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Timing of moderate-to-vigorous exercise and its impact on subsequent energy intake in young males
Physiology & Behavior 151 (2015) 557–562
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Timing of moderate-to-vigorous exercise and its impact on subsequent energy intake in young males Marie-Helene Albert a,b, Vicky Drapeau c,d, Marie-Eve Mathieu a,b,⁎ a
Department of Kinesiology, University of Montreal, 2100 Edouard-Montpetit, Montreal H3C 3J7, Canada Sainte-Justine UHC Research Center, 5757 Decelles, Montreal H3T 1C5, Canada Department of Physical Education, University Laval, Sport and Physical Education Building, Quebec G1V 0A6, Canada d University Institute of Cardiology and Pneumology of Quebec, 2725, Sainte-Foy Road, Quebec G1V 4G5, Canada b c
H I G H L I G H T S • • • •
The impact of exercise timing on energy intake has been previously unknown. An exercise session closer to a meal reduces subsequent energy and lipid intake. In this context, appetite was not linked to actual ingestion. Timing appears to potentially affect energy balance.
a r t i c l e
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Article history: Received 30 June 2015 Received in revised form 2 August 2015 Accepted 22 August 2015 Available online 29 August 2015 Keywords: Physical activity Energy intake Energy balance Adolescents Obesity
a b s t r a c t Exercise can suppress appetite and energy intake but the impact of the timing of exercise remains unknown. Knowing that orexigenic hormone levels decrease during exercise but rapidly increase afterward, the aim of the current study was to investigate whether energy intake is increasingly reduced when exercise immediately precedes a meal compared to when a delay occurs between the exercise and the meal. Non-obese boys (15– 20 years old; N = 12) were individually evaluated while performing two randomly assigned experimental visits: 1) a 30-min exercise session of moderate-to-vigorous intensity followed immediately by an ad libitum buffet at 12 PM and 2), an identical session followed by a 135-min waiting period and an ad libitum buffet-type meal at 12 PM. In both conditions, a snack in the afternoon and a second ad libitum buffet-type meal at 5 PM were served. Findings showed that hunger ratings were similar under both conditions. The exercise session immediately prior to the meal compared with the condition with a N 2 h delay led to reduction of 11% and 23% in overall and lipid energy intakes at lunch, respectively (P-values N 0.05). No significant differences were found in the energy intakes from the afternoon snack and dinner. Apart from lipids at lunch, the proportions of energy from the various macronutrients at each meal were similar. This study reveals that being physically active before a meal plays a role in acute energy intake reduction when a shorter delay is present between exercise and a meal. In addition, the absence of compensation over several hours is noteworthy. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Energy balance is central to body weight control, with energy expenditure and energy intake (EI) independently contributing to energy balance [1]. Interestingly, energy expenditure can also influence energy balance by having an indirect impact via EI. It is currently known that a longer duration, higher intensity and a selection of cardiovascular
⁎ Corresponding author at: Department of Kinesiology, University of Montreal, Room 8223. P.O. Box 6128, Downtown Station, Montreal, H3C 3J7 Quebec, Canada. E-mail addresses: [email protected] (M.-H. Albert), [email protected] (V. Drapeau), [email protected] (M.-E. Mathieu).
http://dx.doi.org/10.1016/j.physbeh.2015.08.030 0031-9384/© 2015 Elsevier Inc. All rights reserved.
rather than resistance exercises can help reduce subsequent hunger, appetite and EI, thereby creating an acute energy deficit [2–7]. Among the mechanisms investigated in this exercise-induced anorexia, changes in acylated ghrelin levels are revealing. A reduction in levels of this orexigenic hormone has been reported during and after exercise, coinciding with hunger and appetite reductions [8–10]. However, hunger and acylated ghrelin levels rapidly increase during the recovery period following exercise [3,8,9]. These observations are in line with the delay in the onset of a meal observed following exercise compared to no exercise [2,11]. These findings suggest that the anorexigenic effect of exercise is transitory and that a window of opportunity might exist that more substantially reduces EI following exercise.
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The timing of physical activity is a relatively novel concept; recent studies address its significance in enhancing cardiometabolic health outcomes. For example, exercising at night reduces blood pressure to a greater extent than morning exercise in hypertensive patients that are usually resistant to the hypotensive effects of exercise [12]. Greater reductions in blood glucose and lipid levels have also been found following night time exercise or when exercise strategically occurs around mealtime [13–19], while enhanced lipid oxidation can occur following morning exercise or fasting [16,20]. To date, the effect of the timing of exercise on energy balance through EI remains unknown. In studies on the anorexigenic effect of exercise, a meal is served either shortly after the end of exercise (b 15 min) [6], within 1 h following exercise [4,10,21,22] or more than 1 h after exercise [8,22]. However, no study has compared the timing as it relates to meals. As a result, the main purpose of the current study was to confirm the hypothesis that EI is reduced when exercise immediately precedes lunch compared to when a delay occurs between exercise and lunch. 2. Materials and methods 2.1. Participants Twelve non-obese males aged between 15 and 20 years old were recruited to participate in this crossover study. The participants met the following exclusion criteria: they were not on any specific diet; did not have a diagnosis of anorexia, bulimia or any metabolic disease; were not taking any medication that could influence appetite; did not have any intestinal disorders and were able to communicate in French. The consent form was approved by the Sainte-Justine University Hospital Centre ethics committee and a physical activity readiness questionnaire [23] was completed by the participants and parents/tutors of minors. After a first preliminary visit, two additional experimental visits were randomly conducted. The participants were presented with a false scenario (hypothesis): the study of cardiac response to exercise, rest and caloric intake to prevent influence on the main outcome of the study (EI); they were asked to wear a heart rate monitor to enhance credibility. Financial compensation ($12 CAN) was provided after each visit. A final consent form indicating the real purpose of the study was administered at the end of the last visit. All participants consented to further use of the data collected.
2.3. Experimental visits Each participant took part in two experimental visits in a counterbalanced measures design with ≥5 and b 21 days between trials using ExMeal and ExdelayMeal (Fig. 1). During ExMeal, the exercise was followed within 15 min by a buffet-type meal. In the ExdelayMeal, the exercise was followed by a waiting period of 135 min before the buffettype meal. This was important for assessing the timing effect since it allowed a comparison of the two Ex sessions performed with the same two meals and with a maximum time difference between them. At 7:00 AM and after an overnight fast, the participants ate at home the standard breakfast provided. It contained ~ 2993 kJ and was composed of white bread (100 g), smooth peanut butter (18 g), orange juice (200 ml), butter (6 g) and cheddar cheese (42 g). Arrival at the laboratory was scheduled for 8:45 AM and compliance with breakfast (start time, duration and consumption of the complete meal provided and nothing more) was confirmed by the participant to the research team. The testing sequence started at 9:00 AM. It included a 30-min moderate-to-vigorous exercise session on the treadmill at 70% maximal oxygen uptake according to the experimental visit either early (9:00 AM) or late (11:15 AM) morning (Fig. 1). Sedentary activities (puzzles, Sudoku, hidden word games, books and listening to personal music) were performed during the morning waiting periods. The order and duration of each activity of the first visit were repeated during the second visit. The first ad libitum buffet-type meal was served at 12:00 PM and the second at 5:00 PM. Between meals, participants remained in or around the laboratory while wearing an NL1000 DigiWalker® pedometer (New-Lifestyles®, Lees Summit, MO, USA) while carrying a prepared snack. 2.4. Energy intake and appetite sensations An ad libitum buffet-type meal composed of 38 liquid and solid items based on a buffet described by Arvaniti et al. (2000) [30] was served at lunch. In the afternoon, each participant was given an ad libitum snack of cheese (~ 50 g), crackers (~ 25 g) and carrots (~ 75 g). At 5:00 PM, the ad libitum buffet was comprised of 35 items (similar to the items included in the lunch buffet, but without the snack items), and one hot meal selected by the participant for both conditions (macaroni and
2.2. Preliminary visit Body mass was measured to the nearest 0.1 kg and body fat percentage determined by bioimpedance analysis on a Tanita BC-418 Segmental Body Composition Analyzer (Tanita Corporation of America Inc., Arlington Heights, IL, USA). Height and waist circumference were measured to the nearest 0.5 cm. The absence of abdominal obesity was confirmed using a waist circumference criterion specific to young [24] and adult [25] subjects. Body mass index (BMI, in kg m−2) was calculated: participants had a BMI percentile ≤ 85th age and sex-specific percentile according to the Centers for Disease Control and Prevention curve (b18 y) or a BMI value ≤ 25 kg m−2 (≥18 y) [26,27]. Maximum oxygen uptake was measured by indirect calorimetry using a Quark CPET system (COSMED Srl, Rome, Italy). A progressive maximal test on a treadmill adapted from the shuttle test was performed [28]. The test started at 6 km h−1 and increased by 1 km h−1 every 2 min. Maximum effort was confirmed by a respiratory exchange ratio (carbon dioxide production·oxygen consumption−1) ≥ 1.1 and/or a maximum heart rate ≥ 200 beats min−1 [29]. These results were used to determine the running speed required for subsequent exercise sessions performed at 70% of individual maximum oxygen uptake. After the running test, each participant was invited to eat from a 38-item ad libitum buffet type meal (see description below) to provide an initial exposure to food prior to the experiment.
Fig. 1. Detailed protocol of experimental visits.
M.-H. Albert et al. / Physiology & Behavior 151 (2015) 557–562
cheese, fettuccini Alfredo or three-mushroom risotto). Lunch and dinner were served in a private room with the same presentation and controlled ambient conditions (light and temperature). The food was weighed before and after meals without participant knowledge. During the entire protocol, participants were instructed to eat only the provided food and drink as usual until satiation. Visual analog scales were completed by the participants upon their arrival at the laboratory as well as before and after lunch and dinner (Fig. 1). The desire to eat, hunger, fullness, anticipated food consumption, desire for specific food types (sweet, fatty, salty and savory) as well as meal palatability, appreciation and visual appeal [31,32] were rated with a validated range of 100 mm [33]. The satiety quotient, a marker of an individual's satiation efficiency, was calculated for lunch and dinner using hunger ratings as follows [34]: −1 Satiety quotient mm kJ ¼
½Pre‐meal ASðmmÞ–Post‐meal ASðmmÞ 100: Energy content of meal ðkJÞ
2.5. Energy expenditure Indirect calorimetry with prior calibration according to manufacturer instructions was used to confirm the equivalent energy expended during the exercise sessions (Quark CPET). Volume and gas compositions were measured during a 10-min period in the middle of each exercise of constant intensity. Energy expenditure was calculated using the formula by Péronnet and Massicotte [35]. 2.6. Statistics The Shapiro–Wilk test was used to confirm normality of data. EI and macronutrient compositions between the two experimental conditions were investigated at each timepoint using paired t-tests. The areas under the curve (AUC) of appetite sensations were calculated for each condition using the trapezoidal rule based on five time points (8:45 AM, 11:45 AM, 12:30 PM, 4:45 PM and 5:30 PM; Fig. 1). Pearson correlations were used to investigate the association between appetite sensations and EI specific to each condition, including sensations and the intake of carbohydrates and lipids. The values presented are the means ± standard deviations (minimum–maximum values) unless otherwise specified. Statistical significance was set at a P-value of 0.05. The data were analyzed using the Statistical Package for the Social Science software version 20 for Mac (IBM Corporation, Armonk, NY). 3. Results The 12 participants were 17.7 ± 1.6 (15.0–20.0) years of age, had a BMI of 23.1 ± 3.1 (19.9–29.0) kg m− 2 with 15.6 ± 5.4 (7.9–30.4) % body fat and a mean waist circumference of 78.5 ± 7.3 (71.0–93.0) cm. All participants were non-obese based on BMI and waist circumference selection criteria. The maximal oxygen uptake was 49.0 ± 5.3 (40.6–59.4) ml kg−1 min−1 and the exercise sessions performed on a treadmill at 70% of the maximum oxygen uptake corresponding to an average speed of 9.6 ± 1.1 (8.0–11.0) km h−1. Each participant complied with the standardized breakfast as requested (time and content). Both experimental conditions led to similar energy expenditure during the exercise sessions and to a similar level of physical activity in the afternoon period as monitored by step count (Table 1). 3.1. Energy and macronutrient intakes A significant difference in EI was measured at lunch between the two experimental conditions, with 646 fewer kilojoules ingested when the exercise immediately preceded lunch compared to when a
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Table 1 Energy expenditure, energy intake and macronutrient profile of the meals.
Energy expenditure of the exercise session, kJ # Steps Energy intake, kJ Lunch Snack Dinner Macronutrient profile, % Lunch Lipids Carbohydrates Proteins Snack Lipids Carbohydrates Proteins Dinner Lipids Carbohydrates Proteins
ExMeal
ExdelayMeal
P-value
1643 (211)
1657 (173)
0.836
4557 (2394) 4823 (2427) 0.627 5072 (1033) 5718 (1343) 0.043 955 (413) 1084 (347) 0.236 4678 (1490) 4632 (1950) 0.925
32.2 (7.04) 49.9 (9.8) 18.8 (4.2)
36.4 (8.8) 45.9 (9.4) 17.6 (3.7)
0.076 0.126 0.242
47.0 (6.3) 31.0 (18.3) 21.9 (13.2)
46.5 (3.1) 34.7 (10.9) 18.8 (9.1)
0.747 0.421 0.317
28.2 (10.2) 57.9 (10.1) 14.0 (3.4)
29.8 (6.4) 54.8 (8.3) 15.4 (5.6)
0.553 0.219 0.293
ExMeal: exercise immediately preceding lunch; ExdelayMeal: exercise followed by a pause before lunch; values are mean (standard deviation).
delay occurred between exercise and lunch (Table 1). No significant differences in EI between ExMeal and ExdelayMeal were found for subsequent meals (Table 1). The macronutrient profile revealed that the intake of energy from lipids was significantly lower at lunch for ExMeal compared to ExdelayMeal by 23% (Fig. 2). When reported as their relative contribution to the meal, a tendency was observed for lipids to contribute less (by 12%) to the total energy content in ExMeal compared to ExdelayMeal (Table 1). The absolute and relative contributions were similar between the conditions for the other macronutrients at lunch (proteins and carbohydrates) as well as for all of the macronutrients at snack and dinner times (Table 1 & Fig. 2). 3.2. Appetite sensations and satiety quotient No differences in the appetite sensations profile, represented by the area under the curve, were observed between conditions for hunger, desire to eat, fullness and anticipated food consumption (Table 2). The individuals' satiation efficiencies were also similar at both meals (lunch and dinner) as revealed by similar satiety quotients (Table 2). The desires for sweet, salty, savory and fatty food were significantly different for sweet food, with a lower score for the ExMeal condition (P = 0.067; Table 2). Three significant associations between pre-meal appetite sensations and subsequent EI at lunch were noted. First, EI was negatively correlated with the savory score of the meal (− 0.678; P = 0.015) in the Exdelaymeal condition. Second, the preference for sweet food was negatively correlated with the proportion of EI via carbohydrates in both ExMeal (r = − 0.663; P = 0.019) and ExdelayMeal (r = − 0.641; P = 0.025) conditions. Third, no other associations between appetite sensations preceding each meal and subsequent EI were significant for the ExMeal or the ExdelayMeal conditions both at lunch and dinner (all P values N 0.05; data not shown). 4. Discussion Strategies to control body weight are constantly evolving towards improved effectiveness. Recent meta-analyses and systematic reviews on the anorexigenic effect of exercise underline the fact that when the impact of exercise on EI reduction is present, it however remains limited [36,37]. Among the various approaches to exercise investigated such as duration of exercise, not all were optimal [37] and none considered the
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Fig. 2. Macronutrients intake when the exercise immediately precedes lunch (ExMeal) and when a delay occurs between exercise and lunch (ExdelayMeal). Values presented are mean ± standard error; *: Significant difference between conditions (P b 0.05).
timing of the exercise as it relates to the timing of the meal. While timing of exercise is mostly recognized for its enhanced cardiometabolic effects [17], the current study is the first study of its kind to specifically address the importance of timing for EI. Results of this study revealed that in young normal-weight males, a reduced caloric intake occurred when exercise was performed immediately prior to lunch compared to delayed exercise and meal. Interestingly, this was observed mainly in a reduction in lipid consumption without increased hunger and without a rebound in EI later during the day. The concept that an anorexigenic effect can explain the suppression of hunger by exercise was first raised approximately 20 years ago [2]. Since then, the short-lived characteristics of the anorexigenic effect have been supported by the following: 1) hunger ratings, which decrease during exercise but return to control levels within minutes during the post-exercise period [2,3,14,16] and 2), a delay in the natural onset of the meal after exercise [2]. The current study demonstrates that the timing of exercise can have a specific impact on subsequent EI; a significant reduction (11%) in EI was measured when no delay was introduced between the exercise session and the meal. Visual analog scales are commonly used to monitor anorexigenic effects in this area of research [2,14,16]. However, the current study and others [6,21,38–41] suggest that that they are not necessarily the best method to predict EI. Total energy intake at the ad libitum buffettype meal contradicted appetite sensation ratings, including AUC. An interesting finding included a reduction in EI for the ExMeal condition that did not lead to increased hunger ratings. Examination of macronutrient intake also revealed discrepancies with subjective ratings: 1) the greater the desire to eat something sweet, the lower was the actual intake of carbohydrates in both conditions; 2) the less savory foods were rated, the more calories were ingested in the ExdelayMeal condition; 3) no association was found between intake of lipids and related VAS scores under both conditions. However, this study found that the intake of calories from lipids at lunch was 23% lower when the meal was immediately preceded by exercise. This significant difference in macronutrient intake corroborates previous findings showing an increased interest towards lowfat food following exercise [42], and that lipid reduction is a more frequently reported change in macronutrient with increased exercise [37]. Such a reduction can be of interest, since reduced intake of lipids contributes to improved weight outcomes [43] and could respond positively to an exercise regimen [44].
The residual effects on the remaining meals go beyond the immediate impact of exercise. In the current case, the afternoon snack and dinner were similar in both conditions in terms of caloric content and macronutrients composition. The timing of exercise thus appears to specifically target only one meal (i.e., the one immediately following the training session). The absence of short-term EI compensation (i.e., no subsequent increase in energy intake at meals following lunch in the ExMeal condition) is also noteworthy. Extrapolation of these findings to a prolong period of time could indicate that the optimal timing of exercise before meals can potentially lead to better body weight outcomes based on the same time and effort investments. Further studies are required to confirm these assumptions given that: 1) normalweight males were tested in the current study; a population known to better respond to the anorexigenic effects of exercise [2,21,22,45,46]; 2) the absence of compensation for the anorexigenic effects of exercise was not tested beyond two days of exercise [47] but was expected to take place at some point [48]; and 3) ad-libitum meals in the laboratory were similar to a real-life setting [49] but might not reflect the real-life ingestion context over a prolong period of time [50]. Current preliminary findings showing reduced EI with optimal exercise timing now justify the assessment of the underlying mechanisms of this relationship, such as the orexigenic and anorexigenic hormonal responses [36,37]. It also supports the desire to better understand the role of exercise timing for the primary and secondary prevention of excess adiposity. The limits of the current study are a small sample size, the narrow age group that limited extrapolations to younger and older individuals and the use of a two-condition protocol. Studies with numerous conditions, including a non-exercise condition, should be undertaken to refine these concepts [3,51] and could be used to identify the optimal timing of exercise with respect to meals. Nevertheless, two-condition protocols have been frequently used in the field of anorexigenic effects of exercise, especially in the earlier stages, such as studies on rest vs. exercise [8,41,47,52,53], low vs. greater duration [2] or comparison of exercise intensities [2,6]. 5. Conclusion In the area of the anorexigenic effects of exercise, the current study suggests for the first time that there might be an optimal time to schedule exercise. Exercise immediately before a meal resulted in young normal-weight males eating fewer calories and lipids compared to a
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the statistical analysis, wrote the paper and had the primary responsibility for the final content of the paper.
Table 2 Appetite sensations area under the curve and associated time points value.
Hunger AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Satiety AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Fullness AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Prospective food consumption AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something sweet AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something salty AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something savory AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something fatty AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm
561
ExMeal
ExDelayMeal
P value
280 (134) 25 (17) 64 (20) 8 (7) 54 (21) 9 (10) 289 (172) 33 (25) 68 (18) 8 (8) 57 (20) 12 (14) 412 (194) 54 (21) 35 (23) 86 (12) 48 (22) 87 (17) 311 (161) 41 (23) 62 (18) 13 (12) 58 (18) 12 (15) 393 (219) 52 (33) 45 (30) 77 (25) 40 (33) 81 (21) 415 (314) 64 (29) 44 (28) 84 (14) 50 (28) 89 (8) 324 (297) 53 (26) 36 (19) 85 (14) 28 (24) 81 (21) 466 (353) 70 (23) 53 (28) 90 (9) 55 (29) 90 (10)
321 (85) 23 (19) 73 (19) 11 (7) 48 (22) 6 (6) 340 (82) 27 (25) 76 (15) 11 (12) 51 (18) 5 (5) 504 (94) 65 (15) 28 (21) 78 (25) 50 (20) 90 (8) 365 (79) 38 (22) 71 (18) 14 (10) 54 (19) 9 (8) 531 (144) 56 (26) 46 (27) 77 (20) 55 (28) 84 (20) 523 (172) 60 (24) 43 (29) 79 (18) 50 (28) 83 (17) 435 (144) 54 (29) 27 (22) 76 (20) 32 (23) 90 (9) 596 (146) 67 (30) 53 (27) 89 (7) 56 (29) 93 (6)
0.338
Acknowledgments We thank all of the participants who took part in this study and the CIRCUIT center for laboratory support. We also thank research assistants Papineau and Portelance.
0.394
References
0.174
0.318
0.067
0.166
0.172
0.132
ExMeal: exercise immediately preceding lunch; ExdelayMeal: exercise followed by a pause before lunch; AUC: area under the curve; values are mean (standard deviation).
delay between exercise and meal. Further studies will be needed to confirm this important finding, especially in other populations, over a longer period of time and in free-living conditions. Financial support The Foundation of Stars, Sainte-Justine UHC (Canada), provided financial support for the purchase of food and beverages and financial compensation for the participants via a grant to Pr. Mathieu. Conflict of interest None. Authorship The authors' responsibilities were as follows: MHA designed and conducted the research, analyzed the data and performed the statistical analysis and wrote the paper; VD designed the research and wrote the paper; MEM designed the research, analyzed the data and performed
[1] K.D. Hall, et al., Energy balance and its components: implications for body weight regulation, Am J Clin Nutr 95 (4) (2012) 989–994. [2] N.A. King, V.J. Burley, J.E. Blundell, Exercise-induced suppression of appetite: effects on food intake and implications for energy balance, Eur. J. Clin. Nutr. 48 (10) (1994) 715–724. [3] D.R. Broom, et al., Influence of resistance and aerobic exercise on hunger, circulating levels of acylated ghrelin, and peptide YY in healthy males, Am J Physiol Regul Integr Comp Physiol 296 (1) (2009) R29–R35. [4] D.A. Thompson, L.A. Wolfe, R. Eikelboom, Acute effects of exercise intensity on appetite in young men, Med. Sci. Sports Exerc. 20 (3) (1988) 222–227. [5] D.J. Laan, et al., Effects and reproducibility of aerobic and resistance exercise on appetite and energy intake in young, physically active adults, Appl Physiol Nutr Metab 35 (6) (2010) 842–847. [6] P. Imbeault, et al., Acute effects of exercise on energy intake and feeding behaviour, Br J Nutr 77 (4) (1997) 511–521. [7] J. Carnier, et al., Aerobic training (AT) is more effective than aerobic plus resistance training (AT + RT) to improve anorexigenic/orexigenic factors in obese adolescents, Appetite 69 (2013) 168–173. [8] D.R. Broom, et al., Exercise-induced suppression of acylated ghrelin in humans, J. Appl. Physiol. 102 (6) (2007) 2165–2171. [9] G.F. Becker, et al., Combined effects of aerobic exercise and high-carbohydrate meal on plasma acylated ghrelin and levels of hunger, Appl Physiol Nutr Metab 37 (1) (2012) 184–192. [10] J.A. King, et al., Influence of prolonged treadmill running on appetite, energy intake and circulating concentrations of acylated ghrelin, Appetite 54 (3) (2010) 492–498. [11] J.A. King, L.K. Wasse, D.J. Stensel, Acute exercise increases feeding latency in healthy normal weight young males but does not alter energy intake, Appetite 61 (1) (2013) 45–51. [12] S. Park, C.A. Jastremski, J.P. Wallace, Time of day for exercise on blood pressure reduction in dipping and nondipping hypertension, J. Hum. Hypertens. 19 (8) (2005) 597–605. [13] A.J. Scheen, et al., Effects of exercise on neuroendocrine secretions and glucose regulation at different times of day, Am J Physiol 274 (6 Pt 1) (1998) E1040–E1049. [14] H. Nygaard, S.E. Tomten, A.T. Hostmark, Slow postmeal walking reduces postprandial glycemia in middle-aged women, Appl Physiol Nutr Metab 34 (6) (2009) 1087–1092. [15] A.T. Hostmark, et al., Postprandial light physical activity blunts the blood glucose increase, Prev. Med. 42 (5) (2006) 369–371. [16] L.H. Enevoldsen, et al., The combined effects of exercise and food intake on adipose tissue and splanchnic metabolism, J. Physiol. 561 (Pt 3) (2004) 871–882. [17] J. Haxhi, A. Scotto Di Palumbo, M. Sacchetti, Exercising for metabolic control: is timing important? Ann Nutr Metab 62 (1) (2013) 14–25. [18] K.T. Borer, et al., Two bouts of exercise before meals, but not after meals, lower fasting blood glucose, Med. Sci. Sports Exerc. 41 (8) (2009) 1606–1614. [19] H.E. Aldred, I.C. Perry, A.E. Hardman, The effect of a single bout of brisk walking on postprandial lipemia in normolipidemic young adults, Metabolism 43 (7) (1994) 836–841. [20] P. Bennard, E. Doucet, Acute effects of exercise timing and breakfast meal glycemic index on exercise-induced fat oxidation, Appl Physiol Nutr Metab 31 (5) (2006) 502–511. [21] M. Pomerleau, et al., Effects of exercise intensity on food intake and appetite in women, Am J Clin Nutr 80 (5) (2004) 1230–1236. [22] M.S. Moore, et al., Short-term appetite and energy intake following imposed exercise in 9- to 10-year-old girls, Appetite 43 (2) (2004) 127–134. [23] CSEP. Canadian Society of Exercise Physiology. [cited 2014 July]; Available from: http://www.csep.ca/CMFiles/publications/parq/Q-AAP.pdf. [24] H.D. McCarthy, K.V. Jarrett, H.F. Crawley, The development of waist circumference percentiles in British children aged 5.0–16.9 y, Eur. J. Clin. Nutr. 55 (10) (2001) 902–907. [25] M.E.J. Lean, T.S. Han, C.E. Morrison, Waist circumference as a measure for indicating need for weight management, Br. Med. J. 311 (6998) (1995) 158–161. [26] D.C.W. Lau, et al., 2006 Canadian clinical practice guidelines on the management and prevention of obesity in adults and children [summary], Can. Med. Assoc. J. 176 (8) (2007) S1–S13. [27] R.J. Kuczmarski, et al., CDC Growth Charts for the United States: methods and development, Vital Health Stat 11 2002 (246) (2000) 1–190. [28] L.A. Leger, et al., The multistage 20 metre shuttle run test for aerobic fitness, J. Sports Sci. 6 (2) (1988) 93–101. [29] S.M. Paridon, et al., Clinical stress testing in the pediatric age group — a statement from the American Heart Association Council on cardiovascular disease in the young, committee on atherosclerosis, hypertension, and obesity in youth, Circulation 113 (15) (2006) 1905–1920.
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[30] K. Arvaniti, D. Richard, A. Tremblay, Reproducibility of energy and macronutrient intake and related substrate oxidation rates in a buffet-type meal, Br J Nutr 83 (5) (2000) 489–495. [31] A.J. Hill, J.E. Blundell, The effects of a high-protein or high-carbohydrate meal on subjective motivation to eat and food preferences, Nutr. Behav. 3 (1986) 133–144. [32] A. Flint, et al., Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies, Int. J. Obes. Relat. Metab. Disord. 24 (1) (2000) 38–48. [33] J.P. Chaput, et al., Comparison of 150-mm versus 100-mm visual analogue scales in free living adult subjects, Appetite 54 (3) (2010) 583–586. [34] V. Drapeau, et al., Appetite sensations as a marker of overall intake, Br J Nutr 93 (2) (2005) 273–280. [35] F. Péronnet, D. Massicote, Table of nonprotein respiratory quotient: an update, Can J Sport Sci 16 (1) (1991) 23–29. [36] M.M. Schubert, et al., Acute exercise and subsequent energy intake. A meta-analysis, Appetite 63 (2013) 92–104. [37] J.E. Donnelly, et al., Does increased exercise or physical activity alter ad-libitum daily energy intake or macronutrient composition in healthy adults? A systematic review, PLoS One 9 (1) (2014) e83498. [38] K. Deighton, J.C. Zahra, D.J. Stensel, Appetite, energy intake and resting metabolic responses to 60 min treadmill running performed in a fasted versus a postprandial state, Appetite 58 (3) (2012) 946–954. [39] D. Thivel, et al., Gender effect on exercise-induced energy intake modification among obese adolescents, Appetite 56 (3) (2011) 658–661. [40] D. Thivel, J.P. Chaput, Are post-exercise appetite sensations and energy intake coupled in children and adolescents? Sports Med. 44 (6) (2014) 735–741. [41] D. Thivel, et al., Obese but not lean adolescents spontaneously decrease energy intake after intensive exercise, Physiol. Behav. 123 (2014) 41–46. [42] E. Bryant, et al., The influence of acute exercice on linking and preferences for food on high trait disinhibition women, Obesity Review 17 (2006) 343.
[43] L. Hooper, et al., Effect of reducing total fat intake on body weight: systematic review and meta-analysis of randomised controlled trials and cohort studies, BMJ 345 (2012) e7666. [44] G. Finlayson, et al., Low fat loss response after medium-term supervised exercise in obese is associated with exercise-induced increase in food reward, J. Obes. 2011 (2011). [45] V.A. George, A. Morganstein, Effect of moderate intensity exercise on acute energy intake in normal and overweight females, Appetite 40 (1) (2003) 43–46. [46] H.R. Kissileff, et al., Acute effects of exercise on food intake in obese and nonobese women, Am J Clin Nutr 52 (2) (1990) 240–245. [47] J.A. Douglas, et al., Appetite, appetite hormone and energy intake responses to two consecutive days of aerobic exercise in healthy young men, Appetite 92 (2015) 57–65. [48] M.E. Riou, et al., Predictors of energy compensation during exercise interventions: a systematic review, Nutrients 7 (5) (2015) 3677–3704. [49] J. McNeil, et al., Reproducibility of a food menu to measure energy and macronutrient intakes in a laboratory and under real-life conditions, Br J Nutr 108 (7) (2012) 1316–1324. [50] N.M. Farah, J.M. Brunstrom, J.M. Gill, Using a novel computer-based approach to assess the acute effects of exercise on appetite-related measures, Appetite 58 (1) (2012) 196–204. [51] S.A. Alkahtani, et al., Interval training intensity affects energy intake compensation in obese men, Int J Sport Nutr Exerc Metab 24 (6) (2014) 595–604. [52] N.A. King, et al., Effects of short-term exercise on appetite responses in unrestrained females, Eur. J. Clin. Nutr. 50 (10) (1996) 663–667. [53] J.A. King, L.K. Wasse, D.J. Stensel, The acute effects of swimming on appetite, food intake, and plasma acylated ghrelin, J. Obes. 2011 (2011).
Contents lists available at ScienceDirect
Physiology & Behavior journal homepage: www.elsevier.com/locate/phb
Timing of moderate-to-vigorous exercise and its impact on subsequent energy intake in young males Marie-Helene Albert a,b, Vicky Drapeau c,d, Marie-Eve Mathieu a,b,⁎ a
Department of Kinesiology, University of Montreal, 2100 Edouard-Montpetit, Montreal H3C 3J7, Canada Sainte-Justine UHC Research Center, 5757 Decelles, Montreal H3T 1C5, Canada Department of Physical Education, University Laval, Sport and Physical Education Building, Quebec G1V 0A6, Canada d University Institute of Cardiology and Pneumology of Quebec, 2725, Sainte-Foy Road, Quebec G1V 4G5, Canada b c
H I G H L I G H T S • • • •
The impact of exercise timing on energy intake has been previously unknown. An exercise session closer to a meal reduces subsequent energy and lipid intake. In this context, appetite was not linked to actual ingestion. Timing appears to potentially affect energy balance.
a r t i c l e
i n f o
Article history: Received 30 June 2015 Received in revised form 2 August 2015 Accepted 22 August 2015 Available online 29 August 2015 Keywords: Physical activity Energy intake Energy balance Adolescents Obesity
a b s t r a c t Exercise can suppress appetite and energy intake but the impact of the timing of exercise remains unknown. Knowing that orexigenic hormone levels decrease during exercise but rapidly increase afterward, the aim of the current study was to investigate whether energy intake is increasingly reduced when exercise immediately precedes a meal compared to when a delay occurs between the exercise and the meal. Non-obese boys (15– 20 years old; N = 12) were individually evaluated while performing two randomly assigned experimental visits: 1) a 30-min exercise session of moderate-to-vigorous intensity followed immediately by an ad libitum buffet at 12 PM and 2), an identical session followed by a 135-min waiting period and an ad libitum buffet-type meal at 12 PM. In both conditions, a snack in the afternoon and a second ad libitum buffet-type meal at 5 PM were served. Findings showed that hunger ratings were similar under both conditions. The exercise session immediately prior to the meal compared with the condition with a N 2 h delay led to reduction of 11% and 23% in overall and lipid energy intakes at lunch, respectively (P-values N 0.05). No significant differences were found in the energy intakes from the afternoon snack and dinner. Apart from lipids at lunch, the proportions of energy from the various macronutrients at each meal were similar. This study reveals that being physically active before a meal plays a role in acute energy intake reduction when a shorter delay is present between exercise and a meal. In addition, the absence of compensation over several hours is noteworthy. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Energy balance is central to body weight control, with energy expenditure and energy intake (EI) independently contributing to energy balance [1]. Interestingly, energy expenditure can also influence energy balance by having an indirect impact via EI. It is currently known that a longer duration, higher intensity and a selection of cardiovascular
⁎ Corresponding author at: Department of Kinesiology, University of Montreal, Room 8223. P.O. Box 6128, Downtown Station, Montreal, H3C 3J7 Quebec, Canada. E-mail addresses: [email protected] (M.-H. Albert), [email protected] (V. Drapeau), [email protected] (M.-E. Mathieu).
http://dx.doi.org/10.1016/j.physbeh.2015.08.030 0031-9384/© 2015 Elsevier Inc. All rights reserved.
rather than resistance exercises can help reduce subsequent hunger, appetite and EI, thereby creating an acute energy deficit [2–7]. Among the mechanisms investigated in this exercise-induced anorexia, changes in acylated ghrelin levels are revealing. A reduction in levels of this orexigenic hormone has been reported during and after exercise, coinciding with hunger and appetite reductions [8–10]. However, hunger and acylated ghrelin levels rapidly increase during the recovery period following exercise [3,8,9]. These observations are in line with the delay in the onset of a meal observed following exercise compared to no exercise [2,11]. These findings suggest that the anorexigenic effect of exercise is transitory and that a window of opportunity might exist that more substantially reduces EI following exercise.
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The timing of physical activity is a relatively novel concept; recent studies address its significance in enhancing cardiometabolic health outcomes. For example, exercising at night reduces blood pressure to a greater extent than morning exercise in hypertensive patients that are usually resistant to the hypotensive effects of exercise [12]. Greater reductions in blood glucose and lipid levels have also been found following night time exercise or when exercise strategically occurs around mealtime [13–19], while enhanced lipid oxidation can occur following morning exercise or fasting [16,20]. To date, the effect of the timing of exercise on energy balance through EI remains unknown. In studies on the anorexigenic effect of exercise, a meal is served either shortly after the end of exercise (b 15 min) [6], within 1 h following exercise [4,10,21,22] or more than 1 h after exercise [8,22]. However, no study has compared the timing as it relates to meals. As a result, the main purpose of the current study was to confirm the hypothesis that EI is reduced when exercise immediately precedes lunch compared to when a delay occurs between exercise and lunch. 2. Materials and methods 2.1. Participants Twelve non-obese males aged between 15 and 20 years old were recruited to participate in this crossover study. The participants met the following exclusion criteria: they were not on any specific diet; did not have a diagnosis of anorexia, bulimia or any metabolic disease; were not taking any medication that could influence appetite; did not have any intestinal disorders and were able to communicate in French. The consent form was approved by the Sainte-Justine University Hospital Centre ethics committee and a physical activity readiness questionnaire [23] was completed by the participants and parents/tutors of minors. After a first preliminary visit, two additional experimental visits were randomly conducted. The participants were presented with a false scenario (hypothesis): the study of cardiac response to exercise, rest and caloric intake to prevent influence on the main outcome of the study (EI); they were asked to wear a heart rate monitor to enhance credibility. Financial compensation ($12 CAN) was provided after each visit. A final consent form indicating the real purpose of the study was administered at the end of the last visit. All participants consented to further use of the data collected.
2.3. Experimental visits Each participant took part in two experimental visits in a counterbalanced measures design with ≥5 and b 21 days between trials using ExMeal and ExdelayMeal (Fig. 1). During ExMeal, the exercise was followed within 15 min by a buffet-type meal. In the ExdelayMeal, the exercise was followed by a waiting period of 135 min before the buffettype meal. This was important for assessing the timing effect since it allowed a comparison of the two Ex sessions performed with the same two meals and with a maximum time difference between them. At 7:00 AM and after an overnight fast, the participants ate at home the standard breakfast provided. It contained ~ 2993 kJ and was composed of white bread (100 g), smooth peanut butter (18 g), orange juice (200 ml), butter (6 g) and cheddar cheese (42 g). Arrival at the laboratory was scheduled for 8:45 AM and compliance with breakfast (start time, duration and consumption of the complete meal provided and nothing more) was confirmed by the participant to the research team. The testing sequence started at 9:00 AM. It included a 30-min moderate-to-vigorous exercise session on the treadmill at 70% maximal oxygen uptake according to the experimental visit either early (9:00 AM) or late (11:15 AM) morning (Fig. 1). Sedentary activities (puzzles, Sudoku, hidden word games, books and listening to personal music) were performed during the morning waiting periods. The order and duration of each activity of the first visit were repeated during the second visit. The first ad libitum buffet-type meal was served at 12:00 PM and the second at 5:00 PM. Between meals, participants remained in or around the laboratory while wearing an NL1000 DigiWalker® pedometer (New-Lifestyles®, Lees Summit, MO, USA) while carrying a prepared snack. 2.4. Energy intake and appetite sensations An ad libitum buffet-type meal composed of 38 liquid and solid items based on a buffet described by Arvaniti et al. (2000) [30] was served at lunch. In the afternoon, each participant was given an ad libitum snack of cheese (~ 50 g), crackers (~ 25 g) and carrots (~ 75 g). At 5:00 PM, the ad libitum buffet was comprised of 35 items (similar to the items included in the lunch buffet, but without the snack items), and one hot meal selected by the participant for both conditions (macaroni and
2.2. Preliminary visit Body mass was measured to the nearest 0.1 kg and body fat percentage determined by bioimpedance analysis on a Tanita BC-418 Segmental Body Composition Analyzer (Tanita Corporation of America Inc., Arlington Heights, IL, USA). Height and waist circumference were measured to the nearest 0.5 cm. The absence of abdominal obesity was confirmed using a waist circumference criterion specific to young [24] and adult [25] subjects. Body mass index (BMI, in kg m−2) was calculated: participants had a BMI percentile ≤ 85th age and sex-specific percentile according to the Centers for Disease Control and Prevention curve (b18 y) or a BMI value ≤ 25 kg m−2 (≥18 y) [26,27]. Maximum oxygen uptake was measured by indirect calorimetry using a Quark CPET system (COSMED Srl, Rome, Italy). A progressive maximal test on a treadmill adapted from the shuttle test was performed [28]. The test started at 6 km h−1 and increased by 1 km h−1 every 2 min. Maximum effort was confirmed by a respiratory exchange ratio (carbon dioxide production·oxygen consumption−1) ≥ 1.1 and/or a maximum heart rate ≥ 200 beats min−1 [29]. These results were used to determine the running speed required for subsequent exercise sessions performed at 70% of individual maximum oxygen uptake. After the running test, each participant was invited to eat from a 38-item ad libitum buffet type meal (see description below) to provide an initial exposure to food prior to the experiment.
Fig. 1. Detailed protocol of experimental visits.
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cheese, fettuccini Alfredo or three-mushroom risotto). Lunch and dinner were served in a private room with the same presentation and controlled ambient conditions (light and temperature). The food was weighed before and after meals without participant knowledge. During the entire protocol, participants were instructed to eat only the provided food and drink as usual until satiation. Visual analog scales were completed by the participants upon their arrival at the laboratory as well as before and after lunch and dinner (Fig. 1). The desire to eat, hunger, fullness, anticipated food consumption, desire for specific food types (sweet, fatty, salty and savory) as well as meal palatability, appreciation and visual appeal [31,32] were rated with a validated range of 100 mm [33]. The satiety quotient, a marker of an individual's satiation efficiency, was calculated for lunch and dinner using hunger ratings as follows [34]: −1 Satiety quotient mm kJ ¼
½Pre‐meal ASðmmÞ–Post‐meal ASðmmÞ 100: Energy content of meal ðkJÞ
2.5. Energy expenditure Indirect calorimetry with prior calibration according to manufacturer instructions was used to confirm the equivalent energy expended during the exercise sessions (Quark CPET). Volume and gas compositions were measured during a 10-min period in the middle of each exercise of constant intensity. Energy expenditure was calculated using the formula by Péronnet and Massicotte [35]. 2.6. Statistics The Shapiro–Wilk test was used to confirm normality of data. EI and macronutrient compositions between the two experimental conditions were investigated at each timepoint using paired t-tests. The areas under the curve (AUC) of appetite sensations were calculated for each condition using the trapezoidal rule based on five time points (8:45 AM, 11:45 AM, 12:30 PM, 4:45 PM and 5:30 PM; Fig. 1). Pearson correlations were used to investigate the association between appetite sensations and EI specific to each condition, including sensations and the intake of carbohydrates and lipids. The values presented are the means ± standard deviations (minimum–maximum values) unless otherwise specified. Statistical significance was set at a P-value of 0.05. The data were analyzed using the Statistical Package for the Social Science software version 20 for Mac (IBM Corporation, Armonk, NY). 3. Results The 12 participants were 17.7 ± 1.6 (15.0–20.0) years of age, had a BMI of 23.1 ± 3.1 (19.9–29.0) kg m− 2 with 15.6 ± 5.4 (7.9–30.4) % body fat and a mean waist circumference of 78.5 ± 7.3 (71.0–93.0) cm. All participants were non-obese based on BMI and waist circumference selection criteria. The maximal oxygen uptake was 49.0 ± 5.3 (40.6–59.4) ml kg−1 min−1 and the exercise sessions performed on a treadmill at 70% of the maximum oxygen uptake corresponding to an average speed of 9.6 ± 1.1 (8.0–11.0) km h−1. Each participant complied with the standardized breakfast as requested (time and content). Both experimental conditions led to similar energy expenditure during the exercise sessions and to a similar level of physical activity in the afternoon period as monitored by step count (Table 1). 3.1. Energy and macronutrient intakes A significant difference in EI was measured at lunch between the two experimental conditions, with 646 fewer kilojoules ingested when the exercise immediately preceded lunch compared to when a
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Table 1 Energy expenditure, energy intake and macronutrient profile of the meals.
Energy expenditure of the exercise session, kJ # Steps Energy intake, kJ Lunch Snack Dinner Macronutrient profile, % Lunch Lipids Carbohydrates Proteins Snack Lipids Carbohydrates Proteins Dinner Lipids Carbohydrates Proteins
ExMeal
ExdelayMeal
P-value
1643 (211)
1657 (173)
0.836
4557 (2394) 4823 (2427) 0.627 5072 (1033) 5718 (1343) 0.043 955 (413) 1084 (347) 0.236 4678 (1490) 4632 (1950) 0.925
32.2 (7.04) 49.9 (9.8) 18.8 (4.2)
36.4 (8.8) 45.9 (9.4) 17.6 (3.7)
0.076 0.126 0.242
47.0 (6.3) 31.0 (18.3) 21.9 (13.2)
46.5 (3.1) 34.7 (10.9) 18.8 (9.1)
0.747 0.421 0.317
28.2 (10.2) 57.9 (10.1) 14.0 (3.4)
29.8 (6.4) 54.8 (8.3) 15.4 (5.6)
0.553 0.219 0.293
ExMeal: exercise immediately preceding lunch; ExdelayMeal: exercise followed by a pause before lunch; values are mean (standard deviation).
delay occurred between exercise and lunch (Table 1). No significant differences in EI between ExMeal and ExdelayMeal were found for subsequent meals (Table 1). The macronutrient profile revealed that the intake of energy from lipids was significantly lower at lunch for ExMeal compared to ExdelayMeal by 23% (Fig. 2). When reported as their relative contribution to the meal, a tendency was observed for lipids to contribute less (by 12%) to the total energy content in ExMeal compared to ExdelayMeal (Table 1). The absolute and relative contributions were similar between the conditions for the other macronutrients at lunch (proteins and carbohydrates) as well as for all of the macronutrients at snack and dinner times (Table 1 & Fig. 2). 3.2. Appetite sensations and satiety quotient No differences in the appetite sensations profile, represented by the area under the curve, were observed between conditions for hunger, desire to eat, fullness and anticipated food consumption (Table 2). The individuals' satiation efficiencies were also similar at both meals (lunch and dinner) as revealed by similar satiety quotients (Table 2). The desires for sweet, salty, savory and fatty food were significantly different for sweet food, with a lower score for the ExMeal condition (P = 0.067; Table 2). Three significant associations between pre-meal appetite sensations and subsequent EI at lunch were noted. First, EI was negatively correlated with the savory score of the meal (− 0.678; P = 0.015) in the Exdelaymeal condition. Second, the preference for sweet food was negatively correlated with the proportion of EI via carbohydrates in both ExMeal (r = − 0.663; P = 0.019) and ExdelayMeal (r = − 0.641; P = 0.025) conditions. Third, no other associations between appetite sensations preceding each meal and subsequent EI were significant for the ExMeal or the ExdelayMeal conditions both at lunch and dinner (all P values N 0.05; data not shown). 4. Discussion Strategies to control body weight are constantly evolving towards improved effectiveness. Recent meta-analyses and systematic reviews on the anorexigenic effect of exercise underline the fact that when the impact of exercise on EI reduction is present, it however remains limited [36,37]. Among the various approaches to exercise investigated such as duration of exercise, not all were optimal [37] and none considered the
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Fig. 2. Macronutrients intake when the exercise immediately precedes lunch (ExMeal) and when a delay occurs between exercise and lunch (ExdelayMeal). Values presented are mean ± standard error; *: Significant difference between conditions (P b 0.05).
timing of the exercise as it relates to the timing of the meal. While timing of exercise is mostly recognized for its enhanced cardiometabolic effects [17], the current study is the first study of its kind to specifically address the importance of timing for EI. Results of this study revealed that in young normal-weight males, a reduced caloric intake occurred when exercise was performed immediately prior to lunch compared to delayed exercise and meal. Interestingly, this was observed mainly in a reduction in lipid consumption without increased hunger and without a rebound in EI later during the day. The concept that an anorexigenic effect can explain the suppression of hunger by exercise was first raised approximately 20 years ago [2]. Since then, the short-lived characteristics of the anorexigenic effect have been supported by the following: 1) hunger ratings, which decrease during exercise but return to control levels within minutes during the post-exercise period [2,3,14,16] and 2), a delay in the natural onset of the meal after exercise [2]. The current study demonstrates that the timing of exercise can have a specific impact on subsequent EI; a significant reduction (11%) in EI was measured when no delay was introduced between the exercise session and the meal. Visual analog scales are commonly used to monitor anorexigenic effects in this area of research [2,14,16]. However, the current study and others [6,21,38–41] suggest that that they are not necessarily the best method to predict EI. Total energy intake at the ad libitum buffettype meal contradicted appetite sensation ratings, including AUC. An interesting finding included a reduction in EI for the ExMeal condition that did not lead to increased hunger ratings. Examination of macronutrient intake also revealed discrepancies with subjective ratings: 1) the greater the desire to eat something sweet, the lower was the actual intake of carbohydrates in both conditions; 2) the less savory foods were rated, the more calories were ingested in the ExdelayMeal condition; 3) no association was found between intake of lipids and related VAS scores under both conditions. However, this study found that the intake of calories from lipids at lunch was 23% lower when the meal was immediately preceded by exercise. This significant difference in macronutrient intake corroborates previous findings showing an increased interest towards lowfat food following exercise [42], and that lipid reduction is a more frequently reported change in macronutrient with increased exercise [37]. Such a reduction can be of interest, since reduced intake of lipids contributes to improved weight outcomes [43] and could respond positively to an exercise regimen [44].
The residual effects on the remaining meals go beyond the immediate impact of exercise. In the current case, the afternoon snack and dinner were similar in both conditions in terms of caloric content and macronutrients composition. The timing of exercise thus appears to specifically target only one meal (i.e., the one immediately following the training session). The absence of short-term EI compensation (i.e., no subsequent increase in energy intake at meals following lunch in the ExMeal condition) is also noteworthy. Extrapolation of these findings to a prolong period of time could indicate that the optimal timing of exercise before meals can potentially lead to better body weight outcomes based on the same time and effort investments. Further studies are required to confirm these assumptions given that: 1) normalweight males were tested in the current study; a population known to better respond to the anorexigenic effects of exercise [2,21,22,45,46]; 2) the absence of compensation for the anorexigenic effects of exercise was not tested beyond two days of exercise [47] but was expected to take place at some point [48]; and 3) ad-libitum meals in the laboratory were similar to a real-life setting [49] but might not reflect the real-life ingestion context over a prolong period of time [50]. Current preliminary findings showing reduced EI with optimal exercise timing now justify the assessment of the underlying mechanisms of this relationship, such as the orexigenic and anorexigenic hormonal responses [36,37]. It also supports the desire to better understand the role of exercise timing for the primary and secondary prevention of excess adiposity. The limits of the current study are a small sample size, the narrow age group that limited extrapolations to younger and older individuals and the use of a two-condition protocol. Studies with numerous conditions, including a non-exercise condition, should be undertaken to refine these concepts [3,51] and could be used to identify the optimal timing of exercise with respect to meals. Nevertheless, two-condition protocols have been frequently used in the field of anorexigenic effects of exercise, especially in the earlier stages, such as studies on rest vs. exercise [8,41,47,52,53], low vs. greater duration [2] or comparison of exercise intensities [2,6]. 5. Conclusion In the area of the anorexigenic effects of exercise, the current study suggests for the first time that there might be an optimal time to schedule exercise. Exercise immediately before a meal resulted in young normal-weight males eating fewer calories and lipids compared to a
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the statistical analysis, wrote the paper and had the primary responsibility for the final content of the paper.
Table 2 Appetite sensations area under the curve and associated time points value.
Hunger AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Satiety AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Fullness AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Prospective food consumption AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something sweet AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something salty AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something savory AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm Desire to eat something fatty AUC, mm Value at 8:45 AM, mm Value at 11:45 AM, mm Value at 12:30 PM, mm Value at 4:45 PM, mm Value at 5:30 PM, mm
561
ExMeal
ExDelayMeal
P value
280 (134) 25 (17) 64 (20) 8 (7) 54 (21) 9 (10) 289 (172) 33 (25) 68 (18) 8 (8) 57 (20) 12 (14) 412 (194) 54 (21) 35 (23) 86 (12) 48 (22) 87 (17) 311 (161) 41 (23) 62 (18) 13 (12) 58 (18) 12 (15) 393 (219) 52 (33) 45 (30) 77 (25) 40 (33) 81 (21) 415 (314) 64 (29) 44 (28) 84 (14) 50 (28) 89 (8) 324 (297) 53 (26) 36 (19) 85 (14) 28 (24) 81 (21) 466 (353) 70 (23) 53 (28) 90 (9) 55 (29) 90 (10)
321 (85) 23 (19) 73 (19) 11 (7) 48 (22) 6 (6) 340 (82) 27 (25) 76 (15) 11 (12) 51 (18) 5 (5) 504 (94) 65 (15) 28 (21) 78 (25) 50 (20) 90 (8) 365 (79) 38 (22) 71 (18) 14 (10) 54 (19) 9 (8) 531 (144) 56 (26) 46 (27) 77 (20) 55 (28) 84 (20) 523 (172) 60 (24) 43 (29) 79 (18) 50 (28) 83 (17) 435 (144) 54 (29) 27 (22) 76 (20) 32 (23) 90 (9) 596 (146) 67 (30) 53 (27) 89 (7) 56 (29) 93 (6)
0.338
Acknowledgments We thank all of the participants who took part in this study and the CIRCUIT center for laboratory support. We also thank research assistants Papineau and Portelance.
0.394
References
0.174
0.318
0.067
0.166
0.172
0.132
ExMeal: exercise immediately preceding lunch; ExdelayMeal: exercise followed by a pause before lunch; AUC: area under the curve; values are mean (standard deviation).
delay between exercise and meal. Further studies will be needed to confirm this important finding, especially in other populations, over a longer period of time and in free-living conditions. Financial support The Foundation of Stars, Sainte-Justine UHC (Canada), provided financial support for the purchase of food and beverages and financial compensation for the participants via a grant to Pr. Mathieu. Conflict of interest None. Authorship The authors' responsibilities were as follows: MHA designed and conducted the research, analyzed the data and performed the statistical analysis and wrote the paper; VD designed the research and wrote the paper; MEM designed the research, analyzed the data and performed
[1] K.D. Hall, et al., Energy balance and its components: implications for body weight regulation, Am J Clin Nutr 95 (4) (2012) 989–994. [2] N.A. King, V.J. Burley, J.E. Blundell, Exercise-induced suppression of appetite: effects on food intake and implications for energy balance, Eur. J. Clin. Nutr. 48 (10) (1994) 715–724. [3] D.R. Broom, et al., Influence of resistance and aerobic exercise on hunger, circulating levels of acylated ghrelin, and peptide YY in healthy males, Am J Physiol Regul Integr Comp Physiol 296 (1) (2009) R29–R35. [4] D.A. Thompson, L.A. Wolfe, R. Eikelboom, Acute effects of exercise intensity on appetite in young men, Med. Sci. Sports Exerc. 20 (3) (1988) 222–227. [5] D.J. Laan, et al., Effects and reproducibility of aerobic and resistance exercise on appetite and energy intake in young, physically active adults, Appl Physiol Nutr Metab 35 (6) (2010) 842–847. [6] P. Imbeault, et al., Acute effects of exercise on energy intake and feeding behaviour, Br J Nutr 77 (4) (1997) 511–521. [7] J. Carnier, et al., Aerobic training (AT) is more effective than aerobic plus resistance training (AT + RT) to improve anorexigenic/orexigenic factors in obese adolescents, Appetite 69 (2013) 168–173. [8] D.R. Broom, et al., Exercise-induced suppression of acylated ghrelin in humans, J. Appl. Physiol. 102 (6) (2007) 2165–2171. [9] G.F. Becker, et al., Combined effects of aerobic exercise and high-carbohydrate meal on plasma acylated ghrelin and levels of hunger, Appl Physiol Nutr Metab 37 (1) (2012) 184–192. [10] J.A. King, et al., Influence of prolonged treadmill running on appetite, energy intake and circulating concentrations of acylated ghrelin, Appetite 54 (3) (2010) 492–498. [11] J.A. King, L.K. Wasse, D.J. Stensel, Acute exercise increases feeding latency in healthy normal weight young males but does not alter energy intake, Appetite 61 (1) (2013) 45–51. [12] S. Park, C.A. Jastremski, J.P. Wallace, Time of day for exercise on blood pressure reduction in dipping and nondipping hypertension, J. Hum. Hypertens. 19 (8) (2005) 597–605. [13] A.J. Scheen, et al., Effects of exercise on neuroendocrine secretions and glucose regulation at different times of day, Am J Physiol 274 (6 Pt 1) (1998) E1040–E1049. [14] H. Nygaard, S.E. Tomten, A.T. Hostmark, Slow postmeal walking reduces postprandial glycemia in middle-aged women, Appl Physiol Nutr Metab 34 (6) (2009) 1087–1092. [15] A.T. Hostmark, et al., Postprandial light physical activity blunts the blood glucose increase, Prev. Med. 42 (5) (2006) 369–371. [16] L.H. Enevoldsen, et al., The combined effects of exercise and food intake on adipose tissue and splanchnic metabolism, J. Physiol. 561 (Pt 3) (2004) 871–882. [17] J. Haxhi, A. Scotto Di Palumbo, M. Sacchetti, Exercising for metabolic control: is timing important? Ann Nutr Metab 62 (1) (2013) 14–25. [18] K.T. Borer, et al., Two bouts of exercise before meals, but not after meals, lower fasting blood glucose, Med. Sci. Sports Exerc. 41 (8) (2009) 1606–1614. [19] H.E. Aldred, I.C. Perry, A.E. Hardman, The effect of a single bout of brisk walking on postprandial lipemia in normolipidemic young adults, Metabolism 43 (7) (1994) 836–841. [20] P. Bennard, E. Doucet, Acute effects of exercise timing and breakfast meal glycemic index on exercise-induced fat oxidation, Appl Physiol Nutr Metab 31 (5) (2006) 502–511. [21] M. Pomerleau, et al., Effects of exercise intensity on food intake and appetite in women, Am J Clin Nutr 80 (5) (2004) 1230–1236. [22] M.S. Moore, et al., Short-term appetite and energy intake following imposed exercise in 9- to 10-year-old girls, Appetite 43 (2) (2004) 127–134. [23] CSEP. Canadian Society of Exercise Physiology. [cited 2014 July]; Available from: http://www.csep.ca/CMFiles/publications/parq/Q-AAP.pdf. [24] H.D. McCarthy, K.V. Jarrett, H.F. Crawley, The development of waist circumference percentiles in British children aged 5.0–16.9 y, Eur. J. Clin. Nutr. 55 (10) (2001) 902–907. [25] M.E.J. Lean, T.S. Han, C.E. Morrison, Waist circumference as a measure for indicating need for weight management, Br. Med. J. 311 (6998) (1995) 158–161. [26] D.C.W. Lau, et al., 2006 Canadian clinical practice guidelines on the management and prevention of obesity in adults and children [summary], Can. Med. Assoc. J. 176 (8) (2007) S1–S13. [27] R.J. Kuczmarski, et al., CDC Growth Charts for the United States: methods and development, Vital Health Stat 11 2002 (246) (2000) 1–190. [28] L.A. Leger, et al., The multistage 20 metre shuttle run test for aerobic fitness, J. Sports Sci. 6 (2) (1988) 93–101. [29] S.M. Paridon, et al., Clinical stress testing in the pediatric age group — a statement from the American Heart Association Council on cardiovascular disease in the young, committee on atherosclerosis, hypertension, and obesity in youth, Circulation 113 (15) (2006) 1905–1920.
562
M.-H. Albert et al. / Physiology & Behavior 151 (2015) 557–562
[30] K. Arvaniti, D. Richard, A. Tremblay, Reproducibility of energy and macronutrient intake and related substrate oxidation rates in a buffet-type meal, Br J Nutr 83 (5) (2000) 489–495. [31] A.J. Hill, J.E. Blundell, The effects of a high-protein or high-carbohydrate meal on subjective motivation to eat and food preferences, Nutr. Behav. 3 (1986) 133–144. [32] A. Flint, et al., Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies, Int. J. Obes. Relat. Metab. Disord. 24 (1) (2000) 38–48. [33] J.P. Chaput, et al., Comparison of 150-mm versus 100-mm visual analogue scales in free living adult subjects, Appetite 54 (3) (2010) 583–586. [34] V. Drapeau, et al., Appetite sensations as a marker of overall intake, Br J Nutr 93 (2) (2005) 273–280. [35] F. Péronnet, D. Massicote, Table of nonprotein respiratory quotient: an update, Can J Sport Sci 16 (1) (1991) 23–29. [36] M.M. Schubert, et al., Acute exercise and subsequent energy intake. A meta-analysis, Appetite 63 (2013) 92–104. [37] J.E. Donnelly, et al., Does increased exercise or physical activity alter ad-libitum daily energy intake or macronutrient composition in healthy adults? A systematic review, PLoS One 9 (1) (2014) e83498. [38] K. Deighton, J.C. Zahra, D.J. Stensel, Appetite, energy intake and resting metabolic responses to 60 min treadmill running performed in a fasted versus a postprandial state, Appetite 58 (3) (2012) 946–954. [39] D. Thivel, et al., Gender effect on exercise-induced energy intake modification among obese adolescents, Appetite 56 (3) (2011) 658–661. [40] D. Thivel, J.P. Chaput, Are post-exercise appetite sensations and energy intake coupled in children and adolescents? Sports Med. 44 (6) (2014) 735–741. [41] D. Thivel, et al., Obese but not lean adolescents spontaneously decrease energy intake after intensive exercise, Physiol. Behav. 123 (2014) 41–46. [42] E. Bryant, et al., The influence of acute exercice on linking and preferences for food on high trait disinhibition women, Obesity Review 17 (2006) 343.
[43] L. Hooper, et al., Effect of reducing total fat intake on body weight: systematic review and meta-analysis of randomised controlled trials and cohort studies, BMJ 345 (2012) e7666. [44] G. Finlayson, et al., Low fat loss response after medium-term supervised exercise in obese is associated with exercise-induced increase in food reward, J. Obes. 2011 (2011). [45] V.A. George, A. Morganstein, Effect of moderate intensity exercise on acute energy intake in normal and overweight females, Appetite 40 (1) (2003) 43–46. [46] H.R. Kissileff, et al., Acute effects of exercise on food intake in obese and nonobese women, Am J Clin Nutr 52 (2) (1990) 240–245. [47] J.A. Douglas, et al., Appetite, appetite hormone and energy intake responses to two consecutive days of aerobic exercise in healthy young men, Appetite 92 (2015) 57–65. [48] M.E. Riou, et al., Predictors of energy compensation during exercise interventions: a systematic review, Nutrients 7 (5) (2015) 3677–3704. [49] J. McNeil, et al., Reproducibility of a food menu to measure energy and macronutrient intakes in a laboratory and under real-life conditions, Br J Nutr 108 (7) (2012) 1316–1324. [50] N.M. Farah, J.M. Brunstrom, J.M. Gill, Using a novel computer-based approach to assess the acute effects of exercise on appetite-related measures, Appetite 58 (1) (2012) 196–204. [51] S.A. Alkahtani, et al., Interval training intensity affects energy intake compensation in obese men, Int J Sport Nutr Exerc Metab 24 (6) (2014) 595–604. [52] N.A. King, et al., Effects of short-term exercise on appetite responses in unrestrained females, Eur. J. Clin. Nutr. 50 (10) (1996) 663–667. [53] J.A. King, L.K. Wasse, D.J. Stensel, The acute effects of swimming on appetite, food intake, and plasma acylated ghrelin, J. Obes. 2011 (2011).