Physical and geometric determinants of transport in fetoplacental microvascular networks

Across mammalian species, solute exchange takes place in complex microvascular networks. In the human placenta, the primary exchange units are terminal villi that contain disordered networks of fetal capillaries and are surrounded externally by maternal blood. We show how the irregular internal structure of a terminal villus determines its exchange capacity for diverse solutes. Distilling geometric features into three parameters, obtained from image analysis and computational fluid dynamics, we capture archetypal features of the structure-function relationship of terminal villi using a simple algebraic approximation, revealing transitions between flow- and diffusion-limited transport at vessel and network levels. Our theory accommodates countercurrent effects, incorporates nonlinear blood rheology, and offers an efficient method for testing network robustness. Our results show how physical estimates of solute transport, based on carefully defined geometrical statistics, provide a viable method for linking placental structure and function and offer a framework for assessing transport in other microvascular systems.