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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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a) A photomicrograph of the human endometrium on the fourth day of menstruation showing an eroded spiral artery (arrowed) projecting freely into the uterine lumen. b) A photomicrograph of spiral arteries in a rhesus monkey during the phase of ovulation injected with India ink in gelatin. The arrow marks the endometrial–myometrial boundary, and a marked constriction (asterisked) can be seen in the spiral artery in the junctional zone just below. c) Reconstruction from serial sections of a converted spiral artery passing through the myometrium (M) and endometrium (E) before opening into the intervillous space through the basal plate of a term placenta. The widest dimension of the opening is given as 2.4 mm. Reproduced from Refs. [83], [15] and [16] respectively with permission of the Carnegie Institute of Washington.
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fig1: a) A photomicrograph of the human endometrium on the fourth day of menstruation showing an eroded spiral artery (arrowed) projecting freely into the uterine lumen. b) A photomicrograph of spiral arteries in a rhesus monkey during the phase of ovulation injected with India ink in gelatin. The arrow marks the endometrial–myometrial boundary, and a marked constriction (asterisked) can be seen in the spiral artery in the junctional zone just below. c) Reconstruction from serial sections of a converted spiral artery passing through the myometrium (M) and endometrium (E) before opening into the intervillous space through the basal plate of a term placenta. The widest dimension of the opening is given as 2.4 mm. Reproduced from Refs. [83], [15] and [16] respectively with permission of the Carnegie Institute of Washington.

Mentions: Most of these pregnancy complications are unique to the human, and may relate to the fact that our invasive form of implantation, and subsequent haemochorial placentation, poses special haemodynamic challenges. These fall into two principal categories. Firstly, the spiral arteries of the human uterus perform contrasting roles during the menstrual cycle and in pregnancy. During the cycle they supply the endometrial stroma and the glands in preparation for implantation by the blastocyst, yet must retain the ability to contract as the upper layers of decidualized endometrium are shed during menstruation, in order to limit blood loss (Fig. 1a). Following implantation and embryogenesis, however, an inviolable supply is required to meet fetal demands, beginning in the second trimester but becoming critical towards the end of gestation due to fetal growth. Secondly, in the haemochorial situation the delicate fetal villi perfused by the low-pressure developing fetal circulation are immersed in maternal blood circulating at a potentially much higher pressure and velocity. It is essential, therefore, that the spiral arteries adapt so that they are capable of delivering large quantities of blood to the placental intervillous space, but at an appropriate rate and pressure. Conversion of the spiral arteries reconciles these various demands, and is key to a successful pregnancy.


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)

a) A photomicrograph of the human endometrium on the fourth day of menstruation showing an eroded spiral artery (arrowed) projecting freely into the uterine lumen. b) A photomicrograph of spiral arteries in a rhesus monkey during the phase of ovulation injected with India ink in gelatin. The arrow marks the endometrial–myometrial boundary, and a marked constriction (asterisked) can be seen in the spiral artery in the junctional zone just below. c) Reconstruction from serial sections of a converted spiral artery passing through the myometrium (M) and endometrium (E) before opening into the intervillous space through the basal plate of a term placenta. The widest dimension of the opening is given as 2.4 mm. Reproduced from Refs. [83], [15] and [16] respectively with permission of the Carnegie Institute of Washington.
© Copyright Policy
Related In: Results  -  Collection

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

fig1: a) A photomicrograph of the human endometrium on the fourth day of menstruation showing an eroded spiral artery (arrowed) projecting freely into the uterine lumen. b) A photomicrograph of spiral arteries in a rhesus monkey during the phase of ovulation injected with India ink in gelatin. The arrow marks the endometrial–myometrial boundary, and a marked constriction (asterisked) can be seen in the spiral artery in the junctional zone just below. c) Reconstruction from serial sections of a converted spiral artery passing through the myometrium (M) and endometrium (E) before opening into the intervillous space through the basal plate of a term placenta. The widest dimension of the opening is given as 2.4 mm. Reproduced from Refs. [83], [15] and [16] respectively with permission of the Carnegie Institute of Washington.
Mentions: Most of these pregnancy complications are unique to the human, and may relate to the fact that our invasive form of implantation, and subsequent haemochorial placentation, poses special haemodynamic challenges. These fall into two principal categories. Firstly, the spiral arteries of the human uterus perform contrasting roles during the menstrual cycle and in pregnancy. During the cycle they supply the endometrial stroma and the glands in preparation for implantation by the blastocyst, yet must retain the ability to contract as the upper layers of decidualized endometrium are shed during menstruation, in order to limit blood loss (Fig. 1a). Following implantation and embryogenesis, however, an inviolable supply is required to meet fetal demands, beginning in the second trimester but becoming critical towards the end of gestation due to fetal growth. Secondly, in the haemochorial situation the delicate fetal villi perfused by the low-pressure developing fetal circulation are immersed in maternal blood circulating at a potentially much higher pressure and velocity. It is essential, therefore, that the spiral arteries adapt so that they are capable of delivering large quantities of blood to the placental intervillous space, but at an appropriate rate and pressure. Conversion of the spiral arteries reconciles these various demands, and is key to a successful pregnancy.

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