First-trimester utero-placental (vascular) development and embryonic and fetal growth: The Rotterdam periconception cohort

Reijnders, Igna F.; Mulders, A.; Koster, Maria P. H.; Kropman, A.; Vos, E.S.; Koning, Anton H. J.; Willemsen, Sten P.; Rousian, Melek; Steegers, Eric A.P.; Steegers‐Theunissen, R.P.M.

doi:10.1016/j.placenta.2021.03.017

Cited by 12 publications

(6 citation statements)

References 41 publications

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“…7A). Both PV and uPVV increase significantly throughout the first trimester (Reijnders et al, 2021). The PV and the uPVV increased at a higher rate than the amounts of uPVS characteristics, resulting in a significant decrease in the density of vascular branching in PV (uPVS:PV ratio) (data not shown) and uPVV (uPVS:uPVV ratio) between 7-9-11 weeks GA (Fig.…”

Section: Upvs Development and Density Of Vascular Branching In The Fi...mentioning

confidence: 81%

Assessment of First-Trimester Utero-Placental Vascular Morphology by 3D Power Doppler Ultrasound Image Analysis Using a Skeletonization Algorithm: The Rotterdam Periconception Cohort

Vos

Koning

Steegers‐Theunissen

et al. 2023

Obstetrical &Amp; Gynecological Survey

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The increasing proportion of elderly Americans has brought about an anticipation of 50% rise in prolapse surgeries by 2050. It is anticipated that 25% to 40% of patients undergoing surgeries will develop de novo stress urinary incontinence (SUI) after prolapse repair. The Outcomes Following Vaginal Prolapse Repair with Midurethral Sling (OPUS) found a 36% reduction in the risk for de novo SUI, but also demonstrated increased risk of bladder perforations, urinary tract infections, and incomplete bladder emptying symptoms (N Engl J Med. 2012;366:2358-2367. As a result, pelvic reconstructive surgeons often vary their approach toward prophylactic MUS at the time of vaginal prolapse repair (VPR). Although a cost-effectiveness analysis found universal MUS placement to be the most cost-effective strategy over both selective and staged strategies (J Urol. 2013;190:1306-1312, this analysis did not include an arm for the less-costly option of using a selective approach via a prolapse-reduced cough stress test (CST). In addition, Richardson analysis of patients undergoing sacral colpopexy lacks generalizability for VPR surgeries (which account for two thirds of all prolapse surgeries). The manuscript described here therefore tested the cost-effectiveness of 3 generalizable MUS utilization strategies for preventing de novo SUI within 1 year post-VPR.Three approaches were compared: (1) staged strategy performing VPR with later MUS placement only for de novo SUI;(2) universal sling placement at the time of VPR; and (3) selective sling placement with MUS at the time of VPR when occult SUI was observed at the time of preoperative prolapse-reduced CST. A representative population of women with symptomatic pelvic organ prolapse (at least stage II) was modeled. Included in the VPR model was colpocleisis, apical suspension, or anterior colporrhaphy, with or without hysterectomy. The base assumption was that all VPRs were uncomplicated and anatomically successful. Subsequent treatment pathways were formed based on the 3 aforementioned options if de novo SUI was to occur.A 2017 systematic review by van der Ploeg was used for obtaining literature to gain point estimates concerning the risk for postoperative SUI (Int Urogynecol J. 2016;27:1029-1038). The search was performed via PubMed through January 2017, and exclusionary criteria were as follows: studies examining urodynamics preoperatively, abdominal prolapse repairs, duplicate studies, and studies lacking clear definitions for VPR, MUS, or SUI. Using data from 3 previous studies, for a selective MUS, the authors estimated the rate of de novo SUI after VPR with a negative preoperative CST to be 33.6%. The authors determined the existence of 4 possible adverse outcomes following MUS: (1) persistent SUI, (2) sling lysis required for voiding dysfunction, (3) mesh exposure requiring excision, and (4) anticholinergic medications required for de novo overactive bladder. Information on costs was gathered Physician Fee Schedules from the 2020 Centers for Medicare and Medicaid Services. Incr...

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Section: Upvs Development and Density Of Vascular Branching In The Fi...mentioning

confidence: 81%

Assessment of First-Trimester Utero-Placental Vascular Morphology by 3D Power Doppler Ultrasound Image Analysis Using a Skeletonization Algorithm: The Rotterdam Periconception Cohort

Vos

Koning

Steegers‐Theunissen

et al. 2023

Obstetrical &Amp; Gynecological Survey

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“…This technique has been extensively described by Reijnders and colleagues [ 4 ], and is a reliable reflection of the uPVV of the maternal side of the placental bed with intra-class correlation coefficients > 0.94 [ 4 ]. Standardized settings for the power Doppler ultrasound were used to obtain scans of the utero-placental vasculature (power Doppler gain ‘-8.0’, pulse repetition frequency ‘0.6 kHz’, wall motion filter ‘low 1’, quality ‘high’) [ 4 , 27 ]. Furthermore, the following default instrument settings were used throughout the examinations: frequency, low; dynamic, set 5; balance, 180; smooth, 4/5; ensemble, 12; line density, 8; power Doppler map, 5; artifact suppression, on; power Doppler line filter, 1; quality, high.…”

Section: Methodsmentioning

confidence: 99%

Corpus luteum number and the maternal renin-angiotensin-aldosterone system as determinants of utero-placental (vascular) development: the Rotterdam Periconceptional Cohort

Wiegel

Karsten

Reijnders

et al. 2021

Reprod Biol Endocrinol

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Background Pregnancies with > 1 corpus luteum (CL) display a hyperdynamic circulation and an increased risk of small-for-gestational age deliveries. Among the factors released by the CL is prorenin, the inactive precursor of renin. Since the renin-angiotensin-aldosterone system (RAAS) is involved in early hemodynamic pregnancy adaptation, we linked both CL number and first-trimester concentrations of prorenin (as an indicator of RAAS activity) and the aldosterone/renin ratio (as an indicator of angiotensin-independent aldosterone effectiveness) to non-invasive markers of utero-placental (vascular) development, measured longitudinally from the first trimester onwards. Methods A total of 201 women, who conceived naturally or after in-vitro fertilization treatment (with 0 (n = 8), 1 (n = 143), or > 1 (n = 51) CL), were selected from the Rotterdam Periconceptional Cohort. Maternal RAAS components were determined at 11 weeks gestation. Placental volume and utero-placental vascular volume were measured from transvaginal 3D ultrasound scans at 7, 9 and 11 weeks gestation, pulsatility and resistance indices of the uterine arteries were assessed by pulsed wave Doppler ultrasounds at 7, 9, 11, 13, 22 and 32 weeks gestation. At birth placental weight was obtained using standardized procedures. Results Pregnancies without a CL show lower uterine artery indices throughout gestation than 1 CL and > 1 CL pregnancies, while parameters of placental development are comparable among the CL groups. After adjustment for patient- and treatment-related factors, first-trimester prorenin concentrations are positively associated with uterine artery pulsatility and resistance indices (β 0.06, 95% CI 0.01;0.12, p = 0.04 and β 0.10, 95% CI 0.01;0.20, p = 0.04, respectively), while high prorenin concentrations are negatively associated with first-trimester utero-placental vascular volume (β -0.23, 95% CI -0.44;-0.02, p = 0.04) and placental weight (β -93.8, 95%CI -160.3;-27.4, p = 0.006). In contrast, the aldosterone/renin ratio is positively associated with first-trimester placental volume (β 0.12, 95% CI 0.01;0.24, p = 0.04). Conclusions The absence of a CL, resulting in low prorenin concentrations, associates with low uterine artery pulsatility and resistance, while high prorenin concentrations associate with a low utero-placental vascular volume and weight. These data support a scenario in which excess prorenin, by upregulating angiotensin II, increases uterine resistance, thereby preventing normal placental (vascular) development, and increasing the risk of small-for-gestational age deliveries. Simultaneously, high aldosterone concentrations, by ensuring volume expansion, exert the opposite.

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“…Associations between utero-placental vascular development and prenatal growth have been investigated by a variety of ultrasound markers, including placental volume (PV), vascularization and flow indices, and uterine artery Dopplers ( Collins et al , 2013 ; Reus et al , 2014 ; Velauthar et al , 2014 ; Alfirevic et al , 2017 ; Chen et al , 2022 ). Evidence suggests utero-placental vascular development and prenatal growth are associated with conception method and fetal sex ( Clifton, 2010 ; Broere-Brown et al , 2016 ; Rizzo et al , 2016 ; Cavoretto et al , 2020 ; Reijnders et al , 2021 ). Combining three-dimensional (3D) power Doppler (PD) ultrasound and virtual reality (VR), a recent study showed positive associations between utero-placental vascular volume (uPVV) development and embryonic growth, with fetal sex specific modifications ( Reijnders et al , 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Morphologic development of the first-trimester utero-placental vasculature is positively associated with embryonic and fetal growth: the Rotterdam Periconception Cohort

De Vos,

Mulders,

Koning

et al. 2024

Human Reproduction

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STUDY QUESTION Is morphologic development of the first-trimester utero-placental vasculature associated with embryonic growth and development, fetal growth, and birth weight percentiles? SUMMARY ANSWER Using the utero-placental vascular skeleton (uPVS) as a new imaging marker, this study reveals morphologic development of the first-trimester utero-placental vasculature is positively associated with embryonic growth and development, fetal growth, and birth weight percentiles. WHAT IS KNOWN ALREADY First-trimester development of the utero-placental vasculature is associated with placental function, which subsequently impacts embryonic and fetal ability to reach their full growth potential. The attribution of morphologic variations in the utero-placental vascular development, including the vascular structure and branching density, on prenatal growth remains unknown. STUDY DESIGN, SIZE, DURATION This study was conducted in the VIRTUAL Placental study, a subcohort of 214 ongoing pregnancies, embedded in the prospective observational Rotterdam Periconception Cohort (Predict study). Women were included before 10 weeks gestational age (GA) at a tertiary referral hospital in The Netherlands between January 2017 and March 2018. PARTICIPANTS/MATERIALS, SETTING, METHODS We obtained three-dimensional power Doppler volumes of the gestational sac including the embryo and the placenta at 7, 9, and 11 weeks of gestation. Virtual Reality-based segmentation and a recently developed skeletonization algorithm were applied to the power Doppler volumes to generate the uPVS and to measure utero-placental vascular volume (uPVV). Absolute vascular morphology was quantified by assigning a morphologic characteristic to each voxel in the uPVS (i.e. end-, bifurcation-crossing-, or vessel point). Additionally, total vascular length (mm) was calculated. The ratios of the uPVS characteristics to the uPVV were calculated to determine the density of vascular branching. Embryonic growth was estimated by crown-rump length and embryonic volume. Embryonic development was estimated by Carnegie stages. Fetal growth was measured by estimated fetal weight in the second and third trimester and birth weight percentiles. Linear mixed models were used to estimate trajectories of longitudinal measurements. Linear regression analysis with adjustments for confounders was used to evaluate associations between trajectories of the uPVS and prenatal growth. Groups were stratified for conception method (natural/IVF-ICSI conceptions), fetal sex (male/female), and the occurrence of placenta-related complications (yes/no). MAIN RESULTS AND THE ROLE OF CHANCE Increased absolute vascular morphologic development, estimated by positive random intercepts of the uPVS characteristics, is associated with increased embryonic growth, reflected by crown-rump length (endpoints β = 0.017, 95% CI [0.009; 0.025], bifurcation points β = 0.012, 95% CI [0.006; 0.018], crossing points β = 0.017, 95% CI [0.008; 0.025], vessel points β = 0.01, 95% CI [0.002; 0.008], and total vascular length β = 0.007, 95% CI [0.003; 0.010], and similarly with embryonic volume and Carnegie stage, all P-values ≤ 0.01. Density of vascular branching was negatively associated with estimated fetal weight in the third trimester (endpoints: uPVV β = −94.972, 95% CI [−185.245; −3.698], bifurcation points: uPVV β = −192.601 95% CI [−360.532; −24.670]) and birth weight percentiles (endpoints: uPVV β = −20.727, 95% CI [−32.771; −8.683], bifurcation points: uPVV β −51.097 95% CI [−72.257; −29.937], and crossing points: uPVV β = −48.604 95% CI [−74.246; −22.961])), all P-values < 0.05. After stratification, the associations were observed in natural conceptions specifically. LIMITATION, REASONS FOR CAUTION Although the results of this prospective observational study clearly demonstrate associations between first-trimester utero-placental vascular morphologic development and prenatal growth, further research is required before we can draw firm conclusions about a causal relationship. WIDER IMPLICATIONS OF THE FINDINGS Our findings support the hypothesis that morphologic variations in utero-placental vascular development play a role in the vascular mechanisms involved in embryonic and fetal growth and development. Application of the uPVS could benefit our understanding of the pathophysiology underlying placenta-related complications. Future research should focus on the clinical applicability of the uPVS as an imaging marker for the early detection of fetal growth restriction. 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).

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First-trimester utero-placental (vascular) development and embryonic and fetal growth: The Rotterdam periconception cohort

Cited by 12 publications

References 41 publications

Assessment of First-Trimester Utero-Placental Vascular Morphology by 3D Power Doppler Ultrasound Image Analysis Using a Skeletonization Algorithm: The Rotterdam Periconception Cohort

Assessment of First-Trimester Utero-Placental Vascular Morphology by 3D Power Doppler Ultrasound Image Analysis Using a Skeletonization Algorithm: The Rotterdam Periconception Cohort

Corpus luteum number and the maternal renin-angiotensin-aldosterone system as determinants of utero-placental (vascular) development: the Rotterdam Periconceptional Cohort

Morphologic development of the first-trimester utero-placental vasculature is positively associated with embryonic and fetal growth: the Rotterdam Periconception Cohort

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