To identify the forces that may exist in the parabronchus of the avian lung and that which may explain the reported strengths of the terminal respiratory units, the air capillaries and the blood capillaries, the arrangement of the parabronchial collagen fibers (CF) of the lung of the domestic fowl, Gallus gallus variant domesticus was investigated by discriminatory staining, selective alkali digestion, and vascular casting followed by alkali digestion. On the luminal circumference, the atrial and the infundibular CF are directly connected to the smooth muscle fibers and the elastic tissue fibers. The CF in this part of the parabronchus form the internal column (the axial scaffold), whereas the CF in the interparabronchial septa and those associated with the walls of the interparabronchial blood vessels form the external, i.e. the peripheral, parabronchial CF scaffold. Thin CF penetrate the exchange tissue directly from the interparabronchial septa and indirectly by accompanying the intraparabronchial blood vessels. Forming a dense network that supports the air and blood capillaries, the CF weave through the exchange tissue. The exchange tissue, specifically the air and blood capillaries, is effectively suspended between CF pillars by an intricate system of thin CF, elastic and smooth muscle fibers. The CF course through the basement membranes of the walls of the blood and air capillaries. Based on the architecture of the smooth muscle fibers, the CF, the elastic muscle fibers, and structures like the interparabronchial septa and their associated blood vessels, it is envisaged that dynamic tensional, resistive, and compressive forces exist in the parabronchus, forming a tensegrity (tension integrity) system that gives the lung rigidity while strengthening the air and blood capillaries.

The terminal respiratory units of the gas exchange tissue of the avian lung, the air capillaries (ACs) and the blood capillaries (BCs), are small and rigid: the basis of this mechanical feature has been highly contentious. Because the strength of the blood-gas barrier (BGB) of the mammalian lung has been attributed to the presence of type-IV collagen (T-IVc), localization of T-IVc in the basement membranes (BM) of the BGB and the epithelial-epithelial cell connections (E-ECCs) of the exchange tissue of the lung of the avian (chicken) lung was performed in order to determine whether it may likewise contribute to the strength of the BGB. T-IVc was localized in both the BM and the E-ECCs. As part of an integrated fibroskeletal scaffold on the lung, T-IVc may directly contribute to the strengths of the ACs and the BCs.

SummaryStructural failure of blood–gas barrier (BGB) and epithelial–epithelial cell connections (EECCs) in different vascular regions of the exchange tissue of the lung was studied in rested and exercised chickens. The number of red blood cells (nRBCs) was counted and protein concentration (PC) measured after lavaging the respiratory system, and blood was sampled to determine the blood lactate levels (BLLs). The numbers of complete BGB breaks (nBGBBs) and those of the EECCs (nEECCBs) were counted in the different vascular territories of the lung. The nRBCs and the PCs increased with increasing exercise intensities but the rate of increase decreased at higher workloads. From rest to the fastest experimental treadmill speed of 2.95 m.sec−1, BLLs increased 4-fold. In all cases, the nEECCBs exceeded those of the BGB, showing that structurally the BGB is relatively weaker than the EECC. The increase in the number of breaks with increasing exercise can be attributed to increase in the pulmonary capillary blood pressure (PCBP) from faster heart rates and higher cardiac outputs, while the leveling out of the measurements made at higher workloads may have arisen from hemodynamic changes that initially ensued from exudation of blood plasma and then flow of blood into the air capillaries on failure of the BGB. The relative differences in the nBGBBs and the nEECCBs in the different vascular regions of the lung were ascribed to diameters of the branches and their points of origin and angles of bifurcation from the pulmonary artery. Presence of RBCs in the air capillaries of the lungs of rested chickens showed that failure of the BGB commonly occurs even in healthy and unstressed birds. Rapid repair and/or defense responses, which were observed, may explain how birds cope with mechanical injuries of the BGB.

Complete blood-gas barrier breaks (BGBBs) and epithelial-epithelial cells connections breaks (E-ECCBs) were enumerated in the lungs of free range chickens, Gallus gallus variant domesticus after vascular perfusion at different pressures. The E-ECCBs surpassed the BGBBs by a factor of ~2. This showed that the former parts of the gas exchange tissue were structurally weaker or more vulnerable to failure than the latter. The differences in the numbers of BGBBs and E-ECCBs in the different regions of the lung supplied with blood by the 4 main branches of the pulmonary artery (PA) corresponded with the diameters of the blood vessels, the angles at which they bifurcated from the PA, and the positions along the PA where they branched off. Most of the BGBBs and the E-ECCBs occurred in the regions supplied by the accessory- and the caudomedial branches: the former is the narrowest branch and the first blood vessel to separate from the PA while the latter is the most direct extension of the PA and is the widest. The E-ECCBs appeared to separate and fail from tensing of the blood capillary walls, as the perfusion- and intramural pressures increased. Compared to the mammalian lungs on which data are available, i.e., those of the rabbit, the dog, and the horse, the blood-gas barrier of the lung of free range chickens appears to be substantially stronger for its thinness.