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1 Laboratoire de Physiologie, ABSTRACT Vaïda, Pierre, Christian Kays, Daniel Rivière,
Pierre Téchoueyres, and Jean-Luc Lachaud.
Pulmonary diffusing capacity and pulmonary capillary blood volume
during parabolic flights. J. Appl.
Physiol. 82(4): 1091-1097, 1997.
capillary distension; gravitational physiology; lung function
INTRODUCTION GRAVITY EXERTS A DEMONSTRABLE INFLUENCE on the
respiratory system, particularly on its vascular compartment (7).
During exposure to microgravity, a headward shift of fluid occurs
because of the loss of hydrostatic gradients (36); hence, blood should be more evenly distributed within the pulmonary system (25). Because of
the headward shifting of fluid and abdominal content, lung and chest
wall volumes are modified (20, 30), and redistribution of blood volume
is presumed to increase central blood volume (29). Taking this increase
into account, it also has been postulated that pulmonary diffusing
capacity (DL) and pulmonary
capillary blood volume (Vc) should increase (31). Because an increase in Vc might result in a rise of pulmonary microvascular pressure, it
has been speculated that fluid filtration may rise (7), leading to a
possible interstitial pulmonary fluid accumulation, an intriguing
possibility. Prisk et al. (32) first reported microgravity data for
cardiac output ( In our previous study (19), partial data on lung mechanics were
gathered by using a whole body plethysmograph during parabolic flights;
we observed slight reductions in the lung compliance and in the
residual volume during the 20 s of exposure to microgravity. These
results are compatible with a rapid rise of pulmonary blood volume and,
more specifically, of Vc.
The present paper reports the first measurements of
DL, Dm, and Vc in 10 subjects at
the onset of microgravity during parabolic trajectories of a plane.
METHODS Subjects
Table 1.
Descriptive statistics for the 10 subjects
Experimental Protocol
Data from the
Spacelab Life Sciences-1 (SLS-1) mission have shown sustained but
moderate increase in pulmonary diffusing capacity
(DL). Because of the occupational constraints of the mission, data were only obtained after
24 h of exposure to microgravity. Parabolic flights are often used to
study some effects of microgravity, and we measured changes in
DL occurring at the very onset
of weightlessness. Measurements of
DL, membrane diffusing capacity,
and pulmonary capillary blood volume were made in 10 male subjects
during the 20-s 0-G phases of parabolic flights performed by the
"zero-G" Caravelle aircraft. Using the standardized single-breath
technique, we measured
DL for CO and
nitric oxide simultaneously. We found significant increases in
DL for CO (62%),
in membrane diffusing capacity for CO (47%), in
DL for nitric oxide (47%), and
in pulmonary capillary blood volume (71%). We conclude that major
changes in the alveolar membrane gas transfers and in the pulmonary
capillary bed occur at the very onset of microgravity. Because these
changes are much greater than those reported during sustained
microgravity, the effects of rapid transition from hypergravity to
microgravity during parabolic flights remain questionable.
c),
DL, and Vc in four subjects
during the 9-day Spacelab Life Sciences-1 (SLS-1) mission. They
observed a sustained but moderate increase in
DL, diffusing membrane capacity
(Dm), and Vc but little variation in c.
Subject
Age, yr
Height, m
Weight, kg
VC, liters
Hb, g/100
ml
CK
43
1.83
74
5.16
12.2
DR
42
1.76
65
4.72
13.9
DT
48
1.73
75
5.01
14.2
JCLP
53
1.64
62
3.94
14.1
JLL
34
1.65
65
4.25
13.6
JPC
55
1.77
82
4.40
13.5
MB
34
1.74
69
4.85
14.6
OB
45
1.80
80
4.73
13.8
PV
44
1.76
69
5.80
13.5
TG
30
1.66
66
4.59
14.3
Mean ± SD
42.8 ± 8.2
1.73 ± 0.06
70.7 ± 6.8
4.75 ± 0.49
13.77 ± 0.63
VC, vital capacity (BTPS); Hb, hemoglobin
concentration.
The same devices were used at ground level (1 Gz) and in flight (0 Gz). Subjects stood and breathed through a mouthpiece while wearing a noseclip. Footstraps and a saddle with a seat belt permitted them to keep a near-standing position during microgravity. Subjects took the same position during ground measurements.
DL, Dm, and Vc determination. The lung diffusing capacity for gas x (DLx) is related to Dm by the equation 1/DLx = 1/Dmx + 1/(
x · Vc),
where x is the specific blood
transfer conductance for gas x. This
equation, which expresses the equivalent resistance to two serial
resistances, can usually be solved by measuring CO transfer
successively at two different known values of (1). Because depends on alveolar
PO2
(PAO2),
conventionally these two values are obtained by breathing 21 and 90%
oxygen fractions.
An alternative solution (4, 16, 22, 23, 26) is to simultaneously
measure the transfer capacities for two different gases and to solve
the set of two equations thus obtained. Nitric monoxide (NO) and CO
gases reacting with hemoglobin can be used as test gases.
DLCO and
DLNO were
determined simultaneously (4). The resulting two equations were
1/DLNO = 1/DmNO + 1/(NO · Vc) and 1/DLCO = 1/DmCO + 1/(CO · Vc).
The rate of uptake of NO being extremely rapid (13), the ratio
1/(NO · Vc)
can be reasonably ignored, and the equation for
DLNO can be
written as
1/DLNO = 1/DmNO.
The relationship between DmCO and
DmNO is
DmNO = a · DmCO,
with a = (MWCO/MWNO)1/2 · (
NO/CO),
where MWCO and
MWNO are the molecular weights of CO and NO (18 and 20, respectively);
CO and
NO are the solubility coefficients for CO and NO in plasma at 37°C (0.0215 and 0.0439 ml/100 ml, respectively; Bunsen coefficient) (13); and where coefficient a was calculated to be
1.97.
Hence,
1/DLNO = 1/DmNO = 1/(a · DmCO).
The Dm and Vc are computed from these two equations
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![Vc = 1/[&thgr;<SUB>CO</SUB> ⋅ (D<SC>l</SC><SUB>CO</SUB> − <IT>a</IT>/D<SC>l</SC><SUB>NO</SUB>)]](/content/vol82/issue4/fulltext/1091/img003.gif)
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The same protocol has been used to study DL and Vc after exercise (22, 23) or in patients with chronic obstructive lung disease (26). Data collection. Data were collected by using a basic protocol similar to the single-breath CO transfer test (Morgan, UK) modified as follows. Gases were collected in two separate bags enclosed in a bag-in-box system, one for inhaled gas and the other for exhaled alveolar gas sampling. Volume variations in the box were measured with a dry 8-liter spirometer (Morgan). The spirometer was verified with a 3-liter calibration syringe (model 5530; Hans Rudolph, Kansas City, MO). We carefully checked that the displacement of the dry spirometer bellows was not affected by G variations between 0 and 1.8 Gz during flights. To avoid such a possible variation, the spirometer was positioned so that the displacement of the bellows was along the x axis of acceleration. CO and He concentrations were measured with Morgan analyzers; NO was measured with a chemiluminescence analyzer (Thermo-Electron, Waltham, MA), which is the current standard physical reference technique for measurement of low concentrations of NO and NOx (8). The analyzers were calibrated during the 10-min horizontal flight period that preceded the first parabola after the cabin pressure had been stabilized [barometric pressure (PB) = 595 mmHg]. A check was performed at mid flight. We used three high-precision gas mixtures (Compagnie Française des Produits Oxygénés, Nantes, France); one tank was filled with 0.29% CO-9.8% He-21% O2 in N2, the second contained 10 parts/million (ppm) of NO in N2 for calibration purposes, and the third one 940 ppm NO in N2 for inhaled gas preparation. A control test unit automatically positioned the breathing valves and allowed the subject to breathe from or into the appropriate bags. The system could be activated by the subject himself, but, in most cases, an operator helped the subject to perform the maneuvers. A gas mixture containing 8-14 ppm NO in 0.29% CO-9.8% He-21% O2 in N2 was prepared in the inspiration bag; this was obtained by adding ~100 ml of 940 ppm NO in N2 with a syringe filled from the third tank; the syringe was emptied at mid filling of the inspiration bag, which contained 5-7 liters from the first tank. This operation took ~30 s and began just after the previous alveolar gas sample had been analyzed. The inhaled gas was immediately analyzed for NO, CO, and He before the breathing maneuver. Because of careful manual pressurization control, pressure did not vary by more than 5 mmHg during the parabolic trajectories; analysis of inhaled and alveolar gases was performed during the 2-min stabilized 1-Gz horizontal phase of flight between two parabolas (Fig. 2). Cabin PO2 during flight was 125 Torr; this was checked during the first flight and did not vary during parabolas due to stability of cabin pressure.
Measurement procedures. DL was measured according to the American Thoracic Society (ATS) standardized single-breath technique (1), except for the apnea duration, which was reduced to 3 s and kept constant between 0 G and ground level. Breath-hold time is of critical importance, since a longer breath-hold time would cause a very small fraction of the NO in the alveolar gas to be analyzed, <1 ppm for 10 ppm in the inhaled gas. Because we used the ambient hypoxic air during flights, we corrected DLCO for this as assumed by ATS recommendations (1) (see DISCUSSION). The experiments were performed in near-standing position, with the subjects breathing through the mouthpiece at the beginning of the parabola. Ten seconds after the beginning of the 0-Gz phase (Fig. 2), the operator asked the subject to exhale to his residual volume, then the inspiratory valve was opened, permitting the rapid inhalation of a preestablished volume (90% of vital capacity). The mouthpiece valve closed, preventing exhalation during 3 s. Then the valve opened, and the subjects rapidly exhaled to their residual volume. During this expiration, after the wash-out of the first 900 ml, a 900-ml alveolar sample was collected. Gas concentration measurements were made during the next 1-Gz horizontal flight phase to avoid any flow fluctuation in the analyzers with Gz variations. At the end of this procedure, the true inspired volume and real breath-hold time, as determined by the control unit, were noted and taped on an eight-channel FM TEAC recorder. Breath-hold time included 70% of the inspiration time, apnea time, and 50% of the sample collection time (1). The gas-analysis procedure lasted ~2 min; breath-hold maneuver could, therefore, only be performed every three or four parabolas. Each subject performed three to four replicates; two or three subjects were studied during each flight. Hemoglobin concentration had been measured on ground beforehand from arterialized blood microsamples with a CO-oximeter (2500 Corning).
Statistical Procedures
For each subject, mean values were compared between the two gravity levels, and a paired t-test was used to compare the mean values of the whole group between the two situations. A 95% confidence interval was used for comparison.RESULTS
Figures 3, 4, 5, and 6 show
the mean individual changes in
DLCO,
DmCO,
DLNO, and
Vc, respectively, from 1 Gz to 0 Gz for the 10 subjects.
Table 3 shows the mean results for DL, DLCO/VA, VA, DLNO, DmCO, and Vc at 1 Gz and 0 Gz. Dispersions for individual results at 1 and 0 G are given in Tables 4 and 5; DL and its components were generally highly reproducible.
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DLCO was found to be significantly higher (P < 0.001) during microgravity in all the subjects compared with ground-based values (62%), with a range from 24 to 103%. Because VA exhibited no statistical differences between the microgravity and the ground, DLCO/VA was largely increased (66%) (P < 0.001). A smaller, but significant, increase (47%, with a range of 12-64%) was observed for Dm (P < 0.001); like Dm, DLNO was significantly higher (P < 0.001) during microgravity (47%); an increase in Vc was very large (P < 0.001) during microgravity (71%), from 21 to 70 ml (29-128%).
DISCUSSION
The main results obtained in this study, on the gas-exchange modifications occurring at the very onset of microgravity, are increases in DL, Dm, and Vc that were much larger than those observed during the steady microgravity conditions of the SLS-1 mission.
Our results were obtained with a method for DLCO determination that differed from the ATS recommendations, since our breath-hold time was shorter than the suggested 10 s. This choice was made because of the rapid NO blood uptake (see Measurement procedures). It has been shown in healthy subjects, that a breath-hold time of 3 s, instead of 10 s, does not introduce any difference in DLCO measurement (14, 26). This 3-s breath-hold time was kept constant between 0 G and ground level. There is a known logarithmic decrease of alveolar NO and CO concentration plotted as a function of breath-hold time from 4 to 10 s (4). It can be thought that NO may dissolve and react within the airway tissue, but NO, like CO, is relatively insoluble in water (at 37°C solubility is 0.0184 ml/ml for CO and 0.035 ml/ml for NO) (12). These solubilities should not be affected by microgravity.
On the ground, data were determined near sea-level mean pressure
(altitude = 45 m or 150 feet), whereas in flight they were determined
at cabin pressure, which was stable along the flight at 595 mmHg, with
a total variation <5 mmHg. It has been shown (9, 21) that
DLCO
increases when PAO2
decreases. Gray et al. (15) showed that
DLCO must
be decreased by 0.3% for each Torr variation in
PAO2 from 120 Torr. ATS
recommendations are either to adjust to a standard
PAO2 of 120 Torr or to make correction for inspired
PO2
(PIO2) when PAO2 is not easily
available. The corrected value is given by the following formula:
altitude-adjusted
DLCO = measured DLCO
[1 + 0.0031 (PIO2 
150)], with estimated
PIO2 = 0.21 (PBZ-47), pressures being
expressed in Torr. It was shown that the correction for
PIO2 was accurate (15), and we chose this last procedure.
Moinard and Guénard (26) observed no differences in DLCO in 10 healthy subjects after a 3- or 9-s breath-hold time. They obtained similar values for Dm and Vc by using the NO-CO method and the two-step method, with the NO-CO method giving less scatter. As previously reported (4), DLNO was independent of the fractional concentration of inhaled oxygen, and no correction was made for DLNO.
NO is well known to induce a rapid dilation of pulmonary vessels and also to become oxidized into NO2. Hence, its use could alter DL. Borland and Higenbottam (4) tested mutual interference of DLCO and DLNO on five subjects, comparing measurements with CO and NO alone with measurements made simultaneously with a gas mixture containing both gases. They showed that the simultaneous presence of CO or NO in the gas mixture did not interact with the uptake of either CO or NO.
NO oxidation leads to NO2, which is very toxic for the lung; this reaction depends on PIO2, NO concentration, and contact duration between NO and O2. When NO is added to air at a concentration <40 ppm, the maximum NO2 concentration tolerated in the ambient air (5 ppm) is obtained after several hours. It is, therefore, reasonable to think that the 8-15 ppm of NO inhaled during four consecutive single-breath maneuvers had no toxic effects on the lung. Furthermore, Frostell et al. (10) failed to demonstrate any toxic effect after exposing lambs to 80 ppm NO for 3 h.
A recent clinical study performed during adult respiratory distress syndrome reported some effects of NO on pulmonary circulation and gas exchange (34). On the other hand, Moinard et al. (27) found that the addition of NO to hypoxemic patients with chronic obstructive lung disease had no circulatory effects 1 min later. Changes in pulmonary arterial pressure and pulmonary vascular resistance appear only 10 min after NO exposure, without any change in the distribution of alveolar ventilation or in lung perfusion. No effect of such small inhaled quantities of NO have yet been reported in normal subjects, and it has also been shown that there was no effect of NO on DLCO in the dog (24).
As noted by Prisk et al. (32), microgravity ground simulations showed
varying results. Water immersion produced a large increase of
DL/VA
(58%) (3). A previous observation (17), in three sitting subjects
immersed to the neck, reported a Vc increase of 47%. Immersion in cold
water (25°C) and in warm water (40°C) produced an increase in
Vc of ~49%, compared with immersion in thermally neutral water, and
of ~118%, compared with standing position in room air (5). Effects
of immersion are well known; c and stroke volume
increase sharply (2), as do pulmonary arterial pressure and central
blood volume. These modifications have been explained (11) by the shift
of the blood from the periphery to the intrathoracic regions; with the
immersion water acting as a hydrostatic counterpressure, a greater
number of pulmonary capillaries are recruited.
During 6° head-down tilt (HDT), previous studies (28) showed only a moderate elevation in DL during the first 90 min, followed by a rapid return to pretilt values. Compared with the 60° head-up position (6), steeper HDT (>15°) leads to larger increases in Vc (40%) and Dm (43%). During prolonged HDT (10 days), there was a small reduction in DL due to the lung volume reduction; hence, an increase (33%) of DL/VA was observed (35).
From these studies, it can be concluded, as did Prisk et al. (32), that neither water immersion nor HDT are a good microgravity model for both gas exchange and lung circulation studies. HDT results in lung volume reduction and raises intravascular pressure in the thorax. Nevertheless, immersion in cold or warm water induces a large rise in Vc, comparable to that observed in this study (5).
The very large and similar increase in
DL, Dm, and
Vc suggests that all pulmonary capillaries are in zone 3 (37). It can be thought that, during short-term microgravity, all lung capillaries may be recruited. Because there are no longer any hydrostatic differences in vascular pressure, capillary filling should be more
uniform. Moreover, a large increase could be expected in c, leading to capillary recruitment. Thus we can
observe both full recruitment and full distension of the capillary
vascular bed. Our observations are in agreement with the results
obtained from Doppler evaluation of cardiac filling and ejection
properties during parabolic flights: Johns et al. (18) observed a large increase in the venous return to right heart chambers for subjects in
sitting position. Our first studies of c during
parabolic flights (33), using thoracic electrical bioimpedance, confirm this large increase. In six men (age 38.7 ± 4.3 yr; height 1.75 ± 0.03 m; weight 71.2 ± 2.8 kg), we found a significant
increase in c (8.3 ± 0.71 liters at 0 G vs. 6.43 ± 0.30 liters at 1 G, P < 0.05)
and stroke volume (92.00 ± 9.35 ml at 0 G vs. 73.57 ± 4.21 ml
at 1 G, P < 0.05). A
c study, using both electrical bioimpedance and
esophageal Doppler effect, is in progress.
We observed a larger increase in gas diffusion and Vc than during
sustained microgravity; this could be explained by a time adaptation
occurring during the first 24 h of microgravity (in fact, because of
the occupational constraints during the SLS-1 mission, the first
measurements were made only 24 h after the launch), by a marked
increase of c during transient microgravity, or by
both.
The 1.8-Gz acceleration level before the microgravity phase could have altered DL, Dm, or Vc. Nevertheless, there is no way available as yet to easily determine the influence of the 20-s hypergravity preceding the 0-Gz phase; hemiparabolas from 1 to 0 Gz would result in only 10 s of microgravity, and the flight engineer did not agree to try any.
A more detailed analysis of the individual results shows (but this has not been statistically validated) less change in DL, Dm, and Vc in two of our ten subjects. These subjects were the two oldest of our group (53 and 55 yr old), and their capillaries are possibly less compliant than those of the younger people. We did not find any correlation between variation during microgravity and the height of the subjects.
In summary, in this study of DL and its subdivisions, we report major modifications of gas exchange and the pulmonary capillary bed at the very onset of microgravity, compared with the 1-Gz standing position. DL, Dm, and Vc rose very quickly, since our measurements were made ~10 s after the beginning of microgravity. These data suggest, in conjunction with results obtained by Prisk et al. (32), that DL, Dm, and Vc increase sharply in the beginning and then decrease within the first 24 h of microgravity. It is also possible that the rapid transition from 1.8 to 0 Gz induces changes that are, as yet, undefined.
ACKNOWLEDGEMENTS
We acknowledge the support from the Centre National d'Etudes Spatiales (CNES) and the Conseil Régional d'Aquitaine (CRA). We acknowledge the dedicated collaboration of the crew of Caravelle 234, the director Henri Marotte, and the technicians of the Laboratoire de Médecine Aérospatiale at the Centre d'Essais en Vol, Brétigny-sur-Orge, France. We thank P. Winterton, who has reviewed the English version of the manuscript.
FOOTNOTES
Address for reprint requests: P. Vaïda, Laboratoire de Physiologie, Médecine Aérospatiale, Université Bordeaux II, F 33076 Bordeaux cedex, France (E-mail: pierre.vaida{at}u-bordeaux2.fr).
Received 19 March 1996; accepted in final form 21 November 1996.
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ABSTRACT
1 · mmHg
