- Top of page
For more than 60 years, muscle mechanical efficiency has been thought to remain unchanged with acclimatization to high altitude. However, recent work has suggested that muscle mechanical efficiency may in fact be improved upon return from prolonged exposure to high altitude. The purpose of the present work is to resolve this apparent conflict in the literature. In a collaboration between four research centers, we have included data from independent high-altitude studies performed at varying altitudes and including a total of 153 subjects ranging from sea-level (SL) residents to high-altitude natives, and from sedentary to world-class athletes. In study A (n=109), living for 20–22 h/day at 2500 m combined with training between 1250 and 2800 m caused no differences in running economy at fixed speeds despite low typical error measurements. In study B, SL residents (n=8) sojourning for 8 weeks at 4100 m and residents native to this altitude (n=7) performed cycle ergometer exercise in ambient air and in acute normoxia. Muscle oxygen uptake and mechanical efficiency were unchanged between SL and acclimatization and between the two groups. In study C (n=20), during 21 days of exposure to 4300 m altitude, no changes in systemic or leg VO2 were found during cycle ergometer exercise. However, at the substantially higher altitude of 5260 m decreases in submaximal VO2 were found in nine subjects with acute hypoxic exposure, as well as after 9 weeks of acclimatization. As VO2 was already reduced in acute hypoxia this suggests, at least in this condition, that the reduction is not related to anatomical or physiological adaptations to high altitude but to oxygen lack because of severe hypoxia altering substrate utilization. In conclusion, results from several, independent investigations indicate that exercise economy remains unchanged after acclimatization to high altitude.
The first systematic measurement of whole-body oxygen consumption during cycle ergometer exercise in high altitude dates back to the International Expedition to Chile in 1935 by Christensen (1937). In this classic study, and several subsequent studies, whole-body oxygen consumption at a given work rate was unchanged at altitude (Pugh et al., 1964; Consolazio et al., 1966; Klausen et al., 1970; Maher et al., 1974; West et al., 1983; Bender et al., 1988; Svedenhag et al., 1991; Wolfel et al., 1991; Grassi et al., 1996; Young et al., 1996; Lundby & van Hall, 2002; Calbet et al., 2003) or slightly increased (Roberts et al., 1996) at high altitude compared with sea level (SL). In support of this observation, during acute hypoxic exposure no alterations in submaximal VO2 have been reported (Dill et al., 1966; Cerretelli et al., 1967; Hughes et al., 1968; Hogan et al., 1983). Also, studies applying intermittent hypoxic exposure report unchanged SL submaximal VO2s after hypoxia (Telford et al., 1996; Levine & Stray-Gundersen, 1997; Rodriguez et al., 2000; Clark et al., 2004; Lundby et al., 2004). Recently, however, both prolonged and intermittent hypoxic exposure have been suggested to increase the mechanical efficiency of exercise when performed at SL (Green et al., 2000b; Gore et al., 2001; Katayama et al., 2003; Saunders et al., 2004). Moreover, it has also been reported that high-altitude natives have a higher mechanical efficiency compared with SL residents (Hochachka et al., 1991).
The purpose of the present study is to resolve this apparent conflict in the literature. The weaknesses of some previous studies include (1) small subject number (Green et al., 2000b; Gore et al., 2001); (2) primitive field conditions where subjects were exposed to varying altitudes for a varying amount of time (Green et al., 2000b). During climbing expeditions, stimuli such as cold, marked changes in exercise habits, reduced availability, and different types of food, all could conceivably have altered muscle structure and function under these extraordinary conditions; (3) high oxygen requirements for a given work rate observed before altitude exposure, whereas more normal values were observed after the hypoxic exposure period (Katayama et al., 2003); and (4) intralaboratory variability in outcome, i.e., with similar study designs, efficiency either remained unchanged (Telford et al., 1996; Clark et al., 2004) or was increased (Gore et al., 2001; Saunders et al., 2004) although the studies were performed by the same research group.
The aim of the present study was to test rigorously whether chronic high-altitude exposure is accompanied by changes in muscle mechanical efficiency. We have investigated the effects of prolonged hypoxic exposure in SL residents and in high-altitude natives on O2 consumption for a given work rate. Our data include leg and whole-body oxygen consumption both during hypoxia and acute normoxia at different altitudes. Furthermore, we have studied oxygen consumption during knee-extensor exercise. The data have been gathered in six high-altitude studies, listed ascending with altitude: (A) the 1994–2000 “live high–train low” studies by Levine and Stray-Gundersen; (B) the 2001 Danish El Alto expedition; (C) the 1987, 1988, and 1991 Pikes Peak expeditions; and (D) the 1998 Danish Chacaltaya expedition. Combining these studies give a total subject number of 153. Some of the data have been published previously, however, not with the emphasis as in the present context.
- Top of page
The aim of the present study was to test rigorously whether chronic high-altitude exposure is accompanied by changes in muscle mechanical efficiency. The combined data of the large number of subjects studied in different laboratories show a remarkable consistency – no change in muscle mechanical efficiency with altitude acclimatization. In the two studies showing a decrease in VO2, the muscle mechanical efficiency was similar with acute and chronic hypoxic exposure, suggesting that hypoxia altered muscle metabolic substrate utilization rather than inducing an anatomical/physiological adaptation to high altitude.
Our finding of unchanged muscle mechanical efficiency during whole-body exercise at altitudes up to 4300 m is in agreement with the literature. Since first reported during the International Expedition to Chile in 1935 by Christensen (1937), this observation has been confirmed on numerous occasions (Pugh et al., 1964; Consolazio et al., 1966; Klausen et al., 1970; Maher et al., 1974; West et al., 1983; Bender et al., 1988; Svedenhag et al., 1991; Wolfel et al., 1991; Grassi et al., 1996; Young et al., 1996; Lundby & van Hall, 2002; Calbet et al., 2003). Of note is that submaximal VO2 in these studies were all measured at altitude. In accordance, submaximal VO2 has also been reported to remain unchanged if measured at SL after altitude acclimatization (Hansen et al., 1967; Klausen et al., 1970). The present investigation reports on the effect of altitude acclimatization on submaximal VO2 measurements at SL, at altitude, and with acute induction of normoxia at altitude. In these studies, no reduction in submaximal VO2 with altitude acclimatization was found.
(1) Green et al. (2000b) showed that in five untrained mountaineers following a 21-day mountaineering expedition to Mt. Denali (6189 m), with varying altitude exposure, that whole-body VO2 during steady-state submaximal cycle ergometer exercise performed 3 days after return to SL was significantly reduced by approximately 0.2 L/min. Accordingly, mechanical efficiency increased from about 25% before the high-altitude sojourn, to values close to 30% after the expedition. This finding contradicts studies where subjects were exposed to 3800 m for 12 days (Klausen et al., 1970) or to 4300 m for 21 days (Hansen et al., 1967). In both studies, VO2 was measured after return to SL and showed no differences compared with before altitude exposure.
The observed decrease in whole-body VO2 after the climbing expedition to Mt. Denali was associated with a 13.8% downregulation in muscle Na+/K+-ATPase in a subsequent publication (Green et al., 2000a). A decrease in Na+/K+-ATPase has been hypothesized to allow a given amount of work to be performed at lower ATP costs, and hence at a lower VO2 (Hochachka et al., 1991). Accordingly, the subjects from study D had a reported higher net release of K+ during submaximal exercise after acclimatization to 5260 m. Net K+ release depends on the balance between K+ uptake and K+ release, and the observed increase in K+ could be a result of downregulated Na+/K+-ATPase (Calbet et al., 2003). However, alterations of the Na+/K+ may also be altitude dependent, and no changes were observed in any of the three Na+/K+ pump subunits in muscle biopsies obtained after 2 and 8 weeks of high-altitude exposure to 4100 m in study B (Juel et al., 2003). Another explanation for the reduced submaximal VO2 after the expedition to Denali could be related to the experimental design. Green and co-workers investigated their subjects at SL, whereas most others studied their subjects at high altitude. As the mechanical power of breathing for a given work rate is higher with hypoxic exposure (Cibella et al., 1996), differences in submaximal VO2 after acclimatization could be masked in hypoxia because of the extra energy required to move air to the lungs (Green et al., 2000b). However, as seen in Figs 2A, B and 3A, B where normoxia is induced acutely in chronic hypoxia, this does not seem to be the case. Finally, climbers on Denali are exposed to very harsh environmental conditions, and stimuli such as cold, marked changes in exercise habits, reduced availability, and different types of food could all conceivably have altered muscle structure and function under these extraordinary conditions. Extrapolation of these data to less severe high-altitude or hypoxic conditions should be carried out with caution.
In study D, we report on decreases in submaximal VO2 during cycle and one-legged kicking exercise with acute and chronic hypoxic exposure to 5260 m as compared with SL. As the alterations were already present in the acute hypoxic situation, this response does not seem to be related to physiological adaptations associated with altitude acclimatization. The point that delta VO2 decreases as the altitude is increased has been observed by Wagner et al. (1986) in the mid-1980s, reporting decreases in submaximal VO2 with increasing acute exposure to altitude as well as with increasing exercise intensity. The underlying regulating mechanism is unknown, but could be speculated to be related to increased carbohydrate utilization.
(2 and 3) Gore et al. (2001) studied the effects of spending 23 nights (9.5 h/day) at 3000 m on exercise performance at SL. In the six competitive cyclists, the investigated submaximal efficiency was improved from 18.9% to 19.7%. Considering the 3% margin of error typically associated with pulmonary gas exchange measurements, it seems unlikely that the reported 0.8% improvements in efficiency are all because of physiological changes. Another limitation in the study by Gore et al. (2001) is that the training was not supervised. Training alone might very well explain the rather small 0.8% increase in muscular efficiency (Franch et al., 1998), as we also observed in the SL training phase of the studies in group A1 (Fig. 1).
Recently, the same research group that conducted the experiments on which the Gore et al. (2001) article is based repeated the protocol except that this time training was controlled, and that the chosen exercise was running instead of cycling. Although no differences could be found in the slope between running speed and VO2 (definition of economy), VO2 was reported to be lower after the hypoxic exposure if the average VO2s for all workload were used (Saunders et al., 2004). In contrast to these reports, however, is the publication of two articles from the same laboratory using similar experimental setups that were not able to detect differences in either mechanical efficiency or VO2 (Telford et al., 1996; Clark et al., 2004). When these small, inconsistent studies are viewed in the light of more than 100 subjects in study A, where reproducible results were observed, it seems reasonable to conclude that “live high–train low” does not consistently alter mechanical efficiency or submaximal VO2. Whether different combinations of duration/intensity of hypobaric or normobaric hypoxic living plus normoxic training could contribute to the divergent results reported in the literature is unknown.
Recently, studies applying repeated and very short-duration hypoxic exposure have been performed in order to evaluate its possible athletic effects. Katayama et al. (2003) reported that exposure to 432 mmHg (equivalent to 4500 m) for 90 min/three times a week/3 weeks reduced SL submaximal VO2 during treadmill running. This is in contrast to exposure to 5500 m for the same time duration where no reductions in SL submaximal VO2 were reported during bike ergometer exercise (Rodriguez et al., 2000). Recently, Katayama et al. (2004) also reported that intermittent exposure to 12.3% O2 (about 4200 m) for 3 h daily for 14 days reduced submaximal running VO2. In contrast, our group has observed no differences in submaximal ergometer cycling VO2 after 2 h daily exposure to 4100 m for 14 consecutive days in eight subjects (Lundby et al., 2005). This difference in results could be explained by the somewhat high values for submaximal economy in Katayama et al.'s (2004) subjects before the hypoxic exposure. For example, at 16.1 km/h before hypoxia exposure, the mean value for VO2 was 54.4 mL/min/kg, with the majority (6/8) of the subjects above 52 mL/min/kg. In contrast, for all the subjects from experiment A reported in Fig. 1, before altitude exposure (after SL training), only 2/39 subjects had oxygen uptakes exceeding that level. Following hypoxia exposure, the hypoxia group had more normal and appropriate values for this work rate (52.5 mL/O2/kg), which were identical to those of the control group, both before and after intervention. Thus, repeat testing, and/or SL training appeared to normalize excessively high oxygen uptakes in the group assigned to hypoxia exposure.
The above-mentioned studies showing reduced submaximal VO2 after hypoxic exposure are supported by the classic paper by Hochachka et al. (1991), where high-altitude Andean natives were reported to have higher mechanical efficiencies than SL residents when compared at SL. However, the high-altitude subjects in that study were anemic and might therefore not serve as the best experimental group. Moreover, the controls were healthy Canadian athletes, with approximately 20 kg more body mass and an obviously different chronic nutritional state. Thus, it is not clear whether the differences reported between these groups are related to altitude acclimatization, or rather socioeconomic or racial differences.
In contrast, in the present study, we did not find that the mechanical efficiency was any higher in high vs low landers, and also Favier et al. (1995) reported similar unchanged muscular efficiencies in high-altitude natives. Accordingly, in a recent publication by Wagner et al. (2002), no differences in whole-body VO2 were found during graded cycling exercise to exhaustion between high-altitude natives and lowlanders acclimatized for 9 weeks to 5260 m. Also, natives to 2000 m altitude in Kenya are reported to have similar whole-body VO2s during graded exercise to maximum effort as compared with lowlanders acclimatized to this altitude for 14 days (Svedenhag et al., 1991). Thus, it seems that high-altitude natives are not different from low landers when it comes to mechanical efficiency.
Finally, further support to our contention that exercise economy remains unchanged after acclimatization to altitude can be found in the data from the Pikes Peak (Table 1). In these studies, not only was whole-body VO2 unchanged with acclimatization but actual leg VO2 remained unchanged as well both at rest and during fixed submaximal exercise. In some of these data, however, leg VO2 were lower at altitude as compared with SL whereas this was never the case for whole-body VO2. The small reduction in leg VO2 can be explained by acute changes in substrate utilization that are offset by a small increase in ventilatory and/or cardiac work so that total VO2 is unchanged.
This would clearly suggest that the exercising muscles have not altered their metabolic efficiency. If muscle efficiency were improved, this would have been reflected in a lower leg VO2 during exercise. This was not the case.
Limitations to our study
Another issue that needs to be addressed is whether or not this study adequately addresses the question of whether altitude exposure changes muscle mechanical efficiency. Numerous studies have shown that whole-body VO2 after a primary fast rise, lasting 2–3 min, increases further by a slow component during intense, but not moderate, submaximal dynamic exercise. Although most of the slow component can be attributed to the exercising skeletal muscles (Poole et al., 1991), it is still debated whether fiber recruitment, muscle acidosis, muscle temperature, or even other factors are also involved (Whipp et al., 2002). In a situation with increases in VO2 over time, potential changes in muscle efficiency are very difficult to measure. While the present studies C and D were performed below a work rate presumed necessary to induce the slow O2 component, and thus unbiased by this factor, studies A and B could be biased by a slow increase in VO2. To test this, we randomly selected data from six subjects from the post-altitude testing in study A, and analyzed breath-by breath-data, which were collected simultaneously with the Douglas bags. We then compared the recordings from the bags filled during the first 30 s, and from the last 30 s of the exercise. The results, as expected, showed that there was absolutely no drift: first 30 s=2930±538 mL; last 30 s=2939±502 mL. The mean difference between the two time periods was thus only 9 mL/min and is absolute proof that there was no drift during the measurements in study A. Moreover, it should be emphasized that although 16.1 km/h may seem like a fast speed for an untrained, or even a fit, non-athletic individual, the subjects for experiment A were all trained runners, and this speed was typical of a base training pace that the subjects could maintain for hours. These oxygen uptakes were well below the ventilatory and lactate thresholds as reported in Levine and Stray-Gundersen (1997) and were even further below the ventilatory threshold for the elite athletes in study A2 (Stray-Gundersen, 2001). Thus, it is highly unlikely that drift during the measurements could be compromising the data. For study B, we performed similar analysis of our data, and Table 3 shows the difference in VO2 between the last two 30-s recordings for all workloads and all conditions. Also, for study B, there was no observed drift in VO2 during any of the measures. Taken together, the above suggests that our measures are valid for the evaluation of muscle mechanical efficiency.
Table 3. Delta VO2 (mL/min) between the last two 30 s recordings of the 2.5 min increments, i.e., the difference in VO2 between recordings from 1.5 to 2 min and from 2 to 2.5 min
|SL||AH||2 W||2 W N||8 W||8 W N||Nat||NatN|
|260||17±0.2||19±0.6||12±0.2||16±0.5||20±0.4||16±0.5|| || |
|(0.5%)||(0.6%)||(0.4%)||(0.5%)||(0.6%)||(0.5%)|| || |
|300||12±0.4|| || ||17±0.5|| ||16±0.5|| || |
|(0.3%)|| || ||(0.5%)|| ||(0.4%)|| || |
|340||18±0.4|| || || || || || || |
|(0.5%)|| || || || || || || |
Submaximal VO2 is unchanged at all times after exposure from moderate altitude (2500–3000 m) up to altitudes of 4300 m. At 5280 m, submaximal VO2 is decreased as compared with SL both with acute and chronic exposure. Based on this stability, we propose that the decrease in VO2 with acute, extreme hypoxia is unrelated to physiological/anatomical adaptations, but is rather a metabolic response associated with severe hypoxia.