Donald School Journal of Ultrasound in Obstetrics and Gynecology

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VOLUME 15 , ISSUE 1 ( January-March, 2021 ) > List of Articles


Early- and Late-onset Intrauterine Growth Retardation

Apostolos Zavlanos, Ioannis Tsakiridis, Ioannis Chatzikalogiannis, Apostolos Athanasiadis

Keywords : Complications, Delivery, Diagnosis, Fetal growth restriction, Intrauterine growth retardation, Management, Other, Prevention, Small-for-gestational-age, Ultrasound

Citation Information : Zavlanos A, Tsakiridis I, Chatzikalogiannis I, Athanasiadis A. Early- and Late-onset Intrauterine Growth Retardation. Donald School J Ultrasound Obstet Gynecol 2021; 15 (1):97-108.

DOI: 10.5005/jp-journals-10009-1686

License: CC BY-NC 4.0

Published Online: 00-03-2021

Copyright Statement:  Copyright © 2021; Jaypee Brothers Medical Publishers (P) Ltd.


Aim and objective: The scope of this literature review was to synthesize the available evidence on the diagnosis and management of early and late-intrauterine growth retardation (IUGR). Background: Intrauterine growth retardation is a common obstetric complication affecting about one out of 10 pregnancies and may be associated with both short- and long-term adverse outcomes. Review results: Risk factors for IUGR include maternal, fetal and placental parameters like smoking, chromosomal abnormalities and placental mosaicism. Early-IUGR, usually correlated with preeclampsia, is difficult to manage, while late-IUGR may not be promptly diagnosed, but is associated with lower mortality. In addition, both entities follow different patterns of progression. For each case, ultrasound growth evaluation at 2-weeks intervals and regular Doppler monitoring are needed, along with cardiotocography. Moreover, a normal umbilical artery Doppler pattern in the third trimester endorses a normal pregnancy in the early-IUGR, but as for the clinical follow-up of late-IUGR fetuses, cerebroplacental ratio is the appropriate parameter for monitoring. Thus, timing of delivery is usually affected by these factors. Finally, the combined first-trimester screening might help in the prediction of IUGR. Conclusion: The diagnosis of fetal hypoxia in the third trimester remains a challenge for modern obstetrics. Hence, all fetal-maternal units should adopt and follow their own protocol for the management of IUGR. Clinical significance: IUGR remains a major problem in both developing and developed countries and several causes have been identified. More research in the field of prevention and the appropriate timing of delivery would probably improve perinatal outcomes of the affected fetuses.

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  1. Cunningham F, Leveno KJ, Bloom SL, et al. Williams obstetrics. 24th ed., New York: McGraw-Hill; 2013.
  2. American College of Obstetricians and Gynecologists. Fetal growth restriction. Practice Bulletin no. 134, May 2013.
  3. Gardosi J, Madurasinghe V, Williams M, et al. Maternal and fetal risk factors for stillbirth: population based study. BMJ 2013;346(jan24 3):f108. DOI: 10.1136/bmj.f108.
  4. Baschat AA. Fetal growth restriction—from observation to intervention. J Perinat Med 2010;38(3):239–246. DOI: 10.1515/jpm.2010.041.
  5. GRIT Study Group. A randomised trial of timed delivery for the compromised preterm fetus: short-term outcomes and bayesian interpretation. BJOG 2003;110(1):27–32. DOI: 10.1046/j.1471-0528.2003.02014.x.
  6. Baschat AA, Cosmi E, Bilardo CM, et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol 2007;109(2 Pt 1):253–261. DOI: 10.1097/01.AOG.0000253215.79121.75.
  7. Bilardo CM, Wolf H, Stigter RH, et al. Relationship between monitoring parameters and perinatal outcome in severe, early intrauterine growth restriction. Ultrasound Obstet Gynecol 2004;23(2):119–125. DOI: 10.1002/uog.965.
  8. Danielian P, Dawson A, Whittle M, et al. When do obstetricians recommend delivery for a high-risk preterm growth-retarded fetus? The GRIT study group. Growth restriction intervention trial. Eur J Obstet Gynecol Reprod Biol 1996;67(2):121–126. DOI: 10.1016/0301-2115(96)02448-7.
  9. Romero R, Kalache KD, Kadar N. Timing the delivery of the preterm severely growth-restricted fetus: Venous Doppler, cardiotocography or the biophysical profile? Ultrasound Obstet Gynecol 2002;19(2):118–121. DOI: 10.1046/j.0960-7692.2002.00653.x.
  10. Baschat AA. Integrated fetal testing in growth restriction: combining multivessel Doppler and biophysical parameters. Ultrasound Obstet Gynecol 2003;21(1):1–8. DOI: 10.1002/uog.21.
  11. Hecher K, Bilardo CM, Stigter RH, et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 2001;18(6):564–570. DOI: 10.1046/j.0960-7692.2001.00590.x.
  12. 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(2):191–195. DOI: 10.1002/uog.7738.
  13. Turan OM, Turan S, Gungor S, et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008;32(2):160–167. DOI: 10.1002/uog.5386.
  14. Crispi F, Domínguez C, Llurba E, et al. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 2006;195(1):201–207. DOI: 10.1016/j.ajog.2006.01.014.
  15. Parker SE, Werler MM. Epidemiology of ischemic placental disease: a focus on preterm gestations. Semin Perinatol 2014;38(3):133–138. DOI: 10.1053/j.semperi.2014.03.004.
  16. Unterscheider J, Daly S, Geary MP, et al. Optimizing the definition of intrauterine growth restriction: the multicenter prospective PORTO study. Am J Obstet Gynecol 2013;208(4):290.e1-6. DOI: 10.1016/j.ajog.2013.02.007.
  17. Schwartz N, Sammel MD, Leite R, et al. First-trimester placental ultrasound and maternal serum markers as predictors of small-for-gestational-age infants. Am J Obstet Gynecol 2014;211(3):253.e1-8. DOI: 10.1016/j.ajog.2014.02.033.
  18. Benton SJ, Hu Y, Xie F, et al. Can placental growth factor in maternal circulation identify fetuses with placental intrauterine growth restriction? Am J Obstet Gynecol 2012;206(2):163. e1-7. DOI: 10.1016/j.ajog.2011.09.019.
  19. Odibo AO, Patel KR, Spitalnik A, et al. Placental pathology, first-trimester biomarkers and adverse pregnancy outcomes. J Perinatol 2014;34(3):186–191. DOI: 10.1038/jp.2013.176.
  20. Figueras F, Gratacos 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):86–98. DOI: 10.1159/000357592.
  21. Unterscheider J, Daly S, Geary MP, et al. Definition and management of fetal growth restriction: a survey of contemporary attitudes. Eur J Obstet Gynecol Reprod Biol 2014;174:41–45. DOI: 10.1016/j.ejogrb.2013.11.022.
  22. Platz E, Newman R. Diagnosis of IUGR: traditional biometry. Semin Perinatol 2008;32(3):140–147. DOI: 10.1053/j.semperi.2008.02.002.
  23. Dashe JS, McIntire DD, Lucas MJ, et al. Effects of symmetric and asymmetric fetal growth on pregnancy outcomes. Obstet Gynecol 2000;96(3):321–327. DOI: 10.1016/S0029-7844(00)00943-1.
  24. Figueras F, Gardosi J. Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 2011;204(4):288–300. DOI: 10.1016/j.ajog.2010.08.055.
  25. Savchev S, Figueras F, Sanz-Cortes M, et al. Evaluation of an optimal gestational age cut-off for the definition of early- and late-onset fetal growth restriction. Fetal Diagn Ther 2014;36(2):99–105. DOI: 10.1159/000355525.
  26. Tsatsaris V. Le retard de croissance intrautérin. Aspects cliniques et fondamentaux. Elsevier Masson; 2012.
  27. 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(6):571–577. DOI: 10.1046/j.0960-7692.2001.00591.x.
  28. Cosmi E, Ambrosini G, D'Antona D, et al. Doppler, cardiotocography, and biophysical profile changes in growth-restricted fetuses. Obstet Gynecol 2005;106(6):1240–1245. DOI: 10.1097/01.AOG.0000187540.37795.3a.
  29. Ferrazzi E, Bozzo M, Rigano S, 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(2):140–146. DOI: 10.1046/j.0960-7692.2002.00627.x.
  30. Vintzileos AM, Fleming AD, Scorza WE, et al. Relationship between fetal biophysical activities and umbilical cord blood gas values. Am J Obstet Gynecol 1991;165(3):707–713. DOI: 10.1016/0002-9378(91)90314-H.
  31. Crovetto F, Crispi F, Scazzocchio E, et al. Performance of first trimester integrated screening for early and late small for gestational age newborns. Ultrasound Obstet Gynecol 2013;208:203.e1-10.
  32. Yinon Y, Kingdom JCP, Odutayo A, 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.
  33. Fouron JC, Gosselin J, Raboisson MJ, et al. The relationship between an aortic isthmus blood flow velocity index and the postnatal neurodevelopmental status of fetuses with placental circulatory insufficiency. Am J Obstet Gynecol 2005;192(2):497–503. DOI: 10.1016/j.ajog.2004.08.026.
  34. Cruz-Lemini M, Crispi F, Van Mieghem T, et al. Risk of perinatal death in early-onset intrauterine growth restriction according to gestational age and cardiovascular Doppler indices: a multicenter study. Fetal Diagn Ther 2012;32(1-2):116–122. DOI: 10.1159/000333001.
  35. Cruz-Martinez R, Figueras F, Hernandez-Andrade E, et al. Changes in myocardial performance index and aortic isthmus and ductus venosus Doppler in term, small-for-gestational age fetuses with normal umbilical artery pulsatility index. Ultrasound Obstet Gynecol 2011;38(4):400–405. DOI: 10.1002/uog.8976.
  36. Figueras F, Benavides A, Del Rio M, et al. Monitoring of fetuses with intrauterine growth restriction: longitudinal changes in ductus venosus and aortic isthmus flow. Ultrasound Obstet Gynecol 2009;33(1):39–43. DOI: 10.1002/uog.6278.
  37. Baschat AA. Neurodevelopment after fetal growth restriction. Fetal Diagn Ther 2014;36(2):136–142. DOI: 10.1159/000353631.
  38. Crovetto F, Crispi F, Scazzocchio E, et al. First-trimester screening for early and late small-for-gestational-age neonates using maternal serum biochemistry, blood pressure and uterine artery Doppler. Ultrasound Obstet Gynecol 2014;43(1):34–40. DOI: 10.1002/uog.12537.
  39. Muresan 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(1):103–109. DOI: 10.11152/mu.2013.2066.181.dop.
  40. Crispi F, Llurba E, Domínguez C, et al. Predictive value of angiogenic factors and uterine artery Doppler for early- versus late-onset pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 2008;31(3):303–309. DOI: 10.1002/uog.5184.
  41. Aardema MW, Oosterhof H, Timmer A, et al. Uterine artery Doppler flow and uteroplacental vascular pathology in normal pregnancies and pregnancies complicated by preeclampsia and small for gestational age fetuses. Placenta 2001;22(5):405–411. DOI: 10.1053/plac.2001.0676.
  42. Apel-Sarid L, Levy A, Holcberg G, et al. Term and preterm (<34 and <37 weeks gestation) placental pathologies associated with fetal growth restriction. Arch Gynecol Obstet 2010;282(5):487–492. DOI: 10.1007/s00404-009-1255-1.
  43. Gardosi JO. Prematurity and fetal growth restriction. Early Hum Dev 2005;81(1):43–49. DOI: 10.1016/j.earlhumdev.2004.10.015.
  44. Frøen JF, Gardosi JO, Thurmann A, et al. Restricted fetal growth in sudden intrauterine unexplained death. Acta Obstet Gynecol Scand 2004;83(9):801–807. DOI: 10.1111/j.0001-6349.2004.00602.x.
  45. Chang TC, Robson SC, Spencer JAD, et al. Prediction of perinatal morbidity at term in small fetuses: comparison of fetal growth and Doppler ultrasound. Br J Obstet Gynaecol 1994;101(5):422–427. DOI: 10.1111/j.1471-0528.1994.tb11916.x.
  46. Doctor BA, O’Riordan MA, Kirchner HL, et al. Perinatal correlates and neonatal outcomes of small for gestational age infants born at term gestation. Am J Obstet Gynecol 2001;185(3):652–659. DOI: 10.1067/mob.2001.116749.
  47. McCowan LM, Harding JE, Stewart AW. Umbilical artery Doppler studies in small for gestational age babies reflect disease severity. BJOG 2000;107(7):916–925. DOI: 10.1111/j.1471-0528.2000.tb11092.x.
  48. Severi FM, Bocchi C, Visentin A, 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):225–228. DOI: 10.1046/j.1469-0705.2002.00652.x.
  49. Cruz-Martínez R, Figueras F, Hernandez-Andrade E, et al. Fetal brain Doppler to predict cesarean delivery for nonreassuring fetal status in term small-for-gestational-age fetuses. Obstet Gynecol 2011;117(3):618–626. DOI: 10.1097/AOG.0b013e31820b0884.
  50. Cetin I, Barberis B, Brusati V, et al. Lactate detection in the brain of growth-restricted fetuses with magnetic resonance spectroscopy. Am J Obstet Gynecol 2011;205(4):350.e1-7. DOI: 10.1016/j.ajog.2011.06.020.
  51. Eixarch E, Meler E, Iraola A, et al. Neurodevelopmental outcome in 2-year-old infants who were small-for-gestational age term fetuses with cerebral blood flow redistribution. Ultrasound Obstet Gynecol 2008;32(7):894–899. DOI: 10.1002/uog.6249.
  52. Hershkovitz R, Kingdom JCP, Geary M, et al. Fetal cerebral blood flow redistribution in late gestation: identification of compromise in small fetuses with normal umbilical artery Doppler. Ultrasound Obstet Gynecol 2000;15(3):209–212. DOI: 10.1046/j.1469-0705.2000.00079.x.
  53. Clausson B, Cnattingius S, Axelsson O. Preterm and term births of small for gestational age infants: a population-based study of risk factors among nulliparous women. Br J Obstet Gynaecol 1998;105(9):1011–1017. DOI: 10.1111/j.1471-0528.1998.tb10266.x.
  54. Gordijn SJ, Beune IM, Thilaganathan B, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol 2016;48(3):333–339. DOI: 10.1002/uog.15884.
  55. Hendrix N, Berghella V. Non-placental causes of intrauterine growth restriction. Semin Perinatol 2008;32(3):161–165. DOI: 10.1053/j.semperi.2008.02.004.
  56. Wilcox MA, Smith SJ, Johnson IR, et al. The effect of social deprivation on birthweight, excluding physiological and pathological effects. Br J Obstet Gynaecol 1995;102(11):918–924. DOI: 10.1111/j.1471-0528.1995.tb10882.x.
  57. Lee K, Ferguson RM, Corpuz M, et al. Maternal age and incidence of low birth weight at term: a population study. Am J Obstet Gynecol 1988;158(1):84–89. DOI: 10.1016/0002-9378(88)90783-1.
  58. Aldous MB, Edmonson MB. Maternal age at first childbirth and risk of low birth weight and preterm delivery in Washington State. JAMA 1993;270(21):2574–2577. DOI: 10.1001/jama.1993.03510210060028.
  59. Strobino DM, Ensminger ME, Kim YJ, et al. Mechanisms for maternal age differences in birth weight. Am J Epidemiol 1995;142(5):504–514. DOI: 10.1093/oxfordjournals.aje.a117668.
  60. Wu Wen S, Goldenberg RL, Cutter GR, et al. Intrauterine growth retardation and preterm delivery: prenatal risk factors in an indigent population. Am J Obstet Gynecol 1990;162(1):213–218. DOI: 10.1016/0002-9378(90)90853-Y.
  61. Berghella V. Prevention of recurrent fetal growth restriction. Obstet Gynecol 2007;110(4):904–912. DOI: 10.1097/01.AOG.0000267203.55718.aa.
  62. Schieve LA, Meikle SF, Ferre C, et al. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med 2002;346(10):731–737. DOI: 10.1056/NEJMoa010806.
  63. Lieberman E, Gremy I, Lang JM, et al. Low birthweight at term and the timing of fetal exposure to maternal smoking. Am J Public Health 1994;84(7):1127–1131. DOI: 10.2105/AJPH.84.7.1127.
  64. Shu XO, Hatch MC, Mills J, et al. Maternal smoking, alcohol drinking, caffeine consumption, and fetal growth: results from a prospective study. Epidemiology 1995;6(2):115–120. DOI: 10.1097/00001648-199503000-00005.
  65. Naeye RL, Blanc W, Leblanc W, et al. Fetal complications of maternal heroin addiction: abnormal growth, infections, and episodes of stress. J Pediatr 1973;83(6):1055–1061. DOI: 10.1016/S0022-3476(73)80550-5.
  66. Fulroth R, Phillips B, Durand DJ. Perinatal outcome of infants exposed to cocaine and/or heroin in utero. Am J Dis Child 1989;143(8):905–910. DOI: 10.1001/archpedi.1989.02150200057018.
  67. Lin CC, Santolaya-Forgas J. Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol 1998;92(6):1044–1055. DOI: 10.1097/00006250-199812000-00030.
  68. Soong YK, Wang TH, Lee YS, et al. Genome-wide detection of uniparental disomy in a fetus with intrauterine growth restriction using genotyping microarrays. Taiwan J Obstet Gynecol 2009;48(2):152–158. DOI: 10.1016/S1028-4559(09)60277-1.
  69. Cordier AG, Nedellec S, Benachi A, et al. Arguments for an infectious cause of IUGR. J Gynecol Obstet Biol Reprod (Paris) 2011;40(2):109–115. DOI: 10.1016/j.jgyn.2011.01.001.
  70. Iqbal S, Kriebs J, Harman C, et al. Predictors of fetal growth in maternal HIV disease. Am J Perinatol 2010;27(7):517–523. DOI: 10.1055/s-0030-1248937.
  71. Heinonen S, Taipale P, Saarikoski S. Weights of placentae from small-for-gestational age infants revisited. Placenta 2001;22(5):399–404. DOI: 10.1053/plac.2001.0630.
  72. Yu KM. Relation between placental morphometry and fetal growth. Zhonghua Fu Chan Ke Za Zhi 1992;27(4):217–219. , 50.
  73. Wilkins-Haug L, Quade B, Morton CC. Confined placental mosaicism as a risk factor among newborns with fetal growth restriction. Prenat Diagn 2006;26(5):428–432. DOI: 10.1002/pd.1430.
  74. Bjoro Jr K. Vascular anomalies of the umbilical cord: I. Obstetric implications. Early Hum Dev 1983;8(2):119–127. DOI: 10.1016/0378-3782(83)90067-1.
  75. Bjoro Jr K. Gross pathology of the placenta in intrauterine growth retardation. Ann Chir Gynaecol 1981;70(6):316–322.
  76. Djakovic A, Rieger L, Wirbelauer J, et al. Severe foetal growth retardation in a patient with uterus bicornis, velamentous insertion and partial placental abruption in the 26th week of gestation—a case report. Z Geburtshilfe Neonatol 2007;211(4):169–173. DOI: 10.1055/s-2007-981219.
  77. Bernstein IM, Horbar JD, Badger GJ, et al. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol 2000;182(1 Pt 1):198–206. DOI: 10.1016/S0002-9378(00)70513-8.
  78. Garite TJ, Clark R, Thorp JA. Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol 2004;191(2):481–487. DOI: 10.1016/j.ajog.2004.01.036.
  79. Chauhan SP, Rice MM, Grobman WA, et al. Neonatal morbidity of small- and large-for-gestational-age neonates born at term in uncomplicated pregnancies. Obstet Gynecol 2017;130(3):511–519. DOI: 10.1097/AOG.0000000000002199.
  80. von Beckerath AK, Kollmann M, Rotky-Fast C, et al. Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction. Am J Obstet Gynecol 2013;208(2):130.e1-6. DOI: 10.1016/j.ajog.2012.11.014.
  81. McIntire DD, Bloom SL, Casey BM, et al. Birth weight in relation to morbidity and mortality among newborn infants. N Engl J Med 1999;340(16):1234–1238. DOI: 10.1056/NEJM199904223401603.
  82. Arcangeli T, Thilaganathan B, Hooper R, et al. Neurodevelopmental delay in small babies at term: a systematic review. Ultrasound Obstet Gynecol 2012;40(3):267–275. DOI: 10.1002/uog.11112.
  83. Barker DJ. Adult consequences of fetal growth restriction. Clin Obstet Gynecol 2006;49(2):270–283. DOI: 10.1097/00003081-200606000-00009.
  84. Royal College of Obstetricians and Gynaecologists. The investigation and Management of the Small-for-Gestational-Age Fetus. Published February 2013. Minor revisions—January 2014.
  85. Pay ASD, Wiik J, Backe B, et al. Symphysis-fundus height measurement to predict small-for-gestational-age status at birth: a systematic review. BMC Pregnancy Childbirth 2015;15(1):22. DOI: 10.1186/s12884-015-0461-z.
  86. Knox AJ, Sadler L, Pattison NS, et al. An obstetric scoring system: its development and application in obstetric management. Obstet Gynecol 1993;81(2):195–199.
  87. Robinson HP, Fleming JE. A critical evaluation of sonar “crown-rump length” measurements. Br J Obstet Gynaecol 1975;82(9):702–710. DOI: 10.1111/j.1471-0528.1975.tb00710.x.
  88. Snijders RJ, Nicolaides KH. Fetal biometry at 14-40 weeks’ gestation. Ultrasound Obstet Gynecol 1994;4(1):34–48. DOI: 10.1046/j.1469-0705.1994.04010034.x.
  89. Chang TC, Robson SC, Boys RJ, et al. Prediction of the small for gestational age infant: which ultrasonic measurement is best? Obstet Gynecol 1992;80(6):1030–1038.
  90. Ott WJ. Sonographic diagnosis of fetal growth restriction. Clin Obstet Gynecol 2006;49(2):295–307. DOI: 10.1097/00003081-200606000-00011.
  91. Gardosi J, Chang A, Kalyan B, et al. Customised antenatal growth charts. Lancet 1992;339(8788):283–287. DOI: 10.1016/0140-6736(92)91342-6.
  92. Baschat AA, Weiner CP. Umbilical artery doppler screening for detection of the small fetus in need of antepartum surveillance. Am J Obstet Gynecol 2000;182(1 Pt 1):154–158. DOI: 10.1016/S0002-9378(00)70505-9.
  93. Proctor LK, Rushworth V, Shah PS, et al. Incorporation of femur length leads to underestimation of fetal weight in asymmetric preterm growth restriction. Ultrasound Obstet Gynecol 2010;35(4):442–448. DOI: 10.1002/uog.7605.
  94. Chauhan SP, Cole J, Sanderson M, et al. Suspicion of intrauterine growth restriction: use of abdominal circumference alone or estimated fetal weight below 10%. J Matern Fetal Neonatal Med 2006;19(9):557–562. DOI: 10.1080/14767050600798267.
  95. Deter RL, Lee W, Sangi-Haghpeykar H, et al. Personalized third-trimester fetal growth evaluation: comparisons of individualized growth assessment, percentile line and conditional probability methods. J Matern Fetal Neonatal Med 2016;29(2):177–185. DOI: 10.3109/14767058.2014.995083.
  96. Gramellini D, Folli MC, Raboni S, et al. Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 1992;79(3):416–420. DOI: 10.1097/00006250-199203000-00018.
  97. Arbeille P, Maulik D, Fignon A, et al. Assessment of the fetal PO2 changes by cerebral and umbilical Doppler on lamb fetuses during acute hypoxia. Ultrasound Med Biol 1995;21(7):861–870. DOI: 10.1016/0301-5629(95)00025-M.
  98. DeVore GR. The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses. Am J Obstet Gynecol 2015;213(1):5–15. DOI: 10.1016/j.ajog.2015.05.024.
  99. Royal College of Obstetricians and Gynaecologists. The investigation and management of the small-for-gestational age fetus. RCOG Green Top Guideline no. 31. London; Nov 2002. [online] Available from: corp/uploadedfiles/GT31SmallGestationalAge Fetus.pdf. [Accessed Aug., 2018].
  100. Alfirevic Z, Stampalija T, Gyte GM. Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev 2010(1):CD007529.
  101. Valcamonico A, Danti L, Frusca T, et al. Absent end-diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage. Am J Obstet Gynecol 1994;170(3):796–801. DOI: 10.1016/S0002-9378(94)70285-3.
  102. Cruz-Martinez R, Figueras F, Hernandez-Andrade E, et al. Longitudinal brain perfusion changes in near-term small-for-gestational-age fetuses as measured by spectral Doppler indices or by fractional moving blood volume. Am J Obstet Gynecol 2010;203(1):42.e1-6. DOI: 10.1016/j.ajog.2010.02.049.
  103. Hecher K, Spernol R, Stettner H, et al. Potential for diagnosing imminent risk to appropriate- and small-for-gestational-age fetuses by Doppler sonographic examination of umbilical and cerebral arterial blood flow. Ultrasound Obstet Gynecol 1992;2(4):266–271. DOI: 10.1046/j.1469-0705.1992.02040266.x.
  104. Bahado-Singh RO, Kovanci E, Jeffres A, et al. The Doppler cerebroplacental ratio and perinatal outcome in intrauterine growth restriction. Am J Obstet Gynecol 1999;180(3 Pt 1):750–756. DOI: 10.1016/S0002-9378(99)70283-8.
  105. Morales-Roselló J, Khalil A, Morlando M, et al. Poor neonatal acid-base status in term fetuses with low cerebroplacental ratio. Ultrasound Obstet Gynecol 2015;45(2):156–161. DOI: 10.1002/uog.14647.
  106. Arbeille P, Patat F, Tranquart F, et al. Doppler examination of the umbilical and cerebral arterial circulation of the fetus. J Gynecol Obstet Biol Reprod (Paris) 1987;16(1):45–51.
  107. Arias F. Accuracy of the middle-cerebral-to-umbilical-artery resistance index ratio in the prediction of neonatal outcome in patients at high risk for fetal and neonatal complications. Am J Obstet Gynecol 1994;171(6):1541–1545. DOI: 10.1016/0002-9378(94)90398-0.
  108. Makhseed M, Jirous J, Ahmed MA, et al. Middle cerebral artery to umbilical artery resistance index ratio in the prediction of neonatal outcome. Int J Gynaecol Obstet 2000;71(2):119–125. DOI: 10.1016/S0020-7292(00)00262-9.
  109. Ebrashy A, Azmy O, Ibrahim M, et al. Middle cerebral/umbilical artery resistance index ratio as sensitive parameter for fetal well-being and neonatal outcome in patients with preeclampsia: case-control study. Croat Med J 2005;46(5):821–825.
  110. Flood K, Unterscheider J, Daly S, et al. The role of brain sparing in the prediction of adverse outcomes in intrauterine growth restriction: results of the multicenter PORTO study. Am J Obstet Gynecol 2014;211(3):288.e1-5. DOI: 10.1016/j.ajog.2014.05.008.
  111. Baschat AA, Gembruch U, Weiner CP, et al. Qualitative venous Doppler waveform analysis improves prediction of critical perinatal outcomes in premature growth-restricted fetuses. Ultrasound Obstet Gynecol 2003;22(3):240–245. DOI: 10.1002/uog.149.
  112. Schwarze A, Gembruch U, Krapp M, et al. Qualitative venous Doppler flow waveform analysis in preterm intrauterine growth-restricted fetuses with ARED flow in the umbilical artery—correlation with short-term outcome. Ultrasound Obstet Gynecol 2005;25(6):573–579. DOI: 10.1002/uog.1914.
  113. Evertson LR, Gauthier RJ, Schifrin BS, et al. Antepartum fetal heart rate testing. I. Evolution of the nonstress test. Am J Obstet Gynecol 1979;133(1):29–33. DOI: 10.1016/0002-9378(79)90406-X.
  114. Pattison N, McCowan L. Cardiotocography for antepartum fetal assessment. Cochrane Database Syst Rev 2000(2):CD001068.
  115. Dawes GS, Redman CW. Automated analysis of the FHR: evaluation? Am J Obstet Gynecol 1992;167(6):1912–1914. DOI: 10.1016/0002-9378(92)91802-H.
  116. Grivell RM, Alfirevic Z, Gyte GM, et al. Antenatal cardiotocography for fetal assessment. Cochrane Database Syst Rev 2010(1):CD007863.
  117. Bracero LA, Morgan S, Byrne DW. Comparison of visual and computerized interpretation of nonstress test results in a randomized controlled trial. Am J Obstet Gynecol 1999;181(5 Pt 1):1254–1258. DOI: 10.1016/S0002-9378(99)70118-3.
  118. Manning FA, Bondaji N, Harman CR, et al. Fetal assessment based on fetal biophysical profile scoring. VIII. The incidence of cerebral palsy in tested and untested perinates. Am J Obstet Gynecol 1998;178(4):696–706. DOI: 10.1016/S0002-9378(98)70479-X.
  119. Miller DA, Rabello YA, Paul RH. The modified biophysical profile: antepartum testing in the 1990s. Am J Obstet Gynecol 1996;174(3):812–817. DOI: 10.1016/S0002-9378(96)70305-8.
  120. Alfirevic Z, Neilson JP. Biophysical profile for fetal assessment in high risk pregnancies. Cochrane Database Syst Rev 2000(2):CD000038.
  121. Boers KE, Vijgen SMC, Bijlenga D, et al. Induction versus expectant monitoring for intrauterine growth restriction at term: randomised equivalence trial (DIGITAT). BMJ 2010;341(dec21 1):c7087. DOI: 10.1136/bmj.c7087.
  122. Miller J, Turan S, Baschat AA. Fetal growth restriction. Semin Perinatol 2008;32(4):274–280. DOI: 10.1053/j.semperi.2008.04.010.
  123. Chauhan SP, Sanderson M, Hendrix NW, et al. Perinatal outcome and amniotic fluid index in the antepartum and intrapartum periods: a meta-analysis. Am J Obstet Gynecol 1999;181(6):1473–1478. DOI: 10.1016/S0002-9378(99)70393-5.
  124. Llurba E, Turan O, Kasdaglis T, et al. Emergence of late-onset placental dysfunction: relationship to the change in uterine artery blood flow resistance between the first and third trimesters. Am J Perinatol 2013;30(6):505–512. DOI: 10.1055/s-0032-1329181.
  125. Velauthar L, Plana MN, Kalidindi M, et al. First-trimester uterine artery Doppler and adverse pregnancy outcome: a meta-analysis involving 55,974 women. Ultrasound Obstet Gynecol 2014;43(5):500–507. DOI: 10.1002/uog.13275.
  126. Monaghan C, Binder J, Thilaganathan B, et al. Perinatal loss at term: the role of uteroplacental and fetal doppler assessment. Ultrasound Obstet Gynecol 2017;52(1):72–77. DOI: 10.1002/uog.17500.
  127. Gulmezoglu AM, Hofmeyr GJ. Plasma volume expansion for suspected impaired fetal growth. Cochrane Database Syst Rev 2000(2):CD000167.
  128. Gulmezoglu AM, Hofmeyr GJ. Betamimetics for suspected impaired fetal growth. Cochrane Database Syst Rev 2001(4):CD000036.
  129. Laurin J, Persson PH. The effect of bedrest in hospital on fetal outcome in pregnancies complicated by intrauterine growth retardation. Acta Obstet Gynecol Scand 1987;66(5):407–411. DOI: 10.3109/00016348709022043.
  130. Say L, Gulmezoglu AM, Hofmeyr GJ. Maternal nutrient supplementation for suspected impaired fetal growth. Cochrane Database Syst Rev 2003(1):CD000148. DOI: 10.1002/14651858.CD000148.
  131. Say L, Gulmezoglu AM, Hofmeyr GJ. Maternal oxygen administration for suspected impaired fetal growth. Cochrane Database Syst Rev 2003(1):CD000137. DOI: 10.1002/14651858.CD000137.
  132. CNGOF, (2013). Recommandations pour la pratique Clinique. Le retard de croissance intra-utérin. [online] Available from: [Accessed Aug., 2018].
  133. 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(4):300–308. DOI: 10.1016/j.ajog.2012.01.022.
  134. Lausman A, Kingdom J, Maternal Fetal Medicine Committee Intrauterine growth restriction: screening, diagnosis, and management. J Obstet Gynaecol Can 2013;35(8):741–748. DOI: 10.1016/S1701-2163(15)30865-3.
  135. American College of Obstetricians and Gynecologist. Antepartum Fetal Surveillance. ACOG Practice Bulletin No. 145. Washington, DC: American College of Obstetricians and Gynecologist; 2014.
  136. Royal College of Physicians of Ireland. Fetal Growth Restriction—Recognition, Diagnosis and Management. RCPI Clinical Practice Guideline No. 28. Dublin, Ireland: Royal College of Physicians of Ireland; 2014.
  137. Lees C, Marlow N, Arabin B, et al. 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(4):400–408. DOI: 10.1002/uog.13190.
  138. Visser GHA, Bilardo CM, Derks JB, et al. Fetal monitoring indications for delivery and 2-year outcome in 310 infants with fetal growth restriction delivered before 32 weeks’ gestation in the TRUFFLE study. Ultrasound Obstet Gynecol 2017;50(3):347–352. DOI: 10.1002/uog.17361.
  139. Crovetto F, Triunfo S, Crispi F, et al. Differential performance of first-trimester screening in predicting small-for-gestational-age neonate or fetal growth restriction. Ultrasound Obstet Gynecol 2017;49(3):349–356. DOI: 10.1002/uog.15919.
  140. Cignini P, Savasta LM, Gulino FA, et al. Predictive value of pregnancy-associated plasma protein-A (PAPP-A) and free beta-hCG on fetal growth restriction: results of a prospective study. Arch Gynecol Obstet 2016;293(6):1227–1233. DOI: 10.1007/s00404-015-3947-z.
  141. Familiari A, Bhide A, Morlando M, et al. Mid-pregnancy fetal biometry, uterine artery Doppler indices and maternal demographic characteristics: role in prediction of small-for-gestational-age birth. Acta Obstet Gynecol Scand 2016;95(2):238–244. DOI: 10.1111/aogs.12804.
  142. Bhutta ZA, Das JK, Bahl R, et al. Can available interventions end preventable deaths in mothers, newborn babies, and stillbirths, and at what cost? Lancet 2014;384(9940):347–370. DOI: 10.1016/S0140-6736(14)60792-3.
  143. Ota E, Hori H, Mori R, et al. Antenatal dietary education and supplementation to increase energy and protein intake. Cochrane Database Syst Rev 2015(6):CD000032. DOI: 10.1002/14651858.CD000032.pub3.
  144. Haider BA, Bhutta ZA. Multiple-micronutrient supplementation for women during pregnancy. Cochrane Database Syst Rev 2015(11):CD004905.
  145. Roberge S, Nicolaides K, Demers S, et al. The role of aspirin dose on the prevention of preeclampsia and fetal growth restriction: systematic review and meta-analysis. Am J Obstet Gynecol 2017;216(2):110–20.e6. DOI: 10.1016/j.ajog.2016.09.076.
  146. Rodger MA, Gris JC, de Vries JIP, et al. Low-molecular-weight heparin and recurrent placenta-mediated pregnancy complications: a meta-analysis of individual patient data from randomised controlled trials. Lancet 2016;388(10060):2629–2641. DOI: 10.1016/S0140-6736(16)31139-4.
  147. Gulmezoglu AM, Hofmeyr GJ. Bed rest in hospital for suspected impaired fetal growth. Cochrane Database Syst Rev 2000(2):CD000034.
  148. Abalos E, Duley L, Steyn DW. Antihypertensive drug therapy for mild to moderate hypertension during pregnancy. Cochrane Database Syst Rev 2014(2):CD002252. DOI: 10.1002/14651858.CD002252.pub3.
  149. Horvath A, Koletzko B, Szajewska H. Effect of supplementation of women in high-risk pregnancies with long-chain polyunsaturated fatty acids on pregnancy outcomes and growth measures at birth: a meta-analysis of randomized controlled trials. Br J Nutr 2007;98(2):253–259. DOI: 10.1017/S0007114507709078.
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