Medicine & Science in Sports & Exercise:
Applied Sciences: Physical Fitness and Performance
Metabolic Recovery in Professional Road Cyclists: A 31P-MRS Study
HUG, FRANÇOIS1,2; BENDAHAN, DAVID3; FUR, YANN LE3; COZZONE, PATRICK J.3; GRÉLOT, LAURENT1
1Department of Sport Physiology, Faculty of Sport Sciences, IFR Marey, Marseille, FRANCE;2Laboratory of Respiratory Physiopathology, Faculty of Medicine, Marseille, FRANCE; and3Centre of Biological and Medical Magnetic Resonance, Faculty of Medicine, Marseille, FRANCE
Address for correspondence: Dr. François Hug, UPRES EA 3285, Department of Sport Physiology, IFR Marey–Faculty of Sport Sciences, University of the Mediteranean (Aix-Marseille II), 163, avenue de Luminy, CC 910, 13288 Marseille Cedex 09, FRANCE; E-mail: email@example.com.
Submitted for publication September 2004.
Accepted for publication December 2004.
Fabrice Salanson—in memoriam.
Many thanks to the professional road cyclists and the sport science students who all gave their best during the various exercises of the protocol. Many thanks also to the team managers who strongly supported this experimental series (Cofidis, Bonjour, FDJeux.com, AG2R Prévoyance, and Crédit Agricole).
This study was supported by a grant from Amaury Sport Organisation (ASO-Société du Tour de France).
Purpose: Aerobic training of professional road cyclists is linked to tremendous aerobic capacities that have never been clearly related to what occur in skeletal muscles submitted to a specific exercise. The aim of the present study was to examine specifically metabolic recovery after an incremental cycling exercise performed until exhaustion in professional road cyclists as compared with moderately trained subjects and so using 31P- MRS.
Methods: Subjects performed a progressive cycling exercise on a cycloergometer until exhaustion, then they were positioned back in the magnet (delay lower than 45 s) for recovery scanning. 31P spectra of thigh muscles were time averaged in 2-s blocks at rest and for 15 min throughout the recovery period.
Results: For a significantly more intense exercise (477 ± 28 vs 334 ± 24 W in controls; P < 0.001), professional road cyclists displayed similar end-of-exercise extrapolated pH values (6.43 ± 0.16 vs. 6.34 ± 0.05 in controls) and a significantly higher PCr concentration (20.1 ± 0.8 vs. 13.3 ± 0.5 mM in controls, P < 0.001). The pH recovery kinetics provided the evidence of metabolic adaptations related to a specific training in professional cyclists with a significantly faster rate (P < 0.01) of pH return toward basal values (32.8 ± 18.9 vs 10.8 ± 6.7 mM·min−1). On the contrary, no significant difference was measured for the PCr recovery kinetics. At rest, PDE concentration was significantly higher in professional cyclists (2.50 ± 0.80 vs 1.76 ± 0.42 mM), likely indicating a difference regarding fiber-type composition.
Discussion: The present data demonstrated for the first time that the tremendous aerobic capacity in professional cyclists is linked to faster pH recovery kinetics after a specific cycling exercise.
Professional cyclists (i.e., most successful cyclists) probably represent the pinnacle of natural selection and physiological adaptation to endurance exercise. The metabolic changes associated with aerobic training in professional road cyclists have been documented in a few studies showing a tremendous aerobic capacity, by far larger than what can be measured in amateur cyclists or untrained subjects. This larger aerobic capacity has been measured using a variety of techniques including gas exchange, metabolites measurements in venous blood samples, and biochemical analyses of muscle samples (27). Each of these techniques has inherent advantages and limitations. Both gas exchange and blood measurements provide indirect and global evaluations of muscle function. On the other hand, biochemical analyses of muscle biopsies provide direct measurements, but this technique has significant limitations regarding its repeatability and feasibility in the in vivo situation. Moreover, extraction procedures associated with the analysis of biopsy materials may lead to hydrolysis of labile metabolites and activation of metabolism, thereby introducing quantitative errors.
In contrast, 31P magnetic resonance spectroscopy (31P-MRS) offers a noninvasive alternative to evaluate within a given muscular group, the dynamic changes in high-energy phosphate compounds (i.e., ATP, phosphocreatine) and pH before, during, and after exercise (5). Metabolic effects of exercise training have been investigated, using 31P-MRS, in a variety of athletes or subjects involved in specifically designed training programs (18,19,21,22,33). However, methodological aspects have pointed out limitations regarding the extrapolation of the corresponding results in terms of athletic performance and metabolic adaptations in athletes. For instance, calf muscle has been investigated in skiers and runners (19,21), whereas in marathon runners and rowers, investigations have been performed in wrist flexor muscles (18,22). Although in these studies aerobic training has been associated with changes affecting exercise-induced acidosis and phosphocreatine (PCr) postexercise recovery rate, it should be underlined that the muscles investigated differed from those involved in the training process, thereby questioning the conclusions related to the local metabolic adaptations linked to exercise training. In addition, due to physical constraints within superconducting magnets, the types of exercises performed for the purpose of MRS investigations were very different from the typical (i.e., ecological situation) exercises performed by the athletes on a regular basis, both in terms of intensity and pattern of muscle recruitment, further questioning the conclusions provided in these studies.
In this line, local metabolic adaptations associated with exercise training should be analyzed in the proper muscles, that is, involved in repeated exercises and throughout a typical exercise performed until exhaustion. Apart from a pilot study (33) conducted in four subjects, no 31P-MRS investigation has been reported so far regarding the metabolic changes in trained cyclists during the short term recovery period of a specific cycling exercise performed until exhaustion. In addition, such a study has never been performed in professional road cyclists with a very high aerobic capacity.
In the present study, we aimed at documenting, using 31P-MRS, the metabolic changes associated with a specific brief cycling exercise performed until exhaustion in a population of highly trained road cyclists (i.e., professionals) as compared with moderately trained subjects.
MATERIALS AND METHODS
Sixteen male volunteers were included in the present study, which was approved by the local ethics committee. Informed written consent was obtained from each subject before inclusion. All subjects had no recent or previous pathology of limb muscles or joints. Eight were among the 200 professional cyclists over the world (P), and eight were students (S) from the Department of Sport Sciences. Professional road cyclists had a 7 ± 3 yr of international competitive experience. During the last season, they had covered an average of 30,000 km (range: 28,000–34,000 km corresponding to 22 ± 3 h of training and competition per week). Three of them had already participated to the World Championships for professional road cyclists with the French team in 2002. A particular characteristic of road cycling is that one third of the season, that is, 90–100 d, is devoted to competition. Therefore, racing days are part of the training program, with unpredictable variables such as weather conditions, team tactics, wind direction, etc. As previously reported by Lucia et al. (20), during the competition period (i.e., spring and summer), professional road cyclists perform 77% of their training/competition time at low intensity (<65% V̇O2max), 15% at moderate intensity (65–90% V̇O2max), and 8% at high intensity (>90% V̇O2max). Sport science students performed 6 ± 2 h of physical activity per week. Each of them practiced several recreational activities including soccer, climbing, basketball, swimming, and/or rugby, but excluding cycling. None of them practiced their sport activities at national or international levels. All subjects were instructed to refrain from intense physical activities during the 2 d before testing. Professional cyclists did not participate to any competition during these 2 d, and students did not perform any physical activity.
To characterize our populations in terms of physical and physiological aptitudes, subjects performed, in the midmorning before the experimentation, an incremental exercise during which the usual cardiorespiratory parameters were measured. Throughout this exercise trial, software (Oxycon Beta, Hellige®, Germany) computed breath-by-breath data of V̇E, V̇O2, V̇CO2, and the ventilatory equivalents for O2 (V̇E·V̇O2−1) and CO2 (V̇E·V̇CO2−1). The first ventilatory threshold (VT1) corresponded to the power output value at which V̇E·V̇O2−1 exhibited a systematic increase without a concomitant increase in V̇E·V̇CO2−1, and the second ventilatory threshold (VT2) was determined by using the criteria of an increase in both V̇E·V̇O2−1 and V̇E·V̇CO2−1 (24). Two independent observers detected VT1 and VT2 following the criteria previously described.
After a 5-h recovery period, including a freely chosen meal, cyclists performed the same progressive exercise in the hallway of the MRI center adjacent to the superconducting magnet room. Ambient conditions (temperature: 20–22°C; relative humidity: 45–50%) were kept constant among exercise sessions. During cycling, the subjects adopted conventional (upright) cycling posture, characterized by a trunk inclination of ≈75°. They placed their hands on the handlebars with elbows slightly bent (≈10° of flexion). Considering that muscle activity can be modulated by the type of saddle as previously described (8), we chose to use the same saddle (San Marco, Italy) for both groups and to keep it horizontal for all the subjects. To ensure optimal performance, pedaling rate was freely chosen by each subject who used sport shoes with clipless pedals. Both groups were investigated in the same period of the year (March–April). All the professional road cyclists were in an active competitive period in order to prepare the “Tour de France,” which was planned 2–3 months later (however, only three of them have really participated in the Tour de France 2002). Both protocols were similar and consisted of a progressive cycling exercise performed on an electrically braked cycloergometer (Excalibur sport, Lode®, the Netherlands). After 3 min of pedaling at 100 W, the load was increased by 26 W every minute until exhaustion and voluntary arrest by the subject. The last 1-min workload entirely completed by the subject was referred to as the maximum tolerated power (MPT). In the afternoon, the ergometer was placed in the hallway of the MRI center immediately adjacent to the superconducting magnet room so that the subjects could be positioned in the magnet and scanned as soon as possible (less than 45 s) after completion of the cycling exercise.
MR spectra of thigh muscles (i.e., rectus femoris, vastus medialis, vastus lateralis) were recorded at 25.9 MHz in the 1.5-T magnet of a Siemens Vision Plus (Siemens AG, Erlangen, Germany) using a commercially available 31P-1H surface coil (liver coil, 14 cm in diameter for the outer coil, and 8 cm in diameter for the inner coil). To be sure that the same muscles were measured on each subject, the localization of the probe was standardized using scout MR images recorded in the x, y, z planes. Magnetic field homogeneity shimming was performed on the proton signal using an automatic procedure. 31P spectra were time averaged in 2-s blocks (two scans, repetition time = 1 s, sweep width = 10 kHz) at rest and during 15 min of the early recovery period after the exercise performed on a cycloergometer. Fully relaxed spectra (N = 10, repetition time = 20 s) were recorded at rest to calculate the saturation factor of each metabolite. Ink marks on the thigh aligned with the cross hairs of the imager allowed for identical positioning in the magnet bore over repeat scans. Relative concentrations of phosphocreatine (PCr), inorganic phosphate (Pi), adenosine triphosphate (ATP), and phosphodiesters (PDE) were obtained by a time–domain fitting routine using the AMARES algorithm and appropriate prior knowledge of the ATP multiplets. Intracellular pH was calculated from the chemical shift of the Pi signal relative to the PCr signal. Proton efflux was calculated considering together proton production from PCr resynthesis and pH changes during the early recovery period as previously described (2).
Subjects were scanned 44.5 ± 17.9 s after the end of cycling exercise, with no significant difference between the two groups. End-of-exercise PCr and pH values were extrapolated at time-zero using regression methods. Regression quality was estimated using Pearson product coefficients. Considering, in agreement with previous studies (2,17), that time-dependent PCr changes are linear during the initial period after exercise, end-of-exercise PCr values were extrapolated using a linear regression over the first 30 s of recovery. Regarding pH, we chose a biexponential regression over the overall data set for each subject in agreement with previous analyses during high-intensity exercise (34).
Results are expressed as mean ± SD. A one-way analysis of variance (ANOVA) with repeated measurements was performed in order to investigate the metabolic variable changes between rest, end of exercise, and end of the recovery period. Student’s t-tests were performed to compare physiological, physical, and metabolic variables between the two groups. To evaluate the relationship between variables, Pearson correlation coefficient was calculated. Statistical significance was established at the P < 0.05 level.
Measurements at rest.
The morphological and physiological characteristics of both groups are detailed in Table 1. Professional cyclists were slightly taller than controls. One representative series of 31P spectra is depicted in Figure 1. Values of PCr/Pi, PCr/ATP, and Pi/ATP ratios and the corresponding absolute concentrations of PCr, Pi, and PDE and pH values measured at rest are summarized in Table 2. The whole set of variables was similar between both groups except the PDE concentration, which was significantly higher in professional cyclists (2.50 ± 0.80 vs 1.76 ± 0.42 mM in controls). On the other hand, it is noteworthy that a 21% reduction of the PCr/Pi ratio was measured in professional cyclists, but this reduction did not achieve the significant threshold.
Metabolic changes in exercise and recovery.
The average maximal power tolerated (MPT) was exactly the same between the morning and the afternoon session and was significantly higher in professional cyclists as compared with controls (477 ± 28 W vs 334 ± 24 W; P < 0.001), and this difference remained when body mass was taken into account (Table 1). In that respect, professional cyclists exercised longer (i.e., 17.5 ± 1.1 vs 12.0 ± 0.9 min for controls; P < 0.001). All other physiological characteristics (V̇O2max, HRmax, and the first and second ventilatory thresholds) measured in both groups are summarized in Table 1. As expected, V̇O2max was significantly greater in cyclists, and ventilatory thresholds were both shifted toward higher values of power (Table 1).
All correlation coefficients were higher than 0.9 for both PCr and pH regressions. Extrapolated end-of-exercise values and values measured at the onset of the recovery period provided similar results for both PCr and pH. Absolute and relative extrapolated [PCr] were significantly higher (P < 0.001) in professional road cyclists at the end of the exercise (Table 3) as compared with controls. Absolute and relative [PCr] values extrapolated at end of the exercise period were significantly higher (P < 0.001) in professional road cyclists (Table 3) as compared with controls. Similarly, absolute and relative [PCr] values measured at the onset of the recovery period (i.e., at the beginning of the 31P-MRS measurements, 44 s after the end of exercise, were also significantly higher in cyclists (P < 0.001). The average PCr time-dependent changes in both groups are superimposed in Fig. 2, and illustrate that PCr concentrations measured throughout the remaining recovery time were similar in both groups.
Time-dependent changes in pH are displayed in Fig. 3, and illustrate that the exhaustive exercise was coupled to a drastic intracellular acidosis (Table 4), which was surprisingly similar in both groups. However, differences were measured throughout the recovery period (Fig. 3). Proton efflux, illustrating pH recovery rate, was significantly faster (P < 0.01) in professional road cyclists (32.8 ± 18.9 mM·min−1) as compared with controls (10.3 ± 6.7 mM·min−1). This faster recovery accounted for the significantly (P < 0.001) higher (i.e., more alkaline) values of pH measured at end of the recovery period in professional road cyclists as compared with controls (7.01 ± 0.01 vs 6.91 ± 0.04; P < 0.001) (Table 4).
In the present study, we reported for the first time intracellular pH and PCr changes in a group of professional cyclists (restricted to approximately 200 members all over the world) performing a specific exercise until exhaustion. Surprisingly, pH changes were similar in both groups at end of exercise whereas kinetics of pH recovery provided the clearest indication of the metabolic adaptation linked to specific cycling training.
From a systemic point of view, the larger aerobic aptitude of professional road cyclists was clearly illustrated by their tremendous aerobic capacity (V̇O2max = 74.6 ± 5.1 mL·min−1·kg−1), by high ventilatory thresholds (i.e., VT1 and VT2), and by the maximum tolerated power, which was 1.5 times higher compared with sport sciences students. Despite a great controversy concerning the protocols that can be used to determine all these parameters, our values are in accordance with values generally reported for such a population (20). As suggested by several authors (20,35), these adaptations could be due to the high intensity training of the professional road cyclists (8% of the total training/competition volume performed above VT2, or about 90% of V̇O2max).
The pH values reported in the present study are in agreement with values reported from biopsy studies and different from those reported in 31P-MRS investigations. More likely, this difference results from differences in exercise type and intensity. In the present study, intracellular acidosis was large and not significantly different in both groups (6.34 ± 0.05 and 6.43 ± 0.16 for untrained subjects and professional cyclists, respectively). As a matter of comparison, a 6.62–6.91 end-of-exercise acidosis has been measured in quadriceps muscle during alternate leg flexions (25,26), whereas measurements in calf muscle during plantar flexions were a bit lower with a large range (6.38–6.91) (6,31,34). More recently, very limited pH changes (6.78–6.93) were measured at the end of the exercise in quadriceps during two-leg cycling in a supine position (14). These high pH values clearly illustrate the limitations of exercises performed inside superconducting magnets, which are very different from specific exercise (i.e., performed in ecological situation). For instance, the absolute maximal power reported in this recent study (166 W) and the corresponding maximal heart rate (150 bpm) further indicate the submaximal nature of the corresponding exercise (14). As a matter of comparison, the maximum tolerated power by our control group averaged 334 W and the maximum heart rate was 189 ± 5 bpm. On the contrary, our pH values (acidosis ranging from 0.56 to 0.71 pH unit) were in close agreement with values reported from muscle biopsy studies during cycling exercise (0.48 and 0.52 pH unit) (11,27,28), whereas the maximum tolerated power was lower (273 vs 308–516 W in the present study).
Biochemical adaptations to aerobic exercise have been characterized in professional road cyclists by using metabolites measured in venous blood samples, and more particularly acidosis and lactate accumulation. Decreased blood lactate concentration has usually been reported as a result of high aerobic aptitude mediated by high-intensity endurance training, thereby illustrating either a lesser reliance on anaerobic metabolism and/or a faster lactate removal and metabolization after high-intensity exercise. However, previous studies have clearly indicated the limitations of such measurements (11). Hermansen and Osnes (11) reported that incremental cycling exercise performed until exhaustion was associated with a progressive muscle acidification of at least 0.5 pH unit (end-of-exercise pH ranging from 6.3 to 6.6), whereas blood pH changes were limited to 0.2 pH units, further indicating that blood measurements should be carefully interpreted. Moreover, Iwanaga and coworkers (13) showed that intracellular pH and blood lactate concentration changes were not correlated during a progressive arm exercise (13).
An additional indication of a metabolic effect of the specific cycling training was given by the difference in proton efflux (faster in cyclists), calculated taking into account both pH changes and the proton load linked to PCr resynthesis. Time-dependent pH changes are modulated by a series of processes acting either positively or negatively on pH values, which have to be taken into account to properly elicit pH recovery kinetics. Foremost, PCr resynthesis through the creatine kinase equilibrium generates proton, a phenomenon that should induce an additional pH decrease (17). At the same time, mechanisms of proton transport such as Na+/H+ antiporters and lactate efflux (15) are activated so that pH recovers back to its basal value despite the proton load from PCr resynthesis. This faster pH recovery, illustrated by significant higher pH values in professional road cyclists at end of the recovery period could be accounted for by several phenomena. Comparative analyses of lactate concentration in muscle and blood have previously suggested that the decrease of muscle lactate was mainly related to lactate transport and that possible local reutilization was unlikely (28). Lactate transport into the bloodstream and the consequent intramuscular alkalosis is related to several active mechanisms involving blood flow and lactate–proton transporters (15). Changes in muscle blood flow could explain metabolic differences between trained and untrained subjects, and such changes could be mediated by increase in muscle capillary density as previously suggested (29). Apart from these anatomical changes, increased oxygen supply has been related to improved kinetics of PCr recovery and thus exclusively in trained subjects (10). The distribution of lactate–proton transporters in skeletal muscle is fiber type–dependent, with a higher capacity in slow-twitch fibers compared with fast-twitch fibers (15), and it has been shown that the lactate–proton transporter can undergo adaptive changes (15). In this line, a recent study showed that well-trained subjects (i.e., middle- and long-distance runners) present significantly higher MCT1 (monocarboxylate transporter) expression compared with less-trained subjects (32). Moreover, this skeletal muscle MCT1 expression is correlated with the velocity constant of net blood lactate removal after a supramaximal exercise (32). The capacity of this system was enhanced after intense training or chronic stimulation, and reduced after denervation (15), indicating in agreement with Juel’s (16) conclusions that the lactate–proton transport system is of major importance for pH regulation in skeletal muscle, and that changes in the amount of transporters are one of the many adaptations to training. However, Pilegaard et al. (23) suggested that a high volume of endurance training is not sufficient to improve the ability to transport lactate, and that regular high-intensity sessions must be included. As previously mentioned in the “Methods,” professional road cyclists performed about 8% of their training/competition time at high intensity (>90% V̇O2max), which could explain their capacity of pH recovery.
As previously described by Fernandez-Garcia et al. (9), in professional road cyclists participating at the Tour de France, the time spent at VT2 is roughly 20 min·d−1 regardless of the type of stage. Based on these results, it is logical to infer that performance in professional road cyclists is highly dependent on the removal of lactate and protons from active skeletal muscles to maintain force and prevent fatigue induced by successive high-intensity cycling bouts. For example, this recovery aptitude could permit to make a break off the front when others cyclists are recovering from the previous acceleration.
The analysis of the recovery period after exercise provides key information related to aerobic energy provision. It has been shown that PCr recovery kinetics is highly coupled to oxygen supply and utilization. PCr resynthesis process simply involves the rephosphorylation of creatine by aerobically produced ATP. Interestingly, it has been reported that PCr recovery kinetics could be accelerated with increased oxygen supply (10) and slowed in mitochondrial disorders, likely in relation with a poor oxygen utilization (1). Several authors (18,19,21,22,36) have shown that individuals with elevated aerobic aptitudes exhibited a faster PCr resynthesis rate in muscles not particularly involved in the exercise training process. In the present study, we failed to observe a faster PCr recovery kinetics in trained subjects. This could be due to the very fast PCr recovery kinetics as compared with the first time point measured about 40 s after the end of exercise. In agreement with this hypothesis, analyses of biopsy samples during the postexercise recovery period of exhausting exercise (mean power output = 270 W) have shown that PCr recovery was almost completed during the first minute of recovery (28). Another possibility would be that PCr recovery kinetics are indeed not different between these two populations of trained subjects. It is noteworthy that extrapolated end-of-exercise PCr consumption was smaller in cyclists, likely illustrating a better energy-buffering capacity in cyclists.
At rest, the 5.5% reduction in [PCr] and 21.2% reduction in PCr/Pi ratio measured in professional cyclists were both nonsignificantly different as compared with control subjects. This would suggest, on the contrary to what has been concluded so far, that exercise training is not linked to changes in high-energy phosphate metabolite concentrations resulting from fiber-type changes. It has been reported that mammalian skeletal muscle fibers can be distinguished by contents of phosphocreatine, ATP, and Pi in both humans and animals (3,19,22). Accordingly, a significant reduction of PCr/Pi ratio has been reported in long-distance runners (3) and cross-country skiers (19) as compared with untrained subjects or sprinters (3) and downhill skiers (19), likely illustrating fiber-type changes resulting from training. The disagreement between the present results and previous measurements could be linked to the fact that measurements were not performed in the same muscles. We performed measurements in thigh muscles (i.e., vastus lateralis, rectus femoris, vastus medialis), which are mostly involved in cycling training, whereas other measurements have been done either in calf (i.e., soleus, gastrocnemius) or wrist flexor muscles (i.e., flexor digitorum superficialis), which are not the main muscles involved in training of skiers, marathon runners, or rowers. Another issue could be linked to physical fitness of our control group. In the present study, control subjects were enrolled in a regular physical activity (about 6 h·wk−1) as illustrated by their fitness level (MPT = 334 W, which was larger than what we reported in young sedentary subjects, i.e., 239 W). In contrast, the increased PDE concentration, at rest, in professional road cyclists would be in keeping with a higher percentage of highly oxidative Type I fibers (4) as previously concluded from biopsy studies in trained cyclists (7,12). The PDE resonance in humans originates basically from glycerophosphorylcholine and glycerophosphorylethanolamine. PDE generation has been reported during the stimulation-mediated fast to slow muscle transformation in the rabbit (4), and a higher PDE concentration has already been reported in long-distance runners as compared with sprinters (3). This is an interesting issue given that numerous studies showed that fiber-type composition could be linked to the performance and reflect the adaptive response to physical training (30). A larger PDE signal has been reported as a sign of a larger relative content of Type I fibers. In that respect and considering the different metabolic capacities of Type I and II fibers, and more particularly the higher oxidative capacity, one could suggest that this larger relative contribution of Type I fibers could account for the faster PCr and pH recovery recorded in professional cyclists.
In the present study, we reported for the first time that in real sport situations, intracellular acidosis is large at end of exhausting exercise and not significantly different between two groups of subjects with different aerobic capacities. An additional indication of the superior aerobic capacity is linked to a reduced PCr consumption and a faster pH recovery in professional cyclists. Finally, a higher resting concentration of PDE was measured in cyclists, suggesting changes in fiber types in relation with the improvement of aerobic capacity.
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