Structure and hemodynamics of vascular networks in the chorioallantoic membrane of the chicken

Abstract

The chick chorioallantoic membrane (CAM) is extensively used as an in vivo model. Here, structure and hemodynamics of CAM vessel trees were analyzed and compared with predictions of Murray's law. CAM microvascular networks of Hamburger-Hamilton stage 40 chick embryos were scanned by videomicroscopy. Three networks with ∼3,800, 580, and 480 segments were digitally reconstructed, neglecting the capillary mesh. Vessel diameters (D) and segment lengths were measured, and generation numbers and junctional exponents at bifurcations were derived. In selected vessels, flow velocities (v) and hematocrit were measured. Hemodynamic simulations, incorporating the branching of capillaries from preterminal vessels, were used to estimate v, volume flow, shear stress (τ), and pressure for all segments of the largest network. For individual arteriovenous flow pathways, terminal arterial and venous generation numbers are negatively correlated, leading to low variability of total topological and morphological pathway lengths. Arteriolar velocity is proportional to diameter (v∝D measured, v∝D modeling), giving nearly uniform τ levels (τ∝D). Venular trees exhibit slightly higher exponents (v∝D, τ∝D). Junctional exponents at divergent and convergent bifurcations were 2.05 ± 1.13 and 1.97 ± 0.95 (mean ± SD) in contrast to the value 3 predicted by Murray's law. In accordance with Murray's law, τ levels are (nearly) maintained in CAM arterial (venular) trees, suggesting vascular adaptation to shear stress. Arterial and venous trees show an interdigitating arrangement providing homogeneous flow pathway properties and have preterminal capillary branches. These properties may facilitate efficient oxygen exchange in the CAM during rapid embryonic growth.

Microvascular hemodynamics in the chick chorioallantoic membrane

“…Diameter against mean velocity for arterioles and venules with diameter <100 μm in Networks 1, 2, and 3 for the terminal sources model, distributed sources model, and experimental data…”

“…A constant blood viscosity of μ = 1.3 cP was assigned, based on values obtained in a viscometer at the same developmental stage . A diameter‐dependent viscosity law was not employed as the rheology of nucleated avian red blood cells may differ from that of mammalian species.…”

“…This function was chosen to give a gradual decrease in pressure with decreasing arteriolar diameter, and a gradual decrease in pressure with increasing venular diameter. Flow BCs were assigned at all other boundary nodes using a linear approximation to the variation of velocity (mm/s) with diameter (μm) in the velocity data, for both arterioles and venules:…”

“…In the systemic microcirculation, the capillary networks typically form connections between the terminal branches of the arteriolar trees and the venular trees. In the intravital observations of the CAM, the connections between the arteriolar and venular trees and the plexus could not be resolved. However, SEM imaging indicates the presence of connections to the capillary plexus not only at the termini of arterioles and venules but also distributed along their lengths, as illustrated in Fig.…”

“…The intravital imaging did not allow resolution of the individual vessels forming the capillary plexus. Imaging at higher resolution, for example, using SEM of corrosion casts, shows that the capillary networks in the CAM have a somewhat regular, mesh‐like structure.…”