Biomechanics of skeletal muscle capillaries: hemodynamic resistance, endothelial distensibility, and pseudopod formation.
The objective of this study was to investigate the structure of capillaries in rat skeletal muscle and their mechanical properties over a wide range of transmural pressures. Capillaries were fixed at controlled pressures and studied with intravital and electron microscopy. Capillary lumen dimensions depend on the local transmural pressure, with irregular and partially collapsed cross-sections at low transmural pressures and circular cross-sections at elevated pressures. The average circumferential wall stress is a nonlinear function of the circumferential stretch. Elevation of the transcapillary pressure serves to increase the endothelial surface area exposed to the lumen and to the basement membrane while the average endothelial thickness and cell volume decrease. The number of vesicles in the endothelium and their average size decrease with the stretching of the endothelial cell. The balance of membrane area measurements on the vesicles and on the cell surface show that the total membrane surface is conserved at all pressures, and the vesicles become unfolded during stretching of the endothelial cells. This suggests that the vesicle membrane serves as a reservoir for the increase of endothelial surface membrane area during capillary distension. Under normal or elevated capillary pressure, virtually no evidence for pseudopod formation by the endothelial cells was detected. If the capillary transmural pressure was reduced to zero in the presence of autologous plasma for periods of about 10 min, limited evidence for pseudopods in less than 10% of the capillary sections was seen. If the muscle capillaries were perfused with plasmalyte and fixed at low pressures, all capillaries exhibited pseudopod formation. Addition of plasma proteins prevented most pseudopod formations. Endothelial pseudopods are depleted of vesicles and form sheet-like projections. Once pseudopods are formed at low pressure, they cannot readily be unfolded by elevation of the capillary transmural pressure. Pseudopods appear to consist of a crosslinked actin matrix and may have a strong effect on the resistance to blood flow in capillaries. These results may be relevant with respect to capillary blood flow at low pressures.
Lee
J
J
Institute for Biomedical Engineering, University of California--San Diego, La Jolla 92093-4012, USA.
Schmid-Schönbein
G W
GW
D000818:Animals; D001696:Biomechanical Phenomena; D002196:Capillaries / Q000502:physiology* / Q000648:ultrastructure; D048429:Cell Size; D006439:Hemodynamics; D008297:Male; D008854:Microscopy, Electron; D018482:Muscle, Skeletal / Q000098:blood supply*; D051381:Rats; D017207:Rats, Sprague-Dawley; D013314:Stress, Mechanical