Effect of Acute Hypoxia on Maximal Oxyge
M. Angermann
H. Hoppeler
M. Wittwer
C. Däpp
H. Howald
M. Vogt
Effect of Acute Hypoxia on Maximal Oxygen
Uptake and Maximal Performance during Leg and
Upper-Body Exercise in Nordic Combined Skiers
We examined the effect of normobaric hypoxia (3200 m) on
maximal oxygen uptake (V˙O2max) and maximal power output
(Pmax) during leg and upper-body exercise to identify functional
and structural correlates of the variability in the decrement of
V˙O2max (∆V˙O2max) and of maximal power output (∆Pmax). Seven
well trained male Nordic combined skiers performed incremental exercise tests to exhaustion on a cycle ergometer (leg exercise) and on a custom built doublepoling ergometer for crosscountry skiing (upper-body exercise). Tests were carried out in
normoxia (560 m) and normobaric hypoxia (3200 m); biopsies
were taken from m. deltoideus. ∆V˙O2max was not significantly different between leg (– 9.1 ± 4.9 %) and upper-body exercise
(– 7.9 ± 5.8 %). By contrast, Pmax was significantly more reduced
during leg exercise (– 17.3 ± 3.3 %) than during upper-body exercise (– 9.6 ± 6.4 %, p < 0.05). Correlation analysis did not reveal
any significant relationship between leg and upper-body exercise neither for ∆V˙O2max nor for ∆Pmax. Furthermore, no relationship was observed between individual ∆V˙O2max and ∆Pmax. Analysis of structural data of m. deltoideus revealed a significant correlation between capillary density and ∆Pmax (R = – 0.80,
p = 0.03), as well as between volume density of mitochondria
and ∆Pmax (R = – 0.75, p = 0.05). In conclusion, it seems that
V˙O2max and Pmax are differently affected by hypoxia. The ability
to tolerate hypoxia is a characteristic of the individual depending
in part on the exercise mode. We present evidence that athletes
with a high capillarity and a high muscular oxidative capacity are
more sensitive to hypoxia.
Training & Testing
Abstract
Key words
Hypoxia · exercise testing · V˙O2max · maximal power · muscle morphology
1
Introduction
It is generally acknowledged that maximal oxygen consumption
(V˙O2max) and exercise performance are reduced at altitude. In
contrast to normoxia (N) altitude environment is characterized
by a lower PO2 leading to reduced alveolar O2 partial pressure
(PAO2). To some extent reduced PAO2 can be compensated for,
e.g. by hyperventilation. Endurance-trained athletes seem to be
particularly sensitive to hypoxia (H). Some authors reported decrements in V˙O2max even at low altitude (∼ 600 m) [10, 22] whereby a great individual variability was observed [3,12,14,15, 22].
From this it seems to be advantageous for mountaineers and athletes training or competing at altitude to know their individual
response to altitude. Hypoxia susceptibility can be tested by performance tests under normoxic and hypoxic conditions, whereby
the hypoxia-dependent decrement can be measured directly.
Several studies tried to identify the factors related to the decline
of V˙O2max (∆V˙O2max) in acute H. It has been demonstrated that
people with high V˙O2max in N [3, 7, 8,14,15,17, 22], low arterial
oxygen saturation in N (SaO2) at exhaustion [5,13], low hypoxic
SaO2 at exhaustion [7,15], high decrement in SaO2 at exhaustion
from N to H [8,10], high anaerobic lactate threshold [14], high
lean body mass [22], and low ventilatory equivalent for O2 [8]
are more susceptible to H. Although functional parameters (e.g.
ventilation or V˙O2max) are held responsible for some of the varia-
Affiliation
Department of Anatomy, University of Bern, Bern, Switzerland
Correspondence
Dr. Michael Vogt · Department of Anatomy · University of Bern · Baltzerstr. 2 · 3012 Bern · Switzerland ·
Phone: + 41316 3184 68 · E-mail: vogt@ana.unibe.ch
Accepted after revision: Accepted after revision: March 25, 2005
Bibliography
Int J Sports Med © Georg Thieme Verlag KG · Stuttgart · New York ·
DOI 10.1055/s-2005-865652 · Published online 2005 ·
ISSN 0172-4622
bility in the decline of V˙O2max, several authors pointed out that
muscular characteristics (e.g. mitochondrial density or capillarity) have also to be taken into account [3, 20 – 22]. This assumption is supported by mathematical models evaluating the interaction of ventilation, cardiac output, O2-transport, and muscular
characteristics in N and H [6, 27]. Moreover, it has been demonstrated extensively that exercise in H leads to muscle structural
modifications [12]. However, there is currently no experimental
data linking hypoxia sensitivity to muscle tissue characteristics.
Training & Testing
Whereas impairment of V˙O2max in H was extensively examined in
the past, less attention was paid to the decrement of Pmax in H
(∆Pmax). Most studies examining the effect of H on V˙O2max and Pmax
used cycle-ergometry [8,10,14,15,17, 21, 22] or treadmill running
[3, 5, 23], thus focusing on the lower limbs. Only few reports exist
about arm [24] or upper-body exercise (e.g. rowing) [20].
The purpose of the present investigation was to evaluate the effect of normobaric H (3200 m) on V˙O2max and Pmax during leg and
upper-body exercise in well trained athletes. Furthermore we
tried to identify performance parameters (ranking based on
cross-country skiing performance, V˙O2max, Pmax, anaerobic lactate
threshold) and muscle tissue characteristics (fibre type distribution, capillary per fibre ratio, capillaries per fibre area, fibre area,
mitochondrial volume density, intramyocellular lipid content),
which could be related to the hypoxia-dependent decrement of
V˙O2max and Pmax. It was hypothesized that H would reduce V˙O2max
to a greater extent than Pmax [8,15, 20, 21, 23]. Furthermore, we
assumed that ∆V˙O2max and ∆Pmax would be the same for both exercise modes (leg vs. upper-body exercise). It was expected that
athletes with good performance values would be more susceptible to H.
2
Materials and Methods
Subjects
Seven well trained male Nordic combined skiers gave their informed consent to participate in this study. With the exception
of one all were members of the A-team of the Swiss Ski Federation. Mean body weight and lean body mass were 70.1 ± 6.5 and
66.3 ± 6.0 kg, respectively. Mean body height was 178 ± 6.0 cm
and age 21.4 ± 2.5 years. Blood analysis revealed a hemoglobin
concentration of 147.4 ± 6.8 g/l and a haematocrit of 45.0 ± 2.8 %.
The study was approved by the Ethical Committee of the Canton
of Bern (KEK-Bern), Switzerland.
Performance tests
Two different incremental step-tests to exhaustion were performed to determine maximal power output (Pmax) and maximal
oxygen consumption (V˙O2max): one on an electromagnetically
braked cycle-ergometer (Ergoline 800 S, Ergoline GmbH, Bitz,
Germany) and the other on a custom-built double-poling ergometer for cross-country skiers (for details see Angermann et al.
[1, 2]). In short, on the double-poling ergometer the athletes were
driving a chain with their poles. The chain was connected to a
normal cycle ergometer through which the load was set. Double-poling mainly involved the muscles of the arms, the shoulders (to move the poles back), and the trunk. Each athlete was
tested under normoxic (560 m) and simulated hypoxic (3200 m,
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
FiO2 = 14.6 %) conditions during leg and upper-body exercise. To
simulate hypoxic conditions inspired air was diluted with nitrogen (“Altitrainer 200”, Sport and Medical Technology, Geneva,
Switzerland) [26]. All tests were carried out in a three-day period,
beginning with tests in H, followed by one day rest after which
tests in N were performed. Upper-body ergometry (morning) and
cycle ergometry (afternoon) were separated at least by 5 hours.
Cycle ergometry (leg exercise) started after 2 min rest followed
by 3 min warm-up with a load of 100 W (N) or 40 W (H). Thereafter the load was increased by 30 W every second minute until
the subjects were unable to maintain a cadence of 60 RPM.
Double-poling ergometry (upper-body exercise) also started
with 2 min rest followed by 3 min warm-up. Initial exercise loads
of 60 W (N) or 40 W (H) were increased by 20 W every 2 minutes
to loads just above anaerobic lactate threshold (determination of
anaerobic lactate threshold see ref. [16]). Blood lactate (Lactate
Pro, Arkray Factory Inc., Shiga, Japan) was measured after each
step during a 30-sec break. After passing the anaerobic threshold
the athletes were allowed a 2.5-min break before they started
their final bout to exhaustion at 60 W below that particular load.
They were encouraged to exercise continuously while the load
was increased by 20 W every 30 sec. This particular protocol
was chosen in order to keep the exercise duration reasonably
short to allow for V˙O2max to be reached. The total load the athletes had to overcome during double-poling ergometry consisted
of the predetermined external load in addition to the resistance
(friction) of the ergometer. Preliminary tests revealed that the resistance caused by friction was close to 70 W. Power output data
presented in this paper represent external load only.
Measurement of heart rate (Accurex Plus, Polar Electro Finland
Oy, Kempele, Finland), arterial oxygen saturation (Oxymeter:
PULSOX-3 i, Minolta, Osaka, Japan), and breath-by-breath analysis of expired air (Oxycon alpha, Jäger GmbH, Würzburg, Germany) was done continuously.
Analysis of muscle structure
Prior to the performance tests fine-needle biopsies were taken
from m. deltoideus. One part of the biopsy was immediately frozen in isopentane cooled with liquid nitrogen. Cryosections from
this part were used for analysis of fibre-type composition determined by ATPase staining [4]. The other part of the biopsy was
fixed in a 6.25 % solution of glutaraldehyde in 0.1 M sodium cacodylate buffer adjusted to 430 mOsm with NaCl (total osmolarity
of the fixative: 1200 mOsm, pH 7.4). The specimens were then
postfixed in a 1 % solution of osmium tetroxide in 0.06 M veronal
acetate buffer (total osmolarity: 386 mOsm, pH 7.4). They were
contrasted with 0.5 % uranyl acetate in 0.05 M maleate buffer,
pH 5.0. After dehydration in increasing concentrations of ethanol
(70 – 100%), they were passed through propylene oxide and embedded in Epon. For stereological analysis, we cut 2 randomly
chosen blocks from each biopsy. Ultrathin sections (50 – 70 nm)
were cut and double-contrasted. The orientation of the sections
was transverse or slightly oblique with regard to the fibre axis.
For estimation of capillary number and fibre cross-sectional area
we used a final magnification of × 1850. A final magnification of
× 24 000 was used for estimation of the volume densities of mitochondria, intramyocellular lipid, myofibrils, and residual sar-
Table 1 Maximal performance values of upper-body and leg exercise tests in normoxia (560 m) and normobaric hypoxia (3200 m)
Upper-body performance test
560 m
Pmax [W/kg]
3200 m
p2
Leg performance test
p1
560 m
3200 m
p1
560 m
3200 m
3.1 ± 0.3
*
5.4 ± 0.2
4.4 ± 0.2
*
n.a.
n.a.
53.6 ± 4.2
49.3 ± 3.4
*
57.3 ± 3.7
52.5 ± 3.0
*
*
(*)
La [mmol/L]
10.2 ± 1.3
14.1 ± 1.4
*
14.0 ± 1.6
14.2 ± 2.1
ns
*
ns
Hf [bpm]
192 ± 10
190 ± 10
ns
193 ± 7
188 ± 8
*
ns
(*)
V˙E [L/min]
144.4 ± 15.6
148.0 ± 14.3
ns
183.2 ± 21.7
174.0 ± 18.3
*
*
*
EQ O2 [unitless]
38.5 ± 3.0
42.9 ± 2.7
*
44.8 ± 4.1
47.3 ± 2.7
(*)
*
*
SaO2 [%]
93.2 ± 2.5
75.0 ± 5.9
*
92.8 ± 1.4
70.1 ± 5.2
*
ns
*
˙ E, ventilation; EQ O2, oxygen equivalent; SaO2, minimal oxygen saturation; p1, significance of differences between
Mean values ± SD; La, blood lactate; Hf, heart rate; V
560 m and 3200 m; p2, significance of differences between upper-body and leg exercise; * p < 0.05; (*) p < 0.10; ns, not significant; n.a., not applicable; n = 7 except for
˙O2max in leg performance test in normoxia (n = 6).
V
coplasmic components per volume of muscle fibre. Morphometry was done using standard procedures [29].
Statistical analysis
Data are presented as means ± SD. Differences in performance
values between N and H and between upper-body and leg exercise were analyzed using a Wilcoxon test for paired samples. Differences between ∆Pmax and ∆V˙O2max in both exercise modes
were evaluated by 2-way ANOVA with Tukey HSD post-hoc test.
Univariate linear regression analyses with ∆Pmax and ∆V˙O2max as
dependent variables were performed. The level of statistical significance was set at p < 0.05, results with p < 0.10 were interpreted as tendencies. The software package STATISTICA for Windows
Version 6.1 (Statsoft Inc., Hamburg, Germany) was used for statistical analysis.
Results
respectively). In contrast, during leg exercise under hypoxic conditions Pmax was reduced almost twice as much as V˙O2max (∆Pmax
– 17.3 ± 3.3 % vs. ∆V˙O2max – 9.1 ± 4.9 %, p < 0.05). ∆V˙O2max was similar for upper-body and leg exercise, whereas the decrement of
maximal power output in H was significantly greater for leg
compared to upper-body exercise. There was no significant relationship between ∆V˙O2max and ∆Pmax when measured during leg
(R = 0.53, p = 0.28) or during upper-body exercise (R = 0.06,
p = 0.90). Correlations between leg and upper-body exercise for
both ∆V˙O2max (R = – 0.09, p = 0.86) and ∆Pmax (R = 0.34, p = 0.46)
were low.
Muscular factors related to ∆V˙O2max and ∆Pmax during
upper-body exercise
Fibre type composition and morphometric data of m. deltoideus
are shown in Table 2. Correlation analysis (Table 3) revealed that
a high capillary density is significantly related to a high decrement of Pmax in H. Furthermore, a high ∆Pmax tended to correlate
with high mitochondrial volume density, high type 2 a fibre content, and cross-country skiing performance (rank). Significantly
greater decrements of V˙O2max under hypoxic conditions were observed in athletes with high intramyocellular lipid contents.
Maximal performance values of upper-body and leg exercise in N
and H are shown in Table 1. Pmax was significantly reduced by H
in both exercise modes. Absolute values recorded during upperbody and leg work cannot be compared due to technical differences in the design of the respective ergometers. V˙O2max reached
slightly higher values during leg ergometry and was significantly
decreased by H compared to N. The V˙O2-measurement of one
cycle ergometer test N was dismissed due to malfunction of the
metabolic cart. Maximum values for both blood lactate and heart
rate indicated that the subjects had reached the point of exhaustion, but there was no systematic difference between either N
and H or upper-body and leg performance. Ventilation at exhaustion was significantly higher with leg compared to upper-body
exercise. Oxygen equivalent was significantly higher under leg
vs. upper-body exercise and significantly lower in N compared
to H in the upper-body performance test. SaO2 significantly decreased under H in both exercise modes.
In order to study athletes with well trained arm and leg muscles
we recruited a group of Nordic combined skiers competing at international level. This limited the number of available athletes
and resulted in a low variability of performance parameters (e.g.
V˙O2max, Pmax). The small sample size and the low variation in variables studied reduced the power of correlation analysis so that
we were unable to perform multiple regression analysis [22]. A
further limitation of the present investigation is that for technical reasons the upper-body exercise protocol was discontinuous,
whereas the leg exercise protocol was uninterrupted.
Effect of hypoxia on V˙O2max and Pmax during upper-body
and leg exercise
No statistically significant difference between the hypoxia-induced reduction of Pmax (∆Pmax) and of V˙O2max (∆V˙O2max) was observed during upper-body exercise (– 9.6 ± 6.4 % and – 7.9 ± 5.8 %,
A major result of the study is that V˙O2max and Pmax were affected
differently by acute normobaric hypoxia corresponding to
3200 m. In contrast to the literature we found larger relative decrements of Pmax compared to V˙O2max during leg exercise under
hypoxic conditions. Another important finding is that during
Discussion
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
Training & Testing
3.4 ± 0.2
V˙O2max [ml/min/kg]
3
Table 2 Fibre type composition and morphometric data of m. deltoideus
Parameter
˙O2max or ∆Pmax and performance
Table 3 Correlations between ∆V
values of upper-body exercise, fibre type composition, and
morphometric data of m. deltoideus, respectively
Value
∆V˙O2max
type 1 fibres
69 ± 11%
type 2 a fibres
23 ± 9%
type 2 x fibres
R
1.8 ± 0.4
NA(c, f)
424 ± 100 mm–2
a(f)
2
4551 ± 1798 µm
– 0.13
0.78
Training & Testing
– Pmax
– 0.19
0.68
0.02
0.96
– LT
– 0.11
0.81
0.57
0.18
0.35
0.45
– 0.74
0.05
– 0.21
0.66
– 0.12
0.80
Vv(ms, f)
1.1 ± 0.5%
Fibre type composition
Vv(mt, f)
6.2 ± 1.5%
– type 1 fibres
0.34 ± 0.20%
– type 2 a fibres
0.46
0.31
– 0.69
0.08
80.1 ± 2.9%
– type 2 x fibres
– 0.13
0.77
0.61
0.14
– NN(c, f)
0.18
0.70
– 0.28
0.54
– NA(c, f)
– 0.41
0.36
– 0.80
0.03
Morphometric data
Mean values ± SD; NN(c, f): capillaries per muscle fibre; NA(c, f): capillaries per fibre
area; a(f): fibre cross sectional area; Vv(mc, f): central mitochondria volume density;
Vv(ms, f): subsarcolemmal mitochondria volume density; Vv(mt, f): total mitochondria volume density; Vv(li, f): intramyocellular lipid content; Vv(fi, f): myofibrils per
fibre volume
upper-body exercise athletes with high muscle capillarity and
high muscle mitochondrial density show larger losses of maximal power output when O2 supply is reduced. They are therefore
more susceptible to hypoxia.
4
0.22
– 0.53
– rank
Vv(fi, f)
p
– V˙O2max
5.1 ± 1.1%
Vv(li, f)
R
Performance values in normoxia
8 ± 12%
NN(c, f)
Vv(mc, f)
∆Pmax
p
Comparison of ∆V˙O2max and ∆Pmax
In general the measured ∆V˙O2max was less pronounced compared
to other studies with similarly trained athletes exposed to similar altitudes [14,15, 21, 25]. Previous work showed that ∆V˙O2max
caused by H is proportional to V˙O2max determined in N [3, 8,
14,15,17, 22] and therefore it is larger in endurance-trained athletes than in sedentary people [7]. We measured lower absolute
V˙O2max values in N compared to others [14,15, 21, 25], and this
could explain the smaller ∆V˙O2max observed in our study. Previously it was found that successful high altitude climbers do not
have extraordinarily high V˙O2max in N [17, 30]. Because individuals with high V˙O2max in N work on the steeper part of the oxygen
equilibrium curve, any fall in inspired O2 partial pressure would
lead to a more pronounced reduction of oxygen saturation [7]
and V˙O2max. Therefore, having a very high V˙O2max must not be an
advantage at least in the case of high altitude climbers. As a practical consequence our group of Nordic combined skiers should
theoretically perform quite well at altitude compared to their
sea-level performance.
During upper-body exercise, ∆V˙O2max was not significantly different from ∆Pmax, but during leg exercise H affected Pmax more than
V˙O2max. This finding is in contrast to the literature where most
studies with trained subjects show that compared to ∆V˙O2max
maximal power output and/or performance is equally [9] or less
influenced by H [8,15, 20, 21, 23]. It was demonstrated that the
amount of activated muscle mass is an important factor influencing the relationship between V˙O2max and Pmax and their hypoxia-dependent decrease [24]. In untrained subjects the hypoxia-dependent (12 % O2, ∼ 4300 m) loss of maximal aerobic power
(∆V˙O2max) is greater than the loss in maximal power output
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
– a(f)
0.45
0.31
0.58
0.17
– Vv(mc, f)
– 0.58
0.17
– 0.75
0.05
– Vv(ms, f)
– 0.51
0.25
– 0.37
0.40
– Vv(mt, f)
– 0.60
0.15
– 0.68
0.09
– Vv(li, f)
– 0.78
0.04
– 0.27
0.56
R, correlation coefficient; for abbreviations see Tables 1 and 2. Bold figures indicate
a significant (p < 0.05) relationship or a tendency (p < 0.10)
(∆Pmax) during two-leg exercise (– 28.2 % vs. – 19.6 % for ∆V˙O2max
and ∆Pmax, respectively), but these values are different for arm
and shoulder exercise (– 5.9 % vs. – 5.2 %), one-leg exercise
(– 7.8 % vs. – 9.0 %) or arm exercise (– 4.6 % vs. – 12.4 %). The authors propose that during maximal exercise smaller muscles
(arms) are more difficult to perfuse and therefore maximal exercise is limited primarily by the intrinsic power of muscles rather
than by O2 supply [24]. In accordance with our study these results show that V˙O2max and Pmax can differently be affected by H
depending on the muscle mass recruited during the exercise
task.
Another possible explanation for the differences between
∆V˙O2max and ∆Pmax in leg exercise could be provided by the concept of the “central governor” [13,18]. This concept postulates
that during exercise in H central drive is reduced as a consequence of the lower inspired O2 fraction, which would lead to reduced muscle recruitment. During an incremental exercise test
V˙O2 increases almost linearly with increasing load but O2 consumption usually levels off some time before the termination of
the test, determining V˙O2max. On the other hand power output increases continuously until the end of the test where Pmax is measured. Thus, V˙O2max is often reached before Pmax. According to the
concept of central governor, reduced muscle recruitment during
maximal exercise in H could affect Pmax to a larger extent than
V˙O2max, but it is questionable whether quadriceps muscles are
fully activated during incremental exercise.
It has been shown previously that V˙O2max correlates well with
rowing time in N (R = – 0.90) but not in H (R = – 0.48) [20]. The
authors of that study summarized that H had a greater influence
on V˙O2max than on exercise performance. This finding suggests
that the relationship between V˙O2max and Pmax is lost in H. Our
results support this result because we did not find a correlation
between ∆Pmax and ∆V˙O2max neither for leg nor for upper-body
exercise. Thus, maximal aerobic power and maximal power output seem to be affected differently by H.
Comparison between leg and upper-body exercise
Our results indicate that average ∆V˙O2max is similar for leg and
upper-body exercise in Nordic combined skiers. V˙O2max during
upper-body exercise was between 92 % and 95 % of the V˙O2max
measured during leg exercise. This suggests that the upper body
exercise mode (double-poling) used in the present study is comparable to whole body exercise at least for trained Nordic combined skiers. As similar V˙O2max values were reached in both exercise modes, it is not surprising that there is no significant difference in ∆V˙O2max caused by H. We conclude that the tested Nordic
combined skiers were well trained in the upper body and that
upper body exercise involves nearly a similar amount of muscle
mass compared to leg exercise on a bicycle ergometer.
Although average ∆V˙O2max was quite similar for leg and upperbody exercise, correlation analysis revealed that significant individual differences exist for the two exercise modes. Measurements identified athletes with a high decrement of V˙O2max induced by H on the cycle ergometer, but with a low decrement of
V˙O2max on the double-poling ergometer, and vice versa. If the hypoxia-dependent decrease of V˙O2max is a general characteristic of
a person we would expect a correlation between leg and upperbody exercise. Our results do not support this conclusion and
therefore challenge the idea of the existence of a general ability
of an individual to tolerate H at maximal exercise. In the other
hand, our findings indicate that the ability to tolerate H depends
in part on the exercise mode.
In contrast to ∆V˙O2max H-induced ∆Pmax was significantly larger
during leg than upper body exercise. In a study of Harms et al.
[11] it was shown that the work of breathing (Wb) can have significant effects on leg blood flow and V˙O2max during maximal exercise. Harms found that with increased Wb whole body V˙O2max
and cardiac output remains unchanged but leg blood flow and
leg O2 consumption are reduced. In contrast, both whole body
V˙O2max and cardiac output are reduced when Wb is lower while
leg blood flow and leg O2 consumption are increased [11]. In our
study, the maximal oxygen equivalent (EQ O2) was higher during
leg compared to upper-body exercise both under N and H, indicating indirectly that Wb per liter O2 was higher during leg exercise on the bicycle ergometer. This might have compromised
maximal power output in H via reduced leg blood flow. In other
words, due to increased Wb in H, leg blood flow and therefore
Muscular factors related to ∆V˙O2max and ∆Pmax for
upper-body exercise
Classical physiological performance parameters (V˙O2max, Pmax,
anaerobic lactate threshold) measured in N did not explain the
variability of ∆V˙O2max and ∆Pmax during upper-body exercise (Table 3).This result was rather unexpected because most studies using leg exercise found a good correlation between V˙O2max in N and
∆V˙O2max [3, 8,14,15,17, 22] while only a few did not [5, 9]. Data analysis of studies showing good correlations between V˙O2max and
∆V˙O2max [15,17, 22] revealed a wide range of V˙O2max values as
trained and untrained subjects were involved in the same experiment. Obviously, a wide range in measured V˙O2max or ∆V˙O2max allows for easier detection of a relationship between the two variables. When the focus is on a sub-group of similarly (endurance)
trained subjects, as was the case in our study, a relationship between V˙O2max and ∆V˙O2max cannot be demonstrated in these studies. This fact challenges the explanatory power of V˙O2max measured in N on ∆V˙O2max for a homogeneous group of trained subjects.
To our knowledge the present study is the first investigating the
relation of ∆V˙O2max and ∆Pmax to muscle morphology. A novel
finding is that athletes with muscles adapted to endurance training (high capacity to supply and to utilise O2) exhibit higher decrements of Pmax in H during upper-body exercise. This was shown
by the correlations between ∆Pmax and muscle capillarity and
density of mitochondria of m. deltoideus, respectively (Fig. 1). It
is generally believed that peripheral (muscular) factors such as
perfusion, diffusion, and mitochondrial capacity modulate the
hypoxia-dependent decrease of V˙O2max and Pmax [3, 6, 21, 22,
24, 27], but so far no direct experimental evidence existed. Regression analysis displayed in Fig. 1 points to a significant or
nearly significant correlation between capillarity and ∆Pmax, and
between mitochondrial volume density and ∆Pmax, respectively.
Although this result is strongly influenced by the one single athlete displaying rather poor oxidative capacities of m. deltoideus,
˙O2max of upper-body exercise in acute hypoxia in
Fig. 1 ∆Pmax and ∆V
dependence of volume density of total mitochondria (Vv [mt, f]) and
of capillaries per fibre area (NA [c, f]).
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
Training & Testing
Finally, influences by the different test protocols for leg and
upper body exercise in our study must also be considered. Faster
increments in the workload during upper-body exercise may
have led to an extension in the anaerobic part of the exercise test,
thus influencing the relationship between ∆V˙O2max and ∆Pmax.
maximal power output is reduced while V˙O2max remains the
same.
5
his example supports the theory that well trained athletes become more sensitive to H compared to untrained subjects.
5
6
Some authors calculated the different contributions of the lung,
the circulatory system, and the muscles to the limitation of
V˙O2max [6, 27, 28]. They concluded that during exercise in H muscular factors become more important in limiting V˙O2max, when
small muscle groups are exercised or for well trained athletes
having a high V˙O2max.
7
8
9
Training & Testing
6
In contrast to ∆Pmax no correlations were found between ∆V˙O2max
and capillarity or mitochondrial density. This can partly be explained by the data structure of ∆V˙O2max and the small sample
size. We have to keep in mind that athletic performance is a complex output of interactions between different body functions.
From this systemic point of view, our study examined only a small
part of the system and when we interpret the results we have to
realize that there exists substantial individual variation in compensatory mechanisms, especially during exercise in hypoxia.
10
11
12
13
Conclusion
Maximal O2 uptake and maximal power output are affected differently by hypoxia. However, it remains an open issue to which
extent they are reduced at altitude. Our results question the
paradigm that the ability to tolerate hypoxia (altitude) depends
only on the athlete’s individuality and training status. The mode
of exercise has also to be taken into account. Furthermore our
findings expand the knowledge about the relation between peripheral factors and the hypoxia-dependent decrease of Pmax
and V˙O2max in trained athletes. The results provide evidence that
the impairment of exercise performance in acute hypoxia, corresponding to an altitude of 3200 m, is more pronounced in athletes with muscles well adapted to endurance training.
14
15
16
17
18
19
20
Acknowledgements
21
This study was funded by the Swiss Sports Commission (ESK).
We thank Christoph Lehmann for constructing the upper-body
ergometer, Franziska Graber for processing and analyzing the biopsies, and Ruth Vock and Silvia Schmutz for their assistance in
the preparation of the manuscript.
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H. Hoppeler
M. Wittwer
C. Däpp
H. Howald
M. Vogt
Effect of Acute Hypoxia on Maximal Oxygen
Uptake and Maximal Performance during Leg and
Upper-Body Exercise in Nordic Combined Skiers
We examined the effect of normobaric hypoxia (3200 m) on
maximal oxygen uptake (V˙O2max) and maximal power output
(Pmax) during leg and upper-body exercise to identify functional
and structural correlates of the variability in the decrement of
V˙O2max (∆V˙O2max) and of maximal power output (∆Pmax). Seven
well trained male Nordic combined skiers performed incremental exercise tests to exhaustion on a cycle ergometer (leg exercise) and on a custom built doublepoling ergometer for crosscountry skiing (upper-body exercise). Tests were carried out in
normoxia (560 m) and normobaric hypoxia (3200 m); biopsies
were taken from m. deltoideus. ∆V˙O2max was not significantly different between leg (– 9.1 ± 4.9 %) and upper-body exercise
(– 7.9 ± 5.8 %). By contrast, Pmax was significantly more reduced
during leg exercise (– 17.3 ± 3.3 %) than during upper-body exercise (– 9.6 ± 6.4 %, p < 0.05). Correlation analysis did not reveal
any significant relationship between leg and upper-body exercise neither for ∆V˙O2max nor for ∆Pmax. Furthermore, no relationship was observed between individual ∆V˙O2max and ∆Pmax. Analysis of structural data of m. deltoideus revealed a significant correlation between capillary density and ∆Pmax (R = – 0.80,
p = 0.03), as well as between volume density of mitochondria
and ∆Pmax (R = – 0.75, p = 0.05). In conclusion, it seems that
V˙O2max and Pmax are differently affected by hypoxia. The ability
to tolerate hypoxia is a characteristic of the individual depending
in part on the exercise mode. We present evidence that athletes
with a high capillarity and a high muscular oxidative capacity are
more sensitive to hypoxia.
Training & Testing
Abstract
Key words
Hypoxia · exercise testing · V˙O2max · maximal power · muscle morphology
1
Introduction
It is generally acknowledged that maximal oxygen consumption
(V˙O2max) and exercise performance are reduced at altitude. In
contrast to normoxia (N) altitude environment is characterized
by a lower PO2 leading to reduced alveolar O2 partial pressure
(PAO2). To some extent reduced PAO2 can be compensated for,
e.g. by hyperventilation. Endurance-trained athletes seem to be
particularly sensitive to hypoxia (H). Some authors reported decrements in V˙O2max even at low altitude (∼ 600 m) [10, 22] whereby a great individual variability was observed [3,12,14,15, 22].
From this it seems to be advantageous for mountaineers and athletes training or competing at altitude to know their individual
response to altitude. Hypoxia susceptibility can be tested by performance tests under normoxic and hypoxic conditions, whereby
the hypoxia-dependent decrement can be measured directly.
Several studies tried to identify the factors related to the decline
of V˙O2max (∆V˙O2max) in acute H. It has been demonstrated that
people with high V˙O2max in N [3, 7, 8,14,15,17, 22], low arterial
oxygen saturation in N (SaO2) at exhaustion [5,13], low hypoxic
SaO2 at exhaustion [7,15], high decrement in SaO2 at exhaustion
from N to H [8,10], high anaerobic lactate threshold [14], high
lean body mass [22], and low ventilatory equivalent for O2 [8]
are more susceptible to H. Although functional parameters (e.g.
ventilation or V˙O2max) are held responsible for some of the varia-
Affiliation
Department of Anatomy, University of Bern, Bern, Switzerland
Correspondence
Dr. Michael Vogt · Department of Anatomy · University of Bern · Baltzerstr. 2 · 3012 Bern · Switzerland ·
Phone: + 41316 3184 68 · E-mail: vogt@ana.unibe.ch
Accepted after revision: Accepted after revision: March 25, 2005
Bibliography
Int J Sports Med © Georg Thieme Verlag KG · Stuttgart · New York ·
DOI 10.1055/s-2005-865652 · Published online 2005 ·
ISSN 0172-4622
bility in the decline of V˙O2max, several authors pointed out that
muscular characteristics (e.g. mitochondrial density or capillarity) have also to be taken into account [3, 20 – 22]. This assumption is supported by mathematical models evaluating the interaction of ventilation, cardiac output, O2-transport, and muscular
characteristics in N and H [6, 27]. Moreover, it has been demonstrated extensively that exercise in H leads to muscle structural
modifications [12]. However, there is currently no experimental
data linking hypoxia sensitivity to muscle tissue characteristics.
Training & Testing
Whereas impairment of V˙O2max in H was extensively examined in
the past, less attention was paid to the decrement of Pmax in H
(∆Pmax). Most studies examining the effect of H on V˙O2max and Pmax
used cycle-ergometry [8,10,14,15,17, 21, 22] or treadmill running
[3, 5, 23], thus focusing on the lower limbs. Only few reports exist
about arm [24] or upper-body exercise (e.g. rowing) [20].
The purpose of the present investigation was to evaluate the effect of normobaric H (3200 m) on V˙O2max and Pmax during leg and
upper-body exercise in well trained athletes. Furthermore we
tried to identify performance parameters (ranking based on
cross-country skiing performance, V˙O2max, Pmax, anaerobic lactate
threshold) and muscle tissue characteristics (fibre type distribution, capillary per fibre ratio, capillaries per fibre area, fibre area,
mitochondrial volume density, intramyocellular lipid content),
which could be related to the hypoxia-dependent decrement of
V˙O2max and Pmax. It was hypothesized that H would reduce V˙O2max
to a greater extent than Pmax [8,15, 20, 21, 23]. Furthermore, we
assumed that ∆V˙O2max and ∆Pmax would be the same for both exercise modes (leg vs. upper-body exercise). It was expected that
athletes with good performance values would be more susceptible to H.
2
Materials and Methods
Subjects
Seven well trained male Nordic combined skiers gave their informed consent to participate in this study. With the exception
of one all were members of the A-team of the Swiss Ski Federation. Mean body weight and lean body mass were 70.1 ± 6.5 and
66.3 ± 6.0 kg, respectively. Mean body height was 178 ± 6.0 cm
and age 21.4 ± 2.5 years. Blood analysis revealed a hemoglobin
concentration of 147.4 ± 6.8 g/l and a haematocrit of 45.0 ± 2.8 %.
The study was approved by the Ethical Committee of the Canton
of Bern (KEK-Bern), Switzerland.
Performance tests
Two different incremental step-tests to exhaustion were performed to determine maximal power output (Pmax) and maximal
oxygen consumption (V˙O2max): one on an electromagnetically
braked cycle-ergometer (Ergoline 800 S, Ergoline GmbH, Bitz,
Germany) and the other on a custom-built double-poling ergometer for cross-country skiers (for details see Angermann et al.
[1, 2]). In short, on the double-poling ergometer the athletes were
driving a chain with their poles. The chain was connected to a
normal cycle ergometer through which the load was set. Double-poling mainly involved the muscles of the arms, the shoulders (to move the poles back), and the trunk. Each athlete was
tested under normoxic (560 m) and simulated hypoxic (3200 m,
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
FiO2 = 14.6 %) conditions during leg and upper-body exercise. To
simulate hypoxic conditions inspired air was diluted with nitrogen (“Altitrainer 200”, Sport and Medical Technology, Geneva,
Switzerland) [26]. All tests were carried out in a three-day period,
beginning with tests in H, followed by one day rest after which
tests in N were performed. Upper-body ergometry (morning) and
cycle ergometry (afternoon) were separated at least by 5 hours.
Cycle ergometry (leg exercise) started after 2 min rest followed
by 3 min warm-up with a load of 100 W (N) or 40 W (H). Thereafter the load was increased by 30 W every second minute until
the subjects were unable to maintain a cadence of 60 RPM.
Double-poling ergometry (upper-body exercise) also started
with 2 min rest followed by 3 min warm-up. Initial exercise loads
of 60 W (N) or 40 W (H) were increased by 20 W every 2 minutes
to loads just above anaerobic lactate threshold (determination of
anaerobic lactate threshold see ref. [16]). Blood lactate (Lactate
Pro, Arkray Factory Inc., Shiga, Japan) was measured after each
step during a 30-sec break. After passing the anaerobic threshold
the athletes were allowed a 2.5-min break before they started
their final bout to exhaustion at 60 W below that particular load.
They were encouraged to exercise continuously while the load
was increased by 20 W every 30 sec. This particular protocol
was chosen in order to keep the exercise duration reasonably
short to allow for V˙O2max to be reached. The total load the athletes had to overcome during double-poling ergometry consisted
of the predetermined external load in addition to the resistance
(friction) of the ergometer. Preliminary tests revealed that the resistance caused by friction was close to 70 W. Power output data
presented in this paper represent external load only.
Measurement of heart rate (Accurex Plus, Polar Electro Finland
Oy, Kempele, Finland), arterial oxygen saturation (Oxymeter:
PULSOX-3 i, Minolta, Osaka, Japan), and breath-by-breath analysis of expired air (Oxycon alpha, Jäger GmbH, Würzburg, Germany) was done continuously.
Analysis of muscle structure
Prior to the performance tests fine-needle biopsies were taken
from m. deltoideus. One part of the biopsy was immediately frozen in isopentane cooled with liquid nitrogen. Cryosections from
this part were used for analysis of fibre-type composition determined by ATPase staining [4]. The other part of the biopsy was
fixed in a 6.25 % solution of glutaraldehyde in 0.1 M sodium cacodylate buffer adjusted to 430 mOsm with NaCl (total osmolarity
of the fixative: 1200 mOsm, pH 7.4). The specimens were then
postfixed in a 1 % solution of osmium tetroxide in 0.06 M veronal
acetate buffer (total osmolarity: 386 mOsm, pH 7.4). They were
contrasted with 0.5 % uranyl acetate in 0.05 M maleate buffer,
pH 5.0. After dehydration in increasing concentrations of ethanol
(70 – 100%), they were passed through propylene oxide and embedded in Epon. For stereological analysis, we cut 2 randomly
chosen blocks from each biopsy. Ultrathin sections (50 – 70 nm)
were cut and double-contrasted. The orientation of the sections
was transverse or slightly oblique with regard to the fibre axis.
For estimation of capillary number and fibre cross-sectional area
we used a final magnification of × 1850. A final magnification of
× 24 000 was used for estimation of the volume densities of mitochondria, intramyocellular lipid, myofibrils, and residual sar-
Table 1 Maximal performance values of upper-body and leg exercise tests in normoxia (560 m) and normobaric hypoxia (3200 m)
Upper-body performance test
560 m
Pmax [W/kg]
3200 m
p2
Leg performance test
p1
560 m
3200 m
p1
560 m
3200 m
3.1 ± 0.3
*
5.4 ± 0.2
4.4 ± 0.2
*
n.a.
n.a.
53.6 ± 4.2
49.3 ± 3.4
*
57.3 ± 3.7
52.5 ± 3.0
*
*
(*)
La [mmol/L]
10.2 ± 1.3
14.1 ± 1.4
*
14.0 ± 1.6
14.2 ± 2.1
ns
*
ns
Hf [bpm]
192 ± 10
190 ± 10
ns
193 ± 7
188 ± 8
*
ns
(*)
V˙E [L/min]
144.4 ± 15.6
148.0 ± 14.3
ns
183.2 ± 21.7
174.0 ± 18.3
*
*
*
EQ O2 [unitless]
38.5 ± 3.0
42.9 ± 2.7
*
44.8 ± 4.1
47.3 ± 2.7
(*)
*
*
SaO2 [%]
93.2 ± 2.5
75.0 ± 5.9
*
92.8 ± 1.4
70.1 ± 5.2
*
ns
*
˙ E, ventilation; EQ O2, oxygen equivalent; SaO2, minimal oxygen saturation; p1, significance of differences between
Mean values ± SD; La, blood lactate; Hf, heart rate; V
560 m and 3200 m; p2, significance of differences between upper-body and leg exercise; * p < 0.05; (*) p < 0.10; ns, not significant; n.a., not applicable; n = 7 except for
˙O2max in leg performance test in normoxia (n = 6).
V
coplasmic components per volume of muscle fibre. Morphometry was done using standard procedures [29].
Statistical analysis
Data are presented as means ± SD. Differences in performance
values between N and H and between upper-body and leg exercise were analyzed using a Wilcoxon test for paired samples. Differences between ∆Pmax and ∆V˙O2max in both exercise modes
were evaluated by 2-way ANOVA with Tukey HSD post-hoc test.
Univariate linear regression analyses with ∆Pmax and ∆V˙O2max as
dependent variables were performed. The level of statistical significance was set at p < 0.05, results with p < 0.10 were interpreted as tendencies. The software package STATISTICA for Windows
Version 6.1 (Statsoft Inc., Hamburg, Germany) was used for statistical analysis.
Results
respectively). In contrast, during leg exercise under hypoxic conditions Pmax was reduced almost twice as much as V˙O2max (∆Pmax
– 17.3 ± 3.3 % vs. ∆V˙O2max – 9.1 ± 4.9 %, p < 0.05). ∆V˙O2max was similar for upper-body and leg exercise, whereas the decrement of
maximal power output in H was significantly greater for leg
compared to upper-body exercise. There was no significant relationship between ∆V˙O2max and ∆Pmax when measured during leg
(R = 0.53, p = 0.28) or during upper-body exercise (R = 0.06,
p = 0.90). Correlations between leg and upper-body exercise for
both ∆V˙O2max (R = – 0.09, p = 0.86) and ∆Pmax (R = 0.34, p = 0.46)
were low.
Muscular factors related to ∆V˙O2max and ∆Pmax during
upper-body exercise
Fibre type composition and morphometric data of m. deltoideus
are shown in Table 2. Correlation analysis (Table 3) revealed that
a high capillary density is significantly related to a high decrement of Pmax in H. Furthermore, a high ∆Pmax tended to correlate
with high mitochondrial volume density, high type 2 a fibre content, and cross-country skiing performance (rank). Significantly
greater decrements of V˙O2max under hypoxic conditions were observed in athletes with high intramyocellular lipid contents.
Maximal performance values of upper-body and leg exercise in N
and H are shown in Table 1. Pmax was significantly reduced by H
in both exercise modes. Absolute values recorded during upperbody and leg work cannot be compared due to technical differences in the design of the respective ergometers. V˙O2max reached
slightly higher values during leg ergometry and was significantly
decreased by H compared to N. The V˙O2-measurement of one
cycle ergometer test N was dismissed due to malfunction of the
metabolic cart. Maximum values for both blood lactate and heart
rate indicated that the subjects had reached the point of exhaustion, but there was no systematic difference between either N
and H or upper-body and leg performance. Ventilation at exhaustion was significantly higher with leg compared to upper-body
exercise. Oxygen equivalent was significantly higher under leg
vs. upper-body exercise and significantly lower in N compared
to H in the upper-body performance test. SaO2 significantly decreased under H in both exercise modes.
In order to study athletes with well trained arm and leg muscles
we recruited a group of Nordic combined skiers competing at international level. This limited the number of available athletes
and resulted in a low variability of performance parameters (e.g.
V˙O2max, Pmax). The small sample size and the low variation in variables studied reduced the power of correlation analysis so that
we were unable to perform multiple regression analysis [22]. A
further limitation of the present investigation is that for technical reasons the upper-body exercise protocol was discontinuous,
whereas the leg exercise protocol was uninterrupted.
Effect of hypoxia on V˙O2max and Pmax during upper-body
and leg exercise
No statistically significant difference between the hypoxia-induced reduction of Pmax (∆Pmax) and of V˙O2max (∆V˙O2max) was observed during upper-body exercise (– 9.6 ± 6.4 % and – 7.9 ± 5.8 %,
A major result of the study is that V˙O2max and Pmax were affected
differently by acute normobaric hypoxia corresponding to
3200 m. In contrast to the literature we found larger relative decrements of Pmax compared to V˙O2max during leg exercise under
hypoxic conditions. Another important finding is that during
Discussion
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
Training & Testing
3.4 ± 0.2
V˙O2max [ml/min/kg]
3
Table 2 Fibre type composition and morphometric data of m. deltoideus
Parameter
˙O2max or ∆Pmax and performance
Table 3 Correlations between ∆V
values of upper-body exercise, fibre type composition, and
morphometric data of m. deltoideus, respectively
Value
∆V˙O2max
type 1 fibres
69 ± 11%
type 2 a fibres
23 ± 9%
type 2 x fibres
R
1.8 ± 0.4
NA(c, f)
424 ± 100 mm–2
a(f)
2
4551 ± 1798 µm
– 0.13
0.78
Training & Testing
– Pmax
– 0.19
0.68
0.02
0.96
– LT
– 0.11
0.81
0.57
0.18
0.35
0.45
– 0.74
0.05
– 0.21
0.66
– 0.12
0.80
Vv(ms, f)
1.1 ± 0.5%
Fibre type composition
Vv(mt, f)
6.2 ± 1.5%
– type 1 fibres
0.34 ± 0.20%
– type 2 a fibres
0.46
0.31
– 0.69
0.08
80.1 ± 2.9%
– type 2 x fibres
– 0.13
0.77
0.61
0.14
– NN(c, f)
0.18
0.70
– 0.28
0.54
– NA(c, f)
– 0.41
0.36
– 0.80
0.03
Morphometric data
Mean values ± SD; NN(c, f): capillaries per muscle fibre; NA(c, f): capillaries per fibre
area; a(f): fibre cross sectional area; Vv(mc, f): central mitochondria volume density;
Vv(ms, f): subsarcolemmal mitochondria volume density; Vv(mt, f): total mitochondria volume density; Vv(li, f): intramyocellular lipid content; Vv(fi, f): myofibrils per
fibre volume
upper-body exercise athletes with high muscle capillarity and
high muscle mitochondrial density show larger losses of maximal power output when O2 supply is reduced. They are therefore
more susceptible to hypoxia.
4
0.22
– 0.53
– rank
Vv(fi, f)
p
– V˙O2max
5.1 ± 1.1%
Vv(li, f)
R
Performance values in normoxia
8 ± 12%
NN(c, f)
Vv(mc, f)
∆Pmax
p
Comparison of ∆V˙O2max and ∆Pmax
In general the measured ∆V˙O2max was less pronounced compared
to other studies with similarly trained athletes exposed to similar altitudes [14,15, 21, 25]. Previous work showed that ∆V˙O2max
caused by H is proportional to V˙O2max determined in N [3, 8,
14,15,17, 22] and therefore it is larger in endurance-trained athletes than in sedentary people [7]. We measured lower absolute
V˙O2max values in N compared to others [14,15, 21, 25], and this
could explain the smaller ∆V˙O2max observed in our study. Previously it was found that successful high altitude climbers do not
have extraordinarily high V˙O2max in N [17, 30]. Because individuals with high V˙O2max in N work on the steeper part of the oxygen
equilibrium curve, any fall in inspired O2 partial pressure would
lead to a more pronounced reduction of oxygen saturation [7]
and V˙O2max. Therefore, having a very high V˙O2max must not be an
advantage at least in the case of high altitude climbers. As a practical consequence our group of Nordic combined skiers should
theoretically perform quite well at altitude compared to their
sea-level performance.
During upper-body exercise, ∆V˙O2max was not significantly different from ∆Pmax, but during leg exercise H affected Pmax more than
V˙O2max. This finding is in contrast to the literature where most
studies with trained subjects show that compared to ∆V˙O2max
maximal power output and/or performance is equally [9] or less
influenced by H [8,15, 20, 21, 23]. It was demonstrated that the
amount of activated muscle mass is an important factor influencing the relationship between V˙O2max and Pmax and their hypoxia-dependent decrease [24]. In untrained subjects the hypoxia-dependent (12 % O2, ∼ 4300 m) loss of maximal aerobic power
(∆V˙O2max) is greater than the loss in maximal power output
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
– a(f)
0.45
0.31
0.58
0.17
– Vv(mc, f)
– 0.58
0.17
– 0.75
0.05
– Vv(ms, f)
– 0.51
0.25
– 0.37
0.40
– Vv(mt, f)
– 0.60
0.15
– 0.68
0.09
– Vv(li, f)
– 0.78
0.04
– 0.27
0.56
R, correlation coefficient; for abbreviations see Tables 1 and 2. Bold figures indicate
a significant (p < 0.05) relationship or a tendency (p < 0.10)
(∆Pmax) during two-leg exercise (– 28.2 % vs. – 19.6 % for ∆V˙O2max
and ∆Pmax, respectively), but these values are different for arm
and shoulder exercise (– 5.9 % vs. – 5.2 %), one-leg exercise
(– 7.8 % vs. – 9.0 %) or arm exercise (– 4.6 % vs. – 12.4 %). The authors propose that during maximal exercise smaller muscles
(arms) are more difficult to perfuse and therefore maximal exercise is limited primarily by the intrinsic power of muscles rather
than by O2 supply [24]. In accordance with our study these results show that V˙O2max and Pmax can differently be affected by H
depending on the muscle mass recruited during the exercise
task.
Another possible explanation for the differences between
∆V˙O2max and ∆Pmax in leg exercise could be provided by the concept of the “central governor” [13,18]. This concept postulates
that during exercise in H central drive is reduced as a consequence of the lower inspired O2 fraction, which would lead to reduced muscle recruitment. During an incremental exercise test
V˙O2 increases almost linearly with increasing load but O2 consumption usually levels off some time before the termination of
the test, determining V˙O2max. On the other hand power output increases continuously until the end of the test where Pmax is measured. Thus, V˙O2max is often reached before Pmax. According to the
concept of central governor, reduced muscle recruitment during
maximal exercise in H could affect Pmax to a larger extent than
V˙O2max, but it is questionable whether quadriceps muscles are
fully activated during incremental exercise.
It has been shown previously that V˙O2max correlates well with
rowing time in N (R = – 0.90) but not in H (R = – 0.48) [20]. The
authors of that study summarized that H had a greater influence
on V˙O2max than on exercise performance. This finding suggests
that the relationship between V˙O2max and Pmax is lost in H. Our
results support this result because we did not find a correlation
between ∆Pmax and ∆V˙O2max neither for leg nor for upper-body
exercise. Thus, maximal aerobic power and maximal power output seem to be affected differently by H.
Comparison between leg and upper-body exercise
Our results indicate that average ∆V˙O2max is similar for leg and
upper-body exercise in Nordic combined skiers. V˙O2max during
upper-body exercise was between 92 % and 95 % of the V˙O2max
measured during leg exercise. This suggests that the upper body
exercise mode (double-poling) used in the present study is comparable to whole body exercise at least for trained Nordic combined skiers. As similar V˙O2max values were reached in both exercise modes, it is not surprising that there is no significant difference in ∆V˙O2max caused by H. We conclude that the tested Nordic
combined skiers were well trained in the upper body and that
upper body exercise involves nearly a similar amount of muscle
mass compared to leg exercise on a bicycle ergometer.
Although average ∆V˙O2max was quite similar for leg and upperbody exercise, correlation analysis revealed that significant individual differences exist for the two exercise modes. Measurements identified athletes with a high decrement of V˙O2max induced by H on the cycle ergometer, but with a low decrement of
V˙O2max on the double-poling ergometer, and vice versa. If the hypoxia-dependent decrease of V˙O2max is a general characteristic of
a person we would expect a correlation between leg and upperbody exercise. Our results do not support this conclusion and
therefore challenge the idea of the existence of a general ability
of an individual to tolerate H at maximal exercise. In the other
hand, our findings indicate that the ability to tolerate H depends
in part on the exercise mode.
In contrast to ∆V˙O2max H-induced ∆Pmax was significantly larger
during leg than upper body exercise. In a study of Harms et al.
[11] it was shown that the work of breathing (Wb) can have significant effects on leg blood flow and V˙O2max during maximal exercise. Harms found that with increased Wb whole body V˙O2max
and cardiac output remains unchanged but leg blood flow and
leg O2 consumption are reduced. In contrast, both whole body
V˙O2max and cardiac output are reduced when Wb is lower while
leg blood flow and leg O2 consumption are increased [11]. In our
study, the maximal oxygen equivalent (EQ O2) was higher during
leg compared to upper-body exercise both under N and H, indicating indirectly that Wb per liter O2 was higher during leg exercise on the bicycle ergometer. This might have compromised
maximal power output in H via reduced leg blood flow. In other
words, due to increased Wb in H, leg blood flow and therefore
Muscular factors related to ∆V˙O2max and ∆Pmax for
upper-body exercise
Classical physiological performance parameters (V˙O2max, Pmax,
anaerobic lactate threshold) measured in N did not explain the
variability of ∆V˙O2max and ∆Pmax during upper-body exercise (Table 3).This result was rather unexpected because most studies using leg exercise found a good correlation between V˙O2max in N and
∆V˙O2max [3, 8,14,15,17, 22] while only a few did not [5, 9]. Data analysis of studies showing good correlations between V˙O2max and
∆V˙O2max [15,17, 22] revealed a wide range of V˙O2max values as
trained and untrained subjects were involved in the same experiment. Obviously, a wide range in measured V˙O2max or ∆V˙O2max allows for easier detection of a relationship between the two variables. When the focus is on a sub-group of similarly (endurance)
trained subjects, as was the case in our study, a relationship between V˙O2max and ∆V˙O2max cannot be demonstrated in these studies. This fact challenges the explanatory power of V˙O2max measured in N on ∆V˙O2max for a homogeneous group of trained subjects.
To our knowledge the present study is the first investigating the
relation of ∆V˙O2max and ∆Pmax to muscle morphology. A novel
finding is that athletes with muscles adapted to endurance training (high capacity to supply and to utilise O2) exhibit higher decrements of Pmax in H during upper-body exercise. This was shown
by the correlations between ∆Pmax and muscle capillarity and
density of mitochondria of m. deltoideus, respectively (Fig. 1). It
is generally believed that peripheral (muscular) factors such as
perfusion, diffusion, and mitochondrial capacity modulate the
hypoxia-dependent decrease of V˙O2max and Pmax [3, 6, 21, 22,
24, 27], but so far no direct experimental evidence existed. Regression analysis displayed in Fig. 1 points to a significant or
nearly significant correlation between capillarity and ∆Pmax, and
between mitochondrial volume density and ∆Pmax, respectively.
Although this result is strongly influenced by the one single athlete displaying rather poor oxidative capacities of m. deltoideus,
˙O2max of upper-body exercise in acute hypoxia in
Fig. 1 ∆Pmax and ∆V
dependence of volume density of total mitochondria (Vv [mt, f]) and
of capillaries per fibre area (NA [c, f]).
Angermann M et al. Hypoxia in Nordic Combined Skiers … Int J Sports Med
Training & Testing
Finally, influences by the different test protocols for leg and
upper body exercise in our study must also be considered. Faster
increments in the workload during upper-body exercise may
have led to an extension in the anaerobic part of the exercise test,
thus influencing the relationship between ∆V˙O2max and ∆Pmax.
maximal power output is reduced while V˙O2max remains the
same.
5
his example supports the theory that well trained athletes become more sensitive to H compared to untrained subjects.
5
6
Some authors calculated the different contributions of the lung,
the circulatory system, and the muscles to the limitation of
V˙O2max [6, 27, 28]. They concluded that during exercise in H muscular factors become more important in limiting V˙O2max, when
small muscle groups are exercised or for well trained athletes
having a high V˙O2max.
7
8
9
Training & Testing
6
In contrast to ∆Pmax no correlations were found between ∆V˙O2max
and capillarity or mitochondrial density. This can partly be explained by the data structure of ∆V˙O2max and the small sample
size. We have to keep in mind that athletic performance is a complex output of interactions between different body functions.
From this systemic point of view, our study examined only a small
part of the system and when we interpret the results we have to
realize that there exists substantial individual variation in compensatory mechanisms, especially during exercise in hypoxia.
10
11
12
13
Conclusion
Maximal O2 uptake and maximal power output are affected differently by hypoxia. However, it remains an open issue to which
extent they are reduced at altitude. Our results question the
paradigm that the ability to tolerate hypoxia (altitude) depends
only on the athlete’s individuality and training status. The mode
of exercise has also to be taken into account. Furthermore our
findings expand the knowledge about the relation between peripheral factors and the hypoxia-dependent decrease of Pmax
and V˙O2max in trained athletes. The results provide evidence that
the impairment of exercise performance in acute hypoxia, corresponding to an altitude of 3200 m, is more pronounced in athletes with muscles well adapted to endurance training.
14
15
16
17
18
19
20
Acknowledgements
21
This study was funded by the Swiss Sports Commission (ESK).
We thank Christoph Lehmann for constructing the upper-body
ergometer, Franziska Graber for processing and analyzing the biopsies, and Ruth Vock and Silvia Schmutz for their assistance in
the preparation of the manuscript.
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