Doppler ultrasound in pregnancy – quality requirements of DEGUM and clinical application (part 2)

Abstract

This second part on Doppler sonography in prenatal medicine and obstetrics reviews its clinical applications. While this has not become the initially anticipated screening tool, it is used for the diagnosis and surveillance of a variety of fetal pathologies. For example, the sonography-based determination of uterine artery blood flow indices is an important parameter for the first trimester multimodal preeclampsia risk assessment, increasing accuracy and providing indication for the prophylactic treatment with aspirin. It also has significant implications for the diagnosis and surveillance of growth-restricted fetuses in the second and third trimesters through Doppler-sonographic analysis of umbilical artery, middle cerebral artery and ductus venosus. Here, especially the hemodynamics of the ductus venosus provides a critical criterium for birth management of severe, early-onset FGR before 34 + 0 weeks of gestation. Further, determination of maximum blood flow velocity of the middle cerebral artery is a central parameter in fetal diagnosis of anemia which has been significantly improved by this analysis. However, it is important to note that the mentioned improvements can only be achieved through highest methodological quality. Importantly, all these analyses are also applied to twins and higher order multiples. Here, for the differential diagnosis of specific complications such as TTTS, TAPS and TRAP, the application of Doppler sonography has become indispensable. To conclude, the successful application of Doppler sonography requires both exact methodology and precise pathophysiological interpretation of the data.

Key words

dopplersonography - fetal surveillance - guideline - clinical application

Publication History

Received: 27 February 2021

Accepted: 16 March 2021

Article published online:
27 April 2021

• References

• 1 Faber R, Heling KS, Steiner H. et al. Dopplersonografie in der Schwangerschaft – Qualitätsanforderungen der DEGUM und klinischer Einsatz (Teil 1). Ultraschall in Med 2019; 40: 319-325
• 2 Harrington K, Cooper D, Lees C. et al. Doppler ultrasound of the uterine arteries: the importance of bilateral notching in the prediction of pre-eclampsia, placental abruption or delivery of a small-for-gestational-age baby. Ultrasound Obstet Gynecol 1996; 7: 182-188
• 3 Albaiges G, Missfelder-Lobos H, Lees C. et al. One-stage screening for pregnancy complications by color Doppler assessment of the uterine arteries at 23 weeks’ gestation. Obstet Gynecol 2000; 96: 559-564
• 4 Garcia B, Llurba E, Valle L. et al. Do knowledge of uterine artery resistance in the second trimester and targeted surveillance improve maternal and perinatal outcome? UTOPIA study: a randomized controlled trial. Ultrasound Obstet Gynecol 2016; 47: 680-689
• 5 Papageorghiou A, Yu C, Bindra R. et al. Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol 2001; 18: 441-449
• 6 Pedrosa AC, Matias A. Screening for pre-eclampsia: a systematic review of tests combining uterine artery Doppler with other markers. J Perinat Med 2011; 39: 619-635
• 7 Singh T, Leslie K, Bhide A. et al. Role of second-trimester uterine artery Doppler in assessing stillbirth risk. Obstet Gynecol 2012; 119: 256-261
• 8 Stampalija T, Gyte GLM, Alfirevic Z. Utero-placental Doppler ultrasound for improving pregnancy outcome. Cochrane Database Syst Rev 2010; 2010: CD008363
• 9 Bahado-Singh RO, Jodicke C. Uterine Artery Doppler in First-trimester Pregnancy Screening. Clin Obstet Gynecol 2010; 53: 879-887
• 10 Akolekar R, Syngelaki A, Poon L. et al. Competing risks model in early screening for preeclampsia by biophysical and biochemical markers. Fetal Diagn Ther 2013; 33: 8-15
• 11 Poon LC, Nicolaides K. Early Prediction of Preeclampsia. Obstet Gynecol Int 2014; 2014: 297-307
• 12 Sotiriadis A, Hernandez-Andrade E, da Silva Costa F. et al. ISUOG Practice Guidelines: role of ultrasound in screening for and follow-up of pre-eclampsia. Ultrasound Obstet Gynecol 2018; 53: 7-22
• 13 Bujold E, Roberge S, Lacasse Y. et al. Prevention of Preeclampsia and Intrauterine Growth Restriction With Aspirin Started in Early Pregnancy. Obstet Gynecol 2010; 116: 402-414
• 14 Roberge S, Villa P, Nicolaides K. et al. Early administration of low-dose aspirin for the prevention of preterm and term preeclampsia: a systematic review and meta-analysis. Fetal Diagn Ther 2012; 31: 141-146
• 15 Rolnik DL, Wright D, Poon LC. et al. Aspirin versus Placebo in Pregnancies at High Risk for Preterm Preeclampsia. N Engl J Med 2017; 377: 613-622
• 16 Khalil A, Nicolaides K. How to record uterine artery Doppler in the first trimester. Ultrasound Obstet Gynecol 2013; 42: 478-479
• 17 Gomez O, Figueras F, Martinez J. et al. Sequential changes in uterine artery blood flow pattern between the first and second trimesters of gestation in relation to pregnancy outcome. Ultrasound Obstet Gynecol 2006; 28: 802-808
• 18 Gallo DM, Wright D, Casanova C. et al. Competing risks model in screening for preeclampsia by maternal factors and biomarkers at 19–24 weeks’ gestation. Am J Obstet Gynecol 2016; 214: 619-627
• 19 Alfirevic Z, Stampalija T, Gyte GML. Fetal and umbilical Doppler ultrasound in normal pregnancy. Cochrane Database Syst Rev 2015; 2015: CD001450
• 20 Prefumo F, Guven M, Ganapathy R. et al. The longitudinal variation in uterine artery blood flow pattern in relation to birth weight. Obstet Gynecol 2004; 103: 764-768
• 21 Khalil A, Garcia-Mandujano R, Maiz N. et al. Longitudinal changes in uterine artery Doppler and blood pressure and risk of pre-eclampsia. Ultrasound Obstet Gynecol 2014; 43: 541-547
• 22 Bakalis S, Stoilov B, Akolekar R. et al. Prediction of small-for-gestational-age neonates: screening by uterine artery Doppler and mean arterial pressure at 30–34 weeks. Ultrasound Obstet Gynecol 2015; 45: 707-714
• 23 Li N, Ghosh G, Gudmundsson S. Uterine artery Doppler in high-risk pregnancies at 23–24 gestational weeks is of value in predicting adverse outcome of pregnancy and selecting cases for more intense surveillance. Acta Obstet Gynecol Scand 2014; 93: 1276-1281
• 24 Zeisler H, Llurba E, Chantraine F. et al. Predictive Value of the sFlt-1:PlGF Ratio in Women with Suspected Preeclampsia. N Engl J Med 2016; 374: 13-22
• 25 Alfirevic Z, Stampalija T, Gyte G. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev 2013; 2013: CD007529
• 26 Turan OM, Turan S, Gungor S. et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008; 32: 160-167
• 27 Baschat AA. Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction. Ultrasound Obstet Gynecol 2011; 37: 501-514
• 28 Figueras F, Gratacos E. Stage-based approach to the management of fetal growth restriction. Prenat Diagn 2014; 34: 655-659
• 29 Lees CC, Marlow N, van Wassenaer-Leemhuis A. et al. 2 year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): a randomised trial. Lancet 2015; 385: 2162-2172
• 30 Kehl S, Dötsch J, Hecher K. et al. Intrauterine Growth Restriction. Guideline of the German Society of Gynecology and Obstetrics (S2k-Level, AWMF Registry No. 015/080, October 2016). Geburtshilfe Frauenheilkd 2017; 77: 1157-1173
• 31 Conde-Agudelo A, Villar J, Kennedy H. et al. Predictive accuracy of cerebroplacental ratio for adverse perinatal and neurodevelopmental outcomes in suspected fetal growth restriction: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2018; 52: 430-441
• 32 Miranda J, Rodriguez-Lopez M, Triunfo S. et al. Prediction of fetal growth restriction using estimated fetal weight vs a combined screening model in the third trimester. Ultrasound Obstet Gynecol 2017; 50: 603-611
• 33 Baschat AA, Gembruch U. The cerebroplacental Doppler ratio revisited. Ultrasound Obstet Gynecol 2003; 21: 124-127
• 34 Oros D, Figueras F, Cruz-Martinez R. et al. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol 2011; 37: 191-195
• 35 Figueras F, Savchev S, Triunfo S. et al. An integrated model with classification criteria to predict small-for-gestational-age fetuses at risk of adverse perinatal outcome. Ultrasound Obstet Gynecol 2015; 45: 279-285
• 36 Bakalis S, Akolekar R, Gallo DM. et al. Umbilical and fetal middle cerebral artery Doppler at 30–34 weeks’ gestation in the prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol 2015; 45: 409-420
• 37 Akolekar R, Syngelaki A, Gallo DM. et al. Umbilical and fetal middle cerebral arteryDoppler at 35–37 weeks’ gestation in the prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol 2015; 46: 82-92
• 38 Oros D, Ruiz-Martinez S, Staines-Urias E. et al. Reference ranges for Doppler indices of umbilical and fetal middle cerebral arteries and cerebroplacental ratio: systematic review. Ultrasound Obstet Gynecol 2019; 53: 454-464
• 39 Mari G, Deter RL, Carpenter RL. et al. Noninvasive diagnosis by Doppler ultrasonography of fetal anemia due to maternal redcell alloimmunization. Collaborative Group for Doppler Assessment of the Blood Velocity in Anemic Fetuses. N Engl J Med 2000; 342: 9-14
• 40 Picklesimer AH, Oepkes D, Moise A. et al. Determinants of the middle cerebral artery peak systolic velocity in the human fetus. Am J Obstet Gynecol 2007; 197: 526.e1-526.e4
• 41 Mari G, Hanif F, Kruger M. et al. Middle cerebral artery peak systolic velocity: a new Doppler parameter in the assessment of growth-restricted fetuses. Ultrasound Obstet Gynecol 2007; 29: 310-316
• 42 Kempe A, Rösing B, Berg C. et al. First-trimester treatment of fetal anemia secondary to parvovirus B19 infection. Ultrasound Obstet Gynecol 2007; 29: 226-228
• 43 Hellmund A, Berg C, Geipel A. et al. Early intrauterine transfusion in fetuses with severe anemia caused by parvovirus B19 infection. Fetal Diagn Ther 2018; 43: 129-137
• 44 Oepkes D, Seaward PG, Vandenbussche FP. et al. DIAMOND Study Group: Doppler ultrasonography versus amniocentesis to predict fetal anemia. N Engl J Med 2006; 355: 156-164
• 45 Pretlove SJ, Fox CE, Khan KS. et al. Noninvasive methods of detecting fetal anaemia: a systematic review and meta-analysis. BJOG 2009; 116: 1558-1567
• 46 Scheffer PG, van der Schoot CE, Page-Christiaens GC. et al. Noninvasive fetal blood group genotyping of rhesus D, c, E and of K in alloimmunised pregnant women: evaluation of a 7-year clinical experience. BJOG 2011; 118: 1340-1348
• 47 Moise Jr KJ, Argoti PS. Management and prevention of red cell alloimmunization in pregnancy: a systematic review. Obstet Gynecol 2012; 120: 1132-1139
• 48 Mari G, Norton ME, Stone J. et al. Society of Maternal-Fetal Medicine (SFMF) Clinical Guideline #8: the fetus at risk for anemia – diagnosis and management. Am J Obstet Gynecol 2015; 212: 697-710
• 49 Detti L, Oz U, Guney I. et al. Collaborative Group for Doppler Assessment of the Blood Velocity in Anemic Fetuses: Doppler ultrasound velocimetry for timing the second intrauterine transfusion in fetuses with anemia from red cell alloimmunization. Am J Obstet Gynecol 2001; 185: 1048-1051
• 50 Scheier M, Hernandez-Andrade E, Fonseca EB. et al. Prediction of severe fetal anemia in red blood cell alloimmunization after previous intrauterine transfusions. Am J Obstet Gynecol 2006; 195: 1550-1556
• 51 Dodd JM, Andersen C, Dickinson JE. et al. MCA Doppler Study Group. Fetal middle cerebral artery Doppler to time intrauterine transfusion in red-cell alloimmunization: a randomized trial. Ultrasound Obstet Gynecol 2018; 51: 306-312
• 52 Garabedian C, Vaast P, Behal H. et al. Management of severe fetal anemia by Doppler measurement of middle cerebral artery: are there other benefits than reducing invasive procedures. Eur J Obstet Gynecol Reprod Biol 2015; 192: 27-30
• 53 Lam YH, Tang MH. Middle cerebral artery Doppler study in fetuses with homozygous alpha-thalassaemia-1 at 12–13 weeks of gestation. Prenat Diagn 2002; 22: 56-58
• 54 Leung TY, Lao TT. Thalassaemia in pregnancy. Best Pract Res Clin Obstet Gynecol 2012; 26: 37-51
• 55 Lamont RF, Sobel JD, Vaisbuch E. et al. Parvovirus B19 infection in human pregnancy. BJOG 2011; 118: 175-186
• 56 de Jong EP, Lindenburg IT, van Klink JM. et al. Intrauterine transfusion for parvovirus B19 infection: long-term neurodevelopmental outcome. Am J Obstet Gynecol 2012; 206: 204.e1-205
• 57 Cosmi E, Mari G, Delle Chiaie L. et al. Noninvasive diagnosis by Doppler ultrasonography of fetal anemia resulting from parvovirus infection. Am J Obstet Gynecol 2002; 187: 1290-1293
• 58 Amann C, Geipel A, Müller A. et al. Fetal anemia of unknown cause – a diagnostic challenge. Ultraschall in Med 2011; 32 (Suppl. 02) E115-E121
• 59 Wylie BJ, D’Alton ME. Fetomaternal hemorrhage. Obstet Gynecol 2010; 115: 1039-1051
• 60 Tamblyn JA, Norton A, Spurgeon L. et al. Prenatal therapy in transient abnormal myelopoiesis: a systematic review. Arch Dis Child Fetal Neonatal Ed 2016; 101: F67-F71
• 61 Khalil A, Rodgers M, Baschat A. et al. ISUOG Practice Guidelines: role of ultrasound in twin pregnancy. Ultrasound Obstet Gynecol 2016; 47: 247-263
• 62 Geipel A, Berg C, Germer U. et al. Doppler assessment of the uterine circulation in the second trimester in twin pregnancies: prediction of pre-eclampsia, fetal growth restriction and birth weight discordance. Ultrasound Obstet Gynecol 2002; 20: 541-545
• 63 Fisk NM, Duncombe GJ, Sullivan M. The basic and clinical science of twin-twin transfusion syndrome. Placenta 2009; 30: 379-390
• 64 Quintero RA, Morales WJ, Allen MH. et al. Staging of twin-twin transfusion syndrome. J Perinatol 1999; 19: 550-555
• 65 Senat MV, Deprest J, Boulvain M. et al. Endoscopic laser surgery versus serial amnioreduction for severe twin-to-twin transfusion syndrome. N Engl J Med 2004; 351: 136-144
• 66 Slaghekke F, Kist WJ, Oepkes D. et al. Twin anemia-polycythemia sequence: diagnostic criteria, classification, perinatal management and outcome. Fetal Diagn Ther 2010; 27: 181-190
• 67 Slaghekke F, Lewi L, Middeldorp JM. et al. Residual anastomoses in twin-twin transfusion syndrome after laser: the Solomon randomized trial. Am J Obstet Gynecol 2014; 211: 285.e1–e7
• 68 van Winden KR, Quintero RA, Kontopoulos EV. et al. Pre-operative twin anemia/polycythemia in the setting of twin-twin transfusion syndrome (TTTS). Fetal Diagn Ther 2015; 37: 274-280
• 69 Slaghekke F, Pasman S, Veujoz M. et al. Middle cerebral artery peak systolic velocity to predict fetal hemoglobin levels in twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol 2015; 46: 432-436
• 70 Tollenaar LSA, Lopriore E, Middeldorp JM. et al. Improved antenatal prediction of twin anemia-polycythemia sequence by delta middle cerebral artery peak systolic velocity: a new antenatal classification system. Ultrasound Obstet Gynecol 2019; 53: 788-793
• 71 Tavares de Sousa M, Fonseca A, Hecher K. Role of fetal intertwin difference in middle cerebral artery peak systolic velocity in predicting neonatal twin anemia-polycythemia sequence. Ultrasound Obstet Gynecol 2019; 53: 794-797
• 72 Lewi L, Valencia C, Gonzales E. et al. The outcome of twin reversed arterial perfusion sequence diagnosed in the first trimester. Am J Obstet Gynecol 2010; 203: 213.e1–4
• 73 von Kaisenberg CS, Klaritsch P, Ochsenbein-Kölble N. et al. AWMF LL 015-087 S24. Überwachung und Betreuung von Zwillingsschwangerschaften.
• 74 Gratacos E, Lewi L, Munoz B. et al. A classification system for selective intrauterine growth restriction in monochorionic pregnancies according to umbilical artery Doppler flow in the smaller twin. Ultrasound Obstet Gynecol 2007; 30: 28-34
• 75 Mackie FL, Rigby A, Morris RK. et al. Prognosis of the co-twin following spontaneous single intrauterine fetal death in twin pregnancies: a systematic review and meta-analysis. BJOG 2019; 126: 569-578