Uterine artery Doppler: Changing Concepts in Prediction and Prevention of PE and FGR

  • Selvaraj Ravi Lakshmy
  • Masilamani Praveenkumar
  • Umapathy Shobana
  • Ziyaulla Thasleem
Review Article
First Online:
Received:
Accepted:
  • 30 Downloads

Abstract

One of the most promising screening tools in detection of PE and FGR is uterine artery Doppler velocimetry. The underlying pathology for the development of PE is thought to be due to defective trophoblastic invasion of uterine spiral arteries. Increased impedance during mid-trimester is known to be associated with a high incidence of adverse pregnancy outcomes. High resistance in uterine arteries can be observed as early in the first trimester in cases with impaired placentation. The predictive efficacy of first trimester UtA Doppler has improved after the development of risk specific algorithm by including maternal characteristics, biophysical and biochemical parameters. With the understanding of late onset FGR and PE, it was realised that first trimester UtA Doppler may not serve as an efficient marker to identify this group which led to the evolution of its assessment in third trimester. The importance of UtA Doppler in third trimester is its ability to differentiate a physiologically small baby from a pathologically small fetus, which is growth restricted. PE and FGR remains an important cause of maternal and fetal mortality and its prediction is a challenging task which needs to be done early in gestation. Low dose aspirin when started before 16 weeks in the truly high risk population has proven to significantly reduce PE and FGR. To initiate aspirin therapy, the development of first trimester risk prediction model remains the key component. This paper is a review of the predictive efficacy of UtA Doppler in detecting uteroplacental insufficiency in each of the three trimesters.

Keywords

Screening Preeclampsia FGR Uterine artery Doppler Pulsatility index Sensitivity 

Abbreviations

PE

Pre-eclampsia

FGR

Fetal growth restriction

UtA

Uterine artery

PAPP-A

Pregnancy associated placental protein A

MAP

Mean arterial pressure

SGA

Small for gestational age

AGA

Appropriate for gestational age

EFW

Expected fetal weight

FPR

False positive rate

RI

Resistance index

PI

Pulsatility index

FMF

Fetal medicine foundation

MCA

Middle cerebral artery

CPR

Cerebroplacental ratio

PLGF

Placental growth factors

CLASP

Collaborative low-dose aspirin study in pregnancy

ASPRE

Aspirin for evidence-based preeclampsia prevention

NICE

National Institute for Health and Care Excellence

WHO

World Health Organisation

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References

  1. 1.
    Campbell S, Griffin DR, Pearce JM, Diaz-Recasens J, Cohen-Overbeek TE, Willson K, Teague MJ. New Doppler technique for assessing uteroplacental blood flow. Lancet. 1983;321(8326):675–7.CrossRefGoogle Scholar
  2. 2.
    Pearce JM, Campbell S, Cohen-Overbeek T, Hackett G, Hernandez J, Royston JP. References ranges and sources of variation for indices of pulsed Doppler flow velocity waveforms from the uteroplacental and fetal circulation. BJOG Int J Obstet Gynaecol. 1988;95(3):248–56.CrossRefGoogle Scholar
  3. 3.
    Papageorghiou AT, Yu CK, Cicero S, Bower S, Nicolaides KH. Second-trimester uterine artery Doppler screening in unselected populations: a review. J Matern Fetal Neonatal Med. 2002;12(2):78–88.PubMedCrossRefGoogle Scholar
  4. 4.
    Asnafi N, Hajian K. Mid-trimester uterine artery Doppler ultrasound as a predictor of adverse obstetric outcome in high-risk pregnancy. Taiwan J Obstet Gynecol. 2011;50(1):29–32.PubMedCrossRefGoogle Scholar
  5. 5.
    Bower S, Schuchter K, Campbell S. Doppler ultrasound screening as part of routine antenatal scanning: prediction of pre-eclampsia and intrauterine growth retardation. BJOG Int J Obstet Gynaecol. 1993;100(11):989–94.CrossRefGoogle Scholar
  6. 6.
    Bewley S, Cooper D, Campbell S. Doppler investigation of uteroplacental blood flow resistance in the second trimester: a screening study for pre-eclampsia and intrauterine growth retardation. BJOG Int J Obstet Gynaecol. 1991;98(9):871–9.CrossRefGoogle Scholar
  7. 7.
    Irion O, Massé J, Forest JC, Moutquin JM. Prediction of pre-eclampsia, low birthweight for gestation and prematurity by uterine artery blood flow velocity waveforms analysis in low risk nulliparous women. BJOG Int J Obstet Gynaecol. 1998;105(4):422–9.CrossRefGoogle Scholar
  8. 8.
    Casmod Y, Van Dyk B, Nicolaou E. Uterine artery Doppler screening as a predictor of pre-eclampsia. Health SA Gesondheid. 2016;21:391–6.CrossRefGoogle Scholar
  9. 9.
    Harrington K, Goldfrad C, Carpenter RG, Campbell S. Transvaginal uterine and umbilical artery Doppler examination of 12–16 weeks and the subsequent development of pre-eclampsia and intrauterine growth retardation. Ultrasound Obstet Gynecol. 1997;9(2):94–100.PubMedCrossRefGoogle Scholar
  10. 10.
    Detti L, Johnson SC, Diamond MP, Puscheck EE. First-trimester Doppler investigation of the uterine circulation. Am J Obstet Gynecol. 2006;195(5):1210–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Poon LC, Akolekar R, Lachmann R, Beta J, Nicolaides KH. Hypertensive disorders in pregnancy: screening by biophysical and biochemical markers at 11–13 weeks. Ultrasound Obstet Gynecol. 2010;35(6):662–70.PubMedGoogle Scholar
  12. 12.
    Gomez O, Martinez JM, Figueras F, Del Rio M, Borobio V, Puerto B, et al. Uterine artery Doppler at 11–14 weeks of gestation to screen for hypertensive disorders and associated complications in an unselected population. Ultrasound Obstet Gynecol. 2005;26(5):490–4.PubMedCrossRefGoogle Scholar
  13. 13.
    Harrington K. Early screening for pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol. 2011;37(5):623–4.PubMedCrossRefGoogle Scholar
  14. 14.
    Tuuli MG, Odibo AO. The role of serum markers and uterine artery Doppler in identifying at-risk pregnancies. Clin Perinatol. 2011;38(1):1–9.PubMedCrossRefGoogle Scholar
  15. 15.
    Velauthar L, Plana MN, Kalidindi M, Zamora 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(5):500–7.PubMedCrossRefGoogle Scholar
  16. 16.
    Bujold E, Roberge S, Nicolaides KH. Low-dose aspirin for prevention of adverse outcomes related to abnormal placentation. Prenat Diagn. 2014;34(7):642–8.PubMedGoogle Scholar
  17. 17.
    Vainio M, Kujansuu E, Iso-Mustajärvi M, Mäenpää J. Low dose acetylsalicylic acid in prevention of pregnancy-induced hypertension and intrauterine growth retardation in women with bilateral uterine artery notches. BJOG Int J Obstet Gynaecol. 2002;109(2):161–7.CrossRefGoogle Scholar
  18. 18.
    Cheema R, Dubiel M, Gudmundsson S. Fetal brain sparing is strongly related to the degree of increased placental vascular impedance. J Perinat Med. 2006;34(4):318–22.PubMedCrossRefGoogle Scholar
  19. 19.
    Vergani P, Roncaglia N, Andreotti C, Arreghini A, Teruzzi M, Pezzullo JC, et al. Prognostic value of uterine artery Doppler velocimetry in growth-restricted fetuses delivered near term. Am J Obstet Gynecol. 2002;187(4):932–6.PubMedCrossRefGoogle Scholar
  20. 20.
    Maroni E, Youssef A, Arcangeli T, Nanni M, De Musso F, Contro E, et al. Increased uterine artery pulsatility index at 34 weeks and outcome of pregnancy. Ultrasound Obstet Gynecol. 2011;38(4):395–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Prefumo F, Sebire NJ, Thilaganathan B. Decreased endovascular trophoblast invasion in first trimester pregnancies with high-resistance uterine artery Doppler indices. Hum Reprod. 2004;19(1):206–9.PubMedCrossRefGoogle Scholar
  22. 22.
    Ferrazzi E, Rigano S, Padoan A, Boito S, Pennati G, Galan HL. Uterine artery blood flow volume in pregnant women with an abnormal pulsatility index of the uterine arteries delivering normal or intrauterine growth restricted newborns. Placenta. 2011;32(7):487–92.PubMedCrossRefGoogle Scholar
  23. 23.
    Aardema MW, Saro MC, Lander M, De Wolf BT, Oosterhof H, Aarnoudse JG. Second trimester Doppler ultrasound screening of the uterine arteries differentiates between subsequent normal and poor outcomes of hypertensive pregnancy: two different pathophysiological entities? Clin Sci. 2004;106(4):377–82.PubMedCrossRefGoogle Scholar
  24. 24.
    Ness RB, Roberts JM. Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications. Am J Obstet Gynecol. 1996;175(5):1365–70.PubMedCrossRefGoogle Scholar
  25. 25.
    Verlohren S, Melchiorre K, Khalil A, Thilaganathan B. Uterine artery Doppler, birth weight and timing of onset of pre-eclampsia: providing insights into the dual etiology of late-onset pre-eclampsia. Ultrasound Obstet Gynecol. 2014;44(3):293–8.PubMedCrossRefGoogle Scholar
  26. 26.
    Cnossen JS, Morris RK, terRiet G, Mol BW, van der Post JA, Coomarasamy A, et al. Use of uterine artery Doppler ultrasonography to predict pre-eclampsia and intrauterine growth restriction: a systematic review and bivariable meta-analysis. Can Med Assoc J. 2008;178(6):701–11.CrossRefGoogle Scholar
  27. 27.
    Gómez O, Figueras F, Fernández S, Bennasar M, Martínez JM, Puerto B, Gratacós E. Reference ranges for uterine artery mean pulsatility index at 11–41 weeks of gestation. Ultrasound Obstet Gynecol. 2008;32(2):128–32.PubMedCrossRefGoogle Scholar
  28. 28.
    North RA, Ferrier C, Long D, Townend K, Kincaid-Smith P. Uterine artery Doppler flow velocity waveforms in the second trimester for the prediction of preeclampsia and fetal growth retardation. Obstet Gynecol. 1994;83(3):378–86.PubMedGoogle Scholar
  29. 29.
    Kofinas AD, Penry M, Simon NV, Swain M. Interrelationship and clinical significance of increased resistance in the uterine arteries in patients with hypertension or preeclampsia or both. Am J Obstet Gynecol. 1992;166(2):601–6.PubMedCrossRefGoogle Scholar
  30. 30.
    Poon LC, Karagiannis G, Leal A, Romero XC, Nicolaides KH. Hypertensive disorders in pregnancy: screening by uterine artery Doppler imaging and blood pressure at 11–13 weeks. Ultrasound Obstet Gynecol. 2009;34(5):497–502.PubMedCrossRefGoogle Scholar
  31. 31.
    Napolitano R, Rajakulasingam R, Memmo A, Bhide A, Thilaganathan B. Uterine artery Doppler screening for pre-eclampsia: comparison of the lower, mean and higher first-trimester pulsatility indices. Ultrasound Obstet Gynecol. 2011;37(5):534–7.PubMedCrossRefGoogle Scholar
  32. 32.
    Albaiges G, Missfelder-Lobos H, Lees C, Parra M, Nicolaides KH. One-stage screening for pregnancy complications by color Doppler assessment of the uterine arteries at 23 weeks’ gestation. Obstet Gynecol. 2000;96(4):559–64.PubMedGoogle Scholar
  33. 33.
    Thaler I, Weiner Z, Itskovitz J. Systolic or diastolic notch in uterine artery blood flow velocity waveforms in hypertensive pregnant patients: relationship to outcome. Obstet Gynecol. 1992;80(2):277–82.PubMedGoogle Scholar
  34. 34.
    Becker R, Vonk R, Vollert W, Entezami M. Doppler sonography of uterine arteries at 20–23 weeks: risk assessment of adverse pregnancy outcome by quantification of impedance and notch. J Perinat Med. 2002;30(5):388–94.PubMedCrossRefGoogle Scholar
  35. 35.
    Lees C, Parra M, Missfelder-Lobos H, Fletcher O, Nicolaides KH. Individualized risk assessment for adverse pregnancy outcome by uterine artery Doppler at 23 weeks. Obstet Gynecol. 2001;98(3):369–73.PubMedGoogle Scholar
  36. 36.
    Arduini D, Rizzo G, Romanini C, Mancuso S. Utero-placental blood flow velocity waveforms as predictors of pregnancy-induced hypertension. Eur J Obstet Gynecol Reprod Biol. 1987;26(4):335–41.PubMedCrossRefGoogle Scholar
  37. 37.
    Valensise H, Bezzeccheri V, Rizzo G, Tranquilli AL, Garzetti GG, Romanini C. Doppler velocimetry of the uterine artery as a screening test for gestational hypertension. Ultrasound Obstet Gynecol. 1993;3(1):18–22.PubMedCrossRefGoogle Scholar
  38. 38.
    Kurdi WS, Campbell S, Aquilina J, England P, Harrington K. The role of color Doppler imaging of the uterine arteries at 20 weeks’ gestation in stratifying antenatal care. Ultrasound Obstet Gynecol. 1998;12(5):339–45.PubMedCrossRefGoogle Scholar
  39. 39.
    Coleman MA, McCowan LM, North RA. Mid-trimester uterine artery Doppler screening as a predictor of adverse pregnancy outcome in high-risk women. Ultrasound Obstet Gynecol. 2000;15(1):7–12.PubMedCrossRefGoogle Scholar
  40. 40.
    Papageorghiou AT, Yu CK, Bindra R, Pandis G, Nicolaides KH. Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol. 2001;18(5):441–9.PubMedCrossRefGoogle Scholar
  41. 41.
    Harrington K, Fayyad A, Thakur V, Aquilina J. The value of uterine artery Doppler in the prediction of uteroplacental complications in multiparous women. Ultrasound Obstet Gynecol. 2004;23(1):50–5.PubMedCrossRefGoogle Scholar
  42. 42.
    Spencer K, Yu CK, Cowans NJ, Otigbah C, Nicolaides KH. Prediction of pregnancy complications by first-trimester maternal serum PAPP-A and free β-hCG and with second-trimester uterine artery Doppler. Prenat Diagn. 2005;25(10):949–53.PubMedCrossRefGoogle Scholar
  43. 43.
    Onwudiwe N, Yu CK, Poon LC, Spiliopoulos I, Nicolaides KH. Prediction of pre-eclampsia by a combination of maternal history, uterine artery Doppler and mean arterial pressure. Ultrasound Obstet Gynecol. 2008;32(7):877–83.PubMedCrossRefGoogle Scholar
  44. 44.
    Yu CK, Khouri O, Onwudiwe N, Spiliopoulos Y, Nicolaides KH. Prediction of pre-eclampsia by uterine artery Doppler imaging: relationship to gestational age at delivery and small-for-gestational age. Ultrasound Obstet Gynecol. 2008;31(3):310–3.PubMedCrossRefGoogle Scholar
  45. 45.
    Pongrojpaw D, Chanthasenanont A, Nanthakomon T. Second trimester uterine artery Doppler screening in prediction of adverse pregnancy outcome in high risk women. J Med Assoc Thai. 2010;93(Suppl 7):S127–30.PubMedGoogle Scholar
  46. 46.
    Garcia B, Llurba E, Valle L, Gómez-Roig MD, Juan M, Pérez-Matos C, Fernández M, García-Hernández JA, Alijotas-Reig J, Higueras MT, Calero I. 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(6):680–9.PubMedCrossRefGoogle Scholar
  47. 47.
    Dugoff L, Lynch AM, Cioffi-Ragan D, Hobbins JC, Schultz LK, Malone FD, FASTER Trial Research Consortium, et al. First trimester uterine artery Doppler abnormalities predict subsequent intrauterine growth restriction. Am J Obstet Gynecol. 2005;193(3):1208–12.PubMedCrossRefGoogle Scholar
  48. 48.
    Fratelli N, Rampello S, Guala M, Platto C, Frusca T. Transabdominal uterine artery Doppler between 11 and 14 weeks of gestation for the prediction of outcome in high-risk pregnancies. J Matern Fetal Neonatal Med. 2008;21(6):403–6.PubMedCrossRefGoogle Scholar
  49. 49.
    Martin AM, Bindra R, Curcio P, Cicero S, Nicolaides KH. Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler at 11–14 weeks of gestation. Ultrasound Obstet Gynecol. 2001;18(6):583–6.PubMedCrossRefGoogle Scholar
  50. 50.
    Pilalis A, Souka AP, Antsaklis P, Basayiannis K, Benardis P, Haidopoulos D, et al. Screening for pre-eclampsia and small for gestational age fetuses at the 11–14 weeks scan by uterine artery Dopplers. Acta Obstet Gynecol Scand. 2007;86(5):530–4.PubMedCrossRefGoogle Scholar
  51. 51.
    Melchiorre K, Wormald B, Leslie K, Bhide A, Thilaganathan B. First-trimester uterine artery Doppler indices in term and preterm pre-eclampsia. Ultrasound Obstet Gynecol. 2008;32(2):133–7.PubMedCrossRefGoogle Scholar
  52. 52.
    Akolekar R, Syngelaki A, Sarquis R, Zvanca M, Nicolaides KH. Prediction of early, intermediate and late pre-eclampsia from maternal factors, biophysical and biochemical markers at 11–13 weeks. Prenat Diagn. 2011;31(1):66–74.PubMedCrossRefGoogle Scholar
  53. 53.
    Nicolaides KH, Bindra R, Turan OM, Chefetz I, Sammar M, Meiri H, et al. A novel approach to first-trimester screening for early pre-eclampsia combining serum PP-13 and Doppler ultrasound. Ultrasound Obstet Gynecol. 2006;27(1):13–7.PubMedCrossRefGoogle Scholar
  54. 54.
    Plasencia W, Maiz N, Bonino S, Kaihura C, Nicolaides KH. Uterine artery Doppler at 11 + 0 to 13 + 6 weeks in the prediction of pre-eclampsia. Ultrasound Obstet Gynecol. 2007;30(5):742–9.PubMedCrossRefGoogle Scholar
  55. 55.
    Audibert F, Boucoiran I, An N, Aleksandrov N, Delvin E, Bujold E, et al. Screening for preeclampsia using first-trimester serum markers and uterine artery Doppler in nulliparous women. Am J Obstet Gynecol. 2010;203(4):383-e1.CrossRefGoogle Scholar
  56. 56.
    Shwarzman P, Waintraub AY, Frieger M, Bashiri A, Mazor M, Hershkovitz R. Third-trimester abnormal uterine artery Doppler findings are associated with adverse pregnancy outcomes. J Ultrasound Med. 2013;32(12):2107–13.PubMedCrossRefGoogle Scholar
  57. 57.
    Lai J, Poon LC, Pinas A, Bakalis S, Nicolaides KH. Uterine artery Doppler at 30–33 weeks’ gestation in the prediction of preeclampsia. Fetal Diagn Ther. 2013;33(3):156–63.PubMedCrossRefGoogle Scholar
  58. 58.
    Rai L, Lekshmi S. Value of third trimester uterine artery doppler in high-risk pregnancies for prediction of adverse perinatal outcome. J South Asian Fed Obstet Gynecol. 2010;2(1):31–5.Google Scholar
  59. 59.
    Tsiakkas A, Saiid Y, Wright A, Wright D, Nicolaides KH. Competing risks model in screening for preeclampsia by maternal factors and biomarkers at 30–34 weeks’ gestation. Am J Obstet Gynecol. 2016;215(1):87-e1.CrossRefGoogle Scholar
  60. 60.
    Oros D, Figueras F, Cruz-Martinez R, Meler E, Munmany M, Gratacos E. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol. 2011;37(2):191–5.PubMedCrossRefGoogle Scholar
  61. 61.
    Figueras F, Gratacós E. Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther. 2014;36(2):86–9.PubMedCrossRefGoogle Scholar
  62. 62.
    Severi FM, Bocchi C, Visentin A, Falco P, Cobellis L, Florio P, et al. Uterine and fetal cerebral Doppler predict the outcome of third-trimester small-for-gestational age fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol. 2002;19(3):225–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Cruz-Martinez R, Savchev S, Cruz-Lemini M, Mendez A, Gratacos E, Figueras F. Clinical utility of third-trimester uterine artery Doppler in the prediction of brain hemodynamic deterioration and adverse perinatal outcome in small-for-gestational-age fetuses. Ultrasound Obstet Gynecol. 2015;45(3):273–8.PubMedCrossRefGoogle Scholar
  64. 64.
    Stepan H, Herraiz I, Schlembach D, Verlohren S, Brennecke S, Chantraine F, Klein E, Lapaire O, Llurba E, Ramoni A, Vatish M. Implementation of the sFlt-1/PlGF ratio for prediction and diagnosis of pre-eclampsia in singleton pregnancy: implications for clinical practice. Ultrasound Obstet Gynecol. 2015;45(3):241–6.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Gomez O, Figueras F, Martinez JM, Del Rio M, Palacio M, Eixarch E, 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(6):802–8.PubMedCrossRefGoogle Scholar
  66. 66.
    Groom KM, North RA, Stone PR, Chan EH, Taylor RS, Dekker GA, et al. Patterns of change in uterine artery Doppler studies between 20 and 24 weeks of gestation and pregnancy outcomes. Obstet Gynecol. 2009;113(2 Part 1):332–8.PubMedCrossRefGoogle Scholar
  67. 67.
    Harrington KD, Cooper D, Lees C, Hecher K, Campbell S. Doppler ultralsound 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(3):182–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Carbillon L, Uzan M, Largilliere C, Perrot N, Tigaizin A, Paries J, et al. Prospective evaluation of uterine artery flow velocity waveforms at 12–14 and 22–24 weeks of gestation in relation to pregnancy outcome and birth weight. Fetal Diagn Ther. 2004;19(4):381–4.PubMedCrossRefGoogle Scholar
  69. 69.
    Prefumo F, Güven M, Ganapathy R, Thilaganathan B. The longitudinal variation in uterine artery blood flow pattern in relation to birth weight. Obstet Gynecol. 2004;103(4):764–8.PubMedCrossRefGoogle Scholar
  70. 70.
    Ghi T, Contro E, Youssef A, Giorgetta F, Farina A, Pilu G, et al. Persistence of increased uterine artery resistance in the third trimester and pregnancy outcome. Ultrasound Obstet Gynecol. 2010;36(5):577–81.PubMedCrossRefGoogle Scholar
  71. 71.
    Kurdi W, Fayyad A, Thakur V, Harrington K. Delayed normalisation of uterine artery Doppler waveforms is not a benign phenomenon. Eur J Obstet Gynecol Reprod Biol. 2004;117(1):20–3.PubMedCrossRefGoogle Scholar
  72. 72.
    Napolitano R, Melchiorre K, Arcangeli T, Dias T, Bhide A, Thilaganathan B. Screening for pre-eclampsia by using changes in uterine artery Doppler indices with advancing gestation. Prenat Diagn. 2012;32(2):180–4.PubMedCrossRefGoogle Scholar
  73. 73.
    Jamal A, Abbasalizadeh F, Vafaei H, Marsoosi V, Eslamian L. Multicenter screening for adverse pregnancy outcomes by uterine artery Doppler in the second and third trimester of pregnancy. Med Ultrasonogr. 2013;15(2):95.CrossRefGoogle Scholar
  74. 74.
    Steel SA, Pearce JM, McParland P, Chamberlain GV. Early Doppler ultrasound screening in prediction of hypertensive disorders of pregnancy. Lancet. 1990;335(8705):1548–51.PubMedCrossRefGoogle Scholar
  75. 75.
    Frusca T, Soregaroli M, Valcamonico A, Guandalini F, Danti L. Doppler velocimetry of the uterine arteries in nulliparous women. Early Human Dev. 1997;48(1):177–85.CrossRefGoogle Scholar
  76. 76.
    Myatt L, Clifton RG, Roberts JM, Spong CY, Hauth JC, Varner MW, et al. The utility of uterine artery Doppler velocimetry in prediction of preeclampsia in a low-risk population. Obstet Gynecol. 2012;120(4):815.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Afrakhteh M, Moeini A, Taheri MS, Haghighatkhah HR, Fakhri M, Masoom N. Uterine Doppler velocimetry of the uterine arteries in the second and third trimesters for the prediction of gestational outcome. Rev Bras Ginecol Obstet. 2014;36(1):35–9.PubMedGoogle Scholar
  78. 78.
    Talari H, Mesdaghinia E, Kalahroudi MA. Aspirin and preeclampsia prevention in patients with abnormal uterine artery blood flow. Iran Red Crescent Med J. 2014;16(8):e17175.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Ebrashy A, Ibrahim M, Marzook A, Yousef D. Usefulness of aspirin therapy in high-risk pregnant women with abnormal uterine artery Doppler ultrasound at 14–16 weeks pregnancy: randomized controlled clinical trial. Croat Med J. 2005;46(5):826.PubMedGoogle Scholar
  80. 80.
    Redman CW, De Swiet M, Collins R, Grant A. CLASP: a randomised trial of low-dose aspirin for the prevention and treatment of pre-eclampsia among 9364 pregnant women. Lancet. 1994;343(8898):619.CrossRefGoogle Scholar
  81. 81.
    Pilalis A, Souka AP, Antsaklis P, Daskalakis G, Papantoniou N, Mesogitis S, et al. Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler and PAPP-A at 11–14 weeks’ gestation. Ultrasound Obstet Gynecol. 2007;29(2):135–40.PubMedCrossRefGoogle Scholar
  82. 82.
    LeFevre ML. Low-dose aspirin use for the prevention of morbidity and mortality from preeclampsia: US preventive services task force recommendation statement low-dose aspirin to prevent morbidity and mortality from preeclampsia. Ann Intern Med. 2014;161(11):819–26.PubMedCrossRefGoogle Scholar
  83. 83.
    Xu TT, Zhou F, Deng CY, Huang GQ, Li JK, Wang XD. Low-dose aspirin for preventing preeclampsia and its complications: a meta-analysis. J Clin Hypertens. 2015;17(7):567–73.CrossRefGoogle Scholar
  84. 84.
    Melchiorre K, Sharma R, Thilaganathan B. Cardiovascular implications in preeclampsia. Circulation. 2014;130(8):703–14.PubMedCrossRefGoogle Scholar
  85. 85.
    Li XL, Chen TT, Dong X, Gou WL, Lau S, Stone P, et al. Early onset preeclampsia in subsequent pregnancies correlates with early onset preeclampsia in first pregnancy. Eur J Obstet Gynecol Reprod Biol. 2014;177:94–9.PubMedCrossRefGoogle Scholar
  86. 86.
    Baschat AA. First-trimester screening for pre-eclampsia: moving from personalized risk prediction to prevention. Ultrasound Obstet Gynecol. 2015;45(2):119–29.PubMedCrossRefGoogle Scholar
  87. 87.
    Kenny LC, Black MA, Poston L, Taylor R, Myers JE, Baker PN, et al. Early pregnancy prediction of preeclampsia in nulliparous women, combining clinical risk and biomarkers novelty and significance. Hypertension. 2014;64(3):644–52.PubMedCrossRefGoogle Scholar
  88. 88.
    Wright D, Syngelaki A, Akolekar R, Poon LC, Nicolaides KH. Competing risks model in screening for preeclampsia by maternal characteristics and medical history. Am J Obstet Gynecol. 2015;213(1):62-e1.CrossRefGoogle Scholar
  89. 89.
    O’Gorman N, Wright D, Rolnik DL, Nicolaides KH, Poon LC. Study protocol for the randomised controlled trial: combined multimarker screening and randomised patient treatment with aspirin for evidence-based preeclampsia prevention (ASPRE). BMJ Open. 2016;6(6):e011801.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Park FJ, Leung CH, Poon LC, Williams PF, Rothwell SJ, Hyett JA. Clinical evaluation of a first trimester algorithm predicting the risk of hypertensive disease of pregnancy. Aust N Z J Obstet Gynaecol. 2013;53(6):532–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Kane SC, Da Silva Costa F, Brennecke SP. New directions in the prediction of pre-eclampsia. Aust N Z J Obstet Gynaecol. 2014;54(2):101–7.PubMedCrossRefGoogle Scholar
  92. 92.
    Poon LC, Nicolaides KH. First-trimester maternal factors and biomarker screening for preeclampsia. Prenat Diagn. 2014;34(7):618–27.PubMedGoogle Scholar
  93. 93.
    Kuc S, Koster MP, Franx A, Schielen PC, Visser GH. Maternal characteristics, mean arterial pressure and serum markers in early prediction of preeclampsia. PLoS ONE. 2013;8(5):e63546.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Tayyar A, Guerra L, Wright A, Wright D, Nicolaides KH. Uterine artery pulsatility index in the three trimesters of pregnancy: effects of maternal characteristics and medical history. Ultrasound Obstet Gynecol. 2015;45(6):689–97.PubMedCrossRefGoogle Scholar
  95. 95.
    Poon LC, Syngelaki A, Akolekar R, Lai J, Nicolaides KH. Combined screening for preeclampsia and small for gestational age at 11–13 weeks. Fetal Diagn Ther. 2013;33(1):16–27.PubMedCrossRefGoogle Scholar
  96. 96.
    Selvaraj LR, Rose N, Ramachandran M. First trimester screening for pre-eclampsia and fetal growth restriction. J Fetal Med. 2016;3(2):77–84.CrossRefGoogle Scholar
  97. 97.
    Anderson UD, Gram M, Åkerström B, Hansson SR. First trimester prediction of preeclampsia. Curr Hypertens Rep. 2015;17(9):74.CrossRefGoogle Scholar
  98. 98.
    Oliveira N, Magder LS, Blitzer MG, Baschat AA. First-trimester prediction of pre-eclampsia: external validity of algorithms in a prospectively enrolled cohort. Ultrasound Obstet Gynecol. 2014;44(3):279–85.PubMedCrossRefGoogle Scholar
  99. 99.
    Christina KH, Smith GC, Papageorghiou AT, Cacho AM, Nicolaides KH, Fetal Medicine Foundation Second Trimester Screening Group. An integrated model for the prediction of preeclampsia using maternal factors and uterine artery Doppler velocimetry in unselected low-risk women. Am J Obstet Gynecol. 2005;193(2):429–36.CrossRefGoogle Scholar
  100. 100.
    Ghosh GS, Gudmundsson S. Uterine and umbilical artery Doppler are comparable in predicting perinatal outcome of growth-restricted fetuses. BJOG Int J Obstet Gynaecol. 2009;116(3):424–30.CrossRefGoogle Scholar
  101. 101.
    Conde-Agudelo A, Villar J, Lindheimer M. World Health Organization systematic review of screening tests for preeclampsia. Obstet Gynecol. 2004;104(6):1367–91.PubMedCrossRefGoogle Scholar
  102. 102.
    Park HJ, Shim SS, Cha DH. Combined screening for early detection of pre-eclampsia. Int J Mol Sci. 2015;16(8):17952–74.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Dekker GA, Sibai BM. Early detection of preeclampsia. Am J Obstet Gynecol. 1991;165(1):160–72.PubMedCrossRefGoogle Scholar

Copyright information

© Society of Fetal Medicine 2017

Authors and Affiliations

  • Selvaraj Ravi Lakshmy
    • 1
  • Masilamani Praveenkumar
    • 1
  • Umapathy Shobana
    • 1
  • Ziyaulla Thasleem
    • 1
  1. 1.Shri Lakshmi Scan CentreKrishnagiriIndia

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