John B West
Department of Medicine, University of California San Diego, La Jolla, CA, USA
Although it is customary to emphasize the ways in which the structure and function of the human lung are wellsuited to its mission of gas exchange, the opposite case can be made. The proposition here is that the avian lung is superior in many respects to the mammalian lung.
It was about 300 million years ago that the ancestors of the present reptiles emerged from water and made a commitment to air breathing, but they were exothermic and could not sustain high levels of exercise. However, from them came the two great evolutionary lines that produced the mammals and birds, both capable of high, sustained levels of oxygen consumption. A fascinating aspect of these two evolutionary paths is that the physiology of the nervous, cardiovascular, renal, gastro-intestinal, endocrine and skeletal muscle systems show many similarities, but the lungs are radically different. The contention here is that the bird lung is superior to that of the mammal and that evolution got off on the wrong track.
Figure 1 shows the anatomy of the avian and mammalian lungs. Ventilation in the latter is reciprocating with the relatively small tidal volume of each breath being delivered to a relatively large volume of gas already in the lung. In the bird the arrangement is quite different. Inspired air is drawn into air sacs which are avascular and play no part in gas exchange. The gas is then moved through the gas-exchanging parabronchi where the pulmonary capillaries are located, and gas exchange occurs. In other words, this is a flow-through system rather like the radiator of a car, and in fact gas exchange is very similar in many respects to heat exchange. Furthermore, although it is not obvious from Fig. 1, the gas flow through the parabronchi is unidirectional as a result of aerodynamic valving in the airways, although the details of this are still not fully understood.
The reciprocating nature of ventilation in mammals results in at least three potential problems.
- Potential for uneven ventilation
In resting man, the inspired tidal volume of about 0.5 litres is delivered into a lung volume of about 3 litres. Although the geometry of the airways allows the inspired gas to penetrate far into the lung, the gas cannot reach the peripheral alveoli by convection, and the last part of its movement is by a complicated combination of convection and diffusion in the small airways. As a result, the more proximal alveoli tend to be better ventilated than the more distal, resulting in stratified inequality of ventilation. This inequality is small at rest but increases on exercise when the time available for diffusion is less. The flow-through system in the bird largely avoids this problem.
- The pool pattern of ventilation reduces the alveolar PO2
Because a small amount of inspired gas is delivered to a large pool of alveolar gas, the PO2 of the latter is substantially below the inspired value. For example, in the human lung, the inspired PO2 is about 150 mm Hg but the PO2 of the alveolar gas and arterial blood is around 100 mm Hg. Again the flowthrough system of the bird largely avoids this problem too.
- The reciprocating pattern necessitates large terminal air units
Because, as already stated, gas movement to the most peripheral alveoli is by a combination of convection and diffusion, the terminal air spaces need to be relatively large to keep the resistance low. The striking differences between the gas-exchanging tissue of the avian and mammalian lungs are shown in Figure 2. The blood capillaries are similar in size but the air spaces are dramatically different. The bird has air capillaries that branch off the parabronchi or their extensions and their diameter is about 10 to 20 µm depending on the species. By contrast the alveoli of the human lung, for example, have a diameter of about 300 µm.
Some of the disadvantages of these relatively large alveoli have only recently been appreciated. Figure 2B shows that the capillaries are strung out along the alveolar wall rather like a string of beads. This means that they have no mechanical support at right angles to the alveolar wall. As a result the capillary wall has to be thicker. In particular, the extracellular matrix of the blood-gas barrier, which is largely responsible for it strength, needs to be very much thicker than in the bird where the pulmonary capillaries are supported by a network of surrounding air capillaries (West et al. 2006). Furthermore, the mammalian alveolar walls require a cable of type 1 collagen that threads its way between the capillaries to maintain the integrity of the relatively large and unsupported alveolar wall. This again thickens part of the blood-gas barrier and thus interferes with diffusive gas exchange.
The mammalian lung has other disadvantages compared with the avian lung but these can only be touched on briefly here. As Fig. 1 indicates, the bird has successfully separated the gasexchange function of the lung from its ventilatory function. The bioengineering requirements of the tissues for these two functions are very different. Gas exchange by diffusion necessitates an extremely thin bloodgas barrier, for example, it is only 0.20.3 µm thick over much of the area of the barrier in the human lung. But the repetitive movement required by ventilation is better done by the more robust air sacs. In fact, one of the commonest, serious lung diseases in humans is emphysema which is characterized by breakdown of the delicate alveolar walls.
Another very practical disadvantage of the mammalian lung is that occlusion of an airway often causes serious impairment of gas exchange. This is a very common problem in the postoperative setting where airways are blocked by retained secretions or aspiration of fluid. Because the same structures are responsible for both ventilation and gas exchange, this is a much more serious problem for mammals than is presumably the case in birds, where aspirated material goes into the nonvascular air sacs.
Another advantage of the avian lung is that the arrangement of air and blood capillaries results in a so-called cross-current pattern of gas exchange, which tends to increase the PO2 of blood leaving the lung. This is well recognized and has been fully discussed elsewhere (Piiper & Scheid, 1972).
Finally, as mammals, we tend to regard ourselves as at the top of the evolutionary heap, but this is arguable. Some birds are superior to any mammals in their mass specific oxygen consumption and their aerobic scope, and there are more species of birds (about 9,000) than mammals (about 4,200).
So why did evolution proceed along an apparently flawed path for mammals. This is probably not a useful question. Evolution does not have a goal but proceeds incrementally. From time to time there is a change in few base pairs which confer an advantage or disadvantage for survival. But the fact that birds have better lungs than ourselves helps to keep a sense of perspective.
The experimental studies were made with Zhenxing Fu and Rebecca Watson. The work was supported by NIH grant RO1 HL 60968.
Piiper J & Scheid P (1972). Maximum gas transfer efficacy of models for fish gills, avian lungs and mammalian lungs. Respir Physiol 14, 115-124.
West JB, Watson RR & Fu Z (2006). The honeycomb-like structure of the bird lung allows a uniquely thin blood-gas barrier. Respir Physiol Neurobiol 152, 115-118.