Rheological and Physiological Consequences of Conversion of the Maternal Spiral Arteries for Uteroplacental Blood Flow during Human Pregnancy

Abstract

Physiological conversion of the maternal spiral arteries is key to a successful human pregnancy. It involves loss of smooth muscle and the elastic lamina from the vessel wall as far as the inner third of the myometrium, and is associated with a 5–10-fold dilation at the vessel mouth. Failure of conversion accompanies common complications of pregnancy, such as early-onset preeclampsia and fetal growth restriction. Here, we model the effects of terminal dilation on inflow of blood into the placental intervillous space at term, using dimensions in the literature derived from three-dimensional reconstructions. We observe that dilation slows the rate of flow from 2 to 3 m/s in the non-dilated part of an artery of 0.4–0.5 mm diameter to approximately 10 cm/s at the 2.5 mm diameter mouth, depending on the exact radius and viscosity. This rate predicts a transit time through the intervillous space of approximately 25 s, which matches observed times closely. The model shows that in the absence of conversion blood will enter the intervillous space as a turbulent jet at rates of 1–2 m/s. We speculate that the high momentum will damage villous architecture, rupturing anchoring villi and creating echogenic cystic lesions as evidenced by ultrasound. The retention of smooth muscle will also increase the risk of spontaneous vasoconstriction and ischaemia–reperfusion injury, generating oxidative stress. Dilation has a surprisingly modest impact on total blood flow, and so we suggest the placental pathology associated with deficient conversion is dominated by rheological consequences rather than chronic hypoxia.

The placenta: a multifaceted, transient organ

“…Hence, there is a danger that the fetal capillaries within the terminal villi will be compressed, impeding the umbilical circulation and preventing the formation of vasculosyncytial membranes [33]. Equally, the high velocity of maternal arterial blood flow can potentially cause mechanical damage to the delicate villous trees [34], with high shear rates also causing oxidative stress [35]. In many mammals, these dangers are avoided as there is either no or only limited invasion of the maternal tissues by the trophoblast, so-called epitheliochorial and endotheliochorial placentation respectively [36].…”

“…In the human, data collected from pregnant hysterectomies near term indicate the diameter of the spiral arteries increases from approximately 0.5 mm at the endometrium/ myometrium boundary to approximately 2.4 mm at their opening through the basal plate [37]. Mathematical modelling based on these dimensions predicts that as a consequence the velocity of maternal blood flow will reduce by an order of magnitude, from 2-3 m s 21 to approximately 10 cm s 21 [35].…”

Alterations in maternal and fetal heart functions accompany failed spiral arterial remodeling in pregnant mice

“…SA remodeling slows maternal blood flow, minimizes turbulence and optimizes exchange time with the fetal circulation. 6 Decidual lymphocytes, mainly uterine natural killer (uNK) cells, contribute to early stages of decidual SA transformation through cytokine secretion [7][8][9][10] as do mechanical flow properties such as shear forces and pressure. 11 The systemic circulatory changes of early normal pregnancy include increases in cardiac output, blood volume and glomerular filtration rate 12,13 that result in an overall maternal state of high blood flow with low vascular resistance.…”

Purinas y ácido úrico en pre-eclampsia: interacciones fisiopatológicas y proyecciones en investigación

“…En este escenario, los vasos espirales maternos mantienen su capacidad de contracción, y pueden provocar un flujo intermitente de sangre hacia la placenta asociado a un aumento en la presión de perfusión; lo que generaría a su vez, un continuo estrés de roce sobre las vellosidades placentarias, y fundamentalmente sobre el sincitiotrofoblasto (que está en directo contacto con la circulación materna) 12 . Estos fenómenos desencadenarían daño celular (i.e., necrosis), lo cual generaría el desprendimiento y liberación de fragmentos celulares (micropartículas o nanopartículas) desde la placenta hacia la circulación materna 13 .…”

“…Al mismo tiempo, estos cambios generarían un cír-culo vicioso que afectaría continuamente el flujo sanguíneo placentario, y con ello, nuevamente comprometerían la función endotelial materna. A su vez, la disfunción endotelial materna, provocaría similar alteración a nivel fetal; lo cual se traduciría en mayor riesgo cardiovascular luego del embarazo tanto en la madre como en su descendencia 12,14 .…”