Morning-evening differences in response to exhaustive severe-intensity exercise.

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Morning–evening differences in response to exhaustive severe-intensity exercise David W. Hill

Abstract: The aim was to investigate the effect of time of day on 4 variables that are related to sport performance. Twenty healthy young men (mean ± SD: 22 ± 3 years, 1.78 ± 0.08 m, 72.0 ± 7.0 kg) performed exhaustive severe-intensity cycle ergometer tests at 278 ± 35 W (3.8 ± 0.4 W·kg–1) in the morning (between 0630 h and 0930 h) and in the evening (between 1700 h and 2000 h). Despite that gross efficiency was lower in the evening (estimated oxygen demand was 6% higher, P < 0.05), time to exhaustion was 20% greater (P < 0.01) in the evening (329 ± 35 s) than in the morning (275 ± 29 s). Performance in the evening was associated with a 4% higher (P < 0.01) maximal oxygen uptake (54 ± 7 mL·kg–1·min–1 vs. 52 ± 6 mL·kg–1·min–1, for the evening and the morning, respectively) and a 7% higher (P < 0.01) anaerobic capacity (as reflected by maximal accumulated oxygen deficit: 75 ± 9 mL·kg–1 vs. 70 ± 7 mL·kg–1, for the evening and the morning, respectively). In addition, oxygen uptake kinetics was faster in the evening, which resulted in slower utilization of the anaerobic reserves. It is concluded that modest morning–evening differences in maximal oxygen uptake, anaerobic capacity, and oxygen uptake kinetics conflate to produce a markedly longer performance in the evening than in the morning. Time of day must be considered for exercise testing and perhaps for exercise training. Key words: aerobic, anaerobic, circadian, diurnal, exercise, kinetics. Résumé : Cette étude se propose d’évaluer l’effet du moment de la journée sur quatre variables associées a` la performance sportive. Vingt jeunes hommes en bonne santé (moyenne ± é-t : 22 ± 3 ans, 1,78 ± 0,08 m, 72,0 ± 7,0 kg) participent a` d’épuisants tests vigoureux sur un cycloergomètre a` une intensité de 278 ± 35 W (3,8 ± 0,4 W·kg–1), et ce, le matin (entre 6 h 30 et 9 h 30) et en soirée (entre 17 h et 20 h). Même si le rendement brut est plus faible en soirée (le besoin estimé d’oxygène est de 6 % plus élevé, P < 0,05), la durée de l’exercice jusqu’a` épuisement augmente de 20 % (P < 0,01) en soirée (329 ± 35 s) comparativement au matin (275 ± 29 s). La performance en soirée est associée a` un plus haut (P < 0,01) de consommation maximale d’oxygène de 4 % en soirée (54 ± 7 mL·kg–1·min–1) comparativement a` celui du matin (52 ± 6 mL·kg–1·min–1) et une capacité anaérobie de 7 % plus élevée (P < 0,01) indiquée par le déficit maximal d’oxygène accumulé : 75 ± 9 mL·kg–1 (soirée) comparativement a` 70 ± 7 mL·kg–1 (matin). En outre, la cinétique du consommation d’oxygène est plus rapide en soirée, ce qui se manifeste par une utilisation plus lente des réserves anaérobies. En conclusion, les faibles différences entre le matin et la soirée du consommation maximale d’oxygène, de la capacité anaérobie et de la cinétique du consommation maximale d’oxygène se combinent pour offrir une performance nettement plus longue en soirée que le matin. On devrait donc prendre en compte le moment de la journée pour effectuer une évaluation et, probablement, un entraînement physique. [Traduit par la Rédaction] Mots-clés : aérobie, anaérobie, circadien, diurne, exercice physique, cinétique.

Introduction The circadian rhythms in virtually all physiological functions in human beings define the body’s internal environment, which changes predictably over a day (Li and Lin 2009; Sollberger 1965). Time of day affects exercise (Baxter and Reilly 1983; Chtourou et al. 2012c; Hill et al. 1992; Melhim 1993) and sport performance (Drust et al. 2005; Teo et al. 2011), with performance generally peaking in the evening (Chtourou and Souissi 2012). Most team sports, and the majority of events in sports including track and field, swimming, rowing, skating, and skiing, involve sustained efforts at severe exercise intensities, defined as intensities above critical power, the asymptote of the power–duration relationship (Gaesser and Poole 1996). Several factors contribute to performance, including (i) exercise efficiency, (ii) maximal rate of oxygen uptake and utilization (V˙O2max), (iii) V˙O2 kinetics, and (iv) anaerobic capacity (Jones and Burnley 2009; Joyner and Coyle 2008). It has not been well established if circadian rhythms in any of these factors influence performance.

There is evidence of a circadian rhythm in exercise efficiency, as steady-state V˙O2 at a given power output is higher in the evening than in the morning (Giacomoni et al. 1999; Hill 1996; Hill et al. 1989; Reilly and Baxter 1983; Reilly and Brooks 1982), but not always (Faisal et al. 2010; Noordhof et al. 2010b). However, if there is a rhythm, and efficiency is worse in the evening (higher V˙O2, lower efficiency), then the rhythm does not contribute in a positive way to the typical pattern of performance across the day. It is equivocal whether there is a circadian rhythm in maximal aerobic power, with some studies reporting V˙O2max values ⬃5% higher in the evening (Hill 1996; Hill et al. 1989) and some reporting no difference (Bessot et al. 2011; Burgoon et al. 1992). The V˙O2 response in severe-intensity exercise has been shown to be faster in the evening than in the morning (Hill 1996; Marth et al. 1998). However, those authors used a simple mono-exponential model and thus were unable to discriminate the fast and slow components of the V˙O2 response. The influence of time of day on maximal accumulated oxygen deficit (MAOD), the most defensible measure of anaerobic capacity (Saltin 1990; Green and Dawson

Received 8 April 2013. Accepted 6 August 2013. D.W. Hill. Applied Physiology Laboratory, Department of Kinesiology, Health Promotion, and Recreation, 1155 Union Circle #310769, University of North Texas, Denton, TX 76203-5017, USA. E-mail for correspondence: [email protected]. Appl. Physiol. Nutr. Metab. 39: 248–254 (2014) dx.doi.org/10.1139/apnm-2013-0140

Published at www.nrcresearchpress.com/apnm on 13 September 2013.


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1995; Noordhof et al. 2010a), has received little attention. Marth et al. (1998) found that MAOD was greater in the evening than in the morning. Exercise performance at different times of day reflects the complex interactions among many systems and coordination between the “master” clock in the hypothalamus and the “slave” oscillators in the peripheral tissues (Li and Lin 2009; McWatters et al. 1999), including muscles (Yang et al. 2006; Zhang et al. 2009). However, the nature of interactions between rhythms in exercise responses and temperature (Drust et al. 2005; Teo et al. 2011) or hormonal expression (Teo et al. 2011) remains to be elucidated. Investigation of possible time-of-day effects in factors that relate to exercise performance is important towards understanding the coordination among oscillators, as well as for explaining the effects of time of day on exercise and training responses. Bessot et al. (2011) noted that the effects of time of day on performance are not explained by 1 or 2 variables, but represent the effect of a combination of factors. The purpose of this study was to investigate the effect of time of day on 4 variables that are related to sport performance O exercise efficiency, V˙O2max, V˙O2 kinetics, and anaerobic capacity O and on exercise performance itself. The hypothesis was that V˙O2max would be higher, the V˙O2 response would be faster, and anaerobic capacity would be larger in the evening.

Materials and methods Overview of the study The study was approved by the Institutional Review Board for the Protection of Human Subjects at the University of North Texas. Each participant reported to the Applied Physiology Laboratory 7 times. The first visit was to obtain consent, to perform screening procedures, to administer the Horne and Östberg (1976) chronotype questionnaire, and to familiarize the participants with testing procedures. Participants were instructed to sleep at least 6 h prior to each test; not to exercise and not to ingest carbonated beverages, caffeine, or alcohol for 12 h before each test; and not to eat a heavy meal in the 3 h before each test. Actual dietary intake was at each participant’s discretion and was not recorded. They were tested only if they verified that they had had a good night’s sleep and that they had adhered to these instructions. On the second, third, and fourth visits, participants performed an incremental, cycle ergometer test for determination of peak power, with tests scheduled as described above. The first test was scheduled either in the morning or the evening, with the time selected by random assignment. For visits 3 and 4, 1 test was in the morning and 1 in the evening; scheduling was counterbalanced across participants, and assigned using randomization. On the fifth, sixth, and seventh visits, participants performed an exhaustive, square-wave test (in which the work rate is abruptly increased, maintained constant thereafter, and sustained by the participant for as long as possible) for determination of aerobic responses, such V˙O2max and V˙O2 kinetics (see Poole and Jones 2012), and anaerobic responses, such as MAOD and peak lactate concentration (see Noordhof et al. 2010a). These tests were scheduled in the same way as the incremental tests. Unbeknownst to the participants, the first incremental test and the first constantpower test were practice trials and the results were discarded. Testing sessions were separated by at least 24 h. In the morning, the participant arrived at 0630 h, 0715 h, 0800 h, or 0845 h, scheduled so as not to compromise his normal sleep patterns, and data collection was completed in 45 min. For the evening tests, the participant arrived at 1700 h, 1745 h, 1830 h, or 1915 h. The 4 tests reported in this paper were carried out in a 2-week period. All tests were performed in similar conditions (20 °C to 22 °C; 45% to 50% relative humidity).

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Participants The participants were 20 healthy young men, who were nonsmokers and were not taking any medications. They were physically active Kinesiology majors who did not exercise regularly at any particular time of day, were not training for competitive sports, and were not particularly experienced with cycling exercise. Participants were informed of the risks and benefits of the study, and they provided written informed consent to participate. Importantly, they did not have to alter their normal sleep–wake cycle to accommodate the testing schedule. The number of participants was determined by the logistics of performing the required number of tests at the specific times of day while avoiding extended holiday periods. Participants’ mean (±SD) age and height were 22 ± 3 years and 1.78 ± 0.08 m, respectively. Each participant was weighed each time upon arriving at the laboratory for testing and the average of the values for each individual was recorded. The group mean value was 72.0 ± 7.0 kg. Based on results from the Horne and Östberg (1976) chronotype questionnaire, 2 participants were moderate evening types (with morningness–eveningness scores of 37 and 39), and the remainder were neither type (mean score, 49 ± 4; range, 42 to 55). Thus, chronotype was not included as a factor in any analyses. Resting measurements Before each constant-power test, the participant lay in a dark, quiet room for 10 min. Then, oral body temperature (SureTemp Plus 690, Welch Allyn, Skaneateles Falls, N.Y., USA), blood pressure (standard auscultatory method), and resting heart rate (HR) (palpation for 30 s) were measured. Data from the sixth and seventh visits to the laboratory are reported. Incremental tests Exercise tests were performed on an electronically braked Lode Excalibur (Groningen, Netherlands) cycle ergometer, with a cadence of 80 revolutions per min (rev·min–1). Saddle and handlebar configuration was recorded and replicated for all of a participant’s tests. A digital readout of the cadence was visible during the tests. The tests began with a 4-min warm-up at 80 W, followed by a 4-min warm-up at 100 W. Then, the work rate was increased 50 W every 2 min. The tests were terminated when the participant allowed the cadence to drop below 76 rev·min–1 for 3 s, despite strong verbal encouragement. The highest work rate sustained for at least 60 s was recorded as the peak power. Constant-power (square-wave) tests The square-wave exercise tests were performed on the Excalibur ergometer, configured as in the incremental tests, and again using 80 rev·min–1. The tests began with a 4-min warm-up at 70 W, followed by a 4-min warm-up at 90 W. Then, the participant sat on the ergometer and rested for 4 min. After the rest, he began pedaling at 80 rev·min–1 and the resistance was rapidly adjusted (in 3 s) to provide the target work rate, which was the peak power from the incremental tests. Six participants had a higher peak power in the evening, so mean peak power in the evening tests (285 ± 43 W) was higher (P < 0.05; ES = 0.40) than in morning tests (270 ± 30 W), and the work rate for constant-power tests was 278 ± 35 W (3.8 ± 0.4 W·kg–1). Each test was terminated when the participant allowed the pedaling cadence to drop below 76 rev·min–1 for 3 s, despite strong verbal encouragement. All participants maintained the proper cadence (±1–2 rev·min–1) until exhaustion was imminent. Time to exhaustion (Texhaustion), the criterion measure of exercise performance, was measured to the nearest second. The participant remained seated on the ergometer for 5 min after termination of the exercise test, and a blood sample was obtained for determination of blood lactate concentration. Published by NRC Research Press


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V˙O2max and other cardiorespiratory measurements During each test, expired gases were analyzed using a MedGraphics CardiO2 Metabolic System (St. Paul, Minn., USA), which was calibrated prior to each test according to the manufacturer’s instructions. Minute ventilation (V˙E), V˙O2, and respiratory exchange ratio (RER; carbon dioxide output/V˙O2) were determined on a breath-by-breath basis and serial 15-s averages and rolling 5-breath averages were calculated. V˙O2max was the highest 30-s value in each constant-power test, calculated from consecutive 15-s V˙O2 values. HR was measured by short-distance telemetry using a Polar heart rate monitor (Lake Success, N.Y., USA). Values from the last 15 s of each minute of exercise were averaged and are reported. Calculation of exercise efficiency Steady-state V˙O2’s from the last 30 s of the 4-min warm-up stages of the incremental and constant-power tests were used to define the linear relationships between work rate and V˙O2, in the morning and in the evening. Each y intercept represents the oxygen demand of unloaded pedaling at 80 rev·min–1 at the particular time of day, and each slope is the “per-watt” oxygen demand. Then, the oxygen demand (mL·min−1) of the exhaustive exercise bouts at each time of day was determined by extrapolation, using the calculated y intercepts and slopes. Thus, while a participant had the same work rate in morning and evening tests, oxygen demands were different. These oxygen demands were used in the calculation of MAOD (below) and were themselves used as the indicators of exercise efficiency, gross efficiency being the inverse of the oxygen demand for a given work rate. Description of the V˙O2 response profile (V˙O2 kinetics) For each individual, for each constant-power test, data from the first 20 s of exhaustive exercise were removed (Whipp and Rossiter 2005), and the remaining 5-breath averages were fit to the following model (Whipp and Rossiter 2005) using the iterative regression procedure in KaleidaGraph 4.0 software (Reading, Pa., USA): V˙O2共t兲 ⫽ V˙O2baseline ⫹ Aprimary × [1 ⫺ e⫺共t⫺TDprimary兲/␶primary] ⫹ Aslow × [1 ⫺ e⫺共t⫺TDslow兲/␶slow] where V˙O2(t) is the VO2 at time = t, V˙O2baseline is the steady-state V˙O2 at the end of the 4-min recovery after the warm-up, Aprimary and Aslow are the projected increases in V˙O2 because of the primary and slow component responses, TDprimary and TDslow are the time delays preceding the 2 responses, and ␶primary and ␶slow are the time constants of the 2 responses. Often, the slow component response is more linear than exponential, so values for Aslow and ␶slow are very high, and the slow component appears to be driving the V˙O2 towards an unattainable value. In this case, a more meaningful descriptor of the response , is the actual increase in V˙O2 because of the slow component, Aslow which was calculated as ⫽ Aslow × [1 ⫺ e⫺共Texhaustion⫺TDslow兲/␶slow] Aslow Aslow and TDslow were used to describe the characteristics of the slow component.

Calculation of anaerobic capacity Calculation of MAOD has 3 steps (Medbø et al. 1988). Total oxygen cost (mL) is the product of oxygen demand and Texhaustion. Accumulated oxygen uptake, representing the aerobic contribution, is the area under the V˙O2 curve, not including the “excess V˙O2” contribution of the slow component (Hill et al. 2012); this area was determined by integration using KaleidaGraph software.

Table 1. Performance and anaerobic capacity measures in square-wave tests performed in the morning and in the evening. Variable

Morning

Evening

Work rate (W) Texhaustion (s) O2 demand (mL·min−1) O2 cost (mL) Accumulated O2 uptake (mL) Excess V˙O2 MAOD (mL) MAOD (mL·kg−1) Blood lactate (mmol·L−1)

278±35 275±29 3889±956 17824±2181 12759±2944 1118±395 5066±665 70±7 15.3±2.7

278±35 329±35** 4136±1077** 22681±2988** 17252±3421** 1248±410* 5428±614** 75±9* 16.8±2.8**

Note: Values are means ± SD. Texhaustion, time to exhaustion; MAOD, maximal accumulated oxygen deficit. *, Evening mean different from morning mean, P < 0.05. **, Evening mean different from morning mean, P < 0.01.

MAOD is calculated by subtraction of the accumulated oxygen uptake from the total oxygen cost. A blood sample was obtained from a warmed fingertip at 5 min after each test, when blood lactate concentration values peak following exercise challenges such as that provided in this study (Oyono-Enguelle et al. 1990). Blood lactate concentration was immediately determined using an Accusport Accutrend analyzer (Hawthorne, N.Y., USA). This analyzer has been validated against bench chemistry reference methods (Fell et al. 1998). Statistical analyses After distribution for each variable was deemed normal (Shapiro– Wilk), paired-means t tests were used to compare the values from the morning and evening tests. Significant was set at P < 0.05). Effect sizes (ES; calculated as the difference divided by the pooled SD) are reported. Data are presented as means ± SD. Whenever values are reported on a per-kilogram basis, they reflect an absolute value that was divided by the participant’s mean body weight over the course of the study. Therefore, reported values are not influenced by day-to-day or time-of-day variability in body mass.

Results Resting measures Body temperature was higher (P < 0.05; ES = 1.96) in the evening (37.1 ± 0.3 °C) than in the morning (36.6 ± 0.2 °C). Systolic blood pressure was higher (P < 0.01; ES = 1.23) in the evening than in the morning (125 ± 7 mm Hg vs. 117 ± 6 mm Hg); diastolic pressure was not different (P > 0.05; ES = 0.36) (72 ± 6 mm Hg vs. 74 ± 5 mm Hg). HR was higher (P < 0.05; ES = 0.93) in the evening (59 ± 8 beats·min−1 vs. 52 ± 7 beats·min−1). Results of the incremental tests As the purpose of this study was to investigate responses in severe-intensity exercise, only a few results from incremental tests are given. Time of day did not affect the value of the highest V˙O2 that was attained in the incremental tests (52 ± 7 mL·kg–1·min–1 in the morning vs. 53 ± 7 mL·kg–1·min–1 in the evening; +2%; P > 0.05; ES = 0.15). As noted above, peak power (the highest work rate sustained for 60 s) was higher in the evening. Performance Texhaustion was the performance measure in this study. The Texhaustion was 54 s (+20%) higher (P < 0.01; ES = 1.72) in the evening tests. Mean values for Texhaustion are presented in Table 1. Exercise efficiency At all warm-up work rates (70 W, 80 W, 90 W, 100 W), HR, V˙E, and RER were slightly higher (P < 0.05) in the evening. It was assumed that the intensity in each and every warm-up was below the lactate threshold and that the V˙O2 equaled the oxygen demand Published by NRC Research Press


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Table 2. Maximal aerobic responses in squarewave tests performed in the morning and in the evening.

Table 3. Oxygen uptake kinetics in square-wave tests performed in the morning and in the evening.

Variable

Morning

Evening

Variable

Morning

Evening

HRmax (beats·min−1) V˙Emax (L·min−1) RERmax V˙O2max (mL·min−1) V˙Omax (mL·kg−1·min−1)

189±11 141±26 1.24±0.09 3715±541 52±6

193±13* 151±28* 1.28±0.09* 3861±569** 54±7**

V˙O2baseline (mL·min−1) TDprimary (s) ␶primary (s) Aprimary (mL·min−1) TDslow (s) Aslow (mL·min−1) Aslow /(Aprimary +Aslow ) (%) V˙O2max (mL·min−1)

323±39 6±4 24±6 2748±533 91±12 644±252 19±4 3715±541

349±41* 5±3* 19±4* 2977±521** 72±12** 535±270 15±4* 3861±569**

Note: Values are means± SD. HRmax, maximal heart rate; V˙Emax, maximal minute ventilation; RER, respiratory exchange ratio; V˙O2max, maximal oxygen uptake. *, Evening mean different from morning mean, P < 0.05. **, Evening mean different from morning mean, P < 0.01.

because (i) inspection of the responses revealed no evidence of a slow component, (ii) each RER was less than 0.96, and (iii) in no case did the V˙O2 exceed 55% of V˙O2max. The y intercept of the V˙O2/work rate relationship appeared to be higher in the evening (8.4 ± 0.4 mL·kg−1·min−1 vs. 8.1 ± 0.4 mL·kg−1·min−1) but the difference was not significant (P > 0.05; ES = 0.12); the slope was greater (P < 0.01; ES = 2.01) in the evening (12.7 ± 0.4 mL·min−1·W−1 vs. 11.9 ± 0.4 mL·min−1·W−1). The data fit the regression model well: across all tests, the SEE was small (0.1 ± 0.1 mL·kg−1·min−1 for the y intercept and 0.1 ± 0.1 mL·kg−1·W−1 for the slope), and the R2 was 0.993 ± 0.004. The estimated oxygen demand in the severe-intensity exercise was 6% higher (P < 0.05; ES = 0.54) in the evening (Table 1); thus, gross efficiency was lower at that time. V˙O2max and other cardiorespiratory responses to severe-intensity exercise Maximal aerobic responses from the constant-power tests are presented in Table 2. V˙O2max was 2 mL·kg–1·min–1 (4%) higher (P < 0.05; ES = 0.31) in the evening. The V˙Emax, RERmax, and HRmax were also higher (P < 0.05) in the evening. V˙O2 kinetics in severe-intensity exercise Characteristics of the V˙O2 response profile are in Table 3. In evening tests, Aprimary was 8% greater (P < 0.05; ES = 0.42), ␶primary was 5 s shorter (P < 0.05; ES = 0.82), TDprimary was 1 s shorter (P < 0.05; ES = 0.21), and TDslow was 19 s shorter (P < 0.01; ES = 1.62); the amplitude of the slow component was significantly smaller in the evening when expressed as a percentage of the overall increase in V˙O2 (P < 0.01; ES = 0.62). Although the participants performed only 1 exercise test at each time of day, the signal-to-noise ratio appears to have been high, as the parameter estimates were obtained with very good confidence: across all tests, the SEE of the estimates were small (48 ± 36 mL·min–1 for Aprimary, 2 ± 2 s for ␶primary, 2 ± 1 s for TDprimary, and 9 ± 5 s for TDslow) and the R2 was 0.981 ± .012. For each test, the residuals were plotted and fitted to a polynomial function; there was no discernible pattern to the residuals. Anaerobic capacity Results related to anaerobic capacity are in Table 1. The higher oxygen demands and greater Texhaustion resulted in a total oxygen cost (mL) that was 27% greater (P < 0.01) in the evening. The MAOD was 5 mL·kg−1 (7%) greater (P < 0.01; ES = 0.63) in the evening. Peak postexercise blood lactate concentration, the estimate of the glycolytic contribution, was 10% (1.5 mmol·L–1) higher (P < 0.01; ES = 0.56) in the evening.

Discussion The important finding was that despite efficiency being lower and the oxygen demand of exercise higher in the evening, higher V˙O2max, faster V˙O2 kinetics, and greater anaerobic capacity conflated to produce a markedly longer performance time in the

Note: Values are means ± SD. See text for definitions. *, Evening mean different from morning mean, P < 0.05. **, Evening mean different from morning mean, P < 0.01.

evening than in the morning. This is the first study to concurrently evaluate the possible contribution of morning–evening differences in 4 distinct physiological characteristics (exercise efficiency, V˙O2max, V˙O2 kinetics described using comprehensive modeling techniques, and anaerobic capacity) that are related to performance. Time of day and resting measures Testing times coincided with typical daytime peaks and troughs in exercise responses. Values for HR, blood pressure, and oral temperature were consistent with the classical sine wave rhythms of body temperature and resting metabolism (Sollberger 1965). Exercise efficiency In agreement with many studies (e.g., Giacomoni et al. 1999, Hill 1996, Hill et al. 1989, Reilly and Baxter 1983, Reilly and Brooks 1982) but not all (e.g., Faisal et al. 2010, Noordhof et al. 2010b), V˙O2 in the moderate-intensity warm-ups was slightly higher in the evening. Higher steady-state V˙O2’s in the evening may be explained by the rhythm in body temperature (Sollberger 1965), which persists in exercise (Martin et al. 2001). Resting body temperature would affect the metabolic rate and the y intercept of the V˙O2/work rate relationship. While previous studies have demonstrated a time-of-day effect on steady-state V˙O2, the effect on the slope of the relationship is a novel finding, and important because the greater slope of the relationship in the evening suggests that something during exercise contributes to the morning–evening differences. Efficiency was lower (“worse”) in the evening; thus, greater Texhaustion in the evening occurred despite a time-of-day effect on efficiency, and certainly not because of it. V˙O2max As in other studies involving severe-intensity, constant-power exercise (Hill 1996; Marth et al. 1998), V˙O2max was higher in the evening. Constant-power exercise may provide a more sportspecific task than an incremental test. V˙O2 has been reported to reach higher peak values in the evening (Hill et al. 1992; Souissi et al. 2010) in exhaustive, extreme-intensity exercise, in which the tolerable duration is too short to attain V˙O2max. Interestingly, the highest V˙O2 that is achieved in incremental tests often appears not to vary with the time of day (Bessot et al. 2011; Burgoon et al. 1992; Reilly and Brooks 1982), as in the present study. One explanation for morning–evening differences in V˙O2max from only constant-power tests might be that the rhythm in anaerobic capacity permits a longer exercise duration in the evening, and time to reach a true V˙O2max. The results of the present study confirm that there is a time-of-day effect on V˙O2max achieved in constantpower exercise, but not on V˙O2max achieved in incremental exercise. Cardiac output was not measured, so it is not known if the higher HRmax in the evening contributed to the higher V˙O2max. Previously, no time-of-day effect was detected in cardiac output in Published by NRC Research Press


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heavy-intensity exercise (Faisal et al. 2010). If there is circadian rhythm in V˙O2max but not in cardiac output, there must be a corresponding rhythm in peripheral extraction of oxygen and (or) utilization by the muscles, possibly enhanced by higher temperatures and increased enzymatic activity in the evening. The time-of-day effect has some obvious implications for exercise testing. It might seem that training in the evening would potentially be more beneficial because the higher V˙O2max in the evening permits greater absolute demands on the aerobic machinery. No study has investigated this possibility with an appropriately large sample size. V˙O2 response profile (V˙O2 kinetics) Faster V˙O2 kinetics contributes to performance by reducing reliance on anaerobic pathways early in exercise (Jones and Burnley 2009; Vanhatalo et al. 2011). In this study, the parameter estimates were obtained with very good confidence (i.e., small SEE), and virtually every aspect of the V˙O2 response profile was affected by the time of day. This is the first study to investigate the effect of time of day on V˙O2 kinetics during exhaustive, severe-intensity exercise using comprehensive modeling techniques. Hill (1996) and Marth and colleagues (1998) reported a faster overall V˙O2 response in severe-intensity exercise in the evening; but they used only a simple mono-exponential model with no time delay. Results obtained using comprehensive modeling techniques revealed no time-of-day effect on the V˙O2 response in nonexhaustive moderate-intensity (Brisswalter et al. 2007; Carter et al. 2002; Faisal et al. 2010) or heavy-intensity exercise (Carter et al. 2002; Faisal et al. 2010; Santana et al. 2008). However, the exhaustive, severeintensity exercise used in the present study presents a different metabolic challenge, allows complete expression of the slow component, and permits attainment of V˙O2max. No time-of-day effect in moderate- or heavy-intensity exercise does not preclude such an effect in severe-intensity exercise: in severe-intensity exercise, the limitation is more complex (Hughson 2009), involves peripheral factors (Hughson 2009; Poole and Jones 2012) that may be subject to influence by the underlying rhythm in core temperature, and may be influenced by the peripheral oscillators (Zhang et al. 2009). V˙O2 at the onset of exercise is projecting toward the oxygen demand (Hebestreit et al. 1998; Hughson et al. 2000), which was higher in the evening. This may explain why Aprimary was larger in the evening. But, in addition, ␶primary, TDprimary, and TDslow were smaller. These differences are not due to differences in oxygen demand (Barstow and Molé 1991; Hebestreit et al. 1998; Hughson et al. 2000). Therefore, something other than oxygen demand is implicated in the time-of-day effect on V˙O2 kinetics. Anaerobic capacity – blood lactate concentration Blood lactate concentration was 1.5 mmol·L–1 higher in the evening. Previously, Racinais and colleagues (2005) found higher concentrations after sprints in the evening than the morning (13 ± 3 mmol·L–1 vs. 11 ± 3 mmol·L–1) as did Reilly and Baxter (1983) after exhaustive exercise at 95% O˙2max (9.8 ± 0.4 mmol·L–1 vs. 8.2 ± 0.5 mmol·L–1). Of note, lactate concentration reflects only the glycolytic part of the anaerobic contribution. Anaerobic capacity – MAOD MAOD was 5 mL·kg−1 higher in the evening. In the only directly comparable study, MAOD was 7 mL·kg−1 greater in the evening in moderately fit women and men (Marth et al. 1998). Many studies found that work in a 30-s Wingate test is greater in the evening (Melhim 1993; Souissi et al. 2007, 2008; Chtourou et al. 2012c). However, while the Wingate is said to measure “anaerobic performance”, the extreme-intensity test is too short to engender maximal utilization of anaerobic reserves. Moreover, performance in a Wingate test is influenced by several factors. Indeed, Souissi and


colleagues (2007) attributed the greater work in the evening to a greater aerobic contribution at that time. The higher anaerobic capacity in the evening underscores the need to consider the time of day in exercise testing as well as training. While it has been shown that there is circadian specificity in training for anaerobic capacity (Chtourou et al. 2012a, 2012b; Hill et al. 1998), i.e., training at a particular time of day enhances performance at that time of day, it remains to be learned if there is any inherent advantage to training when the capacity is greatest. It is not known exactly what causes the slow component of the V˙O2 response (Hughson 2009; Poole and Jones 2012; Vanhatalo et al. 2011). Thus, it was asked if the slow component should be included in calculation of MAOD (Bearden and Moffat 2000), and it was demonstrated that the excess V˙O2 should not be included in the accumulated oxygen uptake (Hill et al. 2012). Possibly the excess V˙O2 is in response to an increasing oxygen demand. In the present study, the excess V˙O2 was not included the measure of aerobic contribution, and the ratio of morning–evening differences in MAOD (+5 mL·kg−1) and lactate concentration (+1.5 mmol·L–1) was 3.3 mL·kg−1 per mmol·L–1, equal to the published value for the oxygen equivalent of blood lactate (di Prampero and Ferretti 1999). Moreover, if the phosphocreatine contribution is ⬃20 mL·kg−1 (Serresse et al. 1988) and if the oxygen equivalent of lactate is indeed 3.3 mL·kg−1 per mmol·L–1, then the sum of the phosphocreatine and glycolytic contributions would be 67 mL·kg−1 and 72 mL·kg−1 in the morning and evening tests, and similar to the calculated values of 70 mL·kg−1 and 75 mL·kg−1 for MAOD. Had the excess V˙O2 been included in the accumulated oxygen uptake, the MAOD values would have been only 55 mL·kg−1 and 58 mL·kg−1. These results show that the higher anaerobic capacity in the evening resides in differences in glycolytic capacity, as well as that the excess V˙O2 should not be included in the accumulated oxygen uptake for the calculation of MAOD. Performance in exhaustive, severe-intensity exercise Exercise performance was greater in the evening, consistent with other studies involving severe-intensity exercise (Baxter and Reilly 1983; Bessot et al. 2006; Hill 1996). The 20% morning–evening difference in Texhaustion was greater than the difference usually reported for extreme-intensity, 30-s Wingate tests (⬃3% to 11%, as reviewed by Chtourou and Souissi 2012) but similar to the 16% difference reported by Melhim (1993) for 30-s Wingate performance and by Bessot and colleagues (2006) for severe-intensity tests of ⬃4½ min duration. Perhaps the ⬃6-min duration was associated with such a large time-of-day effect because it was engenders the truest (highest) expressions of V˙O2max and anaerobic capacity and, therefore, the largest absolute morning–evening differences in aerobic and anaerobic contributions. The morning–evening differences in the factors that contributed to performance were small. The increased oxygen demand in the evening added about 16 mL·kg−1 to the demand over the first 275 s (the exercise duration in the morning); the greater demand was countered by a savings of about 5 mL·kg−1 because of faster kinetics, about 9.5 mL·kg−1 from the higher overall V˙O2, and about 1.5 mL·kg−1 of the 5 mL·kg−1 higher MAOD. The “extra” 3.5 mL·kg−1 of anaerobic capacity seems small, but it explains the longer Texhaustion in the evening tests because the rate of anaerobic contribution near the end of exercise was quite small: about 93% of the oxygen demand was being met aerobically in the latter stages of exercise. This difference in anaerobic capacity in the evening would support only 2½% greater work rate for 275 s or a 2½% shorter time to complete a given amount of work, which is more pertinent to sport performance. The results of the present study do support the previous reports demonstrating the interaction of exercise efficiency, V˙O2max, V˙O2 kinetics, and anaerobic capacity on exercise performance (Jones and Burnley 2009; Joyner and Coyle 2008). Manipulation of the factors, for example by testing at different Published by NRC Research Press

Hill


times of day, provides insight into their roles in exercise performance as well as into the factors that drive or limit them. Possible limitations Although participants received some guidelines about preexercise food and fluid intake, it is quite likely that participants’ dietary intakes differed between the morning and evening tests and may possibly have had a small effect on the responses. For example, RER in the warm-ups was slightly higher in the evening tests, presumably because the intensities were slightly higher in the evening. Even if it also indicated a preferential use of carbohydrate in the evening warm-ups that lightly influenced the caloric equivalent of oxygen, it seems unlikely that the effect would persist and have any bearing on responses in the exhaustive severe-intensity exercise tests. Another possible limitation in the present study was the use of only 1 exercise test at each time of day. However, the 2 tests were performed in randomized order, after 1 familiarization session, 3 exhaustive incremental tests, and 1 exhaustive constant-power test. Efforts were made to minimize the day-to-day variability that is inherent in physiological measures (e.g., Shephard 1984). With regard to the maximal and performance measures, participants gave every effort of providing truly maximal efforts in each and every test. With regard to the V˙O2 kinetics measures, even in studies in which the primary focus was V˙O2 kinetics, a single test has been used to obtain parameter estimates (e.g., Vanhatalo et al. 2011) and, in the present study, the parameter estimates were associated with small SEE, suggesting good signal-to-noise ratio and precise identification of the parameters. The significant differences identified in the present study show that the time-of-day effect prevails despite the day-to-day variability in all physiological variables. Chronotype In a large sample (N = 1600) of university students, Baehr and colleagues (2000) detected few morning types (12%), a sizeable proportion of evening types (27%), and a majority of neither type (61%). In the present study, only 2 of the 20 participants expressed a chronotype, and not strongly. The lack of representation of morning types in the present study (0%) and the low representation of evening types (10%) may reflect that because all of the men were physically active Kinesiology majors; they were, perhaps, less likely in general to prefer an evening dominant schedule. Hill and colleagues (1989) identified 34% morning types, 44% evening types, and 22% neither type in a group of 32 university students who performed incremental exercise tests. Finding that chronotype affected only 1 of 10 measured submaximal and maximal responses, they concluded that diurnal variations in most responses to exercise are the same for morning types and evening types. However, the 1 variable that was impacted was V˙O2max, which was higher in the evening only in evening types. Tamm and colleagues (2009) identified 39% morning types, 39% evening types, and 22% neither type in a group of twenty-three 19- to 53-year-olds (Tamm et al. 2009). These authors also found that chronotype affected only some exercise responses, and reported that only evening types demonstrated greater maximal force production in the evening than in the morning, as a consequence of greater cortical and spinal activity, which might have implications for many kinds of exercise challenges. As noted by Tamm and colleagues (2009), chronotype is often overlooked in studies involving responses at different times of day, and the fact that the time of day may affect responses more (or only) in evening types may explain equivocal findings and certainly suggests that further study is indicated to determine if chronotype influences the effects of time of day on responses during exhaustive, constantpower, severe-intensity exercise.

253

Mechanisms Mechanisms underlying the observed time-of-day effects on exercise efficiency, V˙O2max, V˙O2 kinetics, and anaerobic capacity cannot be deduced from the results of this study. It is known that exercise responses demonstrate a pattern reflective of that of body temperature (Drust et al. 2005; Teo et al. 2011), and might also be related to the profiles of hormonal and other responses (Teo et al. 2011), but a causal relationship between various rhythms and exercise responses is tenuous (Teo et al. 2011). Higher body temperature may support greater enzyme activity and metabolic potential, which could improve anaerobic capacity or V˙O2max (Shephard 1984) or V˙O2 kinetics (Hughson 2009). The possible causative link between rhythms in temperature or hormonal responses and exercise efficiency is not so obvious. In fact, higher muscle temperatures in the evening might be expected to reduce muscle viscosity and improve efficiency (Shephard 1984). There is growing awareness of 2-way communication between the “master” clock in the suprachiasmatic nuclei and the “slave” oscillators in peripheral tissues (Li and Lin 2009; McWatters et al. 1999; Yang et al. 2006). Evidence that contractile activity might be the dominant zeitgeber for oscillators in the muscle (Zhang et al. 2009) suggests fascinating avenues for future research.

Conclusions Despite that efficiency is lower O the oxygen demand is higher O in the evening, small differences in V˙O2max, V˙O2 kinetics, and anaerobic capacity conflate to produce a longer tolerable duration for exhaustive, severe-intensity exercise in the evening than in the morning. The findings demonstrate that the time of day must be considered for exercise testing that involves evaluation of any of the performance-related variables that were examined in the present study. In addition, the results may have implications for designing training programs: the evening may be the optimal time of day to train because it is associated with a greater metabolic demand and because it permits greater levels of both aerobic and anaerobic energy production. Finally, the results suggest that V˙O2max, V˙O2 kinetics, and anaerobic capacity are not just related to performance, but that they contribute to performance: when each of these is affected (e.g., by the time of day) performance is impacted.

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Published by NRC Research Press

Preliminary evidence of a blunted anti-inflammatory response to exhaustive exercise in fibromyalgia.

Exhaustive exercise attenuates the neurovascular coupling by blunting the pressor response to visual stimulation.

Gender differences in the systolic blood pressure response to exercise.

Platelet activity and sensitivity to agonists after exhaustive treadmill exercise.

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Local Pain Dynamics during Constant Exhaustive Exercise.

Exercise and weight loss: no sex differences in body weight response to exercise.

Oxygen transport system during exhaustive exercise in Japanese boys.

Protein synthesis in skeletal muscle following acute exhaustive exercise.

Performance related factors are the main determinants of the von Willebrand factor response to exhaustive physical exercise.

Sex differences in drug addiction and response to exercise intervention: From human to animal studies.

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Metastable Pain-Attention Dynamics during Incremental Exhaustive Exercise.

Sex differences in the response to resistance exercise training in older people.

Sex-related differences in muscle deoxygenation during ramp incremental exercise: response to Peltonen et al.

Differences in the metabolic and hormonal response to exercise between racing cyclists and untrained individuals.

The influence of fitness on neuroendocrine responses to exhaustive treadmill exercise.

Prefrontal and motor cortex EEG responses and their relationship to ventilatory thresholds during exhaustive incremental exercise.

Effects of inspiratory muscle training on resistance to fatigue of respiratory muscles during exhaustive exercise.

Responses of glutathione system and antioxidant enzymes to exhaustive exercise and hydroperoxide.

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Exhaustive exercise increases the TNF-α production in response to flagellin via the upregulation of toll-like receptor 5 in the large intestine in mice.

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