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Intensive exercise: A remedy for childhood obesity?
Physiology & Behavior 102 (2011) 132–136
Contents lists available at ScienceDirect
Physiology & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p h b
Intensive exercise: A remedy for childhood obesity? David Thivel a,b,c,⁎, Laurie Isacco a, Sylvie Rousset b,c, Yves Boirie b,c, Béatrice Morio b,c, Pascale Duché a a b c
Clermont Université, Université Blaise Pascal, EA3533, UFR STAPS, BP 104, F-63000 Clermont-Ferrand, France INRA, UMR1019 Nutrition Humaine, CRNH Auvergne, F-63120 Saint-Genès-Champanelle, France Université Clermont 1, UMR1019 Nutrition Humaine, UFR Medicine, F-63000 Clermont-Ferrand, France
a r t i c l e
i n f o
Article history: Received 13 April 2010 Received in revised form 5 October 2010 Accepted 15 October 2010 Keywords: Intensity Exercise Energy balance Obesity
a b s t r a c t Background: Acute exercise can affect the energy intake regulation, which is of major interest in terms of obesity intervention and weight loss. Objective: To test the hypothesis that intensive exercise can affect the subsequent energy intake and balance in obese adolescents. Design: The study was conducted in 2009 and enrolled 12 obese pubertal adolescents ages 14.4 ± 1.5 years old. Two exercise and one sedentary sessions were completed. The first exercise (EX1) and sedentary session (SED) were randomly conducted 1 week apart. The second exercise session (EX2) was conducted following 6 weeks of diet modification and physical activity (3 × 90 min/week) to produce weight loss. Energy intake was recorded, subjective appetite sensation was evaluated using Visual Analogue Scales and energy expenditure was measured using ActiHerats during EX1, EX2 and SED. Results: Total energy intake over the awakened period was significantly reduced by 31% and 18% during the EX1 and EX2 sessions compared with the SED session, respectively (p b 0.01). Energy balance over the awakened period was negative during EX1, neutral during EX2 and positive during SED. There was no significant difference in terms of subjective appetite rates between sessions during the awakened hours. Conclusions: Intensive exercise favors a negative energy balance by dually affecting energy expenditure and energy intake without changes in appetite sensations, suggesting that adolescents are not at risk of food frustration. © 2010 Elsevier Inc. All rights reserved.
1. Introduction Obesity in childhood and adolescence is becoming a major public health concern and anti-obesity treatments led to an array of diverse efforts aimed at promoting healthful eating and physical activity. Low-to-moderate continuous exercises (≤60% of maximal capacities) are most of the time prescribed, targeting for instance the Lipoxmax point [1] (maximal lipid oxidation point) to enhance fat mobilization and oxidation and then induce fat depots reduction. This exercise intensity has been situated in obese children between 37 and 50% of their maximal aerobic capacities [2,3]. However, such programs have shown limited persistence over time with patients experiencing weight regain within few weeks (8% obese and 30% overweight children and adolescents by the end of the intervention and respectively 60% and 36% 18 months later [4]). Moreover, low-tomoderate intensities only affect energy expenditure whereas intensive work loads (≥65% of maximal capacities) affect both energy expenditure and intake. Indeed in addition to its effectiveness in using
⁎ Corresponding author. INRA, UMR1019 Nutrition Humaine, CRNH Auvergne. E-mail address: [email protected] (D. Thivel). 0031-9384/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2010.10.011
carbohydrates that are then not stored by adipocytes as triglycerides, and for altering body composition in obese [5,6], intensive exercise can also induce anorexia associated to decreased hunger sensation [7]. Prescribing intensive exercise could then facilitate negative energy balance with decreased appetite, which could reduce the difficulties experienced by obese patients during energy restriction. Most studies interested in the relationships between exercise intensity and subsequent energy intake have been conducted in healthy adults [8–10] and few in obese [11]. Data are then required for the most vulnerable population for which prevention and treatment of obesity is of public health concern, i.e., obese children and adolescents. The aim of this study was therefore to determine in obese adolescents, whether intensive exercise can favor a negative energy balance through its impacts on energy intake. 2. Subjects and methods 2.1. Subjects Twelve healthy pubertal obese adolescents (14.4 ± 1.5 years old; 7 girls and 5 boys; Tanner stages 3–4) attending a specialized Children Medical Center (Romagnat, France) were recruited in collaboration
D. Thivel et al. / Physiology & Behavior 102 (2011) 132–136
with the Clermont-Ferrand University Pediatric Department. Body mass was measured to the nearest 0.05 kg with a digital scale (Seca model 873 Omega, Germany). Height was measured with a standing stadiometer and recorded with a precision of 1 mm. Body mass index (kg.m-2) was calculated as body weight divided by height squared, and used to assess for obesity [12]. They were not suffering from any diagnosed diseases. 2.2. Methods The experimental design was given approved by the relevant French authorities (CPPAU814). Information on the objective of the trial was provided to the adolescents and their parents and signed written informed consent obtained from both. Anthropometric measurements and body composition (Dual-Xray absorptiometry, Hologic QDR 4500, Bedford, MA, USA) were assessed and volunteers were asked to complete a graded exhaustive cycling exercise to obtain their maximal oxygen uptake (VO2max). Thereafter two exercise and one sedentary sessions were completed. The first exercise (EX1) and sedentary session (SED) were randomly conducted 1 week apart. The second exercise session (EX2) was conducted following 6 weeks of healthy education, dietary restriction and training with low-intensity activities to produce weight loss. For each session, participants spent one complete day and one night into the Center. Body composition and VO2max were also assessed before EX2. The protocol is presented in Fig. 1. 2.3. Maximal exercise testing VO2max was measured during graded exhaustive cycling tests performed at least 1 week before experimental sessions. The initial power of 30 W was maintained during 3 min and followed by 15 W increments every 1.5 min. Children were strongly encouraged by experimenters throughout the test to perform a maximal effort. Criteria for the achievement of VO2max were subjective exhaustion with heart rate above 195 beats.min−1 and/or respiratory exchange ratio (RER, VCO2/VO2) above 1.02 and/or a plateau of VO2 [13]. An electromagnetically braked cycle ergometer (Ergoline, Bitz, Germany) was used to perform the test. VO2 and VCO2 were measured breathby-breath through a mask connected to O2 and CO2 analyzers (Oxycon Pro-Delta, Jaeger, Hoechberg, Germany). Calibration of gases analysers was performed with commercial gases of known concentration. Ventilatory parameters were averaged every 30 s. ECG was monitored for the duration of tests. 2.4. Session design From 0730h am to 0930h pm, adolescents were asked to carry out sedentary activities (computer-video games, reading…). 2.4.1. Food intake 0830h am, a standardized breakfast was offered (2.1 MJ). Ad libitum buffet meals allowing free access to food and respecting the adolescents’ taste were offered at 1215h and 0700h pm. At each meal food was presented in excess of expected consumption. Participants were told to eat until satisfied and that additional food was available if desired. Participants were to the extent possible not overtly informed Inclusion VO2max DXA
VO2max SED*
DXA
EX1*
133
that the real purpose of the protocol was to assess feeding responses. Food consumption was weighed and recorded by investigators (Bilnut-4 software SCDA, Nutrisoft, France) to calculate total energy intake (TEI). 2.4.2. Rating of appetite At regular intervals from 0730h am until the next morning, participants were asked to rate their hunger, fullness and desire to eat (prospective-consumption) using visual analogue scales (VAS) that have presented satisfactory reliability [14]. 2.4.3. Estimation of energy expenditure Energy expenditure was estimated from 0730h am to 0930h pm, using the Actiheart-technology (Cambridge Neurotechnology Ltd, Papworth, UK). Advanced energy expenditure configuration was chosen to obtain detailed records, using a 30-s epoch setting. Total (TEE)- and activity (AEE)-related energy expenditure were determined over the awakened period (14h from 0730h am), for the morning (0730ham–1200h) and the afternoon (1200h–0930hpm). This technology using accelerometry and heart rate has been previously validated and detailed [15]. 2.4.4. Experimental sessions Between 1100h and 1145h, adolescents were asked either to remain sedentary (SED) or to perform 30 min (3 × 10 min, 2-min rest) of an acute exercise on a cycle-ergometer at 70% of their individual VO2max (EX). Heart rate monitoring (Polar.Inc-RS800CX Multi) was used to set intensity. The exercise intensity was also controlled thanks to the work load corresponding to 70% VO2max using the maximal oxygen uptake test results, that was applied to the ergometer. 2.4.5. Energy balance Energy balance was calculated as the difference between TEI and TEE (0730h am to 0930h pm), i.e., during the awakened period (14 h). 2.4.6. Weight loss intervention After the SED and EX1 sessions, adolescents were enrolled in a 6week weight loss program combining healthy lifestyle and dietary education and physical training. They trained 3 times a week for 90 min using low-intensity exercises in a children medical center. Low intensities were chosen to facilitate the adolescents’ participation in the longer term and improve their adherence to the program. The dietary restriction was set individually. After an initial dietary assessment in order to define the total amount of calories consumed per day, the dietary program was set at −500 kcal/day below the initial dietary records. It was composed of 15% proteins, 55% carbohydrates and 30% lipids. The dietary education was conducted by a nutritionist while the exercise sessions were programmed and supervised by a physical trainer used to work with obese youths. 2.5. Statistical analyses Analyses were performed using Statview 5.0 (SAS Institute, Inc., NC, USA). Results are expressed as mean ± standard deviation. The effect of the experimental sessions (SED, EX1, EX2) on EI, expenditure and energy balance was analyzed using one-way ANOVA with repeated measures. The effect of exercise interventions on appetite was examined using 2-way ANOVA with repeated measures. Bonferroni test was used for post-hoc analyses. Level of significance was set at 5%.
EX2
3. Results 6 weeks of intervention * SED and EX1 were realised in a randomized order
Fig. 1. Chronological presentation of the protocol.
Mean fat mass was 38.7 ± 3.3% and BMI 35.1 ± 7.6 kg.m². The 6week intervention conducted to a significant 3% weight loss (from 96.1 kg to 92.7 kg). The 3 × 10 min of intermittent exercise at 70%
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D. Thivel et al. / Physiology & Behavior 102 (2011) 132–136
VO2max generated a mean energy expenditure of 1.25 ± 0.12 MJ. Participants’ VO2max did not significantly change after the 6 weeks of intervention.
higher during the EX sessions than during SED (p b 0.001). In the afternoon, AEE (EX1: 1.75 ± 0.52; EX2: 1.73 ± 0.88; SED: 1.87 ± 1.12 MJ) and TEE (EX1: 5.66 ± 1.06; EX2: 5.49 ± 0.92; SED: 5.77 ± 1.33 MJ) were similar between all sessions.
3.1. Energy expenditure
3.2. Energy intake
TEE over the awakened period was 9.8% and 5.9% higher during EX1 and EX2 compared with SED respectively, but the difference did not reach the level of significance (Fig. 2A). In the morning, AEE (EX1: 1.37 ± 0.32; EX2: 1.30 ± 0.47; SED: 0.55 ± 0.19 MJ) and TEE (EX1: 3.29 ± 0.43; EX2: 3.13 ± 0.67; SED: 2.37 ± 0.31 MJ) were significantly
TEI over the awakened period was significantly reduced by 31% and 18% during the EX1 and EX2 sessions compared with the SED session, respectively (p b 0.01) (Fig. 2B). This was mainly due to significant reductions in EI during diner following EX compared with the SED situation (SED: 3.07 ± 0.5; EX1: 2.18 ± 0.4. EX2: 2.19 ± 0.5 MJ; p b 0.001). EI during lunch tended to decrease during EX compared to SED, but the level of significance was not reached. 3.3. Energy balance Energy balance over the awakened period was negative during EX1, neutral during EX2 and positive during SED (Fig. 2C). It was 2.07 and 1.39 MJ lower during EX1 and EX2 sessions compared with SED respectively (p b 0.01). 3.4. Rating of appetite There was no significant difference in terms of subjective appetite rates between sessions during the awakened hours (Fig. 3, ANOVA: ns). The same results were obtained concerning hunger sensation and prospective food consumption. 4. Discussion
Fig. 2. Differences in (A) total energy expenditure (TEE), total energy intake (TEI) (B), and energy balance (C) between sedentary (SED) and exercise (EX1 and EX2) sessions. The part B of the figure also exposes the energy intake repartition between the standard breakfast and the ad libitum lunch and dinner times. (*p b 0.05; **p b 0.01; ns: no significance).
Our major finding was that in obese adolescents, a single bout of intermittent intensive exercise by the end of the morning can lead to a substantially significant lower EI during the subsequent ad libitum meals, i.e., both at lunch and dinner time, without modification of appetite or hunger. To our knowledge, this is the first study that demonstrates the relevance of using high intensity exercise to induce a spontaneous decrease in EI in obese adolescents. In addition, our study evidenced that the positive effect of high intensity exercise on EI is maintained after 6 weeks of dietary and physical activity handling. This underlines the possible effectiveness of intensive exercises for creating a negative energy balance in obesity treatment. Compared to healthy counterparts, overweight adults have been presented as less likely to increase their food consumption after an elevation of energy expenditure due to exercise [16] but no one observed any decrease in EI. A previous study involving lean and obese females reported no difference in acute EI between the two populations after acute exercise [17]. Only one study attempted to explore the relationships between intensive exercise and subsequent EI in lean and overweight children [18]. Those children were asked to cycle at 75%VO2peak, twice a day for two days. For 1 day, the two exercises elicited an increase in energy expenditure similar to our conditions, i.e., 1.5 MJ. Food intake was analyzed over 5 days. The authors missed to observe any EI modification suggesting that the duration of exercise may be important to induce changes in subsequent EI. Indeed, children in our study had to exercise for 30 consecutive min, whereas those from Dodd and collaborators’ study exercised about 15 min in the morning and 15 min in the afternoon. In addition, our results demonstrate that the impact of an exercise intervention is more efficient 7 h after the exercise bout. This suggests an adaptive time interval of the EI regulation after an acute exercise. This is moreover maintained and even more pronounced during EX2. The present study did not include blood collection. However, our results may reflect the effect of acute exercise on some of the anorexigenic gastric peptides such as glucagon-like peptide 1 [19,20], cholecystokinine [21,22] and pancreatic polypeptide [10,23] that are
D. Thivel et al. / Physiology & Behavior 102 (2011) 132–136
135
Fig. 3. Subjective appetite was not significantly altered between the sedentary (SED) and the exercise (EX1 and EX2) sessions using Visual Analogue Scales (VAS).
increased following exercise. Authors have effectively described the role of gastric signals in the short-term regulation of the energetic balance [24,25]. The role of leptin, as an anorexigenic factor initiated by adipose tissue, is unlikely to explain the lower EI observed during EX1 compared with SED. Indeed, leptin has been shown to fluctuate after physical activity only during a weight loss stage [26], which was not the case in the present sample at EX1. Moreover, according to the recent writings from Borer, meal-to-meal feedings, appetite and spontaneous physical activity operate in a nonhomeostatic way, whereas insulin and leptin respond to short-term fluctuations in energy availability and bear no relationship to human appetite [27]. The importance of exercise intensity in the regulation of food intake may also involve the increased lactate concentration that follows intensive exercising. A recent animal study from Cha and Lane [28] evidenced the involvement of lactate metabolism in the regulation of food intake. The authors showed that intraperitoneal or intracerebroventricular injections activate the enzyme acetyl-CoA carboxylase [29]. The resulting higher malonyl-CoA level in the hypothalamus has been associated to changes in the expression level of orexigenic and anorexigenic neuropeptides, switching from orexigenic to anorexigenic actors and leading to suppression of food intake [29,30]. Lactate being a serious indicator of exercise intensity, it may therefore be considered as a major mediator between intensive exercise and subsequent EI. Those mechanisms have been drawn thanks to injection studies in animals and further investigations are required to isolate whether or not exercise-induced hyperlactatemia can affect the regulation of EI. The present study, whose main limitation is certainly the reduced sample, demonstrates in obese adolescents, that an acute bout of intensive exercise can favor a negative energy balance by dually affecting energy expenditure and EI. It also shows that this negative energy balance is not associated with changes in appetite sensations, suggesting that adolescents are not at risk of food frustration. We therefore advocate the use of intensive exercise as part of obesity treatment, not only for its metabolic implications, but also for its effective impact on EI. Further studies involving more participants are needed to understand the mechanisms and identified the mediators induced by exercise and its intensity, which link peripheral activities to the central regulation of the energy balance. Intervention studies prescribing intensive training should be conducted to observe whether or not it is more efficient in terms of energy balance and appetite feeling compared with lower intensity works. Acknowledgments The authors thank the thermal Institution of Brides Les Bains, France, which supported this project through its 2009 research grant
in obesity prevention and treatment. We are also grateful to all the adolescents that participated and to the Dr. Taillardat, head of the Obesity Department of the Children Medical Center. There is no conflict of interest.
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[21] Sliwowski Z, Lorens K, Konturek SJ, Bielanski W, Zoladz JA. Leptin, gastrointestinal and stress hormones in response to exercise in fasted or fed subjects and before or after blood donation. J Physiol Pharmacol 2001;52(1):53–70. [22] Bailey DM, Davies B, Castell LM, Newsholme EA, Calam J. Physical exercise and normobaric hypoxia: independent modulators of peripheral cholecystokinin metabolism in man. J Appl Physiol 2001;90(1):105–13. [23] Kraemer RR, Castracane VD. Exercise and humoral mediators of peripheral energy balance: ghrelin and adiponectin. Exp Biol Med 2007;282(2):184–94. [24] Hagobian TA, Braun B. Physical activity and hormonal regulation of appetite: sex differences and weight control. Exerc Sport Sci Rev 2010;38(1):25–30. [25] Borer KT, Wuorinen E, Chao C, Burant C. Exercise energy expenditure is not consciously detected due to oro-gastric, not metabolic, basis of hunger sensation. Appetite 2005;45:177–81.
[26] Kraemer RR, Chu H, Castracane VD. Leptin and exercise. Exp Biol Med 2002;227 (9):701–8. [27] Borer KT. Nonhomeostatic control of human appetite and physical activity in regulation of energy balance. Exerc Sport Sci Rev 2010;38(3):114–21. [28] Cha SH, Lane MD. Central lactate metabolism suppresses food intake via the hypothalamic AMP kinase/malonyl-CoA signaling pathway. Biochem Biophys Res Commun 2009;386:212–6. [29] Wolfgang MJ, Cha SH, Sidhaye A, Chohnan S, Cline G, Shulman JI, et al. Regulation of hypothalamic malonyl-CoA by central glucose and leptin. Proc Natl Acad Sci 2007;104:19285–90. [30] Wolfgang MJ, Lane MD. Hypothalamic malonyl-CoA and the control of energy balance. Mol Endocrinol 2008;22:2012–20.
Contents lists available at ScienceDirect
Physiology & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p h b
Intensive exercise: A remedy for childhood obesity? David Thivel a,b,c,⁎, Laurie Isacco a, Sylvie Rousset b,c, Yves Boirie b,c, Béatrice Morio b,c, Pascale Duché a a b c
Clermont Université, Université Blaise Pascal, EA3533, UFR STAPS, BP 104, F-63000 Clermont-Ferrand, France INRA, UMR1019 Nutrition Humaine, CRNH Auvergne, F-63120 Saint-Genès-Champanelle, France Université Clermont 1, UMR1019 Nutrition Humaine, UFR Medicine, F-63000 Clermont-Ferrand, France
a r t i c l e
i n f o
Article history: Received 13 April 2010 Received in revised form 5 October 2010 Accepted 15 October 2010 Keywords: Intensity Exercise Energy balance Obesity
a b s t r a c t Background: Acute exercise can affect the energy intake regulation, which is of major interest in terms of obesity intervention and weight loss. Objective: To test the hypothesis that intensive exercise can affect the subsequent energy intake and balance in obese adolescents. Design: The study was conducted in 2009 and enrolled 12 obese pubertal adolescents ages 14.4 ± 1.5 years old. Two exercise and one sedentary sessions were completed. The first exercise (EX1) and sedentary session (SED) were randomly conducted 1 week apart. The second exercise session (EX2) was conducted following 6 weeks of diet modification and physical activity (3 × 90 min/week) to produce weight loss. Energy intake was recorded, subjective appetite sensation was evaluated using Visual Analogue Scales and energy expenditure was measured using ActiHerats during EX1, EX2 and SED. Results: Total energy intake over the awakened period was significantly reduced by 31% and 18% during the EX1 and EX2 sessions compared with the SED session, respectively (p b 0.01). Energy balance over the awakened period was negative during EX1, neutral during EX2 and positive during SED. There was no significant difference in terms of subjective appetite rates between sessions during the awakened hours. Conclusions: Intensive exercise favors a negative energy balance by dually affecting energy expenditure and energy intake without changes in appetite sensations, suggesting that adolescents are not at risk of food frustration. © 2010 Elsevier Inc. All rights reserved.
1. Introduction Obesity in childhood and adolescence is becoming a major public health concern and anti-obesity treatments led to an array of diverse efforts aimed at promoting healthful eating and physical activity. Low-to-moderate continuous exercises (≤60% of maximal capacities) are most of the time prescribed, targeting for instance the Lipoxmax point [1] (maximal lipid oxidation point) to enhance fat mobilization and oxidation and then induce fat depots reduction. This exercise intensity has been situated in obese children between 37 and 50% of their maximal aerobic capacities [2,3]. However, such programs have shown limited persistence over time with patients experiencing weight regain within few weeks (8% obese and 30% overweight children and adolescents by the end of the intervention and respectively 60% and 36% 18 months later [4]). Moreover, low-tomoderate intensities only affect energy expenditure whereas intensive work loads (≥65% of maximal capacities) affect both energy expenditure and intake. Indeed in addition to its effectiveness in using
⁎ Corresponding author. INRA, UMR1019 Nutrition Humaine, CRNH Auvergne. E-mail address: [email protected] (D. Thivel). 0031-9384/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2010.10.011
carbohydrates that are then not stored by adipocytes as triglycerides, and for altering body composition in obese [5,6], intensive exercise can also induce anorexia associated to decreased hunger sensation [7]. Prescribing intensive exercise could then facilitate negative energy balance with decreased appetite, which could reduce the difficulties experienced by obese patients during energy restriction. Most studies interested in the relationships between exercise intensity and subsequent energy intake have been conducted in healthy adults [8–10] and few in obese [11]. Data are then required for the most vulnerable population for which prevention and treatment of obesity is of public health concern, i.e., obese children and adolescents. The aim of this study was therefore to determine in obese adolescents, whether intensive exercise can favor a negative energy balance through its impacts on energy intake. 2. Subjects and methods 2.1. Subjects Twelve healthy pubertal obese adolescents (14.4 ± 1.5 years old; 7 girls and 5 boys; Tanner stages 3–4) attending a specialized Children Medical Center (Romagnat, France) were recruited in collaboration
D. Thivel et al. / Physiology & Behavior 102 (2011) 132–136
with the Clermont-Ferrand University Pediatric Department. Body mass was measured to the nearest 0.05 kg with a digital scale (Seca model 873 Omega, Germany). Height was measured with a standing stadiometer and recorded with a precision of 1 mm. Body mass index (kg.m-2) was calculated as body weight divided by height squared, and used to assess for obesity [12]. They were not suffering from any diagnosed diseases. 2.2. Methods The experimental design was given approved by the relevant French authorities (CPPAU814). Information on the objective of the trial was provided to the adolescents and their parents and signed written informed consent obtained from both. Anthropometric measurements and body composition (Dual-Xray absorptiometry, Hologic QDR 4500, Bedford, MA, USA) were assessed and volunteers were asked to complete a graded exhaustive cycling exercise to obtain their maximal oxygen uptake (VO2max). Thereafter two exercise and one sedentary sessions were completed. The first exercise (EX1) and sedentary session (SED) were randomly conducted 1 week apart. The second exercise session (EX2) was conducted following 6 weeks of healthy education, dietary restriction and training with low-intensity activities to produce weight loss. For each session, participants spent one complete day and one night into the Center. Body composition and VO2max were also assessed before EX2. The protocol is presented in Fig. 1. 2.3. Maximal exercise testing VO2max was measured during graded exhaustive cycling tests performed at least 1 week before experimental sessions. The initial power of 30 W was maintained during 3 min and followed by 15 W increments every 1.5 min. Children were strongly encouraged by experimenters throughout the test to perform a maximal effort. Criteria for the achievement of VO2max were subjective exhaustion with heart rate above 195 beats.min−1 and/or respiratory exchange ratio (RER, VCO2/VO2) above 1.02 and/or a plateau of VO2 [13]. An electromagnetically braked cycle ergometer (Ergoline, Bitz, Germany) was used to perform the test. VO2 and VCO2 were measured breathby-breath through a mask connected to O2 and CO2 analyzers (Oxycon Pro-Delta, Jaeger, Hoechberg, Germany). Calibration of gases analysers was performed with commercial gases of known concentration. Ventilatory parameters were averaged every 30 s. ECG was monitored for the duration of tests. 2.4. Session design From 0730h am to 0930h pm, adolescents were asked to carry out sedentary activities (computer-video games, reading…). 2.4.1. Food intake 0830h am, a standardized breakfast was offered (2.1 MJ). Ad libitum buffet meals allowing free access to food and respecting the adolescents’ taste were offered at 1215h and 0700h pm. At each meal food was presented in excess of expected consumption. Participants were told to eat until satisfied and that additional food was available if desired. Participants were to the extent possible not overtly informed Inclusion VO2max DXA
VO2max SED*
DXA
EX1*
133
that the real purpose of the protocol was to assess feeding responses. Food consumption was weighed and recorded by investigators (Bilnut-4 software SCDA, Nutrisoft, France) to calculate total energy intake (TEI). 2.4.2. Rating of appetite At regular intervals from 0730h am until the next morning, participants were asked to rate their hunger, fullness and desire to eat (prospective-consumption) using visual analogue scales (VAS) that have presented satisfactory reliability [14]. 2.4.3. Estimation of energy expenditure Energy expenditure was estimated from 0730h am to 0930h pm, using the Actiheart-technology (Cambridge Neurotechnology Ltd, Papworth, UK). Advanced energy expenditure configuration was chosen to obtain detailed records, using a 30-s epoch setting. Total (TEE)- and activity (AEE)-related energy expenditure were determined over the awakened period (14h from 0730h am), for the morning (0730ham–1200h) and the afternoon (1200h–0930hpm). This technology using accelerometry and heart rate has been previously validated and detailed [15]. 2.4.4. Experimental sessions Between 1100h and 1145h, adolescents were asked either to remain sedentary (SED) or to perform 30 min (3 × 10 min, 2-min rest) of an acute exercise on a cycle-ergometer at 70% of their individual VO2max (EX). Heart rate monitoring (Polar.Inc-RS800CX Multi) was used to set intensity. The exercise intensity was also controlled thanks to the work load corresponding to 70% VO2max using the maximal oxygen uptake test results, that was applied to the ergometer. 2.4.5. Energy balance Energy balance was calculated as the difference between TEI and TEE (0730h am to 0930h pm), i.e., during the awakened period (14 h). 2.4.6. Weight loss intervention After the SED and EX1 sessions, adolescents were enrolled in a 6week weight loss program combining healthy lifestyle and dietary education and physical training. They trained 3 times a week for 90 min using low-intensity exercises in a children medical center. Low intensities were chosen to facilitate the adolescents’ participation in the longer term and improve their adherence to the program. The dietary restriction was set individually. After an initial dietary assessment in order to define the total amount of calories consumed per day, the dietary program was set at −500 kcal/day below the initial dietary records. It was composed of 15% proteins, 55% carbohydrates and 30% lipids. The dietary education was conducted by a nutritionist while the exercise sessions were programmed and supervised by a physical trainer used to work with obese youths. 2.5. Statistical analyses Analyses were performed using Statview 5.0 (SAS Institute, Inc., NC, USA). Results are expressed as mean ± standard deviation. The effect of the experimental sessions (SED, EX1, EX2) on EI, expenditure and energy balance was analyzed using one-way ANOVA with repeated measures. The effect of exercise interventions on appetite was examined using 2-way ANOVA with repeated measures. Bonferroni test was used for post-hoc analyses. Level of significance was set at 5%.
EX2
3. Results 6 weeks of intervention * SED and EX1 were realised in a randomized order
Fig. 1. Chronological presentation of the protocol.
Mean fat mass was 38.7 ± 3.3% and BMI 35.1 ± 7.6 kg.m². The 6week intervention conducted to a significant 3% weight loss (from 96.1 kg to 92.7 kg). The 3 × 10 min of intermittent exercise at 70%
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VO2max generated a mean energy expenditure of 1.25 ± 0.12 MJ. Participants’ VO2max did not significantly change after the 6 weeks of intervention.
higher during the EX sessions than during SED (p b 0.001). In the afternoon, AEE (EX1: 1.75 ± 0.52; EX2: 1.73 ± 0.88; SED: 1.87 ± 1.12 MJ) and TEE (EX1: 5.66 ± 1.06; EX2: 5.49 ± 0.92; SED: 5.77 ± 1.33 MJ) were similar between all sessions.
3.1. Energy expenditure
3.2. Energy intake
TEE over the awakened period was 9.8% and 5.9% higher during EX1 and EX2 compared with SED respectively, but the difference did not reach the level of significance (Fig. 2A). In the morning, AEE (EX1: 1.37 ± 0.32; EX2: 1.30 ± 0.47; SED: 0.55 ± 0.19 MJ) and TEE (EX1: 3.29 ± 0.43; EX2: 3.13 ± 0.67; SED: 2.37 ± 0.31 MJ) were significantly
TEI over the awakened period was significantly reduced by 31% and 18% during the EX1 and EX2 sessions compared with the SED session, respectively (p b 0.01) (Fig. 2B). This was mainly due to significant reductions in EI during diner following EX compared with the SED situation (SED: 3.07 ± 0.5; EX1: 2.18 ± 0.4. EX2: 2.19 ± 0.5 MJ; p b 0.001). EI during lunch tended to decrease during EX compared to SED, but the level of significance was not reached. 3.3. Energy balance Energy balance over the awakened period was negative during EX1, neutral during EX2 and positive during SED (Fig. 2C). It was 2.07 and 1.39 MJ lower during EX1 and EX2 sessions compared with SED respectively (p b 0.01). 3.4. Rating of appetite There was no significant difference in terms of subjective appetite rates between sessions during the awakened hours (Fig. 3, ANOVA: ns). The same results were obtained concerning hunger sensation and prospective food consumption. 4. Discussion
Fig. 2. Differences in (A) total energy expenditure (TEE), total energy intake (TEI) (B), and energy balance (C) between sedentary (SED) and exercise (EX1 and EX2) sessions. The part B of the figure also exposes the energy intake repartition between the standard breakfast and the ad libitum lunch and dinner times. (*p b 0.05; **p b 0.01; ns: no significance).
Our major finding was that in obese adolescents, a single bout of intermittent intensive exercise by the end of the morning can lead to a substantially significant lower EI during the subsequent ad libitum meals, i.e., both at lunch and dinner time, without modification of appetite or hunger. To our knowledge, this is the first study that demonstrates the relevance of using high intensity exercise to induce a spontaneous decrease in EI in obese adolescents. In addition, our study evidenced that the positive effect of high intensity exercise on EI is maintained after 6 weeks of dietary and physical activity handling. This underlines the possible effectiveness of intensive exercises for creating a negative energy balance in obesity treatment. Compared to healthy counterparts, overweight adults have been presented as less likely to increase their food consumption after an elevation of energy expenditure due to exercise [16] but no one observed any decrease in EI. A previous study involving lean and obese females reported no difference in acute EI between the two populations after acute exercise [17]. Only one study attempted to explore the relationships between intensive exercise and subsequent EI in lean and overweight children [18]. Those children were asked to cycle at 75%VO2peak, twice a day for two days. For 1 day, the two exercises elicited an increase in energy expenditure similar to our conditions, i.e., 1.5 MJ. Food intake was analyzed over 5 days. The authors missed to observe any EI modification suggesting that the duration of exercise may be important to induce changes in subsequent EI. Indeed, children in our study had to exercise for 30 consecutive min, whereas those from Dodd and collaborators’ study exercised about 15 min in the morning and 15 min in the afternoon. In addition, our results demonstrate that the impact of an exercise intervention is more efficient 7 h after the exercise bout. This suggests an adaptive time interval of the EI regulation after an acute exercise. This is moreover maintained and even more pronounced during EX2. The present study did not include blood collection. However, our results may reflect the effect of acute exercise on some of the anorexigenic gastric peptides such as glucagon-like peptide 1 [19,20], cholecystokinine [21,22] and pancreatic polypeptide [10,23] that are
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Fig. 3. Subjective appetite was not significantly altered between the sedentary (SED) and the exercise (EX1 and EX2) sessions using Visual Analogue Scales (VAS).
increased following exercise. Authors have effectively described the role of gastric signals in the short-term regulation of the energetic balance [24,25]. The role of leptin, as an anorexigenic factor initiated by adipose tissue, is unlikely to explain the lower EI observed during EX1 compared with SED. Indeed, leptin has been shown to fluctuate after physical activity only during a weight loss stage [26], which was not the case in the present sample at EX1. Moreover, according to the recent writings from Borer, meal-to-meal feedings, appetite and spontaneous physical activity operate in a nonhomeostatic way, whereas insulin and leptin respond to short-term fluctuations in energy availability and bear no relationship to human appetite [27]. The importance of exercise intensity in the regulation of food intake may also involve the increased lactate concentration that follows intensive exercising. A recent animal study from Cha and Lane [28] evidenced the involvement of lactate metabolism in the regulation of food intake. The authors showed that intraperitoneal or intracerebroventricular injections activate the enzyme acetyl-CoA carboxylase [29]. The resulting higher malonyl-CoA level in the hypothalamus has been associated to changes in the expression level of orexigenic and anorexigenic neuropeptides, switching from orexigenic to anorexigenic actors and leading to suppression of food intake [29,30]. Lactate being a serious indicator of exercise intensity, it may therefore be considered as a major mediator between intensive exercise and subsequent EI. Those mechanisms have been drawn thanks to injection studies in animals and further investigations are required to isolate whether or not exercise-induced hyperlactatemia can affect the regulation of EI. The present study, whose main limitation is certainly the reduced sample, demonstrates in obese adolescents, that an acute bout of intensive exercise can favor a negative energy balance by dually affecting energy expenditure and EI. It also shows that this negative energy balance is not associated with changes in appetite sensations, suggesting that adolescents are not at risk of food frustration. We therefore advocate the use of intensive exercise as part of obesity treatment, not only for its metabolic implications, but also for its effective impact on EI. Further studies involving more participants are needed to understand the mechanisms and identified the mediators induced by exercise and its intensity, which link peripheral activities to the central regulation of the energy balance. Intervention studies prescribing intensive training should be conducted to observe whether or not it is more efficient in terms of energy balance and appetite feeling compared with lower intensity works. Acknowledgments The authors thank the thermal Institution of Brides Les Bains, France, which supported this project through its 2009 research grant
in obesity prevention and treatment. We are also grateful to all the adolescents that participated and to the Dr. Taillardat, head of the Obesity Department of the Children Medical Center. There is no conflict of interest.
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