{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T16:30:56Z","timestamp":1786984256249,"version":"build-2736575974"},"reference-count":43,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2018,2,1]],"date-time":"2018-02-01T00:00:00Z","timestamp":1517443200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2018,2,1]],"date-time":"2018-02-01T00:00:00Z","timestamp":1517443200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"content-domain":{"domain":["ajog.org","clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["American Journal of Obstetrics and Gynecology"],"published-print":{"date-parts":[[2018,2]]},"DOI":"10.1016\/j.ajog.2017.12.226","type":"journal-article","created":{"date-parts":[[2018,2,5]],"date-time":"2018-02-05T19:16:59Z","timestamp":1517858219000},"page":"S783-S789","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":59,"special_numbering":"S","title":["Outcome in early-onset fetal growth restriction is\u00a0best combining computerized fetal heart rate analysis with ductus venosus Doppler: insights from the Trial of Umbilical and Fetal Flow in Europe"],"prefix":"10.1016","volume":"218","author":[{"given":"Tiziana","family":"Frusca","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tullia","family":"Todros","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2104-5561","authenticated-orcid":false,"given":"Christoph","family":"Lees","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caterina M.","family":"Bilardo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kurt","family":"Hecher","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerard H.A.","family":"Visser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aris T.","family":"Papageorghiou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neil","family":"Marlow","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Baskaran","family":"Thilaganathan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aleid","family":"van Wassenaer-Leemhuis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karel","family":"Marsal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Birgit","family":"Arabin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Brezinka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan B.","family":"Derks","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anke","family":"Diemert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes J.","family":"Duvekot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enrico","family":"Ferrazzi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.W.","family":"Ganzevoort","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pasquale","family":"Martinelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eva","family":"Ostermayer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dietmar","family":"Schlembach","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Herbert","family":"Valensise","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jim","family":"Thornton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hans","family":"Wolf","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.ajog.2017.12.226_bib1","first-page":"426","article-title":"Correlation between initial neonatal and early childhood outcomes following preterm birth","volume":"210","author":"Manuck","year":"2014","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib2","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1097\/AOG.0000000000000243","volume":"123","author":"Raju","year":"2014","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib3","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1111\/j.1651-2227.2010.01846.x","article-title":"Incidence of and risk factors for neonatal morbidity after active perinatal care: extremely preterm infants study in Sweden (EXPRESS)","volume":"99","year":"2010","journal-title":"Acta Paediatr"},{"key":"10.1016\/j.ajog.2017.12.226_bib4","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1002\/uog.7627","article-title":"Predictors of outcome at 2 years of age after early intrauterine growth restriction","volume":"36","author":"Torrance","year":"2010","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib5","doi-asserted-by":"crossref","first-page":"874","DOI":"10.1542\/peds.2010-1821","article-title":"Cognitive function after intrauterine growth restriction and very preterm birth","volume":"127","author":"Morsing","year":"2011","journal-title":"Pediatrics"},{"key":"10.1016\/j.ajog.2017.12.226_bib6","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1002\/uog.7321","article-title":"Early intervention in management of very preterm growth-restricted fetuses: 2-year outcome of infants delivered on fetal indication before 30 gestational weeks [Erratum in: Ultrasound Obstet Gynecol 2009;34:489]","volume":"34","author":"Brodszki","year":"2009","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib7","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1046\/j.0960-7692.2002.00653.x","article-title":"Timing the delivery of the preterm severely growth-restricted fetus: venous Doppler, cardiotocography or the biophysical profile?","volume":"19","author":"Romero","year":"2002","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib8","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1046\/j.1471-0528.2003.02014.x","article-title":"A\u00a0randomized trial of timed delivery for the compromised preterm fetus: short term outcomes and Bayesian interpretation","volume":"110","year":"2003","journal-title":"BJOG"},{"key":"10.1016\/j.ajog.2017.12.226_bib9","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1016\/S0140-6736(04)16809-8","article-title":"Infant well-being at 2 years of age in the Growth Restriction Intervention Trial (GRIT): multicentered randomized controlled trial","volume":"364","author":"Thornton","year":"2004","journal-title":"Lancet"},{"key":"10.1016\/j.ajog.2017.12.226_bib10","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.ajog.2010.09.019","article-title":"The Growth Restriction Intervention Trial: long-term outcomes in a randomized trial of timing of delivery in fetal growth restriction","volume":"204","author":"Walker","year":"2011","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib11","first-page":"CD008968","article-title":"Immediate versus deferred delivery of the preterm baby with suspected fetal compromise for improving outcomes","volume":"7","author":"Stock","year":"2016","journal-title":"Cochrane Database Syst Rev"},{"key":"10.1016\/j.ajog.2017.12.226_bib12","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/0002-9378(93)90002-Z","article-title":"Fetal biophysical profile score. VI. Correlation with antepartum umbilical venous fetal pH","volume":"169","author":"Manning","year":"1993","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib13","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.1136\/bmj.297.6655.1026","article-title":"Absence of end-diastolic frequencies in umbilical artery: a sign of fetal hypoxia and acidosis","volume":"297","author":"Nicolaides","year":"1988","journal-title":"BMJ"},{"key":"10.1016\/j.ajog.2017.12.226_bib14","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1046\/j.0960-7692.2001.00591.x","article-title":"The sequence of Doppler and biophysical parameters as severe fetal growth restriction worsens","volume":"18","author":"Baschat","year":"2001","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib15","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1016\/S0002-9378(94)70285-3","article-title":"Absent end-diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage","volume":"170","author":"Valcamonico","year":"1994","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib16","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1046\/j.0960-7692.2001.00590.x","article-title":"Monitoring of fetuses with intrauterine growth restriction: a longitudinal study","volume":"18","author":"Hecher","year":"2001","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib17","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1002\/uog.965","article-title":"Relationship between monitoring parameters and perinatal outcome in severe, early intrauterine growth restriction","volume":"23","author":"Bilardo","year":"2004","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib18","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1097\/01.AOG.0000253215.79121.75","article-title":"Predictors of neonatal outcome in early-onset placental dysfunction","volume":"109","author":"Baschat","year":"2007","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib19","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1016\/j.bpobgyn.2009.06.003","article-title":"Risk factors for small for gestational age infants","volume":"23","author":"McGowan","year":"2009","journal-title":"Best Pract Res Clin Obstet Gynaecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib20","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/s40748-016-0041-x","article-title":"Early onset fetal growth restriction","volume":"3","author":"Dall'Asta","year":"2017","journal-title":"Matern Health Neonatol Perinatol"},{"key":"10.1016\/j.ajog.2017.12.226_bib21","unstructured":"RCOG Green Top Guideline No. 31. The investigation and management of the small-for-gestational age fetus. London, UK: 2014."},{"key":"10.1016\/j.ajog.2017.12.226_bib22","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":"10.1016\/j.ajog.2017.12.226_bib23","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1016\/0002-9378(91)90277-X","article-title":"Short term variation in abnormal antenatal fetal heart rate records","volume":"165","author":"Street","year":"1991","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib24","first-page":"673","article-title":"Short-term fetal heart rate variation, decelerations and fetal umbilical flow waveforms before labor","volume":"80","author":"Dawes","year":"1992","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib25","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1111\/j.1471-0528.1991.tb13489.x","article-title":"Relation of fetal blood gases and data from computer-assisted analysis of fetal heart rate patterns in small for gestational fetuses","volume":"98","author":"Ribbert","year":"1991","journal-title":"Br J Obstet Gynaecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib26","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 randomized trial","volume":"385","author":"Lees","year":"2015","journal-title":"Lancet"},{"key":"10.1016\/j.ajog.2017.12.226_bib27","doi-asserted-by":"crossref","first-page":"1122","DOI":"10.1097\/01.AOG.0000429658.85846.f9","article-title":"Fetal growth restriction. ACOG Practice bulletin no. 134","volume":"121","year":"2013","journal-title":"Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib28","doi-asserted-by":"crossref","first-page":"290.e1","DOI":"10.1016\/j.ajog.2013.02.007","article-title":"Optimizing the definition of intrauterine growth restriction: the multicenter prospective PORTO study","volume":"208","author":"Unterscheider","year":"2013","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib29","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":"Gordijin","year":"2016","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib30","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1159\/000358058","article-title":"Fetal growth restriction at the limits of viability","volume":"36","author":"Visser","year":"2014","journal-title":"Fetal Diagn Ther"},{"key":"10.1016\/j.ajog.2017.12.226_bib31","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1046\/j.0960-7692.2002.00627.x","article-title":"Temporal sequence of abnormal Doppler changes in the peripheral and central circulatory systems of the severely growth-restricted fetus","volume":"19","author":"Ferrazzi","year":"2002","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib32","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1002\/uog.5386","article-title":"Progression of Doppler abnormalities in intrauterine growth restriction","volume":"32","author":"Turan","year":"2008","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib33","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1016\/j.jpeds.2011.09.047","article-title":"Relationship between test scores using the second and third editions of the Bayley Scales in extremely preterm children","volume":"160","author":"Moore","year":"2012","journal-title":"J\u00a0Pediatr"},{"key":"10.1016\/j.ajog.2017.12.226_bib34","unstructured":"American College of Obstetricians and Gynecologists; Task Force on Hypertension in Pregnancy 2013. Available at: https:\/\/www.acog.org\/Clinical-Guidance-and-Publications\/Task-Force-and-Work-Group-Reports\/Hypertension-in-Pregnancy. Accessed January 11, 2018."},{"key":"10.1016\/j.ajog.2017.12.226_bib35","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1046\/j.0960-7692.2001.00572.x","article-title":"Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation","volume":"18","author":"Papageorghiou","year":"2001","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib36","doi-asserted-by":"crossref","first-page":"521.e1","DOI":"10.1016\/j.ajog.2017.01.001","article-title":"Is middle cerebral artery Doppler related to neonatal and 2-year infant outcome in early fetal growth restriction?","volume":"216","author":"Stampalija","year":"2017","journal-title":"Am J Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib37","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1002\/uog.17361","article-title":"The TRUFFLE study; fetal monitoring indications for delivery in 310 IUGR infants with 2 year's outcome delivered before 32 weeks of gestation","volume":"50","author":"Visser","year":"2017","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib38","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":"Van Wassenaer-Leemhuis","year":"2017","journal-title":"BJOG"},{"key":"10.1016\/j.ajog.2017.12.226_bib39","first-page":"43","article-title":"Antenatal prediction of fetal pH in growth-restricted fetuses using computer analysis of the fetal heart rate","volume":"7","author":"Guzman","year":"1998","journal-title":"J\u00a0Matern Fetal Med"},{"key":"10.1016\/j.ajog.2017.12.226_bib40","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1016\/S0140-6736(98)08229-4","article-title":"Effect of antenatal betamethasone administration on placental vascular resistance","volume":"353","author":"Wallace","year":"1999","journal-title":"Lancet"},{"key":"10.1016\/j.ajog.2017.12.226_bib41","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1002\/uog.17215","article-title":"Longitudinal study of computerized cardiotocography in early fetal growth restriction","volume":"50","author":"Wolf","year":"2017","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib42","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1002\/uog.14714","article-title":"An integrated model with classification criteria to predict small-for-gestational-age fetuses at risk of adverse perinatal outcome","volume":"45","author":"Figueras","year":"2015","journal-title":"Ultrasound Obstet Gynecol"},{"key":"10.1016\/j.ajog.2017.12.226_bib43","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1002\/uog.18815","article-title":"Severe fetal growth restriction at 26-32 weeks: key messages from the TRUFFLE study","volume":"50","author":"Bilardo","year":"2017","journal-title":"Ultrasound Obstet Gynecol"}],"container-title":["American Journal of Obstetrics and Gynecology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0002937817327254?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0002937817327254?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,11]],"date-time":"2025-09-11T11:16:59Z","timestamp":1757589419000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0002937817327254"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,2]]},"references-count":43,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2018,2]]}},"alternative-id":["S0002937817327254"],"URL":"https:\/\/doi.org\/10.1016\/j.ajog.2017.12.226","relation":{},"ISSN":["0002-9378"],"issn-type":[{"value":"0002-9378","type":"print"}],"subject":[],"published":{"date-parts":[[2018,2]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Outcome in early-onset fetal growth restriction is\u00a0best combining computerized fetal heart rate analysis with ductus venosus Doppler: insights from the Trial of Umbilical and Fetal Flow in Europe","name":"articletitle","label":"Article Title"},{"value":"American Journal of Obstetrics and Gynecology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.ajog.2017.12.226","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2018 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}