Exercise prior to a freely requested meal modifies pre and postprandial glucose profile, substrate oxidation and sympathovagal balance
© Charlot et al; licensee BioMed Central Ltd. 2011
Received: 19 July 2011
Accepted: 24 September 2011
Published: 24 September 2011
The effects of exercise on glucose and metabolic events preceding and following a freely initiated meal have never been assessed. Moreover, the relationship between these events and sympathovagal balance is not known. The objective of this study was to determine whether exercise prior to a freely requested meal modifies the pre- and postprandial glucose profile, substrate oxidation and sympathovagal balance.
Nine young active male subjects consumed a standard breakfast (2298 ± 357 kJ). After 120 min, they either performed 75 min of exercise on a cycle ergometer (EX - 70% VO2max) or rested (RT). Lunch was freely requested but eaten ad libitum only during the 1st session, and then energy intake was fixed across conditions. Glucose and sympathovagal balance were assessed continuously using a subcutaneous glucose monitoring system and analysis of heart rate variability, respectively. Every 5 min, a mean value was calculated for both glucose and sympathovagal balance. Substrate oxidation was determined by calculating the gas exchange ratio when lunch was requested and 180 min after the onset of eating.
Preprandial glucose profiles were found in 72% of the sessions and with a similar frequency under both conditions. Meals were requested after a similar delay (40 ± 12 and 54 ± 10 min in EX and RT respectively; ns). At meal request, sympathovagal balance was not different between conditions but CHO oxidation was lower and fat oxidation higher in EX than in RT (-46% and +63%, respectively; both p < 0.05). Glucose responses to the meal were higher in incremental (+ 48%) but not in absolute value in EX than in RT, with a higher fat oxidation (+ 46%, p < 0.05), and a greater vagal withdrawal (+ 15%, p < 0.05).
These results show that exercise does not impair preprandial glucose declines at the following meal freely requested, but leads to an increased postprandial glucose response and an elevated fat oxidation, an effect that vagal withdrawal may contribute to explain.
KeywordsExercise preprandial glucose decline interstitial glucose postprandial glucose fat oxidation heart rate variability sympathovagal balance freely requested meal
List of abbreviations used
Area under the curve
predicted theoretical maximal heart rate
heart rate variability
preprandial glucose decline
visual analogue scale
maximal oxygen consumption
respiratory exchange ratio.
Exercise is now considered to contribute to both the reduction in the prevalence of type 2 diabetes and the improvement of glucose tolerance . The effect on postprandial glucose was observed even after a single bout of exercise [2, 3]; however, the delay between the exercise session and the test meal is an important parameter. In the immediate post-exercise period and up to 90 min later, postprandial glucose concentrations have been reported to be increased [4–11] or unchanged [5, 12–17]. This is thought to be mainly the consequence of reduced insulin concentrations [5, 7, 13, 14]. Another hypothesis is that exercise may transiently blunt glucose tolerance by changing the sympathovagal balance. Prior exercise has been shown to stimulate postprandial sympathetic activity , leading to a reduction in pancreatic insulin release . In addition, partially impairing vagal activity before a meal resulted in reduced glucose tolerance [11, 20], indicating that an exercise-induced withdrawal of vagal activity may also contribute to this effect either directly or indirectly by alleviating the inhibition of sympathetic stimulation . The continuous evaluation of sympathovagal balance is now possible with the analysis of heart rate variability (HRV), a non-invasive method that investigates the autonomic modulation via changes in RR intervals  and may be employed to gain insight into the mechanism underlying exercise-mediated glucose tolerance.
Exercise is usually not followed by an increase in hunger or energy intake [23–31]. In some studies, hunger scores were even found to be briefly reduced [23–25]. The mechanism for this absence of energy compensation is not known. Moreover, a longer delay of meal initiation after exercise has been reported . Thus, it is important to study the sequence preceding meals spontaneously initiated. In animals  and humans [33–36], meals are requested after a decline in blood glucose, illustrating central glucopenia . It was found that this phenomenon could even discriminate between meals and snacks . To this day, a possible modification of the glucose profile by prior exercise has not been studied. To detect these preprandial glucose declines, a continuous blood withdrawal system allowing measurements every 5 min is required. However, this method is not fully compatible with exercise. Recently, using a subcutaneous glucose monitoring system (CGMS®), these preprandial glucose declines were measured under everyday life conditions . This system represents a promising alternative and is already being used to monitor glucose profiles during exercise in young diabetic patients .
The current study was planned with two main objectives. The first was to determine whether prior exercise would alter the neurometabolic state in which a meal is spontaneously initiated. The second was to verify whether the glucose response to this meal would be altered by prior exercise and whether it was accompanied by a change in fat oxidation and sympathovagal balance.
Subjects' characteristics (n = 9)
21.9 ± 1.8
Body weight (kg)
73 ± 6
1.80 ± 0.06
Body mass index (kg.m-2)
22.7 ± 1.6
Body fat (%)
13.4 ± 1.5
Restrained eating score*
3.3 ± 2
49 ± 9
At least 3 days prior to the experimental trial, individuals' maximal oxygen consumption (VO2max) was determined using a maximal workload test conducted on a bicycle ergometer (Ergoselect 100P, Ergoline, Bitz, Deutschland). Subjects wore a facemask (Hans Rudolph, 8940 Series, Kansas City, KA, USA), and gas exchange rates were measured using an open-circuit spirometry Vmax Encore (Viasys Healthcare, Palm Springs, CA, USA). The same equipment was used for all calorimetry measurements throughout the study. The VO2max was considered to be reached when two of the following criteria were met: 1) a less than 2 mL·kg-1·min-1 VO2 increase despite workload increase; and 2) a respiratory energy ratio (RER) > 1.15.
On the eve of each test day, subjects were required to eat their dinner at home at the same hour. The 2 meals consisted of traditional main dishes (couscous and paella) with similar carbohydrate (CHO), fat and protein compositions (33, 43 and 24 energy percent [En%], respectively). Beverages, dessert and bread were freely added by the subjects before the first session; however, participants were instructed to keep their dinner meals similar before the next session.
On the day of the test, the energy content of the breakfast meal was calculated based on each participant's usual intake at this meal, which ranged from 1700 to 2900 kJ. The same foods were provided for each subject (i.e., bread, butter, marmalade, fruit yogurt and sweetened milk) equal to the energy value calculated for each subject. In addition, the macronutrient composition (in %) was matched but with an energy value corresponding to their usual breakfast.
Energy and macronutrient intake at each experimental meal
2298 ± 357
5225 ± 998
92.8 ± 15.6
117.4 ± 22.1
67.4 ± 1.7
37.8 ± 3.9
12.7 ± 1.8
63.9 ± 14.1
20.9 ± 1.6
45.8 ± 3.5
16.0 ± 2.4
51.3 ± 10.2
11.7 ± 0.4
16.4 ± 0.4
% of TDEE
22 ± 4
49 ± 11
After a 5 min warm-up period at 75 W, the workload was progressively increased for a 10 min period until the subject reached 70% of his VO2max. This intensity was then maintained for 60 min. Continuous gas exchange allowed for the measurement of energy expenditure (EE) and constant adjustment of the workload so that exercise was maintained at the desired intensity.
Motivation to eat
From the beginning of breakfast to the end of the 75 min of exercise or rest, motivation to eat was assessed on 100 mm visual analogue scales (VAS) addressing the questions ''Do you feel hungry?'' (hunger scale), ''Do you want to eat something?'' (desire to eat scale) and ''How full do you feel?'' (gastric fullness scale) every 30 min for 3 hours, and then every 15 min until a meal was requested. These scales were anchored with "not at all" and "extremely" at the left and right ends, respectively. The distance between the extreme left and the subject's vertical dash represented the rating score, expressed in mm.
A continuous glucose monitoring system (CGMS®, Medtronic Minneapolis, USA) was used to determine the glucose profile. It consists of an electrochemical sensor with glucose oxidase immobilized on an electrode. Interstitial glucose is measured every 5 min. Four calibrations on venous blood taken from the fingertip during a stable state period (i.e., not in the postprandial state) were carried out every 24 h using the glucometer, Optium Xceed (Witney, Oxon, UK). Interstitial glucose has been reported to be a valid surrogate for the blood glucose level  and allows transient glucose fluctuations to be assessed. It is important to note that a lag, varying from 4 to 10 min, between plasma and interstitial glucose levels has been reported, with the former usually preceding the latter . The duration of the lag seems to depend on the glucose level and kinetics. The lag between 2 CGMS® sensors is also important. However, no fixed value has been proposed to this day. Thus, we decided to present and analyze the glucose data without an arbitrary lag.
Energy expenditure and substrate oxidation
At rest, EE was calculated using the energy equivalent of O2 derived from the Weir equation  and substrate oxidation was calculated using the Péronnet & Massicotte equations  with the assumption that protein oxidation is negligible. During exercise, the Jeukendrup & Wallis equation  for moderate to high-intensity exercise (50-75% VO2max) was used to calculate CHO oxidation and EE. This stoichiometric equation is more appropriate to exercise since it takes into account that only 20% of the glucose oxidized is derived from plasma, with 80% being provided by glycogen. Allowing a delay of 10 min to reach stability, only the last 5 min of the preprandial and the postprandial measurements were used for analyses.
Assessment of the autonomic nervous system
Autonomous modulation was evaluated by the frequency domain analysis of HRV. The RR intervals were recorded during the day using a cardiofrequencemeter (T6, Suunto, Finland), stored for analysis and then screened for artifact (less than 2%). The determination of a suitable series of 256 RR intervals for each 5 min generated indices of HRV that correspond with each value measured by the CGMS®. Power spectral analyses were performed with the HRV Analysis Software 1.1 for Windows . Total power in the frequency range (0 - 0.40 Hz) was divided into low frequency (LF: 0.04 - 0.15 Hz) and high frequency (HF: 0.15 - 0.40 Hz) bands. The LF band has been attributed to both the vagal and sympathetic modulations, the HF band to vagal modulation and the LF to HF ratio (LF/HF) to the sympathetic modulation of total activity . The use of normalized units (nu) for the HF component (HFnu = (HFms2/(LFms2 + HFms2) × 100) has been recommended . Our subjects breathed spontaneously but reproducibility has been shown to be similar between spontaneous and paced breathing techniques .
Preprandial glucose declines (PPGD) were based on the definitions of Melanson et al. [34, 35]: at least 5% magnitude and 5 min duration. Since the CGMS® only provided an average value every 5 min, and in accordance with our observations from a previous study , we decided that the criteria needed to be more conservative. Therefore, we decided that PPGD should be defined by a decline that lasted at least 10 min (from 2 consecutive time points) and that the meal had to be requested before the return of glucose concentrations to the basal level.
Areas under the curve (AUC) were calculated by the trapezoidal method over the 180 min following the start of the lunch meal for both the glucose and HRV indices. For glucose, two postprandial AUCs were calculated: an incremental area (values minus basal level, AUCinc), and an absolute level area (AUCabs). The first was used to specifically determine the glucose response to the meal and the second to evaluate whether differences in this response actually resulted in differences in glucose levels.
All variables means and AUCs were compared using paired Student's t- tests. Glucose and HRV indices profiles were analyzed using analyses of variance (ANOVA) for repeated measures with condition (RT and EX) and time as within-subject factors. According to the proposed approach of analysis of serial measures , time was divided into 4 periods of interest: 1) from breakfast to rest or exercise, 2) rest or exercise and the delay until one subject asked for his meal (the interruption of the comparison is due to the reduction in the sample size), 3) prelunch and 4) postlunch. The prelunch period consisted of the 45 min preceding meal intake (i.e., 30 min before the lunch request and 15 min during gas exchange measurement). The postprandial period was divided into 30 min periods (6 time points). When an effect was significant, appropriate comparisons using Scheffe's tests were conducted. Statistical significance was set at p < 0.05. All results are expressed as mean ± SEM, unless otherwise stated. All data were obtained for 9 subjects except postprandial HRV during which the recording failed for 1 subject.
HRV indices, energy expenditure and substrate oxidation during the rest or exercise period
HRV indices, energy expenditure and substrate oxidation during the rest or exercise period
64 ± 4
151 ± 3‡
2443 ± 184
68 ± 20‡
2952 ± 757
41 ± 18†
47 ± 6
21 ± 3†
1.7 ± 0.5
8.2 ± 1.8*
418 ± 39
3109 ± 222‡
0.807 ± 0.008
0.931 ± 0.003‡
10.7 ± 3.4
146.3 ± 11.2‡
6.3 ± 0.6
17.6 ± 1.4*
Appetite, meal request delay and preprandial glucose declines
Pre and postprandial energy expenditure and substrate oxidation
Energy expenditure and substrate oxidation at meal request and 3 h after the lunch meal
At meal request
3 h after lunch
5.96 ± 0.12
5.96 ± 0.31
6.93 ± 0.17
6.71 ± 0.23
0.870 ± 0.021
0.784 ± 0.027*
0.885 ± 0.027
0.818 ± 0.030*
0.22 ± 0.03
0.12 ± 0.04*
0.28 ± 0.05
0.18 ± 0.04*
0.06 ± 0.01
0.10 ± 0.02*
0.07 ± 0.01
0.10 ± 0.02*
Pre and postprandial heart rate variability indices
At meal request, an effect of condition was found only for HR (p < 0.005), and an interaction between time and condition for LFms2 (p < 0.05). Comparisons showed that LF was higher in RT than in EX until 15 min prior to the lunch request (p < 0.05) but this difference was not observed afterwards (data not shown). HR was higher in EX than in RT from 30 min prior to the meal request until 15 min after the meal (p < 0.05, data not shown).
In this study, sympathovagal modulation and interstitial glucose concentrations were for the first time recorded continuously and in parallel to assess the effects of exercise on the pre- and postprandial sequences of a spontaneously requested meal. Our results show, firstly, that in young male adults, exercise did not alter the preprandial sequence (delay, motivation to eat, preprandial glucose decline) but that under this condition the meal was requested in a metabolic state that was characterized by a higher proportion of energy being derived from fat. Secondly, the postprandial glucose response was increased in relative but not absolute values after exercise, and this was associated with an increase in fat oxidation and vagal withdrawal.
Exercise did not alter the motivation to eat or delay request for the meal. After a similar physical workload, exercise has been reported to reduce hunger ratings in some [23–25] but not all studies [26–31]. This effect was brief (<10 min) and no longer present at meal onset. Although these results were reported for a study with a similar number of subjects, the non-significant trend that we observed in the immediate post-exercise period for hunger and desire to eat suggests that a larger sample size may be required. While a slightly longer delay (5 min) until eating onset has been previously reported , this delay was not significantly changed in our study. Again, a higher number of subjects may be required in order to observe this effect. Therefore, specific research into this matter is needed in the future.
One of our hypotheses was that the glucose decline preceding a meal request would be altered by prior exercise. When an exercise that depleted muscle glycogen was performed on the day before testing, it has been reported that most meals were requested without a prior glucose decline . This was accompanied by a very low RER that was corrected after re-feeding. According to the criteria proposed by Melanson et al. [34, 35] that we adapted to be more conservative, a glucose decline was observed before 72% of lunch requests. In the other cases, glucose actually decreased during the preprandial interval, but the magnitude and duration of our modified criteria were not fulfilled. The mean delay between the onset of this preprandial glucose decline and the meal request was consistent with previous observations [33–35]. Exercise did not seem to impair this preprandial glucose profile since it was observed with a similar frequency in both conditions. However, our exercise was not designed to deplete muscle glycogen. Based on our glucose oxidation results (~ 146 g) and the energy partitioning proposed by Jeukendrup  (i.e., 80% of the glucose oxidized derived from glycogen) and the glucose oxidized at rest (~ 11 g), ~ 106 g of glycogen was used [(146 × 0.8) - 11]. According to the subjects' leg muscle mass, which was estimated at ~ 21 kg by the bioelectrical impedance analyzer, and a mean glycogen muscle concentration of 150 mmol/kg wet weight, it can be assumed that the exercise depleted glycogen of the whole leg muscle mass by only 18%. In our study, the RER also decreased after exercise when compared with the rest condition, but this did not prevent the occurrence of glucose declines. Therefore, it seems that the glycogen status, more than the exercise per se, is the reason behind the absence of a preprandial glucose decline, or more likely, the absence of its detection.
It must be noted that there was a much larger glucose decline at the onset of the exercise session (from ~ 5.0 to ~ 4.2 mmol.L-1), a well-known phenomenon mediated by the increase in muscle glucose uptake . This occurs despite the fact that liver potently increases its glucose output due to lower insulin and higher glucagon and catecholamine secretion . However, when preprandial glucose declines were observed, glucose concentrations were in a stable state in each subject.
Between the end of exercise and the meal request, carbohydrate oxidation was 46% lower than in the rest condition. Considering that ~ 20% of the CHO oxidized during exercise came from blood glucose , ~ 20 g of glucose needed to be compensated for, compared to the rest condition. Although the post-exercise reduction in glucose oxidation could not completely account for the compensation of this glucose difference, it may contribute to preclude an earlier preprandial glucose decline and meal request.
Glucose  and ghrelin  are the main putative determinants of meal initiation. We have previously reported that ghrelin is increased before meal request  but there are arguments against its role as a necessary factor in meal initiation . Moreover, ghrelin was not found to be altered after an exercise session of intensity and duration similar to the one used in our study . Cholecystokinin and glucagon-like peptide-1 have been reported to be increased after a single bout of exercise [11, 56, 57], but these hormones are involved in satiation or satiety and not in hunger.
Since the HRV indices were not different between conditions at the time subjects requested their meal, it seems that hunger occurs in a similar sympathovagal state after exercise or rest.
After exercise, the glucose peak was reached more than 30 min later than after rest. Since the rate of eating was kept similar across conditions, this may indicate that gastric emptying was slowed by prior exercise. The transit time of a 3331 kJ meal with 67% fat was not previously reported to be modified by prior exercise . However, mean energy intake at lunch in our study was higher (5225 ± 998 kJ), and the fat load was lower (45%) than in this previous study, so that this explanation cannot be excluded.
Based on the incremental profiles, exercise induced a higher postprandial glucose peak level and a 48% increase in total glucose response to the meal compared with the rest condition. Although our subjects were young and healthy, this could be interpreted as a detrimental effect of exercise since a sustained elevated postprandial glucose level is now considered an independent cardiovascular risk factor . However, the absolute values preclude such a conclusion because the glucose AUC over the 180 min was not different between conditions. These results suggest that this response might be explained by a lower basal glucose level after the exercise session, although it failed to reach statistical significance. It has been demonstrated that exercise consisting of a sufficient workload before a meal can induce a lower postprandial insulin level [5, 7, 13, 14]. This has been found to be partially explained by a reduced second-phase insulin secretion  and higher insulin clearance . Therefore, the exercise-induced increase in postprandial glucose response might be the result of reduced glucose transport into the muscles due to both lower insulin and a greater glucose output from the splanchnic region, which was facilitated by prior exercise . The increased post-exercise fatty oxidation observed in the muscle might also contribute to the increase in postprandial glucose. It has been documented that increasing fatty acid levels induces an increase in fat oxidation and decreased glucose oxidation via the inhibition of glucose transport/phosphorylation . The involvement of fat oxidation according to the well-known Randle cycle  has, to this day, only been demonstrated indirectly . That fat oxidation remained elevated by 46% in the exercise condition when compared to the rest condition 180 min after the meal supports this hypothesis. However, it is true that no study has yet demonstrated an increase in plasma glucose concentration due to an increase in fatty acid concentration. This absence has been attributed to a compensatory increase in insulin secretion , a phenomenon that might not occur following exercise.
Although increased heart rate indirectly suggests some sympathetic activation, the differences in LF/HF of the HRV analyses failed to reach significance. Interestingly, we actually observed that the previously described postprandial vagal withdrawal  was much more pronounced in the exercise than in the rest condition. The fact that this difference involved not only the HFms2 but also the HFnu suggests its vagal origin. Pancreatic β-cells express several G protein-coupled receptors that respond to parasympathetic innervation and in turn increase glucose-stimulated insulin secretion . Recently, the importance of vagal activity was demonstrated using atropine which partially blocked insulin sensitivity in the postprandial period . Thus, the effect of prior exercise on postprandial metabolism could involve postprandial vagal withdrawal and sympathetic activation, both of which would result in a transiently blunted glucose tolerance mediated by reduced insulin secretion [21, 66]. Importantly, this decrease in global HRV is not consecutive to a lower ability to detect variability . HRV is lower after exercise than after rest because exercise induces a significant decrease in parasympathetic activity and an increase in sympathetic activity (leading to the increased HR) but with a global diminution in global HRV . However, changes in vagal activity that are determined using HRV (i.e., heart branch) are not always associated with consistent changes in hormones, which are known to be highly dependent on the abdominal vagal activity . Therefore, this hypothesis requires further investigation.
In young and healthy male adults, a meal is requested during the same preprandial glucose decline after exercise than after rest but in a metabolic state that is characterized by higher oxidation of fat. This difference is still observed 3 h after meal consumption and is accompanied by a higher glucose response to the meal. Our results suggest that a shift in the sympathovagal balance toward a sympathetic predominance may contribute to this effect of exercise.
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