{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,17]],"date-time":"2026-03-17T11:03:24Z","timestamp":1773745404730,"version":"3.50.1"},"reference-count":46,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,2,19]],"date-time":"2023-02-19T00:00:00Z","timestamp":1676764800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: Monitoring pregnancies with fetal growth restriction (FGR) presents a challenge, especially concerning the time of delivery in cases of early preterm pregnancies below 32 weeks. The aim of our study was to compare different diagnostic parameters in growth-restricted preterm neonates with and without morbidity\/mortality and to determine sensitivity and specificity of diagnostic parameters for monitoring preterm pregnancies with early preterm fetal growth restriction below 32 weeks. Materials and Methods: Our clinical study evaluated 120 cases of early preterm deliveries, with gestational age \u2264 32 + 0 weeks, with prenatally diagnosed placental FGR. All the patients were divided into three groups of 40 cases each based on neonatal condition,: I\u2014Neonates with morbidity\/mortality (NMM); II\u2014Neonates without morbidity with acidosis\/asphyxia (NAA); III\u2014Neonates without neonatal morbidity\/acidosis\/asphyxia (NWMAA). Results: Amniotic fluid index (AFI) was lower in NMM, while NWMAA had higher biophysical profile scores (BPS). UA PI was lower in NWMAA. NWMAA had higher MCA PI and CPR and fewer cases with CPR &lt;5th percentile. NMM had higher DV PI, and more often had ductus venosus (DV) PI &gt; 95th\u2030 or absent\/reversed A wave, and pulsatile blood flow in umbilical vein (UV). The incidence of pathological fetal heart rate monitoring (FHRM) was higher in NMM and NAA, although the difference was not statistically significant. ROC calculated by defining a bad outcome as NMM and a good outcome as NAA and NWMAA showed the best sensitivity in DV PIi. ROC calculated by defined bad outcome in NMM and NAA and good outcome in NWMAA showed the best sensitivity in MCA PI. Conclusions: In early fetal growth restriction normal cerebral blood flow strongly predicts good outcomes, while pathological venous blood flow is associated with bad outcomes. In fetal growth restriction before 32 weeks, individualized expectant management remains the best option for the optimal timing of delivery.<\/jats:p>","DOI":"10.3390\/medicina59020406","type":"journal-article","created":{"date-parts":[[2023,2,20]],"date-time":"2023-02-20T03:56:07Z","timestamp":1676865367000},"page":"406","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Diagnostic Tests in the Prediction of Neonatal Outcome in Early Placental Fetal Growth Restriction"],"prefix":"10.3390","volume":"59","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0005-8443","authenticated-orcid":false,"given":"Vesna","family":"Mandi\u0107-Markovi\u0107","sequence":"first","affiliation":[{"name":"Faculty of Medicine, University of Belgrade, Dr Subotica 8, 11000 Belgrade, Serbia"},{"name":"Department of High-Risk Pregnancies, University Clinic for Gynecology and Obstetrics \u201cNarodni Front\u201d, Kraljice Natalije 62, 11000 Belgrade, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mirjana","family":"Bogavac","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Faculty of Medicine University of Novi Sad, Branimira \u0106osi\u0107a 37, 21000 Novi Sad, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"\u017deljko","family":"Mikovi\u0107","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, University of Belgrade, Dr Subotica 8, 11000 Belgrade, Serbia"},{"name":"Department of High-Risk Pregnancies, University Clinic for Gynecology and Obstetrics \u201cNarodni Front\u201d, Kraljice Natalije 62, 11000 Belgrade, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Milan","family":"Pani\u0107","sequence":"additional","affiliation":[{"name":"Department of High-Risk Pregnancies, University Clinic for Gynecology and Obstetrics \u201cNarodni Front\u201d, Kraljice Natalije 62, 11000 Belgrade, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dejan M.","family":"Pavlovi\u0107","sequence":"additional","affiliation":[{"name":"Department of High-Risk Pregnancies, University Clinic for Gynecology and Obstetrics \u201cNarodni Front\u201d, Kraljice Natalije 62, 11000 Belgrade, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jelena","family":"Mitrovi\u0107","sequence":"additional","affiliation":[{"name":"Department of High-Risk Pregnancies, University Clinic for Gynecology and Obstetrics \u201cNarodni Front\u201d, Kraljice Natalije 62, 11000 Belgrade, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Milica","family":"Mandi\u0107","sequence":"additional","affiliation":[{"name":"Department of High-Risk Pregnancies, University Clinic for Gynecology and Obstetrics \u201cNarodni Front\u201d, Kraljice Natalije 62, 11000 Belgrade, Serbia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1002\/ijgo.13522","article-title":"FIGO (international Federation of Gynecology and obstetrics) initiative on fetal growth: Best practice advice for screening, diagnosis, and management of fetal growth restriction","volume":"152","author":"Melamed","year":"2021","journal-title":"Int. J. Gynaecol. Obstet."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"B2","DOI":"10.1016\/j.ajog.2020.05.010","article-title":"Society for Maternal-Fetal Medicine Consult Series #52: Diagnosis and management of fetal growth restriction: (Replaces Clinical Guideline Number 3, April 2012)","volume":"223","author":"Martins","year":"2020","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1002\/uog.15884","article-title":"Consensus definition of fetal growth restriction: A Delphi procedure","volume":"48","author":"Gordijn","year":"2016","journal-title":"Ultrasound. Obstet. Gynecol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1111\/jpc.15310","article-title":"Does detection of fetal growth restriction improve neonatal outcomes?","volume":"57","author":"Selvaratnam","year":"2021","journal-title":"J. Paediatr. Child Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1072","DOI":"10.1111\/1471-0528.14511","article-title":"The association of neonatal morbidity with long-term neurological outcome in infants who were growth restricted and preterm at birth: Secondary analyses from TRUFFLE (Trial of Randomized Umbilical and Fetal Flow in Europe)","volume":"124","author":"Marlow","year":"2017","journal-title":"BJOG"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/S0140-6736(04)16809-8","article-title":"Infant wellbeing at 2 years of age in the Growth Restriction Intervention Trial (GRIT): Multicentred randomised controlled trial","volume":"364","author":"Thornton","year":"2004","journal-title":"Lancet"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1038\/jp.2014.233","article-title":"The smallest of the small: Short-term outcomes of profoundly growth restricted and profoundly low birth weight preterm infants","volume":"35","author":"Griffin","year":"2015","journal-title":"J. Perinatol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"516.e1","DOI":"10.1016\/j.ajog.2017.02.001","article-title":"Fetal and neonatal outcomes of preterm infants born before 32 weeks of gestation according to antenatal vs postnatal assessments of restricted growth","volume":"216","author":"Monier","year":"2017","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/0002-9378(85)90298-4","article-title":"Estimation of fetal weight with the use of head, body, and femur measurements\u2014A prospective study","volume":"151","author":"Hadlock","year":"1985","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_10","unstructured":"Durutovic-Gligorovic, S. (2000). Intrauterine Growth of Newborn Babies, Medical Faculty, University of Belgrade."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"F273","DOI":"10.1136\/adc.2004.060723","article-title":"Skinfold measurements at birth: Sex and anthropometric influence","volume":"90","author":"Samper","year":"2005","journal-title":"Arch Dis. Child Fetal Neonatal Ed."},{"key":"ref_12","first-page":"369","article-title":"Individualized risk assesment for adverse pregnancy outcome by uterine artery Doppler at 23 weeks","volume":"98","author":"Lees","year":"2001","journal-title":"Obstet. Gynecol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1016\/0002-9378(81)90004-1","article-title":"Qualitative amniotic fluid volume determination by ultrasound: Antepartum detection of intrauterin growth retardation","volume":"139","author":"Manning","year":"1981","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1016\/0002-9378(80)90457-3","article-title":"Antepartum fetal evaluation: Development of fetal biophysical profile","volume":"136","author":"Manning","year":"1980","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1016\/j.ajog.2004.09.019","article-title":"Reference ranges for serial measurements of umbilical artery Doppler indices in the second part of pregnancy","volume":"192","author":"Acharyia","year":"2005","journal-title":"Am J. Obstet. Gynecol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1002\/uog.20157","article-title":"Fetal Medicine Foundation reference ranges for umbilical artery and middle cerebral artery pulsatility index and cerebroplacental ratio","volume":"53","author":"Ciobanu","year":"2019","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1002\/uog.4088","article-title":"Middle cerebral artery blood flow velocities and pulsatility index and the cerebroplacental pulsatility ratio: Longitudinal reference ranges and terms for serial measurements","volume":"30","author":"Ebbing","year":"2007","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1002\/uog.3857","article-title":"Longitudinal reference ranges for ductus venosus flow velocities and waveform indices","volume":"28","author":"Kessler","year":"2006","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.bpobgyn.2018.02.009","article-title":"Planning management and delivery of the growth-restricted fetus","volume":"49","author":"Baschat","year":"2018","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"F192","DOI":"10.1136\/archdischild-2017-314171","article-title":"Adverse effects of small for gestational age differ by gestational week among very preterm infants","volume":"104","author":"Jensen","year":"2019","journal-title":"Arch Dis. Child Fetal Neonatal Ed."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1002\/uog.17361","article-title":"Fetal monitoring indications for delivery and 2-year outcome in 310 infants with fetal growth restriction delivered before 32 weeks\u2019 gestation in the TRUFFLE study","volume":"50","author":"Visser","year":"2017","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1055\/s-2007-972926","article-title":"Intrauterine growth restriction and oligohydramnios among high-risk patients","volume":"24","author":"Chauhan","year":"2007","journal-title":"Am. J. Perinatol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1159\/000324570","article-title":"Oligohydramnios, small for gestational age and pregnancy outcomes: An analysis using precise measures","volume":"72","author":"Magann","year":"2011","journal-title":"Gynecol. Obstet. Invest."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1016\/j.ajog.2004.05.066","article-title":"What antepartum fetal test should guide the timing of delivery of the preterm growth-restricted fetus? A decision-analysis","volume":"191","author":"Odibo","year":"2004","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"264.e1","DOI":"10.1016\/j.ajog.2008.06.074","article-title":"Biophysical profile in the treatment of intrauterine growth-restricted fetuses who weigh <1000 g","volume":"199","author":"Kaur","year":"2008","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"669.e1","DOI":"10.1016\/j.ajog.2014.06.022","article-title":"A comparison of Doppler and biophysical findings between liveborn and stillborn growth-restricted fetuses","volume":"211","author":"Crimmins","year":"2014","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/j.ajog.2022.01.020","article-title":"The role of the fetal biophysical profile in the management of fetal growth restriction","volume":"226","author":"Baschat","year":"2022","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.tjog.2012.04.039","article-title":"Two-year neurological outcome of very-low-birth-weight children with prenatal absent or reversed end-diastolic flow velocity in the umbilical artery","volume":"52","author":"Chen","year":"2013","journal-title":"Taiwan J. Obstet. Gynecol."},{"key":"ref_29","first-page":"e1","article-title":"Defining the residual risk of adverse perinatal outcome in growth-restricted fetuses with normal umbilical artery blood flow","volume":"211","author":"Burke","year":"2014","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.ejogrb.2005.07.008","article-title":"Intrauterine growth restriction and absent or reverse end-diastolic blood flow in umbilical artery (Doppler class II or III): A retrospective study of short- and long-term fetal morbidity and mortality","volume":"126","author":"Gerber","year":"2006","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"837","DOI":"10.7863\/ultra.34.5.837","article-title":"Estimation of the growth rate in fetuses with an abnormal cerebroplacental ratio compared to those with suspected growth restriction without evidence of centralization of blood flow","volume":"34","author":"Regan","year":"2015","journal-title":"J. Ultrasound Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3201","DOI":"10.1080\/14767058.2017.1369519","article-title":"Relationship between Doppler findings and fetal brain apparent diffusion coefficient in early-onset intra-uterine growth restriction","volume":"31","author":"Kutuk","year":"2018","journal-title":"J. Matern. Fetal Neonatal Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1002\/uog.18809","article-title":"Prognostic accuracy of cerebroplacental ratio and middle cerebral artery Doppler for adverse perinatal outcome: Systematic review and meta-analysis","volume":"51","author":"Heymans","year":"2018","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1111\/1471-0528.16287","article-title":"Cerebroplacental ratio in predicting adverse perinatal outcome: A meta-analysis of individual participant data","volume":"128","author":"Heymans","year":"2021","journal-title":"BJOG"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1111\/aogs.13782","article-title":"Ductus venosus Doppler waveform pattern in fetuses with early growth restriction","volume":"99","author":"Fratelli","year":"2020","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1002\/uog.13190","article-title":"Perinatal morbidity and mortality in early-onset fetal growth restriction: Cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE)","volume":"42","author":"Lees","year":"2013","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"S783","DOI":"10.1016\/j.ajog.2017.12.226","article-title":"TRUFFLE Investigators. Outcome in early-onset fetal growth restriction is best combining computerized fetal heart rate analysis with ductus venosus Doppler: Insights from the Trial of Umbilical and Fetal Flow in Europe","volume":"218","author":"Frusca","year":"2018","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2162","DOI":"10.1016\/S0140-6736(14)62049-3","article-title":"2 year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): A randomised trial","volume":"385","author":"Lees","year":"2015","journal-title":"Lancet"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1002\/jcu.21970","article-title":"Umbilical Venous Blood Flow and Its Measurement in the Human Fetus","volume":"40","author":"Najafzadeh","year":"2012","journal-title":"J. Clin. Ultrasound"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1002\/uog.20354","article-title":"Comparative analysis of 2-year outcomes in GRIT and TRUFFLE trials","volume":"55","author":"Ganzevoort","year":"2020","journal-title":"Ultrasound Obstet. Gynecol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.ejogrb.2019.01.005","article-title":"The prognostic accuracy of short-term variation of fetal heart rate in early-onset fetal growth restriction: A systematic review","volume":"234","author":"Pels","year":"2019","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"3221","DOI":"10.1080\/14767058.2018.1461313","article-title":"Management of fetal growth restriction using the contraction stress test: A case-control study","volume":"32","author":"Tanaka","year":"2019","journal-title":"J. Matern Fetal Neonatal Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1002\/pd.4412","article-title":"Stage-based approach to the management of fetal growth restriction","volume":"34","author":"Figueras","year":"2014","journal-title":"Prenatal Diagnosis"},{"key":"ref_44","first-page":"CD007529","article-title":"Fetal and umbilical Doppler ultrasound in high-risk pregnancies","volume":"6","author":"Alfirevic","year":"2017","journal-title":"Cochrane Database Syst. Rev."},{"key":"ref_45","first-page":"139","article-title":"Combined Sonographic testing index and prediction of adverse outcome in preterm Fetal growth restriction","volume":"31","author":"Odibo","year":"2014","journal-title":"Am. J. Perinatol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.ejogrb.2019.08.007","article-title":"A prediction model for short-term neonatal outcomes in severe early-onset fetal growth restriction","volume":"241","author":"Sharp","year":"2019","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/59\/2\/406\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:36:37Z","timestamp":1760121397000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/59\/2\/406"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,19]]},"references-count":46,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["medicina59020406"],"URL":"https:\/\/doi.org\/10.3390\/medicina59020406","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,19]]}}}