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Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy.

Burton GJ, Woods AW, Jauniaux E, Kingdom JC - Placenta (2009)

Bottom Line: Physiological conversion of the maternal spiral arteries is key to a successful human pregnancy.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.

View Article: PubMed Central - PubMed

Affiliation: Centre for Trophoblast Research, University of Cambridge, Cambridge, UK. gjb2@cam.ac.uk

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 3m/s in the non-dilated part of an artery of 0.4-0.5mm diameter to approximately 10 cm/s at the 2.5mm diameter mouth, depending on the exact radius and viscosity. This rate predicts a transit time through the intervillous space of approximately 25s, 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 1-2m/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.

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Diagrammatic representation (not to scale) of the effects of spiral artery conversion on the inflow of maternal blood into the intervillous space and on lobule architecture predicted by modelling. Dilation of the distal segment in normal pregnancies will reduce the velocity of incoming blood, and the residual momentum will carry the blood into the central cavity (CC) of the lobule, from where it will disperse evenly through the villous tree. Transit time to the uterine vein is estimated to be in the order of 25–30 s, allowing adequate time for oxygen exchange. The pressure of the maternal blood, indicated in mmHg by the figures in blue, will drop across the non-dilated segment of the spiral artery, the dimensions of which are given alongside. In pathological pregnancies, where no or very limited conversion occurs, the maternal blood will enter the intervillous space at speeds of 1–2 m/s. The high Reynolds number predicts turbulent flow, indicated by the circular arrows. We suggest that the high momentum ruptures anchoring villi (asterisked) and displaces others to form echogenic cystic lesions (ECL) lined by thrombus (brown). The transit time will be reduced, so that oxygen exchange is impaired and blood leaves in the uterine vein with a higher oxygen concentration than normal. Trophoblastic microparticulate debris (dotted) may be dislodged from the villous surface, leading to maternal endothelial cell activation. Finally, the retention of smooth muscle cells (SMC) around the spiral artery will increase the risk of spontaneous vasoconstriction and ischaemia–reperfusion injury.
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fig6: Diagrammatic representation (not to scale) of the effects of spiral artery conversion on the inflow of maternal blood into the intervillous space and on lobule architecture predicted by modelling. Dilation of the distal segment in normal pregnancies will reduce the velocity of incoming blood, and the residual momentum will carry the blood into the central cavity (CC) of the lobule, from where it will disperse evenly through the villous tree. Transit time to the uterine vein is estimated to be in the order of 25–30 s, allowing adequate time for oxygen exchange. The pressure of the maternal blood, indicated in mmHg by the figures in blue, will drop across the non-dilated segment of the spiral artery, the dimensions of which are given alongside. In pathological pregnancies, where no or very limited conversion occurs, the maternal blood will enter the intervillous space at speeds of 1–2 m/s. The high Reynolds number predicts turbulent flow, indicated by the circular arrows. We suggest that the high momentum ruptures anchoring villi (asterisked) and displaces others to form echogenic cystic lesions (ECL) lined by thrombus (brown). The transit time will be reduced, so that oxygen exchange is impaired and blood leaves in the uterine vein with a higher oxygen concentration than normal. Trophoblastic microparticulate debris (dotted) may be dislodged from the villous surface, leading to maternal endothelial cell activation. Finally, the retention of smooth muscle cells (SMC) around the spiral artery will increase the risk of spontaneous vasoconstriction and ischaemia–reperfusion injury.

Mentions: The potential impact of the jets of maternal blood emerging from the arteries within the intervillous space depends on the distance they travel prior to meeting other tissues. Jets emerging from arteries with a diameter of 0.4 mm at a speed in the order of 1.0 m/s will tend to mix and entrain blood within the intervillous space, but may require distances of a few millimetres to centimetres to decelerate to speeds in the order of 10 cm/s. In contrast, the slower flow from the dilated arteries will already emerge at these lower speeds, and will continue to slow as it moves out. Therefore, the potential damage of the momentum flux in the inflowing blood will be considerably smaller if the distal end of the artery dilates (Fig. 6). Reynolds suggested that it is the force of the maternal arterial spurts that shapes the placental lobules towards the end of the first trimester and forms the central cavities [41]. However, if the incoming jet has too high a velocity it may create villous damage as will be discussed later.


Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy.

Burton GJ, Woods AW, Jauniaux E, Kingdom JC - Placenta (2009)

Diagrammatic representation (not to scale) of the effects of spiral artery conversion on the inflow of maternal blood into the intervillous space and on lobule architecture predicted by modelling. Dilation of the distal segment in normal pregnancies will reduce the velocity of incoming blood, and the residual momentum will carry the blood into the central cavity (CC) of the lobule, from where it will disperse evenly through the villous tree. Transit time to the uterine vein is estimated to be in the order of 25–30 s, allowing adequate time for oxygen exchange. The pressure of the maternal blood, indicated in mmHg by the figures in blue, will drop across the non-dilated segment of the spiral artery, the dimensions of which are given alongside. In pathological pregnancies, where no or very limited conversion occurs, the maternal blood will enter the intervillous space at speeds of 1–2 m/s. The high Reynolds number predicts turbulent flow, indicated by the circular arrows. We suggest that the high momentum ruptures anchoring villi (asterisked) and displaces others to form echogenic cystic lesions (ECL) lined by thrombus (brown). The transit time will be reduced, so that oxygen exchange is impaired and blood leaves in the uterine vein with a higher oxygen concentration than normal. Trophoblastic microparticulate debris (dotted) may be dislodged from the villous surface, leading to maternal endothelial cell activation. Finally, the retention of smooth muscle cells (SMC) around the spiral artery will increase the risk of spontaneous vasoconstriction and ischaemia–reperfusion injury.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2697319&req=5

fig6: Diagrammatic representation (not to scale) of the effects of spiral artery conversion on the inflow of maternal blood into the intervillous space and on lobule architecture predicted by modelling. Dilation of the distal segment in normal pregnancies will reduce the velocity of incoming blood, and the residual momentum will carry the blood into the central cavity (CC) of the lobule, from where it will disperse evenly through the villous tree. Transit time to the uterine vein is estimated to be in the order of 25–30 s, allowing adequate time for oxygen exchange. The pressure of the maternal blood, indicated in mmHg by the figures in blue, will drop across the non-dilated segment of the spiral artery, the dimensions of which are given alongside. In pathological pregnancies, where no or very limited conversion occurs, the maternal blood will enter the intervillous space at speeds of 1–2 m/s. The high Reynolds number predicts turbulent flow, indicated by the circular arrows. We suggest that the high momentum ruptures anchoring villi (asterisked) and displaces others to form echogenic cystic lesions (ECL) lined by thrombus (brown). The transit time will be reduced, so that oxygen exchange is impaired and blood leaves in the uterine vein with a higher oxygen concentration than normal. Trophoblastic microparticulate debris (dotted) may be dislodged from the villous surface, leading to maternal endothelial cell activation. Finally, the retention of smooth muscle cells (SMC) around the spiral artery will increase the risk of spontaneous vasoconstriction and ischaemia–reperfusion injury.
Mentions: The potential impact of the jets of maternal blood emerging from the arteries within the intervillous space depends on the distance they travel prior to meeting other tissues. Jets emerging from arteries with a diameter of 0.4 mm at a speed in the order of 1.0 m/s will tend to mix and entrain blood within the intervillous space, but may require distances of a few millimetres to centimetres to decelerate to speeds in the order of 10 cm/s. In contrast, the slower flow from the dilated arteries will already emerge at these lower speeds, and will continue to slow as it moves out. Therefore, the potential damage of the momentum flux in the inflowing blood will be considerably smaller if the distal end of the artery dilates (Fig. 6). Reynolds suggested that it is the force of the maternal arterial spurts that shapes the placental lobules towards the end of the first trimester and forms the central cavities [41]. However, if the incoming jet has too high a velocity it may create villous damage as will be discussed later.

Bottom Line: Physiological conversion of the maternal spiral arteries is key to a successful human pregnancy.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.

View Article: PubMed Central - PubMed

Affiliation: Centre for Trophoblast Research, University of Cambridge, Cambridge, UK. gjb2@cam.ac.uk

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 3m/s in the non-dilated part of an artery of 0.4-0.5mm diameter to approximately 10 cm/s at the 2.5mm diameter mouth, depending on the exact radius and viscosity. This rate predicts a transit time through the intervillous space of approximately 25s, 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 1-2m/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.

Show MeSH
Related in: MedlinePlus