Development of the pharyngeal arch system related to the pulmonary and bronchial vessels in the avian embryo. With a concept on systemic-pulmonary collateral artery formation.

BACKGROUND: The literature is ambiguous as to the question of the developmental background of systemic-pulmonary collateral arteries. These are found in combination with various congenital heart malformations such as pulmonary atresia. From a clinical point of view, it is of interest to know whether we are dealing with the persistence of transient embryological vessels such as ventral segmental arteries or parts of pharyngeal arch arteries or with the prenatal or postnatal recruitment of the bronchial vasculature that normally supplies the lung. This study of the embryology of the extrapulmonary and intrapulmonary vasculature aims at a better understanding of the variations in origin, course, branching pattern, and histology of collateral arteries. METHODS AND RESULTS: Serial sections of quail embryos ranging between stage HH11 and stage HH28 were incubated with a monoclonal antibody (alpha MB1) against endothelial cells and their precursors. Additional series of chick embryos were injected with india ink to study the lumenized vascular patterns. A splanchnic plexus consisting of endothelial cells and precursors is present around the foregut before the lung buds develop. This plexus expands and gives rise to the pharyngeal arch arteries, the ventral pharyngeal veins, the pulmonary vessels, and the bronchial vessels, including the intrapulmonary vessel network. During two subsequent periods, the splanchnic plexus is transiently connected to the systemic arteries and veins. The bronchial arteries and veins develop in the second period from these transient vessels. The expansion and extension of the splanchnic plexus to many organs during the formation of the bronchial vessels explains the varying course and branching pattern of the bronchial vasculature. CONCLUSIONS: These results show that we are not dealing with two or more individual vascular systems that contribute to the developing vessels of the lungs but with one vascular plexus that normally gives rise to the pulmonary and bronchial vasculature but has the potential to give rise to other systemic-pulmonary connections.

Early formation of the vascular system in quail embryos.

The relation between vascular development and translocation of the splanchnic mesodermal layers was studied in presomite to 20-somite quail embryos by scanning electron microscopy. In addition, serially sectioned embryos were stained immunohistochemically with monoclonal antibodies (alpha QH1 or alpha MB1) specific for endothelial and hemopoietic cells. By the formation of the foregut the anterior borders of the two splanchnic mesodermal layers of a presomite embryo are translocated to the lateral and ventral sides of the foregut and fuse in the ventral midline of a 4-somite embryo. Meanwhile the splanchnic mesoderm differentiates into a splanchnic mesothelial layer and a plexus of endothelial cells, facing the endoderm. From 4 somites onward the foregut is covered by a single endothelial plexus. At first the endothelial precursors bordering the anterior intestinal portal and those in the area of the ventral mesocardium lumenize, subsequently giving rise to the endocardium of the heart tube. Hereafter, the pharyngeal arch arteries and the dorsal aortae develop from the remaining precursors. During formation of the pharyngeal arches, the pharyngeal arch arteries maintain their connections with the splanchnic plexus through the developing ventral pharyngeal veins. After disappearance of the dorsal mesocardium, the midpharyngeal endothelial strand, which is a longitudinal strand of proendocardial cells, remains connected to the foregut. This strand will contribute to the formation of the pulmonary venous drainage into the left atrium. A bilateral accumulation of cardiac jelly developing between the promyocardium and proendocardial plexus only suggests that the heart develops from two tubes. The proendocardial layer, however, is not divided by the ventral mesocardium but initially forms just one endocardial heart tube.