Appetite, food intake and gut hormone responses to intense aerobic exercise of different duration

in Journal of Endocrinology

The purpose of the study is to investigate the effect of acute bouts of high-intensity aerobic exercise of differing durations on subjective appetite, food intake and appetite-associated hormones in endurance-trained males. Twelve endurance-trained males (age = 21 ± 2 years; BMI = 21.0 ± 1.6 kg/m2; VO2max = 61.6 ± 6.0 mL/kg/min) completed four trials, within a maximum 28 day period, in a counterbalanced order: resting (REST); 15 min exercise bout (15-min); 30 min exercise bout (30-min) and 45 min exercise bout (45-min). All exercise was completed on a cycle ergometer at an intensity of ~76% VO2max. Sixty minutes post exercise, participants consumed an ad libitum meal. Measures of subjective appetite and blood samples were obtained throughout the morning, with plasma analyzed for acylated ghrelin, total polypeptide tyrosine-tyrosine (PYY) and total glucagon-like peptide 1 (GLP-1) concentrations. The following results were obtained: Neither subjective appetite nor absolute food intake differed between trials. Relative energy intake (intake – expenditure) was significantly greater after REST (2641 ± 1616 kJ) compared with both 30-min (1039 ± 1520 kJ) and 45-min (260 ± 1731 kJ), and significantly greater after 15-min (2699 ± 1239 kJ) compared with 45-min (condition main effect, P < 0.001). GLP-1 concentration increased immediately post exercise in 30-min and 45-min, respectively (condition × time interaction, P < 0.001). Acylated ghrelin was transiently suppressed in all exercise trials (condition × time interaction, P = 0.011); the greatest, most enduring suppression, was observed in 45-min. PYY concentration was unchanged with exercise. In conclusion, high-intensity aerobic cycling lasting up to 45 min did not suppress subjective appetite or affect absolute food intake, but did reduce relative energy intake, in well-trained endurance athletes. Findings question the role of appetite hormones in regulating subjective appetite in the acute post-exercise period.

Abstract

The purpose of the study is to investigate the effect of acute bouts of high-intensity aerobic exercise of differing durations on subjective appetite, food intake and appetite-associated hormones in endurance-trained males. Twelve endurance-trained males (age = 21 ± 2 years; BMI = 21.0 ± 1.6 kg/m2; VO2max = 61.6 ± 6.0 mL/kg/min) completed four trials, within a maximum 28 day period, in a counterbalanced order: resting (REST); 15 min exercise bout (15-min); 30 min exercise bout (30-min) and 45 min exercise bout (45-min). All exercise was completed on a cycle ergometer at an intensity of ~76% VO2max. Sixty minutes post exercise, participants consumed an ad libitum meal. Measures of subjective appetite and blood samples were obtained throughout the morning, with plasma analyzed for acylated ghrelin, total polypeptide tyrosine-tyrosine (PYY) and total glucagon-like peptide 1 (GLP-1) concentrations. The following results were obtained: Neither subjective appetite nor absolute food intake differed between trials. Relative energy intake (intake – expenditure) was significantly greater after REST (2641 ± 1616 kJ) compared with both 30-min (1039 ± 1520 kJ) and 45-min (260 ± 1731 kJ), and significantly greater after 15-min (2699 ± 1239 kJ) compared with 45-min (condition main effect, P < 0.001). GLP-1 concentration increased immediately post exercise in 30-min and 45-min, respectively (condition × time interaction, P < 0.001). Acylated ghrelin was transiently suppressed in all exercise trials (condition × time interaction, P = 0.011); the greatest, most enduring suppression, was observed in 45-min. PYY concentration was unchanged with exercise. In conclusion, high-intensity aerobic cycling lasting up to 45 min did not suppress subjective appetite or affect absolute food intake, but did reduce relative energy intake, in well-trained endurance athletes. Findings question the role of appetite hormones in regulating subjective appetite in the acute post-exercise period.

Introduction

High-intensity aerobic exercise (≥60% VO2max) commonly elicits a transient suppression of appetite in lean, recreationally active individuals (Broom et al. 2007, 2009, Martins et al. 2007, Ueda et al. 2009a,b, King et al. 2010). This phenomenon, termed the ‘anorexia of exercise’ (King et al. 1994), is often coupled with anorexigenic changes in appetite-associated hormones (Schubert et al. 2014).

While the exercise intensity dependency of post-exercise appetite suppression appears well established, the effect of the duration of exercise is yet to be comprehensively investigated. Suppressions in appetite, accompanied by increases in the plasma concentration of satiety peptides peptide tyrosine–tyrosine (PYY) and glucagon-like peptide 1 (GLP-1) have been observed with continuous, high-intensity aerobic bouts of exercise lasting as little as 30 min (Ueda et al. 2009a), and with intermittent exercise bouts yielding energy expenditure values of as little as ~150 kcal (~628 kJ) (Deighton et al. 2013a). Conversely, bouts of very low energy cost (~51 kcal (213 kJ)) have elicited increases in subjective appetite (Bellissimo et al. 2007). In contrast, appetite has been shown to be unaffected after continuous exercise bouts lasting as long as 90 min (King et al. 2011a). When directly comparing exercise of different durations, Erdman and coworkers observed an increase in total ghrelin with low intensity exercise (cycling at 50 W), lasting 30, 60 and 120 min, that was not duration dependent (Erdmann et al. 2007). Similarly, Broom and coworkers observed a comparable immediate post-exercise suppression of hunger and acylated ghrelin after 45 min and 90 min of aerobic exercise at 70% VO2max; however, the suppression was more enduring after the 90 min bout (Broom et al. 2017). It remains unknown whether any of the appetite-associated hormones are released in a dose–response manner to exercise duration or energy cost, or whether there is a duration or energy cost threshold for a hormonal response.

The transient nature of both a suppression of subjective appetite and changes in plasma appetite-associated hormone concentration means that ad libitum food intake can be reduced when administered in close proximity to the cessation of exercise (~10 min (Westerterp-Plantenga et al. 1997); ~15 min (Kissileff et al. 1990); ~30 min (Ueda et al. 2009a); ~60 min (Ueda et al. 2009b)), but is largely unaffected when a meal is consumed ≥60 min after exercise (Thompson et al. 1988, King et al. 1997, 2010, 2011b, Martins et al. 2007, Schubert et al. 2013).

The majority of previous studies have used study populations of recreationally active individuals, and the study of trained individuals is limited (Howe et al. 2016). Trained endurance athletes regularly complete very strenuous bouts of exercise that are of high intensity, long duration and continuous in nature. It is yet to be confirmed whether appetite responses to such strenuous bouts in athletic populations is akin to exercise of a less strenuous nature in untrained individuals. It is possible that a more strenuous bout of exercise may elicit a greater and more enduring appetite suppression.

Any post-exercise appetite suppression could have implications for trained athletes. Post-exercise nutrition is often considered of crucial importance to optimize recovery and maximize adaptations to training (Burke 1997). In addition, many athletes value weight management highly (Filaire et al. 2007, Sundgot-Borgen et al. 2013), as an increase in body mass can result in an increase in the energy cost of performing. Nevertheless, few investigations have addressed the effect of exercise on any appetite-related measures in athletic populations. Both increases (O’Connor et al. 1995, 2019;Connor et al. 2006, Jurimae et al. 2003, 2005, 2006, 2009, Jürimäe et al. 2007) and decreases (Jurimae et al. 2003, Jürimäe et al. 2005) in anorexigenic gut hormones with strenuous exercise have been observed, while increases in the orexigenic hormone ghrelin have also been reported (Jurimae et al. 2007, 2009). These data suggest that changes in the concentration of appetite-associated hormones in response to high-intensity aerobic exercise may be affected by training status. However, it has yet to be investigated whether this translates to altered appetite and food intake responses.

The purpose of the current study was to address the effect of exercise duration on subjective appetite, food intake and circulating concentrations of acylated ghrelin, total PYY and total GLP-1 in trained endurance athletes, utilizing high-intensity exercise bouts, akin to the habitual training of endurance athlete, lasting 15, 30 and 45 min.

It was hypothesized that exercise would elicit a transient suppression of appetite in a dose–response fashion, with longer duration of exercise resulting in more enduring appetite suppression. It was surmised that this would be accompanied by anorexigenic changes to appetite-associated hormones. An enduring appetite suppression with greater exercise load of the 45 min condition may lead to a lower post-exercise energy intake.

Materials and methods

Participants

Twelve endurance-trained male athletes were recruited for the study (Table 1). Inclusion criteria were a minimum total training duration of 6 h per week, habitual breakfast eaters, self-reported weight stable for the past 6 months and aged between 18 and 40 years. Exclusion criteria were a score of 3.5 or greater for restricted eating on the Dutch Eating Behaviour Questionnaire (DEBQ; van Strien et al. 1986); illness such as upper respiratory tract infections; smoking and the taking of medication likely to affect appetite or induce weight loss. Ethical approval was obtained from the Ethics Subcommittee of the School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham.

Table 1

Participant characteristics.

Age (years)21 ± 2
Height (cm)179.3 ± 7.2
Weight (kg)67.3 ± 5.2
BMI (kg/m2)21.0 ± 1.6
VO2max (mL/kg/min)61.6 ± 6.0
Wmax (W)309 ± 45
DEBQ score for restraint1.9 ± 0.4

Values are mean ± s.d.

RPE, rating of perceived exertion; VO2max, maximal aerobic capacity; Wmax, maximal work load.

Study design

Using a within-subject, counterbalanced, crossover study design, participants were randomly assigned to each trial condition: resting (REST), 15 min of cycling exercise (15-min), 30 min of cycling exercise (30-min) and 45 min of cycling exercise (45-min). Exercise was completed at an intensity of ~80% VO2max, with measures of subjective appetite and circulating hormone concentrations recorded throughout each trial.

Pre-testing

A single session of pre-testing preceded study trials in order to calculate the specific intensity of exercise for each participant. Participants reported to the Exercise Metabolism Laboratory, in the School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham after a minimum 2 h fast and having refrained from strenuous exercise during the previous 48 h. The participant information pack was administered and explained, and the participant was given the opportunity to ask any questions regarding the study. Informed written consent was obtained before the completion of a health questionnaire and the DEBQ, which was used to assess the participants’ habitual degree of eating restraint. Height and weight were recorded. An incremental exhaustive exercise test was completed to obtain VO2max. The exercise test was carried out on an electromagnetically braked cycle ergometer (Lode Excalibur Sport, Groningen, Netherlands). The test, preceded by a 10 min warm-up at a self-selected power output, consisted of 3 min stages, starting at a power output of 95 W and increasing in increments of 35 W. Breath-by-breath measures of exhaled gas, averaged every eight breaths, were recorded using Oxycon Pro (Jaeger, Wuerzburg, Germany) apparatus. Participants were adjudged to have reached the end of the test when they voluntarily stopped pedaling, if their cadence dropped to <60 rpm or if VO2 or heart rate ceased to increase with increasing workload. VO2max was calculated as the highest mean value obtained for any 1 min period. Submaximal VO2 values were obtained for each stage by disregarding data from the first 2 min of the stage. From the VO2max value obtained, linear regression was used to calculate the work output (in Watts), which would equate to an exercise intensity of 80% VO2max. This value was used for each of the three exercise trials.

Procedure and protocol

A minimum period of 3 days separated the pre-testing session and the first of four study trials. Participants were asked to refrain from moderate- or high-intensity exercise during the 24 h prior to each trial. A food diary was completed for the 24 h prior to the first trial, with participants asked to replicate food intake as closely as possible for the 24 h prior to subsequent trials. There was a minimum wash-out period of 3 days between trials, but typically trials were separated by 7 days.

Participants arrived at the laboratory at approximately 08:00, after a minimum 10 h overnight fast. On arrival, and after voiding, participants were weighed (body mass was recorded at each visit to ensure participants were weight stable throughout). A resting blood sample was obtained following the insertion of a venous cannula into the antecubital vein, prior to the measure of baseline subjective appetite.

The exercise bout then commenced. Exercise consisted of cycling on an electromagnetically braked cycle ergometer (Lode Excalibur Sport, Groningen, Netherlands) at a target intensity of 80% VO2max, for a duration of 15, 30 or 45 min. During each exercise bout, exhaled gas samples were obtained intermittently to monitor VO2 and to retrospectively calculate energy expenditure. Initial monitoring during minutes 3 and 4 allowed the ergometer resistance to be adjusted to achieve the target VO2. A blood sample was obtained at the half way point of the exercise trial. At 5 min intervals throughout the exercise bout, measures of heart rate and perceived exertion were obtained. The mean of these values were calculated for the entire bout.

Exercise ceased upon reaching the exercise duration target. A blood sample was obtained and measures of subjective appetite were completed immediately post exercise. The 60 min rest period then commenced, during which the participant sat reading or watching television. Subjective appetite measures and blood samples were collected at 20, 40 and 60 min post exercise. In REST, the participant remained sedentary throughout, resting for an additional 30 min to equate to the median duration of time spent exercising in the three exercise trials.

At 60 min post exercise, the participant consumed an ad libitum breakfast meal. This consisted of a buffet, offering the following food: cornflakes, semi-skimmed milk, sugar, bread, margarine, strawberry jam, orange juice and apple juice (nutritional information shown in Supplementary Table 1, see section on supplementary data given at the end of this article). All food was pre-weighed and presented in excess. After volitional satiation was reached, the remaining food was weighed and subtracted from the known quantity provided, allowing for the determination of consumed food. From this, energy intake was calculated. As the macronutrient content of each food item was known, absolute (g) and relative (percentage of total energy) macronutrient intake was also calculated.

Measures

Post-exercise energy intake was assessed using the ad libitum breakfast test meal, as described previously. A carbohydrate-rich breakfast meal was selected and participants were screened prior to enrolment in the study to ensure that they habitually consumed breakfasts of a similar composition. Participants were allocated a maximum of 15 min in which to complete the meal. Subjective appetite was assessed using the 4 questions, 150 mm, Visual Analogue Scale (VAS) test for subjective appetite, as adapted from Hill and Blundell (Hill & Blundell 1982). Measures of ‘hunger,’ ‘fullness,’ ‘desire to eat’ and ‘expected food intake’ were obtained. A composite appetite score was calculated to simplify data analysis and presentation (Holliday & Blannin 2017). (Composite appetite score = hunger score + desire score + expected intake score + (150-fullness score). The fullness score was reversed due to its opposing direction to the other three questions.)

Blood sampling and analysis

All blood samples were immediately transferred to disodium EDTA-treated tubes for analysis of appetite-associated hormones. For the measure of PYY, GLP-1 and acylated ghrelin concentrations, test tubes were pre-treated with the protease inhibitors DPP IV inhibitor (Millipore) and 4-(2-aminoethyl)benzenesulfonylfluoride hydrochloride (AEBSF, Alexis Biochemicals, Lausen, Switzerland). Blood was centrifuged at 906 g and at a temperature of 4°C for 15 min to isolate plasma. Plasma was separated and transferred to micro tubes for later analysis. Two micro tubes were pre-treated with hydrochloric acid (1 M, 100 µL per milliliter of plasma) to further protect acylated ghrelin from degradation. Plasma was stored at −70°C until hormone assays were conducted. Acylated ghrelin, total PYY and total GLP-1 were measured in duplicate using ELISA (Human Ghrelin(active) ELISA kit, Millipore; Human PYY(total) ELISA kit, Millipore; Multi Species GLP-1(total) ELISA kit, Millipore). The sensitivity of these ELISA kits were 8, 1.4 and 1.5 pg/mL, respectively, and the coefficient of variation values were 2.36, 5.26 and 3.28%, respectively.

Statistical analysis

Data are presented as means ± standard deviation (s.d.) in tables and text and as mean ± standard error of the mean (s.e.m.) in figures. For the determination of differences in energy intake from the test meal between each exercise condition, a one-way analysis of variance (ANOVA) with repeated measures was conducted. To compare the differences in both subjective appetite and plasma concentration of appetite-associated hormones with time and between-trial conditions, a 2-way factorial ANOVA with repeated measures was conducted. Post hoc pairwise comparisons were conducted using the Bonferroni correction for multiple comparisons. For all analyses of variance, there were no significant between-condition differences at baseline. The Shapiro–Wilks test for normality revealed that data for all outcome measures were normally distributed.

To further investigate the relationship between changes in appetite hormones and changes in subjective appetite with exercise, correlation analysis was conducted for within-subject comparisons. For data of REST, subjective appetite scores and hormone concentrations immediately prior to the ad libitum test meal were correlated with energy intake using Pearson product–moment correlation. Hormone concentration was correlated with appetite scores immediately prior to the test meal, as well as at t = 0. Data of all three exercise trials were collated and Pearson product–moment correlation coefficients with repeated observations were calculated, as described by Bland and Altman (Bland & Altman 1995). With this collated data, subjective appetite scores and hormone concentrations immediately prior to the ad libitum test meal were correlated with energy intake. Hormone concentrations were correlated with subjective appetite scores immediately prior to the test meal. To assess the relationship between changes in appetite-associated hormones and subjective appetite in the immediate post-exercise period, absolute values at t = 0 and change-from-baseline values at t = 0 were correlated for hormone concentration and subjective appetite scores.

A statistical significance level of P < 0.05 was used throughout. When significant differences were observed, effect sizes were calculated. For all analyses of variance (ANOVA), effect size was calculated as partial eta squared (η2p). For pairwise comparisons of note, effect size was calculated as Cohen’s d (d) and 95% confidence intervals (CI) are expressed. All statistical analyses were carried out using the SPSS software programme (SPSS).

An a priori power calculation was conducted using data from an unpublished study conducted within our laboratory (effect size η2p = 0.291 from a repeated-measures factorial ANOVA model. A Holliday and AK Blannin). Attributing subjective appetite as the primary outcome measure, and using an alpha level of 0.05 and a statistical power of 0.8, the calculation yielded a required sample size of 12 participants. This sample is powered to detect a medium effect (f = 0.62 in the power calculation) which, based on the aforementioned unpublished data, represents minimum difference of 12% in subjective appetite.

Compliance with ethical standards

Ethical approval

Ethical approval was obtained from the Ethics Subcommittee of the School of Sport, Exercise and Rehabilitation Sciences at the University of Birmingham. Ethical Review Number – ERN_09-996. All research was performed in accordance with the 1964 Declaration of Helsinki.

Ethics, consent and permission

Informed written consent was obtained from each participant after both written and verbal information about the study was provided. This consent included permission to publish research data.

Consent to publish

Informed written consent was obtained from each participant after both written and verbal information about the study was provided. This consent included permission to publish research data. No personal information of any participant is included in the manuscript.

Availability of data

The raw data is available from the corresponding author upon request.

Results

Exercise trials

The characteristics of the four trial conditions are shown in Table 2. Absolute and relative intensity (VO2 and %VO2max) did not differ between exercise trials. There was, however, a trend for a main effect of trial for mean power output (P = 0.052). Rating of perceived exertion was significantly lower for 15-min than both 30-min and 45-min, with no difference between 30-min and 45-min. The energy expenditure of the exercise bouts differed significantly between the three exercise conditions (P < 0.001), resulting in significant differences in total energy expenditure of the entire trial period between the four conditions (P < 0.001).

Table 2

Characteristics of exercise.

REST15-MIN30-MIN45-MIN
VO2 (mL/min)341 ± 33*3150 ± 3683180 ± 4053138 ± 416
% VO2max6 ± 4*76 ± 877 ± 876 ± 8
Power output (W)218 ± 30207 ± 30207 ± 33
% Wmax70 ± 466 ± 666 ± 4
Heart rate (beats/min)153 ± 13156 ± 15157 ± 14
% HRmax84 ± 584 ± 586 ± 3
RPE13 ± 1#14 ± 115 ± 2
Energy expenditure of bout (kJ)156 ± 95*989 ± 111*1987 ± 252*2929 ± 381*
EE of trial (bout + rec. period, kJ)623 ± 52*1420 ± 110*2516 ± 157*3414 ± 228*

Values are mean ± s.d.

Significantly different to all other conditions, P < 0.001; significantly different to 45-min, P < 0.05; #significantly different to 30-min and 45-min, P < 0.05.

RPE, rating of perceived exertion; VO2max, maximal aerobic capacity; Wmax, maximal work load.

Subjective appetite

VAS

Appetite profiles obtained using the VAS technique are shown in Fig. 1 for each condition. There was no condition × time interaction (P = 0.083, η2p = 0.163), nor condition main effect (P = 0.244, η2p = 0.119). There was a significant main effect for time (P < 0.001, η2p = 0.779), which showed that appetite rose from the cessation of exercise (t = 0) until the test meal (t = 60), before falling after feeding.

Figure 1
Figure 1

Mean appetite scores, as measured using VAS. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m.

Citation: Journal of Endocrinology 235, 3; 10.1530/JOE-16-0570

Food intake at the ad libitum test meal

The mean energy intake values for each of the four trial conditions are shown in Fig. 2A. There was no condition effect for energy intake (P = 0.223, η2p = 0.130), suggesting that intakes were similar (REST = 3268 ± 1397 kJ, 15-min = 3474 ± 1233 kJ, 30-min = 3636 ± 1254 kJ, 45-min = 3769 ± 1591 kJ). When accounting for the energy expenditure of exercise and assessing relative energy intake (REI, intake–expenditure), there was a significant main effect for condition (P = 0.003, η2p = 0.573, Fig. 2B). REI was significantly greater in REST (2641 ± 1616 kJ) vs 30-min (1039 ± 1520 kJ, P < 0.001, d = 1.03, 95% CI = 908–2297 kJ) and 45-min (260 ± 1731 kJ, P = 0.001, d = 1.42, 95% CI = 1113–3648 kJ), while REI in 45-min was also significantly lower than that in 15-min (2699 ± 1239 kJ, P = 0.039, d = 1.62, 95% CI = −4761 to −117 kJ). There were no significant differences in macronutrient content of the food consumed between the four conditions (Table 3).

Figure 2
Figure 2

Energy intake (A) and relative energy intake (B) at the ad libitum breakfast test meal for REST, 15-MIN, 30-MIN and 45-min. Values are mean ± s.e.m. *Significantly lower than REST. Significantly lower than 15-min.

Citation: Journal of Endocrinology 235, 3; 10.1530/JOE-16-0570

Table 3

Summary of food intake at the ad libitum test meal for each of the four conditions.

REST15-min30-min45-min
Weight consumed (g)735 ± 331793 ± 281836 ± 262822 ± 264
Carbohydrate (g)148 ± 64157 ± 55167 ± 55165 ± 57
% Energy CHO76.3 ± 6.777.2 ± 5.777.5 ± 5.775.4 ± 9.3
Fat (g)11.1 ± 6.611.3 ± 6.411.5 ± 6.417.2 ± 21.2
% Energy fat13.4 ± 5.812.9 ± 4.812.5 ± 4.715.3 ± 10.6
Protein (g)20.6 ± 9.420.9 ± 8.222.3 ± 9.220.3 ± 8.3
% Energy protein10.3 ± 2.29.9 ± 2.010.0 ± 2.19.3 ± 2.3

Values are mean ± s.d.

Plasma appetite-associated hormone concentrations

Acylated ghrelin

There was a significant condition × time interaction for acylated ghrelin concentration (P = 0.011, η2p = 0.285, Fig. 3). Post hoc analysis of between-condition comparisons showed that, immediately post exercise (t = 0), acylated ghrelin was significantly lower in 45-min (198 ± 29 pg/mL) vs REST (369 ± 48 pg/mL, P = 0.009, d = 1.307, 95% CI = −286 to −40 pg/mL). Concentrations were also lower than REST in 15-min (273 ± 42 pg/mL) and 30-min (246 ± 33 pg/mL) immediately post exercise, with these differences approaching statistical significance (P = 0.077, d = 0.910, 95% CI = −193 to 8 pg/mL and P = 0.055, d = 0.971, 95% CI = −239 to 2 pg/mL, respectively). The difference in acylated ghrelin concentration between 45-min and 30-min also approached significance (P = 0.057, d = 0.963, 95% CI = −89 to 1 pg/mL). The difference in plasma ghrelin concentration between 45-min and REST remained significant at t = 20 (239 ± 35 pg/mL vs 365 ± 47 pg/mL, P = 0.023, d = 1.096, 95% CI = −203 to −14 pg/mL). There were no significant differences between conditions at t = 40 onwards.

Figure 3
Figure 3

Mean plasma concentration of acylated ghrelin. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m. *Significant within-condition, lower than baseline. Significant between-condition effect, 45-min lower than REST.

Citation: Journal of Endocrinology 235, 3; 10.1530/JOE-16-0570

Within-condition comparisons showed that acylated ghrelin concentration did not change, relative to baseline, in REST or 15-min. In the 30-min condition acylated ghrelin decreased during exercise, with a trend for lower concentration immediately post exercise vs baseline (246 ± 33 pg/mL vs 396 ± 48 pg/mL, P = 0.098, d = 1.093, 95% CI = −305 to 16 pg/mL). This difference approached statistical significance at t = 20 (249 ± 7 pg/mL vs 396 ± 8 pg/mL, P = 0.05, d = 1.216, 95% CI = −283 to 0 pg/mL). Mean acylated ghrelin concentration decreased to the greatest extent in the 45-min trial, with concentrations significantly lower immediately post exercise (198 ± 29 pg/mL) and at t = 20 (239 ± 35 pg/mL), vs baseline (366 ± 47 pg/mL, P = 0.038, d = 1.269, 95% CI = −312 to −7 pg/mL and P = 0.025, d = 1.346, 95% CI = −207 to −10 pg/mL respectively).

PYY

There was no significant condition × time interaction for PYY concentration (P = 0.472, η2p = 0.080), nor was there a significant main effect for condition (P = 0.691, η2p = 0.252) (Fig. 4). A significant time main effect (P < 0.001, η2p = 0.522) demonstrated a decrease in PYY concentration during the post-exercise period, compared with baseline, until the test meal (t = 60).

Figure 4
Figure 4

Mean plasma concentration of PYY. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m.

Citation: Journal of Endocrinology 235, 3; 10.1530/JOE-16-0570

GLP-1

There was a significant time × condition interaction for GLP-1 plasma concentration (P < 0.001 η2p = 0.433; Fig. 5). Post hoc analysis of between-condition comparisons showed that, at t = 0, there was a trend for a greater GLP-1 concentration in the 30-min trial (33.4 ± 11.1 pg/mL) compared with REST (26.5 ± 10.0 pg/mL, P = 0.093, d = 0.878, 95% CI = −0.9 to 14.7 pg/mL) and a greater concentration in 45-min (38.5 ± 19.2 pg/mL) vs 15-min (28.4 ± 13.8 pg/mL, P = 0.076, d = 0.912, 95% CI = −0.7 to 18.2 pg/mL). At t = 20, the trend for a greater concentration in 30-min vs REST was maintained, while plasma GLP-1 concentration was significantly greater in 45-min (40.6 ± 19.9) vs 15-min (27.1 ± 13.8 pg/mL, P = 0.024, d = 1.121, 95% CI = 1.4–22.7 pg/mL) and greater in 45-min (40.6 ± 19.9) vs REST, with the difference approaching significance (vs 26.7 ± 10.1 pg/mL, P = 0.080, d = 0.905, 95% CI = −1.1 to 25.9 pg/mL). This elevated concentration in 45-min was significantly greater than both REST and 15-min at t = 40 (P = 0.035 and P = 0.047 respectively) and t = 60 (P = 0.012 and P = 0.040, respectively), remaining higher than REST immediately after the test meal (P = 0.035). Plasma GLP-1 concentration was significantly higher in 30-min, compared with REST at t = 60 (P = 0.032).

Figure 5
Figure 5

Mean plasma concentration of GLP-1. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m. *Significant within-condition effect, vs baseline. Significant between-condition effect.

Citation: Journal of Endocrinology 235, 3; 10.1530/JOE-16-0570

Post hoc analysis of within-condition differences showed that, in 30-min, plasma GLP-1 increased above baseline concentration at t = 0 (33.4 ± 11.1 vs 25.9 ± 9.0 pg/mL, P = 0.018, d = 1.418, 95% CI = 1.1–14.0 pg/mL), remaining elevated until t = 40. In 45-min, GLP-1 concentration increased significantly above baseline at t = 0 (38.5 ± 19.2 vs 25.8 ± 12.4 pg/mL, P = 0.043, d = 1.243, 95% CI = 0.2–22.4 pg/mL) and stayed elevated for the remainder of the trial period.

Relationship between hormones, subjective appetite and food intake

In REST, there were no significant correlations, or trends for correlations, between hormone concentration and subjective appetite scores, either at t = 0 or immediately prior to the test meal (all r < |0.5|, P > 0.1). In addition neither VAS score nor concentrations of acylated ghrelin, PYY or GLP-1 were significantly correlated with energy intake (r < |0.5|, P > 0.1).

After exercise, there was a trend for a strong positive correlation between acylated ghrelin concentration and subjective appetite score at t = 0 (r = 0.665, P = 0.087). However, there were no other significant relationships, or trends for relationships, between hormone concentration and subjective appetite scores, either at t = 0, as change-from-baseline at t = 0, or immediately prior to the test meal (all r < |0.6|, P > 0.1). PYY concentration immediately prior to the test meal showed a moderate, negative correlation with energy intake (r = −0.484, P = 0.019) and with REI (r = −0.417, P = 0.048). GLP concentration immediately prior to the test meal showed a moderate, negative correlation with REI (r = −0.599, P = 0.002), but was not significantly associated with absolute energy intake. Acylated ghrelin concentration was not associated with either absolute or relative energy intake.

Discussion

The aim of the current study was to assess the effect of the duration of high-intensity aerobic exercise on subjective appetite, food intake and appetite-regulating hormones in highly trained male endurance athletes. Subjective appetite was not significantly suppressed post exercise in any of the three exercise conditions, with only modest, non-significant reductions of ~10–15% in appetite scores from baseline, and scores in none of the three exercise conditions differed significantly from the resting condition scores at any point in the trial period. This was despite significant responses of both acylated ghrelin and GLP-1 toward a more anorexigenic state.

Exercise at an intensity ≥60% VO2max often elicits a transient suppression of appetite in untrained, lean individuals (Martins et al. 2007, King et al. 2010, Laan et al. 2010, Deighton et al. 2013a,b, Kawano et al. 2013). To the knowledge of the authors, the exercise of the present study is the highest intensity bout of continuous exercise utilized in research of this nature. Yet, no suppression of appetite was observed. It is possible that this lack of a commonly observed appetite suppression is due to a difference in responses to exercise between athletic and non-athletic populations. Though equivocal, studies conducted in recreationally active young males with mean VO2max values of ~55–57 mL/kg/min, utilizing prolonged bouts of continuous exercise at ~65–70% VO2max have elicited modest, non-significant appetite suppression similar to those of the present study (King et al. 2011a,b, Wasse et al. 2013, Deighton et al. 2014). These data, allied with the findings of the current study, suggest that appetite response to high-intensity aerobic exercise may be somewhat different for individuals of differing training/activity status or fitness. However, in contrast to the findings of the current study, Howe and coworkers did observe a suppression of appetite after both moderate- (60% VO2max) and high-intensity (80% VO2max) in trained females(Howe et al. 2016). The differing responses could be due to the different sex of participants (although there is currently minimal evidence to suggest sex differences in acute appetite responses to exercise in non-athletes (Thackray et al. 2016)). A limitation of the present study is the lack of a female study cohort for the direct investigation of sex differences. Nonetheless, the present findings suggest that regular endurance exercise training may blunt the appetite suppression response typically observed in those less familiar with such exercise.

Aligned with the absence of a post-exercise appetite suppression, there was no significant difference in food intake at the ad libitum test meal, administered 60 min after the cessation of exercise. No difference in food intake post-exercise is a commonly observed finding, especially when the test meal is consumed 60 min post exercise (Thompson et al. 1988, King et al. 1997, 2010, 2011b, Schubert et al. 2013). The absence of a reduction in food intake after exercise would indicate, in contrast to the hypothesis, that the prolonged bout of continuous, high-intensity exercise of the present study was not sufficient to induce an appetite suppression that was sufficiently enduring to influence food intake 60 min post exercise. It is acknowledged that a limitation of the present study is the acute measure of food intake. There is evidence that compensatory increases in food intake can occur in the hours and days after exercise, and that this response may differ depending on physical activity status (Rocha et al. 2013). Therefore, monitoring food intake over the remainder of the trial day and perhaps over the following 48 h would have proved insightful.

REI did differ between trial conditions. This has often been observed in the absence of a lower post-exercise absolute energy intake (Imbeault et al. 1997, Lluch et al. 2000, King et al. 2010, Unick et al. 2010), or even after absolute energy intake is greater post-exercise (Pomerleau et al. 2004, Martins et al. 2007). As such, it would appear there was a lack of an immediate compensatory increase in drive to eat after prolonged strenuous exercise and extensive energy expenditure, and that such exercise can elicit short-term energy deficit, compared with rest. However, the monitoring of food intake, physical activity and metabolic rate over the course of the whole day and beyond would be required to determine likely effects of the exercise bout, and subsequent appetite response, on energy balance.

The post-exercise period is important for athletes with regard to nutrition for recovery and adaptation to training. Post-exercise carbohydrate intake is valued by many endurance athletes, with exercise-induced GLUT-4 translocation leading to an increased potential for glucose uptake and glycogen resynthesis after exercise (Goodyear et al. 1998, Ivy 1998, Jentjens & Jeukendrup 2003). In addition, amino acid delivery and a positive energy balance stimulate net muscle protein synthesis after resistance (Tipton et al. 1999) and endurance-type exercise (Howarth et al. 2009), meaning that the ingestion of protein in close proximity to exercise is often desired for optimal rates of muscle protein synthesis and subsequent adaptation (Phillips 2006, Phillips & Van Loon 2011). Therefore, a suppression of appetite post-exercise may be detrimental for recovery and adaptation, should it impact upon nutrition. The findings of the present study would suggest that this was not the case, even after a strenuous bout of 45 min of cycling at 76% VO2max.

A lack of significant exercise-induced suppression of appetite in the present study was allied with no significant change in plasma concentration of the satiety peptide PYY with exercise. While PYY concentration has commonly been observed to be responsive to high-intensity aerobic exercise (Martins et al. 2007, Broom et al. 2009, Russel et al. 2009, Ueda et al. 2009a,b, Larson-Meyer et al. 2012), this was not the case in the present study. It is possible that this is due to the study population; well-trained athletes, familiar with exercising at such a high-intensity may be resistant to exercise-induced alterations in PYY secretion. Chronic exercise training has been postulated to sensitize satiety peptides to food intake, with greater late post-prandial period concentrations of PYY and GLP-1 with food intake after exercise training (Martins et al. 2010). In addition, exercise training (Jones et al. 2009) and exercise-induced weight loss (Roth et al. 2005) have been shown to increase fasting PYY concentrations. These may be mechanisms by which regular physical activity assists with tighter regulation of energy balance, through limiting overeating. Similarly, the blunting of an exercise-induced increase in PYY with regular exercise may regulate energy balance through the avoidance of appetite suppression and increased energy deficit post exercise. A limitation of the present study is that concentrations of total PYY were measured, rather than the active form PYY(3–36). However, the abundance of PYY(3–36) is greater than that of PYY(1–36), meaning that most of the total circulating PYY in plasma is in the form of PYY(3–36). Additionally, total PYY and PYY(3–36) have been shown to respond similarly to food intake (Pfluger et al. 2006) and have demonstrated similar responses to exercise of a similar nature (Deighton et al. 2013a,b). Hence, responses of total PYY to exercise are likely to reflect those of PYY(3–36).

Despite no significant suppression of appetite, there was a clear response of GLP-1 during and after exercise. Concentrations rose with exercise in the 30-min (29%) and 45-min (49%) conditions, with levels remaining elevated during the 60 min recovery period. This finding is in agreement with previous studies in obese (Ueda et al. 2009b) and healthy-weight (Martins et al. 2007, Ueda et al. 2009a) individuals, after exercise of an intensity lower than that of the current study, lasting 30–60 min. No such response was observed in the 15-min condition, however, with the GLP-1 profile closely resembling that of REST. This is in contrast to previous studies that have observed a suppression of GLP-1 with very low-volume, high-intensity interval exercise in recreationally active (Bailey et al. 2015) and overweight (Martins et al. 2015) individuals. These data would suggest that just 15 min of high-intensity cycling at 76% VO2max was an insufficient stimulus to cause any exercise-induced increase in plasma GLP-1 in trained endurance athletes and that the contrast with observations from maximal, or near maximal, high-intensity interval exercise studies could be due to the differing intensity of exercise or differing study populations. These data would also suggest that GLP-1 concentration during high-intensity aerobic exercise exhibits some duration or energy expenditure dependency, possibly with a threshold duration for its secretion.

Acylated ghrelin also proved responsive to exercise. The plasma concentration declined with exercise in all three exercise conditions, with the greatest decrease seen after 45 min of cycling. This suppression of acylated ghrelin was transient, with concentrations not significantly different to baseline by 40 min post-exercise, even in 45-min; neither was there a significant difference between any exercise condition and REST at this time point. This was despite acylated ghrelin concentration being 28, 20 and 23% lower than REST in the 15-MIN, 30-MIN and 45-min conditions, respectively. As with the finding of Broom and coworkers, this present study would indicate that acylated ghrelin responses to exercise may be duration dependent (Broom et al. 2017). However, while the findings of Broom and coworkers suggest duration-dependent differences in the longevity of the suppression, the present findings suggest difference in the magnitude of the suppression (Broom et al. 2017). Data of the present study would suggest that, with high-intensity aerobic exercise, plasma acylated ghrelin concentration begins to decline in the very early stages of exercise and continues to decline as the bout continues. While this would suggest a physiological mechanism by which the duration of exercise is an important regulatory factor in post-exercise appetite suppression, the absence of a significant suppression of appetite (either compared with baseline or with REST) dispels this theory somewhat and also questions the role of acylated ghrelin as a regulator of appetite in the post-exercise state.

It would appear there are some inconsistencies in the hormonal response and appetite in the present study. Firstly, changes in acylated ghrelin and GLP-1 in favor of an anorexigenic state were not observed with PYY. It has generally been observed that alterations in appetite-associated hormones occur concurrently, especially with regards to satiety peptides (Broom et al. 2009, King et al. 2011a). Differential responses in PYY and GLP-1 have, however, been observed following 30 min of cycling at 50% VO2max and 75% VO2max (Ueda et al. 2009a). It was found that PYY secretion appeared to be exercise intensity-dependent, with concentration elevated to a greater extent after exercise at 70% VO2max, compared with after exercise at 50% VO2max. In contrast, GLP-1 concentration increased similarly in both exercise trials. The authors suggest that their data would advocate specific exercise responses in plasma kinetics of PYY and GLP-1. The data of the present study would support the notion of a specific response, but contrasts the findings somewhat, with GLP-1, but not PYY, suggested to change in a duration- or energy expenditure-dependant manner. Further, if an increase in plasma PYY is exercise intensity dependent, then it may be the case that athletes possess a blunted response, or have elevated their threshold intensity for PYY release.

Secondly, the anorexigenic stimulus of an increase in GLP-1 concentration and a decrease in acylated ghrelin was not reflected by a suppression of subjective appetite or reduced absolute food intake. Both total (Wren et al. 2001) and acylated ghrelin (Druce et al. 2005) have been shown to be potent appetite regulators when administered pharmaceutically in the resting state. However, some studies infused non-physiological concentrations (Wren et al. 2001), while lower concentration infusion has yielded conflicting effects on food intake on overweight and lean individuals (Druce et al. 2005). Studies investigating the effect of GLP-1 administration, at a physiological concentration, on food intake are equivocal (Verdich et al. 2001). In the present study, exercise-induced alterations that would be expected to favor an anorexigenic state did not lead to a suppression of subjective appetite in the post-exercise period.

Assessment of the relationships for within-subject changes in appetite, hormone concentration and energy showed little consistent association between concentration of hormones and subjective appetite, both at rest and post exercise. There was a trend for a strong correlation between acylated ghrelin and VAS score immediately post exercise, which does suggest that immediate post-exercise appetite responses may be mediated by changes in acylated ghrelin. However, this association was not statistically significant and was not evident at other post-exercise measures. Neither PYY nor GLP-1 was associated with subjective appetite at any time. However, PYY concentration immediately prior to the test meal was inversely related to energy intake, and both PYY and GLP-1 concentration were inversely related to REI. Such inconsistencies are not uncommon (Broom et al. 2007, 2009), and there is evidence that in the post-exercise period, there is blunting to hormonal regulators of appetite. In a study by Heden and coworkers, acylated ghrelin and subjective appetite responded differently with exercise in healthy-weight and obese individuals, and Deighton and coworkers (Deighton et al. 2013a,b, Heden et al. 2013) observed contrasting positive and negative correlations between acylated ghrelin and subjective appetite in the period after endurance and sprint-interval exercise, respectively, in healthy-weight males. Further, previous studies have also shown weak (Broom et al. 2009, Hagobian et al. 2013, Wasse et al. 2013, Beaulieu et al. 2014) or inconsistent (Ueda et al. 2009a, Deighton et al. 2014, Bailey et al. 2015) relationships between hormone concentration and both subjective appetite and food intake; yet, the relevance of such findings are largely overlooked. These data question the commonly accepted importance of exercise-induced changes in appetite-associated hormones for appetite regulation and acute absolute energy intake. Although the data of the present study suggest that the satiety peptides PYY and GLP-1 may influence REI. As such, it is possible that the role of these hormones is to defend against overeating and a compensation for energy expenditure, as opposed to suppressing food intake per se. Further investigation is required to clarify the regulatory role of these hormones, at physiological concentrations, in appetite and food intake responses, especially in the post-exercise period.

In conclusion, neither 15, 30 nor 45 min of cycling at 76% VO2max significantly suppressed subjective appetite in male highly trained endurance athletes. Acute absolute food intake was unaffected by exercise, although with no compensatory increase in energy intake, exercise of 30 min and 45 min in duration induced an acute energy deficit, compared with remaining rested. The lack of observed appetite suppression was despite a transient suppression of acylated ghrelin and a sustained increase in GLP-1, with some evidence that the concentration of these hormones change in an exercise-duration-dependent manner. These findings suggest that those accustomed to high-intensity aerobic exercise may exhibit a blunted response to exercise-induced appetite suppression or a dissociation of appetite perception and hormonal signals post exercise. The role of appetite-associated hormones in regulating post-exercise appetite, food intake and acute energy balance warrants further investigation.

Supplementary data

This is linked to the online version of the paper at http://dx.doi.org/10.1530/JOE-17-0570.

Declaration of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

Funding

Adrian Holliday was funded by a University of Birmingham PhD Studentship.

Author contribution statement

A H and A B conceived the study question and study design; A H completed the data collection and data analysis; A H wrote the manuscript; A B assisted with the drafting of the manuscript.

Acknowledgements

The authors would like to acknowledge and thank Dr Oliver Wilson for assisting with the drafting of the manuscript.

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    Mean appetite scores, as measured using VAS. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m.

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    Energy intake (A) and relative energy intake (B) at the ad libitum breakfast test meal for REST, 15-MIN, 30-MIN and 45-min. Values are mean ± s.e.m. *Significantly lower than REST. Significantly lower than 15-min.

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    Mean plasma concentration of acylated ghrelin. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m. *Significant within-condition, lower than baseline. Significant between-condition effect, 45-min lower than REST.

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    Mean plasma concentration of PYY. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m.

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    Mean plasma concentration of GLP-1. ●, solid line = REST; ○, large dash = 15-min; ■, medium dash = 30-min; □, small dash = 45-min. Hollow rectangle = exercise; filled, black rectangle = ad libitum breakfast meal. Values are mean ± s.e.m. *Significant within-condition effect, vs baseline. Significant between-condition effect.

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