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Research Papers

Association of Placental Jets and Mega-Jets With Reduced Villous Density

[+] Author and Article Information
Rojan Saghian

Auckland Bioengineering Institute,
University of Auckland,
Auckland 1142, New Zealand
e-mail: rsag063@aucklanduni.ac.nz

Joanna L. James

Department of Obstetrics and Gynaecology,
Faculty of Medical and Health Sciences,
University of Auckland,
Auckland 1023, New Zealand
e-mail: j.james@auckland.ac.nz

Merryn H. Tawhai

Professor
Auckland Bioengineering Institute,
University of Auckland,
Auckland 1142, New Zealand
e-mail: m.tawhai@auckland.ac.nz

Sally L. Collins

Nuffield Department of Obstetrics
and Gynaecology,
University of Oxford,
Oxford OX3 9DU, UK
e-mail: sally.collins@obs-gyn.ox.ac.uk

Alys R. Clark

Auckland Bioengineering Institute,
University of Auckland,
Auckland 1142, New Zealand
e-mail: alys.clark@auckland.ac.nz

1Corresponding authors.

Manuscript received July 13, 2016; final manuscript received February 14, 2017; published online March 20, 2017. Assoc. Editor: Thao (Vicky) Nguyen.

J Biomech Eng 139(5), 051001 (Mar 20, 2017) (10 pages) Paper No: BIO-16-1293; doi: 10.1115/1.4036145 History: Received July 13, 2016; Revised February 14, 2017

Spiral arteries (SAs) lie at the interface between the uterus and placenta, and supply nutrients to the placental surface. Maternal blood circulation is separated from the fetal circulation by structures called villous trees. SAs are transformed in early pregnancy from tightly coiled vessels to large high-capacity channels, which is believed to facilitate an increased maternal blood flow throughout pregnancy with minimal increase in velocity, preventing damage to delicate villous trees. Significant maternal blood flow velocities have been theorized in the space surrounding the villi (the intervillous space, IVS), particularly when SA conversion is inadequate, but have only recently been visualized reliably using pulsed wave Doppler ultrasonography. Here, we present a computational model of blood flow from SA openings, allowing prediction of IVS properties based on jet length. We show that jets of flow observed by ultrasound are likely correlated with increased IVS porosity near the SA mouth and propose that observed mega-jets (flow penetrating more than half the placental thickness) are only possible when SAs open to regions of the placenta with very sparse villous structures. We postulate that IVS tissue density must decrease at the SA mouth through gestation, supporting the hypothesis that blood flow from SAs influences villous tree development.

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Figures

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Fig. 1

(a) The progression of SA remodeling. At the start of pregnancy SAs are small tortuous vessels and they are progressively remodeled by trophoblast to have large funnel-like openings. (b) Flow from SAs enters the intervillous space and supplies placental tissue with nutrients. Inadequate SA remodeling has been theorized to induce an excessive blood flow velocity and pressure on the placental tissue.

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Fig. 2

A schematic of the idealized placentome represented in our model. Geometric parameters are dependent on gestational age.

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Fig. 4

The relationship between ultrasonographic measurements of length and jet mouth velocity at 11 + 0 to 13 + 6 weeks of pregnancy. Trends are similar at later stages of pregnancy. There is no significant relationship between the two parameters. This lack of relationship, and the predictions that flow velocity at the SA mouth must be much higher than ultrasound measured values to predict accurate jet length, suggest that the density of villous tissue distal to the SA mouth must be a primary determinant of jet penetration.

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Fig. 3

Ultrasonographic measurements of jet length in normal pregnancies (solid line, dashed lines represent 95% confidence intervals, from Ref. [11] compared with jet length predicted by the model with ultrasound measured flow velocities at the SA mouth (crosses represent predictions at nominal parameters for each gestation, error bars represent jet length predicted at minimum and maximum of 95% confidence range for velocity at SA mouth). The model underpredicts jet length at all but the earliest gestation. Note that the predicted jet length at 35 weeks is small, but nonzero, and the level of jet length is defined as flow velocity less than 1 × 10−1 m s−1 for consistency with ultrasound, so there is still circulation predicted in the IVS under these conditions.

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Fig. 5

(a) The predicted volume fraction of the villous tissue required to generate a jet with average jet lengths, a mega-jet and a comparison to the whole placenta tissue volume fraction determined from literature data. (b) The predicted length of a villus-free cavity required to produce jets and mega-jets compared to average placental thickness. Both predictions suggest a reduced tissue density, compared with the whole placenta average, at the opening of SA where significant jets are observed, particularly in the later stages of gestation.

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Fig. 6

Model predictions of (a) average blood flow velocity through the SA and into the placental tissue in a region of the same diameter as the opening of the SA, and (b) average blood pressure in a spiral artery cross section relative to minimum pressure along the z-axis at 25 weeks gestation. Results shown represent a placentome with a 2 mm central cavity (average ψ = 0.21), a 5 mm central cavity (average ψ = 0.21), no central cavity (average ψ = 0.21), and a homogenously reduced tissue volume fraction (ψ = 0.02). All simulations have the same fixed inlet velocity. Visible jet length is sensitive to the structure of villous tissue distal to the SA opening.

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Fig. 7

(a) The predicted jet length for a given central cavity long axis dimension at 35 weeks gestation. Average jet length is given along with an expected range for mega-jet lengths based on data from Collins et al. [11]. Jet length is predicted to follow the size of the central cavity up to a maximum value at which the jet length becomes reduced compared with the length of the central cavity (the effect of reaching the porous placental tissue is no longer the dominant determinant of jet penetration). (b) The predicted proportion of jet length that must be comprised of a villus-free cavity to predict a jet and mega-jet through gestation. Early in gestation blood is able to penetrate significantly beyond the length of the cavity, however from approximately 20 weeks jet length becomes indicative of cavity length.

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