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Comparative Physiology of the Pulmonary Circulation

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Abstract

Two selective pressures have shaped the evolution of the pulmonary circulation. First, as animals evolved from heterothermic ectotherms to homeothermic endoderms with their corresponding increase in the ability to sustain high oxygen consumptions, the blood‐gas barrier had to become successively thinner, and also provide an increasingly large area for diffusive gas exchange. Second, the barrier had to find a way to maintain its mechanical integrity in the face of extreme thinness, and this was assisted by the increasing separation of the pulmonary from the systemic circulation. A remarkable feature throughout the evolution of air‐breathing vertebrates has been the tight conservation of the tripartite structure of the blood‐gas barrier with its three layers: capillary endothelium, extracellular matrix, and alveolar epithelium. The strength of the barrier can be ascribed to the very thin layer of type IV collagen in the extracellular matrix. In the phylogenic progression from amphibia and reptiles to mammals and birds, the blood‐gas barrier became successively thinner. Also, the area increased greatly reflecting the greater oxygen demands of the organism. The gradual separation of the pulmonary from the systemic circulation continued from amphibia through reptiles to mammals and birds. Only in the last two classes are the circulations completely separate with the result that the pulmonary capillary pressures can be maintained low enough to avoid stress failure of the blood‐gas barrier. Remarkably, the barrier is generally much thinner in birds than mammals, and it is also much more uniform in thickness. These advantages for gas exchange can be explained by the support of avian pulmonary capillaries by the surrounding air capillaries. This arrangement was made possible by the adoption of the flow‐through system of ventilation in birds as opposed to the reciprocating pattern in mammals. © 2011 American Physiological Society. Compr Physiol 1:1525‐1539, 2011.

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Figure 1. Figure 1.

Electron micrograph of the blood‐gas barrier of the tree frog Chiromantis petersi. The three layers are seen very clearly in this amphibian. Note the central electron‐dense region of the extracellular matrix. ep, epithelium; bl, basal lamina; en, endothelium; p, plasma; e, erythrocyte.

Modified from Reference
Figure 2. Figure 2.

(A) A high‐power electron micrograph of the blood‐gas barrier in rat. The central electron‐dense lamina densa (LD) is well seen. LRE, lamina rara externa; LRI, lamina rara interna. Bar, 0.1 μm.

Modified from Reference . (B) A diagram of the thin part of the blood‐gas barrier. Note the lamina densa in the center of the extracellular matrix (ECM) where most of the type IV collagen is located. This is believed to be responsible for the strength of the barrier
Figure 3. Figure 3.

Blood‐gas barrier of a reptile, the black Mamba snake Dendroaspis polylepis. The three layers of the barrier are clearly seen including the central electron‐dense layer in the center of the extracellular matrix. e, erythrocyte; p, plasma; en, endothelium; bl, basal lamina; ep, epithelium.

Modified from Reference
Figure 4. Figure 4.

Blood‐gas barrier in the chicken Gallus gallus. Again, the three layers can be seen. a, air capillary; e, erythrocyte; c, blood capillary. From Reference .

Figure 5. Figure 5.

Blood‐gas barriers from three lungfish. (A) The South American lungfish Lepidosiren paradoxa. a, Air space; en, endothelium; i, interstitium; e, epithelium; c, capillary. A surface layer covering the epithelium is also seen. Modified from Reference . (B) The Australian lungfish Neoceratodus forsteri. From Reference . (C) The African lungfish Protopterus aethiopicus. e, Erythrocyte; p, plasma; en, endothelium; bl, basal lamina; a, air space; ep, epithelium; in, interstitium.

Modified from Reference
Figure 6. Figure 6.

Cross section of a lamella of the gill of the rainbow trout Oncorhynchus mykiss. R, red cell; EP, epithelium; X, subepithelium space; P, pillar cell. Note that the blood‐water barrier shows some similarities with the blood‐gas barrier of the lung. There is an epithelial layer and an endothelial layer (seen best in the capillary on the far right). However, there are also prominent pillar cells, and their extensions also form part of the blood‐water barrier. From Reference .

Figure 7. Figure 7.

Harmonic mean thicknesses ± SD for the birds, mammals, reptiles, and amphibians included in Table 1 of Reference . This includes 34 species of birds, 37 of mammals, 16 or reptiles, and 10 of amphibians. Note the progressive increase in mean thickness.

Figure 8. Figure 8.

The relationship between the mean harmonic thickness of the blood‐gas barrier and alveolar surface area, and the body mass. The upper line shows the harmonic mean thicknesses, and the lower line shows the surface areas of the blood‐gas barrier for a large range of mammals. Note that the mean thickness has a weak relationship with body weight but this is very strong for surface area. From Gehr et al. .

Figure 9. Figure 9.

Diagram showing some features of type IV collagen. Each molecule is about 400‐nm long. Two molecules join at the COOH‐terminal region (C) and four join at the NH2‐terminal region (N). The result is a matrix that has a high ultimate tensile strength.

Modified from Reference
Figure 10. Figure 10.

Diagram showing the two mechanism that result in stresses in the blood‐gas barrier. Indicates the hoop stress caused by the capillary transmural pressure. Represents the tension in the alveolar wall that increases as the lung is inflated. P, capillary hydrostatic pressure.

From Reference
Figure 11. Figure 11.

Pulmonary capillary from a rabbit preparation showing two examples of stress failure of the blood‐gas barrier. At the top, there is a disruption of the alveolar epithelial layer. At the bottom, the endothelial layer is broken and a blood platelet is adhering to the exposed basement membranes. ALV, Alveolus; CAP, capillary.

From Reference
Figure 12. Figure 12.

Simplified diagram showing stages in the evolution of the pulmonary circulation. In fishes, the gill capillaries are exposed to the full dorsal aorta pressure. In amphibia and noncrocodilian reptiles, partial separation of the pulmonary circulation from the systemic circulation occurs because of streaming of blood within the heart. However, only in the fully endothermic mammals and birds is there complete separation of the pulmonary circulation. The result is to protect the vulnerable blood‐gas barrier from the high vascular pressure.

From Reference
Figure 13. Figure 13.

Comparison of the pulmonary gas‐exchanging tissue in a rabbit (A) and chicken (B). In (A), the alveoli are relatively large and the capillaries that are located in the alveolar wall are completely unsupported at right angles to the wall. However, in (B) the blood capillaries are supported by the honeycomb‐like network of air capillaries surrounding them.

Figure 14. Figure 14.

Comparison of the blood‐gas barrier in chicken (A) and dog (B). Note that in the chicken, the blood‐gas barrier is not only very thin but also very uniform in thickness. a, Air capillary; c, blood capillary; e, erythrocyte. From Reference . In contrast, the dog (B) has a much thicker blood‐gas barrier, and furthermore it is much thicker on one side (labeled 2) than the other (labeled 1). The thick side has an expanded interstitium containing type I collagen fibers (F). A, Alveolar space; C, blood capillary; EPI, epithelium; EN, endothelium; FB, fibroblast.

From Reference
Figure 15. Figure 15.

Average thicknesses ± SD of all layers of the blood‐gas barrier in the lungs of chicken, horse, dog, and rabbit. Note that the total thickness of the barrier in the chicken is less than that in the mammals. Also, the thickness of the interstitium is far less in the chicken.

From Reference
Figure 16. Figure 16.

High‐powered electron micrographs of two epithelial bridges that surround the pulmonary capillaries in chickens. Note the extreme thinness. However, these are not struts like pencils but are actually thin epithelial sheets.

Figure 17. Figure 17.

Diagram showing the type I collagen cable that runs along the alveolar wall of the mammalian lung to maintain its integrity. Because it traverses one side of each capillary, the wall is thickened there, thus interfering with the diffusion of gases through it.



Figure 1.

Electron micrograph of the blood‐gas barrier of the tree frog Chiromantis petersi. The three layers are seen very clearly in this amphibian. Note the central electron‐dense region of the extracellular matrix. ep, epithelium; bl, basal lamina; en, endothelium; p, plasma; e, erythrocyte.

Modified from Reference


Figure 2.

(A) A high‐power electron micrograph of the blood‐gas barrier in rat. The central electron‐dense lamina densa (LD) is well seen. LRE, lamina rara externa; LRI, lamina rara interna. Bar, 0.1 μm.

Modified from Reference . (B) A diagram of the thin part of the blood‐gas barrier. Note the lamina densa in the center of the extracellular matrix (ECM) where most of the type IV collagen is located. This is believed to be responsible for the strength of the barrier


Figure 3.

Blood‐gas barrier of a reptile, the black Mamba snake Dendroaspis polylepis. The three layers of the barrier are clearly seen including the central electron‐dense layer in the center of the extracellular matrix. e, erythrocyte; p, plasma; en, endothelium; bl, basal lamina; ep, epithelium.

Modified from Reference


Figure 4.

Blood‐gas barrier in the chicken Gallus gallus. Again, the three layers can be seen. a, air capillary; e, erythrocyte; c, blood capillary. From Reference .



Figure 5.

Blood‐gas barriers from three lungfish. (A) The South American lungfish Lepidosiren paradoxa. a, Air space; en, endothelium; i, interstitium; e, epithelium; c, capillary. A surface layer covering the epithelium is also seen. Modified from Reference . (B) The Australian lungfish Neoceratodus forsteri. From Reference . (C) The African lungfish Protopterus aethiopicus. e, Erythrocyte; p, plasma; en, endothelium; bl, basal lamina; a, air space; ep, epithelium; in, interstitium.

Modified from Reference


Figure 6.

Cross section of a lamella of the gill of the rainbow trout Oncorhynchus mykiss. R, red cell; EP, epithelium; X, subepithelium space; P, pillar cell. Note that the blood‐water barrier shows some similarities with the blood‐gas barrier of the lung. There is an epithelial layer and an endothelial layer (seen best in the capillary on the far right). However, there are also prominent pillar cells, and their extensions also form part of the blood‐water barrier. From Reference .



Figure 7.

Harmonic mean thicknesses ± SD for the birds, mammals, reptiles, and amphibians included in Table 1 of Reference . This includes 34 species of birds, 37 of mammals, 16 or reptiles, and 10 of amphibians. Note the progressive increase in mean thickness.



Figure 8.

The relationship between the mean harmonic thickness of the blood‐gas barrier and alveolar surface area, and the body mass. The upper line shows the harmonic mean thicknesses, and the lower line shows the surface areas of the blood‐gas barrier for a large range of mammals. Note that the mean thickness has a weak relationship with body weight but this is very strong for surface area. From Gehr et al. .



Figure 9.

Diagram showing some features of type IV collagen. Each molecule is about 400‐nm long. Two molecules join at the COOH‐terminal region (C) and four join at the NH2‐terminal region (N). The result is a matrix that has a high ultimate tensile strength.

Modified from Reference


Figure 10.

Diagram showing the two mechanism that result in stresses in the blood‐gas barrier. Indicates the hoop stress caused by the capillary transmural pressure. Represents the tension in the alveolar wall that increases as the lung is inflated. P, capillary hydrostatic pressure.

From Reference


Figure 11.

Pulmonary capillary from a rabbit preparation showing two examples of stress failure of the blood‐gas barrier. At the top, there is a disruption of the alveolar epithelial layer. At the bottom, the endothelial layer is broken and a blood platelet is adhering to the exposed basement membranes. ALV, Alveolus; CAP, capillary.

From Reference


Figure 12.

Simplified diagram showing stages in the evolution of the pulmonary circulation. In fishes, the gill capillaries are exposed to the full dorsal aorta pressure. In amphibia and noncrocodilian reptiles, partial separation of the pulmonary circulation from the systemic circulation occurs because of streaming of blood within the heart. However, only in the fully endothermic mammals and birds is there complete separation of the pulmonary circulation. The result is to protect the vulnerable blood‐gas barrier from the high vascular pressure.

From Reference


Figure 13.

Comparison of the pulmonary gas‐exchanging tissue in a rabbit (A) and chicken (B). In (A), the alveoli are relatively large and the capillaries that are located in the alveolar wall are completely unsupported at right angles to the wall. However, in (B) the blood capillaries are supported by the honeycomb‐like network of air capillaries surrounding them.



Figure 14.

Comparison of the blood‐gas barrier in chicken (A) and dog (B). Note that in the chicken, the blood‐gas barrier is not only very thin but also very uniform in thickness. a, Air capillary; c, blood capillary; e, erythrocyte. From Reference . In contrast, the dog (B) has a much thicker blood‐gas barrier, and furthermore it is much thicker on one side (labeled 2) than the other (labeled 1). The thick side has an expanded interstitium containing type I collagen fibers (F). A, Alveolar space; C, blood capillary; EPI, epithelium; EN, endothelium; FB, fibroblast.

From Reference


Figure 15.

Average thicknesses ± SD of all layers of the blood‐gas barrier in the lungs of chicken, horse, dog, and rabbit. Note that the total thickness of the barrier in the chicken is less than that in the mammals. Also, the thickness of the interstitium is far less in the chicken.

From Reference


Figure 16.

High‐powered electron micrographs of two epithelial bridges that surround the pulmonary capillaries in chickens. Note the extreme thinness. However, these are not struts like pencils but are actually thin epithelial sheets.



Figure 17.

Diagram showing the type I collagen cable that runs along the alveolar wall of the mammalian lung to maintain its integrity. Because it traverses one side of each capillary, the wall is thickened there, thus interfering with the diffusion of gases through it.

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How to Cite

John B. West. Comparative Physiology of the Pulmonary Circulation. Compr Physiol 2011, 1: 1525-1539. doi: 10.1002/cphy.c090001