Journal of Science and Medicine in Sport (2009) 12, 6772

Improved running economy and increased

hemoglobin mass in elite runners after extended
moderate altitude exposure
P.U. Saunders
a,
, R.D. Telford
b
, D.B. Pyne
a,b
, A.G. Hahn
a
, C.J. Gore
a,c
a
Department of Physiology, Australian Institute of Sport, Australia
b
Medical School, Australian National University, Australia
c
School of Education, Flinders University, Australia
Received 18 January 2007; received in revised form 17 August 2007; accepted 18 August 2007
KEYWORDS
Hypoxia;
Red blood cells;
and Elite athletes
Summary There is conicting evidence whether hypoxia improves running econ-
omy (RE), maximal O
2
uptake (

V
O
2 max
), haemoglobin mass (Hb
mass
) and performance,
and what total accumulated dose is necessary for effective adaptation. The aim of
this study was to determine the effect of an extended hypoxic exposure on these
physiological and performance measures. Nine elite middle distance runners were
randomly assigned to a live hightrain low simulated altitude group (ALT) and spent
46 8 nights (mean S.D.) at 2860 41 m. A matched control group (CON, n = 9)
lived and trained near sea level (600 m). ALT decreased submaximal

V
O
2
(L min
1
)
(3.2%, 90% condence intervals, 1.0% to 5.2%, p= 0.02), increased Hb
mass
(4.9%,
2.37.6%, p= 0.01), decreased submaximal heart rate (3.1%, 1.8% to 4.4%,
p= 0.00) and had a trivial increase in

V
O
2 max
(1.5%, 1.6 to 4.8; p= 0.41) compared
with CON. There was a trivial correlation between change in Hb
mass
and change
in

V
O
2 max
(r = 0.04, p= 0.93). Hypoxic exposure of 400 h was sufcient to improve
Hb
mass
, a response not observed with shorter exposures. Although total O
2
carry-
ing capacity was improved, the mechanism(s) to explain the lack of proportionate
increase in

V
O
2 max
were not identied.
2007 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
Introduction
There remains controversy about the magnitudes
of change in maximal oxygen uptake (

V
O
2 max
),
haemoglobin mass (Hb
mass
) and exercise economy
after altitude exposure in trained athletes.
1
Our

Corresponding author.
E-mail address: philo.saunders@ausport.gov.au
(P.U. Saunders).
laboratory has demonstrated a 3.3% improvement
in running economy (RE) after 20 days moder-
ate simulated live hightrain low (LHTL) altitude
exposure in elite distance runners.
2
We have also
consistently demonstrated only trivial changes in
Hb
mass
after various altitude interventions in elite
runners and cyclists of durations of 1231 days
27
; in contrast with reports of 59% increases in
red cell mass after altitude training in endurance
athletes.
811
Those studies nding little change in
1440-2440/$ see front matter 2007 Sports Medicine Australia. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jsams.2007.08.014
68 P.U. Saunders et al.
Hb
mass
after altitude exposure could be explained
by either an insufcient altitude (<20002200 m)
and/or an inadequate time at altitude (<34 weeks
for >12 h day
1
).
12
Several studies have demonstrated improved
exercise economy after altitude acclimati-
zation,
2,7,1318
although this is strongly contested
by others.
19
With the association between RE
and performance well documented,
20
the ability
to improve RE after altitude training is likely
to lead to signicant improvements in running
performance. The present study aimed to test
the hypothesis that a total of 400 h (50 days
of 9 h d
1
) of LHTL simulated altitude exposure
would enhance RE, Hb
mass
and

V
O
2 max
over and
above that occurring with a similar exposure to
a normoxic environment and to a greater extent
than previously documented after exposures of a
shorter duration.
Methods
Eighteen elite middle distance runners participated
in this study with over half (n = 10) representing Aus-
tralia at major international competitions (Table 1).
Participants were informed of the experimental
procedures and possible risks involved with par-
ticipation before written consent was obtained.
The Ethics Committee at the Australian Institute of
Sport approved all testing procedures.
Nine runners were randomly assigned to the LHTL
simulated altitude group (ALT), consisting of 46 8
nights (415 75 h) at 2860 41 m altitude; where
values are mean standard deviation. During the
12-week period participants spent 5 days each week
(9 h d
1
) in a normobaric hypoxic chamber and 2
days each week at the ambient altitude (600 m).
The control group (CON) consisted of nine runners
who lived and trained at the same location (600 m
altitude) as ALT. The study was conducted during
2 6 month periods in consecutive years because
of the limited space in the hypoxic chamber. Four
participants in both the ALT and CON groups were
tested in the rst year and ve in the second
year. Prior to and within 2 days of completion of
the intervention all participants performed testing
under normoxic conditions in Canberra, Australia
(600 m).
RE was determined from submaximal oxygen
consumption (

V
O
2
) for 4 min at constant running
speeds of 14, 16 and 18 kmh
1
on a custom-built
motorised treadmill. Ventilation (

V
E
), respiratory
exchange ratio, heart rate (HR) and blood lactate
concentration [Lac-] were also measured. RE was
dened as the

V
O
2
during the last 60 s of each 4 min
stage.

V
O
2 max
was measured during an incremental
test to volitional exhaustion performed 2 min after
the third submaximal effort. The treadmill and
gas analysis procedures have been fully described
previously.
21
The typical error of measurement (TE)
established from pre- and post-tests on the CON
participants in the current study were 1.8% for sub-
maximal

V
O
2
and 2.4% for

V
O
2 max
.
Before and after the 3 months experimen-
tal period, participants underwent measurement
of total Hb
mass
using the carbon monoxide re-
breathing technique that we have described
previously.
2
The TE for Hb
mass
from pre- and post-
tests on the CON participants in the current study
was 1.2% when using capillary blood samples.
Data were analysed in a spreadsheet for
randomized controlled trials (www.sportsci.
org/resource/stats) using unpaired t-tests with
the natural logarithm of dependent variables
used to reduce non-uniformity of error. Statistical
signicance was accepted at p< 0.05. Measures of
centrality and spread are shown as mean standard
deviation. RE was analysed as pooled values of
the three running speeds because differences
from pre- to post-treatment were independent
of speed. The magnitude of differences between
change scores (pre versus post) was expressed as
the effect of ALT compared to CON with the mean
percentage change 90% condence intervals. The
percentage likelihood are expressed qualitatively
(<1%, almost certainly not; <5%, very unlikely;
<25%, unlikely or probably not; <50%, possibly not;
>50%, possibly; >75%, likely or probable; >95%, very
likely; >99%, almost certain) based on previous
recommendations.
22
Effect sizes (ES) to represent
the magnitude of the difference between two
Table 1 Participant characteristics of the elite runners in both altitude and control groups (mean standard
deviation)
Variable Simulated altitude (n = 9) Control (n = 9)
Age (year) 23.9 3.8 27.4 5.5
Body mass (kg) 63.3 7.4 68.1 7.6

V
O
2 max
(ml min
1
kg
1
) 71.0 3.0 71.3 2.5
Training volume (kmweek
1
) 127 31 113 38
Running economy, hemoglobin mass and hypoxia 69
groups in terms of standard deviations, were cal-
culated from the log-transformed data by dividing
the change in the mean by the average of the
standard deviations of the repeated analysis. A
modied scale to interpret ES was established
as trivial, <0.2%; small, 0.20.6%; moderate,
0.61.2%; large, >1.2%.
23
Results
The pre- and post-test scores and the corresponding
percentage changes for all physiological variables
are shown in Table 2. The decrease in submaximal

V
O
2
was present at all three running speeds (Fig. 1)
and the increase in Hb
mass
was present in eight of
the nine runners in ALT (Fig. 2). There was only a
trivial relationship between change in

V
O
2 max
and
change in Hb
mass
(r = 0.04) in ALT. ALT undertook 11%
more training than CON (p= 0.42, ES = 0.42, small
Figure 1 Percentage change in submaximal

V
O
2
at the
three running speeds from pre- to post-intervention in (A)
control (CON, n = 8) and (B) altitude (ALT, n = 9) groups.
The group means standard deviations are shown in
heavy grey with a slight offset for clarity. Negative values
indicate a decrease in

V
O
2
and improved running econ-
omy.
Figure 2 Individual changes in hemoglobin mass (Hb
mass
)
pre and post 46 8 d intervention period in (A) con-
trol (CON, n = 9) and (B) altitude (ALT, n = 9) groups. The
group means standard deviations are shown in heavy
grey with a slight offset for clarity.
effect). The coefcient of variation (CV) for per-
formance over 1500 m of the athletes during this
period was 1.7% with a range of 1.02.3% (ALT 1.8%,
1.32.3%; CON 1.6%, 1.02.3%), which are similar
to the CV previously reported for well-trained to
elite runners (1.21.9% in cross-country and road
runs, 2.7% and 4.2% in half marathons, and 2.6% in
marathons).
24
Discussion
The major nding of the present study was that
sleeping at moderate simulated altitude for 400 h
during a 3 months period and training near sea level
was sufcient to substantially increase Hb
mass
com-
pared to a matched control group, which contrasts
previous reports from our laboratory using hypoxic
exposures of a shorter duration (180250 h). Nev-
ertheless, the current study elicited a similar
magnitude of improvement in RE to those studies
with shorter durations of hypoxia.
2,7,1316,18
7
0
P
.
U
.
S
a
u
n
d
e
r
s
e
t
a
l
.
Table 2 Physiological characteristics pre- and post-altitude training intervention for simulated altitude (ALT, n = 9) and control (CON, n = 8 except Hb
mass
where
n = 9) groups
Variable ALT CON Effect Likelihood P-value
Pre-mean S.D. Post-mean S.D. Pre-mean S.D. Post-mean S.D. % (90% CI) % Qualitative descriptor
Submaximal

V
O
2
(L min
1
) 3.38 0.56 3.26 0.57 3.61 0.52 3.60 0.52 3.2 (1.0, 5.2) 95 very likely 0.02

V
E
(L min
1
) 94.0 19.7 97.2 20.0 97.8 18.6 100.8 19.0 0.2 (3.0, 3.5) 18 unlikely 0.92
RER ratio 0.94 0.05 0.92 0.04 0.93 0.05 0.93 0.06 2.9 (0.7, 5.0) 76 likely 0.03
HR (bmin
1
) 157.7 14.2 152.9 12.9 156.4 16.5 156.6 17.2 3.1 (1.8, 4.4) 92 likely 0.00
[Lac-] (mM) 2.3 1.2 2.3 1.2 2.5 1.3 2.2 1.1 13.9 (2.9, 26.1) 72 possibly 0.04
Maximal

V
O
2
(L min
1
) 4.53 0.57 4.50 0.57 4.86 0.49 4.74 0.46 1.5 (1.6, 4.8) 61 possibly 0.41

V
E
(L min
1
) 157.4 16.2 161.7 16.6 169.8 9.5 165.2 8.5 5.6 (1.3, 10.2) 96 very likely 0.04
RER ratio 1.15 0.04 1.13 0.04 1.13 0.02 1.13 0.04 1.9 (4.7, 1.0) 71 possibly 0.26
HR (bmin
1
) 188.4 8.6 186.1 7.0 182.9 15.3 182.6 16.9 1.0 (2.6, 0.6) 51 possibly 0.28
[Lac-] (mM) 11.1 1.8 12.3 2.6 10.9 1.6 11.9 3.6 11.2 (10.6, 38.2) 78 likely 0.40
Hb
mass
(g) 951 172 987 173 978 87 969 94 4.9 (2.3, 7.6) 97 very likely 0.01
Values are means and standard deviations, and effects as percentages along with the lower and upper 90% condence intervals. Submaximal results are for pooled data from three
running speeds (14, 16, 18 kmh
1
). No variable was signicantly different between groups at pre.

V
O
2
, oxygen consumption;

V
E
, minute ventilation (BTPS); RER, respiratory exchange
ratio; HR, heart rate; [Lac-], concentration of blood lactate; Hb
mass
, haemoglobin mass.
Running economy, hemoglobin mass and hypoxia 71
The modest increase in Hb
mass
in the current
study contrasts to those of our earlier studies
with LHTL exposures ranging from 12 to 23 days
(911 h d
1
) that failed to elicit a substantial
increase in Hb
mass
.
25,7
Although the increase in
Hb
mass
in ALT was small, its magnitude is substan-
tially above the 1.2% TE for this method in our
hands, indicating that the increase is unlikely to
be measurement error. The increase in Hb
mass
in
the current study was less than that (79%) deter-
mined by others using a similar altitude stimulus
and duration.
8,9
One explanation for such discrep-
ancies is that increases in Hb
mass
after altitude
exposure may be an artefact of experimental error,
with methods used to determine red cell mass
or volume differing between laboratories.
25
For
instance, a study of Nordic skiers reported a 9.5%
reduction in red cell volume (from 2.87 to 2.62 L,
p= 0.08) of a control group that may be attributable
to errors in the baseline values rather than a real
decrease.
26
Failure of many investigators to rou-
tinely report their TE makes it difcult to interpret
condently the magnitude of reported changes.
The current nding supports the contention of
Rusko et al.
12
that the inability of studies to elicit
an increase Hb
mass
after altitude exposure may be
attributable to an inadequate duration or severity
of hypoxia. Rusko et al.
12
recommend >12 h d
1
, for
>3 weeks, at altitudes >21002500 m for an accel-
erated erythropoiesis. The current study totalled
415 h during 12 weeks at 2860 m simulated alti-
tude, supporting the theory that the total duration
of hypoxic exposure (hd) provides the overall
stimulus to increase Hb
mass
rather than any sin-
gle parameter. The current ndings challenge the
recommendations from Rusko et al.
12
by obtain-
ing an increase in Hb
mass
using only 9 h d
1
, 3 h
less than the recommended >12 h d
1
. We pro-
pose that the total duration of hypoxia over an
extended period is probably the primary consid-
eration for the prescription of altitude exposure.
However, there appears to be a threshold of daily
exposure to hypoxia because there were minimal
change in Hb
mass
after 3 h d
1
simulated altitude of
40005500 m, 5 dweek
1
for 4 weeks
27
.
Although the current altitude exposure substan-
tially increased Hb
mass
, there was not a correspond-
ing increase in

V
O
2 max
. The lack of increase in

V
O
2 max
after the LHTL exposure suggests that although
total O
2
carrying capacity is improved there may be
a parallel reduction in cardiac output (

Q), vascular
regulation or some other mechanism. The current
study adds credence to the proposed impairment
in vascular regulation and reduced

Q after altitude
training,
28
with a non-signicant 1% reduction in
maximal HR during the

V
O
2 max
test for ALT compared
with CON. A gradual decrease in maximal HR is
related to changes in myocardial -adrenergic and
myocardial receptor density after hypoxic exposure
and may account for a decreased

Q
28
.
Our ndings are consistent with a growing num-
ber of studies that have demonstrated that various
altitude exposures can reduce submaximal

V
O
2
by
310%, hence improving exercise economy.
2,7,1318
Others have demonstrated that submaximal

V
O
2
at
sea level remains largely unchanged after altitude
exposure.
19
However, it is our view that in elite
runners, 2050 days of LHTL exposure to moderate
simulated altitude substantially improves RE. Plau-
sible mechanisms for improved RE after a period of
altitude exposure include an increase in ATP pro-
duction per mole of O
2
used,
14
a decrease in the
ATP cost of muscle contraction,
29
and/or a decrease
in the cardiorespiratory cost of O
2
transport.
13
The
latter mechanism is supported by the reduced HR
at the three submaximal running speeds after sim-
ulated altitude in the ALT group compared to CON.
In conclusion, the current study demonstrated
that 400 h of simulated LHTL altitude (2900 m)
substantially improved RE, decreased submaximal
HR and increased Hb
mass
in elite runners. A triv-
ial increase in

V
O
2 max
was unrelated to the increase
in Hb
mass
possibly due to a decrease in

Q and/or
decrease in vascular regulation. Improved RE and
increased Hb
mass
are likely to contribute to improve
race performance giving credence to the use of
extended LHTL altitude training in the lead up to
competitions. A potential limitation of the study
was the extra training undertaken by ALT, although
not signicant, and our belief is that the groups
were well matched and the differences were due
to the hypoxic exposure.
Practical implications
Sleeping at moderate altitude for approx-
imately 400 hours increases total body
haemoglobin, allowing a greater oxygen car-
rying capacity.
Extended altitude exposure results in elite
runners being more economical at typical
training speeds.
Altitude exposure in the lead up to major
competitions appears worthwhile in improv-
ing running performance in elite runners.
Acknowledgements
The technical and nancial support from BOC Gases
Australia is gratefully acknowledged, as is the fund-
ing from the Australian Sports Commission.
72 P.U. Saunders et al.
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