LA VENTANA DEL ENTRENADOR - ENE - RFEA.
Ergonomics,
Vol. 48, Nos. 11 – 14, 15 September – 15 November 2005, 1535 – 1546
The effects of intermittent hypoxic training
on aerobic and anaerobic performance
JAMES PETER MORTON* and NIGEL TIM CABLE
Research Institute for Sport and Exercise Sciences, Liverpool John Moores University,
15 – 21 Webster Street, Liverpool, L3 2ET, UK
The aim of the present study was to determine whether short-term
intermittent hypoxic training would enhance sea level aerobic and anaerobic
performance over and above that occurring with equivalent sea level training.
Over a 4-week period, two groups of eight moderately trained team sports
players performed 30 min of cycling exercise three times per week. One group
trained in normobaric hypoxia at a simulated altitude of 2750 m (FIO2=
0.15), the other group trained in a laboratory under sea level conditions. Each
training session consisted of ten 1-min bouts at 80% maximum workload
maintained for 2 min (Wmax) during the incremental exercise test at sea level
separated by 2-min active recovery at 50% Wmax. Training intensities were
increased by 5% after six training sessions and by a further 5% (of original
Wmax) after nine sessions. Pre-training assessments of VO2max, power output
at onset of 4 mM blood lactate accumulation (OBLA), Wmax and Wingate
anaerobic performance were performed on a cycle ergometer at sea level and
repeated 4 – 7 d following the training intervention. Following training there
were significant increases (p 5 0.01) in VO2max (7.2 vs. 8.0%), Wmax (15.5 vs.
17.8%), OBLA (11.1 vs. 11.9%), mean power (8.0 vs. 6.5%) and peak power
(2.9 vs. 9.3%) in both the hypoxic and normoxic groups respectively. There
were no significant differences between the increases in any of the abovementioned performance parameters in either training environment (p40.05).
In addition, neither haemoglobin concentration nor haematocrit were
significantly changed in either group (p40.05). It is concluded that acute
exposure of moderately trained subjects to normobaric hypoxia during a
short-term training programme consisting of moderate- to high-intensity
intermittent exercise has no enhanced effect on the degree of improvement in
either aerobic or anaerobic performance. These data suggest that if there are
any advantages to training in hypoxia for sea level performance, they would
not arise from the short-term protocol employed in the present study.
Keywords: Normobaric hypoxia; Altitude; WAnT; VO2max
*Corresponding author. Email: [email protected]
Ergonomics
ISSN 0014-0139 print/ISSN 1366-5847 online ª 2005 Taylor & Francis
http://www.tandf.co.uk/journals
DOI: 10.1080/00140130500100959
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J. P. Morton and N. T. Cable
1. Introduction
The concept of training at altitude in order to improve sea level performance is now an
established and highly researched area within the sport and exercise sciences. However,
despite approximately 30 years of research no unequivocal evidence exists to suggest that
any of the altitude training strategies (i.e. live high – train low, constant exposure or
intermittent hypoxic training (IHT)) can improve sea level performance over and above
that of equivalent sea level training.
One form of altitude training that has received recent attention, not only within the
literature (see table 1 for a summary of research findings) but also in a practical sports
setting (Cable 2000), is that of IHT. The strategy of IHT allows the athlete to effectively
‘live low – train high’, where brief periods of hypoxic exposure are interspersed with
prolonged sea level stays (Levine 2002). It is believed that the stress of hypoxic exposure,
in addition to training stress, will compound the training adaptations experienced
with normal endurance training, which, in turn, will lead to greater improvements in
performance (Wolski et al. 1996). The repeated transient reductions in PIO2 during
exercise may trigger various biochemical and structural changes to skeletal muscle that
favour oxidative processes (Terrados et al. 1990, Melissa et al. 1997, Geiser et al. 2001)
and the hypoxia per se may also induce the important haematological changes needed to
enhance oxygen transport in the blood (Rodriguez et al. 2000) ultimately leading to an
increase in VO2max.
In addition to the proposed benefits of IHT on aerobic performance is the hypothesis
that the combination of hypoxia with exercise could also prove to be beneficial for
Table 1. Effects of intermittent hypoxic training on endurance performance at sea level. The
findings compiled are taken from the last two decades of research.
Author (year)
Altitude (m)
Rodriguez et al. (1999)
Rodriguez et al. (2000)
Casas et al. (1998)
Terrados et al. (1988)
Terrados et al. (1990)
Meeuwsen et al. (2001)
4000–5000
4000
4000–5500
2300
2300
2500
Vallier et al. (1996)
Levine et al. (1990)
Levine et al. (1992)
Desplanches et al. (1993)
Engfred et al. (1994)
Favier et al. (1995)
Melissa et al. (1997)
Emonson et al. (1997)
Messonnier et al. (2001)
Masuda et al. (2001)
4000
2500
2500
4100–5700
2500
3345
3292
2500
4500
2500
Exposure
(days)
Sub-maximal
improvement
Potentiating Effects
9
Yes*
9
Yes*
18
Yes*
21–28
Yes*
16
Yes*
10
ND
Change in
VO2max (%)
Control
group
NS–
NS–
NS–
NS
ND
+7*
No
No
No
Yes
Yes
Yes
NS–
NS
NS
NS
NS
NS
NS
NS
ND
NS
No
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
No Potentiating Effects
21
28
35
21
25
42
24
15
24
28
ND
No
ND
ND
No
ND
ND
No
No
ND
*p 5 0.05.
ND=no data reported; NS–=not significantly different from pre-altitude value, p 4 0.05; NS=not
significantly different from control group, p 4 0.05.
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Hypoxic training
anaerobic performance (Martino et al. 1996, Saltin 1996, Wolski et al. 1996). These
claims have recently been supported by data from a well-designed, cross-over study
(Meeuwsen et al. 2001, Hendriksen and Meeuwsen 2003) indicating that moderate
intensity cycling exercise (2 h per d for 10 d) at an altitude of 2500 m significantly
improves mean power on a Wingate anaerobic test (WAnT) to a greater extent than that
observed with equivalent sea level training. This observation may be related to the
reported enhancement in gene expression of phosphofructokinase (PFK) after a period of
high-intensity hypoxic training (30 min per d, 5 d per week for 6 weeks) at an altitude of
3850 m (Vogt et al. 2001). Taken together, these data therefore suggest that moderate- to
high-intensity exercise in combination with hypoxia is a sufficient stimulus to improve sea
level anaerobic performance possibly via the mechanism of an increase in glycolytic flux.
These findings are of important significance for those athletes involved in team sport
games of an intermittent nature (e.g. soccer, rugby, netball) where the activity profiles are
characterized by a number of higher-intensity anaerobic efforts superimposed (workloads
greater than the ‘anaerobic threshold’) on a larger background of aerobic activity
(workloads below the ‘anaerobic threshold’). With this in mind, the aim of the present
study was to determine the efficacy of short-term IHT (4 weeks) on both sea level aerobic
and anaerobic performance in moderately trained team sports players. A short-term
training protocol consisting of moderate- to high-intensity intermittent exercise was
chosen as the training stimulus in an attempt to mirror applied practice that is currently
found in pre-season training programmes.
2. Methodology
2.1. Subjects
Sixteen male, moderately trained team sports players, born and living at sea level,
volunteered for the study. Although all subjects were physically active none had
undergone any previous cycle endurance training. Before giving their written consent to
participate, they were informed of the nature and purpose of the study and made aware
of any potential risks involved. The study was approved by the Ethics Committee of
Liverpool John Moores University. All subjects were non-smokers and none was under
any pharmacological or special dietetic treatment during the study. They all maintained
their regular diet throughout the study period. Subjects’ physical characteristics
(mean + SD) are shown in table 2.
Table 2. Pre-training characteristics of the sea level and hypoxic training groups.
Age (years)
Height (m)
Body mass (kg)
Haemoglobin (g/dl)
Haematocrit (%)
VO2max (ml.kg71.min71)
Wmax (watts)
OBLA (watts)
Peak power (watts)
Mean power (watts)
Sea level
Hypoxic
20.1 + 0.6
1.76 + 0.3
75.2 + 4.9
14.3 + 1.2
43.9 + 3.5
53.5 + 5.4
295 + 52
199 + 31*
729 + 95*
579 + 61
20.9 + 0.8
1.79 + 0.3
83.9 + 12.5
15.4 + 1.1
44.9 + 2.7
51.2 + 9.4
314 + 41
230 + 23
872 + 147
625 + 61
*Significant difference between groups, p 5 0.05.
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2.2. Design
Subjects were divided into two groups matched for initial physical fitness as indicated by
both aerobic and anaerobic performance parameters. Eight subjects were assigned to a
hypoxic training group (HT) and trained in a normobaric hypoxic chamber at a
simulated altitude of approximately 2750 m. The remaining eight subjects were assigned
to a sea level training group (SLT) and performed the same training protocol in the
laboratory at sea level conditions. All subjects lived at sea level during the study. Before
and after the training period, performance at sea level was evaluated in the laboratory by
means of an incremental test until exhaustion (during which exercise blood lactate
concentration was measured) and a WAnT. Resting haemoglobin concentration and
haematocrit were also measured pre- and post-training. Several weeks before the main
study all subjects performed two familiarization trials (separated by at least 48 h)
encompassing a WAnT and a VO2max protocol.
2.3. Test protocol
Between 4 and 7 d pre- and post-training, subjects performed an incremental test
until exhaustion on an electrodynamically braked (Cybex, Sweden) and a WAnT on a
mechanically braked (834E, Monark, Sweden) cycle ergometer in the laboratory at sea
level conditions. During familiarization, the subjects’ preferred ergometer saddle height
and handle bar position were recorded and these positions maintained for all exercise
tests. The WAnT was always performed first followed by the incremental test until
exhaustion after a break of at least 24 h. Subjects abstained from caffeine and alcohol
intake for at least 24 h prior to any of the exercise tests. Each subject completed pre- and
post-tests at approximately the same time of day so as to eliminate any diurnal variation
in the performance variables measured (Reilly and Brooks 1986).
The WAnT is the most widely used anaerobic performance test (Inbar et al. 1996) and
was recently confirmed as a valid means to assess anaerobic performance (Beneke et al.
2002). After a ‘warm-up’ period of 5 min pedalling against light resistance (50 W),
interspersed with three ‘all-out sprints’ each lasting 4 – 8 s, the subjects pedalled at
maximal speed for 30 s against a constant resistance. The resistance, corresponding to
7.5% of the subject’s body mass, was applied after an initial acceleration phase lasting
3 s. Peak power and mean power in both absolute (W) and relative values (W.kg71) were
measured. Peak power was defined as the highest mechanical power elicited during the
test, which typically occurred during the first 5 s segment. Mean power was defined as the
average power sustained throughout the 30 s period.
The incremental exercise test began with a 3-min warm-up period at a workload of
100 W followed by increments of 30 W at 2-min intervals until exhaustion. Exhaustion
was defined as the point at which the subjects could no longer maintain the requested
pedalling frequency of 70 rev.min71 despite strong verbal encouragement. The highest
work intensity that could be performed for 2 min during the test was called Wmax and was
used in the calculation of relative workloads for the training programme. Capillary blood
samples were collected from the fingertip prior to exercise and during 20-s rest periods
between each increment, for the determination of blood lactate concentration. The power
output corresponding to a 4 mM blood lactate concentration (i.e. OBLA) was taken to be
an indicator of lactate threshold so as to compare with previous studies that also used the
same methodological approach (e.g. Terrados et al. 1988, Messonnier et al. 2001).
Resting haemoglobin concentration and haematocrit were also determined prior to
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exercise. Oxygen uptake (VO2) during exercise was measured by collecting expired air in
Douglas bags during the last minute of each exercise stage. Oxygen and carbon dioxide
content were assessed using a gas analyser (Servomex 1440, Sussex, England) after
calibration with known reference gases and expired ventilatory volume was determined
using a Harvard dry gas meter. Oxygen uptake was calculated and expressed in both
absolute (l.min71) and relative (ml.kg71.min71) values.
2.4. Training programme
The training programme consisted of 30 min of cycling exercise occurring three times per
week for 4 weeks. All subjects exercised on the same mechanically braked cycle ergometer
model (818E, Monark, Sweden). The HT group trained in a normobaric hypoxic
chamber (Edge 4 Health Systems, Kent, UK) at a simulated altitude that was held at
approximately 2750 m (FIO2&0.15) and had an air refreshment rate of 1000 l.min71. The
SLT group performed the same training protocol in the laboratory at sea level conditions.
The temperature in both the laboratory and hypoxic chamber throughout training was
approximately 218C.
Each training session consisted of ten 1-min bouts at 80% Wmax separated by 2-min active
recovery at 50% Wmax. The individual training intensities were increased by 5% after six
training sessions and by a further 5% (of original Wmax) after nine training sessions. The
intermittent nature of the training programme enabled individual subjects to exercise at
intensities above (110 – 130% of pre-training OBLA) and below (70 – 90% of pre-training
OBLA) the lactate threshold during the 4-week period. The training protocol was therefore
considered to consist of moderate- to high-intensity exercise. Both groups trained at the
same absolute intensity throughout the study. Subjects were given unrestricted access to
water intake throughout training. The subjects wore a heart rate monitor (Polar, Kempele,
Finland) during all training sessions and were asked to communicate heart rate every 5 min
during exercise as a check for comparison between training conditions.
2.5. Blood analyses
All samples were collected from fingertip capillary blood. The finger was warmed and
wiped with a Mediswab, the first drop of blood was discarded and the required amount
was then collected. Haemoglobin concentration was determined by placing a droplet of
whole blood in a hemocue and placing it in the Hemocue reader (Hemocue, Drumfield,
UK). Haemoglobin was automatically determined and expressed in g.dl71. To assess
haematocrit, 100 ml of whole blood was collected in a heparinized glass capillary tube. The
tube was sealed at one end with critoseal and spun in a Hettich centrifuge (Tuttlingen,
Germany) at 1500 rev.min71 5 min. Upon completion, the sample was removed and
assessed using a Hawksley haematocrit reader for the determination of cellular volume
and plasma volume. Data were expressed as a percentage of cell to total volume. To assess
lactate concentration, 30 ml of whole blood was collected in a heparinized glass capillary
tube and lactate was automatically expressed in mM using an Analox GM7 automatic
analyser (Analox Instruments, London, UK). All samples were analysed in duplicate.
2.6. Statistical analysis
All statistical tests were conducted using SPSS for Windows (version 11) computer
software. Students t-tests for independent samples were used to compare baseline
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characteristics of both training groups and average heart rates measured during each
week of training. A two-way repeated measures ANOVA (with main effects of time (prevs. post-training) and training environment (hypoxic vs. normoxic)) was used to examine
changes in physiological and performance variables. All data are expressed as means
(+ SD) with p values of less than 0.05 (*) and 0.01 (**) assumed to indicate statistical
significance.
3. Results
3.1. Baseline characteristics
With the exception of peak power on the WAnT and the work intensity corresponding to
OBLA, there were no significant differences between baseline characteristics of the HT
and SLT groups (table 2).
3.2. Aerobic performance
Maximal oxygen uptake was significantly increased (p 5 0.01) in both groups following
training (figure 1A). In the HT group, the increase in VO2max was 7.2% with pre-training
values increasing from 51.2 + 9.4 to 54.9 + 7.5 ml.kg71.min71. The SLT group showed
an 8% increase in VO2max with pre-training values increasing from 53.5 + 5.4 to
57.8 + 5.5 ml.kg71.min71. There was no significant difference in the improvement in VO2max
between the two groups regardless of whether VO2 was expressed in ml.kg71.min71
(F1,14 = 0.14, p = 0.71) or in l.min71 (F1,14 = 0.66, p = 0.43). Maximal power output during
the incremental exercise test (i.e. Wmax) was also significantly increased (p 5 0.01) in both
groups following training (figure 1B). The mean increase in the HT group was 15.5% (pretraining: 313.8 + 40.7, post-training: 362.5 + 38.5 W) and the increase in the SLT group was
17.8% (pre-training: 295 + 51, post-training: 347.5 + 41.8 W). The improvement in Wmax did
not differ between groups (F1,14 = 0.16, p = 0.69).
3.3. Blood lactate responses
The work intensity corresponding to a 4 mmol.l71 blood lactate concentration was
significantly increased (p 5 0.01) in both groups following training (figure 1C). In the
SLT group, the observed increase was 11.9%, with pre-training values increasing from
199 + 31 to 223 + 32 W. The HT group showed a similar increase of 11.1% with pretraining values increasing from 230 + 23 to 258 + 33 W. The improvement in OBLA did
not differ between groups (F1,14 = 0.47, p = 0.50).
3.4. Anaerobic performance
Performance scores on the WAnT of the HT and SLT groups are presented in table 3.
Both groups showed significant increases (p 5 0.05) in both absolute (SLT: 8.5%; HT:
2.1%) and relative peak power (SLT: 9.3%; HT: 2.9%). Differences in the improvements
in peak power, however, just failed to achieve significance between groups when expressed
in either absolute (F1,14 = 4.2, p = 0.06) or relative values (F1,14 = 4.43, p = 0.054). Both
groups also demonstrated significant increases (p 5 0.01) in both absolute (SLT: 6.1%;
HT: 6.5%) and relative mean power (SLT: 6.5%; HT: 8.0%). The improvement in mean
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Figure 1. (A), VO2max of the sea level and hypoxic training groups before and after
training. (B), Maximal power output, during the incremental exercise test, of the sea level
and hypoxic training groups before and after training. (C), Power output of the sea level
and hypoxic groups at a 4 mmol.l71 blood lactate concentration before and after
training. ** denotes significant difference (p 5 0.01) between pre- and post-training
values.
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Table 3. Performance scores on the Wingate anaerobic test of the sea level and hypoxic
training groups pre- and post-training.
Sea level
Hypoxic
Pre-
Post-
% increase
Pre-
Post-
% increase
Peak power
absolute (W)
729 + 95
791 + 67*
8.5
872 + 147
882 + 103*
2.1
Peak power
relative (W.kg71)
9.7 + 1.1
10.6 + 0.6*
9.3
10.4 + 1.1
10.7 + 1.1*
2.9
Mean power
absolute (W)
579 + 61
614 + 50**
6.1
625 + 61
666 + 75**
6.5
Mean power
relative (W.kg71)
7.7 + 0.5
8.2 + 0.6**
6.5
7.5 + 0.9
8.1 + 1.1**
8.0
*Significant difference between pre- and post-training values, p 5 0.05.
**Significant difference between pre- and post-training values, p 5 0.01.
power did not differ between groups regardless of whether mean power was expressed in
absolute (F1,14 = 0.208, p = 0.66) or relative values (F1,14 = 0.85, p = 0.78).
3.5. Haemoglobin and haematocrit
Neither haemoglobin concentration nor haematocrit was significantly changed in either
the HT or SLT groups following the training programme (table 4).
3.6. Training conditions
Although both groups performed the same training schedule in terms of absolute work
rates, the HT group worked significantly harder than the SLT group in terms of relative
workloads. Average heart rates measured during each week of training were significantly
different (p 5 0.05) between training conditions (table 5).
4. Discussion
The aim of the present study was to determine whether short-term IHT would enhance
sea level aerobic and anaerobic performance over and above that occurring with
equivalent sea level training. It was demonstrated that 4 weeks of moderate- to highintensity IHT (i.e. intensities corresponding to 70 – 90% and 110 – 130% of lactate
threshold respectively) in moderately trained subjects resulted in similar increases in
aerobic and anaerobic performance when compared to equivalent sea level training.
Specifically, VO2max, Wmax, OBLA, mean power and peak power displayed similar
increases in response to hypoxic and sea level training. To the authors’ knowledge, this is
the first study to investigate the efficacy of IHT on aerobic and anaerobic performance
parameters using a training protocol consisting of moderate- to high-intensity
intermittent exercise.
The increase in VO2max and Wmax arising from training was not enhanced by acute
exposure to normobaric hypoxia, in agreement with previous studies (e.g. Terrados et al.
1988, Levine et al. 1992, Engfred et al. 1994, Emonson et al. 1997, Geiser et al. 2001,
Masuda et al. 2001). Of the previously cited research, Levine et al. (1992), Engfred
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Table 4. Haematocrit and haemoglobin concentration of the sea level and hypoxic training
groups pre- and post-training.
Sea level
Haematocrit (%)
Haemoglobin (g.dl71)
Hypoxic
Pre-
Post-
Pre-
Post-
43.9 + 3.5
14.3 + 1.2
44.0 + 2.7
14.5 + 1.2
44.9 + 2.7
15.4 + 1.1
44.8 + 2.9
15.3 + 1.6
Table 5. Heart rates of the sea level and hypoxic training groups during each week of training.
Week 1
Week 2
Week 3
Week 4
Heart rate (beats.min71)
Sea level
165 + 10
Hypoxic
177 + 8*
161 + 8
172 + 8*
160 + 10
172 + 8*
163 + 8
174 + 8*
*Significant difference between conditions, p 5 0.05.
et al. (1994) and Geiser et al. (2001) used protocols that were most similar to that of
the present design, where training was performed at the same absolute intensity
throughout. It therefore appears that repeated short-term exposures to hypoxia during
intense physical training does not significantly contribute to the mechanisms responsible for the improvements in aerobic performance observed with sea level endurance
training.
In terms of sea level aerobic performance, it is widely accepted that the most important
physiological adaptation to a reduced PIO2 is the increased renal release of erythropoetin
(EPO), which causes a transient increase in red cell volume (Bailey and Davies 1997).
However, the present short-term protocol (three 30-min sessions per week for 4 weeks) did
not significantly alter haemoglobin concentration or haematocrit in either the hypoxia or
the sea level training groups. This finding is in agreement with the earlier research of
Levine et al. (1992), Engfred et al. (1994) and Emonson et al. (1997), who with similar
protocols also concluded that short-term intermittent exposure to hypoxia for approximately 1 h per d, 3 – 5 times per week for 4 – 5 weeks does not result in acclimatization.
This assertion is consistent with the findings that at least 1.5 h of hypoxic exposure is
needed to increase EPO levels significantly (Eckardt et al. 1989, Knaupp et al. 1992,
Rodriguez et al. 2000).
Although the absence of significant changes in haemoglobin and haematocrit in the
present study have been attributed to the short duration of each hypoxic exposure, it is
important to consider that other IHT investigations (e.g. Terrados et al. 1988) have also
reported no significant changes in haematological variables despite significantly longer
exposures to hypoxia. The hypothesis that has been suggested for the apparent absence of
haematological adaptations after intense hypoxic training relies on the fact that EPO
secretion is inhibited by the metabolic acidosis caused by peak physical work (Eckardt
et al. 1990, Schmidt et al. 1991). The proposed mechanism for this inhibition is a right
shift in the oxygen dissociation curve during maximal exercise caused by the Bohr effect.
This leads to increased capillary oxygen tensions, which in combination with higher
haemoglobin concentrations caused by the slight haemoconcentration observed with
altitude ascent, could preserve the kidney from low oxygen tensions (Schmidt et al. 1991).
In more recent IHT investigations (Vallier et al. 1996) this mechanism has also been put
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J. P. Morton and N. T. Cable
forward as a feasible explanation for the lack of erythropoietic response during and after
a period of hypoxic training.
The present results disagree with Meeuwsen et al. (2001), where only hypoxic training
induced improvements in maximal oxygen uptake. Given that no haematological changes
occurred in the previous study, the researchers speculated that the increase in VO2max may
be related to the increase in muscle oxidative enzyme levels previously observed by Terrados
et al. (1990) and Melissa et al. (1997). It remains to be proven that this is a valid explanation,
considering that the authors did not quantify skeletal muscle enzymes in their study. An
alternative explanation for the discrepancy between the present results and those of
Meeuwsen et al. (2001) is the notion that the longer exposures to hypoxia in the previous
study may have resulted in greater increases in maximal ventilation caused by a possible
training effect of the respiratory muscles due to the marked hyperventilation associated with
exercise at high altitudes (Wolski et al. 1996, Boning 1997). Indeed, in a recent investigation
by Borisch et al. (2003), this mechanism was also proposed to explain increases in maximal
ventilation and VO2max after 4 weeks of strength endurance training in hypoxia.
The present data do not support the claim that hypoxic exercise is potentially
advantageous for sea level anaerobic performance (Martino et al. 1996; Saltin 1996,
Wolski et al. 1996). These findings disagree with the recent research of Meeuwsen et al.
(2001) and Hendriksen and Meeuwsen (2003), where only hypoxic training induced
significant improvements in anaerobic performance parameters, also determined via a
WAnT. Although the previous authors failed to propose a clear mechanism for the
increased performance, such an improvement may be related to increases in muscle
buffering capacity and in activity of glycolytic enzymes observed previously by Mizuno
et al. (1990) and Vogt et al. (2001) respectively. The latter factor may indeed be of great
significance, considering that the glycolytic metabolic pathway is heavily stressed during
the WAnT (Beneke et al. 2002).
At the cellular level, adaptation to hypoxia is brought about by activation of a
transcriptional factor, hypoxia-inducible factor 1 (HIF-1). Transactivation of HIF-1 is
necessary for the induction of several genes, such as those encoding EPO, glucose
transporter 1 and several glycolytic enzymes (Wenger and Gassmann 1997). Vogt et al.
(2001) found greater improvements in gene expression of PFK and citrate synthase after
6 weeks of high intensity training at an altitude of 3850 m than when compared to
equivalent sea level training. It was therefore concluded that training under hypoxic
conditions elicits specific effects at the molecular level of human skeletal muscle to a
greater extent than when compared to training under normoxic conditions. If an increase
in PFK activity is a feasible explanation for the improved anaerobic performance
observed by Meeuwsen et al. (2001) and Hendriksen and Meeuwsen (2003) then why was
no such performance increase demonstrated in the present study given that high intensity
training under hypoxic conditions appears to be a prerequisite for improving glycolytic
flux? It is possible that the present protocol may not have been sufficient in terms of
intensity or duration to induce an increase in transcription sufficient to generate the
molecular adaptations needed to increase energy efficiency. It is indeed worth noting that
the total hypoxic exposure time studied by Vogt et al. (2001), Meeuwsen et al. (2001) and
Hendriksen and Meeuwsen (2003) was 15 – 20 h, whereas the total exposure time in the
present study was only 6 h.
The present data therefore suggest that if there is any potential advantage to training in
hypoxia for sea level anaerobic performance, it does not come from repeated short-term
exposures. It is thus recommended that if inducing cellular adaptations and improving
anaerobic performance is the specific goal of any IHT programme, that hypoxia be
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Hypoxic training
1545
provided during high intensity exercise in repeated exposures that accumulate to at least
20 h total exposure time. Employing such a protocol is more likely to elicit the molecular
mechanisms (i.e. activation of HIF-1) needed to improve the structural and biochemical
properties of human skeletal muscle.
5. Conclusions
It is concluded that short-term moderate- to high-intensity IHT performed 3 times/week
for 4 weeks in moderately trained subjects resulted in similar increases in aerobic and
anaerobic performance to those occurring with equivalent normoxic training. This is the
case, even when training in hypoxia can be accomplished at the same absolute intensity as
sea level controls. The present data suggest that if there are any advantages to training in
hypoxia for sea level performance they would not arise from the short-term training
protocol used in the present study. Future studies should subject individuals to longer
exposures to hypoxia (during high-intensity exercise) as these are more likely to elicit the
molecular mechanisms needed to enhance the oxygen-carrying capacity of the blood,
improve muscle metabolism and enhance performance. Particular attention should be
given to local structural, biochemical and molecular adaptations occurring in human
skeletal muscle after a period of hypoxic training and examine whether such changes are
actually recognized at the global level.
References
BAILEY, D.M. and DAVIES, B., 1997, Physiological implications of altitude training for endurance performance at
sea level: a review. British Journal of Sports Medicine, 31, 183 – 190.
BENEKE, R., POLLMANN, C., BLEIF, I., LEITHAUSER, R.M. and HUTLER, M., 2002, How anaerobic is the Wingate
anaerobic test for humans? European Journal of Applied Physiology, 87, 388 – 392.
BONING, D., 1997, Altitude and hypoxia training – a short review. International Journal of Sports Medicine, 18,
565 – 570.
BORISCH, S., BARTSCH P. and FRIEDMANN, B., 2003, Effects of strength endurance training in hypoxia on
endurance capacity, blood volume and erythropoietin. International Journal of Sports Medicine, 22,
(abstract) S81.
CABLE, T., 2000, Improving performance with hypoxic training. Insight, The FA Coaches Journal, 3, 14 – 16.
CASAS, M., CASAS, H., IBANEZ, J., PAGES, T., PALACIOS, L., RICART, A., VENTURA, J.L., VISCOR G. and
RODRIGUEZ, F.A., 1998, Short-term intermittent exposure to hypobaric hypoxia and exercise induces
haematological adaptations and acclimation. Journal of Sports Sciences, 16, 450 – 451.
CLANTON, T.L. and KLAWITTER, P.F., 2001, Adaptive responses of skeletal muscles to intermittent hypoxia: the
known and the unknown. Journal of Applied Physiology, 90, 2476 – 2487.
DESPLANCHES, D., HOPPELER, H., LINOSSIER, M.T., DERIS, C., CLASSEN, H., DORMOIS, D., LACOUR, J.-R. and
GREYSSANT, A., 1993, Effects of training in normoxia and normobaric hypoxia on human muscle
ultrastructure. European Journal of Physiology, 425, 263 – 267.
ECKARDT, K.U., BOUTELLIER, U., KURTZ, A., SCHOPEN, M., KOLLER, E.A. and BLAUER, C., 1989, Rate of
erythropoietin formation in humans in response to acute hypobaric hypoxia. Journal of Applied Physiology,
66, 1785 – 1788.
ECKARDT, K.U., KURTZ, A. and BLAUER, C., 1990, Triggering of erythropoietin production is inhibited by
respiratory and metabolic acidosis. American Journal of Physiology, 258, R678 – R683.
EMONSON, D.L., AMINUDDIN, A.H., WRIGHT, R.L., SCROOP, G.C. and GORE, C.J., 1997, Training induced
increases in sea level VO2max and endurance are not enhanced by acute hypobaric exposure. European Journal
of Applied Physiology, 76, 8 – 12.
ENGFRED, K., KJAER, M., SECHER, N.H., FRIEDMANN, D.B., HANEL, B., NIELSEN, O.J., BACH, F.W., GALBO, H. and
LEVINE, B.D., 1994, Hypoxia and training induced adaptation of hormonal responses to exercise in humans.
European Journal of Applied Physiology, 68, 303 – 309.
FAVIER, R., SPIELVOGEL, D., DESPLANCHES, D., FERRETI, G., KAYSER, B. and GRUNENFELDER, A., 1995, Training in
hypoxia versus training in normoxia in high altitude natives. Journal of Applied Physiology, 78, 2286 – 2293.
DOCUMENTO DE INTRANET. PROHIBIDA SU PUBLICACION.
LA VENTANA DEL ENTRENADOR - ENE - RFEA.
1546
J. P. Morton and N. T. Cable
GEISER, J., VOGT, M., BILLETER, R., ZULEGER, C., BELFORTI, F. and HOPPELER, H., 2001, Training high–living low:
changes of aerobic performance and muscle structure with training at simulated altitude. International Journal
of Sports Medicine, 22, 579 – 585.
HENDRIKSEN, I.J.M. and MEEUWSEN, T., 2003, The effect of intermittent training in hypobaric hypoxia on sea
level exercise: a cross-over study in humans. European Journal of Applied Physiology, 88, 396 – 403.
INBAR, O., BAR-OR, O. and SKINNER, J.S., 1996, The Wingate Anaerobic Test (Champaign, IL: Human Kinetics).
KNAUPP, W., KHILNANI, S. and SHERWOOD, J., 1992, Erythropoietin response to acute normobaric hypoxia in
humans. Journal of Applied Physiology, 73, 837 – 840.
LEVINE, B.D., 2002, Intermittent hypoxic training: fact and fancy. High Altitude Medicine and Biology, 3,
177 – 193.
LEVINE, B.D., ENGFRED, K., FRIEDMANN, D.B., KJAER, M., SALTIN, B., CLIFFORD, P.S. and SECHER, N.H., 1990,
High altitude endurance training: effect on aerobic capacity and work performance. Medicine and Science in
Sports and Exercise, 22, (abstract) 209.
LEVINE, B.D., FRIEDMANN, D.B., ENGFRED K., HANEL, B., KJAER, M., CLIFFORD, P.S. and SECHER, N.H., 1992,
The effect of normoxic or hypobaric hypoxic endurance training on the hypoxic ventilatory response.
Medicine and Science in Sports and Exercise, 24, 769 – 775.
MARTINO, M., MYERS, K. and BISHOP, P., 1996, Effects of 21 days training at altitude on sea-level anaerobic
performance in competitive swimmers. Medicine and Science in Sports and Exercise, 27, S5 (abstract 37).
MASUDA, K., OKAZAKI, K., KUNO, S., ASANO, K., SHIMOJO, H. and KATSUTA, S., 2001, Endurance training under
2500 m hypoxia does not increase myoglobin content in human skeletal muscle. European Journal of Applied
Physiology, 85, 486 – 490.
MEEUWSEN, T., INGRID, J.M.H. and HOLEWIJN, M., 2001, Training induced increases in sea-level performance are
enhanced by acute intermittent hypobaric hypoxia. European Journal of Applied Physiology, 84, 283 – 290.
MELISSA, L., MACDOUGALL, J.D., TARNOPOLSKY, M.A., CIPRIANO, N. and GREEN, H.J., 1997, Skeletal muscle
adaptations to training under normobaric hypoxia versus normoxic conditions. Medicine and Science in
Sports and Exercise, 29, 238 – 243.
MESSONNIER, L., FREUND, H., FEASSON, L., PRIER, F., CASTELLS, J., DENIS, C., LINOSSIER, M.T., GEYSSANT, A. and
LACOUR, J.R., 2001, Blood lactate exchange and removal abilities after relative high intensity exercise: effects
of training in normoxia and hypoxia. European Journal of Applied Physiology, 84, 403 – 412.
MIZUNO, M., JUEL, C., BRO-RASMUSSEN, T., MYGIND, E., SCHIBYE, B., RASMUSSEN, B. and SALTIN, B., 1990, Limb
skeletal muscle adaptation in athletes after training at altitude. Journal of Applied Physiology, 68, 496 – 502.
REILLY, T. and BROOKS, G.A., 1986, Exercise and the circadian variation in body temperature measures.
International Journal of Sports Medicine, 7, 358 – 362.
RODRIGUEZ, F.A., CASAS, H., CASAS, M., PAGES, T., RAMA, R., RICART, A., VENTURA, J.L., IBANEZ, J. and
VISCOR, G., 1999, Intermittent hyopbaric hypoxia stimulates erythropoiesis and improves aerobic capacity.
Medicine and Science in Sports and Exercise, 31, 264 – 268.
RODRIGUEZ, F.A., VENTURA, J.L., CASAS, M., RAMA, R. and VISCOR, J.L., 2000, Erythropoietin acute reaction and
haematological adaptations to short, intermittent hypobaric hypoxia. European Journal of Applied Physiology,
82, 170 – 177.
SALTIN, B., 1996, Exercise and the environment: focus on altitude. Research Quarterly for Exercise and Sport, 67,
1 – 10.
SCHMIDT, W., ECKARDT, K.U., HILGENDORF, A., STRAUCH, S. and BLAUER, C., 1991, Effects of maximal and submaximal exercise under normoxic and hypoxic conditions on serum erythropoietin levels. International
Journal of Sports Medicine, 12, 457 – 461.
TERRADOS, N., JANSSON, E., SYLVEN, C. and KAIJSER, L., 1990, Is hypoxia a stimulus for synthesis of oxidative
enzymes and myoglobin? Journal of Applied Physiology, 68, 2369 – 2372.
TERRADOS, N., MELICHNA, J., SYLVEN, C., JANSSON, E. and KAIJSER, L., 1988, Effects of training at simulated
altitude on performance and muscle metabolic capacity in competitive road cyclists. European Journal of
Applied Physiology, 57, 203 – 209.
VALLIER, J.M., CHATEAU, P. and GUEZENNEC, C.Y., 1996, Effects of physical training in a hypobaric chamber on
the physical performance of competitive triathletes. European Journal of Applied Physiology, 73, 471 – 478.
VOGT, M., PUNTSCHART, A., GEISER, J., ZULEGER, C., BILLETER, R. and HOPPELLER, H., 2001, Molecular
adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. Journal of
Applied Physiology, 91, 173 – 182.
WENGER, R.H. and GASSMANN, M., 1997, Oxygen(es) and the hypoxia inducible factor-1. Biology and Chemistry,
378, 609 – 616.
WOLSKI, L.A., MCKENZIE, D.C. and WENGER, H.A., 1996, Altitude training for improvements in sea level
performance: is there scientific evidence of benefit? Sports Medicine, 22, 251 – 263.
DOCUMENTO DE INTRANET. PROHIBIDA SU PUBLICACION.
LA VENTANA DEL ENTRENADOR - ENE - RFEA.
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