Arterio-venous fetoplacental vascular geometry and hemodynamics in the mouse placenta

Abstract

Introduction: The fetoplacental vasculature network is essential for the exchange of nutrients, gases and wastes with the maternal circulation and for normal fetal development. The present study quantitatively compares arterial and venous morphological and functional differences in the mouse fetoplacental vascular network.

Methods: High resolution X-ray micro-computed tomography was used to visualize the 3D geometry of the arterial and venous fetoplacental vasculature in embryonic day 15.5 CD-1 mice (n = 5). Automated image analysis was used to measure the vascular geometry of the approximately 4100 arterial segments and 3200 venous segments per specimen to simulate blood flow through these networks.

Results: Both the arterial and venous trees demonstrated a hierarchical branching structure with 8 or 9 (arterial) or 8 (venous) orders. The venous tree was smaller in volume and overall dimensions than the arterial tree. Venous vessel diameters increased more rapidly than arteries with each successive order, leading to lower overall resistance, although the umbilical vein was notably smaller and of higher resistance than these scaling relationships would predict. Simulation of blood flow for these vascular networks showed that 57% of total resistance resides in the umbilical artery and arterial tree, 17% in the capillary bed, and 26% in the venous tree and umbilical vein.

Discussion: A detailed examination of the mouse fetoplacental arterial and venous tree revealed features, such as the distribution of resistance and the dimension of the venous tree, that were both morphologically distinct from other vascular beds and that appeared adapted to the specialized requirements of sustaining a fetus.

Keywords: Arteries; Fetoplacental vasculature; Hemodynamics; Micro-computed tomography; Mouse; Veins.

Figure 1. Vascular Tree Dimensions

Maximum intensity projection images of example (A) arterial and (D) venous trees. (B) Umbilical vessel diameter, (C) volume, (E) span and (F) depth of the arterial (black bars) and venous (open bars) vasculatures are shown as mean ± SEM where n=5 placentas/group. *p<0.05. Scale bar = 1 mm.

Figure 2. Distribution and Number of Vessel Segments

(A) The cumulative number of vessel segments at a given diameter are shown for arteries (solid line) and veins (hatched line). The shaded grey area represents SEM. (B) The total number of vessel segments and (C) diameter scaling coefficient are shown for the arterial (black bars) and venous (open bars) vasculatures. Hatched black line in (C) denotes a scaling coefficient of 3, which is predicted by Murray’s Law. Data shown as mean ± SEM where n =5 placentas/group. *p<0.05.

Figure 3. Strahler Ordering of the Vascular Tree

Colored-rendered isosurfaces showing the Strahler order of each vessel for example (A) arterial and (D) venous trees. (B) Number of segments, (C) average diameter, (E) average length and (F) length-to-diameter ratio with Strahler order number of the arterial (black circles) and venous (open squares) vasculatures. Percent difference in average diameter between arteries and veins are shown below the arterial data in (C). The measurements of vessel length are only reported for orders 1–7. The length of the umbilical cord in the specimens is dependent on where the cord has been cut after perfusion. Data are presented as mean ± SEM where n=5 placentas/group. *p<0.05.

Figure 4

Distribution of total fetoplacental vascular resistance determined by computational flow modeling.