Stress failure of alveolar epithelial cells studied by scanning electron microscopy

Stress failure of capillary walls has previously been demonstrated in anesthetized rabbit lungs at high capillary transmural pressures, and the ultrastructural changes in the walls have been described with transmission electron microscopy. In the present study, the pattern of alveolar epithelial disruptions was studied using scanning electron microscopy (SEM). Lungs of anesthetized rabbits were perfused with autologous blood at capillary transmural pressures of 12.5, 32.5, 52.5, and 72.5 +/- 2.5 cm H2O and fixed by intravascular perfusion. Samples for SEM were processed by critical point-drying and freeze-drying, and the results of the two techniques agreed well. Out of a total of 433 alveolar epithelial breaks examined, 93% were elongated, with the remainder being roughly circular; 68% of the elongated breaks were oriented perpendicular to the capillary axis, suggesting that the surface tension of the alveolar lining layer played an important role in protecting the blood-gas barrier against stress failure. Most of the breaks involved the full blood-gas barrier, but 17% were limited to the epithelial cells. This finding is consistent with our earlier conclusion that the extracellular matrix, particularly the type IV collagen, is responsible for much of the strength of the blood-gas barrier. The dimensions of the elongated breaks of the epithelium were approximately 4 microns (length) and 1 micron (width). They varied little with pressure, suggesting that once the disruption had occurred the stresses were greatly relieved. Breaks affecting the complete blood-gas barrier tended to be larger than those confined to the epithelium, again consistent with the protective role of the extracellular matrix. Almost no breaks occurred at intercellular junctions although many were seen within 1 micron of the junctions. This finding suggests that the junctions themselves have considerable mechanical strength, but that their rigidity may make the cell in the vicinity of the junction more vulnerable to mechanical failure.