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(A) Classic drawing of the placenta by Ranice W. Crosby, showing structure and circulation, based on Elisabeth Ramsey's work. (B) Spiral artery jet entering the intervillous space from the utero‐placental interface (yellow line; UPI) at 15 weeks’ pregnancy. (C) Confocal microscopy section of a 9‐week villus with CD31‐stained vessels and cords (Lisman et al. Human Reprod 2007). (D) Detailed drawing of arcuate‐, radial‐ and spiral arteries. (E) 3D‐VR image of spiral‐ and radial arteries at the UPI of a 9‐week pregnancy. (F) Area of interest used in automated 3D power Doppler fractional moving blood volume measurements from the whole UPI to 5 mm in the intervillous space (Collins et al. Plos One 2017;12:e0178675).

(A) Classic drawing of the placenta by Ranice W. Crosby, showing structure and circulation, based on Elisabeth Ramsey's work. (B) Spiral artery jet entering the intervillous space from the utero‐placental interface (yellow line; UPI) at 15 weeks’ pregnancy. (C) Confocal microscopy section of a 9‐week villus with CD31‐stained vessels and cords (Lisman et al. Human Reprod 2007). (D) Detailed drawing of arcuate‐, radial‐ and spiral arteries. (E) 3D‐VR image of spiral‐ and radial arteries at the UPI of a 9‐week pregnancy. (F) Area of interest used in automated 3D power Doppler fractional moving blood volume measurements from the whole UPI to 5 mm in the intervillous space (Collins et al. Plos One 2017;12:e0178675).

Citations

... This approach is, of course, not suitable for in vivo assessment and longitudinal data collection, which requires non-invasive testing in ongoing pregnancies (Roberts et al., 2017;Maric-Bilkan et al., 2019). In the last decade, several study groups, including our own, have developed new non-invasive imaging methods for the in vivo investigation of utero-placental vascular development in early pregnancy (Mathewlynn and Collins, 2019;Exalto et al., 2021). The application of offline image processing has been key in this research (Elsayes et al., 2009;Collins et al., 2012a,b;Roberts et al., 2017;Stevenson et al., 2018;Mathewlynn and Collins, 2019;Ridder et al., 2019). ...
Article
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STUDY QUESTION Can three-dimensional (3D) Power Doppler (PD) ultrasound and a skeletonization algorithm be used to assess first-trimester development of the utero-placental vascular morphology? SUMMARY ANSWER The application of 3D PD ultrasonography and a skeletonization algorithm facilitates morphologic assessment of utero-placental vascular development in the first trimester and reveals less advanced vascular morphologic development in pregnancies with placenta-related complications than in pregnancies without placenta-related complications. WHAT IS KNOWN ALREADY Suboptimal development of the utero-placental vasculature is one of the main contributors to the periconceptional origin of placenta-related complications. The nature and attribution of aberrant vascular structure and branching patterns remain unclear, as validated markers monitoring first-trimester utero-placental vascular morphologic development are lacking. STUDY DESIGN, SIZE, DURATION In this prospective observational cohort, 214 ongoing pregnancies were included before 10 weeks gestational age (GA) at a tertiary hospital between January 2017 and July 2018, as a subcohort of the ongoing Rotterdam Periconception Cohort study. PARTICIPANTS/MATERIALS, SETTING, METHODS By combining 3D PD ultrasonography and virtual reality, utero-placental vascular volume (uPVV) measurements were obtained at 7, 9 and 11 weeks GA. A skeletonization algorithm was applied to the uPVV measurements to generate the utero-placental vascular skeleton (uPVS), a network-like structure containing morphologic characteristics of the vasculature. Quantification of vascular morphology was performed by assigning a morphologic characteristic to each voxel in the uPVS (end-, vessel-, bifurcation- or crossing-point) and calculating total vascular network length. A Mann–Whitney U test was performed to investigate differences in morphologic development of the first-trimester utero-placental vasculature between pregnancies with and without placenta-related complications. Linear mixed models were used to estimate trajectories of the morphologic characteristics in the first trimester. MAIN RESULTS AND THE ROLE OF CHANCE All morphologic characteristics of the utero-placental vasculature increased significantly in the first trimester (P < 0.005). In pregnancies with placenta-related complications (n = 54), utero-placental vascular branching was significantly less advanced at 9 weeks GA (vessel points P = 0.040, bifurcation points P = 0.050, crossing points P = 0.020, total network length P = 0.023). Morphologic growth trajectories remained similar after adjustment for parity, conception mode, foetal sex and occurrence of placenta-related complications. LIMITATIONS, REASONS FOR CAUTION The tertiary setting of this prospective observational study provides high internal, but possibly limited external, validity. Extrapolation of the study’s findings should therefore be addressed with caution. WIDER IMPLICATIONS OF THE FINDINGS The uPVS enables assessment of morphologic development of the first-trimester utero-placental vasculature. Further investigation of this innovative methodology needs to determine its added value for the assessment of (patho-) physiological utero-placental vascular development. STUDY FUNDING/COMPETING INTEREST(S) This research was funded by the Department of Obstetrics and Gynecology of the Erasmus MC, University Medical Centre, Rotterdam, The Netherlands. There are no conflicts of interest. TRIAL REGISTRATION NUMBER Registered at the Dutch Trial Register (NTR6854).
... 15,16 When Virtual Reality (VR) is combined with 3D power Doppler ultrasonography, uteroplacental vascularisation volumes (uPVV) can be measured in a reproducible and accurate manner, using depth perception and offering 3D interaction by creating a hologram from the 3D ultrasound data set. [17][18][19] The uPVV measurements were performed on a 3D VR desktop system, allowing for more precise and detailed evaluation of placental structures because of the option of image enlargement, image rotation and the actual use of all 3D dimensions. 19 As such, uPVV in the first trimester can be considered a marker representing not only maternal haemodynamic adaptation to pregnancy but also placental development. ...
Article
Full-text available
Objective: To investigate whether first-trimester maternal haemodynamic adaptation impacts placental, embryonic and fetal development as well as birth outcomes in pregnancies with and without placenta-related complications. Design: Prospective observational cohort. Setting: A Dutch tertiary hospital. Population: Two hundred and fourteen ongoing pregnancies. Methods: At 7, 9 and 11 weeks of gestation, we assessed maternal haemodynamic adaptation (mean arterial blood pressure [MAP], uterine artery [UtA] blood flow) and placental development (placental volume [PV], uteroplacental vascular volume [uPVV]) using three-dimensional power Doppler ultrasound volumes, and embryonic development (crown-rump length, embryonic volume). At 22 and 32 weeks of gestation, fetal development was assessed by estimated fetal weight. Birth outcomes (birthweight, placental weight) were extracted from medical records. Linear mixed modelling and linear regression analyses were applied. Main outcome measures: Birthweight centile and placental weight. Results: In placenta-related complications (n= 55, 25.7%), reduced haemodynamic adaptation, i.e. higher UtA pulsatility index (PI) and resistance index (RI) trajectories, was associated with smaller increase in PV (β = -0.559, 95% CI -0.841 to -0.278, P< 0.001; β = -0.579, 95% CI -0.878 to -0.280, P< 0.001) and uPVV trajectories (UtA PI: β = -0.301, 95% CI -0.578 to -0.023, P= 0.034). At birth, reduced haemodynamic adaptation was associated with lower placental weight (UtA PI: β = -0.502, 95% CI -0.922 to -0.082, P= 0.022; UtA RI: β = -0.435, 95% CI -0.839 to -0.032, P= 0.036). In pregnancies without placenta-related complications, higher MAP trajectories were positively associated with birthweight centile (β = 0.398, 95% CI 0.049-0.748, P= 0.025). Conclusions: Reduced first-trimester maternal haemodynamic adaptation impacts both placental size and vascularisation and birthweight centile, in particular in pregnancies with placenta-related complications. Tweetable abstract: Reduced first-trimester maternal haemodynamic adaptation to pregnancy impairs early placental development.