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INTRODUCTION

Weightlessness certainly is not a new phenomenon. Indeed, it was about 400

million years ago that some vertebrates transitioned from an aquatic to a terrestrial
environment. An aquatic environment is a de facto weightless environment, since
the surrounding water provides support to its inhabitants. In contrast, the ter-
restrial vertebrate must support itself against the forces of gravity. Adaptation
to gravitational forces, in turn, leads to specific “structural” and functional
changes.
However, all this occurred over millions of years and, of course, no one
knew about it until the seventeenth century, when Galileo Galilei recognized
gravity as a physical entity. That century has been termed the “Age of the Scien-
tific Revolution,” and during that time speculation was replaced by experimenta-
tion. Among all the giants of the times, Galileo ranks as possibly the greatest;
he developed the mathematical basis of the laws of motion in the terrestrial envi-
ronment.
Today we live in another age of scientific revolution. Although we can
safely pinpoint its beginning—the middle of the twentieth century—there is no
end in sight, nor can we define the limits of this revolution. Just think, from space
to molecules and genes!
The International Space Station is being built and is becoming operational,
and space may also become the “recreational” area of the future (at least for
some). But we have to recognize that the full potential of the Space Station rests
on how physiological systems built to operate under forces of gravity can function
in the absence of these forces.
This is the subject of this monograph. The editors of Gravity and the Lung:
Lessons from Microgravity, Drs. G. Kim Prisk, Manuel Paiva, and John B. West,
and the contributors to this volume are all experts in their own fields and bring
with them years of experience and research.
Over the years, and by way of its many contributors, the Lung Biology in
Health and Disease series has focused on lung physiology and pathology in
the most common, not to say usual, environment. The series has also explored
known responses to one extreme environment, that is, the undersea world (Vol.

iii
iv Introduction

132). The current volume presents some aspects of human response to another
extreme!
As the Executive Editor of this series of monographs, I am as proud to
introduce this volume as I am grateful to the editors and the authors for having
given me the opportunity to do do.

Claude Lenfant, M.D.

Bethesda, Maryland
PREFACE

Although humans have been traveling in space for 40 years (since the first flight
of Yuri Gagarin in 1961), for the first 20 or so years only a few scientific studies
were performed in space, and those studies were limited. Given the difficulties
of placing and sustaining humans in that distant and hostile environment, this is
hardly surprising. However, the first flight of the European-built Spacelab module
(a laboratory placed in the cargo bay of the space shuttle) in 1983 provided the
opportunity for well-designed and properly controlled experiments. The pressur-
ized Spacelab module flew 14 times during the period from 1983 to 1998. Of
those 14 flights, 11 carried a significant proportion of physiological experiments,
and 3 of those were dedicated to life sciences research. Many of those flights
carried payload specialists—professional scientists who were recruited because
of their highly specialized knowledge and skills. Spacelab was decommissioned
in 1998, following the Neurolab mission, which carried the most complex series
of life sciences experiments performed in space. In the future, the International
Space Station will provide the opportunity for more elaborate studies in micro-
gravity.
Knowledge of environmental physiology comes from understanding how
the organism reacts to changes in the environment. For example, thermoregula-
tory processes might be studied by raising or lowering ambient temperature.
However, for subjects here on earth, gravity is a constant force that cannot be
eliminated. We know that gravity has a large effect on the behavior between the
top and bottom of the lung in an upright subject. There are substantial vertical
gradients in alveolar size and ventilation, in perfusion, and in gas exchange.
Therefore, we would expect to see large differences in the behavior of the lung
in microgravity. In addition, because the lung presents such a large surface area
to the environment (⬃50–100 m2), it is vulnerable to polluted atmospheres such
as might occur in the closed environment of a spacecraft. Yet none of these
factors are unique to the microgravity environment. People routinely change the
gravitational influence on their lungs every time they lie down, and many terres-
trial dwellers are exposed to both indoor and outdoor atmospheric pollution.
Thus, this volume focuses on using measurements made in the absence of gravity

v
vi Preface

(or, in some cases, at high gravity levels) to understand how the lung is affected
by gravity here on earth. The title Gravity and the Lung: Lessons from Micrograv-
ity reflects this approach.
We had the good fortune to be closely involved with several experiments
on Spacelab, and its demise provides an ideal time to summarize those findings
in the field of respiratory physiology before the transition of the Space Station.
We are grateful to Claude Lenfant, Executive Editor, who agreed to place this
volume in the Lung Biology in Health and Disease series.
It is always challenging to perform first-class experiments in a difficult
environment. Performing studies in space presents numerous difficulties, but the
result is exhilarating. It has been a privilege to participate.

G. Kim Prisk
Manuel Paiva
John B. West
CONTRIBUTORS

Jay C. Buckey, Jr., M.D. Research Associate Professor, Department of Medi-

cine, Dartmouth Medical School, Hanover, New Hampshire

Bruce D. Butler, Ph.D. Professor and Vice Chairman of Research, Department

of Anesthesiology, The University of Texas–Houston Medical School, Houston,
Texas

Chantal Darquenne, Ph.D. Assistant Research Physiologist, Department of

Medicine, University of California, San Diego, La Jolla, California

Marc Estenne, M.D., Ph.D. Professor of Medicine, Chest Service, Erasme

University Hospital, Brussels, Belgium

David H. Glaister, O.St.J., Ph.D., M.B., B.S., F.F.O.M. Group Captain (re-
tired), Royal Air Force, Talywern Consultancy Ltd., Powys, United Kingdom

Robb W. Glenny, M.D. Associate Professor, Department of Medicine and

Department of Physiology and Biophysics, University of Washington, Seattle,
Washington

Michael P. Hlastala, Ph.D. Professor, Department of Physiology and Bio-

physics and Department of Medicine, University of Washington, Seattle, Wash-
ington

Dag Linnarsson, M.D., Ph.D. Professor, Department of Physiology and Phar-

macology, Karolinska Institutet, Stockholm, Sweden

Giuseppe Miserocchi, M.D. Professor of Physiology and Chairman, Depart-

ment of Experimental and Environmental Medicine, Università Milano-Bicocca,
Monza, Italy

vii
viii Contributors

Daniela Negrini Associate Professor, Department of Medicine, Surgery and

Dentistry, Università Degli Studi di Milano, Milan, Italy

William T. Norfleet, M.D. Principal Coordinating Scientist for Space Medi-

cine, National Aeronautics and Space Administration, Houston, Texas

Manuel Paiva, Ph.D. Professor, Biomedical Physics Laboratory, Université

Libre de Bruxelles, Brussels, Belgium

G. Kim Prisk, Ph.D. Professor, Department of Medicine, University of Cali-

fornia, San Diego, La Jolla, California

H. Thomas Robertson, M.D. Professor, Pulmonary and Critical Care Medi-

cine, Department of Medicine and Department of Physiology and Biophysics,
University of Washington, Seattle, Washington

John B. West, M.D., Ph.D. Professor, Department of Medicine, University of

California, San Diego, La Jolla, California
CONTENTS

Introduction Claude Lenfant iii

Preface v
Contributors vii

1. Historical Introduction 1
John B. West
I. Normal Gravity 1
II. Increased Acceleration 17
III. Microgravity 21
IV. Epilogue 34
References 34

2. Effects of Acceleration on the Lung 39

David H. Glaister
I. Introduction 39
II. Instrumentation 41
III. Pulmonary Ventilation 42
IV. Pulmonary Perfusion 50
V. Consequences of Acceleration-Induced Ventilation
and Perfusion Inequalities 58
VI. Effect of ⫾Gy Acceleration on Ventilation 65
VII. Modeling 69
VIII. Zero-G Predictions 71
IX. Summary and Conclusions 71
References 72

3. Lung Volumes and Chest Wall Mechanics 75

Marc Estenne
I. Introduction 75

ix
x Contents

II. Lung and Chest Wall Volumes at End-Expiration 75

III. Static Lung Volumes 82
IV. Forced Expiratory Volumes and Flows 85
V. Pattern of Breathing and Chest Wall Compliance 86
VI. Summary 89
References 89

4. Ventilation Distribution 93
Manuel Paiva and G. Kim Prisk
I. Introduction 93
II. Topographical Ventilation Inhomogeneity 94
III. Nontopographical Convection-Dependent Ventilation
Inhomogeneity 101
IV. Nontopographical Diffusion-Convection-Dependent
Ventilation Inhomogeneity 108
V. Clinical Applications 112
References 113

5. Aerosol Transport in the Lung 117

Chantal Darquenne
I. Introduction 117
II. Total Deposition Studies 121
III. Aerosol Bolus Studies 126
IV. Summary and Perspectives 142
References 145

6. Pulmonary Perfusion: Gravitational Components 149

G. Kim Prisk
I. Introduction 149
II. Differences in Pulmonary Perfusion 150
III. Studies in Microgravity 155
References 160

7. Pulmonary Perfusion Distribution: Nongravitational Factors 163

Michael P. Hlastala, H. Thomas Robertson, and Robb W. Glenny
I. Resolution of Methods 163
II. Vascular Structure Dependence 169
III. Microgravity 175
Contents xi

IV. Summary 178

References 178

8. Pulmonary Gas Exchange 183

John B. West
I. Normal Gravity 183
II. Increased Acceleration 191
III. Microgravity 191
References 203

9. Exercise and Gas Exchange 207

Dag Linnarsson
I. Introduction 207
II. Gas Transport in the Lungs 208
III. Circulatory Transport 213
IV. Oxygen Requirements of Exercising Muscles 219
V. Lessons from Microgravity: Exercise Gas Exchange 221
References 222

10. Central Venous Pressure 225

Jay C. Buckey, Jr.
I. Introduction 225
II. Measuring Central Venous Pressure in Space 227
III. Parabolic Flight and Space-Flight Results 231
IV. Components of Central Venous Pressure 235
V. The Paradox: Increased Stroke Volume with Reduced
Central Venous Pressure 244
VI. Conclusion 249
References 250

11. Pulmonary Interstitial Fluid Balance 255

Daniela Negrini and Giuseppe Miserocchi
I. Introduction 255
II. Structure of Pulmonary Interstitium 256
III. The Pleural Cavity 257
IV. Measurements of Hydraulic Pressures in Intact
Pleuropulmonary Compartment: The Pleural
Window Technique 257
xii Contents

V. Height Distribution of Hydraulic Pressure Values

in Pleuropulmonary Compartments 258
VI. Transmembrane Fluid Fluxes in Pleuropulmonary
Compartments 260
VII. Transition from Physiological Condition to Pulmonary
Interstitial Edema 263
VIII. Alteration in Extracellular Matrix Integrity During
Development of Pulmonary Edema 265
IX. Simulated Microgravity in Experimental Animals 266
X. Pleural and Pulmonary Compartments in Microgravity 267
References 268

12. Control of Ventilation 271

G. Kim Prisk
I. Introduction 271
II. Response to Lowered Oxygen 273
III. Response to Raised Carbon Dioxide 279
IV. Physiological Implications 283
References 285

13. Decompression Sickness in Extravehicular Activities 289

William T. Norfleet and Bruce D. Butler
I. Introduction 289
II. Decompression Sickness 290
III. Prevention of Decompression Sickness 310
IV. Treatment of Decompression Sickness 314
V. Conclusions 321
References 321

14. Overall Summary 335

G. Kim Prisk, John B. West, and Manuel Paiva
I. Lessons Learned 335
II. Future Research in Microgravity 343
References 344

Author Index 347

Subject Index 367
1
Historical Introduction

JOHN B. WEST

University of California, San Diego

La Jolla, California

I. Normal Gravity
A. Introduction

It could be argued that, of all the organs in the body, the lung is the most vulnera-
ble to gravity, increased acceleration, and weightlessness. One of the reasons is
that the blood in the pulmonary capillaries is separated from the air in the alveoli
by an extremely thin blood–gas barrier over a vertical height of some 30 cm.
Because blood has a much greater density than air, substantial pressure differ-
ences across the capillary walls therefore exist at different levels in the lung, and
consequently there is a striking topographical inequality of blood flow. Another
reason why gravity affects the lung is that the lung is very distensible and there-
fore it distorts under its own weight. Consequently, there are regional differences
of alveolar expansion, mechanical stresses, intrapleural pressures, and ventilation.
Finally, the fact that ventilation and blood flow do not match each other at differ-
ent levels in the upright lung means that there are topographical differences of
pulmonary gas exchange, and these can have important effects on overall gas
exchange.
The normal gravitational field in which we live therefore causes marked
differences of blood flow, ventilation, gas exchange, intrapleural pressure, alveo-

1
2 West

lar expansion, and parenchymal stresses in the upright human lung. These will
be the subject of this first section. Subsequently, we shall see that increased accel-
eration markedly exaggerates these topographical differences with correspond-
ingly greater degrees of interference with normal lung function. Finally weight-
lessness, or microgravity, results in a more uniform distribution of these various
aspects of lung function and, in some cases, improvements of gas exchange.
However, recent measurements done in microgravity allow us to see that the lung
has some intrinsic inequality of ventilation and blood flow.

B. Early Predictions

One of the first persons to recognize that gravity may have an important effect
on pulmonary function was Johannes Orth (Fig. 1), a pathologist working in
Göttingen in the 1880s. In 1887, he wrote a short treatise (1) entitled Atiolog-
isches und Anatomisches uber Lungenschwindsucht (Etiological and Anatomical
Considerations of Phthisis) in which he speculated on the cause of the apical
localization of adult tuberculosis. He stated on page 20:
First, anemia has to be considered. It occurs more readily at the apex than in other
parts. Presumably the weight of the blood under normal conditions will not be of
very great importance due to the small difference in height between the hilum and
the apex of the lung, especially as this only exists in the erect posture. However I
believe that if the total quantity of blood is reduced and there is incomplete filling
of the vessels in the smaller circulation, the apex will be particularly affected, espe-
cially if the heart’s action is reduced and the blood pressure is low. That an existing
anemia as such contributes to a disposition for tuberculosis is suggested by the fact
(which cannot be disregarded) that a relative very high percentage of those individu-
als with a stenosis of the lung arteries die from tuberculosis.

Note that he argued that gravity would not have great importance under
normal conditions, but he was clearly aware of the possible influence of the
weight of the blood in determining its distribution. It is interesting that he empha-
sized that the effects of gravity would be seen more clearly when the ‘‘blood
pressure is low’’ (he presumably meant the pressure in the pulmonary circula-
tion). This is precisely what is seen in animal preparations where the pulmonary
artery pressure can be controlled and reduced (2). Orth also argued that pulmo-
nary stenosis (which he knew increased the risk of pulmonary tuberculosis) would
reduce blood flow to the apex of the lung, and subsequent measurements in pa-
tients with the tetralogy of Fallot have confirmed this (3).
Some 60 years later, the first measurements of right ventricular pressures in
humans were reported by Cournand et al. (4) using the new technique of cardiac
catheterization. William Dock (5) became aware of these data and argued that
the pulmonary artery pressure might not be sufficient to raise blood to the top
of the lung (Fig. 2). He reasoned that the reduced blood flow would impair the
Historical Introduction 3

Figure 1 Johannes Orth (1847–1923), professor of pathology in Göttingen in the 1880s.

He argued that the weight of the blood would affect its distribution in the lung, and was
therefore perhaps the first person to recognize that gravity has an effect on pulmonary
function. (From Ref. 59.)

defenses of the lung to infection by the tubercle bacillus. Dock also made an
additional remarkable prediction. He knew that the incidence of adult pulmonary
tuberculosis was slightly greater in the right lung compared with the left, and
therefore argued that the blood flow to the right apex would be less than that on
the left side. Subsequent measurements with radioactive carbon dioxide con-
firmed this prediction in normal subjects (3), the reason presumably being the
slight inclination of the main pulmonary artery trunk to the left, which therefore
preferentially distributes blood flow to the left lung. Dock also referred to the
4 West

Figure 2 Diagram from Dock (5) in which he suggested that the pulmonary artery pres-
sure would not be sufficient to raise blood to the top of the upright human lung. The two
broken lines marked C indicate the extent to which the blood would rise based on the
right ventricular pressure tracing shown in the inset (lower left). He used a reference point
in the middle of the right ventricle indicated by the horizontal line. Note that he also
thought that the blood flow to the apex of the right lung would be less than that of the
left. (From Ref. 5.)

high incidence of pulmonary tuberculosis in patients with pulmonic stenosis (as

did Orth) and added that patients with mitral stenosis who have an increased
blood flow to the lung apices are known to have a low incidence of the disease.
A particularly colorful set of studies was carried out by Rothlin and Undritz
(6) when they showed that while humans develop tuberculosis at the apex of the
lung, and quadrupeds such as the rabbit and cow do the same in the dorsal (top)
region of the lung, the bat, which spends much of its life inverted, tends to de-
velop pulmonary tuberculosis at the lung bases (Fig. 3). Incidentally, we now
know that the reason why adult tuberculosis has a predilection for the apex of
the human lung is not so much that the blood flow is reduced there, but that the
ventilation–perfusion ratio is high (largely because the blood flow is reduced)
and this results in a higher alveolar PO2 , which provides a better environment for
growth of the tubercle bacillus.
Historical Introduction 5

Figure 3 Composite of diagrams from the article by Rothlin and Undritz (6) where they
pointed out that tuberculosis affects the upper parts of the lungs and kidneys, even in the
bat, which spends most of its life upside down. They also claimed that the disease occurs
in the upper part of the human brain. (From Ref. 6.)

C. Early Measurements by Sampling Gas in Different Lobes

of the Lung

Evidence that gravity caused regional differences of blood flow and gas exchange
was obtained by passing catheters into different regions of the lung and analyzing
the gas that was withdrawn. Martin et al. (7), for example, passed fine catheters
into individual lobes of the lungs of human subjects who were seated upright,
and showed that the respiratory exchange ratio was higher in the upper lobes
than in the lower. As already stated, this results from the higher ventilation–
perfusion ratio in the upper regions of the lung, primarily because the blood flow
there is so low. Mattson and Carlens (8) used a special bronchospirometry cathe-
ter that allowed them to separate the gas exhaled from the right upper lobe from
that exhaled from the rest of the right lung, and they showed a very low oxygen
uptake in the right upper lobe that increased when the subject lay supine. Rahn
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