Computational Fluid Dynamic Simulations of Maternal Circulation: Wall Shear Stress in the Human Placenta and Its Biological Implications

PLoS One. 2016 Jan 27;11(1):e0147262. doi: 10.1371/journal.pone.0147262. eCollection 2016.

Abstract

Introduction: In the human placenta the maternal blood circulates in the intervillous space (IVS). The syncytiotrophoblast (STB) is in direct contact with maternal blood. The wall shear stress (WSS) exerted by the maternal blood flow on the STB has not been evaluated. Our objective was to determine the physiological WSS exerted on the surface of the STB during the third trimester of pregnancy.

Material and methods: To gain insight into the shear stress levels that the STB is expected to experience in vivo, we have formulated three different computational models of varying levels of complexity that reflect different physical representations of the IVS. Computations of the flow fields in all models were performed using the CFD module of the finite element code COMSOL Multiphysics 4.4. The mean velocity of maternal blood in the IVS during the third trimester was measured in vivo with dynamic MRI (0.94±0.14 mm.s-1). To investigate if the in silico results are consistent with physiological observations, we studied the cytoadhesion of human parasitized (Plasmodium falciparum) erythrocytes to primary human STB cultures, in flow conditions with different WSS values.

Results: The WSS applied to the STB is highly heterogeneous in the IVS. The estimated average values are relatively low (0.5±0.2 to 2.3±1.1 dyn.cm-2). The increase of WSS from 0.15 to 5 dyn.cm-2 was associated with a significant decrease of infected erythrocyte cytoadhesion. No cytoadhesion of infected erythrocytes was observed above 5 dyn.cm-2 applied for one hour.

Conclusion: Our study provides for the first time a WSS estimation in the maternal placental circulation. In spite of high maternal blood flow rates, the average WSS applied at the surface of the chorionic villi is low (<5 dyn.cm-2). These results provide the basis for future physiologically-relevant in vitro studies of the biological effects of WSS on the STB.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blood Flow Velocity / physiology
  • Computer Simulation*
  • Erythrocytes / physiology
  • Female
  • Hemodynamics / physiology
  • Humans
  • Hydrodynamics
  • Models, Biological*
  • Placenta / blood supply
  • Placenta / physiology*
  • Pregnancy
  • Shear Strength
  • Stress, Mechanical*

Grants and funding

EL received a grant from Institut National de la Santé et de la Recherche Médicale (France) to perform this work. This work was supported by the PremUP Foundation. This work was partially funded by a permanent endowment in Cardiovascular Cellular Engineering from the AXA Research Fund (to AIB). MB was supported by an international summer scholarship from Ecole Polytechnique. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.