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J Appl Physiol 70: 1731-1742, 1991;
8750-7587/91 $5.00
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Journal of Applied Physiology, Vol 70, Issue 4 1731-1742, Copyright © 1991 by American Physiological Society

ARTICLES

Stress failure in pulmonary capillaries

J. B. West, K. Tsukimoto, O. Mathieu-Costello and R. Prediletto
Department of Medicine, University of California, San Diego, La Jolla 92093-0623.

In the mammalian lung, alveolar gas and blood are separated by an extremely thin membrane, despite the fact that mechanical failure could be catastrophic for gas exchange. We raised the pulmonary capillary pressure in anesthetized rabbits until stress failure occurred. At capillary transmural pressures greater than or equal to 40 mmHg, disruption of the capillary endothelium and alveolar epithelium was seen in some locations. The three principal forces acting on the capillary wall were analyzed. 1) Circumferential wall tension caused by the transmural pressure. This is approximately 25 dyn/cm (25 mN/m) at failure where the radius of curvature of the capillary is 5 microns. This tension is small, being comparable with the tension in the alveolar wall associated with lung elastic recoil. 2) Surface tension of the alveolar lining layer. This contributes support to the capillaries that bulge into the alveolar spaces at these high pressures. When protein leakage into the alveolar spaces occurs because of stress failure, the increase in surface tension caused by surfactant inhibition could be a powerful force preventing further failure. 3) Tension of the tissue elements in the alveolar wall associated with lung inflation. This may be negligible at normal lung volumes but considerable at high volumes. Whereas circumferential wall tension is low, capillary wall stress at failure is very high at approximately 8 x 10(5) dyn/cm2 (8 x 10(4) N/m2) where the thickness is only 0.3 microns. This is approximately the same as the wall stress of the normal aorta, which is predominantly composed of collagen and elastin. The strength of the thin part of the capillary wall is probably attributable to the collagen IV of the basement membranes. The safety factor is apparently small when the capillary pressure is raised during heavy exercise. Stress failure causes increased permeability with protein leakage, or frank hemorrhage, and probably has a role in several types of lung disease.


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J. T. BERG, E. C. BREEN, Z. FU, O. MATHIEU-COSTELLO, and J. B. WEST
Alveolar Hypoxia Increases Gene Expression of Extracellular Matrix Proteins and Platelet-derived Growth Factor-B in Lung Parenchyma
Am. J. Respir. Crit. Care Med., December 1, 1998; 158(6): 1920 - 1928.
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J. C. Parker, C. L. Ivey, and A. Tucker
Phosphotyrosine phosphatase and tyrosine kinase inhibition modulate airway pressure-induced lung injury
J Appl Physiol, November 1, 1998; 85(5): 1753 - 1761.
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C. M. St. Croix, C. A. Harms, S. R. McClaran, G. A. Nickele, D. F. Pegelow, W. B. Nelson, and J. A. Dempsey
Effects of prior exercise on exercise-induced arterial hypoxemia in young women
J Appl Physiol, October 1, 1998; 85(4): 1556 - 1563.
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J. C. Parker, C. L. Ivey, and J. A. Tucker
Gadolinium prevents high airway pressure-induced permeability increases in isolated rat lungs
J Appl Physiol, April 1, 1998; 84(4): 1113 - 1118.
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S. R. Hopkins, R. B. Schoene, W. R. Henderson, R. G. Spragg, and J. B. West
Sustained submaximal exercise does not alter the integrity of the lung blood-gas barrier in elite athletes
J Appl Physiol, April 1, 1998; 84(4): 1185 - 1189.
[Abstract] [Full Text] [PDF]

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J. C. Parker and C. L. Ivey
Isoproterenol attenuates high vascular pressure-induced permeability increases in isolated rat lungs
J Appl Physiol, December 1, 1997; 83(6): 1962 - 1967.
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J. C. Parker, E. C. Breen, and J. B. West
High vascular and airway pressures increase interstitial protein mRNA expression in isolated rat lungs
J Appl Physiol, November 1, 1997; 83(5): 1697 - 1705.
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 Am. J. Respir. Cell Mol. Bio.Home page
C. Planès, B. Escoubet, M. Blot-Chabaud, G. Friedlander, N. Farman, and C. Clerici
Hypoxia Downregulates Expression and Activity of Epithelial Sodium Channels in Rat Alveolar Epithelial Cells
Am. J. Respir. Cell Mol. Biol., October 1, 1997; 17(4): 508 - 518.
[Abstract] [Full Text]

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J. T. Berg, Z. Fu, E. C. Breen, H.-C. Tran, O. Mathieu-Costello, and J. B. West
High lung inflation increases mRNA levels of ECM components and growth factors in lung parenchyma
J Appl Physiol, July 1, 1997; 83(1): 120 - 128.
[Abstract] [Full Text] [PDF]

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E. K. Birks, O. Mathieu-Costello, Z. Fu, W. S. Tyler, and J. B. West
Very high pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred racehorses
J Appl Physiol, May 1, 1997; 82(5): 1584 - 1592.
[Abstract] [Full Text] [PDF]

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L. Ermert, H.-R. Duncker, H. Bruckner, F. Grimminger, T. Hansen, R. Rossig, K. Aktories, and W. Seeger
Ultrastructural changes of lung capillary endothelium in response to botulinum C2 toxin
J Appl Physiol, February 1, 1997; 82(2): 382 - 388.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
D. DREYFUSS and G. SAUMON
Ventilator-induced Lung Injury . Lessons from Experimental Studies
Am. J. Respir. Crit. Care Med., January 1, 1997; 157(1): 294 - 323.
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 NEJMHome page
E. H. Jerome and J. W. Severinghaus
High-Altitude Pulmonary Edema
N. Engl. J. Med., March 7, 1996; 334(10): 662 - 664.
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 Circ. Res.Home page
M. I. Townsley, Z. Fu, O. Mathieu-Costello, and J. B. West
Pulmonary Microvascular Permeability : Responses to High Vascular Pressure After Induction of Pacing-Induced Heart Failure in Dogs
Circ. Res., August 1, 1995; 77(2): 317 - 325.
[Abstract] [Full Text]

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 CirculationHome page
J. B. West and O. Mathieu-Costello
Vulnerability of Pulmonary Capillaries in Heart Disease
Circulation, August 1, 1995; 92(3): 622 - 631.
[Abstract] [Full Text]

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C.A. Hales and E.J. Mark
Case 17-1995- An 81-year-old woman with mitral regurgitation and a left-upper-lobe pulmonary infiltrate
N. Engl. J. Med., June 8, 1995; 332(23): 1566 - 1572.
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