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Cited by 30Pregnancy and preeclampsia studiesPrenatal Screening and DiagnosticsUltrasound in Clinical Applications

Volume and vascularity: Using ultrasound to unlock the secrets of the first trimester placenta

Open access
Mathewlynn, S., Collins, S.L.·2019·Placenta
DOI 10.1016/j.placenta.2019.06.379PMC PMC7586067
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Abstract

Fetal growth restriction (FGR) is a major cause of perinatal morbidity and mortality. Identifying which pregnancies are at risk of FGR facilitates enhanced surveillance and early delivery before fetal demise can ensue. However, existing risk stratification strategies yield an unacceptably low detection rate. A robust and reliable first trimester screening test for FGR would not only enable high-risk women to be appropriately monitored but would facilitate future trials for possible interventions to enhance fetal growth. Both the volume and vascularity of the first trimester placenta has been demonstrated to be linked to adverse pregnancy outcomes including FGR and pre-eclampsia. The investigation of novel ultrasound markers for FGR are discussed along with the development of methods for fully automatic placental volume estimation which has the potential for use as part of a multi-variable population-based screening test.

AI snapshot

Written from the paper’s full text.

TL;DR

This review argues that first-trimester placental volume and vascularity measured by ultrasound are promising markers for fetal growth restriction (FGR) and pre-eclampsia, and that fully automated segmentation tools could enable population-based screening. It surveys manual, semi-automated (VOCAL™, random walker) and deep-learning (OxNNet) methods for placental volume estimation, plus spiral artery jet and 3-D power Doppler vascularity indices.

Key findings

  • Low placental volume (PlaV) at 11–13 weeks is associated with SGA/FGR and pre-eclampsia, independent of PAPP-A and nuchal translucency; predictive accuracy improves when PlaV is combined with maternal characteristics, PAPP-A and placental growth factor.
  • The deep-learning tool OxNNet achieved a mean dice similarity coefficient of 0.84 (range 0.72–0.92) against clinician-quality-assured random-walker segmentations, and its volume estimates outperform VOCAL™ in predicting cSGA.
  • In a pilot study of 143 women, standardised placental volume (sPlaV) differed significantly between cSGA and AGA pregnancies (p = <0.001); ROC AUC for predicting cSGA was 0.77 (0.66–0.87) for sPlaV alone and 0.80 (0.69–0.92) combined with PAPP-A and NT.
  • Spiral artery jet pulsatility index is significantly altered in cSGA pregnancies, an effect not seen in uterine artery Doppler indices; jet mouth opening increases between 11–13 and 34 weeks, with cSGA showing a trend toward smaller change (p = 0.05). A small pilot study found pre-eclampsia-destined pregnancies have small hypovascular placentas, whereas normotensive cSGA pregnancies have small placentas with normal vascularity.

Methods

  • Narrative review of ultrasound-based first-trimester placental markers for FGR/SGA and pre-eclampsia, covering placental volume measurement techniques (2-D estimates, 3-D manual delineation, VOCAL™, random walker, deep learning/OxNNet) and utero-placental vascularity assessment (spiral artery jets, 2-D and 3-D power Doppler, fractional moving blood volume).
  • Cites the authors' own pilot and validation studies, including a 143-woman pilot of sPlaV derived via the random walker algorithm and a small pilot measuring FMBV of the utero-placental interface and intervillous space.
  • No new primary data are collected; the paper synthesises published literature and pilot results.

Limitations

  • Stated in the paper: the sPlaV pilot requires further investigation with a larger cohort; the vascularity pilot studies are small; visualisation of individual spiral arteries and jets remains time-consuming and requires considerable training; power Doppler is influenced by body habitus and machine settings (especially gain), so standardisation is essential; complete automation of the 3-D FMBV vascularity index has not yet been achieved.
  • Evident from the text: the review relies heavily on the authors' own work and on pilot data, and several cited comparisons (e.g., OxNNet vs VOCAL™) are noted as "in print" rather than fully peer-reviewed at the time of writing.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.placenta.2019.06.379

Cites

63 of 63 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 84 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    Risk stratification for growth restriction in the UK is generally based on assessment of maternal characteristics and history at the booking appointment.

    “Risk stratification for growth restriction in the UK is generally based on an assessment of maternal characteristics and history at the booking appointment with the community midwife [10].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] 2014

      Not checked in the free run.

  • Premisecitation

    First trimester placental volume and vascularity are linked to adverse pregnancy outcomes including FGR and pre-eclampsia.

    “Both the volume and vascularity of the first trimester placenta has been demonstrated to be linked to adverse pregnancy outcomes including FGR and pre-eclampsia.”
    Quote in the paperSubstantial claim0 of 5 sources checked
    • cites [23] Hafner, 2001, Correlation of first trimester placental volume and second trimester uterine artery Doppler flow, Placenta source

      Not checked in the free run.

    • cites [26] Plasencia, 2011, Placental volume at 11-13 weeks' gestation in the prediction of birth weight percentile, Fetal Diagn. Ther. source

      Not checked in the free run.

    • cites [27] Law, 2009, Which ultrasound or biochemical markers are independent predictors of small for gestational age?, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

    • cites [28] Hafner, 2006, Comparison between three-dimensional placental volume at 12 weeks and uterine artery impedance/notching at 22 weeks in screening for pregnancy-induced hypertension, pre-eclampsia and fetal growth restriction in a low-risk population, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

    • cites [29] Hashish, 2015, Could 3D placental volume and perfusion indices measured at 11-14 weeks predict occurrence of preeclampsia in high-risk pregnant women?, J. Matern. Fetal Neonatal Med. source

      Not checked in the free run.

  • Premisecitation

    Birth weight is dependent on gestational age at delivery, maternal characteristics, and placental volume, vasculature and function.

    “Birth weight is dependent upon numerous factors including gestational age at the time of delivery [1]; maternal characteristics [1–3]; and placental volume, vasculature and function [4].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [1] Poon, 2011, Reference range of birth weight with gestation and first-trimester prediction of small-for-gestation neonates, Prenat. Diagn. source

      Not checked in the free run.

    • cites [2] Wen, 1990, Smoking, maternal age, fetal growth, and gestational age at delivery, Am. J. Obstet. Gynecol. source

      Not checked in the free run.

    • cites [3] Clausson, 1998, Preterm and term births of small for gestational age infants: a population-based study of risk factors among nulliparous women, Br. J. Obstet. Gynaecol. source

      Not checked in the free run.

    • cites [4] M Salafia, 2006, Placenta and fetal growth restriction, Clin. Obstet. Gynecol. source

      Not checked in the free run.

  • Premisecitation

    The majority of FGR is not diagnosed prior to birth.

    “As the majority of FGR is not diagnosed prior to birth [8, 9], early identification triggering appropriate management may prove to be the key to reducing this dismal figure.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [8] Hepburn, 1986, An audit of the detection and management of small-for-gestational age babies, Br. J. Obstet. Gynaecol. source

      Not checked in the free run.

    • cites [9] Kean, 1996, Antenatal care as a screening tool for the detection of small for gestational age babies in the low risk population, J. Obstet. Gynaecol. source

      Not checked in the free run.

  • Premisecitation

    Customised SGA (cSGA) is associated with adverse perinatal outcomes including stillbirth.

    “Nevertheless, SGA, especially SGA defined using customised centiles (cSGA), has been shown to be associated with adverse perinatal outcomes including stillbirth and therefore cSGA has been used as a surrogate outcome for FGR in most of the studies discussed in this review.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [6] Clausson, 2001, Perinatal outcome in SGA births defined by customised versus population-based birthweight standards, BJOG

      Not checked in the free run.

    • cites [7] Flenady, 2011, Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis, Lancet source

      Not checked in the free run.

  • Classified as probably not a substantial claim. 3
  • May combine two claims. 24

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    Existing risk stratification strategies for FGR yield an unacceptably low detection rate.

    “However, existing risk stratification strategies yield an unacceptably low detection rate.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Gene therapy has been suggested as a possible candidate for treatment of FGR and has shown promise in animal models.

    “Gene therapy [18] has also been suggested as a possible candidate for treatment of FGR and has shown promise in animal models.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [18] Jones, 2013, Adenoviral-mediated placental gene transfer of IGF-1 corrects placental insufficiency via enhanced placental glucose transport mechanisms, PLoS One source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    There is uncertainty regarding the repeatability and reproducibility of volume results produced using VOCALTM, with certain iterations producing less reliable results.

    “There is also some uncertainty regarding the repeatability and reproducibility of volume results produced using this method, with certain iterations of the VOCAL™ software producing less reliable results [36].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [36] Cheong, 2010, Comparison of inter- and intraobserver agreement and reliability between three different types of placental volume measurement technique (XI VOCAL, VOCAL and multiplanar) and validity in the in-vitro setting, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Placental weight at delivery is positively correlated with birth weight.

    “It has long been understood that the weight of the placenta at delivery is positively correlated to birth weight [19, 20].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [19] Little, 1960, The significance of placental/fetal weight ratios, Am. J. Obstet. Gynecol. source

      Not checked in the free run.

    • cites [20] Sinclair, 1948, Placental-fetal weight ratios, Tex. Rep. Biol. Med.

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The random walker algorithm allows semi-automated image segmentation, producing a 3-D outline of the placenta in considerably less time and a less operator dependent manner.

    “The random walker algorithm allows for semi-automated image segmentation [37], which can produce a 3-D outline of the placenta in considerably less time and a less operator dependent manner.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [37] Grady, 2006, Random walks for image segmentation, IEEE Trans. Pattern Anal. Mach. Intell. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A pilot study of 143 women showed that sPlaV, derived using the random walker algorithm, is significantly different in cSGA compared with AGA pregnancies (p < 0.001) and that combining sPlaV with PAPP-A and NT produces a predictive model for cSGA.

    “A pilot study of 143 women has shown that sPlaV, derived using the random walker algorithm, is significantly different in cSGA compared with appropriate for gestational age (AGA) pregnancies (p = <0.001) and that combining sPlaV with PAPP-A and NT produces a predictive model for cSGA.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [42] Cohen-Overbeek, 1985, The antenatal assessment of utero-placental and feto-placental blood flow using Doppler ultrasound, Ultrasound Med. Biol. source

      Not checked in the free run.

    • Rests on an assumption: Placental volume increases with gestational age.

  • May combine two claims.

    Premisecitation

    The random walker method is comparable to manual segmentation with respect to reproducibility and outperforms VOCALTM in terms of inter-observer reliability.

    “Despite faster volume acquisition, the random walker method is comparable to manual segmentation with respect to reproducibility and outperforms VOCAL™ in terms of inter-observer reliability [35].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [35] Stevenson, 2015, 3-D ultrasound segmentation of the placenta using the random walker algorithm: reliability and agreement, Ultrasound Med. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Assessment of PlaV using VOCALTM is time consuming, requires considerable training, and is therefore not suitable for use as a screening tool.

    “Assessment of PlaV using this commercially available tool is still time consuming and requires considerable training and is therefore not suitable for use as a screening tool.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Low placental volume (PlaV) at 11-13 weeks is associated with SGA/FGR and pre-eclampsia, independent of PAPP-A and nuchal translucency measurements.

    “It has now been shown that low placental volume (PlaV) at 11–13 weeks is associated with SGA/FGR [23, 26–28] and pre-eclampsia [28, 29], and that this is independent of PAPP-A and nuchal translucency (NT) measurements [27].”
    Quote in the paperSubstantial claim0 of 5 sources checked
    • cites [23] Hafner, 2001, Correlation of first trimester placental volume and second trimester uterine artery Doppler flow, Placenta source

      Not checked in the free run.

    • cites [26] Plasencia, 2011, Placental volume at 11-13 weeks' gestation in the prediction of birth weight percentile, Fetal Diagn. Ther. source

      Not checked in the free run.

    • cites [27] Law, 2009, Which ultrasound or biochemical markers are independent predictors of small for gestational age?, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

    • cites [28] Hafner, 2006, Comparison between three-dimensional placental volume at 12 weeks and uterine artery impedance/notching at 22 weeks in screening for pregnancy-induced hypertension, pre-eclampsia and fetal growth restriction in a low-risk population, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

    • cites [29] Hashish, 2015, Could 3D placental volume and perfusion indices measured at 11-14 weeks predict occurrence of preeclampsia in high-risk pregnant women?, J. Matern. Fetal Neonatal Med. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Placental volume estimates generated with OxNNet perform well in the prediction of SGA when compared with those generated by the random walker algorithm, and outperform PlaV estimates generated with VOCALTM.

    “The placental volume estimates generated with this method perform well in the prediction of SGA when compared with those generated by the random walker algorithm, and outperform PlaV estimates generated with VOCAL™ [35, 38, 41] (see Figure 2).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [35] Stevenson, 2015, 3-D ultrasound segmentation of the placenta using the random walker algorithm: reliability and agreement, Ultrasound Med. Biol. source

      Not checked in the free run.

    • cites [38] Stevenson, 2010, A novel semi-automated (SA) technique for 3D ultrasound measurement of placental volume, Ultrasound Obstet. Gynecol.

      Not checked in the free run.

    • cites [41] Looney, 2018

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The standardised placental volume (sPlaV) produces dimensionless and normally distributed results, making it more mathematically sound than the placental quotient.

    “This produces dimensionless and normally distributed results making it more mathematically sound than the placental quotient from which it was derived, the latter being calculated as crown rump length (mm) divided by PlaV (mL or mm3) and having a unit of mm−2 [43].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [43] Brosens, 1977, Fetal growth retardation and the arteries of the placental bed, Br. J. Obstet. Gynaecol. source

      Not checked in the free run.

    • Rests on an assumption: Placental volume increases with gestational age.

  • May combine two claims.

    Premisecitation

    ROC curves for prediction of cSGA in an unselected population using sPlaV alone give an area under the curve of 0.77 (0.66 to 0.87), or 0.80 (0.69 to 0.92) when used in combination with PAPP-A and NT.

    “Receiver operating characteristic (ROC) curves for prediction of cSGA in an unselected population using sPlaV alone give an area under the curve of 0.77 (0.66 to 0.87), or 0.80 (0.69 to 0.92) when used in combination with PAPP-A and NT [42].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [42] Cohen-Overbeek, 1985, The antenatal assessment of utero-placental and feto-placental blood flow using Doppler ultrasound, Ultrasound Med. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The VOCALTM method is purely geometric and estimation of volume in an irregularly shaped organ may be more prone to error.

    “This method is purely geometric and consequently estimation of volume in an irregularly shaped organ may be more prone to error [35], this is important as it has been demonstrated that the shape of the placenta in the first trimester is not always regular [34].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [35] Stevenson, 2015, 3-D ultrasound segmentation of the placenta using the random walker algorithm: reliability and agreement, Ultrasound Med. Biol. source

      Not checked in the free run.

    • cites [34] Aye, 2015, Comparison of 2-D and 3-D estimates of placental volume in early pregnancy, Ultrasound Med. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Use of the random walker method requires relatively little training, demonstrates good intra and inter-observer repeatability, and is non-proprietary, reducing some barriers to use as a screening test.

    “Use of the random walker method requires relatively little training, demonstrates good intra and inter-observer repeatability and is also non-proprietary, thus some of the barriers to use as a screening test are reduced.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The random walker algorithm overcomes limitations of VOCALTM with respect to an irregularly shaped placenta, is less likely to over-estimate placental volume compared with 2-D techniques, and its initialisation is significantly faster compared with VOCAL (p < 0.001).

    “The random walker algorithm overcomes the limitations of VOCAL™ with respect to an irregularly shaped placenta, is less likely to over-estimated placental volume compared with 2-D techniques and its initialisation is significantly faster compared with VOCAL (p = <0.001) [34, 35].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [34] Aye, 2015, Comparison of 2-D and 3-D estimates of placental volume in early pregnancy, Ultrasound Med. Biol. source

      Not checked in the free run.

    • cites [35] Stevenson, 2015, 3-D ultrasound segmentation of the placenta using the random walker algorithm: reliability and agreement, Ultrasound Med. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The ASPRE trial demonstrated that aspirin reduced the incidence of pre-eclampsia compared with placebo in a population identified as high risk using a first trimester screening test, but was underpowered to detect an effect on FGR/SGA and stillbirth.

    “The recent ASPRE trial demonstrated that administration of aspirin to a population identified as high risk using a first trimester screening test reduced the incidence of pre-eclampsia compared with placebo [17], but was underpowered to detect an effect on FGR/SGA and stillbirth.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [17] Rolnik, 2017, Aspirin versus placebo in pregnancies at high risk for preterm preeclampsia, N. Engl. J. Med. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Manual delineation of the placenta is highly operator dependent and time-consuming, making this method impractical for use as a screening test.

    “Consequently, manual delineation of the placenta is highly operator dependent and time-consuming, making this method impractical for use as a screening test.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Assessments of PlaV generated using 2-D ultrasound correlate poorly with validated 3-D ultrasound techniques and are probably less reliable with certain placental shapes, particularly in the first trimester.

    “However, assessments of PlaV generated using 2-D ultrasound correlate poorly with validated 3-D ultrasound techniques and are probably less reliable with certain placental shapes, particularly in the first trimester [34].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [34] Aye, 2015, Comparison of 2-D and 3-D estimates of placental volume in early pregnancy, Ultrasound Med. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    OxNNet provides a fully automated and fast method for PlaV estimation with the distinct potential to be part of a population-based screening test.

    “As OxNNet provides a fully automated and fast method for PlaV estimation this has the distinct potential to be part of a population-based screening test [40].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [40] Looney, 2018, Fully automated, real-time 3D ultrasound segmentation to estimate first trimester placental volume using deep learning, JCI insight

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Pilot data demonstrates that the Jet PI is significantly altered in cSGA pregnancies, an effect that was not seen in the UtA Doppler indices.

    “Indeed, pilot data demonstrates that the Jet PI is significantly altered in cSGA pregnancies, an effect that was not seen in the UtA Doppler indices [16].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [16] Collins, 2012, Measurement of spiral artery jets: general principles and differences observed in small-for-gestational-age pregnancies, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Power Doppler is virtually angle independent, which allows better detection of low-flow velocities compared with colour Doppler.

    “Power Doppler is also virtually angle independent which allows better detection of low-flow velocities compared with colour Doppler [58–60].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [58] MacSweeney, 1996, Colour Doppler energy (power) mode ultrasound, Clin. Radiol. source

      Not checked in the free run.

    • cites [59] Collins, 2012, Influence of power Doppler gain setting on Virtual Organ Computer-aided AnaLysis indices in vivo: can use of the individual sub-noise gain level optimize information?, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

    • cites [60] Hernandez-Andrade, 2004, Validation of fractional moving blood volume measurement with power Doppler ultrasound in an experimental sheep model, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    FGR/SGA and PET are associated with disordered remodelling of the spiral arteries.

    “There is also histological evidence that FGR/SGA and PET are associated with disordered remodelling of the spiral arteries [45–47].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [45] Khong, 2011, Defective deep placentation, Best Pract. Res. Clin. Obstet. Gynaecol. source

      Not checked in the free run.

    • cites [46] Schaaps, 2005, Shunting the intervillous space: new concepts in human uteroplacental vascularization, Am. J. Obstet. Gynecol. source

      Not checked in the free run.

    • cites [47] Collins, 2011, Abdominal pregnancy: a perfusion confusion?, Placenta source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The jet mouth opening increases between 11-13 weeks and 34 weeks, and cSGA pregnancies show a trend towards a smaller change in mouth size (p=0.05).

    “Further, the jet mouth opening has been shown to increase between 11–13 weeks and 34 weeks, and cSGA pregnancies show a trend towards a smaller change in mouth size (p=0.05) [57].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [57] Welsh, 2004, Quantification of power Doppler and the index 'fractional moving blood volume' (FMBV), Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Pilot data suggests that both placental volume and vascularity measurements have utility in the prediction of pre-eclampsia and cSGA.

    “Pilot data suggests that both placental volume and vascularity measurements have utility in the prediction of pre-eclampsia and cSGA.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [42] Cohen-Overbeek, 1985, The antenatal assessment of utero-placental and feto-placental blood flow using Doppler ultrasound, Ultrasound Med. Biol. source

      Not checked in the free run.

    • cites [65]

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Early attempts at identification of the spiral arteries based on approximate location and distinctive bidirectional waveform are flawed because lack of defined anatomical landmarks makes consistent measurement impossible, angle correction is not appropriate due to tortuous nature, and seeking the classic waveform might lead to preferential selection of normal vessels.

    “Unfortunately this method is flawed as lack of defined anatomical landmarks means it is impossible to measure vessels consistently at the same point, angle correction is not appropriate due to the tortuous nature of the spiral artery, and seeking the classic waveform might lead to preferential selection of normal vessels for measurement [16].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [16] Collins, 2012, Measurement of spiral artery jets: general principles and differences observed in small-for-gestational-age pregnancies, Ultrasound Obstet. Gynecol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Pregnancies destined to develop pre-eclampsia have small hypovascular placentas, whereas those destined to result in normotensive cSGA have small placentas but with normal vascularity.

    “This demonstrated that pregnancies destined to develop pre-eclampsia have small hypovascular placentas, whereas those destined to result in normotensive cSGA have small placentas but with normal vascularity.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [65]

      Not checked in the free run.

26 of 26

  • The paper relies on this without support.

    Early identification of pregnancies at risk of FGR and appropriate management reduces perinatal morbidity and mortality.

    “Identifying which pregnancies are at risk of FGR facilitates enhanced surveillance and early delivery before fetal demise can ensue.”
    “This would likely reduce perinatal morbidity and mortality by facilitating enhanced surveillance of higher risk pregnancies, with intervention when necessary.”

  • The authors state this as an assumption.

    In FMBV standardisation, beam path factors alter signals from the area of interest and the standardisation point to the same degree.

    “on the assumption that any beam path factors will alter signals from the area of interest and the standardisation point to the same degree [63].”

  • The paper relies on this without support.

    Placental volume increases with gestational age.

    “Placental volume increases with gestational age and therefore measurements taken at different gestational ages between 11 and 13 weeks must take this physiological variation into account.”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Poor vascularity of the first-trimester placenta increases the risk of developing pre-eclampsia later in pregnancy.

    “Poor vascularity of the first-trimester placenta has also been demonstrated to increase the risk of developing pre-eclampsia later in pregnancy [40].”

    From Deep Learning Strategies for Ultrasound in Pregnancy (2020) · cites this paper as [40]

Cites

1 retracted

Flagged first, then by citations

2 of the 65 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Stevenson, 2010, A novel semi-automated (SA) technique for 3D ultrasound measurement of placental volume, Ultrasound Obstet. Gynecol.

Cited by

Sorted by citations

Related

Authors
Mathewlynn, S., & Collins, S. L.
Affiliations
  • Milton Keynes Hospital (GB)
  • John Radcliffe Hospital (GB)
Corresponding author
Collins, S.L.
ORCID
Venue
Placenta
Publisher
Elsevier BV
Published
2019-09
Volume
84
Pages
32-36
ISSN
0143-4004 (ISSN-L)
DOI
10.1016/j.placenta.2019.06.379
PMC
PMC7586067
OpenAlex
W2954909334
Semantic Scholar
a6befc2ed2585f12558b4a649ea783ac87b75fd6
Cited by
30
References
65
Citations by year
2026: 2 · 2025: 6 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 2 · 2020: 7
FWCI
0.59
Type
journal article
Language
en
Open access
Licence
Locations
  • Placenta (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (UO1-HD087209)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development
Topics
  • Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Screening and Diagnostics
  • Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Ultrasound in Clinical Applications
Keywords
fetal growth restriction, first trimester placenta, placental volume, placental vascularization, ultrasound markers, first-trimester screening, preeclampsia, risk stratification
MeSH terms
Female, Humans, Organ Size, Placenta, Placentation, Pregnancy, Pregnancy Trimester, First, Ultrasonography, Prenatal, Fetal Development

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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