Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
BMC Pregnancy and Childbirth
Published in: BMC Pregnancy and Childbirth 1/2020

Open Access 01-12-2020 | Pre-Eclampsia | Research article

“Screening for small-for-gestational age neonates at early third trimester in a high-risk population for preeclampsia”

Authors: Raquel Mula, Eva Meler, Sandra García, Gerard Albaigés, Bernat Serra, Elena Scazzocchio, Pilar Prats

Published in: BMC Pregnancy and Childbirth | Issue 1/2020

Login to get access

Abstract

Background

Strategies to improve prenatal detection of small-for-gestational age (SGA) neonates are necessary because its association with poorer perinatal outcome. This study evaluated, in pregnancies with first trimester high risk of early preeclampsia, the performance of a third trimester screening for SGA combining biophysical and biochemical markers.

Methods

This is a prospective longitudinal study on 378 singleton pregnancies identified at high risk of early preeclampsia according to a first trimester multiparametric algorithm with the cutoff corresponding to 15% false positive rate. This cohort included 50 cases that delivered SGA neonates with birthweight < 10th centile (13.2%) and 328 cases with normal birthweight (86.8%). At 27–30 weeks’ gestation, maternal weight, blood pressure, estimated fetal weight, mean uterine artery pulsatility index and maternal biochemical markers (placental growth factor and soluble FMS-Like Tyrosine Kinase-1) were assessed. Different predictive models were created to evaluate their performance to predict SGA neonates.

Results

For a 15% FPR, a model that combines maternal characteristics, estimated fetal weight, mean uterine artery pulsatility index and placental growth factor achieved a detection rate (DR) of 56% with a negative predictive value of 92.2%. The area under receiver operating characteristic curve (AUC) was 0.79 (95% confidence interval (CI), 0.72–0.86). The DR of a model including maternal characteristics, estimated fetal weight and mean uterine artery pulsatility index was 54% (AUC, 0.77 (95% CI, 0.70–0.84)). The DR of a model that includes maternal characteristics and placental growth factor achieved a similar performance (DR 56%, AUC 0.75, 95% CI (0.67–0.83)).

Conclusions

The performance of screening for SGA neonates at early third trimester combining biophysical and biochemical markers in a high-risk population is poor. However, a high negative predictive value could help in reducing maternal anxiety, avoid iatrogenic interventions and propose a specific plan for higher risk patients.
Literature
1.
Pay AS, Wiik J, Backe B, Jacobsson B, Strandell A, Klovning A. Symphysis-fundus height measurement to predict small-for-gestational-age status at birth: a systematic review. BMC Pregnancy Childbirth. 2015;15:2.CrossRef
2.
De Reu PA, Smits LJ, Oosterbaan HP, Nijhuis JG. Value of a single early third trimester fetal biometry for the prediction of birth weight deviations in a low risk population. J Perinat Med. 2008;36(4):324–9.PubMed
3.
David C, Tagliavini G, Pilu G, Rudenholz A, Bovicelli L. Receiver–operator characteristic curves for the ultrasonographic prediction of small-for-gestational-age fetuses in low-risk pregnancies. Am J Obstet Gynecol. 1996;174:1037–42. .CrossRef
4.
Sovio U, White IR, Dacey A, Pasupathy D, Smith GCS. Screening for fetal growth restriction with universal third trimester ultrasonography in nulliparous women in the Pregnancy Outcome Prediction (POP) study: a prospective cohort study. Lancet. 2015;386:2089–97.CrossRef
5.
Bricker L, Medley N, Pratt JJ. Routine ultrasound in late pregnancy (after 24 weeks’ gestation) (Review). Cochrane Database Syst Rev. 2015 Jun;29(6):CD001451.
6.
Figueras F, Eixarch E, Meler E, Iraola A, Figueras J, Puerto B, Gratacos E. Small-for-gestational-age fetuses with normal umbilical artery Doppler have suboptimal perinatal and neurodevelopmental outcome. Eur J Obstet Gynecol Reprod Biol. 2008;136:34–8.CrossRef
7.
Bartsch E, Medcalf KE, Park AL, Ray JG. High Risk of Pre-eclampsia Identification Group. Clinical risk factors for pre-eclampsia determined in early pregnancy: systematic review and meta-analysys of large cohort studies. BMJ. 2016;353:i1753. .CrossRef
8.
Seed PT, Chappell LC, Black MA, Poppe KK, Hwang YC, Kasabov N, McCowan L, Shennan AH, Wu SH, Poston L, North RA. Prediction of preeclampsia and delivery of small for gestational age babies based on a combination of clinical risk factors in high-risk women. Hypertens Pregnancy. 2011;30(1):58–73.CrossRef
9.
Roberto Romero JK, Nien J, Espinoza D, Todem W, Fu H, Chung JP, Kusanovic F, Gotsch O, Erez SMazaki-Tovi, Gomez R, Edwin S, Chaiworapongsa T, Levine RJ. & S. Ananth Karumanchi. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med. 2008 Jan;21(1):9–23.
10.
O’Gorman N, Wright D, Syngelaki A, Akolekar R, Wright A, Poon LC, Nicolaides KH. Competing risks model in screening for preeclampsia by maternal factors and biomarkers at 11–13 weeks gestation. Am J Obstet Gynecol. 2016;214(1):103.e1-103.e12. .CrossRef
11.
Bakalis S, Peeva G, Gonzalez R, Poon LC, Nicolaides KH. Prediction of small-for-gestational-age neonates: screening by biophysical and biochemical markers at 30–34 weeks. Ultrasound Obstet Gynecol. 2015;46:446–51.CrossRef
12.
Miranda J, Rodriguez-Lopez M, Triunfo S, Sairane M, Kouru H, Parra Saavedra M, Crovetto F, Figueras F, Crispi F, Gratacós E. Prediction of fetal growth restriction using estimated fetal weight vs a combined screening model in the third trimester. Ultrasound Obstet Gynecol. 2017;50:603–11.CrossRef
13.
Triunfo S, Parra-Saavedra M, Rodriguez-Sureda V, Crovetto F, Dominguez C, Gratacós E, Figueras F. Angiogenic Factors and Doppler Evaluation in Normally Growing Fetuses at Routine Third-Trimester Scan: Prediction of Subsequent Low Birth Weight. Fetal Diagn Ther. 2016;40(1):13–20.CrossRef
14.
Robinson HP, Fleming JE. A critical evaluation of sonar “crown-rump length” measurements. Br J Obstet Gynaecol. 1975;82(9):702–10.CrossRef
15.
Gómez O, Figueras F, Fernández S, Bennasar M, Martínez JM, Puerto B, Gratacós E. Reference range for uterine artery mean pulsatility index at 11–41 weeks of gestation. Ultrasound Obstet Gynecol. 2008;32(2):128–32.CrossRef
16.
Brown MA, Lindheimer MD, de Swiet M, Van Assche A, Moutquin JM. The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society for the study of Hypertension in Pregnancy (ISSHP). Hypertens Pregnancy. 2001;20:IX–XIV. .CrossRef
17.
Scazzocchio E, Figueras F, Crispi F, Meler E, Masoller N, Mula R, Gratacos E. Performance of a first-trimester screening of preeclampsia in a routine care low-risk setting. Am J Obstet Gynecol. 2013;208(3):203.e1-203.e10. .CrossRef
18.
Salomon LJ, Alfirevic Z, Berghella V, Bilardo C, Hernandez-Andrade E, Johnsen SL, Kalache K, Leung KY, Malinger G, Munoz H, Prefumo F, Toi A, Lee W. ISUOG Clinical Standards Committee. Practice guidelines for performance of the routine mid-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol. 2011 Jan;37(1):116–26.
19.
Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK. Estimation of fetal weight with the use of head, body, and femur measurements—a prospective study. Am J Obstet Gynecol. 1985;151:333–7.CrossRef
20.
Arduini D, Rizzo G. Normal values of Pulsatility Index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J Perinat Med. 1990;18(3):165–72.CrossRef
21.
Baschat AA, Gembruch U. The cerebroplacental Doppler ratio revisited. Ultrasound Obstet Gynecol. 2003 Feb;21(2):124–7.
22.
Hecher K, Campbell S, Snijders R, Nicolaides K. Reference ranges for fetal venous and atrioventricular blood flow parameters. Ultrasound Obstet Gynecol. 1994 Sep;4(5)(1):381–90.
23.
Figueras F, Gratacos E. Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther. 2014;36(2):86–98.CrossRef
24.
Departament de Salut. Generalitat de Catalunya. Corbes de referència de pes. perímetre cranial i longitud en néixer de nounats d’embarassos únics, de bessons i de trigèmins a Catalunya. 2008 .
25.
Shahabi J, Garakyaraghi M, Shafie D, Khaledifar A, Hedayat A, Givi M, Yadegarfar G. The association of anthropometric indices and cardiac function in healthy adults. ARYA Atheroscler. 2019. Jan;15(1):9–13.
26.
Sung KU, Roh JA, Eoh KJ, Kim E. Maternal serum placental growth factor and pregnancy associated plasma protein A measured in the first trimester as parameters of subsequent pre-eclampsia and small-for-gestational age infants: A prospective observational study. Obstet Gynecol. 2017. Mar;60(2):154–62.
27.
Birdir C, Fryze J, Frölich S, Schmidt M, Köninger A, Kimmig R, Schmidt B, Gellhaus A. Impact of maternal serum levels of Visfatin, AFP, PAPP-A, sFlt-1 and PlGF at 11–13 weeks’ gestation on small for gestational age births. J Matern Fetal Neonatal Med. 2017 Mar;30(6):629–34.
28.
Sotiriadis A, Figueras F, Eleftheriades M, Papaioannou GK, Chorozoglou G, Dinas K, Papantoniou N. First-trimester and combined first- and second-trimester prediction of small-for-gestational age and late fetal growth restriction. Ultrasound Obstet Gynecol. 2019 Jan;53(1):55–61.
29.
Seravalli V, Block-Abraham DM, Turan OM, Doyle LE, Kopelman JN, Atlas RO, Jenkins CB, Blitzer MG, Baschat AA. First-trimester prediction of small-for-gestational age neonates incorporating fetal Doppler parameters and maternal characteristics. Am J Obstet Gynecol. 2014 Sep;211(3):261.e1-8.
30.
Poon LC, Syngelaki A, Akolekar R, Lai J, Nicolaides KH. Combined screening for preeclampsia and small for gestational age at 11–13 weeks. Fetal Diagn Ther. 2013;33(1):16–27.CrossRef
31.
Schoofs K, Grittner U, Engels T, Pape J, Denk B, Henrich W, Verlohren S. The importance of repeated measurements of the sFlt-1/PlGF ratio for the prediction of preeclampsia and intrauterine growth restriction. J Perinat Med. 2014 Jan;42(1):61–8.
32.
Birdir C, Droste L, Fox L, Frank M, Fryze J, Enekwe A, Köninger A, Kimmig R, Schmidt B, Gellhaus A. Predictive value of sFlt-1, PlGF, sFlt-1/PlGF ratio and PAPP-A for late-onset preeclampsia and IUGR between 32 and 37 weeks of pregnancy. Pregnancy Hypertens. 2018 Apr;12:124–8.
33.
34.
Anca Ciobanu MD, Angeliki Rouvali MD, Argyro Syngelaki PhD, Ranjit Akolekar MD, Kypros H, Nicolaides MD. Prediction of small for gestational age neonates: screening by maternal factors, fetal biometry, and biomarkers at 35–37 weeks’ gestation. Am J Obstet Gynecol. 2019;220(5):486.e1-486.e11.CrossRef
35.
Benton Samantha J, McCowan LM, Heazell Alexander EP, Grynspan D, Hutcheon JA, Senger C, Burke O, Chan Y, Harding JE, Yockell-Lelievr Julien, Hu Yuxiang, Chappell Lucy C, Griffin MJ, Shennan AH, Magee LA, Gruslin Andree, von Dadelszen Peter. Placental growth factor as a marker of fetal growth restriction caused by placental dysfunction. Placenta. 2016;42:1–8. .CrossRef
36.
Triunfo S, Lobmaier S, Parra-Saavedra M, Crovetto F, Peguero A, Nadal A, Gratacos E, Figueras F. Angiogenic factors at diagnosis of late-onset small-for-gestational age and histological placental underperfusion. Placenta. 2014 Jun;35(6):398–403.
37.
MacDonald Teresa M, Tran C, Kaitu’u-Lino Tu’uhevaha J, Brennecke SP, Hiscock RJ, Hui Lisa, Dane KM, Middleton AL, Cannon Ping, Walker Susan P, Tong Stephen. Assessing the sensitivity of placental growth factor and soluble fms-like tyrosine kinase 1 at 36 weeks’ gestation to predict small-for-gestational-age infants or late-onset preeclampsia: a prospective nested case-control study. BMC Pregnancy Childbirth. 2018;18:354. .CrossRef
38.
Francesca Gaccioli U, Sovio E, Cook M, Hund DS, Charnock-Jones, Gordon CS, Smith P. Screening for fetal growth restriction using ultrasound and the sFLT1/PlGF ratio in nulliparous women: a prospective cohort study. Lancet Child Adolesc Health. 2018 Aug;2(8):569–81.
39.
Herraiz I, Quezada MS, Rodriguez-Calvo J, Gomez-Montes E, Villalain C, Galindo A. Longitudinal change of sFlt-1/PlGF ratio in singleton pregnancy with early-onset fetal growth restriction. Ultrasound Obstet Gynecol. 2018;52:631–8.CrossRef
40.
Triunfo S, Crovetto F, Scazzocchio E, Parra-Saavedra M, Gratacós E, Figueras F. Contingent versus routine third-trimester screening for late fetal growth restriction. Ultrasound Obstet Gynecol. 2016;47:81–8.CrossRef
41.
Poon C, Lesmes C, Gallo DM, Akolekar R. and K. H. Nicolaides. Prediction of small-for-gestational-age neonates: screening by biophysical and biochemical markers at 19–24 weeks. Ultrasound Obstet Gynecol. 2015;46:437–45.
42.
Lesmes C, Gallo DM, Gonzalez R, Poon LC, Nicolaides KH. Prediction of small-for-gestational-age neonates: screening by maternal serum biochemical markers at 19–24 weeks. Ultrasound Obstet Gynecol. 2015;46:341–9.CrossRef
43.
Tan MY, Poon LC, Rolnik DL, Syngelaki A, de Paco Matallana C, Akolekar R, Cicero S, Janga D, Singh M, Molina FS, Persico N, Jani JC, Plasencia W, Greco E, Papaioannou G, Wright D, Nicolaides KH. Prediction and prevention of small-for-gestational-age neonates: evidence from SPREE and ASPRE. Ultrasound Obstet Gynecol. 2018;52(1):52–9. .CrossRef
Metadata
Title
“Screening for small-for-gestational age neonates at early third trimester in a high-risk population for preeclampsia”
Authors
Raquel Mula
Eva Meler
Sandra García
Gerard Albaigés
Bernat Serra
Elena Scazzocchio
Pilar Prats
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Pre-Eclampsia
Published in
BMC Pregnancy and Childbirth / Issue 1/2020
Electronic ISSN: 1471-2393
DOI
https://doi.org/10.1186/s12884-020-03167-5

Other articles of this Issue 1/2020

BMC Pregnancy and Childbirth 1/2020 Go to the issue

Research Article

Interventions to improve adherence to antenatal and postnatal care regimens among pregnant women in sub-Saharan Africa: a systematic review

Research article

Perinatal outcomes of frequent attendance in midwifery care in the Netherlands: a retrospective cohort study

Research article

Cross-cultural adaptation and psychometric evaluation of the Brazilian Portuguese version of the childbirth experience questionnaire

Correction

Correction to: Obstetric fistulas in Uganda: scoping review using a determinant of health approach to provide a framework for health policy improvement

Case report

Misdiagnosis of a twin pregnancy with double-corner uterine rupture following salpingectomy and protrusion of the amniotic sac as an adnexal cyst: a case report

Research article

Appendectomy, cholecystectomy and diagnostic laparoscopy conducted before pregnancy and risk of adverse birth outcomes: a nationwide registry-based prevalence study 1996–2015