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1 Dipartimento di Medicina Sperimentale, Ambientale e Biotecnologie Mediche, Università di Milano-Bicocca, I-20052 Monza (MI), Italy; 2 Médecine Aerospatiale, Université de Bordeaux, F-33076 Bordeaux; 4 Centre Chirurgical Marie Lannelougue, UPRES EA2397, Université Paris XI, F-92350 Le Plessis Robinson; and 3 Hôpital Lariboisière, F-75010 Paris, France
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ABSTRACT |
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The volume-pressure relationship of the lung was studied in six subjects on changing the gravity vector during parabolic flights and body posture. Lung recoil pressure decreased by ~2.7 cmH2O going from 1 to 0 vertical acceleration (Gz), whereas it increased by ~3.5 cmH2O in 30° tilted head-up and supine postures. No substantial change was found going from 1 to 1.8 Gz. Matching the changes in volume-pressure relationships of the lung and chest wall (previous data), results in a decrease in functional respiratory capacity of ~580 ml at 0 Gz relative to 1 Gz and of ~1,200 ml going to supine posture. Microgravity causes a decrease in lung and chest wall recoil pressures as it removes most of the distortion of lung parenchyma and thorax induced by changing gravity field and/or posture. Hypergravity does not greatly affect respiratory mechanics, suggesting that mechanical distortion is close to maximum already at 1 Gz. The end-expiratory volume during quiet breathing corresponds to the mechanical functional residual capacity in each condition.
lung compliance; esophageal pressure; functional residual capacity; interstitial pressure
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INTRODUCTION |
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IN A PREVIOUS STUDY (3), we evaluated how changes in the gravity vector (Gz) obtained during parabolic flights affect chest wall mechanics. In the present work, we show data gathered in the same subjects previously studied to describe how similar changes modify the elastic properties of the lung. The knowledge of the elastic features of the chest wall and of the lung allows a full mechanical analysis of the respiratory system. In particular, coupling the volume-pressure curve of the lung and of the chest wall allows the mechanical definition of functional residual capacity (FRC), corresponding to the resting point of the respiratory system. This volume represents the end of expiration during quiet breathing at 1 Gz; indications from previous studies did not allow clarification of how gravity-dependent changes would influence the end-expiratory point (10, 11, 18, 30) in relation to changes in elastic properties of the respiratory system and of its two main components: the chest wall and the lung. This study also integrates previous information on how changes in gravity influence other aspects of the respiratory function, such as regional ventilation and perfusion (17, 20, 26, 33, 34) and diffusion capacity (32, 35, 37).
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METHODS |
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Parabolic flights. All experiments were done during three European Space Agency (ESA)-Centre National d'Etudes Spatiales (CNES) campaigns of parabolic flights in the period between October 1999 and April 2000. Each campaign included 3 flight days; an Airbus A300 aircraft was used; and each flight lasted 2.5-3 h and included 30 parabolas (90 parabolas per campaign). During the parabolic flight, the vertical acceleration vector Gz changes relative to steady horizontal flight corresponding to the 1-Gz phase: during pull-up, an acceleration of 1.8 Gz is reached; subsequently, reducing engine thrust allows the aircraft to enter a free-falling parabolic trajectory generating a 0-Gz phase, and, finally, during pull-out another 1.8-Gz phase is reached. All three phases lasted ~20 s.
Subjects. Respiratory variables (lung volume and esophageal pressure) were obtained during steady horizontal flight and during short periods of microgravity and hypergravity in four male (age: 53 ± 2 yr; weight: 74 ± 3 kg; height: 174 ± 1 cm) and two female (age: 42 ± 6 yr; weight: 52 ± 5 kg; height: 165 ± 4 cm) subjects. The same subjects were also studied in ground experiments in sitting and supine posture by use of the same equipment. The subjects were members of the experimental team, were nonsmokers, were in good health, and had no report of pulmonary disease. The subjects were trained to perform the respiratory maneuvers (see below); furthermore, they took part in previous parabolic flight campaigns and were well accustomed to the challenge of abruptly changing Gz several times during each flight.
Experimental equipment and system.
Subjects were sitting in a body plethysmograph made of wood (empty
volume of 360 liters) equipped with a pneumotachograph and transducers
to measure pressure in the box and at the mouthpiece (Pm); the
mouthpiece was also provided with an electromagnetic shutter. We also
performed some parabolas with subjects off the transducers to evaluate
the dependence of transducer signals from acceleration. To minimize the
effect of changes in aircraft accelerations on both transducers, they
were oriented along the aircraft's transverse axis. Lung volumes were
measured by flow integration. Esophageal pressure (Pes) was derived
from a pressure transducer mounted on a Gaeltec CTO-2 catheter, 2 mm
external diameter (12). Transducer sensitivity was 5 µV · V
1 · mmHg
1;
the linear pressure range was ±300 mmHg. Subjects advanced the catheter through the nose until the proper positioning of the esophageal probe was reached on the basis of preliminary experiments aiming at determining the best recording site. On average, the approximate location of the esophageal recording site was ~15 cm
below the jugular notch, which roughly corresponds to the apex of the
lung. The location of the esophageal transducer was chosen on the basis
of a minimal cardiac artifact and a stable pressure signal.
Calibration.
Before takeoff, calibration of the plethysmograph was done by use of a
2-liter syringe. A syringe volume control was made for each subject
during the flight. Pressure transducer calibration for body box
pressure and Pm was carried out by using a water manometer.
Cabin pressure tends to decrease during the ascending phase relative to
level flight and to increase during the descending phase. In terms of
volume signal, the plethysmograph would overestimate lung volume during
the ascending phase and underestimate lung volume during the descending
phase. Cabin pressure was manually corrected during the parabola, and
over 30 parabolas we checked that the overall change in lung volume
during the 0-Gz phase due to mismatch in pressure
correction averaged
0.029 ± 0.27 liters, 0.6% of vital
capacity (VC) (a nonsignificant underestimate).
Protocols for in-flight experiments. Subjects were sitting inside the plethysmograph and breathing through the mouthpiece. During 0 Gz exposure, there was a tendency for the subject to float up in the air because of the changing trajectory of the aircraft; to counteract such an inertia-dependent phenomenon, the subject was kept strapped at the thighs and feet; other loose bands around the arms kept them in a natural position parallel to the chest. During level flight, a check was performed to ensure regular recording of all variables. The time frame for data acquisition during respiratory maneuvers started in the last minute of level flight and lasted 2 min as follows: level flight (1 Gz, 1 min), pull-up (1.8 Gz, 20 s), injection (0 Gz, 20 s), pull-out (1.8 Gz, 20 s).
Subjects were instructed to perform different respiratory maneuvers within each phase, as shown by the experimental record of Fig. 1. After few control breaths, thoracic gas volume (TGV) was measured close to the end-expiratory volume by closing the mouthpiece shutter and performing inspiratory and expiratory efforts against closed airways for 3 s (panting maneuver, indicated as phase 1 in Fig. 1). In the records of Pm and Pes, one can easily detect the oscillations referring to the panting maneuver. Occasionally TGV was measured also at the end of the 2-min time frame. Subsequently, the subjects performed either of these two maneuvers: 1) volume-pressure curve of the lung. The subjects inspired to 70% of VC, indicated by phase 2 in Fig. 1, and expired slowly down to residual volume (RV), indicated by phase 3. Lung volume and Pes recorded during slow expiration allowed determination of the volume-pressure relationships of the lung. During such maneuvers, the alveolar pressure may be considered atmospheric and, therefore, Pes =
PL, where Pes represents an estimate of pleural surface pressure (Ppl) and
PL is the elastic recoil pressure of the lung.
2) VC maneuver (not shown in Fig. 1). The subjects inspired
up to TLC and expired relatively rapidly down to RV.
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Protocol for ground experiments. Ground experiments were performed on the same subjects adopting the same general protocols and equipment in sitting, supine posture, and 30° tilted head-up relative to supine. The change in posture was obtained by leaning the plethysmograph backward; this implied that legs remained as in the sitting posture.
Data analysis.
TGV, computed from Boyle's law is given by TGV
Pc · (
V/
Pm), where Pc is in-flight cabin
pressure and
V/
Pm is the ratio of change in thoracic volume to
change in alveolar pressure during panting maneuvers. This ratio was
inferred as the slope of the linear regression between the two
variables. Before the regression was executed, the drift affecting the
volume of the panting maneuvers was subtracted so we generally obtained
regression coefficients near 0.99, ensuring an accurate TGV measurement.
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(1) |
and 

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RESULTS |
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Figure 2 and Table
1 summarize the data of RV, VC and TLC
(= RV + VC). No significant differences were found in RV; VC was significantly decreased in supine and 30° tilted head-up postures (~550 ml, ~10% VC) relative to 1 Gz on ground; the
decrease in VC accounted for a similar decrease in TLC.
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Figure 3 reports the average
volume-pressure curves of the lung from all the subjects in the various
conditions. The relationship was displaced to the right going from 1 Gz (pooling data on ground and in flight) to 0 Gz. No substantial change was observed going from 1 to 1.8 Gz, whereas a leftward shift occurred in supine and 30°
tilted head-up postures. The changes in the position of the
volume-pressure curve are reflected in the corresponding changes in the
Pes values estimated at 40% VC that are reported in Fig. 4A (and Table
2). Relative to 1 Gz
(pooled on-ground and in-flight data), Pes became significantly less
subatmospheric at 0 Gz (by ~2.7
cmH2O), whereas it became significantly more subatmospheric in supine and 30° tilted head-up postures (by ~3.5
cmH2O). No change was observed going from 1 to 1.8 Gz. Lung compliance (Fig. 4B and Table
3), calculated from 20 to 40% VC, was
found to significantly decrease, relative to 1 Gz (pooled
on-ground and in-flight data) only in supine posture.
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Figure 5 displays the lung
volume-pressure curves of the subjects obtained in the various
conditions revealing individual differences. In subject F, 0 Gz exposure did not result in a clear rightward shift of
the lung volume-pressure curve. Furthermore, in subject D,
no difference in compliance was observed between 1 Gz
(pooled on-ground and in-flight data) and supine and 30° tilted
head-up postures.
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In one subject, we compared in-flight results obtained by the classic esophageal balloon technique and by the Gaeltec transducer probe. No differences were found when superimposing the lung volume-pressure curves obtained by the two techniques. This finding confirms that the two methods provide similar results, as previously found (31), also considering the intrinsic noise of the Pes due to heart rate. We also compared the volume-pressure curves at 1 Gz obtained with the catheter at different times, up to 1 h apart, and found no difference, indicating that the response characteristic of the miniaturized probe remains constant over time.
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DISCUSSION |
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This paper provides data on how lung recoil pressure is affected by varying the gravity vector by means of parabolic flights and body position. The present results integrate previous data (3) gathered from the same subjects concerning the effect of changing gravity on the mechanical properties of the chest wall. Adding the present to the previous data allows a mechanical analysis of the respiratory system when exposed to changing posture and gravity, in particular to the microgravity environment that characterizes spaceflights.
Static lung volumes. Despite some intra- and interindividual variability, on the average no significant difference in RV, VC, and TLC was found on comparing 1 Gz in-flight to 1 Gz on-ground data (Fig. 2). This finding suggests that the mechanical properties of the lung are not altered by repeated exposure to changing gravity vector between 0 and 1.8 Gz. The effects of changing lung volume and body position are similar to those reported in previous studies, in particular as far as the decrease in VC observed in supine posture (1, 11), reflecting a corresponding decrease in TLC (Fig. 2). We also observed no difference in RV after acute switching to supine posture, in line with previous studies (11, 18, 30). However, our finding of no change in RV after acute exposure to microgravity contrasts with the significant decrease (~300 ml) observed in sustained microgravity (11). A possible explanation of the difference might reside in the progressive increase in intrathoracic and intrapulmonary blood volume in sustained microgravity.
Volume-pressure curves of the lung.
As shown in Fig. 3, the volume-pressure relationship of the lung seems
to be affected by changing either Gz or posture. In Fig.
6, we attempt an interpretation of the
observed changes based on the following considerations. In the gravity
field, lung distortion results in a vertical gradient of alveolar size,
and the alveoli in the less dependent regions being more inflated
(15); accordingly, a vertical gradient of tissue
recoil pressure also exists, determining a vertical gradient of Ppl
(27). The indirect evidence of such deformation is given
by the shape of the washout curves of inert gases, in particular the
change in slope from phase III to phase IV in head-up (4, 6,
9) and supine postures (17, 21). The elastic
properties of the lung are commonly described by its volume-pressure
relationship; however, one should observe that total lung volume is
plotted as a function of local Ppl measured in the mid portion of the
esophagus: this is the case for the 1 Gz and supine curves
shown in Fig. 6. The deformation undergone by the lung in the gravity
field should be reduced in weightlessness, as suggested by the decrease
in slope of phase III and in height of phase IV of the Ar and
N2 washout curves (17, 26). Therefore, in
microgravity, one may assume that all lung regions should be more
uniformly expanded; as a consequence, regional and total lung volume
are the same percentage of VC. Accordingly, a one-to-one correspondence
between regional volume and regional pleural pressure should define
more accurately the intrinsic elastic properties of the lung (curve
labeled "Regional Lung Volume" in Fig. 6). The differences between
the regional percentage expansion and the overall lung volume for
similar pleural pressure reflect lung distortion.
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1.9
cmH2O, corresponding to ~30% regional VC (Fig. 6,
).
At 1 Gz, the end-expiratory Ppl is
6.4 cmH2O,
corresponding to ~40% VC (Fig. 6,
). Note that, at this same
value of Ppl, the regional volume would be 55% VC (Fig. 6,
). In
supine posture, the end-expiratory Ppl value is
3.8
cmH2O, corresponding to only 15% VC (Fig. 6,
); at this
Ppl value, the regional volume would be as high as 35% regional VC
(Fig. 6,
). Switching from 0 to 1.8 Gz would cause changes in percentage total lung volume similar to those found when
going from 0 to 1 Gz because of similarity of the
volume-pressure curve of the lung (Fig. 3) and end-expiratory Ppl
values (Table 4). In particular, at 1 Gz (and also at 1.8 Gz,) the lower total lung
volume compared with regional midthoracic volume (~40 vs. 55% VC,
respectively) suggests that alveolar units below the esophageal pressure recording site (~15 cm below the lung apex) must be less inflated. This finding is in line with the increase in slope of phase
III and IV of the washout curves of inert gases going from 0 to 1 Gz in upright posture (17, 26). Previous data
(26) showed that the hypergravity condition, relative to 1 Gz, induced a further increase in the slope of phases III
and IV of the washout curves for Ar and N2, an increase in
cardiogenic oscillation of O2, CO2, and closing
volume, indicating a further increase in uneven distribution of blood
perfusion and regional lung volume, namely greater expansion of apical
alveoli and greater collapse at the base of the lung. Because
end-expiratory pleural pressure, and therefore regional lung volume,
are similar at 1 and 1.8 Gz, one may hypothesize that the
increase in nonuniformity of regional lung volume involves the most
dependent region of the lung.
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Volume-pressure curves of the respiratory system. Because the lung and the chest wall are arranged in parallel, the total pressure exerted by the respiratory system (Prs) in relaxed conditions is given by Prs = PL + Pw = Palv, where PL and Pw are the recoil pressure of the lung and chest wall, respectively, and Palv is the alveolar pressure. Both lung and chest wall recoil pressures are derived from Ppl by appropriate respiratory maneuvers. Respiratory mechanics assume that local Ppl recording can be representative for the whole structure being analyzed, either the lung or the chest wall; therefore, one considers the volume-pressure curves of lung and chest wall as reflecting their average "functional" mechanical behavior.
Figure 7 presents the average volume-pressure curves of the lung and of the chest wall obtained for the same subjects in a previous study (3). The lung and chest wall volume-pressure curves cross at the resting volume of the respiratory system (FRC) where one has Pw =
PL = Ppl
and therefore Palv = 0.
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390 ± 150 ml reported in previous studies (10, 11, 18, 30).
The data presented in Fig. 7 allow critical reconsideration of the
frequently proposed similarity between supine posture and microgravity
exposure. In fact, although the changes in chest wall mechanical
behavior are qualitatively similar (rightward shift of the curve and
increase in compliance), the changes in overall elastic properties of
the lung are opposite. Going from upright (1 Gz) to supine
posture results in an expiratory effect on the volume-pressure curve
both of the chest wall and of the lung, causing FRC to drop to as low
as ~16% VC (
1,200 ml), as previously documented (11, 22,
23).
The volume-pressure curve of the chest wall is minimally affected by
hypergravity as exposure to 1 Gz generates a loading on the
chest wall that already brings its compliance close to its minimum, as
described in the previous study (3). Because the
volume-pressure curve of the lung is not significantly affected by
hypergravity, no significant changes in FRC were observed when in the
shift from 1 to 1.8 Gz. Our conclusions are in line with some data based on flowmeter measurement (18) but not with
others based on flowmeter measurement and inductive plethysmography
revealing an increase of ~200 ml (10, 30).
Lung volumes corresponding to the mechanical FRC are reported in Fig.
8 and in Table 4 to be compared with the
end-expiratory lung volumes measured by the panting maneuver (TGV) on
changing Gz and posture. As one can appreciate, there is a
very good matching between the two estimates, suggesting that
1) despite the limitation concerning the coupling of total
lung volume to esophageal pressure, the mechanical analysis
appears still valid for discussing the interaction between lung and
chest wall, and 2) subjects remain essentially relaxed at
end expiration during quiet breathing despite abrupt changes in either
Gz or posture.
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Interaction between Ppl and pulmonary interstitial pressure.
Some speculation is due concerning pulmonary interstitial fluid
dynamics in microgravity. At end expiration, the hydraulic pressure in
the pulmonary interstitium is physiologically subatmospheric (
10
cmH2O), reflecting a complex interaction between
microvascular and/or interstitial fluid exchanges and parenchymal
forces (29). Pulmonary interstitial pressure was
found to become more subatmospheric with decreasing (more negative) Ppl
(28); for this reason, increasing lung volume should lead
to an increase in microvascular filtration. Microgravity is a
potential cause of interstitial edema in the lung because of capillary
recruitment that, in turn, increases microvascular filtration. Because
in microgravity Ppl values are less negative during the respiratory
activity (end-expiratory volume decreases by ~600 ml), this should be
considered a protective factor counteracting the potential edematous
condition due to increased capillary perfusion.
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ACKNOWLEDGEMENTS |
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We are grateful to Suzel Bussières, Isabelle Désormes, and Daniel Rivière for precious support in the experimental sessions during parabolic flights. A special thank to Prof. Daniela Negrini who pioneered respiratory mechanics experiments aboard the Soyuz spacecraft during the MIR '95 mission. We also thank the Microgravity Division of the ESA, CNES, and NOVESPACE for the organization of the parabolic flight campaigns, and in particular Christophe Mora, local accountable for NOVESPACE.
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FOOTNOTES |
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Pierre Vaïda was the recipient of grants 793/1999/CNES/7660 and 793/2000/CNES/8147. Giuseppe Miserocchi was the recipient of a research grant from the Agenzia Spaziale Italiana.
Address for reprint requests and other correspondence: G. Miserocchi, Dipartimento di Medicina Sperimentale, Ambientale e Biotecnologie Mediche, Università di Milano-Bicocca, via Cadore, 48 I-20052 Monza (MI) (E-mail: giuseppe.miserocchi{at}unimib.it).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
August 30, 2002;10.1152/japplphysiol.00492.2002
Received 5 June 2002; accepted in final form 26 August 2002.
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A. Vovk and A. P. Binks Raising end-expiratory volume relieves air hunger in mechanically ventilated healthy adults J Appl Physiol, September 1, 2007; 103(3): 779 - 786. [Abstract] [Full Text] [PDF] |
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G. K. Prisk, J. M. Fine, T. K. Cooper, and J. B. West Vital capacity, respiratory muscle strength, and pulmonary gas exchange during long-duration exposure to microgravity J Appl Physiol, August 1, 2006; 101(2): 439 - 447. [Abstract] [Full Text] [PDF] |
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R. L. Dellaca, D. Bettinelli, C. Kays, P. Techoueyres, J. L. Lachaud, P. Vaida, and G. Miserocchi Effect of changing the gravity vector on respiratory output and control J Appl Physiol, October 1, 2004; 97(4): 1219 - 1226. [Abstract] [Full Text] [PDF] |
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