CC BY 4.0 · Rev Bras Ginecol Obstet 2022; 44(05): 519-531
DOI: 10.1055/s-0042-1743097
Review

Doppler Ultrasound of the Umbilical Artery: Clinical Application

Ultrassonografia Doppler da artéria umbilical: Aplicação clínica
1   Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal
,
2   Departamento da Mulher e da Medicina Reprodutiva, Centro Materno Infantil do Norte, Centro Hospitalar Universitário do Porto EPE, Porto, Portugal
,
2   Departamento da Mulher e da Medicina Reprodutiva, Centro Materno Infantil do Norte, Centro Hospitalar Universitário do Porto EPE, Porto, Portugal
,
1   Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Porto, Portugal
2   Departamento da Mulher e da Medicina Reprodutiva, Centro Materno Infantil do Norte, Centro Hospitalar Universitário do Porto EPE, Porto, Portugal
3   Departamento da Mulher e da Medicina Reprodutiva, Centro Materno Infantil do Norte, Unidade de Investigação e Formação, Porto, Portugal
4   Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
› Institutsangaben

Abstract

Objective To provide a survey of relevant literature on umbilical artery Doppler ultrasound use in clinical practice, technical considerations and limitations, and future perspectives.

Methods Literature searches were conducted in PubMed and Medline, restricted to articles written in English. Additionally, the references of all analyzed studies were searched to obtain necessary information.

Results The use of this technique as a routine surveillance method is only recommended for high-risk pregnancies with impaired placentation. Meta-analyses of randomized trials have established that obstetric management guided by umbilical artery Doppler findings can improve perinatal mortality and morbidity. The values of the indices of Umbilical artery Doppler decrease with advancing gestational age; however, a lack of consensus on reference ranges prevails.

Conclusion Important clinical decisions are based on the information obtained with umbilical artery Doppler ultrasound. Future efforts in research are imperative to overcome the current limitations of the technique.

Resumo

Objetivo Compilar informação relevante proveniente da literatura atual sobre a ultrassonografia Doppler das artérias umbilicais (AUs) na prática clínica, considerações e limitações técnicas e perspectivas futuras.

Métodos A pesquisa bibliográfica foi realizada nos bancos de dados PubMed e Medline e restringiu-se a artigos escritos na língua inglesa. Recorreu-se também à bibliografia dos artigos selecionados, quando necessário, para obter informação relevante.

Resultados A utilização desta técnica como método de vigilância de rotina está apenas recomendada em gravidezes de alto risco com disfunção placentar. Metanálises de estudos randomizados mostraram que o seguimento obstétrico baseado nos achados do Doppler da artéria umbilical pode melhorar a mortalidade e a morbilidade perinatal. É consensual que os valores dos índices Doppler da AU decrescem com o avanço da idade gestacional. No entanto, há ainda muita incerteza quanto aos valores de referência.

Conclusão As informações obtidas através da AU Doppler US são a base para muitas decisões clínicas importantes. Trabalhos de investigação nesta área são essenciais para tentar colmatar atuais limitações da técnica.

Conclusion

The UA Doppler US is an invaluable screening tool for high-risk pregnancies and on which important clinical decisions depend. Future investments in research are imperative to attempt to overcome the current limitations of the technique.




Publikationsverlauf

Eingereicht: 05. Juli 2021

Angenommen: 18. November 2021

Artikel online veröffentlicht:
11. April 2022

© 2022. Federação Brasileira de Ginecologia e Obstetrícia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Su EJ. Role of the fetoplacental endothelium in fetal growth restriction with abnormal umbilical artery Doppler velocimetry. Am J Obstet Gynecol 2015; 213 (4, Suppl) S123-S130 DOI: 10.1016/j.ajog.2015.06.038.
  • 2 Lorigo M, Mariana M, Feiteiro J, Cairrao E. How is the human umbilical artery regulated?. J Obstet Gynaecol Res 2018; 44 (07) 1193-1201 DOI: 10.1111/jog.13667.
  • 3 Salemme S, Rebolledo A, Speroni F, Petruccelli S, Milesi V. L, P-/Q- and T-type Ca2+ channels in smooth muscle cells from human umbilical artery. Cell Physiol Biochem 2007; 20 (1-4): 55-64 DOI: 10.1159/000104153.
  • 4 Milesi V, Raingo J, Rebolledo A, Grassi de Gende AO. Potassium channels in human umbilical artery cells. J Soc Gynecol Investig 2003; 10 (06) 339-346 DOI: 10.1016/s1071-5576(03)00117-5.
  • 5 Reilly FD, Russell PT. Neurohistochemical evidence supporting an absence of adrenergic and cholinergic innervation in the human placenta and umbilical cord. Anat Rec 1977; 188 (03) 277-286 DOI: 10.1002/ar.1091880302.
  • 6 Fox SB, Khong TY. Lack of innervation of human umbilical cord. An immunohistological and histochemical study. Placenta 1990; 11 (01) 59-62 DOI: 10.1016/s0143-4004(05)80443-6.
  • 7 Poston L, McCarthy AL, Ritter JM. Control of vascular resistance in the maternal and feto-placental arterial beds. Pharmacol Ther 1995; 65 (02) 215-239 DOI: 10.1016/0163-7258(94)00064-a.
  • 8 Krzyżanowski A, Kwiatek M, Gęca T, Stupak A, Kwaśniewska A. Modern ultrasonography of the umbilical cord: prenatal diagnosis of umbilical cord abnormalities and assessement of fetal wellbeing. Med Sci Monit 2019; 25: 3170-3180 DOI: 10.12659/MSM.913762.
  • 9 Sankaran S, Kyle PM. Aetiology and pathogenesis of IUGR. Best Pract Res Clin Obstet Gynaecol 2009; 23 (06) 765-777 DOI: 10.1016/j.bpobgyn.2009.05.003.
  • 10 Mureșan D, Rotar IC, Stamatian F. The usefulness of fetal Doppler evaluation in early versus late onset intrauterine growth restriction. Review of the literature. Med Ultrason 2016; 18 (01) 103-109 DOI: 10.11152/mu.2013.2066.181.dop.
  • 11 Alfirevic Z, Stampalija T, Medley N. Fetal and umbilical Doppler ultrasound in normal pregnancy. Cochrane Database Syst Rev 2015; (04) CD001450 DOI: 10.1002/14651858.CD001450.pub4.
  • 12 Sun J, Wang L, Li Y. Clinical value of color doppler ultrasound in prenatal diagnosis of umbilical cord entry abnormity. Pak J Med Sci 2016; 32 (06) 1414-1418 DOI: 10.12669/pjms.325.10518.
  • 13 Tanis JC, Boelen MR, Schmitz DM, Casarella L, van der Laan ME, Bos AF. et al. Correlation between Doppler flow patterns in growth-restricted fetuses and neonatal circulation. Ultrasound Obstet Gynecol 2016; 48 (02) 210-216 DOI: 10.1002/uog.15744.
  • 14 Baschat AA. Neurodevelopment after fetal growth restriction. Fetal Diagn Ther 2014; 36 (02) 136-142 DOI: 10.1159/000353631.
  • 15 Figueira CO, Surita FG, Dertkigil MS, Pereira SL, Bennini Jr. JR, Morais SS. et al. Fetal Hemodynamic parameters in low risk pregnancies: Doppler velocimetry of uterine, umbilical, and middle cerebral artery. ScientificWorldJournal 2016; 2016: 1693704 DOI: 10.1155/2016/1693704.
  • 16 Richardson BS, Bocking AD. Metabolic and circulatory adaptations to chronic hypoxia in the fetus. Comp Biochem Physiol A Mol Integr Physiol 1998; 119 (03) 717-723 DOI: 10.1016/s1095-6433(98)01010-1.
  • 17 Frusca T, Todros T, Lees C, Bilardo CM. 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. Am J Obstet Gynecol 2018; 218 (2S, 2s): S783-S789 DOI: 10.1016/j.ajog.2017.12.226.
  • 18 Vollgraff Heidweiller-Schreurs CA, De Boer MA, Heymans MW, Schoondmade LJ, Bossuyt PMM, Mol BWJ. et al. Prognostic accuracy of cerebroplacental ratio and middle cerebral artery Doppler for adverse perinatal outcome: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2018; 51 (03) 313-322 DOI: 10.1002/uog.18809.
  • 19 Bakalis S, Akolekar R, Gallo DM, Poon LC, Nicolaides KH. Umbilical and fetal middle cerebral artery Doppler at 30-34 weeks' gestation in the prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol 2015; 45 (04) 409-420 DOI: 10.1002/uog.14822.
  • 20 Alfirevic Z, Stampalija T, Dowswell T. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev 2017; 6 (06) CD007529 DOI: 10.1002/14651858.CD007529.pub4.
  • 21 American College of Obstetricians and Gynecologists' Committee on Practice Bulletins—Obstetrics and the Society forMaternal-FetalMedicin. ACOG Practice Bulletin No. 204: fetal growth restriction. Obstet Gynecol 2019; 133 (02) e97-e109 DOI: 10.1097/AOG.0000000000003070.
  • 22 Berkley E, Chauhan SP, Abuhamad A. Society for Maternal-Fetal Medicine Publications Committee. Doppler assessment of the fetus with intrauterine growth restriction. Am J Obstet Gynecol 2012; 206 (04) 300-308 DOI: 10.1016/j.ajog.2012.01.022.
  • 23 Oglat AA, Matjafri MZ, Suardi N, Oqlat MA, Abdelrahman MA, Oqlat AA. A review of medical Doppler ultrasonography of blood flow in general and especially in common carotid artery. J Med Ultrasound 2018; 26 (01) 3-13 DOI: 10.4103/JMU.JMU_11_17.
  • 24 Moorthy RS. Doppler ultrasound. Med J Armed Forces India 2002; 58 (01) 1-2 DOI: 10.1016/S0377-1237(02)80001-6.
  • 25 Wood MM, Romine LE, Lee YK, Richman KM, O'Boyle M, Paz DA. et al. Spectral Doppler signature waveforms in ultrasonography: a review of normal and abnormal waveforms. Ultrasound Q 2010; 26 (02) 83-99 DOI: 10.1097/RUQ.0b013e3181dcbf67.
  • 26 Widnes C, Flo K, Wilsgaard T, Kiserud T, Acharya G. Sex differences in umbilical artery Doppler indices: a longitudinal study. Biol Sex Differ 2018; 9 (01) 16 DOI: 10.1186/s13293-018-0174-x.
  • 27 Nelson TR, Pretorius DH. The Doppler signal: where does it come from and what does it mean?. AJR Am J Roentgenol 1988; 151 (03) 439-447 DOI: 10.2214/ajr.151.3.439.
  • 28 Mone F, McConnell B, Thompson A, Segurado R, Hepper P, Stewart MC. et al. Fetal umbilical artery Doppler pulsatility index and childhood neurocognitive outcome at 12 years. BMJ Open 2016; 6 (06) e008916 DOI: 10.1136/bmjopen-2015-008916.
  • 29 Trudinger BJ, Stevens D, Connelly A, Hales JR, Alexander G, Bradley L. et al. Umbilical artery flow velocity waveforms and placental resistance: the effects of embolization of the umbilical circulation. Am J Obstet Gynecol 1987; 157 (06) 1443-1448 DOI: 10.1016/s0002-9378(87)80241-7.
  • 30 Giles WB, Trudinger BJ, Baird PJ. Fetal umbilical artery flow velocity waveforms and placental resistance: pathological correlation. Br J Obstet Gynaecol 1985; 92 (01) 31-38 DOI: 10.1111/j.1471-0528.1985.tb01045.x.
  • 31 Oros D, Ruiz-Martinez S, Staines-Urias E, Conde-Aguiedo A, Villar J, Fabre 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 (04) 454-464 DOI: 10.1002/uog.20102.
  • 32 Hecher K, Campbell S. Characteristics of fetal venous blood flow under normal circumstances and during fetal disease. Ultrasound Obstet Gynecol 1996; 7 (01) 68-83 DOI: 10.1046/j.1469-0705.1996.07010068.x.
  • 33 Najafzadeh A, Dickinson JE. Umbilical venous blood flow and its measurement in the human fetus. J Clin Ultrasound 2012; 40 (08) 502-511 DOI: 10.1002/jcu.21970.
  • 34 Bhide A, Acharya G, Bilardo CM, Brezinka C, Cafici D, Hernandez-Andrade E. et al. ISUOG practice guidelines: use of Doppler ultrasonography in obstetrics. Ultrasound Obstet Gynecol 2013; 41 (02) 233-239 DOI: 10.1002/uog.12371.
  • 35 Bahlmann F, Fittschen M, Reinhard I, Wellek S, Puhl A. Blood flow velocity waveforms of the umbilical artery in a normal population: reference values from 18 weeks to 42 weeks of gestation. Ultraschall Med 2012; 33 (07) E80-E87 DOI: 10.1055/s-0031-1299294.
  • 36 Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins L. Fetal umbilical artery flow velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol 1985; 92 (01) 23-30 DOI: 10.1111/j.1471-0528.1985.tb01044.x.
  • 37 Todros T, Piccoli E, Rolfo A, Cardaropoli S, Guiot C, Gaglioti P. et al. Review: Feto-placental vascularization: a multifaceted approach. Placenta 2011; 32 (Suppl. 02) S165-S169 DOI: 10.1016/j.placenta.2010.12.020.
  • 38 Lees C, Marlow N, Arabin B, Bilardo CM, Brezinka C, Derks JB. et al; TRUFFLE Group. Perinatal morbidity and mortality in early-onset fetal growth restriction: cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE). Ultrasound Obstet Gynecol 2013; 42 (04) 400-408 DOI: 10.1002/uog.13190.
  • 39 Caradeux J, Martinez-Portilla RJ, Basuki TR, Kiserud T, Figueras F. Risk of fetal death in growth-restricted fetuses with umbilical and/or ductus venosus absent or reversed end-diastolic velocities before 34 weeks of gestation: a systematic review and meta-analysis. Am J Obstet Gynecol 2018; 218 (2S): S774-82.e21, 782.e21 DOI: 10.1016/j.ajog.2017.11.566.
  • 40 Kalache KD, Dückelmann AM. Doppler in obstetrics: beyond the umbilical artery. Clin Obstet Gynecol 2012; 55 (01) 288-295 DOI: 10.1097/GRF.0b013e3182488156.
  • 41 Giles WB, Lingman G, Marsál K, Trudinger BJ. Fetal volume blood flow and umbilical artery flow velocity waveform analysis: a comparison. Br J Obstet Gynaecol 1986; 93 (05) 461-465
  • 42 Marsál K. Rational use of Doppler ultrasound in perinatal medicine. J Perinat Med 1994; 22 (06) 463-474
  • 43 Thompson RS, Trudinger BJ. Doppler waveform pulsatility index and resistance, pressure and flow in the umbilical placental circulation: an investigation using a mathematical model. Ultrasound Med Biol 1990; 16 (05) 449-458 DOI: 10.1016/0301-5629(90)90167-b.
  • 44 Fisk NM, MacLachlan N, Ellis C, Tannirandorn Y, Tonge HM, Rodeck CH. Absent end-diastolic flow in first trimester umbilical artery. Lancet 1988; 2 (8622): 1256-1257 DOI: 10.1016/s0140-6736(88)90854-9.
  • 45 Borrell A, Martinez JM, Farre MT, Azulay M, Cararach V, Fortuny A. Reversed end-diastolic flow in first-trimester umbilical artery: an ominous new sign for fetal outcome. Am J Obstet Gynecol 2001; 185 (01) 204-207 DOI: 10.1067/mob.2001.114872.
  • 46 Borrell A, Costa D, Martinez JM, Farré MT, Palacio M, Mortera C, Fortuny A. et al. Reversed end-diastolic umbilical flow in a first-trimester fetus with congenital heart disease. Prenat Diagn 1998; 18 (10) 1001-1005 DOI: 10.1002/(sici)1097-0223(1998100)18:10<1001:aid-pd395>3.0.co;2-v.
  • 47 Martinez Crespo JM, Comas C, Borrell A, Puerto B, Antolin E, Ojuel J. et al. Reversed end-diastolic umbilical artery velocity in two cases of trisomy 18 at 10 weeks' gestation. Ultrasound Obstet Gynecol 1996; 7 (06) 447-449 DOI: 10.1046/j.1469-0705.1996.07060447.x.
  • 48 Murta CG, Moron AF, Avila MA. Reversed diastolic umbilical artery flow in the first trimester associated with chromosomal fetal abnormalities or cardiac defects. Obstet Gynecol 2000; 95 (6 Pt 2): 1011-1013 DOI: 10.1016/s0029-7844(99)00603-1.
  • 49 Comas C, Carrera M, Devesa R, Muñoz A, Torrents M, Ribas I. et al. Early detection of reversed diastolic umbilical flow: should we offer karyotyping?. Ultrasound Obstet Gynecol 1997; 10 (06) 400-402 DOI: 10.1046/j.1469-0705.1997.10060400.x.
  • 50 Bellver J, Lara C, Rossal LP, Remohí J, Pellicer A, Serra V. First-trimester reversed end-diastolic flow in the umbilical artery is not always an ominous sign. Ultrasound Obstet Gynecol 2003; 22 (06) 652-655 DOI: 10.1002/uog.922.
  • 51 Simonazzi G, Curti A, Cattani L, Rizzo N, Pilu G. Outcome of severe placental insufficiency with abnormal umbilical artery Doppler prior to fetal viability. BJOG 2013; 120 (06) 754-757 DOI: 10.1111/1471-0528.12133.
  • 52 Piazze J, Dillon KC, Cerekja A. Betamethasone effects on umbilical arteries and ductus venosus Doppler velocity waveforms in growth-restricted fetuses. J Matern Fetal Neonatal Med 2012; 25 (07) 1179-1182 DOI: 10.3109/14767058.2011.624216.
  • 53 Nordenvall M, Ullberg U, Laurin J, Lingman G, Sandstedt B, Ulmsten U. Placental morphology in relation to umbilical artery blood velocity waveforms. Eur J Obstet Gynecol Reprod Biol 1991; 40 (03) 179-190 DOI: 10.1016/0028-2243(91)90115-2.
  • 54 Su EJ, Ernst L, Abdallah N, Chatterton R, Xin H, Monsivais D. et al. Estrogen receptor-β and fetoplacental endothelial prostanoid biosynthesis: a link to clinically demonstrated fetal growth restriction. J Clin Endocrinol Metab 2011; 96 (10) E1558-E1567 DOI: 10.1210/jc.2011-1084.
  • 55 Su EJ, Lin ZH, Zeine R, Yin P, Reierstad. Innes JE. et al. Estrogen receptor-beta mediates cyclooxygenase-2 expression and vascular prostanoid levels in human placental villous endothelial cells. Am J Obstet Gynecol 2009; 200 (04) 427.e1-427.e8 DOI: 10.1016/j.ajog.2009.01.025.
  • 56 Gupta S, Chauhan M, Sen J, Nanda S. Effect of transdermal nitroglycerine on Doppler velocity waveforms of the uterine, umbilical and fetal middle cerebral arteries in patients with chronic placental insufficiency: a prospective RCT. J Clin Diagn Res 2017; 11 (07) QC13-QC17 DOI: 10.7860/JCDR/2017/21438.10282.
  • 57 Mishra M, Sawhney R, Kumar A, Bapna KR, Kohli V, Wasir H. et al. Cardiac surgery during pregnancy: continuous fetal monitoring using umbilical artery Doppler flow velocity indices. Ann Card Anaesth 2014; 17 (01) 46-51 DOI: 10.4103/0971-9784.124141.
  • 58 Yildirim G, Turhan E, Aslan H, Gungorduk K, Guven H, Idem O. et al. Perinatal and neonatal outcomes of growth restricted fetuses with positive end diastolic and absent or reversed umbilical artery doppler waveforms. Saudi Med J 2008; 29 (03) 403-408
  • 59 Karsdorp VH, van Vugt JM, van Geijn HP, Kostene PJ, Arduini D, Montenegro N. et al. Clinical significance of absent or reversed end diastolic velocity waveforms in umbilical artery. Lancet 1994; 344 (8938): 1664-1668 DOI: 10.1016/s0140-6736(94)90457-x.
  • 60 Al Hamayel NA, Baghlaf H, Blakemore K, Crino JP, Burd I. Significance of abnormal umbilical artery Doppler studies in normally grown fetuses. Matern Health Neonatol Perinatol 2020; 6: 1 DOI: 10.1186/s40748-020-0115-7.
  • 61 Tolu LB, Ararso R, Abdulkadir A, Feyissa GT, Worku Y. Perinatal outcome of growth restricted fetuses with abnormal umbilical artery Doppler waveforms compared to growth restricted fetuses with normal umbilical artery Doppler waveforms at a tertiary referral hospital in urban Ethiopia. PLoS One 2020; 15 (06) e0234810 DOI: 10.1371/journal.pone.0234810.
  • 62 Byun YJ, Kim HS, Yang JI, Kim JH, Kim HY, Chang SJ. Umbilical artery Doppler study as a predictive marker of perinatal outcome in preterm small for gestational age infants. Yonsei Med J 2009; 50 (01) 39-44 DOI: 10.3349/ymj.2009.50.1.39.
  • 63 Valcamonico A, Danti L, Frusca T, Soregaroli M, Zucca S, Abrami F. et al. Absent end-diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage. Am J Obstet Gynecol 1994; 170 (03) 796-801 DOI: 10.1016/s0002-9378(94)70285-3.
  • 64 Valcamonico A, Accorsi P, Battaglia S, Soregaroli M, Beretta D, Frusca T. Absent or reverse end-diastolic flow in the umbilical artery: intellectual development at school age. Eur J Obstet Gynecol Reprod Biol 2004; 114 (01) 23-28 DOI: 10.1016/j.ejogrb.2003.09.033.
  • 65 Brütsch S, Burkhardt T, Kurmanavicius J, Bassler D, Zimmermann R, Natalucci G. et al. Neurodevelopmental outcome in very low birthweight infants with pathological umbilical artery flow. Arch Dis Child Fetal Neonatal Ed 2016; 101 (03) F212-F216 DOI: 10.1136/archdischild-2014-307820.
  • 66 Corry E, Mone F, Segurado R, Downey P, McParland P, McAuliffe FM. et al. Placental disease and abnormal umbilical artery Doppler waveforms in trisomy 21 pregnancy: A case-control study. Placenta 2016; 47: 24-28 DOI: 10.1016/j.placenta.2016.09.001.
  • 67 Melamed N, Baschat A, Yinon Y, Athanasiadis A, Mecacci F, Figueras F. et al. FIGO (international Federation of Gynecology and obstetrics) initiative on fetal growth: best practice advice for screening, diagnosis, and management of fetal growth restriction. Int J Gynaecol Obstet 2021; 152 (Suppl. 01) 3-57 DOI: 10.1002/ijgo.13522.
  • 68 Tejada-Martínez AE, Borberg CJ, Venugopal R, Carballo C, Moreno WA, Quintero RA. Computational fluid dynamic analysis of flow velocity waveform notching in umbilical arteries. Am J Physiol Regul Integr Comp Physiol 2011; 300 (01) R76-R84 DOI: 10.1152/ajpregu.00864.2009.
  • 69 Struijk PC, Fernando KL, Mathews VJ, Steegers EAP, Wladimiroff JW, Clark EB. et al. Application of the magnitude-squared coherence function between uterine and umbilical flow velocity waveforms for predicting placental dysfunction: a preliminary study. Ultrasound Med Biol 2007; 33 (07) 1057-1063 DOI: 10.1016/j.ultrasmedbio.2007.01.012.
  • 70 Dias T, Abeykoon S, Mendis P, Gunawardena C, Pragasan G, Padeniya T. et al. Fetal Doppler reference values in women with a normal body mass index. Ceylon Med J 2019; 64 (02) 59-65 DOI: 10.4038/cmj.v64i2.8888.
  • 71 Ciobanu A, Wright A, Syngelaki A, Wright D, Akolekar R, Nicolaides KH. Fetal Medicine Foundation reference ranges for umbilical artery and middle cerebral artery pulsatility index and cerebroplacental ratio. Ultrasound Obstet Gynecol 2019; 53 (04) 465-472 DOI: 10.1002/uog.20157.
  • 72 Drukker L, Staines-Urias E, Villar J, Barros FC, Carvalho M, Munim S. et al. International gestational age-specific centiles for umbilical artery Doppler indices: a longitudinal prospective cohort study of the INTERGROWTH-21st Project. Am J Obstet Gynecol 2020; 222 (06) 602.e1-602.e15 DOI: 10.1016/j.ajog.2020.01.012.
  • 73 Acharya G, Wilsgaard T, Berntsen GK, Maltau JM, Kiserud T. Reference ranges for serial measurements of umbilical artery Doppler indices in the second half of pregnancy. Am J Obstet Gynecol 2005; 192 (03) 937-944 DOI: 10.1016/j.ajog.2004.09.019.
  • 74 Ayoola OO, Bulus P, Loto OM, Idowu BM. Normogram of umbilical artery Doppler indices in singleton pregnancies in south-western Nigerian women. J Obstet Gynaecol Res 2016; 42 (12) 1694-1698 DOI: 10.1111/jog.13114.
  • 75 Srikumar S, Debnath J, Ravikumar R, Bandhu HC, Maurya VK. Doppler indices of the umbilical and fetal middle cerebral artery at 18-40 weeks of normal gestation: A pilot study. Med J Armed Forces India 2017; 73 (03) 232-241 DOI: 10.1016/j.mjafi.2016.12.008.
  • 76 Baschat AA, Gembruch U. The cerebroplacental Doppler ratio revisited. Ultrasound Obstet Gynecol 2003; 21 (02) 124-127 DOI: 10.1002/uog.20.
  • 77 Contro E, Cataneo I, Morano D, Farina A. Reference charts for umbilical Doppler pulsatility index in fetuses with isolated two-vessel cord. Arch Gynecol Obstet 2019; 299 (04) 947-951 DOI: 10.1007/s00404-019-05086-z.
  • 78 Mulcahy C, McAuliffe FM, Breathnach F, Geary M, Daly S, Higgins J. et al. Umbilical and fetal middle cerebral artery Doppler reference ranges in a twin population followed longitudinally from 24 to 38 weeks' gestation. Ultrasound Obstet Gynecol 2014; 44 (04) 461-467 DOI: 10.1002/uog.13302.
  • 79 Casati D, Pellegrino M, Cortinovis I, Spada E, Lanna M, Faiola S. et al. Longitudinal Doppler references for monochorionic twins and comparison with singletons. PLoS One 2019; 14 (12) e0226090 DOI: 10.1371/journal.pone.0226090.
  • 80 Haugen G, Bollerslev J, Henriksen T. Human umbilical and fetal cerebral blood flow velocity waveforms following maternal glucose loading: a cross-sectional observational study. Acta Obstet Gynecol Scand 2016; 95 (06) 683-689 DOI: 10.1111/aogs.12913.
  • 81 Mulders LG, Muijsers GJ, Jongsma HW, Nijhuis JG, Hein PR. The umbilical artery blood flow velocity waveform in relation to fetal breathing movements, fetal heart rate and fetal behavioural states in normal pregnancy at 37 to 39 weeks. Early Hum Dev 1986; 14 (3-4): 283-293 DOI: 10.1016/0378-3782(86)90191-x.
  • 82 Soneji S, Beltrán-Sánchez H. Association of maternal cigarette smoking and smoking cessation with preterm birth. JAMA Netw Open 2019; 2 (04) e192514 DOI: 10.1001/jamanetworkopen.2019.2514.
  • 83 Tikkanen M, Nuutila M, Hiilesmaa V, Paavonen J, Ylikorkala O. Prepregnancy risk factors for placental abruption. Acta Obstet Gynecol Scand 2006; 85 (01) 40-44 DOI: 10.1080/00016340500324241.
  • 84 Reeves S, Bernstein I. Effects of maternal tobacco-smoke exposure on fetal growth and neonatal size. Expert Rev Obstet Gynecol 2008; 3 (06) 719-730 DOI: 10.1586/17474108.3.6.719.
  • 85 Stalzer A, Seybold D, Hossino D, Broce M, Calhoun B. Doppler screening and predictors of adverse outcomes in high risk pregnancies affected by tobacco. Reprod Toxicol 2017; 67: 10-14 DOI: 10.1016/j.reprotox.2016.11.006.
  • 86 Janeczek S, Karlman R, MacMillan W. Left versus right intra-abdominal umbilical arteries: comparison of their Doppler waveforms. J Ultrasound Med 2012; 31 (05) 679-683 DOI: 10.7863/jum.2012.31.5.67.
  • 87 Ruiz-Martinez S, Papageorghiou AT, Staines-Urias E, Villar J, Gonzalez de Agüero R, Oros D. Clinical impact of Doppler reference charts to manage fetal growth restriction: need for standardization. Ultrasound Obstet Gynecol 2020; 56 (02) 166-172 DOI: 10.1002/uog.20380.
  • 88 ACOG Practice bulletin no. 134: fetal growth restriction. Obstet Gynecol 2013; 121 (05) 1122-1133 DOI: 10.1097/01.AOG.0000429658.85846.f9.
  • 89 Bolz N, Kalache KD, Proquitte H, Slowinski T, Hartung JP, Henrich W. et al. Value of Doppler sonography near term: can umbilical and uterine artery indices in low-risk pregnancies predict perinatal outcome?. J Perinat Med 2013; 41 (02) 165-170 DOI: 10.1515/jpm-2012-0042.
  • 90 Doppler French Study Group. A randomised controlled trial of Doppler ultrasound velocimetry of the umbilical artery in low risk pregnancies. Br J Obstet Gynaecol 1997; 104 (04) 419-424 DOI: 10.1111/j.1471-0528.1997.tb11492.x.
  • 91 Goffinet F, Paris-Llado J, Nisand I, Bréart G. Umbilical artery Doppler velocimetry in unselected and low risk pregnancies: a review of randomised controlled trials. Br J Obstet Gynaecol 1997; 104 (04) 425-430 DOI: 10.1111/j.1471-0528.1997.tb11493.x.
  • 92 Nkosi S, Makin J, Hlongwane T, Pattinson RC. Screening and managing a low-risk pregnant population using continuous-wave Doppler ultrasound in a low-income population: A cohort analytical study. S Afr Med J 2019; 109 (05) 347-352 DOI: 10.7196/SAMJ.2019.v109i5.13611.
  • 93 Hugo EJ, Odendaal HJ, Grove D. Evaluation of the use of umbilical artery Doppler flow studies and outcome of pregnancies at a secondary hospital. J Matern Fetal Neonatal Med 2007; 20 (03) 233-239 DOI: 10.1080/14767050601134926.
  • 94 Gudmundsson S, Flo K, Ghosh G, Wilsgaard T, Acharya G. Placental pulsatility index: a new, more sensitive parameter for predicting adverse outcome in pregnancies suspected of fetal growth restriction. Acta Obstet Gynecol Scand 2017; 96 (02) 216-222 DOI: 10.1111/aogs.13060.
  • 95 FitzGerald DE, Drumm JE. Non-invasive measurement of human fetal circulation using ultrasound: a new method. BMJ 1977; 2 (6100): 1450-1451 DOI: 10.1136/bmj.2.6100.1450.
  • 96 Morris RK, Malin G, Robson SC, Kleijnen J, Zamora J, Khan KS. Fetal umbilical artery Doppler to predict compromise of fetal/neonatal wellbeing in a high-risk population: systematic review and bivariate meta-analysis. Ultrasound Obstet Gynecol 2011; 37 (02) 135-142 DOI: 10.1002/uog.7767.
  • 97 Vayssière C, Benoist G, Blondel B, Deruelle P, Favre R, Gallot D. et al; French College of Gynaecologists and Obstetricians. Twin pregnancies: guidelines for clinical practice from the French College of Gynaecologists and Obstetricians (CNGOF). Eur J Obstet Gynecol Reprod Biol 2011; 156 (01) 12-17 DOI: 10.1016/j.ejogrb.2010.12.045.
  • 98 Graves CR. Antepartum fetal surveillance and timing of delivery in the pregnancy complicated by diabetes mellitus. Clin Obstet Gynecol 2007; 50 (04) 1007-1013 DOI: 10.1097/GRF.0b013e31815a63cc.
  • 99 de Rochambeau B, Jabbour N, Mellier G. [Umbilical Doppler velocimetry in prolonged pregnancies]. Rev Fr Gynécol Obstet 1992; 87 (05) 289-294 French.
  • 100 Adekanmi AJ, Roberts A, Akinmoladun JA, Adeyinka AO. Uterine and umbilical artery doppler in women with pre-eclampsia and their pregnancy outcomes. Niger Postgrad Med J 2019; 26 (02) 106-112 DOI: 10.4103/npmj.npmj_161_18.
  • 101 Velauthar L, Plana MN, Kalidindi M, Zammora J, Thilaganathan B, Illanes SE. et al. First-trimester uterine artery Doppler and adverse pregnancy outcome: a meta-analysis involving 55,974 women. Ultrasound Obstet Gynecol 2014; 43 (05) 500-507 DOI: 10.1002/uog.13275.
  • 102 Shen G, Huang Y, Jiang L, Gu J, Wang Y, Hu B. Ultrasound prediction of abnormal infant development in hypertensive pregnant women in the second and third trimester. Sci Rep 2017; 7: 40429 DOI: 10.1038/srep40429.
  • 103 Gardosi J, Madurasinghe V, Williams M, Malik A, Francis A. Maternal and fetal risk factors for stillbirth: population based study. BMJ 2013; 346: f108 DOI: 10.1136/bmj.f108.
  • 104 Pilliod RA, Cheng YW, Snowden JM, Doss AE, Caughey AB. The risk of intrauterine fetal death in the small-for-gestational-age fetus. Am J Obstet Gynecol 2012; 207 (04) 318.e1-318.e6 DOI: 10.1016/j.ajog.2012.06.039.
  • 105 Figueras F, Gardosi J. Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 2011; 204 (04) 288-300 DOI: 10.1016/j.ajog.2010.08.055.
  • 106 Bardien N, Whitehead CL, Tong S, Ugoni A, McDonald S, Walker SP. Placental insufficiency in fetuses that slow in growth but are born appropriate for gestational age: a prospective longitudinal study. PLoS One 2016; 11 (01) e0142788 DOI: 10.1371/journal.pone.0142788.
  • 107 Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker N. et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol 2016; 48 (03) 333-339 DOI: 10.1002/uog.15884.
  • 108 Figueras F, Caradeux J, Crispi F, Eixarch E, Peguero A, Gratacos E. Diagnosis and surveillance of late-onset fetal growth restriction. Am J Obstet Gynecol 2018; 218 (2S, 2s): S790-, 802.e1 DOI: 10.1016/j.ajog.2017.12.003.
  • 109 Mifsud W, Sebire NJ. Placental pathology in early-onset and late-onset fetal growth restriction. Fetal Diagn Ther 2014; 36 (02) 117-128 DOI: 10.1159/000359969.
  • 110 Yinon Y, Kingdom JC, Odutayo A, Moineddin R, Drewlo S, Lai V. et al. Vascular dysfunction in women with a history of preeclampsia and intrauterine growth restriction: insights into future vascular risk. Circulation 2010; 122 (18) 1846-1853 DOI: 10.1161/CIRCULATIONAHA.110.948455.
  • 111 Turan OM, Turan S, Gungor S, Berg C, Moyano D, Gembruch U. et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008; 32 (02) 160-167 DOI: 10.1002/uog.5386.
  • 112 Baschat AA, Gembruch U, Harman CR. The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens. Ultrasound Obstet Gynecol 2001; 18 (06) 571-577 DOI: 10.1046/j.0960-7692.2001.00591.x.
  • 113 Hecher K, Bilardo CM, Stigter RH, Ville Y, Hackelöer BJ, Kok HJ. et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 2001; 18 (06) 564-570 DOI: 10.1046/j.0960-7692.2001.00590.x.
  • 114 Ferrazzi E, Bozzo M, Rigano S, Bellotti M, Morabito A, Pardi G. et al. Temporal sequence of abnormal Doppler changes in the peripheral and central circulatory systems of the severely growth-restricted fetus. Ultrasound Obstet Gynecol 2002; 19 (02) 140-146 DOI: 10.1046/j.0960-7692.2002.00627.x.
  • 115 Gardosi J, Kady SM, McGeown P, Francis A, Tonks A. Classification of stillbirth by relevant condition at death (ReCoDe): population based cohort study. BMJ 2005; 331 (7525): 1113-1117 DOI: 10.1136/bmj.38629.587639.7C.
  • 116 Geerts L, Van der Merwe E, Theron A, Rademan K. Placental insufficiency among high-risk pregnancies with a normal umbilical artery resistance index after 32weeks. Int J Gynaecol Obstet 2016; 135 (01) 38-42 DOI: 10.1016/j.ijgo.2016.03.038.
  • 117 Townsend R, Khalil A. Twin pregnancy complicated by selective growth restriction. Curr Opin Obstet Gynecol 2016; 28 (06) 485-491 DOI: 10.1097/GCO.0000000000000326.
  • 118 Gratacós E, Lewi L, Muñoz B, Acosta-Rojas R, Hernandez-Andrade E, Martinez JM. 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 (01) 28-34 DOI: 10.1002/uog.4046.
  • 119 Maulik D, Mundy D, Heitmann E, Maulik D. Evidence-based approach to umbilical artery Doppler fetal surveillance in high-risk pregnancies: an update. Clin Obstet Gynecol 2010; 53 (04) 869-878 DOI: 10.1097/GRF.0b013e3181fbb5f5.
  • 120 Morin L, Lim K. DIAGNOSTIC IMAGING COMMITTEE, SPECIAL CONTRIBUTOR, GENETICS COMMITTEE, MATERNAL FETAL MEDICINE COMMITTEE. Ultrasound in twin pregnancies. J Obstet Gynaecol Can 2011; 33 (06) 643-656 DOI: 10.1016/S1701-2163(16)34916-7.
  • 121 Niromanesh S, Shirazi M, Eftekhariyazdi M, Mortazavi F. Comparison of umbilical artery Doppler and non-stress test in assessment of fetal well-being in gestational diabetes mellitus: A prospective cohort study. Electron Physician 2017; 9 (12) 6087-6093 DOI: 10.19082/6087.
  • 122 Malhotra N, Chanana C, Kumar S, Roy K, Sharma JB. Comparison of perinatal outcome of growth-restricted fetuses with normal and abnormal umbilical artery Doppler waveforms. Indian J Med Sci 2006; 60 (08) 311-317 DOI: 10.4103/0019-5359.26607.
  • 123 Lees C. Perinatal and 2 year neurodevelopmental outcome in late preterm fetal compromise: the TRUFFLE 2 Randomised Trial [Study protocol] [Internet]. 2020 [cited 2021 Jan 12]. Available from: https://www.fundingawards.nihr.ac.uk/award/NIHR127976
  • 124 D'Antonio F, Patel D, Chandrasekharan N, Thilaganathan B, Bhide A. Role of cerebroplacental ratio for fetal assessment in prolonged pregnancy. Ultrasound Obstet Gynecol 2013; 42 (02) 196-200 DOI: 10.1002/uog.12357.