study in rodents (25) demonstrated aerobic exercise induced improvements in the central action of certain satiety-regulating hormones, thus contributing to appetite suppression. Likewise, certain studies suggest that aerobic exercise increases leptin receptor binding and leptin gene expression in the arcuate nucleus (14, 24). Systemic administration of PYY3–36 has also been shown to inhibit food intake in humans (29) and experimental animals (22). Gastric bypass patients demonstrated increased levels of PYY and that inhibition of the PYY responses resulted in the return of appetite and increased food intake (17). In our study, the concentration of the long-term satiety signal leptin was maintained, whereas the short-term satiety signal, PYY3–36, increased acutely after the exercise session. Previously Dood et al (5) demonstrated that both lean and overweight girls undergoing exercise at 75% VO2max did not alter daily EI, contrary to a decrease in EI in obese boys after high intensity exercise sessions observed by Thivel et al (31). Nemet et al (23) reported higher EI in obese and overweight children following exercise compared with a control session. These conflicting observations are intriguing, but the exact reasons are not clear. A variety of factors might have contributed to the conflicting data in different studies. One potential contributing factor may be related to the sample cohort and the difference in their maturity stages. While Nemet et al (23) studied early-pubertal stage children, our study was confined to adolescents. Potential differences in the exercise intensity and duration and limitations and/or differences in the methodologies used in the measurement of hunger feelings and EI such as prefixed meals, ad libitum meals, and food diaries are less sophisticated. Total EI as well as macronutrient content, consumption and timing may also have influenced the outcomes. Taken together, a comprehensive assessment that includes serial, quantifiable measures of hunger and food intake in addition to questions regarding other factors that can affect food intake is necessary (23). In the current study, carbohydrate and protein consumption tended to increase after the exercise session. The exact mechanisms are not readily available from the current study. However, reduced catecholamine and GH response to exercise compared with normal weight
controls have been reported in obese adolescents. This suggests reduced CHO and lipid energy sources for exercise and presumably greater need for proteins as an energy source. This may explain, in part, the increase in protein intake, potentially promoting muscle recovery (7,28). Of note, most previous studies that have assessed the effects of exercise intensity on energy balance have used relative exercise intensity based on maximum oxygen uptake (VO2max) or maximum heart rate, assuming that it would decrease the variability of the physiological response. This normalization process may not be the most appropriate method since individuals could show different metabolic, cardiovascular, and hormonal changes during exercise at the same relative VO2max or maximum heart rate (11). The use of the anaerobic threshold (AT) to normalize exercise intensity likely reduces variability between participants (1). One of the methods available to identify the AT is the VT. Although the study included both short-term and long-term satiety signals such as PYY3–36 and leptin respectively, we were unable to include other circulating satiety-regulating peptides such as ghrelin, insulin, and GLP-1. Further the insulin resistance status is not available in the participants. Future studies including these factors in a larger population may shed light on the underlying mechanisms and allow generalization of these findings. The use of self-reported food intake records for the quantification of energy intake has limitations and hence the data should be considered cautiously. Although the participants in the study were asked to avoid consumption of caffeine and other dehydrating agents at least 24 hr before the test and all tests were performed in the fasted condition, we cannot rule out potential overestimation of body fat by BIA, which is likely to be influenced by the hydration level. The small sample size is a potential limitation of the study, but the relatively homogeneous group of participants (see Table 1) and the randomized crossover design of the study rendered strength to the analysis of data. In conclusion, our data suggest that aerobic exercise performed at ventilatory threshold acutely evokes a transient anorexia state in obese adolescent girls. The exercise session, while not decreasing the hunger scores, does not appear to increase it. The clinical implications of this observation appear to be important. This exerciseinduced transient anorexia, if suitably modulated, can have important implications in weight maintenance and/or reduction in obese children. Additional research is warranted in larger populations using sophisticated approaches to determine the optimum dose of exercise (exercise duration, intensity, and time of the day) needed to inhibit hunger and compensatory eating behavior, thus facilitating a net negative energy balance in obese adolescents, helping these children in their fight against obesity. Acknowledgments We would like to thank the National Council for Scientific and Technological Development and the Foundation for Science
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and Technology of the State of Pernambuco (FACEPE) for financial support and Raphael M. Ritti-Dias for the support on data interpretation. Special thanks to patients and their parents for the participation in this study. The authors declare no conflicts of interest.
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Effect of Aerobic Exercise on Hunger Feelings and Satiety Regulating Hormones in Obese Teenage Girls Wagner L. Prado
P. Babu Balagopal
Federal University of São Paulo
Nemours Children’s Clinic
Mara C. Lofrano-Prado
Lila M. Oyama
University of Pernambuco
Federal University of São Paulo
Thiago Ricardo S. Tenório
João Paulo Botero
University of Pernambuco
Federal University of São Paulo
James O. Hill University of Colorado Denver Exercise is implicated in modifying subsequent energy intake (EI) through alterations in hunger and/or satiety hormones. Our aim was to examine the effects of aerobic exercise on hunger, satiety regulatory peptides, and EI in obese adolescents. Nine obese girls (age: 13–18 years old, BMI: 33.74 ± 4.04 kg/m2) participated in this randomized controlled crossover study. Each participant randomly underwent 2 experimental protocols: control (seated for 150 min) and exercise (exercised for 30 min on a treadmill performed at ventilatory threshold [VT] intensity and then remained seated for 120 min). Leptin, peptide YY3–36 (PYY3–36), and subjective hunger were measured at baseline as well as 30 min and 150 min, followed by 24-hr EI measurement. Exercise session resulted in an acute increase in PYY3–36 (p < .01) without changes in leptin and/or hunger scores. The control session increased hunger scores (p < .01) and decreased circulating leptin levels (p = .03). There was a strong effect size for carbohydrate intake (d = 2.14) and a modest effect size for protein intake (d = 0.61) after the exercise compared with the control session. Exercise performed at VT intensity in this study appears to provoke a state of transient anorexia in obese girls. These changes may be linked to an increase in circulating PYY3–36 and maintenance of leptin levels. Keywords: adolescent, obesity, hunger, satiety, exercise, peptide YY Physical activity (PA)/exercise-based lifestyle modification strategies are the cornerstones of obesity treatment. PA creates a net negative energy balance, primarily by increasing energy expenditure (EE; 13). Recently, considerable attention has been focused on the effect of Prado is with the Dept. of Human Movement Sciences, Oyama the Dept. of Physiology, and Botero the Dept. of Human Movement Sciences, Federal University of São Paulo, São Paulo, Brazil. Balagopal is with the Biomedical Research Laboratory, Nemours Children’s Clinic, Jacksonville, FL. Lof rano-Prado is with the University of Pernambuco, Recife, Brazil. Tenório is with the Physical Education Postgraduate Program, University of Pernambuco, Recife, Brazil. Hill is with the Colorado Center for Health & Wellness, University of Colorado, Denver, CO. Address author correspondence to Wagner L. Prado at wagner. [email protected]
exercise on appetite and energy intake (EI; 19). Some, but not all, studies in adults and experimental animals have reported that exercise, mainly high intensity, creates a transient anorexic state as the decrease in hunger after an exercise bout appears to be short lived (26). Exercise is also implicated in modifying subsequent EI through alterations in hunger and/or appetite and regulatory peptides, both at the short- and long-term signaling levels (18). The regulation of energy balance (feeding, EI, and EE) involves an intricate interplay between central nervous system (CNS) and various organs involved in energy homeostasis (32). Several peptides released by peripheral tissues, interact with specific brain areas, stimulating or inhibiting neurons to release anorexigenic or orexigenic neuropeptides that are involved in the control of eating behavior and EE pattern (27). The peripheral signals can be divided in 2 major categories: 1) the adiposity signals,
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such as leptin, which are involved in the long-term regulation of energy balance, acting directly in response to alterations in body fatness, and 2) gut hormones such as peptide YY (PYY), which comprises signals of satiety and hunger and are released between and during meals, involved in the acute control of feeding behavior. The negative energy balance produced by exercise bouts may also stimulate compensatory eating behaviors (eg, hunger, food intake, and appetite; 9), which, in turn, could offset the exercise-induced energy deficit altering its effects on weight loss (16). A few studies have shown that aerobic exercise resulted in no detectable acute increase in EI in obese children (21) and adolescents (5). However, others have shown that high intensity exercise leads to a pronounced reduction in 24-hr EI in obese adolescent boys (31). In normal weight children Bozinovski et al (2) demonstrated that exercise at VT promoted increase in subjective appetite and desire to eat, without changes on EI after exercise sessions. In obese boys, Tamam et al (30) reported an increase in subjective satiety without apparent EI compensation in response to a single bout of exercise at VT intensity. The changes in EI following exercise may be, at least in part, dependent on changes in circulating satietyregulating peptides such as leptin and peptide YY (PYY; 12). However, little is known about the acute effects of exercise at VT intensity on food intake and these appetite regulatory peptides in obese adolescents. The primary aim of this study was to examine the effects of aerobic exercise on subjective hunger feelings, long-term and short-term satiety signals (leptin and PYY3–36), and the 24-hr EI in obese adolescents.
Material and Methods The study protocol was approved by the ethical committee of the University of Pernambuco (#154/09) and informed consent was obtained from all volunteers and/ or their parents. After baseline measurements we implemented a randomized controlled crossover design for the 2 experimental protocols described below. From 15 initially screened for the study, nine tightly controlled obese teenage girls with the following inclusion criteria were recruited through the outpatient clinic of the University of Pernambuco/Brazil for this study: age: 13–18 years, pubertal stage: Tanner 3–4, obesity: BMI > 95th (4) and absence of hypertension and/or other complications (metabolic, respiratory or genetics).
Figure 1 — Experimental design. VAS = visual analog scale.
In this crossover study design, the participants underwent 2 experimental conditions in a randomized order: 1) control (volunteers remained seated for 150 min) and 2) exercise (volunteers exercised on a treadmill for 30 min at a target intensity corresponding to VT and then remained seated for 120 min, after the conclusion of the of exercise session, or150 min from baseline). During the exercise session energy expenditure was measured by indirect calorimetry. During the first visit, anthropometry, body composition, and pubertal stage were measured and the participants underwent a maximal incremental test to determine VT. On the other visits, volunteers arrived at the laboratory around 7 AM after an overnight fast. They were asked to avoid moderate to vigorous PA for 48 hr before the experimental sessions. All participants were given a 350 kcal standard snack (composed of 61.7% carbohydrates, 13.44% proteins and 24.86% lipids), to minimize potential differences in the thermic effect of food (TEF) between participants. At 7:30 AM, participants followed the experimental protocols (control or exercise) in a randomized and counterbalanced order. All experiments were conducted in a temperature-controlled room (21–23 °C) and at the same time of the day. Subjective hunger feelings and the concentration of hormones were assessed at baseline, immediately after the session (30 min) and after 2 hr of passive recovery (150 min). In addition the 24-hr EI was estimated from the 24-hr recordings of food and beverage intake, which began immediately after the completion of the study or the 150 min measurement. Figure 1 depicts the overall experimental protocol. Obese adolescents were weighed wearing light clothing and without shoes on a Filizola scale (Model 160/300, Brazil) to the nearest 0.1 kg. Height was measured to nearest 0.5 cm by using a wall-mounted stadiometer Filizola (Model 160/300, Brazil). Body mass index (BMI) was calculated by dividing body weight (kg) by squared height (m2). Body composition was determined by bioelectrical impedance (Byodinamics A-310 body composition analyzer) under standardized conditions and the participants were asked to avoid consumption of caffeine and other dehydrating agents at least 24 hr before the test and all tests were performed in the fasted condition. Each participant was given drawings of the 5 stages of breast and pubic hair development. In an isolated room, the adolescents were asked to look at the drawings, read the descriptions, think about how they looked in compari-
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Exercise and Satiety Regulating Hormones 465
son with the drawings, and pick the 1that most closely resembled them; in case of a mismatch, pubic hair was used to determine the pubertal stage (6). Oxygen uptake (VO2) was measured directly in an open circuit respiratory metabolic system (Quark PFT, Cosmed, Italy), during a continuous incremental test on a treadmill (Cosmed T200, Italy). The initial load was set at 3 kph (warm up 3 min) and increased 1km/h each minute until exhaustion, inclination was kept constant at 1% (20). The termination criteria were volitional fatigue, Borg scale and gas exchange ratio higher than 18 and 1.15, respectively (15). The greatest VO2 obtained before test interruption was considered as VO 2peak. Before each test, the instruments were calibrated for gas composition and volume following manufacturers’ recommendations. VT was determined as the point at which there was a systematic increase in VE/VO2 without a corresponding increase in VE/VCO2, by 2 independent researchers. Participants were asked to complete a validated visual analog scale (VAS) to rate hunger (10). The questionnaire consisted of 6 visual analog scales to rate hunger, fullness, desire to eat, how much you can eat now, urge to eat and preoccupation with thoughts of food. The VAS consisted of horizontal lines of 100 mm with defined marks at each extremity that portrayed the expressed desire to eat excessively in the right extremity and the lack the desire to eat or not hungry in the left extremity. VAS was measured by hand, from left (minimum score of 0 cm) to right (maximum score of 10 cm). Each subject recorded all food and beverage consumed for 24 hr from the time when the study was completed (150 min measurement) and they left the laboratory (around 10 AM). A dietitian taught the parents and the adolescents upfront how to record food consumption. They were asked to measure portions in terms of familiar volume and size and by reference to an atlas of local food portions supplied to them. To minimize accuracy bias, the volunteers documented on a sheet what they ate and drank at the time of consumption. All dietary data were transferred to a computer by the same dietitian and EI (Kcal/day) and nutrient intake (carbohydrate, fat and protein) were analyzed using Nutwin software for Windows (Federal University of São Paulo—Paulista Medicine School, 2002) based on Western and local food tables. Blood samples were taken from anticubital vein at baseline, 30 and 150 min. Serum was separated by centrifugation and stored in a deep freezer at –80 °C until analysis. Serum leptin and PYY3–36 were measured by specific enzyme-linked immunosorbent multiplex panel assay kits (Lincoplex-Millipore Corporation, USA; assay sensitivity-leptin [157.2 pg/ml] and PYY [8.4 pg/ml]) using a Luminex system. The multiplex panel kits were developed with polystyrene microspheres with fluorescent dye that acted as both the identifier and the solid surface to build the immunoassay. Data analysis was performed using Statistical and SPSS for Windows. Data are expressed as mean ± SD, and
magnitude of change in percentage (Δ%). Trials (control vs exercise) and time points (basal, 30 min and 150 min) were compared using 2-way ANOVA for repeated measures with Duncan test as post hoc. Difference in 24 hr EI was assessed by paired Students t test. In addition, the effect size was calculated and is displayed when it was moderate (>0.30), as proposed by Cohen (3). Significance was set at p < .05. No order effect was noticed for any of study variables.
3. Results Table 1 summarizes the characteristics of the participants. The intensity of exercise during the session was 68.43 ± 8.31% of the VO2peak and the energy expenditure was 350 ± 15.34 Kcal. Baseline values of hunger scores, EI, leptin, and PYY3–36 were similar between control and exercise conditions (Figure 2 and 3). An interaction effect was observed for hunger (p = .012), indicating that after the control condition the participants’ hunger scores steadily increased from 0.63 ± 0.07 cm to 1.27 ± 0.38 cm at 30 min and 2.30 ± 0.89 cm at 150min, whereas it remained unaltered after the exercise condition (0.90 ± 0.08cm, 1.04 ± 0.08cm, 1.30 ± 0.06cm, for baseline, 30 min and 150 min respectively; Figure 2). In addition, hunger scores at 150 min were significantly higher in the control condition compared with exercise session (p = .01). An interaction effect was observed for leptin (p = .048), indicating that it decreased from 45.8 ± 18.0 ng/ dl to 41.6 ± 16.3 ng/dl at 30 min and 39.4 ± 15.6 ng/dl at 150 min in control condition, whereas it did not change after exercise condition (44.1 ± 15.2 ng/dl, 47.1 ± 20.1 ng/dl and 44.9 ± 17.4 ng/dl, for baseline, 30 min, and 150 min respectively; Figure 3). With respect to PYY3–36, the exercise condition resulted in a significant increase at 30 min (from 54.3 ± 22.9pg/ml to 72.4 ± 20.5pg/ml, which eventually tapered off after 150 min (59.3 ± 15.9 pg/ml; condition effect = 0.019; time effect = 0.031; interaction = 0.0117; Figure 3). However, similar changes were not observed in the Table 1 Participant Characteristics Variables
Mean (SD)
Age (y)
14.90 (1.14)
Body weight (kg)
86.70 (11.10)
BMI (kg/m2)
33.74 (4.03)
BMI percentile
97.78 (0.66)
Fat mass (%)
39.87 (5.40)
VO2peak (ml/kg/min–1) VO2peak at VT
(ml/kg/min–1)
28.25 (1.83) 19.34 (2.80)
Note. BMI= body mass index; VO2peak = peak oxygen uptake represented as ml of oxygen per kg of body mass per min; VT = ventilatory threshold.
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Figure 2 — Effects of exercise at ventilatory threshold on hunger feelings in obese teenage girls. *Denotes significant difference vs. basal; #Denotes significant difference vs. 30 min; ¥Denotes significant difference vs. control.
Figure 3 — Effects of exercise at ventilatory threshold on leptin and PYY3-36 levels in obese teenage girls. *Denotes significant difference vs basal; #Denotes significant difference vs. 30 min.
control condition (63.5 ± 17.3pg/ml, 71.6 ± 16.2 pg/ml, 61.8 ± 8.9 pg/ml, for baseline, 30 min, and 150 min, respectively). The Δ% increase in hunger scores in the control condition was almost 100% and 275% from baseline to 30 min and 150 min respectively. Interestingly, the Δ% increase in hunger scores in the exercise condition was only 13% from baseline to 30 min (nonsignificant; p > .05), but it increased by 139% from baseline to 150 min (p = .01). With regard to the regulatory peptides, the largest Δ% changes were observed after the exercise condition compared with control. The Δ % changes in leptin were 4.33% (p = .05) and 3.36% (p = .01) from baseline to 30 min and 150 min respectively. The corresponding changes for the control condition were –8.43% and –13.45% respectively. In the case of PYY3–36, Δ% increase in the exercise condition by 61% at 30 min (p = .04) and 35.36% at 150 min (p = .15). The corresponding Δ% changes in PYY3–36 for the control condition were 15.94% and 4.28% (both nonsignificant) respectively. The effect of exercise on energy and macronutrient intake is summarized in Table 2. Despite the absence of changes in the 24 hr EI and macronutrient intake between protocols, the results show a high effect size for carbohydrate intake after the exercise bout (d = 2.14); and a modest effect size in protein intake after exercise (d = 0.61) compared with the control session.
Table 2 Effects of Exercise at Ventilatory Threshold on Energy and Macronutrient Intake in Obese Teenage Girls TEI (Kcal/day)
Control
Exercise
p
1526+ 510
1626+ 300
.21
CHO (g/day)
192± 52
346± 108
.47
LIP (g/day)
55± 31
50± 23
.47
Protein (g/day)
80± 30
108± 68
.16
Note. TEI= total energy intake, CHO= carbohydrates, LIP= lipids.
Discussion The present study indicates that exercise performed at VT intensity elicits a transient anorexic effect in obese adolescent girls. Such notion is based on the following findings: (I) an acute increase in PYY3–36, in response to the exercise session and (II) a lack of increase in subjective hunger scores in response to the exercise session. Interestingly, the participants in the control session showed a precipitous increase in subjective hunger scores, but no appreciable change in PYY3–36. Further, the concentration of leptin, remained unaltered by the exercise session. The subjective hunger scores were remarkably lower in the exercise session compared with the control session, both
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Exercise and Satiety Regulating Hormones 467
at 30 min and after 150 min from baseline. The magnitude of changes in PYY3–36 observed in the current study suggests its potential role in the regulation of exercise-induced anorexia in obese adolescent girls, but this observation warrants further exploration in carefully conducted larger studies. It also appears that the anorexic effect was, at least in part, reversed by a compensatory increase in carbohydrate and protein intake over the 24 hr after the completion of the study or the 150 min measurement. The impact of exercise on subsequent EI and satiety signals in obese children and adolescents remains poorly understood, partly because of methodological limitations to address these issues (31). A recent study suggests that high intensity acute exercise reduces the neuronal brain response in food reward regions, potentially leading to decrease food intake (8). Another study in rodents (25) demonstrated aerobic exercise induced improvements in the central action of certain satiety-regulating hormones, thus contributing to appetite suppression. Likewise, certain studies suggest that aerobic exercise increases leptin receptor binding and leptin gene expression in the arcuate nucleus (14, 24). Systemic administration of PYY3–36 has also been shown to inhibit food intake in humans (29) and experimental animals (22). Gastric bypass patients demonstrated increased levels of PYY and that inhibition of the PYY responses resulted in the return of appetite and increased food intake (17). In our study, the concentration of the long-term satiety signal leptin was maintained, whereas the short-term satiety signal, PYY3–36, increased acutely after the exercise session. Previously Dood et al (5) demonstrated that both lean and overweight girls undergoing exercise at 75% VO2max did not alter daily EI, contrary to a decrease in EI in obese boys after high intensity exercise sessions observed by Thivel et al (31). Nemet et al (23) reported higher EI in obese and overweight children following exercise compared with a control session. These conflicting observations are intriguing, but the exact reasons are not clear. A variety of factors might have contributed to the conflicting data in different studies. One potential contributing factor may be related to the sample cohort and the difference in their maturity stages. While Nemet et al (23) studied early-pubertal stage children, our study was confined to adolescents. Potential differences in the exercise intensity and duration and limitations and/or differences in the methodologies used in the measurement of hunger feelings and EI such as prefixed meals, ad libitum meals, and food diaries are less sophisticated. Total EI as well as macronutrient content, consumption and timing may also have influenced the outcomes. Taken together, a comprehensive assessment that includes serial, quantifiable measures of hunger and food intake in addition to questions regarding other factors that can affect food intake is necessary (23). In the current study, carbohydrate and protein consumption tended to increase after the exercise session. The exact mechanisms are not readily available from the current study. However, reduced catecholamine and GH response to exercise compared with normal weight
controls have been reported in obese adolescents. This suggests reduced CHO and lipid energy sources for exercise and presumably greater need for proteins as an energy source. This may explain, in part, the increase in protein intake, potentially promoting muscle recovery (7,28). Of note, most previous studies that have assessed the effects of exercise intensity on energy balance have used relative exercise intensity based on maximum oxygen uptake (VO2max) or maximum heart rate, assuming that it would decrease the variability of the physiological response. This normalization process may not be the most appropriate method since individuals could show different metabolic, cardiovascular, and hormonal changes during exercise at the same relative VO2max or maximum heart rate (11). The use of the anaerobic threshold (AT) to normalize exercise intensity likely reduces variability between participants (1). One of the methods available to identify the AT is the VT. Although the study included both short-term and long-term satiety signals such as PYY3–36 and leptin respectively, we were unable to include other circulating satiety-regulating peptides such as ghrelin, insulin, and GLP-1. Further the insulin resistance status is not available in the participants. Future studies including these factors in a larger population may shed light on the underlying mechanisms and allow generalization of these findings. The use of self-reported food intake records for the quantification of energy intake has limitations and hence the data should be considered cautiously. Although the participants in the study were asked to avoid consumption of caffeine and other dehydrating agents at least 24 hr before the test and all tests were performed in the fasted condition, we cannot rule out potential overestimation of body fat by BIA, which is likely to be influenced by the hydration level. The small sample size is a potential limitation of the study, but the relatively homogeneous group of participants (see Table 1) and the randomized crossover design of the study rendered strength to the analysis of data. In conclusion, our data suggest that aerobic exercise performed at ventilatory threshold acutely evokes a transient anorexia state in obese adolescent girls. The exercise session, while not decreasing the hunger scores, does not appear to increase it. The clinical implications of this observation appear to be important. This exerciseinduced transient anorexia, if suitably modulated, can have important implications in weight maintenance and/or reduction in obese children. Additional research is warranted in larger populations using sophisticated approaches to determine the optimum dose of exercise (exercise duration, intensity, and time of the day) needed to inhibit hunger and compensatory eating behavior, thus facilitating a net negative energy balance in obese adolescents, helping these children in their fight against obesity. Acknowledgments We would like to thank the National Council for Scientific and Technological Development and the Foundation for Science
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and Technology of the State of Pernambuco (FACEPE) for financial support and Raphael M. Ritti-Dias for the support on data interpretation. Special thanks to patients and their parents for the participation in this study. The authors declare no conflicts of interest.
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