JEPonline
Journal
of
Exercise
Physiologyonline
Official
Journal of the American
Society
of Exercise Physiologists (ASEP)
ISSN
1097-9751
An
International Electronic Journal
Volume
3 Number 2 April 2000
Environmental
Exercise Physiology
Effectiveness
of Three Short Intermittent Hypobaric Hypoxia Protocols: Hematological
Responses
HÉCTOR CASAS1,
MIREIA CASAS1, ANTONI
RICART2, RAMÓN
RAMA1, JORDI IBÁÑEZ1,
LUIS PALACIOS1, FERRAN
A. RODRÍGUEZ3,
JOSEP L. VENTURA2,
GINÉS VISCOR1
and TERESA PAGÉS1
1Departament
de Fisiologia, Facultat de Biologia, Universitat de Barcelona, Barcelona,
Spain; 2Ciutat Sanitària
i Universitària de Bellvitge, L’Hospitalet de Llobregat, Barcelona,
Spain; and 3Institut
Nacional d’Educació Física de Catalunya, Barcelona, Spain.
HÉCTOR CASAS, MIREIA
CASAS, ANTONI RICART, RAMÓN RAMA, JORDI IBÁÑEZ, LUIS
PALACIOS, FERRAN A. RODRÍGUEZ, JOSEP L. VENTURA, GINÉS VISCOR
and TERESA PAGÉS. Effectiveness of Three Short Intermittent Hypobaric
Hypoxia Protocols: Hematological Responses. JEPonline,
Vol 3, No 2, 2000. The objective of this study was to compare and
evaluate the effectiveness of three protocols of intermittent exposure
to simulated altitude (hypobaric hypoxia). This was done in order to determine
the shortest protocol in which hematological changes were induced. In addition
to having some potential therapeutic applications, these protocols have
also been used to pre-acclimation of climbers to altitude, and to improve
the performance capacity of athletes. These applications are supported
by the available evidence that living in hypoxia while training in normoxia
is probably more effective than training and living in hypoxia. Three protocols
of different duration (days) and exposure (hours) at a simulated altitude
of 4,000-5,500m (462-379 Torr) were compared (Protocol A: 17 days and 60
hours; Protocol B: 9 days and 31 hours; and Protocol C: 21 days and 14
hours). The three experimental procedures showed to effectively elicit
a significant increase (p<0.05) in packed cell volume (mean increase
= 6.6% to 12.6%), hemoglobin concentration (mean increase = 14.7% to 18.7%),
red blood cell counts (mean increase = 7.7% to 13.7%), and reticulocyte
count (mean increase = 120% to 180%). We conclude that the three protocols
we used for intermittent exposure to hypobaric hypoxia effectively elicited
hematological adaptative responses. However, protocol B (9 consecutive
days, 3-4 h/d) shows to be the most efficient per day of exposure, in terms
of hematological adaptation, followed by protocol C (21 alternate day sessions,
1.5 h/d), most efficient in terms of total time (per hours of exposure).
Nevertheless, it may be the time availability of the subjects and/or the
facility, which will ultimately determine the model of exposure that is
chosen.
Key Words: Altitude, Hypobaric
chamber, Intermittent exposure, Erythropoiesis, Hypoxia
INTRODUCTION
Adaptation to altitude is a relatively
long process achieved by spending anything from a few days to many weeks
at high altitude. At high altitudes, a number of physiological responses
occur. The main changes are ventilatory variations (early responses), and
hematological changes with increase in red blood cell (RBC), packed cell
volume (PCV) and hemoglobin concentration ([Hb]) (half and long term responses),
which contribute at increasing the oxygen-carrying of the blood (1).
Chronic exposure to altitude in a hypobaric
chamber has been used as an alternative method for achieving acclimation
to altitude (2,3,4), and also for improving performance
at sea level (5,6). However, even when these protocols
have been effective in obtaining good acclimation, the time required to
obtain significant adaptative responses makes them incompatible with the
daily activity of subjects. “Living high-training low” might be a way of
improving physical performance, given that living at high altitude gives
rise to a series of advantageous physiological adaptations – mainly hematological
– while training at sea level maximizes training, improving performance
(7,8), but it is certainly a laborious procedure.
In contrast, studies of acclimation
to hypoxia by means of a protocol of intermittent exposure in a hypobaric
chamber have been undertaken (9), but the results obtained
were not optimal, as only ventilatory changes were found with no significant
hematological response. However, this was probably due to the short duration
of this protocol (3 days).
In previous studies in our laboratory,
intermittent hypobaric hypoxia was shown to induce acclimation to altitude
and hematological adaptations in healthy mountaineers (10,11,12).
Based in these investigations, new experimental protocols were planned
and compared, searching for the minimal intermittent exposure time capable
to stimulate erythropoiesis, as well as for the optimal level of hypoxia
and program duration that could be both effective and efficient for repeated
short exposures, and causing minimal interference with the daily activity.
The application of this protocol combined
training in normoxia and a few hours in hypoxia with the aim of improving
the performance and endurance of subjects. It also allows the pre-acclimation
of elite climbers and probably could have therapeutic applications, such
as the improvement of the anemia associated to end stage renal disease,
or as a supplementary erythropoietic stimulus during autotransfusion programs.
METHODS
Three protocols of intermittent exposure
to hypobaric hypoxia of varying duration were applied in the INEFC-UB hypobaric
chamber located at sea level (Barcelona, Spain). The protocols investigated
are described in Table 1.
As can be observed, total exposure time
was reduced progressively to a half. The three protocols began at a simulated
altitude of 4,000 m (462 Torr) and increased 500 m per session until an
altitude of 5,500 m (379 Torr) was reached. This last simulated altitude
was then maintained for the rest of the program.
Table 1. Description of the protocols
applied.
| Protocol |
Subjects |
Days of acclimation |
Exposure sessions |
Hours |
|
Altitude |
|
|
|
|
per day |
total |
|
| A |
6 |
17 |
17 |
3-5 |
60 |
4,000-5,500 |
| B |
17 |
9 |
9 |
3-5 |
31 |
4,000-5,500 |
| C |
8 |
21 |
9 |
1.5 |
14 |
4,000-5,500 |
Protocol A: 17 consecutive
days with sessions between 3 and 5 hours with a total of 60 hours exposure.
Protocol B: approximately
half the above in terms of duration and exposure. Nine consecutive days
with 31 hours of exposure (between 3 and 5 h/d).
Protocol C: three weeks
(21 days) in duration, with only 9 alternate days of exposure, a total
of 14 hours in sessions of 1.5 hours.
The characteristics of the subjects
were as follows; Group A: 6 subjects who were elite climbers and members
of a high-altitude expedition (28±5 years, 76.9±5.9 kg and
183.8±6.6 cm); Group B: 17 subjects who were members of three high-altitude
expeditions, 14 men (28±5 years, 73±5 kg, and 177±5
cm) and 3 women (27±5 yr, 63±? 13 kg and 167±3 cm);
Group C: 8 novice subjects (23.8±3 years, 67.1±9.0 kg and
172.9±6.7 cm).
All subjects participating in the study
were informed about its objectives, the experimental protocol, and the
possible risks involved. The study was undertaken with their written consent,
and in accordance with the recommendations of the Declaration of Helsinki.
All subjects were healthy and free of any hematological, cardiorespiratory,
or renal disorders. Specific recommendations were given to the subjects
in relation to their diet, in order to keep it balanced and free of potential
deficits. Special attention was paid to prevent an insufficient iron intake.
Before and after exposure to the hypobaric
hypoxia program, medical status, and performance capacity were evaluated.
The full medical examination included a medical history, physical characteristics,
and cardiovascular and respiratory parameters. Hematological and hemorheological
profiles were determined in 10 ml of venous blood samples collected from
the antecubital vein. The first blood extraction was conducted before exposure
to the hypobaric chamber. The last blood sample was taken a minimum of
22 hours after the last day of exposure in order to minimize the acute
effect of hypoxia exposure on circulating erythrocytes (13,14).
The analysis includes packed cell volume (PCV), red blood cells count (RBC
count), hemoglobin concentration ([Hb]), reticulocyte count, plasma osmolality,
and the apparent and relative viscosity of whole blood and plasma. All
venous blood samples were taken without stasis using plastic syringes.
Samples were immediately placed on ice in K2EDTA (hematology) and lithium
heparin (hemorheology) tubes, where they were kept awaiting assay.
Measurement of PCV was made following
centrifugation of capillary samples (Haemofuge Heraeus Sepatech, Germany)
for 5 min at 11,500 g and was expressed as a percentage value. RBC count
was determined using an automated cytological cell counter (Coulter Counter
Model ZF, UK). Hemoglobin concentration was determined using the Drabkin’s
method involving spectophotometry (Spectronic 2000, Bausch & Lomb,
Germany) at 540 nm. Reticulocytes were identified with a cresyl brilliant
blue stain. Venous blood was centrifuged at 3,000 g for 10 min (URA
2640, Germany) and the separated plasma was kept in Eppendorf tubes. Plasma
osmolality was measured by means of freeze-point depression using a micro-osmometer
(3MO, Advanced Instruments, USA).
The rheological behavior of blood was
studied by measuring plasma and whole blood apparent viscosity at shear
rates ranging from 4.5 to 450 s, using a cone-plate (0.8º) microviscosimeter
(LVT-IIc/p, Brookfield Engineering Laboratories, Inc.; USA). Given the
well-established Newtonian behavior of the plasma, and due to its low viscosity
value, plasma viscosity was measured only at 450 s, in order to obtain
the highest accuracy. Relative viscosity of blood was calculated for each
shear rate as the quotient between the apparent viscosity of whole blood
and plasma.
The time of exposure effect on
hematological determinations (Figure 1) was analyzed using a one-way analysis
of variance for repeated measures (RM ANOVA). Specific mean comparisons
were performed with a t-test without alpha correction. The paired t-test
and the non-parametric Wilcoxon matched-pairs signed ranks test were used
to compare pre- vs. post-hypoxia hematological and hemorheological results
for all variables. All tests were performed using the SigmaStat and SPSS
statistical packages (SPSS, USA). Differences were considered statistically
significant when p<0.05. Unless otherwise indicated, values are expressed
as mean±standard deviation.
RESULTS
Hematological changes are shown in Figures
1-3. In these figures we compare the pre-acclimation versus post-acclimation
values for each protocol.
Figure 1. PCV (%) values before
(filled bars) and after (hollow bars) the acclimation periods in the hypobaric
chamber for each protocol. * = significant pre- vs. post-acclimation differences
(p<0.05).
Figure 2. Hb (g/dL) values
before (filled bars) and after (hollow bars) the acclimation periods in
the hypobaric chamber for each protocol. * = significant pre- vs. post-acclimation
differences (p<0.05).
Figure 3. RBC (x106/?L)
values before (filled bars) and after (hollow bars) the acclimation periods
in the hypobaric chamber for each protocol. Mean values and standard error
bars are depicted. * = significant pre- vs. post-acclimation differences
(p<0.05).
The hematological changes before and
after intermittent exposure to hypobaric hypoxia were characterized by
a significant increase (p<0.05; paired t-test) in PCV, RBC count and
[Hb] in all and sundry of the three protocols (Table 2).
Table 2. Hematological changes
after the three intermittent hypoxia protocols (p<0.05; paired t-test).
| Protocol |
|
Pre-post relative increase (%change) |
|
Absolute and relative [Hb] increase per day of acclimation |
|
Absolute and relative [Hb] increase per hour of exposure |
|
|
PCV |
RBC |
[Hb] |
(g/L/d) |
(%change/d) |
(g/L/h) |
(%change/h) |
| A |
10.8 |
9.6 |
14.7 |
0.5 |
0.9 |
0.1 |
0.2 |
| B |
12.6 |
13.7 |
18.7 |
2.8 |
2.1 |
0.8 |
0.6 |
| C |
6.6 |
7.7 |
15.9 |
0.9 |
0.8 |
1.4 |
1.1 |
Reticulocytes also increased significantly
(p<0.01; paired t-test) in all the cases studied (mean diff.=+120% to
+180%). No significant changes were observed in plasma osmolality after
the three protocols, allowing us to discard the possibility of hemoconcentration
in all cases.
No significant differences were found
in the hemorheological profile at shear rates between 4.5 and 450 s, although
slight increases in relative and apparent blood viscosity were observed
after the acclimation period, as a reflection of increased PCV (Table 3).
Table 3. Hemorheological profile
at shear rates between 4.50 and 450 s.
|
Protocol A |
|
Protocol B |
|
Protocol C |
|
Shear
Rate |
Pre acclimation |
Post acclimation |
Pre acclimation |
Post acclimation |
Pre aclimation |
Post acclimation |
Apparent viscosity
4.50 s-1 |
18.33
±3.57 |
17.40
±3.56 |
18.25
±4.87 |
16.80
±4.80 |
17.75
±5.46 |
16.29
±5.33 |
Apparent vicosity
450 s-1 |
3.97
±0.62 |
3.76
±0.33 |
4.21
±0.53 |
4.30
±0.93 |
4.31
±0.59 |
3.91
±0.25 |
Relative viscosity
4.50 s-1 |
9.27
±2.06 |
10.6
±2.39 |
10.48
±4.07 |
8.60
±2.52 |
9.40
±2.96 |
8.47
±2.27 |
Relative viscosity
450 s-1 |
1.83
±1.24 |
2.35
±0.35 |
2.39
±0.57 |
2.20
±0.50 |
2.26
±0.17 |
2.07
±0.26 |
DISCUSSION
All three intermittent protocols of
exposure to hypobaric hypoxia in a decompression chamber gave similar hematological
adaptative responses, characterized by a significative increase of the
main indicators of blood erythrocytic mass (PCV, RBC, [Hb] and reticulocytes),
without significant increases in blood viscosity or plasma osmolality.
The new experimental protocols were
carried out at a safe level – for healthy subjects -- using acute hypobaric
hypoxia, and were designed having two points in mind: 1) the minimum exposure
time (hours) needed to stimulate erythropoietin (EPO) secretion, as established
previously in humans under a single hypoxic stimulus (15,16,17);
and 2) the minimum time range (days) needed to detect hematological changes
in chronic hypoxia (17).
The aim of study was to know the adequate
level of hypoxia and program duration that could be both effective and
efficient for repeated short exposures. Consequently, in order to validate
the effect of intermittent exposure protocols, we selected hematological
status as a reliable indicator of the half-term acclimation response, whereas
ventilatory responses (occur prior to hematological changes) were used
as an indicator of the minimum protocol to apply.
In a previous study conducted in our
laboratory using a shorter protocol, we recorded a significant ventilatory
response (19), while at the hematological level a non-significant
changes were observed. In another study, a protocol was designed taking
into account the minimum necessary days of exposure to detect the hematological
response to hypoxia (12,18).
Taking these results into account, two
longer protocols were then designed and carried out and compared with a
third protocol (protocol B) used previously in our laboratory. Thus, the
first protocol conducted (protocol A) was designed with a long exposure
(double than protocol B in hours and days) in order to determine whether
similar changes were elicited than in protocol B. Finally, with protocol
C the objective was to determine whether a discontinuous exposure, with
minimal session duration (only 90 min) over a three-week period of acclimation
and half the exposure time of protocol B was also sufficient to induce
hematological changes.
As mentioned above, the acclimation
protocols applied led to a significant increase in all indicators of the
erythrocytic mass, as shown by a significant rise in PCV, RBC count, [Hb]
and reticulocytes relative values. These results clearly indicated an enhancement
of the erythropoietic response, as described elsewhere (16,20).
The initial hematological characteristics
in PCV and [Hb] of the subjects of the three groups were largely identical.
Nevertheless, group B subjects showed RBC count levels significantly higher
than those in the other two groups. In contrast, the adaptative hematological
response to hypobaric hypoxia was evident and, moreover, showed similar
efficacy in the three groups, as indicated by the reticulocyte data. However,
when comparing the pre-post relative increase (see Table 2), protocol B
shows to be the most efficient (highest absolute and relative increase
per day of exposure), whereas the fastest procedure of protocol C (shortest
duration), shows to be largely the most efficient in terms of total time
spent in the hypobaric chamber (highest absolute and relative increase
per hour of exposure). Nevertheless, although the adaptative response induced
by protocol C was good, due to its shorter intensity, it may not have induced
an erythropoietic response as high as in protocol B.
Protocol A was the most efficient in
absolute terms, because high stable hematology levels were reached. However,
the long duration of protocol A caused a lower time efficiency. Given the
time (7 days) required for the presence of mature erythrocytes in circulation
(21), the comparison between the results of protocols
A and B, with 17 and 9 days of exposure respectively, suggest that values
measured were near maximal. In fact, in the analysis following to the return
of expeditions, the differences found on hematological values were not
significant compared with post-acclimation values.
The data presented are in agreement
with those reported in previous studies, both for chronic exposure and
intermittent exposure to hypoxia. Winslow et al. (22)
found an increment of 22% in [Hb] and 15.9% in PCV after continuous exposure
to an altitude of 5,400 m (base camp) for more than a month on an Everest
expedition. We found increments up to 17.5% in [Hb] and 11.0% in PCV, which
although lower than Winslow’s data, indicate that the intermittent exposure
protocols described here were effective. Richalet et al. (2)
using a hypobaric chamber for the pre-acclimation of an expedition to Mount
Everest reported an increase of 12% in [Hb], after one-week on Mont-Blanc
combined with 38 hours in the hypobaric chamber. Our results are similar
or even higher, with a shorter exposure time to hypoxia and much lower
simulated altitude.
Savourey et al. (3)
described a protocol of intermittent exposure of 5 days and 36 hours at
simulated altitudes over 5,500 m, reaching altitudes of 8,500 m. They reported
an increase in reticulocytes of 44.4%, but found no significant differences
in PCV or in RBC count, probably because these analyses were performed
too early in order to detect the changes in progress suggested by reticulocyte
count increase. In two of our protocols, which were shorter in terms of
hours of exposure, though not in terms of days of acclimation than that
applied by Savourey et al., we found a much higher relative increase in
reticulocytes (120% to 180%). Moreover, we also observed significant differences
in PCV and RBC counts.
As a consequence of the rise in erythrocytic
mass, one would expect an increase in blood viscosity, but the hemorheological
characteristics were not significantly altered after the acclimation periods,
although a positive trend was observed. This might be explained by the
presence of compensatory mechanisms, possibly related to erythrocyte aggregability
(reflected at low shear rates) and to erythrocyte deformability, which
might eventually prevent the negative effects of an increase in blood viscosity.
This phenomenon acquires particular significance when hemoglobin concentrations
are in excess of 18 g/dl, since blood viscosity increases greatly over
these values (1).
CONCLUSIONS
When comparing the results between the
three protocols of intermittent exposure to hypobaric hypoxia described
here (attaining a maximal simulated altitude of 5,500 m, 379 Torr), it
can be concluded that all the three programs were able to elicit hematological
adaptative responses. Interestingly, this polycythemia was not accompanied
by a significant increase in blood viscosity.
In terms of hematological adaptation,
protocol B (9 consecutive days, 3-4 h/d- seems to be the most efficient
per day of exposure, followed by protocol C, which with only 14 hours of
exposure (21 alternate day sessions, 1.5 h/d) is already efficient in terms
of total time (per hours of exposure). The data presented indicate that
intermittent hypoxia works well, even with limited exposure, and show a
trend for added benefits from more prolonged and frequent exposures. Nevertheless,
the time availability of the subjects and/or their facility may ultimately
determine the choice of exposure protocol.
ACKNOWLEDGEMENTS: The
authors are grateful to J.M. Valentín for her valuable technical
assistance. We thank Mr. Robin Rycroft (Language Advisory Service, Universitat
de Barcelona) for his help in editing the manuscript. This study was partially
supported by DGICYT grant PB96-0999, CSD 20/UNI21/97 and CSD 28/UNI21/97.
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Address for Correspondence:
Teresa Pagés, M.D., Departament de Fisiologia, Facultat de Biologia,
Universitat de Barcelona, Av. Diagonal, 645, E-08028, Barcelona, Spain.
Phone number: +34 934021556, Fax number: +34 934110358, e-mail: tpages@bio.ub.es
Copyright ©1997-2000
American Society of Exercise Physiologists. All rights reserved.
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