Physiology & Behavior 135 (2014) 130–134
Contents lists available at ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Is energy intake altered by a 10-week aerobic exercise intervention in obese adolescents?☆,☆☆ D. Thivel a,⁎, J.P. Chaput a,b, K.B. Adamo a,b, G.S. Goldfield a,b a b
Healthy Active Living and Obesity Research Group, Children's Hospital of Eastern Ontario Research Institute, Ottawa, Ontario, Canada School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada
H I G H L I G H T S • Physical activity program leads to a 10% decreased energy intake in obese youth. • Interventions have to consider potential energy expenditure compensations to physical activity. • Physical activity not only acts on energy expenditure but also intake in obese adolescents.
a r t i c l e
i n f o
Article history: Received 29 April 2014 Received in revised form 20 May 2014 Accepted 12 June 2014 Available online 19 June 2014 Keywords: Energy expenditure Physical activity Energy intake Pediatric obesity
a b s t r a c t Aim: To examine energy intake adaptations to a 10-week aerobic exercise program in obese adolescents. Methods: Twenty-six 12–17 year old obese adolescents were asked to cycle twice a week for an hour in a research laboratory. Body composition, aerobic fitness (submaximal fitness test) and energy intake (3-day food record) were assessed before and immediately after the 10-week intervention. Results: The average time spent pedaling per session was 55.3 ± 12.1 min for a mean energy expenditure of 2196 ± 561 kJ per session. The intervention produced significant improvements in percentage of body fat (44.5 ± 10.6% vs. 43.4 ± 9.8%; p b 0.05) but no significant weight and fat-free mass change. Peak workload (79.5 ± 20.8 W vs. 87.3 ± 17.6 W; p b 0.05) and peak heart rate (174.6 ± 18.7 bpm vs. 166.2 ± 21.0 bpm; p b 0.01) were improved. The mean total daily energy intake (in kJ/day) showed a tendency to decrease through the intervention (7440 ± 1744 to 6740 ± 2124 kJ; p = 0.07) but a high interindividual variability observed in the energy intake response to the intervention may explain the nonsignificant association between the energy intake response and weight loss. Conclusion: A 10-week aerobic exercise program may result in a small decrease in energy intake and an associated decrease in percentage of body fat but no weight loss in obese adolescents. This lack of weight loss could be explained by a decrease in spontaneous energy expenditure outside the intervention sessions. © 2014 Elsevier Inc. All rights reserved.
1. Introduction The alarming progression of pediatric overweight and obesity has led to an array of diverse efforts aimed at promoting healthy eating and physical activity. The understanding and control of energy balance is certainly a key factor in the elaboration of effective recommendations and weight loss strategies. About 50 years ago it was commonly Abbreviations: VO2max, maximal oxygen consumption; BMI, body mass index; EI, energy intake; EE, energy expenditure; EB, energy balance; HR, heart rate; CHO, carbohydrates. ☆ Disclosure: No conflict of interest was declared. ☆☆ Clinical Trial. ClinicalTrial.gov: NCT00983970 ⁎ Corresponding author at: Healthy Active Living and Obesity Research Group, Children's Hospital of Eastern Ontario Research Institute, 401 Smyth Road, Ottawa, Ontario K1H 8L1, Canada. Tel.: +1 613 737 7600x3288; fax: +1 613 738 4800. E-mail address: [email protected] (D. Thivel).
http://dx.doi.org/10.1016/j.physbeh.2014.06.013 0031-9384/© 2014 Elsevier Inc. All rights reserved.
considered that energy consumption was regulated with such flexibility that increasing energy expenditure by exercise automatically led to an equivalent increased energy intake [13]. However, Mayer himself showed that physical activity was not perfectly coupled to food consumption and that a very low level of activity was related to higher caloric intake [14]. Many studies have been conducted during the last decades regarding the effects of acute exercise on the short-term control of appetite and energy intake in adults [3,12]. Although data remain conflicting so far, in lean children and adolescents, acute intensive exercise (N70% of maximal aerobic capacity — VO2max) seems to promote a negative energy balance mainly due to a decreased daily energy intake [19,22,23]. This reduction of the subsequent energy intake is not accompanied by any alteration in appetite sensations, which is consistent with the previously observed uncoupling between appetite feelings and energy intake after exercise in obese adults [3].
D. Thivel et al. / Physiology & Behavior 135 (2014) 130–134
Although acute exercise affects daily energy intake, exercise has to be sustained over time to favor weight loss which questioned the nutritional adaptations to long term exercise. In 2009, Caudwell and collaborators tested the effects of a 12-week physical activity program (approximate energy expenditure of 500 kcal per week) [4]. The authors concluded that physical activity alone was not enough to induce weight loss mainly because of a possible compensatory response to exercise with some patients decreasing their fruit and vegetable consumption and increasing their total energy intake [4]. This increased energy intake with exercise could be explained by the extremely powerful appetite system mechanisms that tend to protect individuals against under-eating and weight loss [2]. Previously published data in obese adolescents showed that a 6-week exercise program increased hunger and decreased fullness but the authors did not assess energy intake [9]. The nutritional (energy intake and appetite) adaptations to an exercise program are of particular interest in terms of weight loss achievement, but show an important inter-individual variability [9,10] with some patients recruiting adaptive mechanisms to oppose the negative or reduced energy balance induced by exercise [17]. To date no data are available examining the possible nutritional adaptations to an exercise program in obese youth. Accordingly, the aim of this study was to test the impact of a 10-week aerobic program on obese adolescents' energy intake and weight loss. Extrapolating from the literature, we hypothesize that adolescents will not show significant changes in energy intake or weight loss in response to the exercise intervention. 2. Methods 2.1. Population This is a secondary analysis of data collected from participants in the GameBike trial [1] where the participants were screened through the Endocrinology Clinic at the Children's Hospital of Eastern Ontario (CHEO; Ottawa, Ontario, Canada) to determine eligibility. Of the 30 overweight/obese 12–17 year old participants that were selected (body mass index (BMI) above the 95th percentile for age and gender according to the Center for Disease Control and Prevention's growth chart data/available from http://www.cdc.gov/growthcharts), 4 dropped out prematurely due to a lack of interest and then 26 adolescents completed the study (14 females and 12 males; 14.5 ± 1.8 years old). The inclusion and exclusion criteria have been previously detailed [1]. The screening and recruitment were done between May 2007 and January 2009 and the last assessments were completed in March 2009. The protocol was approved by the Children's Hospital of Eastern Ontario (CHEO) research ethics board. All the participants and their legal guardians received information sheets and completed consent forms. 2.2. Experimental design After a medical examination, to ensure the adolescents' ability to complete the protocol, their aerobic fitness, anthropometric characteristics, body composition and daily energy intake were assessed before and after a physical activity program. Participants were asked to visit the laboratory twice a week for 60 min for 10 weeks. During these 60minute exercise sessions, the adolescents were asked to cycle while playing video games or listening to music. Although they were asked to stay in the lab for 60 min, they remained free to take breaks or stop cycling when they wanted. During each session, heart rate (HR) was individually monitored by a polar heart rate monitor (Polar S-510, Polar Electro Y, Kempele, Finland) for both safety and research purposes. Estimates of energy expenditure and exercise intensity were measured using the Polar heart rate monitor data, and the distance cycled was assessed by the stationary exercise bike computer system. The energy expenditure estimation was determined by a proprietary algorithm from Polar that takes into account the subject's gender, age, height
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and weight along with heart rate. The intensity at which the adolescents were exercising was evaluated by comparing their theoretical predicted maximal heart rate (using the 220 − age calculation) to their average heart rate during the exercise session. The 220 − age formula was chosen according to the Canadian Health Measures Survey that uses it for measuring submaximal fitness in children and youth [24]. 2.2.1. Anthropometric measurements and body composition A wall-mounted stadiometer (Seca GmBH & Co. Kg., Hamburg, Germany) was used to assess height while body weight and body composition (fat mass and fat-free mass) were assessed using a Tanita (model 300-A) bioelectrical impedance scale (Tanita Corporation of America Inc., Arlington Heights III, USA). Body mass index (BMI) was then calculated as body weight (kg) / height (m)2. All measures were done in duplicate and the means used to resolve any discrepancies in measurements. We controlled for food consumption and hydration by measuring these at baseline and asking that subjects consume the same amount of liquids and food at the same time of day prior to post-intervention assessment. Accordingly, the adolescents were tested at the same time of the day before and after the intervention. It has been previously shown that measures from the Tanita bioelectrical impedance scale and from dual-energy X-ray absorptiometry are highly correlated in overweight and obese youth [7], demonstrating strong concurrent validity. A Seca retractable and locking ergonomic measuring tape (Seca GmBH & Co. Kg.) was also used to measure waist circumference (cm) and each measurement was taken at the midpoint between the floating rib and the iliac crest after a gentle expiration. 2.2.2. Aerobic fitness test Pre- and post-intervention the adolescents had to complete a graded exercise protocol on a cycle ergometer to assess their submaximal aerobic fitness. They were asked to pedal at a constant speed for 3 min at a low work load and then the work load increased every 2 min by 10 W until they reached volitional fatigue. Wattage and heart rate were measured and recorded through the duration of the test. 2.2.3. Energy intake Energy intake was assessed before and right after the 10-week intervention with the use of a 3-day food diary and the energy and macronutrient consumption was analyzed using the online dietary analysis program (www.fitday.com). This program has been shown to be a scientifically valid tool to explore energy intake in children and youth [25]. Prior to the program, the research staff have met individually with the adolescents and their parents and explained precisely how to complete the food records and how to quantify the food consumed (advices concerning the completion of the food diary were also given to the adolescents at the end of the 10 weeks). 2.2.4. Statistical analysis Variables are presented as means ± standard deviations and the level of statistical significance set at p b 0.05. Statistical analyses were conducted using the SPSS software version 19.0 for Windows. Paired t-tests were used to compare baseline and post-intervention values on anthropometric measurements (height, weight, BMI, waist circumference) body composition (fat mass and fat-free mass), physical fitness (peak workload, time to exhaustion, peak heart rate) and energy intake (daily energy consumption and macronutrient intake). 3. Results 3.1. Exercise sessions' characteristics As shown in Table 1, the participants pedaled for an average time of 55.3 ± 12.1 min during the exercise sessions with an average of 33.5 ± 15.3 min spent at moderate to vigorous intensity (60 to 79% peak heart rate) and 19.3 ± 17.4 min at vigorous intensity (80 to 100% peak heart
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4. Discussion
Table 1 Characteristics of the exercise sessions.
Average time pedaled (min/session) Average minutes spent in 60%–79% peak HR Average minutes spent in 80%–100% peak HR Average energy expenditure (kJ)
Mean
SD
55.3 33.5 19.3 2196
12.1 15.3 17.4 561
Data presented as mean ± standard deviation; HR: heart rate.
rate). The estimated energy expenditure per session reached 2196 ± 561 kJ.
3.1.1. Anthropometric measurements, body composition and physical fitness parameters As shown in Table 2, only the height (164.4 ± 6.2 to 165.1 ± 6.6 cm) significantly increased through the 10 weeks (p b 0.05). Participants' weight, BMI and waist circumference and fat-free mass did not significantly differ between baseline and the end of the program (Table 2). Although fat mass expressed in kilograms was not significantly modified by the intervention, it was significantly decreased once expressed as a percentage of total mass (44.5 ± 10.6% to 42.8 ± 9.8%; p b 0.05). The mean weight variation (weight post intervention minus baseline weight) was 1.1 ± 3.6 kg but when considered individually, the adolescents showed an important inter-individual weight loss variability from an 8 kg weight loss to a weight gain of 9.2 kg (Fig. 1A). As previously shown in this specific group of adolescents [1], a training effect was observed with a significant increase of the participants' aerobic fitness indicators. Peak workload (p b 0.05), peak heart rate (p b 0.01) and the time to reach exhaustion (p b 0.05) were all significantly improved by the intervention (Table 2).
3.1.2. Energy intake and macronutrient consumption As shown in Table 3, we observed that daily energy intake tended to be lower after the 10-week aerobic intervention but did not reach statistical significance (difference of 699 kJ; p = 0.07). Daily carbohydrate (CHO) and protein intake did not significantly differ between baseline and the post-intervention assessment while daily fat intake was significantly lower after the aerobic exercise program (difference of 12.2 g). As for Fig. 1A that shows the important inter-individual weight changes' variability, part B of the figure illustrates the energy intake response for each participant. The figure highlights an important variability of the energy intake changes going from − 6070 kJ to + 1108 kJ. Changes in body weight and body fat are not related to the energy intake modifications (as illustrated in Fig. 1 for body weight). Table 2 Effect of the exercise intervention on anthropometric characteristics, body composition and aerobic fitness indicators. Pre-intervention
Height (cm) Weight (kg) BMI (kg/m2) WC (cm) Fat mass (kg) Fat mass (%) Fat-free mass (kg) Peak workload (W) Time to exhaustion (min) Peak heart rate (bpm)
Postintervention
Mean
SD
Mean
SD
164.4 99.2 37.4 113.8 45.5 44.5 54.4 79.5 12.4 174.6
6.2 22.8 9.1 15.4 20.8 10.6 11,7 20.8 1.3 18.7
165.1 100.3 37.5 113.5 46.8 42.8 55.5 87.3 12.9 166.2
6.6 23.4 9.4 15.6 22.4 9.8 11.1 17.6 0.5 21.0
⁎
⁎ ⁎ ⁎ ⁎⁎
Data are presented as mean ± standard deviation; WC: waist circumference; BMI: body mass index. ⁎ p b 0.05. ⁎⁎ p b 0.01.
Although several studies have questioned the impact of acute physical exercise on subsequent nutritional adaptations in obese youth, the present work is the first to directly explore their energy intake response to a long term (10 weeks) physical activity program. According to the present results, exercising twice a week (with a mean pedaling time of 55.3 ± 12.1 min per session) for 10 weeks led to a slight (statistical trend with p = 0.07) decrease in energy intake of about 700 kJ/day (or 10%) in obese youth. In 2007, King and collaborators showed that a 6-week physical activity (skill-based activities) program increased 14-year-old obese adolescents' hunger and decreased their fullness feeling but they did not report any data regarding their caloric intake [9]. It could be argued that this higher hunger sensation found by King et al. is in contradiction with the decreased energy intake observed here. However, this can be explained by the possible uncoupling effect of physical activity on energy intake and appetite feelings, as already underlined after acute exercise in both adults [3] and adolescents [20,22,23]. Although the intervention led to a significant reduction in percent body fat which could be attributed to both the energy expenditure from the physical activity program and a significant decrease in dietary fat consumption, no differences were found in terms of body weight (kg), BMI (kg/m2), fat-free mass or absolute fat mass. Our results are similar to those of Caudwell and colleagues who reported that a 12week physical activity intervention (5 h a week) was not effective in inducing weight loss in obese adults [4]. This lack of weight loss was explained by an important inter-individual variability in the nutritional response to the program [4]. In the present study, the increased energy expenditure induced by the exercise sessions was accompanied by a slight decrease in energy intake which should have favored a negative energy balance and then weight loss. However, when considered individually, the data showed an important inter-individual variability in terms of energy intake response to the program. As already demonstrated by King and collaborators in adults [10], Fig. 1B illustrates the important variability found between adolescents in their energy intake adaptations through the intervention. This figure clearly illustrates the fact that some adolescents did increase their energy consumption while others reduced it, underlying the necessity to consider the highly variable individual nutritional adaptations to exercise interventions. It is important to note, however, that those inter-adolescent differences in terms of energy intake response in our data do not explain the differences observed in terms of weight loss (Fig. 1A). Participants who decreased their food consumption effectively did not have a greater weight loss. This result suggests that other behavioral compensatory responses to the intervention might be responsible for the lack of weight loss. Possible energetic adaptations in other behavioral aspects of energy expenditure may effectively lead to a lower than expected efficacy of exercise in the control of energy balance [5,8]. For instance, Meijer, Westerterp and Verstappen [15] have shown a significant decline (8%) in the number of accelerometer counts per day in adults illustrating a reduction of their spontaneous free-living physical activity level through a 12-week exercise program [15]. Others also reported such a decrease in spontaneous physical activity energy expenditure after prescribed exercise in adults [5,16,26]. Although Fremeaux, Mallam, Metcalf, Hosking, Voss and Wilkin [6] highlighted this compensatory trend in lean children [6], the present results seem to be the first to suggest that such a mechanism exists in obese adolescents. Obese youth have been shown to significantly reduce their spontaneous physical activity energy expenditure after an acute session of intensive exercise [11,18,21,22] but to our knowledge it has never been assessed on a longer term (several weeks of intervention). Looking at the important individual variability observed in terms of energy intake response and at its lack of coherence regarding the absence of weight loss, the presence of potential compensatory mechanisms that lead to a reduced spontaneous physical activity-induced
D. Thivel et al. / Physiology & Behavior 135 (2014) 130–134
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Fig. 1. Individual body weight changes (A) and energy intake changes (B) over the course of the aerobic exercise intervention. Data are presented as mean values (pre–post assessment).
energy expenditure outside the prescribed exercise sessions may be the best explanation for the inefficiency of physical activity alone in inducing weight loss in obese youth. The present study has several limitations. Although the use of a 3day food diary is one of the most common methods for assessing energy intake in the natural environment, it is commonly associated with inaccurate recall, particularly in youth, as is the case with most self-reports of energy balance behaviors, thereby possibly limiting the accuracy of our data (7-day records could have been used but this might be too long to complete and might decrease the accuracy of the results, particularly in adolescents). The absence of indication regarding the appetite feelings as well as objective measurement of energy expenditure through accelerometers in free living conditions are additional limitations that need to be addressed in future research. Despite these limitations, the current study makes an important contribution to the
Table 3 Baseline and post-intervention energy intake and macronutrient intake.
Energy intake (kJ/day) Fat intake (g/day) CHO intake (g/day) Protein intake (g/day)
Pre-intervention
Post-intervention
Mean
SD
Mean
SD
7440 63.9 233.4 75.7
1744 21.5 52.6 26.2
6740 51.6 221.6 68.7
2124 19.4 78.1 34.3
Data are presented as mean ± standard deviation; CHO: carbohydrate. ⁎⁎ p b 0.01.
⁎⁎
literature as it is the first to examine the nutritional adaptations to an exercise program of several months in obese youth. 5. Conclusion The present study provides new information regarding the impact of aerobic exercise on obese adolescents' energy balance. As highlighted by Caudwell, Hopkins, King, Stubbs and Blundell [4] in obese adults [4], physical activity alone might not be enough to induce weight loss in obese adolescents, depending on their individual energy intake response and certainly mainly on their tendency to reduce their physical activity level outside the prescribed sessions. Looking at such results, it seems necessary to consider the impact of physical activity on both sides of the energy balance (expenditure and intake) equation during and outside the exercise hours, to obtain a better understanding of which participants lose weight in response to structured aerobic exercise. Future research should be conducted to clearly and objectively explore both the nutritional and energetic adaptations to a physical activity program (depending on the program's characteristics such as duration, and intensity) in obese youth providing then important results to optimize our weight loss strategies and identify which participants would benefit most from exercise intervention. Authors' contribution GG and AK were investigators of this work and built the design. TD and JPC analyzed the data. DT, JPC, KA, GG were in-charged of the interpretation of the results and wrote the manuscript.
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Acknowledgments The authors thank the Children's Hospital of Eastern Ontario Research Institute and the Canadian Diabetes Association for the funding support to conduct this study. We also thank Dr. Stasia Hadjiyannakis who is the director of the Endocrinology/Obesity clinic at the Children's Hospital of Eastern Ontario from whose clinic the majority of participants were recruited. In addition we are grateful to Jane Rutherford for coordinating the trial, Dr. Rachel Colley, Karen Dickey, Mike Bourghese, Emily Knight, Nick Levasseur, and Andree-Anne Morrisey for their effort in data collection and data entry. We would also like to thank all the participants in the study. Dr. Thivel is supported by the 2011 Clinical Nutrition and Metabolism Society Award (SFNEP). Dr. Chaput holds a Junior Research Chair in Healthy Active Living and Obesity Research. Dr. Goldfield was supported by a New Investigator Award from the Canadian Institute of Health Research when the trial was conducted and is currently supported by an Endowed Scholarship by the Children's Hospital of Eastern Ontario Volunteer Association. Dr. Adamo is currently supported by a New Investigator Award from the Canadian Institutes of Health Research. References [1] Adamo KB, Rutherford JA, Goldfield GS. Effects of interactive video game cycling on overweight and obese adolescent health. Appl Physiol Nutr Metab 2010;35(6):805–15. [2] Blundell JE, Stubbs JR. Diet composition and the control of food intake in humans. In: Bray GA, Bouchard C, James WPT, editors. Handbook of obesity. New-Yok City: Marcel Dekker Inc.; 1998. p. 243–72. [3] Blundell JE, Stubbs RJ, Hughes DA, Whybrow S, King NA. Cross talk between physical activity and appetite control: does physical activity stimulate appetite? Proc Nutr Soc 2003;62(3):651–61. [4] Caudwell P, Hopkins M, King NA, Stubbs RJ, Blundell JE. Exercise alone is not enough: weight loss also needs a healthy (Mediterranean) diet? Public Health Nutr 2009;12(9A):1663–6. [5] Donnelly JE, Kirk EP, Jacobsen DJ, Hill JO, Sullivan DK, Johnson SL. Effects of 16 mo of verified, supervised aerobic exercise on macronutrient intake in overweight men and women: the Midwest Exercise Trial. Am J Clin Nutr 2003;78(5):950–6. [6] Fremeaux AE, Mallam KM, Metcalf BS, Hosking J, Voss LD, Wilkin TJ. The impact of school-time activity on total physical activity: the activitystat hypothesis (EarlyBird 46). Int J Obes (Lond) 2012;35(10):1277–83. [7] Goldfield GS, Cloutier P, Mallory R, Prud'homme D, Parker T, Doucet E. Validity of foot-to-foot bioelectrical impedance analysis in overweight and obese children and parents. J Sports Med Phys Fitness 2006;46(3):447–53. [8] King NA, Caudwell P, Hopkins M, Byrne NM, Colley R, Hills AP, et al. Metabolic and behavioral compensatory responses to exercise interventions: barriers to weight loss. Obesity (Silver Spring) 2007;15(6):1373–83.
[9] King NA, Hester J, Gately PJ. The effect of a medium-term activity- and diet-induced energy deficit on subjective appetite sensations in obese children. Int J Obes (Lond) 2007;31(2):334–9. [10] King NA, Horner K, Hills AP, Byrne NM, Wood RE, Bryant E, et al. Exercise, appetite and weight management: understanding the compensatory responses in eating behaviour and how they contribute to variability in exercise-induced weight loss. Br J Sports Med 2011;46(5):315–22. [11] Kriemler S, Hebestreit H, Mikami S, Bar-Or T, Ayub BV, Bar-Or O. Impact of a single exercise bout on energy expenditure and spontaneous physical activity of obese boys. Pediatr Res 1999;46(1):40–4. [12] Martins C, Morgan L, Truby H. A review of the effects of exercise on appetite regulation: an obesity perspective. Int J Obes (Lond) 2008;32(9):1337–47. [13] Mayer J. Glucostatic mechanism of regulation of food intake. N Engl J Med 1953;249(1):13–6. [14] Mayer J, Roy P, Mitra KP. Relation between caloric intake, body weight, and physical work: studies in an industrial male population in West Bengal. Am J Clin Nutr 1956;4(2):169–75. [15] Meijer EP, Westerterp KR, Verstappen FT. Effect of exercise training on total daily physical activity in elderly humans. Eur J Appl Physiol Occup Physiol 1999;80(1):16–21. [16] Morio B, Montaurier C, Pickering G, Ritz P, Fellmann N, Coudert J, et al. Effects of 14 weeks of progressive endurance training on energy expenditure in elderly people. Br J Nutr 1998;80(6):511–9. [17] Stubbs RJ, Hughes DA, Johnstone AM, Whybrow S, Horgan GW, King N, et al. Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. Am J Physiol Regul Integr Comp Physiol 2004;286(2):R350–8. [18] Thivel D, Aucouturier J, Metz L, Morio B, Duche P. Is there spontaneous energy expenditure compensation in response to intensive exercise in obese youth? Pediatr Obes Apr 2014;9(2):147–54. [19] Thivel D, Blundell JE, Duche P, Morio B. Acute exercise and subsequent nutritional adaptations: what about obese youths? Sports Med 2012;42(7):607–13. [20] Thivel D, Chaput JP. Are post-exercise appetite sensations and energy intake coupled in children and adolescents? Sports Med Jun 2014;44(6):735–41. [21] Thivel D, Duche P. Physical activity for weight loss in children: is there any compensatory mechanism? Pediatr Exerc Sci May 2014;26(2):121–3. [22] Thivel D, Isacco L, Montaurier C, Boirie Y, Duche P, Morio B. The 24-h energy intake of obese adolescents is spontaneously reduced after intensive exercise: a randomized controlled trial in calorimetric chambers. PLoS One 2012;7(1):e29840. [23] Thivel D, Isacco L, Rousset S, Boirie Y, Morio B, Duché P. Intensive exercise: a remedy for childhood obesity? Physiol Behav 2011;102(2):132–6. [24] Tremblay MS, Shields M, Laviolette M, Craig CL, Janssen I, Gorber SC. Fitness of Canadian children and youth: results from the 2007–2009 Canadian Health Measures Survey. Health Rep 2010;21(1):7–20. [25] Vereecken C, Covents M, Maes L. Comparison of a food frequency questionnaire with an online dietary assessment tool for assessing preschool children's dietary intake. J Hum Nutr Diet 2010;23(5):502–10. [26] Wang X, Nicklas BJ. Acute impact of moderate-intensity and vigorous-intensity exercise bouts on daily physical activity energy expenditure in postmenopausal women. J Obes 2011;2011. http://dx.doi.org/10.1155/2011/342431 [Article ID 342431, 5 pages].
Contents lists available at ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Is energy intake altered by a 10-week aerobic exercise intervention in obese adolescents?☆,☆☆ D. Thivel a,⁎, J.P. Chaput a,b, K.B. Adamo a,b, G.S. Goldfield a,b a b
Healthy Active Living and Obesity Research Group, Children's Hospital of Eastern Ontario Research Institute, Ottawa, Ontario, Canada School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada
H I G H L I G H T S • Physical activity program leads to a 10% decreased energy intake in obese youth. • Interventions have to consider potential energy expenditure compensations to physical activity. • Physical activity not only acts on energy expenditure but also intake in obese adolescents.
a r t i c l e
i n f o
Article history: Received 29 April 2014 Received in revised form 20 May 2014 Accepted 12 June 2014 Available online 19 June 2014 Keywords: Energy expenditure Physical activity Energy intake Pediatric obesity
a b s t r a c t Aim: To examine energy intake adaptations to a 10-week aerobic exercise program in obese adolescents. Methods: Twenty-six 12–17 year old obese adolescents were asked to cycle twice a week for an hour in a research laboratory. Body composition, aerobic fitness (submaximal fitness test) and energy intake (3-day food record) were assessed before and immediately after the 10-week intervention. Results: The average time spent pedaling per session was 55.3 ± 12.1 min for a mean energy expenditure of 2196 ± 561 kJ per session. The intervention produced significant improvements in percentage of body fat (44.5 ± 10.6% vs. 43.4 ± 9.8%; p b 0.05) but no significant weight and fat-free mass change. Peak workload (79.5 ± 20.8 W vs. 87.3 ± 17.6 W; p b 0.05) and peak heart rate (174.6 ± 18.7 bpm vs. 166.2 ± 21.0 bpm; p b 0.01) were improved. The mean total daily energy intake (in kJ/day) showed a tendency to decrease through the intervention (7440 ± 1744 to 6740 ± 2124 kJ; p = 0.07) but a high interindividual variability observed in the energy intake response to the intervention may explain the nonsignificant association between the energy intake response and weight loss. Conclusion: A 10-week aerobic exercise program may result in a small decrease in energy intake and an associated decrease in percentage of body fat but no weight loss in obese adolescents. This lack of weight loss could be explained by a decrease in spontaneous energy expenditure outside the intervention sessions. © 2014 Elsevier Inc. All rights reserved.
1. Introduction The alarming progression of pediatric overweight and obesity has led to an array of diverse efforts aimed at promoting healthy eating and physical activity. The understanding and control of energy balance is certainly a key factor in the elaboration of effective recommendations and weight loss strategies. About 50 years ago it was commonly Abbreviations: VO2max, maximal oxygen consumption; BMI, body mass index; EI, energy intake; EE, energy expenditure; EB, energy balance; HR, heart rate; CHO, carbohydrates. ☆ Disclosure: No conflict of interest was declared. ☆☆ Clinical Trial. ClinicalTrial.gov: NCT00983970 ⁎ Corresponding author at: Healthy Active Living and Obesity Research Group, Children's Hospital of Eastern Ontario Research Institute, 401 Smyth Road, Ottawa, Ontario K1H 8L1, Canada. Tel.: +1 613 737 7600x3288; fax: +1 613 738 4800. E-mail address: [email protected] (D. Thivel).
http://dx.doi.org/10.1016/j.physbeh.2014.06.013 0031-9384/© 2014 Elsevier Inc. All rights reserved.
considered that energy consumption was regulated with such flexibility that increasing energy expenditure by exercise automatically led to an equivalent increased energy intake [13]. However, Mayer himself showed that physical activity was not perfectly coupled to food consumption and that a very low level of activity was related to higher caloric intake [14]. Many studies have been conducted during the last decades regarding the effects of acute exercise on the short-term control of appetite and energy intake in adults [3,12]. Although data remain conflicting so far, in lean children and adolescents, acute intensive exercise (N70% of maximal aerobic capacity — VO2max) seems to promote a negative energy balance mainly due to a decreased daily energy intake [19,22,23]. This reduction of the subsequent energy intake is not accompanied by any alteration in appetite sensations, which is consistent with the previously observed uncoupling between appetite feelings and energy intake after exercise in obese adults [3].
D. Thivel et al. / Physiology & Behavior 135 (2014) 130–134
Although acute exercise affects daily energy intake, exercise has to be sustained over time to favor weight loss which questioned the nutritional adaptations to long term exercise. In 2009, Caudwell and collaborators tested the effects of a 12-week physical activity program (approximate energy expenditure of 500 kcal per week) [4]. The authors concluded that physical activity alone was not enough to induce weight loss mainly because of a possible compensatory response to exercise with some patients decreasing their fruit and vegetable consumption and increasing their total energy intake [4]. This increased energy intake with exercise could be explained by the extremely powerful appetite system mechanisms that tend to protect individuals against under-eating and weight loss [2]. Previously published data in obese adolescents showed that a 6-week exercise program increased hunger and decreased fullness but the authors did not assess energy intake [9]. The nutritional (energy intake and appetite) adaptations to an exercise program are of particular interest in terms of weight loss achievement, but show an important inter-individual variability [9,10] with some patients recruiting adaptive mechanisms to oppose the negative or reduced energy balance induced by exercise [17]. To date no data are available examining the possible nutritional adaptations to an exercise program in obese youth. Accordingly, the aim of this study was to test the impact of a 10-week aerobic program on obese adolescents' energy intake and weight loss. Extrapolating from the literature, we hypothesize that adolescents will not show significant changes in energy intake or weight loss in response to the exercise intervention. 2. Methods 2.1. Population This is a secondary analysis of data collected from participants in the GameBike trial [1] where the participants were screened through the Endocrinology Clinic at the Children's Hospital of Eastern Ontario (CHEO; Ottawa, Ontario, Canada) to determine eligibility. Of the 30 overweight/obese 12–17 year old participants that were selected (body mass index (BMI) above the 95th percentile for age and gender according to the Center for Disease Control and Prevention's growth chart data/available from http://www.cdc.gov/growthcharts), 4 dropped out prematurely due to a lack of interest and then 26 adolescents completed the study (14 females and 12 males; 14.5 ± 1.8 years old). The inclusion and exclusion criteria have been previously detailed [1]. The screening and recruitment were done between May 2007 and January 2009 and the last assessments were completed in March 2009. The protocol was approved by the Children's Hospital of Eastern Ontario (CHEO) research ethics board. All the participants and their legal guardians received information sheets and completed consent forms. 2.2. Experimental design After a medical examination, to ensure the adolescents' ability to complete the protocol, their aerobic fitness, anthropometric characteristics, body composition and daily energy intake were assessed before and after a physical activity program. Participants were asked to visit the laboratory twice a week for 60 min for 10 weeks. During these 60minute exercise sessions, the adolescents were asked to cycle while playing video games or listening to music. Although they were asked to stay in the lab for 60 min, they remained free to take breaks or stop cycling when they wanted. During each session, heart rate (HR) was individually monitored by a polar heart rate monitor (Polar S-510, Polar Electro Y, Kempele, Finland) for both safety and research purposes. Estimates of energy expenditure and exercise intensity were measured using the Polar heart rate monitor data, and the distance cycled was assessed by the stationary exercise bike computer system. The energy expenditure estimation was determined by a proprietary algorithm from Polar that takes into account the subject's gender, age, height
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and weight along with heart rate. The intensity at which the adolescents were exercising was evaluated by comparing their theoretical predicted maximal heart rate (using the 220 − age calculation) to their average heart rate during the exercise session. The 220 − age formula was chosen according to the Canadian Health Measures Survey that uses it for measuring submaximal fitness in children and youth [24]. 2.2.1. Anthropometric measurements and body composition A wall-mounted stadiometer (Seca GmBH & Co. Kg., Hamburg, Germany) was used to assess height while body weight and body composition (fat mass and fat-free mass) were assessed using a Tanita (model 300-A) bioelectrical impedance scale (Tanita Corporation of America Inc., Arlington Heights III, USA). Body mass index (BMI) was then calculated as body weight (kg) / height (m)2. All measures were done in duplicate and the means used to resolve any discrepancies in measurements. We controlled for food consumption and hydration by measuring these at baseline and asking that subjects consume the same amount of liquids and food at the same time of day prior to post-intervention assessment. Accordingly, the adolescents were tested at the same time of the day before and after the intervention. It has been previously shown that measures from the Tanita bioelectrical impedance scale and from dual-energy X-ray absorptiometry are highly correlated in overweight and obese youth [7], demonstrating strong concurrent validity. A Seca retractable and locking ergonomic measuring tape (Seca GmBH & Co. Kg.) was also used to measure waist circumference (cm) and each measurement was taken at the midpoint between the floating rib and the iliac crest after a gentle expiration. 2.2.2. Aerobic fitness test Pre- and post-intervention the adolescents had to complete a graded exercise protocol on a cycle ergometer to assess their submaximal aerobic fitness. They were asked to pedal at a constant speed for 3 min at a low work load and then the work load increased every 2 min by 10 W until they reached volitional fatigue. Wattage and heart rate were measured and recorded through the duration of the test. 2.2.3. Energy intake Energy intake was assessed before and right after the 10-week intervention with the use of a 3-day food diary and the energy and macronutrient consumption was analyzed using the online dietary analysis program (www.fitday.com). This program has been shown to be a scientifically valid tool to explore energy intake in children and youth [25]. Prior to the program, the research staff have met individually with the adolescents and their parents and explained precisely how to complete the food records and how to quantify the food consumed (advices concerning the completion of the food diary were also given to the adolescents at the end of the 10 weeks). 2.2.4. Statistical analysis Variables are presented as means ± standard deviations and the level of statistical significance set at p b 0.05. Statistical analyses were conducted using the SPSS software version 19.0 for Windows. Paired t-tests were used to compare baseline and post-intervention values on anthropometric measurements (height, weight, BMI, waist circumference) body composition (fat mass and fat-free mass), physical fitness (peak workload, time to exhaustion, peak heart rate) and energy intake (daily energy consumption and macronutrient intake). 3. Results 3.1. Exercise sessions' characteristics As shown in Table 1, the participants pedaled for an average time of 55.3 ± 12.1 min during the exercise sessions with an average of 33.5 ± 15.3 min spent at moderate to vigorous intensity (60 to 79% peak heart rate) and 19.3 ± 17.4 min at vigorous intensity (80 to 100% peak heart
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4. Discussion
Table 1 Characteristics of the exercise sessions.
Average time pedaled (min/session) Average minutes spent in 60%–79% peak HR Average minutes spent in 80%–100% peak HR Average energy expenditure (kJ)
Mean
SD
55.3 33.5 19.3 2196
12.1 15.3 17.4 561
Data presented as mean ± standard deviation; HR: heart rate.
rate). The estimated energy expenditure per session reached 2196 ± 561 kJ.
3.1.1. Anthropometric measurements, body composition and physical fitness parameters As shown in Table 2, only the height (164.4 ± 6.2 to 165.1 ± 6.6 cm) significantly increased through the 10 weeks (p b 0.05). Participants' weight, BMI and waist circumference and fat-free mass did not significantly differ between baseline and the end of the program (Table 2). Although fat mass expressed in kilograms was not significantly modified by the intervention, it was significantly decreased once expressed as a percentage of total mass (44.5 ± 10.6% to 42.8 ± 9.8%; p b 0.05). The mean weight variation (weight post intervention minus baseline weight) was 1.1 ± 3.6 kg but when considered individually, the adolescents showed an important inter-individual weight loss variability from an 8 kg weight loss to a weight gain of 9.2 kg (Fig. 1A). As previously shown in this specific group of adolescents [1], a training effect was observed with a significant increase of the participants' aerobic fitness indicators. Peak workload (p b 0.05), peak heart rate (p b 0.01) and the time to reach exhaustion (p b 0.05) were all significantly improved by the intervention (Table 2).
3.1.2. Energy intake and macronutrient consumption As shown in Table 3, we observed that daily energy intake tended to be lower after the 10-week aerobic intervention but did not reach statistical significance (difference of 699 kJ; p = 0.07). Daily carbohydrate (CHO) and protein intake did not significantly differ between baseline and the post-intervention assessment while daily fat intake was significantly lower after the aerobic exercise program (difference of 12.2 g). As for Fig. 1A that shows the important inter-individual weight changes' variability, part B of the figure illustrates the energy intake response for each participant. The figure highlights an important variability of the energy intake changes going from − 6070 kJ to + 1108 kJ. Changes in body weight and body fat are not related to the energy intake modifications (as illustrated in Fig. 1 for body weight). Table 2 Effect of the exercise intervention on anthropometric characteristics, body composition and aerobic fitness indicators. Pre-intervention
Height (cm) Weight (kg) BMI (kg/m2) WC (cm) Fat mass (kg) Fat mass (%) Fat-free mass (kg) Peak workload (W) Time to exhaustion (min) Peak heart rate (bpm)
Postintervention
Mean
SD
Mean
SD
164.4 99.2 37.4 113.8 45.5 44.5 54.4 79.5 12.4 174.6
6.2 22.8 9.1 15.4 20.8 10.6 11,7 20.8 1.3 18.7
165.1 100.3 37.5 113.5 46.8 42.8 55.5 87.3 12.9 166.2
6.6 23.4 9.4 15.6 22.4 9.8 11.1 17.6 0.5 21.0
⁎
⁎ ⁎ ⁎ ⁎⁎
Data are presented as mean ± standard deviation; WC: waist circumference; BMI: body mass index. ⁎ p b 0.05. ⁎⁎ p b 0.01.
Although several studies have questioned the impact of acute physical exercise on subsequent nutritional adaptations in obese youth, the present work is the first to directly explore their energy intake response to a long term (10 weeks) physical activity program. According to the present results, exercising twice a week (with a mean pedaling time of 55.3 ± 12.1 min per session) for 10 weeks led to a slight (statistical trend with p = 0.07) decrease in energy intake of about 700 kJ/day (or 10%) in obese youth. In 2007, King and collaborators showed that a 6-week physical activity (skill-based activities) program increased 14-year-old obese adolescents' hunger and decreased their fullness feeling but they did not report any data regarding their caloric intake [9]. It could be argued that this higher hunger sensation found by King et al. is in contradiction with the decreased energy intake observed here. However, this can be explained by the possible uncoupling effect of physical activity on energy intake and appetite feelings, as already underlined after acute exercise in both adults [3] and adolescents [20,22,23]. Although the intervention led to a significant reduction in percent body fat which could be attributed to both the energy expenditure from the physical activity program and a significant decrease in dietary fat consumption, no differences were found in terms of body weight (kg), BMI (kg/m2), fat-free mass or absolute fat mass. Our results are similar to those of Caudwell and colleagues who reported that a 12week physical activity intervention (5 h a week) was not effective in inducing weight loss in obese adults [4]. This lack of weight loss was explained by an important inter-individual variability in the nutritional response to the program [4]. In the present study, the increased energy expenditure induced by the exercise sessions was accompanied by a slight decrease in energy intake which should have favored a negative energy balance and then weight loss. However, when considered individually, the data showed an important inter-individual variability in terms of energy intake response to the program. As already demonstrated by King and collaborators in adults [10], Fig. 1B illustrates the important variability found between adolescents in their energy intake adaptations through the intervention. This figure clearly illustrates the fact that some adolescents did increase their energy consumption while others reduced it, underlying the necessity to consider the highly variable individual nutritional adaptations to exercise interventions. It is important to note, however, that those inter-adolescent differences in terms of energy intake response in our data do not explain the differences observed in terms of weight loss (Fig. 1A). Participants who decreased their food consumption effectively did not have a greater weight loss. This result suggests that other behavioral compensatory responses to the intervention might be responsible for the lack of weight loss. Possible energetic adaptations in other behavioral aspects of energy expenditure may effectively lead to a lower than expected efficacy of exercise in the control of energy balance [5,8]. For instance, Meijer, Westerterp and Verstappen [15] have shown a significant decline (8%) in the number of accelerometer counts per day in adults illustrating a reduction of their spontaneous free-living physical activity level through a 12-week exercise program [15]. Others also reported such a decrease in spontaneous physical activity energy expenditure after prescribed exercise in adults [5,16,26]. Although Fremeaux, Mallam, Metcalf, Hosking, Voss and Wilkin [6] highlighted this compensatory trend in lean children [6], the present results seem to be the first to suggest that such a mechanism exists in obese adolescents. Obese youth have been shown to significantly reduce their spontaneous physical activity energy expenditure after an acute session of intensive exercise [11,18,21,22] but to our knowledge it has never been assessed on a longer term (several weeks of intervention). Looking at the important individual variability observed in terms of energy intake response and at its lack of coherence regarding the absence of weight loss, the presence of potential compensatory mechanisms that lead to a reduced spontaneous physical activity-induced
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Fig. 1. Individual body weight changes (A) and energy intake changes (B) over the course of the aerobic exercise intervention. Data are presented as mean values (pre–post assessment).
energy expenditure outside the prescribed exercise sessions may be the best explanation for the inefficiency of physical activity alone in inducing weight loss in obese youth. The present study has several limitations. Although the use of a 3day food diary is one of the most common methods for assessing energy intake in the natural environment, it is commonly associated with inaccurate recall, particularly in youth, as is the case with most self-reports of energy balance behaviors, thereby possibly limiting the accuracy of our data (7-day records could have been used but this might be too long to complete and might decrease the accuracy of the results, particularly in adolescents). The absence of indication regarding the appetite feelings as well as objective measurement of energy expenditure through accelerometers in free living conditions are additional limitations that need to be addressed in future research. Despite these limitations, the current study makes an important contribution to the
Table 3 Baseline and post-intervention energy intake and macronutrient intake.
Energy intake (kJ/day) Fat intake (g/day) CHO intake (g/day) Protein intake (g/day)
Pre-intervention
Post-intervention
Mean
SD
Mean
SD
7440 63.9 233.4 75.7
1744 21.5 52.6 26.2
6740 51.6 221.6 68.7
2124 19.4 78.1 34.3
Data are presented as mean ± standard deviation; CHO: carbohydrate. ⁎⁎ p b 0.01.
⁎⁎
literature as it is the first to examine the nutritional adaptations to an exercise program of several months in obese youth. 5. Conclusion The present study provides new information regarding the impact of aerobic exercise on obese adolescents' energy balance. As highlighted by Caudwell, Hopkins, King, Stubbs and Blundell [4] in obese adults [4], physical activity alone might not be enough to induce weight loss in obese adolescents, depending on their individual energy intake response and certainly mainly on their tendency to reduce their physical activity level outside the prescribed sessions. Looking at such results, it seems necessary to consider the impact of physical activity on both sides of the energy balance (expenditure and intake) equation during and outside the exercise hours, to obtain a better understanding of which participants lose weight in response to structured aerobic exercise. Future research should be conducted to clearly and objectively explore both the nutritional and energetic adaptations to a physical activity program (depending on the program's characteristics such as duration, and intensity) in obese youth providing then important results to optimize our weight loss strategies and identify which participants would benefit most from exercise intervention. Authors' contribution GG and AK were investigators of this work and built the design. TD and JPC analyzed the data. DT, JPC, KA, GG were in-charged of the interpretation of the results and wrote the manuscript.
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Acknowledgments The authors thank the Children's Hospital of Eastern Ontario Research Institute and the Canadian Diabetes Association for the funding support to conduct this study. We also thank Dr. Stasia Hadjiyannakis who is the director of the Endocrinology/Obesity clinic at the Children's Hospital of Eastern Ontario from whose clinic the majority of participants were recruited. In addition we are grateful to Jane Rutherford for coordinating the trial, Dr. Rachel Colley, Karen Dickey, Mike Bourghese, Emily Knight, Nick Levasseur, and Andree-Anne Morrisey for their effort in data collection and data entry. We would also like to thank all the participants in the study. Dr. Thivel is supported by the 2011 Clinical Nutrition and Metabolism Society Award (SFNEP). Dr. Chaput holds a Junior Research Chair in Healthy Active Living and Obesity Research. Dr. Goldfield was supported by a New Investigator Award from the Canadian Institute of Health Research when the trial was conducted and is currently supported by an Endowed Scholarship by the Children's Hospital of Eastern Ontario Volunteer Association. Dr. Adamo is currently supported by a New Investigator Award from the Canadian Institutes of Health Research. References [1] Adamo KB, Rutherford JA, Goldfield GS. Effects of interactive video game cycling on overweight and obese adolescent health. Appl Physiol Nutr Metab 2010;35(6):805–15. [2] Blundell JE, Stubbs JR. Diet composition and the control of food intake in humans. In: Bray GA, Bouchard C, James WPT, editors. Handbook of obesity. New-Yok City: Marcel Dekker Inc.; 1998. p. 243–72. [3] Blundell JE, Stubbs RJ, Hughes DA, Whybrow S, King NA. Cross talk between physical activity and appetite control: does physical activity stimulate appetite? Proc Nutr Soc 2003;62(3):651–61. [4] Caudwell P, Hopkins M, King NA, Stubbs RJ, Blundell JE. Exercise alone is not enough: weight loss also needs a healthy (Mediterranean) diet? Public Health Nutr 2009;12(9A):1663–6. [5] Donnelly JE, Kirk EP, Jacobsen DJ, Hill JO, Sullivan DK, Johnson SL. Effects of 16 mo of verified, supervised aerobic exercise on macronutrient intake in overweight men and women: the Midwest Exercise Trial. Am J Clin Nutr 2003;78(5):950–6. [6] Fremeaux AE, Mallam KM, Metcalf BS, Hosking J, Voss LD, Wilkin TJ. The impact of school-time activity on total physical activity: the activitystat hypothesis (EarlyBird 46). Int J Obes (Lond) 2012;35(10):1277–83. [7] Goldfield GS, Cloutier P, Mallory R, Prud'homme D, Parker T, Doucet E. Validity of foot-to-foot bioelectrical impedance analysis in overweight and obese children and parents. J Sports Med Phys Fitness 2006;46(3):447–53. [8] King NA, Caudwell P, Hopkins M, Byrne NM, Colley R, Hills AP, et al. Metabolic and behavioral compensatory responses to exercise interventions: barriers to weight loss. Obesity (Silver Spring) 2007;15(6):1373–83.
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