Cited by 354Pregnancy and preeclampsia studiesBirth, Development, and HealthCardiovascular Conditions and Treatments

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Progression of Doppler abnormalities in intrauterine growth restriction

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Turan, O. M., Turan, S., Gungor, S., Berg, C., Moyano, D., Gembruch, U., Nicolaides, K. H., Harman, C. R., Baschat, A. A.·2008·Ultrasound in Obstetrics & Gynecology

DOI 10.1002/uog.5386

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Abstract

Objective: To identify the sequence of progression of arterial and venous Doppler abnormalities from the onset of placental insufficiency in intrauterine growth restriction (IUGR). Methods: Prospective observational study of singletons with IUGR (abdominal circumference < 5th percentile) who underwent serial standardized umbilical artery (UA), middle cerebral artery (MCA), ductus venosus (DV) and umbilical vein (UV) Doppler surveillance. Time intervals between progressive Doppler abnormalities and patterns of deterioration were related to UA Doppler status and gestational age. Results: Six hundred and sixty‐eight longitudinal examinations were performed in 104 fetuses, identifying three patterns of progression: (1) Mild placental dysfunction (n = 34) that remained confined to the UA/MCA. The UA became abnormal at a median of 32 weeks' gestation but the pulsatility index never exceeded 3 SD above normal. Progression took a median of 33 days, requiring delivery at a median of 35 weeks. (2) Progressive placental dysfunction (n = 49). Initially normal UA Doppler PI at 29 weeks' gestation increased beyond 3 SD, progressing to abnormal MCA, absent/reversed UA diastolic flow, abnormal DV, UV pulsations in 9‐day intervals requiring delivery by 33 weeks. (3) Severe early‐onset placental dysfunction (n = 21). Markedly elevated UA PI established by 27 weeks' gestation was associated with rapid (7‐day intervals) progression to abnormal venous Doppler with median delivery at 30.6 weeks. Gestational age at onset, time to delivery and progression intervals were different between patterns (all P < 0.05). Conclusion: The characteristics of cardiovascular manifestations in IUGR are determined by the gestational age at onset and the severity of placental disease. Recognition of these factors is critical for planning fetal surveillance in IUGR. Copyright © 2008 ISUOG. Published by John Wiley & Sons, Ltd.

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Method
Thymic volume in healthy, small for gestational age and growth restricted fetuses
Olearo, E., Oberto, M., Oggè, G., Botta, G., Pace, C., Gaglioti, P., & Todros, T. (2012) · Prenatal Diagnosis · doi:10.1002/pd.3883 · Cited by 42
“All IUGR with abnormal umbilical artery FVW presented with worsening umbilical artery Doppler and compromise of fetal well-being before 30weeks of GA, a condition that Turan et al.26 defined as ‘severe early-onset placental dysfunction’.”
Background
sFlt ‐1/ PlGF ratio and timing of delivery in early‐onset fetal growth restriction with antegrade umbilical artery flow
Quezada, M. S., Rodríguez‐Calvo, J., Villalaín, C., Gómez‐Arriaga, P. I., Galindo, A., & Herraı̀z, I. (2019) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.21949 · Cited by 42
Abnormal antenatal Doppler velocimetry and cognitive outcome in very‐low‐birth‐weight infants at 2 years of age
Leppänen, M. H., Ekholm, E. M. K., Palo, P., Maunu, J., Munck, P., Parkkola, R. K., Matomäki, J., Lapinleimu, H., Haataja, L. M., Lehtonen, L., et al. (2010) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7694 · Cited by 42
Gene expression patterns of vascular endothelial growth factor (VEGF-A) in human placenta from pregnancies with intrauterine growth restriction
Szentpéteri, I., Rab, A., Kornya, L., Kovacs, P. L., & Joó, J. G. (2013) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2013.766702 · Cited by 40
Ten‐year experience of protocol‐based management of small‐for‐gestational‐age fetuses: perinatal outcome in late‐pregnancy cases diagnosed after 32 weeks
Meler, E., Mazarico, E., Eixarch, E., Gonzalez, A., Peguero, A., Martinez, J., Boada, D., Vellvé, K., Gomez‐Roig, M. D., Gratacós, E., et al. (2021) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.23537 · Cited by 36
Systematic examination of the fetal abdominal precordial veins: a cohort study
Yagel, S., Cohen, S. M., Valsky, D. V., Shen, O., Lipschuetz, M., & Messing, B. (2014) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.13444 · Cited by 38
Impaired Fetoplacental Angiogenesis in Growth-Restricted Fetuses With Abnormal Umbilical Artery Doppler Velocimetry Is Mediated by Aryl Hydrocarbon Receptor Nuclear Translocator (ARNT)
Su, E. J., Xin, H., Yin, P., Dyson, M. T., Coon, J. S., Farrow, K. N., Mestan, K. K. L., & Ernst, L. M. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2385 · Cited by 37
Examination of the fetal cardiovascular system
Baschat, A. (2010) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2010.09.002 · Cited by 37
Self-citation
Local Over-Expression of VEGF-DΔNΔC in the Uterine Arteries of Pregnant Sheep Results in Long-Term Changes in Uterine Artery Contractility and Angiogenesis
Mehta, V., Abi-Nader, K. N., Shangaris, P., Shaw, S. W., Filippi, E., Benjamin, E., Boyd, M. B., Peebles, D., Martin, J. F., Zachary, I. C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100021 · Cited by 36
“4SD above the mean for gestation) could be considered at a very high risk for morbidity and mortality [34].”
Mid‐pregnancy fetal biometry, uterine artery Doppler indices and maternal demographic characteristics: role in prediction of small‐for‐gestational‐age birth
Familiari, A., Bhidé, A., Morlando, M., Scala, C., Khalil, A. A., & Thilaganathan, B. (2015) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.12804 · Cited by 36
Does pre‐eclampsia influence fetal cardiovascular function in early‐onset intrauterine growth restriction?
Crispi, F., Comas, M., Hernandez‐Andrade, E. A., Eixarch, E., Gómez, O., Figueras, F., & Gratacós, E. (2009) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7450 · Cited by 36
Umbilical venous blood flow and its measurement in the human fetus
Najafzadeh, A., & Dickinson, J. E. (2012) · Journal of Clinical Ultrasound · doi:10.1002/jcu.21970 · Cited by 35
Fetal cerebrovascular response to maternal hyperoxygenation in congenital heart disease: effect of cardiac physiology
Hogan, W. J., Moon‐Grady, A. J., Zhao, Y., Cresalia, N. M., Nawaytou, H. M., Quezada, E., Brook, M. M., McQuillen, P. S., & Peyvandi, S. (2020) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.22024 · Cited by 33
Clinical impact of Doppler reference charts on management of small‐for‐gestational‐age fetuses: need for standardization
Ruiz, S., Papageorghiou, A. T., Staines-Urias, E., Villar, J., de Agüero, R. G., & Oros, D. (2019) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20380 · Cited by 30
Diagnostic accuracy of Doppler ultrasound in predicting perinatal outcome in pregnancies at term: A prospective longitudinal study
D’Antonio, F., Rizzo, G., Gustapane, S., Buca, D. I. P., Flacco, M. E., Martellucci, C. A., Manzoli, L., Makatsariya, A. D., Nappi, L., Pagani, G. A., et al. (2019) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.13705 · Cited by 30
Functional echocardiography in the fetus with non-cardiac disease
Mieghem, T. V., Hodges, R. J., JAEGGI, E. T., & Ryan, G. (2013) · Prenatal Diagnosis · doi:10.1002/pd.4254 · Cited by 28
“This can be documented as a progressive increase in pulsatility index in the ductus venosus,(22) manifested initially as deepening and ultimately reversal of the a-wave.(24) A pulsatile flow pattern can occur in the umbilical vein.”
Background
Angiogenic factors for planning fetal surveillance in fetal growth restriction and small‐for‐gestational‐age fetuses: A prospective observational study
Bonacina, E., Mendoza, M., Farràs, A., García‐Manau, P., Serrano, B., Hurtado, I., Ferrer‐Oliveras, R., Illan, L., Armengol‐Alsina, M., & Carreras, E. (2022) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.17151 · Cited by 27
Doppler US in the Evaluation of Fetal Growth and Perinatal Health
Uquillas, K. R., Grubbs, B. H., Prosper, A. E., Chmait, R. H., Grant, E. G., & Walker, D. K. (2017) · Radiographics · doi:10.1148/rg.2017170020 · Cited by 26
“The temporal sequence of Doppler-measured flow abnormalities in the arterial and venosus circulations of growth-restricted fetuses has been documented in the literature (21).”
Background
Venous Doppler Evaluation of the Growth-Restricted Fetus
Baschat, A. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2010.12.001 · Cited by 25
Self-citation
Patterns of Brain Sparing in a Fetal Growth Restriction Cohort
Steller, J. G., Gumina, D. L., Driver, C., Peek, E., Galan, H. L., Reeves, S. A., & Hobbins, J. C. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11154480 · Cited by 25
Antenatal Surveillance of Fetal Growth Restriction
Thompson, J. L., Kuller, J. A., & Rhee, E. H. J. (2012) · Obstetrical & Gynecological Survey · doi:10.1097/ogx.0b013e31826a5c6f · Cited by 25
“There is also a decrease in umbilical venous volume flow, which precedes clinical recognition of growth delay.(87) Impaired fetal growth is then observed initially as a lag in the fetal abdominal circumference.”
Background
Use of Placental Growth Factor and Uterine Artery Doppler Pulsatility Index in Pregnancies Involving Intrauterine Fetal Growth Restriction or Preeclampsia to Predict Perinatal Outcomes
Gómez‐Roig, M. D., Mazarico, E., Sabrià, J., Parra, J., Otón, L., & Vela, A. (2015) · Gynecologic and Obstetric Investigation · doi:10.1159/000370332 · Cited by 24
Two‐dimensional and three‐dimensional Doppler assessment of fetal growth restriction with different severity and onset
Luria, O., Barnea, O., Shalev, J., Barkat, J., Kovo, M., Golan, A., & Bar, J. (2012) · Prenatal Diagnosis · doi:10.1002/pd.3980 · Cited by 24
Foetal Haemodynamic Response to Anaemia
Thammavong, K., Luewan, S., Jatavan, P., & Tongsong, T. (2020) · ESC Heart Failure · doi:10.1002/ehf2.12969 · Cited by 23
“or a longstanding increase in afterload in foetal growth restriction and is usually considered an ominous sign.(51)”
Background
Pregnancy outcome and placental pathology in small for gestational age neonates in relation to the severity of their growth restriction
Gluck, O., Schreiber, L., Marciano, A., Mizrachi, Y., Bar, J., & Kovo, M. (2017) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2017.1408070 · Cited by 22
CpG signalling, H2A.Z/H3 acetylation and microRNA-mediated deferred self-attenuation orchestrate foetal NOS3 expression
Postberg, J., Kanders, M., Forcob, S., Willems, R., Orth, V., Hensel, K. O., Weil, P. P., Wirth, S., & Jenke, A. C. W. (2015) · Clinical Epigenetics · doi:10.1186/s13148-014-0042-4 · Cited by 22
“Patients were grouped with respect to blood flow characteristics in the uterine artery (UA), the mediocerebral artery (MCA), and the ductus venosus (DV) as follows [50]:”
Method
When is the optimal time to deliver late preterm IUGR fetuses with abnormal umbilical artery Dopplers?
Lee, V. R., Pilliod, R. A., Frias, A. E., Rasanen, J. P., Shaffer, B. L., & Caughey, A. B. (2015) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2015.1018170 · Cited by 21
“5 [16] Relative risk of stillbirth in SGA fetuses with elevated UADs 3.”
BackgroundMethodInfluential
Stillbirth: we can do better
Silver, R. M., & Reddy, U. M. (2024) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2024.05.042 · Cited by 22
Fetal Growth Restriction – Diagnostic Work-up, Management and Delivery
Schlembach, D. (2020) · Geburtshilfe und Frauenheilkunde · doi:10.1055/a-1232-1418 · Cited by 21
“…or increased pulsatility in the ductus veno-sus including loss of the positive a-wave; absent a-wave or reverse blood flow is an indication of cardiovascular instability and may be a sign of imminent or already present acidemia [47 – 49], with the risk of intrauterine death doubling daily [45,47].”
The sFlt1/PlGF ratio predicts faster fetal deterioration in early fetal growth restriction: A historical cohort study
dos Reis, C. R. P., Brás, S. A., Meneses, T., Cerdeira, A. S., Vatish, M., & Martins, A. T. (2023) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.14546 · Cited by 20
“16 The sFlt1/PlGF ratio could be a useful tool to predict fetal deterioration in this setting.”
BackgroundMethod
Third-trimester Reference Ranges for Cerebroplacental Ratio, Middle Cerebral Artery, and Umbilical Artery Pulsatility Index in Normal-growth Singleton Fetuses in the Israeli Population
Zohav, E., Zohav, E., Rabinovich, M., Alasbah, A., Shenhav, S., Sofer, H., Ovadia, Y. S., Anteby, E. Y., & Grin, L. (2019) · Rambam Maimonides Medical Journal · doi:10.5041/rmmj.10379 · Cited by 19
Childhood cognitive development after fetal growth restriction
Llurba, E., Baschat, A., Turan, O., Harding, J. E., & McCowan, L. M. E. (2013) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.12388 · Cited by 19
Self-citation
An assessment of predictive value of the biophysical profile in women with preeclampsia using data from the fullPIERS database
Payne, B. A., Kyle, P. M., Lim, K. I., Lisonkova, S., Magee, L. A., Pullar, B., Qu, Z., & von Dadelszen, P. (2013) · Pregnancy Hypertension · doi:10.1016/j.preghy.2013.03.001 · Cited by 19
“In the setting of IUGR, the biophysical changes measured by the BPP have been shown to occur late in the sequence of events caused by chronic fetal hypoxia [16,17].”
Background
Individual risk assessment for prenatal counseling in early‐onset growth‐restricted and small‐for‐gestational‐age fetuses
Mendoza, M., Hurtado, I., Bonacina, E., García‐Manau, P., Serrano, B., Tur, H., Rodó, C., Maíz, N., & Carreras, E. (2020) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.14032 · Cited by 19
Pregnancy Programming and Preeclampsia: Identifying a Human Endothelial Model to Study Pregnancy-Adapted Endothelial Function and Endothelial Adaptive Failure in Preeclamptic Subjects
Boeldt, D. S., Hankes, A., Alvarez, R. E., Khurshid, N., Balistreri, M., Grummer, M. A., Yi, F.-X., & Bird, I. M. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1031-1_4 · Cited by 19
Cardiovascular adaptation to extrauterine life after intrauterine growth restriction
Guerineau, L. R., Pérez‐Cruz, M., Gómez‐Roig, M. D., Lasaosa, F. J. C., Carretero, J. M., Prada, F., Gómez, O., Crispi, F., & Bartrons, J. (2017) · Cardiology in the Young · doi:10.1017/s1047951117001949 · Cited by 19
“The study group was formed by neonates with late-onset intrauterine growth restriction with significant changes in the uterine artery Doppler and cerebroplacental ratio in the prenatal ultrasound, which showed that placental insufficiency and haemodynamic redistribution took place in the foetal life.(19) One of the mo…”
Prediction of perinatal survival in early‐onset fetal growth restriction: role of placental growth factor
Rodríguez‐Calvo, J., Villalaín, C., Gómez‐Arriaga, P. I., Quezada, M. S., Herraı̀z, I., & Galindo, A. (2022) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.26116 · Cited by 18
Alterations in time intervals of ductus venosus and atrioventricular flow velocity waveforms in growth‐restricted fetuses
Wada, N., Tachibana, D., Kurihara, Y., Nakagawa, K., Nakano, A., Terada, H., Tanaka, K., Fukui, M., Koyama, M., & Hecher, K. (2014) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.14717 · Cited by 18

Authors: Turan, O. M., Turan, S., Gungor, S., Berg, C., Moyano, D., Gembruch, U., Nicolaides, K. H., Harman, C. R., & Baschat, A. A.
Affiliations: University of Maryland, Baltimore (US)
University of Bonn (DE)
Harris Birthright Research Centre for Fetal Medicine (GB)
Corresponding author: Baschat, A. A.
ORCID: Turan, O. M.
Turan, S.
Berg, C.
Gembruch, U.
Nicolaides, K. H.
Harman, C. R.
Baschat, A. A.
Venue: Ultrasound in Obstetrics & Gynecology
Publisher: Wiley
Published: 2008-07-15
Volume: 32
Issue: 2
Pages: 160-167
ISSN: 0960-7692 (ISSN-L)
1469-0705
DOI: 10.1002/uog.5386
OpenAlex: W2136237774
Semantic Scholar: a3107662a43e356994ae81184ea4120ca9962b26
Cited by: 353
References: 20
Citations by year: 2026: 16 · 2025: 9 · 2024: 16 · 2023: 20 · 2022: 17 · 2021: 30 · 2020: 27 · 2019: 18 · 2018: 22 · 2017: 23 · 2016: 18 · 2015: 18 · 2014: 27 · 2013: 20 · 2012: 19
FWCI: 19.88
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Ultrasound in Obstetrics and Gynecology (publishedVersion)
PubMed (publishedVersion)
Research Portal (King's College London) (submittedVersion)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Cardiovascular Conditions and Treatments
Keywords: fetal growth restriction, placental insufficiency, umbilical artery Doppler, middle cerebral artery Doppler, ductus venosus Doppler, pulsatility index, fetal monitoring, gestational age at onset
MeSH terms: Adolescent, Adult, Female, Fetal Growth Retardation, Gestational Age, Humans, Infant, Newborn, Middle Aged, Placental Insufficiency, Pregnancy, Prospective Studies, Pulsatile Flow, Umbilical Arteries, Ultrasonography, Prenatal, Disease Progression, Ultrasonography, Doppler, Pulsed, Young Adult

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Progression of Doppler abnormalities in intrauterine growth restriction

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