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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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Representative real-time and colour/pulsed Doppler images of placental development at 12 weeks gestation. a) Transverse view of body of uterus outlining the uterine wall (outer line) with an anteriorly located placenta (inner line). b) The same view with colour Doppler (at conventional arterial setting of 38 cm/s). Note flow signals in this range are confined to the myometrium. c) Colour/pulsed Doppler identification of the proximal left uterine artery. Note low-impedance waveform with high (135 cm/s) peak systolic velocity. d) Colour-pulsed Doppler identification of arterial signals in the lateral myometrium, above the left proximal uterine artery. Note low-impedance waveform similar to Fig. 3c but at lower (56 cm/s) velocity. No such signals are observed entering the basal plate of the placenta. Whilst these images suggest intra-myometrial shunting at the end of the first trimester, the extent to which this phenomenon occurs in the second and third trimesters requires further research.
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fig3: Representative real-time and colour/pulsed Doppler images of placental development at 12 weeks gestation. a) Transverse view of body of uterus outlining the uterine wall (outer line) with an anteriorly located placenta (inner line). b) The same view with colour Doppler (at conventional arterial setting of 38 cm/s). Note flow signals in this range are confined to the myometrium. c) Colour/pulsed Doppler identification of the proximal left uterine artery. Note low-impedance waveform with high (135 cm/s) peak systolic velocity. d) Colour-pulsed Doppler identification of arterial signals in the lateral myometrium, above the left proximal uterine artery. Note low-impedance waveform similar to Fig. 3c but at lower (56 cm/s) velocity. No such signals are observed entering the basal plate of the placenta. Whilst these images suggest intra-myometrial shunting at the end of the first trimester, the extent to which this phenomenon occurs in the second and third trimesters requires further research.

Mentions: The final outcome was elegantly demonstrated by Harris and Ramsey, who performed three-dimensional reconstructions of a number of spiral arteries from hysterectomy specimens at various stages of pregnancy [16]. They observed that the arteries undergo a generalised, but non-uniform, dilation as pregnancy advances, with considerable variation in size between arteries within the same specimen, and even at different points along individual arteries. Most importantly, they found that the terminal coils of the spiral arteries are enormously dilated, often reaching 2–3 mm in diameter. This transition is quite abrupt, so that the dilated segments form a funnel-shaped chamber that opens through the basal plate, often with a slit-like orifice. Thus, they depicted the terminal part of a spiral artery at term having a maximum diameter of 2.4 mm (Fig. 1c), which represents an approximately 4-fold increase in the diameter of the vessel at the myometrial–endometrial boundary and within the endometrium. Why only the final section of a converted artery is involved in this exaggerated dilatation is not clear, but it may be sculpted by the extent of the endovascular invasion of the vessels in early pregnancy. Initially the invasion is so extensive that the tips of the arteries are effectively plugged by the trophoblast cells [14,20], and so there is little, if any, maternal blood flow into the placenta (Fig. 3).


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)

Representative real-time and colour/pulsed Doppler images of placental development at 12 weeks gestation. a) Transverse view of body of uterus outlining the uterine wall (outer line) with an anteriorly located placenta (inner line). b) The same view with colour Doppler (at conventional arterial setting of 38 cm/s). Note flow signals in this range are confined to the myometrium. c) Colour/pulsed Doppler identification of the proximal left uterine artery. Note low-impedance waveform with high (135 cm/s) peak systolic velocity. d) Colour-pulsed Doppler identification of arterial signals in the lateral myometrium, above the left proximal uterine artery. Note low-impedance waveform similar to Fig. 3c but at lower (56 cm/s) velocity. No such signals are observed entering the basal plate of the placenta. Whilst these images suggest intra-myometrial shunting at the end of the first trimester, the extent to which this phenomenon occurs in the second and third trimesters requires further research.
© Copyright Policy
Related In: Results  -  Collection

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

fig3: Representative real-time and colour/pulsed Doppler images of placental development at 12 weeks gestation. a) Transverse view of body of uterus outlining the uterine wall (outer line) with an anteriorly located placenta (inner line). b) The same view with colour Doppler (at conventional arterial setting of 38 cm/s). Note flow signals in this range are confined to the myometrium. c) Colour/pulsed Doppler identification of the proximal left uterine artery. Note low-impedance waveform with high (135 cm/s) peak systolic velocity. d) Colour-pulsed Doppler identification of arterial signals in the lateral myometrium, above the left proximal uterine artery. Note low-impedance waveform similar to Fig. 3c but at lower (56 cm/s) velocity. No such signals are observed entering the basal plate of the placenta. Whilst these images suggest intra-myometrial shunting at the end of the first trimester, the extent to which this phenomenon occurs in the second and third trimesters requires further research.
Mentions: The final outcome was elegantly demonstrated by Harris and Ramsey, who performed three-dimensional reconstructions of a number of spiral arteries from hysterectomy specimens at various stages of pregnancy [16]. They observed that the arteries undergo a generalised, but non-uniform, dilation as pregnancy advances, with considerable variation in size between arteries within the same specimen, and even at different points along individual arteries. Most importantly, they found that the terminal coils of the spiral arteries are enormously dilated, often reaching 2–3 mm in diameter. This transition is quite abrupt, so that the dilated segments form a funnel-shaped chamber that opens through the basal plate, often with a slit-like orifice. Thus, they depicted the terminal part of a spiral artery at term having a maximum diameter of 2.4 mm (Fig. 1c), which represents an approximately 4-fold increase in the diameter of the vessel at the myometrial–endometrial boundary and within the endometrium. Why only the final section of a converted artery is involved in this exaggerated dilatation is not clear, but it may be sculpted by the extent of the endovascular invasion of the vessels in early pregnancy. Initially the invasion is so extensive that the tips of the arteries are effectively plugged by the trophoblast cells [14,20], and so there is little, if any, maternal blood flow into the placenta (Fig. 3).

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