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

Abstract

Watson RR, Fu Z, West JB. Morphometry of the extremely thin pulmonary blood-gas barrier in the chicken lung. Am J Physiol Lung Cell Mol Physiol 292: L769-L777, 2007. First published November 17, 2006; doi:10.1152/ajplung.00355.2006.-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 (ϳ86% 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. capillary stress failure; lung morphology; bird respiratory physiology; air capillary; extracellular matrix; interstitium IN THE VERTEBRATE LUNG, OPTIMAL thickness of the pulmonary blood-gas barrier (BGB) is affected by opposing selective pressures (65). The barrier thickness is minimized to allow efficient exchange of oxygen and carbon dioxide, yet the capillary walls must also be strong enough to withstand high pulmonary capillary pressures that are incurred during extreme physical exertion. The BGB is composed of three layers: capillary endothelium, an interstitial layer or extracellular matrix, and an epithelial layer (Fig. 1). Combined, these cellular layers are relatively thin, usually measuring Ͻ2 m in total thickness under normal conditions (5,33,36). This three-ply ultrastructure of the BGB appears to be evolutionally well conserved over a variety of vertebrate taxa, indicating that its basic structure is efficient and relatively immalleable (18,25,27,31,33). The strength of the pulmonary capillary walls is likely related to the morphometry of the BGB, where the thickness of the interstitium determines the fragility of the capillaries (5). Where the BGB is thinnest, the interstitial layer is composed of only the fused basement membranes of the endothelium and epithelium laye...

Implicit mechanistic role of the collagen, smooth muscle, and elastic tissue components in strengthening the air and blood capillaries of the avian lung

“…The particular structures and ⁄ or mechanisms that can explain this property have remained obscure and contentious. Klika et al (1997), Scheuermann et al (1997), West et al (2006West et al ( , 2007a, and Watson et al (2007Watson et al ( , 2008 ascribed the strength to the presence of what they termed 'retinacula', 'cross-braces', 'struts', 'plates', 'extensions', and 'cross-bridges', pairs of thin parallel epithelial cell processes that separate the ACs while connecting the BCs; Klika et al (1997) Figs 10-18 (Fig. 10) Collagen fibers of the atrial septa (star) connecting to the infundibula ones (arrows) which in turn connect to the very thin collagen fibers of the exchange tissue (dot).…”

Major differences in the pulmonary circulation between birds and mammals

“…For example, this allows the avian lung to have an extremely thin blood-gas barrier West et al 2006). The mechanical support of the pulmonary capillaries presumably comes from the epithelial struts or bridges that link the air capillaries to the blood capillaries (Klika et al 1997;Weidner et al 2002;Watson et al 2006;West et al 2006). These struts also apparently prevent expansion of the pulmonary capillaries when the pressure inside them increases as in the experiments shown in Fig 1, and as a result pulmonary vascular resistance remains unchanged in spite of increases in capillary pressure.…”

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

“…Figure 5 shows electron micrographs from the lungs of chicken (Gallus gallus; A) and dog (Canis familiaris; B), and the much thinner barrier in the bird is immediately evident. Studies of the total thickness of the barrier and also the thicknesses of the endothelial, ECM, and epithelial layers have been carried out in our laboratory comparing chicken, rabbit, dog, and horse lungs (33). The total thickness of the avian blood-gas barrier is much less than that for mammals, as would be expected from Fig.…”

“…By contrast, on the thick side, the interstitium includes fibrils of type I collagen and even occasional cells, such as fibroblasts (34). We have documented the much smaller variation in the thickness of the blood-gas barrier in the chicken compared with that in rabbit, dog, and horse by calculating the coefficient of variation of the total thickness of the barrier (33). The measurements show that the coefficient of variation in the chicken is less than one-half the value found in the dog, for example.…”