Maternal and fetal microvasculature in sheep placenta at several stages of gestation

Abstract

Maternal and fetal microvasculature was studied in ewes at days 50, 90 and 130 of gestation using microvascular corrosion casting and scanning electron microscopy. Microvascular corrosion casts of caruncles at day 50 were cup-shaped with a centrally located cavity. Branches of radial arteries entered the caruncle from its base and ramified on the maternal surface of the caruncle. Stem arteries broke into an extensive mesh of capillaries forming crypts on the fetal surface. The architecture of the caruncle at day 90 was similar to what was found at day 50 but the vascularity and the depth of the crypts increased in correspondence to increased branching of fetal villi. The substance of the caruncle was thicker at day 130 compared with day 50, with no remarkable difference compared with day 90. Capillary sinusoids of irregular form and diameter were observed on the fetal surface of the caruncle at all stages. These sinusoids may reduce blood flow resistance and subsequently increase transplacental exchange capacity. A microvascular corrosion cast of the cotyledon was cup-shaped with wide and narrow sides. Cotyledonary vessels entered and left the cotyledon from the narrow side. A cotyledonary artery gave proximal collateral branches immediately after entering the cotyledon and then further branched to supply the remaining portion of the cotyledon. Vessel branches broke into a mesh of capillaries forming the fetal vascular villi. Fetal villi that were nearest to the center of the cotyledon were the longest. Capillaries forming villi were in the form of a web-like mesh, were irregular in size and had sinusoidal dilations. The architecture of the cotyledon at day 90 was similar to day 50, but the vascularity increased. Branching of the fetal villi became more abundant. This extensive branching presumably allows a higher degree of invasion and surface contact to maternal tissues. At day 130, the distal portions of the fetal villi showed low ridges and troughs to increase the surface area for diffusion. Branching of fetal villi appears to influence the elaboration of maternal crypts in all stages of gestation. However, correspondence between crypts and villi is restricted to distal portions of fetal villi.

Fig. 1

A photographic image of a microvascular corrosion cast of a caruncle from a pregnant ewe at day 50 that has been coated with gold/palladium. Branches and tributaries of radial vessels (BRV) pursue a tortuous course to and from the base of the caruncle and ramify on its maternal surface (shown surface). Scale bar = 3 mm.

Fig. 2

Scanning electron micrograph of a microvascular corrosion cast of a caruncle from a pregnant ewe at day 50 showing that branches of radial arteries (BRA) bend and follow the convex contour of the maternal surface, where they give rise to stem arteries. Scale bar = 1 mm.

Fig. 3

Scanning electron micrograph of a microvascular corrosion cast of a caruncle from a pregnant ewe at day 50 showing the angle of branching of stem arteries. They tend to run parallel to each other and branch in a narrow angle (arrows). Scale bar = 100 μm.

Fig. 4

Scanning electron micrograph of a microvascular corrosion cast of a caruncle from a pregnant ewe at day 50 viewed from the fetal side, displaying maternal crypts (CR). CS, capillary sinusoid. Scale bar = 100 μm.

Fig. 5

Scanning electron micrograph of a microvascular corrosion cast of a sectioned caruncle from a pregnant ewe at day 50 viewed from an angle perpendicular to the longitudinal axis of the caruncle displaying maternal crypts (CR). Scale bar = 100 μm.

Fig. 6

Scanning electron micrograph of a microvascular corrosion cast of an artery (A) and vein (B). Note the impression patterns made by the endothelial cell borders and nuclei. On an artery (a in A), they are deep, slender and arranged parallel to the longitudinal axis of the vessel. On a vein (v in B), they are shallow, more round and randomly oriented. Scale bar = 10 μm in A and 100 μm in B.

Fig. 7

Scanning electron micrograph of a microvascular corrosion cast of a sectioned cotyledon from a pregnant ewe at day 50 showing cotyledonary vessels (CV) entering the cotyledon from its narrow end. BCV, branches of cotyledonary vessels; FV, fetal villi. Spaces (S) between villi are for interdigitation with maternal tissues. Scale bar = 1 mm.

Fig. 8

Scanning electron micrograph of a microvascular corrosion cast of a cotyledon from a pregnant ewe at day 50 viewed from the maternal side displaying fetal villi (FV) (A). Spaces (S) between villi are for interdigitation with maternal tissues. (B) Capillary sinusoids (CS) on the fetal villi. Scale bar = 100 μm.

Fig. 9

Scanning electron micrograph of a microvascular corrosion cast of a caruncle from a pregnant ewe at day 90 viewed from the fetal side. Note the presence of deep crypts (CR) and capillary sinusoids (CS). Scale bar = 100 μm.

Fig. 10

Scanning electron micrograph of a microvascular corrosion cast of a sectioned cotyledon from a pregnant ewe at day 90. Note the increased branching of cotyledonary vessels (CV). Scale bar = 1 mm.

Fig. 11

Scanning electron micrograph of a microvascular corrosion cast of a cotyledon from a pregnant ewe at day 90 viewed from the maternal side showing extensive branching of fetal villi. The entire image is filled with fetal villi. Scale bar = 100 μm.

Fig. 12

Scanning electron micrograph of a microvascular corrosion cast of a sectioned cotyledon from a pregnant ewe at day 90 displaying the depth of the spaces (S) where the maternal tissues interdigitate with the fetal tissues. Scale bar = 100 μm.

Fig. 13

Scanning electron micrograph of a microvascular corrosion cast of a sectioned caruncle from a pregnant ewe at day 130 displaying the depth of the crypts (CR). The fetal surface of the caruncle is at the lower right hand corner. Scale bar = 1 mm.

Fig. 14

Scanning electron micrograph of a microvascular corrosion cast of a cotyledon from a pregnant ewe at day 130 viewed from the maternal side displaying ridges (Rd) and troughs (Tr) on the distal portions of fetal villi. Scale bar = 100 μm.