Pulmonary capillaries are more resistant to stress failure in dogs than in rabbits

1995 ◽  
Vol 79 (3) ◽  
pp. 908-917 ◽  
Author(s):  
O. Mathieu-Costello ◽  
D. C. Willford ◽  
Z. Fu ◽  
R. M. Garden ◽  
J. B. West
Keyword(s):  
Autologous Blood ◽  
Transmural Pressure ◽  
Blood Gas ◽  
Barrier Thickness ◽  
Rabbit Lung ◽  
Gas Barrier ◽  
Athletic Ability ◽  
Pulmonary Capillaries ◽  
Glutaraldehyde Solution

We previously showed that stress failure of pulmonary capillaries occurs at transmural pressures of approximately 50 cmH2O (40 mmHg) and above in rabbit lung. In this study, we examined whether pulmonary capillaries are more resistant to failure in dogs than in rabbits. This might be expected because of the greater athletic ability of dogs and therefore their presumably greater tolerance to large cardiac outputs and higher pulmonary vascular pressures. The lungs of 12 anesthetized mongrel dogs [22.1 +/- 5.2 (SD) kg] were perfused in situ with autologous blood and then with saline-dextran (5 min) and glutaraldehyde solution (10 min), all three perfusions at the same preset transmural pressure of 32.5, 72.5, 92.5, or 112.5 cmH2O. In dogs, the stress failure curves relating break number per millimeter of epithelium and endothelium were right shifted by approximately 40 cmH2O compared with rabbits. Blood-gas barrier thickness was significantly greater than in rabbits at 32.5 cmH2O, and unlike in rabbits, neither total nor interstitial thickness increased significantly with increasing pressure. These results indicate that pulmonary capillaries are more resistant to stress failure in dogs than rabbits.

Effect of reducing alveolar surface tension on stress failure in pulmonary capillaries

1995 ◽  
Vol 79 (6) ◽  
pp. 2114-2121 ◽  
Author(s):  
Y. Namba ◽  
S. S. Kurdak ◽  
Z. Fu ◽  
O. Mathieu-Costello ◽  
J. B. West
Keyword(s):  
Surface Tension ◽  
Autologous Blood ◽  
Outer Boundary ◽  
Transmural Pressure ◽  
Basement Membranes ◽  
Blood Gas ◽  
Gas Barrier ◽  
Alveolar Epithelial ◽  
Pulmonary Capillaries ◽  
Alveolar Surface

We previously showed that when pulmonary capillaries are exposed to high transmural pressures, stress failure of the blood-gas barrier occurs. It has been suggested that the surface tension of the alveolar lining layer may protect against stress failure because at high transmural pressures the capillaries bulge into the alveolar spaces. To test this hypothesis, we abolished the gas-liquid surface tension of the alveoli by filling rabbit lungs with normal saline. The lungs were then perfused at capillary transmural pressures of 32.5 or 52.5 cmH2O for 1 min with autologous blood, the blood was washed out with a saline-dextran mixture (3 min), and the lungs were fixed for electron microscopy with buffered glutaraldehyde; all perfusions were done at the same pressure. The frequency of breaks was measured in the capillary endothelial layer, alveolar epithelial layer, and basement membranes, and the data were compared with those in air-filled lungs at the same capillary transmural pressure and lung volume. We found that the frequency of breaks in the endothelium was not significantly different between air and saline filling and that there were fewer breaks in the outer boundary of the epithelial cells. By contrast, after saline filling, a larger number of breaks were seen in the inner boundary of the epithelium. The frequency of disruptions of the inner boundary of the epithelium was closely correlated with the volume of edema fluid collected at the trachea during the perfusion. These breaks in the inner boundary of the epithelium had not previously been seen in air-filled lungs exposed to the same pressures. The results suggest that abolishing the surface tension of the alveolar lining layer removes support from parts of the blood-gas barrier when the capillaries are subjected to a high transmural pressure but that not all portions of the barrier are subjected to the same forces.

Ultrastructural appearances of pulmonary capillaries at high transmural pressures

1991 ◽  
Vol 71 (2) ◽  
pp. 573-582 ◽  
Author(s):  
K. Tsukimoto ◽  
O. Mathieu-Costello ◽  
R. Prediletto ◽  
A. R. Elliott ◽  
J. B. West
Keyword(s):  
Autologous Blood ◽  
Alveolar Epithelium ◽  
Basement Membranes ◽  
Capillary Endothelium ◽  
Blood Gas ◽  
Gas Barrier ◽  
Pulmonary Capillaries ◽  
The Mean ◽  
Cell Lining

Electronmicroscopic appearances of pulmonary capillaries were studied in rabbit lungs perfused in situ when the capillary transmural pressure (Ptm) was systematically raised from 12.5 to 72.5 +/- 2.5 cmH2O. The animals were anesthetized and exsanguinated, and after the chest was opened, the pulmonary artery and left atrium were cannulated and attached to reservoirs. The lungs were perfused with autologous blood for 1 min, and this was followed by saline-dextran and then buffered glutaraldehyde to fix the lungs for electron microscopy. Normal appearances were seen at 12.5 cmH2O Ptm. At 52.5 and 72.5 cmH2O Ptm, striking discontinuities of the capillary endothelium and alveolar epithelium were seen. A few disruptions were seen at 32.5 cmH2O Ptm (mostly in one animal), but the number of breaks per millimeter cell lining increased markedly up to 72.5 cmH20 Ptm, where the mean frequency was 27.8 +/- 8.6 and 13.6 +/- 1.4 (SE) breaks/mm for endothelium and epithelium, respectively. In some instances, all layers of the blood-gas barrier were disrupted and erythrocytes could be seen moving into the alveolar spaces. In about half the endothelial and epithelial breaks, the basement membranes remained intact. The average break lengths for both endothelium and epithelium did not change significantly with pressure. The width of the blood-gas barrier increased at 52.5 and 72.5 cmH2O Ptm as a result of widening of the interstitium caused by edema. The cause of the disruptions is believed to be stress failure of the capillary wall. The results show that high capillary hydrostatic pressures cause major changes in the ultrastructure of the walls of the capillaries, leading to a high-permeability form of edema.

scholarly journals Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution

2009 ◽  
Vol 297 (6) ◽  
pp. R1625-R1634 ◽  
Author(s):  
John B. West
Keyword(s):  
Gas Exchange ◽  
Complete Separation ◽  
External Support ◽  
Blood Gas ◽  
Large Area ◽  
Gas Barrier ◽  
Type Iv ◽  
Pulmonary Capillaries ◽  
The Face ◽  
Flow Through

Two opposing selective pressures have shaped the evolution of the structure of the blood-gas barrier in air breathing vertebrates. The first pressure, which has been recognized for 100 years, is to facilitate diffusive gas exchange. This requires the barrier to be extremely thin and have a large area. The second pressure, which has only recently been appreciated, is to maintain the mechanical integrity of the barrier in the face of its extreme thinness. The most important tensile stress comes from the pressure within the pulmonary capillaries, which results in a hoop stress. The strength of the barrier can be attributed to the type IV collagen in the extracellular matrix. In addition, the stress is minimized in mammals and birds by complete separation of the pulmonary and systemic circulations. Remarkably, the avian barrier is about 2.5 times thinner than that in mammals and also is much more uniform in thickness. These advantages for gas exchange come about because the avian pulmonary capillaries are unique among air breathers in being mechanically supported externally in addition to the strength that comes from the structure of their walls. This external support comes from epithelial plates that are part of the air capillaries, and the support is available because the terminal air spaces in the avian lung are extremely small due to the flow-through nature of ventilation in contrast to the reciprocating pattern in mammals.

Very high pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred racehorses

1997 ◽  
Vol 82 (5) ◽  
pp. 1584-1592 ◽  
Author(s):  
Eric K. Birks ◽  
Odile Mathieu-Costello ◽  
Zhenxing Fu ◽  
Walter S. Tyler ◽  
John B. West
Keyword(s):  
High Pressures ◽  
Autologous Blood ◽  
Pulmonary Hemorrhage ◽  
Capillary Endothelium ◽  
Gas Barrier ◽  
Thoroughbred Racehorses ◽  
Pulmonary Capillaries ◽  
Thoroughbred Horses ◽  
Exercise Induced ◽  
Very High

Birks, Eric K., Odile Mathieu-Costello, Zhenxing Fu, Walter S. Tyler, and John B. West. Very high pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred racehorses. J. Appl. Physiol. 82(5): 1584–1592, 1997.—Thoroughbred horses develop extremely high pulmonary vascular pressures during galloping, all horses in training develop exercise-induced pulmonary hemorrhage, and we have shown that this is caused by stress failure of pulmonary capillaries. It is known that the capillary transmural pressure (Ptm) necessary for stress failure is higher in dogs than in rabbits. The present study was designed to determine this value in horses. The lungs from 15 Thoroughbred horses were perfused with autologous blood at Ptm values (midlung) of 25, 50, 75, 100 and 150 mmHg, and then perfusion fixed, and samples (dorsal and ventral, from caudal region) were examined by electron microscopy. Few disruptions of capillary endothelium were observed at Ptm ≤ 75 mmHg, and 5.3 ± 2.2 and 4.3 ± 0.7 breaks/mm endothelium were found at 100 and 150 mmHg Ptm, respectively. Blood-gas barrier thickness did not change with Ptm. At low Ptm, interstitial thickness was greater than previously found in rabbits but not in dogs. We conclude that the Ptm required to cause stress failure of pulmonary capillaries is between 75 and 100 mmHg and is greater in Thoroughbred horses than in both rabbits and dogs.

Morphometry of the extremely thin pulmonary blood-gas barrier in the chicken lung

2007 ◽  
Vol 292 (3) ◽  
pp. L769-L777 ◽  
Author(s):  
Rebecca R. Watson ◽  
Zhenxing Fu ◽  
John B. West
Keyword(s):  
Type I Collagen ◽  
Arithmetic Mean ◽  
Type I ◽  
Blood Gas ◽  
Gas Barrier ◽  
Structural Support ◽  
Pulmonary Capillaries ◽  
Mammalian Lung ◽  
Avian Lung ◽  
To Come

The gas exchanging region in the avian lung, although proportionally smaller than that of the mammalian lung, efficiently manages respiration to meet the high energetic requirements of flapping flight. Gas exchange in the bird lung is enhanced, in part, by an extremely thin blood-gas barrier (BGB). We measured the arithmetic mean thickness of the different components (endothelium, interstitium, and epithelium) of the BGB in the domestic chicken lung and compared the results with three mammals. Morphometric analysis showed that the total BGB of the chicken lung was significantly thinner than that of the rabbit, dog, and horse (54, 66, and 70% thinner, respectively) and that all layers of the BGB were significantly thinner in the chicken compared with the mammals. The interstitial layer was strikingly thin in the chicken lung (∼86% thinner than the dog and horse, and 75% thinner than rabbit) which is a paradox because the strength of the BGB is believed to come from the interstitium. In addition, the thickness of the interstitium was remarkably uniform, unlike the mammalian interstitium. The uniformity of the interstitial layer in the chicken is attributable to a lack of the supportive type I collagen cable that is found in mammalian alveolar lungs. We propose that the surrounding air capillaries provide additional structural support for the pulmonary capillaries in the bird lung, thus allowing the barrier to be both very thin and extremely uniform. The net result is to improve gas exchanging efficiency.

Role of the fragility of the pulmonary blood-gas barrier in the evolution of the pulmonary circulation

2013 ◽  
Vol 304 (3) ◽  
pp. R171-R176 ◽  
Author(s):  
John B. West
Keyword(s):  
Pulmonary Circulation ◽  
Complete Separation ◽  
Blood Gas ◽  
Gas Barrier ◽  
Pulmonary Capillaries ◽  
Pulmonary Capillary ◽  
Resolution Electron ◽  
Two Factors ◽  
Key Factor ◽  
Capillary Pressures

In 1953 Frank Low published the first high-resolution electron micrographs of the human pulmonary blood-gas barrier. These showed that a structure only 0.3-μm thick separated the capillary blood from the alveolar gas, immediately suggesting that the barrier might be vulnerable to mechanical failure if the capillary pressure increased. However, it was 38 years before stress failure was recognized. Initially it was implicated in the pathogenesis of High Altitude Pulmonary Edema, but it was soon clear that stress failure of pulmonary capillaries is common. The vulnerability of the blood-gas barrier is a key factor in the evolution of the pulmonary circulation. As evolution progressed from the ancestors of fishes to amphibians, reptiles, and finally birds and mammals, two factors challenged the integrity of the barrier. One was the requirement for the barrier to become increasingly thin because of the greater oxygen consumption. The other was the high pulmonary capillary pressures that were inevitable before there was complete separation of the pulmonary and systemic circulations.

Thickness of the blood-gas barrier in premature and 1-day-old newborn rabbit lungs

2003 ◽  
Vol 285 (1) ◽  
pp. L130-L136 ◽  
Author(s):  
Zhenxing Fu ◽  
Gregory P. Heldt ◽  
John B. West
Keyword(s):  
Pulmonary Circulation ◽  
Alveolar Epithelium ◽  
Capillary Endothelium ◽  
Blood Gas ◽  
Gas Barrier ◽  
Newborn Rabbit ◽  
Pulmonary Capillaries ◽  
Normal Gestation ◽  
Neonatal Lungs ◽  
Extensive Pilot

The pulmonary capillaries of neonatal lungs are potentially vulnerable to stress failure because of the complex changes in the pulmonary circulation that occur at birth. We studied the ultrastructure of the blood-gas barrier (BGB) in premature and 1-day-old rabbit lungs and compared it with the ultrastructure of adult lungs. Normal gestation of rabbits is 30 days. After extensive pilot measurements, three premature (27 days gestation) and three newborn (1 day old) rabbit lungs were perfusion-fixed at arterial, venous, and airway pressures of 25, 0, and 10 cmH2O, respectively, and the measurements were compared with those of three adult lungs. The thickness of the capillary endothelium, alveolar epithelium, and interstitium of the BGB was measured at right angles to the barrier at random points. A striking finding was the large number of measurements of the interstitial thickness in 1-day-old lungs that were very thin (0–0.1 μm). The percentages of occurrence of very thin interstitium in premature, 1-day-old, and adult lungs were 35.3 ± 9.4, 71.7 ± 5.2, and 43.0 ± 2.6, respectively ( P < 0.02 for 1 day old vs. premature and adult). Given the previously found relationship between stress failure and interstitial thickness, this large proportion of very thin interstitial layers in the capillaries of 1-day-old lungs is a reasonable explanation for their previously demonstrated vulnerability to stress failure.

Effect of prior high-intensity exercise on exercise-induced arterial hypoxemia in Thoroughbred horses

2001 ◽  
Vol 90 (6) ◽  
pp. 2371-2377 ◽  
Author(s):  
Murli Manohar ◽  
Thomas E. Goetz ◽  
Aslam S. Hassan
Keyword(s):  
High Intensity ◽  
Structural Changes ◽  
Pulmonary Hemorrhage ◽  
Exercise Bout ◽  
Blood Gas ◽  
Gas Barrier ◽  
Arterial Hypoxemia ◽  
Pulmonary Capillaries ◽  
Thoroughbred Horses ◽  
Exercise Induced

Strenuously exercising horses exhibit arterial hypoxemia and exercise-induced pulmonary hemorrhage (EIPH), the latter resulting from stress failure of pulmonary capillaries. The present study was carried out to examine whether the structural changes in the blood-gas barrier caused by a prior bout of high-intensity short-term exercise capable of inducing EIPH would affect the arterial hypoxemia induced during a successive bout of exercise performed at the same workload. Two sets of experiments, double- and single-exercise-bout experiments, were carried out on seven healthy, sound Thoroughbred horses. Experiments were carried out in random order, 7 days apart. In the double-exercise experiments, horses performed two successive bouts (each lasting 120 s) of galloping at 14 m/s on a 3.5% uphill grade, separated by an interval of 6 min. Exertion at this workload induced arterial hypoxemia within 30 s of the onset of galloping as well as desaturation of Hb, a progressive rise in arterial Pco 2, and acidosis as exercise duration increased from 30 to 120 s. In the single-exercise-bout experiments, blood-gas/pH data resembled those from the first run of the double-exercise experiments, and all horses experienced EIPH. Thus, in the double-exercise experiments, before the horses performed the second bout of galloping at 14 m/s on a 3.5% uphill grade, stress failure of pulmonary capillaries had occurred. Although arterial hypoxemia developed during the second run, arterial Po 2 values were significantly ( P < 0.01) higher than in the first run. Thus prior exercise not only failed to accentuate the severity of arterial hypoxemia, it actually diminished the magnitude of exercise-induced arterial hypoxemia. The decreased severity of exercise-induced arterial hypoxemia in the second run was due to an associated increase in alveolar Po 2, as arterial Pco 2 was significantly lower than in the first run. Thus our data do not support a role for structural changes in the blood-gas barrier related to the stress failure of pulmonary capillaries in causing the exercise-induced arterial hypoxemia in horses.

Endothelin Receptor B Expression in the Rat and Rabbit Lung as Determined by In Situ Hybridization Using Nonisotopic Probes

1993 ◽  
Vol 22 (Supplement 8) ◽  
pp. S1-S3 ◽  
Author(s):  
S. K. Durham ◽  
N. L. Goller ◽  
J. S. Lynch ◽  
S. M. Fisher ◽  
P. M. Rose
Keyword(s):  
In Situ Hybridization ◽  
Endothelin Receptor ◽  
Rabbit Lung ◽  
Endothelin Receptor B

scholarly journals Mechanical ventilation-induced alterations of intracellular surfactant pool and blood–gas barrier in healthy and pre-injured lungs

2020 ◽  
Author(s):  
Jeanne-Marie Krischer ◽  
Karolin Albert ◽  
Alexander Pfaffenroth ◽  
Elena Lopez-Rodriguez ◽  
Clemens Ruppert ◽  
...  
Keyword(s):  
Mechanical Ventilation ◽  
Blood Gas ◽  
Control Groups ◽  
Gas Barrier ◽  
Alveolar Epithelial ◽  
Alveolar Surfactant ◽  
Healthy Control ◽  
Mean Size ◽  
The Mean ◽  
Injury Progression

AbstractMechanical ventilation triggers the manifestation of lung injury and pre-injured lungs are more susceptible. Ventilation-induced abnormalities of alveolar surfactant are involved in injury progression. The effects of mechanical ventilation on the surfactant system might be different in healthy compared to pre-injured lungs. In the present study, we investigated the effects of different positive end-expiratory pressure (PEEP) ventilations on the structure of the blood–gas barrier, the ultrastructure of alveolar epithelial type II (AE2) cells and the intracellular surfactant pool (= lamellar bodies, LB). Rats were randomized into bleomycin-pre-injured or healthy control groups. One day later, rats were either not ventilated, or ventilated with PEEP = 1 or 5 cmH2O and a tidal volume of 10 ml/kg bodyweight for 3 h. Left lungs were subjected to design-based stereology, right lungs to measurements of surfactant proteins (SP−) B and C expression. In pre-injured lungs without ventilation, the expression of SP-C was reduced by bleomycin; while, there were fewer and larger LB compared to healthy lungs. PEEP = 1 cmH2O ventilation of bleomycin-injured lungs was linked with the thickest blood–gas barrier due to increased septal interstitial volumes. In healthy lungs, increasing PEEP levels reduced mean AE2 cell size and volume of LB per AE2 cell; while in pre-injured lungs, volumes of AE2 cells and LB per cell remained stable across PEEPs. Instead, in pre-injured lungs, increasing PEEP levels increased the number and decreased the mean size of LB. In conclusion, mechanical ventilation-induced alterations in LB ultrastructure differ between healthy and pre-injured lungs. PEEP = 1 cmH2O but not PEEP = 5 cmH2O ventilation aggravated septal interstitial abnormalities after bleomycin challenge.

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