An integrated approach to fetal growth restriction

Best Practice and Research: Clinical Obstetrics and Gynaecology

Volumn 38, Issue , 2017, Pages 48-58

  Figueras, Francesc ^a,b   Gratacos, Eduard ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

Doppler; fetal growth restriction; small for gestational age

Indexed keywords

AMNION FLUID; AORTA; AORTIC ISTHMUS; CARDIOTOCOGRAPHY; CEREBROPLACENTAL RATIO; DUCTUS VENOSUS; FETAL BIOPHYSICAL PROFILE; FETAL DOPPLER; FETUS; FETUS HEART RATE; FETUS MONITORING; FIRST TRIMESTER PREGNANCY; HUMAN; INTRAUTERINE GROWTH RETARDATION; META ANALYSIS (TOPIC); OBSTETRIC DELIVERY; PARAMETERS CONCERNING THE FETUS, NEWBORN AND PREGNANCY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SMALL FOR DATE INFANT; THIRD TRIMESTER PREGNANCY; ULTRASOUND; DIAGNOSTIC IMAGING; DOPPLER ULTRASONOGRAPHY; FEMALE; FETAL GROWTH RETARDATION; FETUS ECHOGRAPHY; FETUS WEIGHT; GESTATIONAL AGE; MIDDLE CEREBRAL ARTERY; NEWBORN; PREGNANCY; UMBILICAL ARTERY; UTERINE ARTERY;

DELIVERY, OBSTETRIC; FEMALE; FETAL GROWTH RETARDATION; FETAL WEIGHT; GESTATIONAL AGE; HUMANS; INFANT, NEWBORN; INFANT, SMALL FOR GESTATIONAL AGE; MIDDLE CEREBRAL ARTERY; PREGNANCY; ULTRASONOGRAPHY, DOPPLER; ULTRASONOGRAPHY, PRENATAL; UMBILICAL ARTERIES; UTERINE ARTERY;

EID: 85006371358     PISSN: 15216934     EISSN: 15321932     Source Type: Journal    
DOI: 10.1016/j.bpobgyn.2016.10.006     Document Type: Review

References (91)

1. [1] Hepburn, M., Rosenberg, K., An audit of the detection and management of small-for-gestational age babies. Br J Obstet Gynaecol 93 (1986), 212–216.
2. [2] Backe, B., Nakling, J., Effectiveness of antenatal care: a population based study. Br J Obstet Gynaecol 100 (1993), 727–732.
3. [3] Richardus, J.H., Graafmans, W.C., Verloove-Vanhorick, S.P., et al. EuroNatal International Audit P, EuroNatal Working G. Differences in perinatal mortality and suboptimal care between 10 European regions: results of an international audit. BJOG 110 (2003), 97–105.
4. [4] Cnossen, J.S., Morris, R.K., ter Riet, G., et al. Use of uterine artery Doppler ultrasonography to predict pre-eclampsia and intrauterine growth restriction: a systematic review and bivariable meta-analysis. CMAJ 11:178 (2008), 701–711.
5. [5] 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 43 (2014), 34–40.
6. [6] Figueras, F., Eixarch, E., Gratacos, E., et al. Predictiveness of antenatal umbilical artery Doppler for adverse pregnancy outcome in small-for-gestational-age babies according to customised birthweight centiles: population-based study. BJOG 115 (2008), 590–594.
7. [7] Karagiannis, G., Akolekar, R., Sarquis, R., et al. Prediction of small-for-gestation neonates from biophysical and biochemical markers at 11-13 weeks. Fetal Diagn Ther 29 (2011), 148–154.
8. [8] 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 105 (1998), 1011–1017.
9. [9] Clausson, B., Gardosi, J., Francis, A., et al. Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. BJOG 108 (2001), 830–834.
10. [10] Moraitis, A.A., Wood, A.M., Fleming, M., et al. Birth weight percentile and the risk of term perinatal death. Obstet Gynecol 124 (2014), 274–283.
11. [11] Savchev, S., Figueras, F., Cruz-Martinez, R., et al. Estimated weight centile as a predictor of perinatal outcome in small-for-gestational-age pregnancies with normal fetal and maternal Doppler indices. Ultrasound Obstet Gynecol 39 (2012), 299–303.
12. [12] van Wyk, L., Boers, K.E., van der Post, J.A., et al., Group DS. Effects on (neuro)developmental and behavioral outcome at 2 years of age of induced labor compared with expectant management in intrauterine growth-restricted infants: long-term outcomes of the DIGITAT trial. Am J Obstet Gynecol 206:406 (2012), e1–e7.
13. [13] Kean, L., Liu, D., Antenatal care as a screening tool for the detection of small for gestational age babies in the low risk population. J Obstet Gynaecol 16 (1996), 77–82.
14. [14] Lindqvist, P.G., Molin, J., Does antenatal identification of small-for-gestational age fetuses significantly improve their outcome?. Ultrasound Obstet Gynecol 25 (2005), 258–264.
15. [15] Souka, A.P., Papastefanou, I., Pilalis, A., et al. Performance of third-trimester ultrasound for prediction of small-for-gestational-age neonates and evaluation of contingency screening policies. Ultrasound Obstet Gynecol 39 (2012), 535–542.
16. [16] Sovio, U., White, I.R., Dacey, A., et al. Screening for fetal growth restriction with universal third trimester ultrasonography in nulliparous women in the Pregnancy Outcome Prediction (POP) study: a prospective cohort study. Lancet 386 (2015), 2089–2097.
17. [17] Triunfo, S., Crovetto, F., Scazzocchio, E., et al. Contingent versus routine third-trimester screening for late fetal growth restriction. Ultrasound Obstet Gynecol 47 (2015), 81–88.
18. [18] Bricker, L., Neilson, J.P., Dowswell, T., Routine ultrasound in late pregnancy (after 24 weeks’ gestation). Cochrane Database Syst Rev, 2008, CD001451.
19. [19] Skrastad, R.B., Eik-Nes, S.H., Sviggum, O., et al. A randomized controlled trial of third-trimester routine ultrasound in a non-selected population. Acta Obstet Gynecol Scand 92 (2013), 1353–1360.
20. [20] McKenna, D., Tharmaratnam, S., Mahsud, S., et al. A randomized trial using ultrasound to identify the high-risk fetus in a low-risk population. Obstet Gynecol 101 (2003), 626–632.
21. [21] Duff, G.B., A randomized controlled trial in a hospital population of ultrasound measurement screening for the small for dates baby. Aust N Z J Obstet Gynaecol 33 (1993), 374–378.
22. [22] Neilson, J.P., Munjanja, S.P., Whitfield, C.R., Screening for small for dates fetuses: a controlled trial. Br Med J (Clin Res Ed) 289 (1984, 3), 1179–1182.
23. [23] Roma, E., Arnau, A., Berdala, R., et al. Ultrasound screening for fetal growth restriction at 36 vs 32 weeks’ gestation: a randomized trial (ROUTE). Ultrasound Obstet Gynecol 46 (2015), 391–397.
24. [24] Alfirevic, Z., Neilson, J.P., Doppler ultrasonography in high-risk pregnancies: systematic review with meta-analysis. Am J Obstet Gynecol 172 (1995), 1379–1387.
25. [25] Trudell, A.S., Cahill, A.G., Tuuli, M.G., et al. Risk of stillbirth after 37 weeks in pregnancies complicated by small-for-gestational-age fetuses. Am J Obstet Gynecol 208:376 (2013), e1–e7.
26. [26] Gardosi, J., Madurasinghe, V., Williams, M., et al. Maternal and fetal risk factors for stillbirth: population based study. BMJ, 346, 2013, f108.
27. [27] De Wit, M.C., Srebniak, M.I., Joosten, M., et al. Prenatal and postnatal findings in small for gestational age fetuses without structural ultrasound anomalies at 18-24 weeks. Ultrasound Obstet Gynecol, 2016 Apr 22, 10.1002/uog.15949 [Epub ahead of print].
28. [28] Shaffer, L.G., Rosenfeld, J.A., Dabell, M.P., et al. Detection rates of clinically significant genomic alterations by microarray analysis for specific anomalies detected by ultrasound. Prenat Diagn 32 (2012), 986–995.
29. [29] Gordijn, S.J., Beune, I.M., Thilaganathan, B., et al. Consensus definition for placental fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol 48 (2016), 333–339.
30. [30] Westergaard, H.B., Langhoff-Roos, J., Lingman, G., et al. A critical appraisal of the use of umbilical artery Doppler ultrasound in high-risk pregnancies: use of meta-analyses in evidence-based obstetrics. Ultrasound Obstet Gynecol 17 (2001), 466–476.
31. [31] 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 30 (2013), 505–512.
32. [32] Chang, T.C., Robson, S.C., Spencer, J.A., et al. Prediction of perinatal morbidity at term in small fetuses: comparison of fetal growth and Doppler ultrasound. Br J Obstet Gynaecol 101 (1994), 422–427.
33. [33] 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 37 (2011), 191–195.
34. [34] Parra-Saavedra, M., Crovetto, F., Triunfo, S., et al. Added value of umbilical vein flow as a predictor of perinatal outcome in term small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 42 (2013), 189–195.
35. [35] Morrow, R.J., Adamson, S.L., Bull, S.B., et al. Effect of placental embolization on the umbilical arterial velocity waveform in fetal sheep. Am J Obstet Gynecol 161 (1989), 1055–1060.
36. [36] Thompson, R.S., Stevens, R.J., Mathematical model for interpretation of Doppler velocity waveform indices. Med Biol Eng Comput 27 (1989), 269–276.
37. [37] Hershkovitz, R., Kingdom, J.C., 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 15 (2000), 209–212.
38. [38] Severi, F.M., 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 19 (2002), 225–228.
39. [39] Cruz-Martinez, R., Figueras, F., Oros, D., et al. Cerebral blood perfusion and neurobehavioral performance in full-term small-for-gestational-age fetuses. Am J Obstet Gynecol 201:474 (2009), e1–e7.
40. [40] Eixarch, E., Batalle, D., Illa, M., et al. Neonatal neurobehavior and diffusion MRI changes in brain reorganization due to intrauterine growth restriction in a rabbit model. PloS One, 7, 2012, e31497.
41. [41] 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 21 (1995), 861–870.
42. [42] Bahado-Singh, R.O., Kovanci, E., Jeffres, A., et al. The Doppler cerebroplacental ratio and perinatal outcome in intrauterine growth restriction. Am J Obstet Gynecol 180 (1999), 750–756.
43. [43] Gramellini, D., Folli, M.C., Raboni, S., et al. Cerebral-umbilical Doppler ratio as a predictor of adverse perinatal outcome. Obstet Gynecol 79 (1992), 416–420.
44. [44] Ghosh, G.S., Gudmundsson, S., Uterine and umbilical artery Doppler are comparable in predicting perinatal outcome of growth-restricted fetuses. BJOG 116 (2009), 424–430.
45. [45] Vergani, P., Roncaglia, N., Andreotti, C., et al. Prognostic value of uterine artery Doppler velocimetry in growth-restricted fetuses delivered near term. Am J Obstet Gynecol 187 (2002), 932–936.
46. [46] Fratelli, N., Valcamonico, A., Prefumo, F., et al. Effects of antenatal recognition and follow-up on perinatal outcomes in small-for-gestational age infants delivered after 36 weeks. Acta Obstet Gynecol Scand 92 (2013), 223–229.
47. [47] Figueras, F., Savchev, S., Triunfo, S., et al. An integrated model with classification criteria to predict small-for-gestational fetuses at risk of adverse perinatal outcome. Ultrasound Obstet Gynecol 45 (2015), 279–285.
48. [48] Lobmaier, S.M., Figueras, F., Mercade, I., et al. Angiogenic factors vs Doppler surveillance in the prediction of adverse outcome among late-pregnancy small-for- gestational-age fetuses. Ultrasound Obstet Gynecol 43 (2014), 533–540.
49. [49] Aviram, R., Shental, B., Kidron, D., Placental aetiologies of foetal growth restriction: clinical and pathological differences. Early Hum Dev 86 (2010), 59–63.
50. [50] Benton, S.J., Hu, Y., Xie, F., et al. Angiogenic factors as diagnostic tests for preeclampsia: a performance comparison between two commercial immunoassays. Am J Obstet Gynecol 205:469 (2011), e1–e8.
51. [51] Triunfo, S., Lobmaier, S., Parra-Saavedra, M., et al. Angiogenic factors at diagnosis of late-onset small-for-gestational age and histological placental underperfusion. Placenta 35 (2014), 398–403.
52. [52] Hecher, K., Bilardo, C.M., Stigter, R.H., et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 18 (2001), 564–570.
53. [53] Turan, O.M., Turan, S., Gungor, S., et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 32 (2008), 160–167.
54. [54] Baschat, A.A., Cosmi, E., Bilardo, C.M., et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol 109 (2007), 253–261.
55. [55] 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 42 (2013), 400–408.
56. [56] 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 36 (2014), 99–105.
57. [57] McCowan, L.M., Harding, J.E., Roberts, A.B., et al. A pilot randomized controlled trial of two regimens of fetal surveillance for small-for-gestational-age fetuses with normal results of umbilical artery doppler velocimetry. Am J Obstet Gynecol 182 (2000), 81–86.
58. [58] Boers, K.E., Vijgen, S.M., Bijlenga, D., et al. Induction versus expectant monitoring for intrauterine growth restriction at term: randomised equivalence trial (DIGITAT). BMJ, 341, 2010, c7087.
59. [59] Nabhan, A.F., Abdelmoula, Y.A., Amniotic fluid index versus single deepest vertical pocket as a screening test for preventing adverse pregnancy outcome. Cochrane Database Syst Rev, 2008, CD006593.
60. [60] Chauhan, S.P., Sanderson, M., Hendrix, N.W., et al. Perinatal outcome and amniotic fluid index in the antepartum and intrapartum periods: a meta-analysis. Am J Obstet Gynecol 181 (1999), 1473–1478.
61. [61] Alfirevic, Z., Stampalija, T., Gyte, G.M., Fetal and umbilical Doppler ultrasound in high-risk pregnancies. Cochrane Database Syst Rev, 2010, CD007529.
62. [62] 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 19 (2002), 140–146.
63. [63] Cosmi, E., Ambrosini, G., D'Antona, D., et al. Doppler, cardiotocography, and biophysical profile changes in growth-restricted fetuses. Obstet Gynecol 106 (2005), 1240–1245.
64. [64] Thornton, J.G., Hornbuckle, J., Vail, A., et al., Group GS. Infant wellbeing at 2 years of age in the Growth Restriction Intervention Trial (GRIT): multicentred randomised controlled trial. Lancet 364 (2004), 513–520.
65. [65] A randomised trial of timed delivery for the compromised preterm fetus: short term outcomes and Bayesian interpretation. BJOG 110 (2003), 27–32.
66. [66] 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 32 (2012), 116–122.
67. [67] 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 32 (2008), 894–899.
68. [68] Cruz-Martinez, 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 117 (2011), 618–626.
69. [69] Boers, K.E., van Wyk, L., van der Post, J.A., et al., Group DS. Neonatal morbidity after induction vs expectant monitoring in intrauterine growth restriction at term: a subanalysis of the DIGITAT RCT. Am J Obstet Gynecol 206:344 (2012), e1–e7.
70. [70] Meher, S., Hernandez-Andrade, E., Basheer, S.N., et al. Impact of cerebral redistribution on neurodevelopmental outcome in small-for-gestational-age or growth-restricted babies: a systematic review. Ultrasound Obstet Gynecol 46 (2015), 398–404.
71. [71] Oros, D., Figueras, F., Cruz-Martinez, R., et al. Middle versus anterior cerebral artery Doppler for the prediction of adverse outcome in term small-for-gestational-age fetuses. Ultrasound Obstet Gynecol 35 (2010), 456–461.
72. [72] 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 203:42 (2010), e1–e6.
73. [73] Baschat, A.A., Gembruch, U., Harman, C.R., The sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens. Ultrasound Obstet Gynecol 18 (2001), 571–577.
74. [74] 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 25 (2005), 573–579.
75. [75] Baschat, A.A., Gembruch, U., Weiner, C.P., et al. Qualitative venous Doppler waveform analysis improves prediction of critical perinatal outcomes in premature growth-restricted fetuses. Ultrasound Obstet Gynecol 22 (2003), 240–245.
76. [76] Fouron, J.C., Skoll, A., Sonesson, S.E., et al. Relationship between flow through the fetal aortic isthmus and cerebral oxygenation during acute placental circulatory insufficiency in ovine fetuses. Am J Obstet Gynecol 181 (1999), 1102–1107.
77. [77] Makikallio, K., Jouppila, P., Rasanen, J., Retrograde aortic isthmus net blood flow and human fetal cardiac function in placental insufficiency. Ultrasound Obstet Gynecol 22 (2003), 351–357.
78. [78] Del Rio, M., Martinez, J.M., Figueras, F., et al. Doppler assessment of the aortic isthmus and perinatal outcome in preterm fetuses with severe intrauterine growth restriction. Ultrasound Obstet Gynecol 31 (2008), 41–47.
79. [79] Fouron, J.C., Gosselin, J., Raboisson, M.J., 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 192 (2005), 497–503.
80. [80] 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 38 (2011), 400–405.
81. [81] 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 33 (2009), 39–43.
82. [82] Evertson, L.R., Gauthier, R.J., Schifrin, B.S., et al. Antepartum fetal heart rate testing. I. Evolution of the nonstress test. Am J Obstet Gynecol 133 (1979), 29–33.
83. [83] Pattison, N., McCowan, L., Cardiotocography for antepartum fetal assessment. Cochrane Database Syst Rev, 2000, CD001068.
84. [84] Kaur, S., Picconi, J.L., Chadha, R., et al. Biophysical profile in the treatment of intrauterine growth-restricted fetuses who weigh <1000 g. Am J Obstet Gynecol 199:264 (2008), e1–e4.
85. [85] Alfirevic, Z., Neilson, J.P., Biophysical profile for fetal assessment in high risk pregnancies. Cochrane Database Syst Rev, 2000, CD000038.
86. [86] Gulmezoglu, A.M., Hofmeyr, G.J., Plasma volume expansion for suspected impaired fetal growth. Cochrane Database Syst Rev, 2000, CD000167.
87. [87] Gulmezoglu, A.M., Hofmeyr, G.J., Betamimetics for suspected impaired fetal growth. Cochrane Database Syst Rev, 2001, CD000036.
88. [88] Laurin, J., Persson, P.H., The effect of bedrest in hospital on fetal outcome in pregnancies complicated by intra-uterine growth retardation. Acta Obstet Gynecol Scand 66 (1987), 407–411.
89. [89] Say, L., Gulmezoglu, A.M., Hofmeyr, G.J., Maternal nutrient supplementation for suspected impaired fetal growth. Cochrane Database Syst Rev, 2003, CD000148.
90. [90] Say, L., Gulmezoglu, A.M., Hofmeyr, G.J., Maternal oxygen administration for suspected impaired fetal growth. Cochrane Database Syst Rev, 2003, CD000137.
91. [91] Lees, C.C., Marlow, N., van Wassenaer-Leemhuis, A., et al. 2 year neurodevelopmental and intermediate perinatal outcomes in infants with very preterm fetal growth restriction (TRUFFLE): a randomised trial. Lancet 385 (2015, 30), 2162–2172.