Medicine & Science in Sports & Exercise:
Basic Sciences: Original Investigations
O2 Arterial Desaturation in Endurance Athletes Increases Muscle Deoxygenation
LEGRAND, RENAUD1,2; AHMAIDI, SAÏD2; MOALLA, WASSIM2; CHOCQUET, DOMINIQUE2; MARLES, ALEXANDRE1; PRIEUR, FABRICE1; MUCCI, PATRICK1
1Laboratory of Multidisciplinary Analysis of Physical Activity, Faculty of Sport Sciences, University of Artois, Liévin, FRANCE; and 2Laboratory EA 3300–Physical Activity and Motor Behaviour: Adaptation, Readaptation, Faculty of Sport Sciences, University of Picardie Jules Vernes, Amiens, FRANCE
Address for correspondence: Patrick Mucci, UFR STAPS de Liévin, Laboratoire d’Analyse Multidisciplinaire des Pratiques Sportives, Chemin du marquage, 62800 Liévin, FRANCE; E-mail: firstname.lastname@example.org.
Submitted for publication May 2004.
Accepted for publication January 2005.
We are grateful to the member of the “Centre de réadaptation cardiaque du Centre Hospitalier Universitaire de Corbie” team for their medical and technical assistance.
Purpose: The aim of this study was to compare the muscle deoxygenation measured by near infrared spectroscopy in endurance athletes who presented or not with exercise-induced hypoxemia (EIH) during a maximal incremental test in normoxic conditions.
Methods: Nineteen male endurance sportsmen performed an incremental test on a cycle ergometer to determine maximal oxygen consumption (V̇O2max) and the corresponding power output (Pmax). Arterial O2 saturation (SaO2) was measured noninvasively with a pulse oxymeter at the earlobe to detect EIH, which was defined as a drop in SaO2 > 4% between rest and the end of the exercise. Muscle deoxygenation of the right vastus lateralis was monitored by near infrared spectroscopy and was expressed in percentage according to the ischemia–hyperemia scale.
Results: Ten athletes exhibited arterial hypoxemia (EIH group) and the nine others were nonhypoxemic (NEIH group). Training volume, competition level, V̇O2max, Pmax, and lactate concentration were similar in the two groups. Nevertheless, muscle deoxygenation at the end of the exercise was significantly greater in the EIH group (P < 0.05).
Conclusion: Greater muscle deoxygenation at maximal exercise in hypoxemic athletes seems to be due, at least in part, to reduced oxygen delivery—that is, exercise-induced hypoxemia—to working muscle added to the metabolic demand. In addition, our finding is also consistent with the hypothesis of greater muscle oxygen extraction in order to counteract reduced O2 availability.
During exercise, most healthy individuals are able to maintain arterial oxygenation adequately to meet the increased metabolic demands at sea level. However, it is well known that some endurance athletes (about 50%) exhibit arterial oxygen desaturation, that is, arterial hypoxemia during incremental exercise (9,30).
The detrimental effect of exercise-induced hypoxemia (EIH) on maximal oxygen consumption (V̇O2max) has been demonstrated in studies by adding sufficient O2 to the inspired air to prevent the hypoxemia (15,29). Powers et al. (29) suggested that EIH limits V̇O2max in endurance athletes who exhibit this phenomenon. They reported that V̇O2max decreases approximately by 1% for each 1% decrease of oxygen arterial saturation (SaO2) (29). Recently, Harms et al. (15) reported that preventing arterial O2 desaturation during exercise via a mild hyperoxic inhalation leads to significantly higher V̇O2max in EIH endurance-trained women than nonhypoxemic women. Moreover, Koskolou and McKenzie (19), who induced arterial hypoxemia by reducing the inspired O2 fraction during exercise, showed that total work output is significantly impaired when SaO2 is below 87%. According to the literature, the reduction of both V̇O2max and aerobic performance in hypoxemic athletes is likely due to limited O2 delivery to working locomotor muscles (10,11,19).
However, studies that compared hypoxemic and nonhypoxemic endurance-trained athletes with similar competition levels generally reported equivalent values of V̇O2max and maximal power output (2,7,15). This observation seems to be inconsistent with the reduced muscle O2 delivery hypothesis. It might suggest the presence of mechanisms compensating for the reduced oxygen availability in the working muscle. Hence, the effect of EIH on muscle oxygenation remains unclear and has not yet been specifically investigated by comparison between hypoxemic and nonhypoxemic athletes.
The aim of this work was to investigate the impact of exercise-induced arterial O2 desaturation on muscle deoxygenation. We compared muscle oxygenation monitored by near infrared spectroscopy (NIRS) between hypoxemic and nonhypoxemic endurance athletes performing incremental exercises.
Nineteen endurance sportsmen volunteered to participate in this study: 15 runners, 3 triathletes, and 1 cyclist. All practiced competitive endurance sports at the regional or national level and had trained 9.8 ± 3.4 h·wk−1 for 7.8 ± 3.6 yr. They also participated in competition events 2–4 h·wk−1 during their competitive seasons, which lasted for 4 months a year. The experiment was approved by the local ethics committee in accordance with the ethical standards of the Helsinki declaration of 1975. Written informed consent was obtained from all subjects before participation, and they were allowed to withdraw from the study without any restrictions. Before entering the study, the cardiovascular and pulmonary health status of each subject was evaluated. None of the subjects reported respiratory or cardiac disease, or were known to be suffering from any chronic disease. None were taking medication. All were nonsmokers and presented normal hemoglobin concentration and spirometric values.
All subjects performed a maximal incremental test on a cycle ergometer (Ergometrics 900, Ergoline, Bitz, Germany). After a 5-min resting period, the exercise began with a 3-min, 60-W warm-up at a 60-rpm pedaling frequency that was maintained until the end of the test. The workload was then increased by 30-W increments every minute until exhaustion. The exercise was considered to be maximal when three of the following criteria were obtained: change in V̇O2 < 100 mL·min−1 while increasing workload (leveling off criterion), respiratory exchange ratio (RER) > 1.1, heart rate (HR) within 10% of maximal predicted value, and inability of the subjects to maintain the pedaling frequency despite maximum effort and verbal encouragement.
Pulmonary gas exchanges and cardiac measures.
ECG and HR were continuously recorded during the exercise with a 12-lead ECG (Formula Biomedica, Esaote, Florence, Italy). Minute ventilation (V̇E), oxygen uptake (V̇O2), and CO2 output (V̇CO2) were measured continuously before and during the test with an automatic breath-by-breath metabolic system (CPX-D, Medical Graphics, St. Paul, MN), and averaged for the last 30 s of each stage. The system was calibrated before each test.
Hemoglobin concentration at rest and blood lactate concentration at the end of the exercise [La] were established with a spectrophotometric method (Miniphotometer LP-20, Dr. Lange, Berlin, Germany). For each measurement, 10 μL of blood were collected from the fingertip with a capillary tube and were analyzed immediately with the spectrophotometer. The apparatus was calibrated with solutions of known concentration before each measurement.
Oxygen arterial saturation and exercise-induced hypoxemia determination.
Arterial oxygen saturation (SaO2) was continuously estimated at rest and during exercise via a pulse oximeter (Biox 3800, Datex Ohmeda, Louisville, KY) placed and maintained on the earlobe. The apparatus was automatically calibrated before each experiment. Use of pulse oximeter for estimating SaO2 during exercise has been validated (24,28). The pulse oximeter clearly provides qualitative information concerning the presence or absence of hypoxemia (1). In addition, we confirmed the validity of our particular pulse oximeter by comparing the occurrence of hypoxemia estimated from our pulse oximeter data to hypoxemia demonstrated by blood gas measurements (unpublished data). To avoid artifacts in recording signals, the ear was warmed with a vasodilator ointment 10–15 min before starting measurements. The probe was held in place with a plastic earpiece and adhesive tape assuring permanent contact between the probe and the earlobe during all head movements. The pulse oximeter used for this experiment also evaluates wave-form signal quality pulse by pulse, allowing us to exclude inadequate signals associated with possible blood-flow or head-movement artifacts. Before exercise, SaO2 was recorded and averaged over 3 min, whereas during exercise, SaO2 was recorded during the last 10 s of each minute. These measurements allowed us to detect EIH and to discriminate between athletes who exhibited EIH (EIH group) and those who did not (NEIH group). EIH was defined as a progressive and persistent decrease in SaO2 during exercise and a drop (ΔSaO2) between rest (SaO2 rest) and the end of the exercise (SaO2end) of more than 4% (26,30). This definition takes into account the cumulative effects of temperature, metabolic acidosis, and errors in the pulse oximeter measurements that, together, are insufficient to induce such a drop in SaO2 during incremental exercise (1,30).
Evaluation of muscle oxygenation.
Oxygenation of the right vastus lateralis was estimated during the incremental test with a near infrared spectrometer (NIRS) (RunMan Unit, NIM, Philadelphia, PA). The principles of the measurement have been fully described (3,6). Briefly, NIRS is a noninvasive method based on the principle of differential absorption properties of oxygenated and deoxygenated forms of hemoglobin and myoglobin at wavelengths between 760 and 850 nm. Thus, subtracting these two absorbencies (760–850 nm) gives the change in the HbO2/Hb ratio, that is, the change in oxygenation level in the small blood vessels (capillaries and venules). Furthermore, the sum of these two wavelengths (760 + 850 nm) reflects the change in blood volume (BV) that is attributed to change in total hemoglobin. The validity of the NIRS method in human during exercise has been well established (22). The superficial probe of the NIRS was placed on the right vastus lateralis, approximately 12–14 cm from the knee, along the vertical axis of the thigh, as described in the literature (3). A piece of plastic wrap was used to prevent the probe from being fogged by sweat from the skin during exercise. At the end of the exercise, a thigh cuff was inflated above the probe. The minimal signal during thigh-cuff ischemia was considered as the minimal oxygenation level and was assigned the value of 0%. After releasing the cuff, the maximal value recorded during the reactive hyperemia was assigned the value of 100% oxygenation (22). During this procedure, the signal was continuously checked to ensure that a plateau of minimal and maximal oxygenation occurred, indicating that 0 and 100% values were reached. The NIRS signal was collected at rest and during exercise across a 1-s period with NIRCOM software supplied with the NIRS. Averaged values were kept over the last 15 s of the warm-up and over the last 15 s of each stage, and were expressed in percent according to the relative ischemia–hyperemia scale. Before each test, the apparatus was calibrated according to procedures described by the manufacturer. In accordance with Grassi et al. (14), variations in the NIRS signal (muscle oxygenation and blood volume) were expressed according to the values of the start of exercise (Oxystart and BVstart) instead of resting values because studies have shown that skin blood flow can influence the NIRS signal at rest (21) but can be neglected during exercise (22,23). Figure 1A (muscle deoxygenation) and Figure 1B (blood volume) illustrate an example of the NIRS signal recorded during the incremental test. We studied the maximum muscle deoxygenation during exercise (Deoxmax) and the muscle deoxygenation at the end of the exercise (Deoxend). Deoxmax was the difference in muscle oxygenation between the starting value (Oxystart) and the minimum value reached during the exercise (Oxymin), that is, Deoxmax = Oxystart − Oxymin. Deoxend was the difference between Oxystart and the value at the end of the exercise (Oxyend), that is, Deoxend = Oxystart − Oxyend. Concerning blood volume, we studied the changes in blood volume between the starting value (BVstart) and the blood volume corresponding to Oxymin (BVmin) called ΔBVmax, that is, ΔBVmax = BVstart − BVmin. ΔBVend was the amplitude between BVstart and the blood volume at the end of the exercise (BVend), that is, ΔBVend = BVstart − BVend.
Values are expressed as mean ± standard deviation (SD). Student’s t-test was used to compare values between the two groups. Mann–Whitney’s rank sum test was used when the sample normality test failed. Statistical significance was defined at the P < 0.05 level.
Ten of the nineteen subjects included in this study showed a drop of more than 4% in SaO2 during the incremental test and were included in the EIH group. The nine other athletes were included in the NEIH group (Fig. 2). According to Dempsey and Wagner’s classification (11), five of the EIH subjects presented moderate hypoxemia (93% > SaO2 > 91%), and the five others showed severe hypoxemia (SaO2 < 91%).
Anthropometric values (Table 1).
The EIH and NEIH group presented similar anthropometric values, hemoglobin concentration, and training volume.
Maximal cardiorespiratory and metabolic data.
The maximal values obtained during the incremental exercise are presented in Table 2. V̇O2max, Pmax, RER, maximal HR, and [La] were similar between the two groups. As shown in Figure 2, the only difference in maximal values between the two groups was oxygen arterial saturation at the end of exercise, which was significantly lower in EIH groups (P < 0.001), and the drop in SaO2 between rest and maximal exercise, which was greater in this group (ΔSaO2 = 6.2 ± 0.8% in HIE vs 2.4 ± 1.0% in NHIE, P < 0.05).
Muscle oxygenation and blood volume.
The starting value of muscle oxygenation (Oxystart) was similar in the two groups (49.72 ± 21.95% in EIH vs 44.83 ± 26.22% in NEIH, P = 0.66). Maximal deoxygenation appeared at 91.8 ± 10.1% V̇O2max, in a range between 89.6 ± 12.0% V̇O2max in NEIH and at 93.8 ± 10.1% V̇O2max in the EIH group. As shown in Figure 3A, the Deoxmax values were not different between the hypoxemic and the nonhypoxemic athletes. However, at the end of the exercise, the hypoxemic athletes showed a greater deoxygenation (Deoxend) than the nonhypoxemic athletes (P < 0.05) (Fig. 3A). The starting values of blood volumes were not different between EIH and NEIH athletes (29.53 ± 26.45% in HIE vs 18.37 ± 24.54% in NEIH, P = 0.11). The change in BV corresponding to the maximum muscle deoxygenation (ΔBVmax) and the change in BV at the end of the exercise (ΔBVend) seemed to be less important in the hypoxemic group, but this difference was not statically significant (P = 0.15 and P = 0.48, respectively) (Fig. 3B). Finally, no significant correlation was found between SaO2 and muscle oxygenation parameters.
The main finding of this study was a greater muscle deoxygenation at maximal workload (Deoxend) monitored by NIRS in hypoxemic athletes compared with nonhypoxemic athletes performing a maximal incremental exercise. This result was associated with similar values of maximal oxygen uptake, maximal power output, and training volume between these endurance athlete groups.
As described in the Methods section, according to the manufacturer and several studies (3,4,8,22,23), all precautions were taken during the NIRS measurements to obtain a consistent signal. Furthermore, the NIRS signal is known to be influenced by the subcutaneous fat (17), but the subjects who participated in this study were well trained and had a low body-fat percentage.
Muscle deoxygenation in athletes.
Several studies that have described the muscle oxygenation trends during incremental exercise on a cycle ergometer in healthy subjects have reported that muscle deoxygenation is related to exercise intensity (phase 2) and tends to level off (phase 3) near maximal exercise (3,5,14). This latest phase suggests that muscles have reached their maximal oxygen extraction or that the O2 delivery cannot be increased. In this phase, we found that 10 subjects reached maximal muscle deoxygenation before the end of the exercise. To our knowledge, the observation of two tendencies in oxygenation kinetics in the third phase has not yet been reported. This could be explained by the fact that muscle oxygenation kinetics during incremental exercise on a cycle ergometer has not been yet studied in endurance-trained athletes. Indeed, our subjects were endurance trained and showed higher aerobic performance than in previous studies (V̇O2max = 60.7 ± 4.9 (NEIH) and 62.6 ± 9.2 (EIH) versus 44 ± 10 (3); 47.0 ± 9.0 (5) and 51.0 ± 4.2 mL·min−1·kg−1 (14)). In other respects, although we are the first to our knowledge to report the achievement of Deoxmax before the end of the exercise, one can note in the study of Belardinelli et al. (3) (on Fig. 4: example of the NIRS signal during a ramp test in one subject) that maximum muscle deoxygenation occurs before the end of the exercise in this subject. The achievement of Deoxmax before the end of the exercise in our 10 athletes could be explained by the hyperpnea occurring at heavy exercise that is known to increase the arterial oxygenation level in some endurance-trained athletes (13). Consequently, this could lead to slightly reduce muscle deoxygenation at the end of the exercise in comparison with submaximal workload in these subjects.
Muscle deoxygenation and EIH.
The maximum muscle deoxygenation during the exercise was not different between the two groups. Nevertheless, at the end of the exercise, the muscle deoxygenation was significantly greater in the hypoxemic group. The lack of difference in Deoxmax could be due to the fact that, as discussed above, Deoxmax appeared at submaximal workload, that is, at different metabolic levels depending on subjects (80.2–100% V̇O2max in EIH and 69.0–100% V̇O2max in NEIH). In addition, at submaximal levels, SaO2 was not always reduced enough in EIH to lead to increased muscle deoxygenation, and for the most part, EIH subjects showed their maximal muscle deoxygenation at the end of the exercise versus a third in NEIH. Otherwise, in our point of view, Deoxend is the most interesting result because all subjects were most likely at the same metabolic level (maximal workload), and EIH is defined as a drop in SaO2 between rest and the end of the exercise (see Methods) (26,30).
Several hypotheses could be put forward to explain the difference in deoxygenation. The first hypothesis is that the greater muscle deoxygenation in hypoxemic sportsmen could be due to the greater arterial O2 desaturation in EIH compared with NEIH athletes. Indeed, although muscle deoxygenation in nonhypoxemic athletes is likely due essentially to muscle O2 extraction, the greater muscle deoxygenation in hypoxemic subjects could result from the combined effect of muscle O2 extraction and the reduced level of arterial oxygenation in EIH. This hypothesis is in agreement with the data reported by Costes et al. (8), who compared muscle deoxygenation measured by NIRS in normoxic and hypoxic conditions during a constant-workload exercise. These authors observed a greater muscle deoxygenation at the end of the exercise in the hypoxic condition. They suggested that during exercise in normoxia, muscle deoxygenation is due to the exercise-induced metabolic demand, whereas during exercise in hypoxia, the reduced arterial oxygenation plus metabolic demand induces a greater decrease in muscle oxygen content. Consequently, both factors would explain the greater muscle deoxygenation in artificial hypoxia. Nevertheless, if the fall in SaO2 were the only explanation for the greater muscle deoxygenation in EIH athletes, and if we consider that EIH limits V̇O2max (15,29), V̇O2max and maximal power output would be lower than in the nonhypoxemic athletes. Indeed, in this first hypothesis, the reduced O2 content associated with normal O2 extraction would have to lead to reduced V̇O2max in EIH subjects, which was not the case in our study. Therefore, these observations suggest that other mechanisms such as metabolic or muscle adaptations that compensate for the reduced oxygen delivery to working muscle could be implicated.
Adaptations to explain the greater muscle deoxygenation in hypoxemic athletes.
Consequently, a second hypothesis could be an implication of metabolic acidosis. Indeed, in common individuals, muscle deoxygenation at heavy exercise is known to be increased by a local acidosis (34). The greater muscle deoxygenation in hypoxemic athletes could result from more pronounced acidosis, which leads to a reduced affinity of hemoglobin for oxygen at the end of exercise in the EIH than in the NEIH group. This hypothesis is, however, not supported by the blood-lactate concentration measurements taken at the end of exercise in our subjects. Indeed, values were not significantly different between the two groups, even if mean blood lactate concentrations were ∼ 7% higher in EIH. One hypothesis could be that the number of subjects was too small to detect significant differences. However, Nielsen et al. (27) reported that muscle oxygenation is not affected by infusion of sodium bicarbonate, which enlarges blood-buffering capacity, in EIH subjects. In addition, other studies that compared blood lactate (2,16,32) or pH (16,33) between hypoxemic and nonhypoxemic athletes did not report any differences.
A third potential hypothesis could be muscle adaptations in response to hypoxemic stimuli. Indeed, the hypoxemic athletes who participated in this study trained about 10 h·wk−1 in addition to time spent in competition. All of them used the high-intensity interval training method. The aim of this method is to exercise at an intensity approaching V̇O2max (20). It can therefore be assumed that during their training sessions and competitive events, these athletes exercised at working levels corresponding to the appearance of EIH. Thus, this means that they were frequently exercising into mild hypoxic conditions. To our knowledge, muscle adaptations in hypoxemic athletes in normoxic conditions have not been reported to date. There are some data concerning the effects of training under hypoxic conditions on the muscle function (12,18). In a recent study, Hoppeler and Vogt (18) studied subjects who trained under normoxic and acute hypoxic conditions. Their analysis of muscle biopsies after the training adaptations suggests that high-intensity training in hypoxia leads to adaptations that compensate for the reduced availability of oxygen during training. These adaptations include enhanced capillarity, a higher myoglobin concentration, higher mitochondrial density, and upregulated oxidative pathways, which result in more efficient use of oxygen. One possibility is that such adaptations could occur in athletes with EIH.
Attainment of similar values of V̇O2max in the EIH group, despite the reduced arterial oxygenation, may be compensated by an increase in blood volume in the working muscle. To compensate for the reduced SaO2, the total hemoglobin may be increased by enhanced perfusion. Studies about high-intensity training to acute hypoxia have revealed higher levels of vascular endothelial growth factor (VEGF) mRNA, which leads to increased capillarity density (18). Thus, an increase in blood volume would increase both total Hb and HbO2 without any change in the HbO2/Hbtotal ratio. That is why we estimated the blood volume values with NIRS technology. The change in blood volume during exercise in the EIH group seemed to be weaker than in the NEIH group, but this difference was not statistically significant, probably because of the high standard deviation due to the interindividual variability observed with NIRS (8). Thus, our data do not confirm the hypothesis of greater blood volume compensating for reduced SaO2 in hypoxemic athletes. Nevertheless, it would be interesting to obtain complementary data on blood flow using more efficient methods (e.g., Doppler).
The remaining muscle adaptations that could occur in response to EIH stimuli could involve enhanced O2 extraction associated with better oxidative capacity within the working muscle. First, as reported in studies about training in hypoxia, a higher concentration of myoglobin can improve the capacity for storing and transporting O2 within muscle cells (18). Although myoglobin seems to contribute to only a small part of the NIRS signal, the variation in absorption from Mb and Hb cannot be distinguished (23). Secondly, the oxidative capacity could be improved by an increased mitochondrial density (18). Oxygen would be then used more efficiently (18). This greater oxidative capacity hypothesis is in agreement with 1) the achievement of the same V̇O2max in EIH compared with NEIH in spite of reduced O2 delivery in EIH, 2) the greater muscle deoxygenation in EIH at maximal exercise in our study, and 3) the greater improvement of V̇O2max with mild hyperoxia reported in some studies (15,29). Therefore, further investigations (e.g., recovery kinetics of the NIRS signal (25) and muscle biopsies) are needed to study cellular adaptations in hypoxemic athletes and to confirm or reject this hypothesis.
Several other points are also noteworthy: 1) the chronic nature of EIH during the training schedule of athletes remains to be established, and 2) the SaO2 values (91.0 ± 1.2%) measured in the EIH group in this study were greater than those obtained in hypoxic conditions by Hoppeler and Vogt (18) (SaO2 < 77%, corresponding to ∼3850 m), so peripheral effects in response to EIH stimuli could be less significant. Nevertheless, the fall in SaO2 observed in our hypoxemic athletes pedaling a cycle ergometer might be less than that occurring during their regular training sessions and competition events, generally running events. Indeed, in the hypoxemic group, only one subject was a cycle specialist. The others one were triathletes and runners, and it has been reported that arterial hypoxemia is greater during running than cycling (31).
In summary, it appears that EIH in normoxic conditions in endurance athletes is associated with a high level of muscle deoxygenation estimated with NIRS technology at maximal exercise. This greater muscle deoxygenation in hypoxemic than in nonhypoxemic athletes at the end of the exercise could be explained, at least in part, by reduced arterial oxygenation combined with increased metabolic demand. However, the finding of high deoxygenation levels associated with similar V̇O2max and maximal power output in hypoxemic subjects compared with nonhypoxemic is also in agreement with the hypothesis of muscle adaptations compensating for reduced O2 delivery. This hypothesis opens new perspectives concerning cellular alterations in EIH.
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EXERCICE-INDUCED HYPOXEMIA; HEMOGLOBIN SATURATION; AEROBIC PERFORMANCE; ENDURANCE TRAINING; MUSCLE OXYGENATION
©2005The American College of Sports Medicine
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