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Chapter 18.2 - Intrauterine growth restriction

differential diagnosis and management

from Section 2 - Fetal disease

Published online by Cambridge University Press:  05 February 2013

Mark D. Kilby
Affiliation:
Department of Fetal Medicine, University of Birmingham
Anthony Johnson
Affiliation:
Baylor College of Medicine, Texas
Dick Oepkes
Affiliation:
Department of Obstetrics, Leiden University Medical Center
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Summary

Introduction

Intrauterine growth restriction (IUGR) is defined as failure of the fetus to achieve its biologically determined growth potential and is therefore likely due to an underlying pathological process [1]. The majority of cases of IUGR are discovered during the latter part of the third trimester and are caused by a degree of placental insufficiency and therefore generally have a good perinatal prognosis. However, a minority of cases of IUGR are diagnosed earlier as a result of severe placental insufficiency, or are due to some other cause and therefore require careful consideration of the likely diagnosis before a management plan can be developed.

To illustrate the potential difficulty in managing IUGR, a comprehensive differential diagnosis of maternal, fetal, placental, and genetic factors that may cause IUGR is summarized in Tables 18.2.1–18.2.4. The list expands with new knowledge, for example the recent demonstration of epigenetic dysregulation of specific genes in the placenta that may indirectly regulate fetal growth, such as WNT2 [9]. Identifying the underlying etiology of IUGR during the antepartum period is important both to reduce the rate of preventable perinatal losses, especially stillbirth of normally formed fetuses [10], and to avoid inappropriate delivery by Cesarean section for poor prognosis scenarios. Considerable advances in this area of perinatal medicine mean that increasing numbers of IUGR pregnancies are referred to maternal-fetal medicine centers for further assessment, such that increasingly accurate diagnoses are being made during the antenatal period; as such greater numbers of intact infants born with IUGR survive with careful intensive fetal monitoring, coordinated delivery, and optimal neonatal care [11].

Type
Chapter
Information
Fetal Therapy
Scientific Basis and Critical Appraisal of Clinical Benefits
, pp. 355 - 369
Publisher: Cambridge University Press
Print publication year: 2012

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References

Royal College of Obstetricians and Gynecologists. The Investigation and Management of the Small-for-Gestational Age Fetus. Guideline No. 31. London, RCOG, 2002.
American College of Obstetricians and Gynecologists. Intrauterine Growth Restriction. Practice Bulletin No. 12. Washington DC, ACOG, 2000.
Cunningham, FGLK, Bloom, SL, Hauth, JC, Gilstrap III, LC, Wenstrom, KD. Fetal Growth Disorders. Williams Obstetrics, 22nd edn. New York: McGraw Hill. 2001; 893–910.
Beck, B. Epidemiology of Cornelia de Lange’s syndrome. Acta Paediat Scand 1976;65(5):631–8.Google Scholar
Gicquel, C, Rossignol, S, Cabrol, S, et al. Epimutation of the telomeric imprinting center region on chromosome 11p15 in Silver-Russell syndrome. Nat Genet 2005;37(9):1003–7.Google Scholar
Psiachou, H, Mitton, S, Alaghband-Zadeh, J, et al. Leprechaunism and homozygous nonsense mutation in the insulin receptor gene. Lancet 1993;342(8876):924.Google Scholar
Grannum, PA, Berkowitz, RL, Hobbins, JC. The ultrasonic changes in the maturing placenta and their relation to fetal pulmonic maturity. Am J Obstet Gynecol 1979;133(8):915–22.Google Scholar
Proctor, LK, Whittle, WL, Keating, S, Viero, S, Kingdom, JC. Pathologic basis of echogenic cystic lesions in the human placenta: role of ultrasound-guided wire localization. Placenta 2010;31(12):1111–15.Google Scholar
Ferreira, JC, Choufani, S, Grafodatskaya, D, et al. WNT2 promoter methylation in human placenta is associated with low birthweight percentile in the neonate. Epigenetics 2011;6(4):440–9.Google Scholar
Smith, GC, Fretts, RC. Stillbirth. Lancet 2007;370(9600):1715–25.Google Scholar
Figueras, F, Gardosi, J. Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 2011;204(4):288–300.Google Scholar
Chauhan, SP, Magann, EF. Screening for fetal growth restriction. Clin Obstet Gynecol. 2006;49(2):284–94.Google Scholar
Gardosi, J. Customized fetal growth standards: rationale and clinical application. Semin Perinatol 2004;28(1):33–40.Google Scholar
Ego, A, Subtil, D, Grange, G, et al. Customized versus population-based birth weight standards for identifying growth restricted infants: a French multicenter study. Am J Obstet Gynecol 2006;194(4):1042–9.Google Scholar
Gardosi, J, Chang, A, Kalyan, B, Sahota, D, Symonds, EM. Customised antenatal growth charts. Lancet 1992;339(8788):283–7.Google Scholar
Clausson, B, Gardosi, J, Francis, A, Cnattingius, S. Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. BJOG 2001;108(8):830–4.Google Scholar
Gardosi, J, Francis, A. Controlled trial of fundal height measurement plotted on customised antenatal growth charts. Br J Obstet Gynaecol 1999;106(4):309–17.Google Scholar
Sciscione, AC, Gorman, R, Callan, NA. Adjustment of birth weight standards for maternal and infant characteristics improves the prediction of outcome in the small-for-gestational-age infant. Am J Obstet Gynecol 1996;175(3 Pt 1):544–7.Google Scholar
de Jong, CL, Gardosi, J, Dekker, GA, Colenbrander, GJ, van Geijn, HP. Application of a customised birthweight standard in the assessment of perinatal outcome in a high risk population. Br J Obstet Gynaecol 1998;105(5):531–5.Google Scholar
Maulik, D. Fetal growth compromise: definitions, standards, and classification. Clin Obstet Gynecol 2006;49(2):214–18.Google Scholar
Bamberg, C, Kalache, KD. Prenatal diagnosis of fetal growth restriction. Semin Fetal Neonatal Med 2004;9(5):387–94.Google Scholar
Campbell, S, Thoms, A. Ultrasound measurement of the fetal head to abdomen circumference ratio in the assessment of growth retardation. Br J Obstet Gynaecol 1977;84(3):165–74.Google Scholar
Dashe, JS, McIntire, DD, Lucas, MJ, Leveno, KJ. Effects of symmetric and asymmetric fetal growth on pregnancy outcomes. Obstet Gynecol 2000;96(3):321–7.Google Scholar
Nyberg, DA, Abuhamad, A, Ville, Y. Ultrasound assessment of abnormal fetal growth. Semin Perinatol 2004;28(1):3–22.Google Scholar
You, JJ, Alter, DA, Stukel, TA, et al. Proliferation of prenatal ultrasonography. CMAJ 2010;182(2):143–51.Google Scholar
Al Riyami, N, Walker, MG, Proctor, LK, et al. Utility of head/abdomen circumference ratio in the evaluation of severe early-onset intrauterine growth restriction. J Obstet Gynaecol Can 2011;33(7):715–19.Google Scholar
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):442–8.Google Scholar
Schoen, C, Rosen, T. Maternal and perinatal risks for women over 44 – a review. Maturitas 2009;64(2):109–13.Google Scholar
Creasy, RK, Resnik, R, Iams, JD, Lockwood, CJ, Moore, TR. Intrauterine Growth Restriction. Maternal Fetal Medicine, 5th edn. Philadelphia, WB Saunders. 2004; 569–84.
Presbitero, P, Somerville, J, Stone, S, et al. Pregnancy in cyanotic congenital heart disease. Outcome of mother and fetus. Circulation 1994;89(6):2673–6.Google Scholar
McDonald, SD, Han, Z, Mulla, S, et al. Preterm birth and low birth weight among in vitro fertilization singletons: a systematic review and meta-analyses. Eur J Obstet Gynecol Reprod Biol 2009;146(2):138–48.Google Scholar
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):731–7.Google Scholar
Helmerhorst, FM, Perquin, DA, Donker, D, Keirse, MJ. Perinatal outcome of singletons and twins after assisted conception: a systematic review of controlled studies. BMJ 2004;328(7434):261.Google Scholar
Howarth, C, Gazis, A, James, D. Associations of Type 1 diabetes mellitus, maternal vascular disease and complications of pregnancy. Diabetic Med 2007;24(11):1229–34.Google Scholar
Smyth, A, Oliveira, GH, Lahr, BD, et al. A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin J Am Soc Nephrol 2010;5(11):2060–8.Google Scholar
Steegers, EA, von Dadelszen, P, Duvekot, JJ, Pijnenborg, R. Pre-eclampsia. Lancet 2010;376(9741):631–44.Google Scholar
von Dadelszen, P, Ornstein, MP, Bull, SB, et al. Fall in mean arterial pressure and fetal growth restriction in pregnancy hypertension: a meta-analysis. Lancet 2000;355(9198):87–92.Google Scholar
Said, JM, Higgins, JR, Moses, EK, et al. Inherited thrombophilia polymorphisms and pregnancy outcomes in nulliparous women. Obstet Gynecol 2010;115(1):5–13.Google Scholar
Facco, F, You, W, Grobman, W. Genetic thrombophilias and intrauterine growth restriction: a meta-analysis. Obstet Gynecol 2009;113(6):1206–16.Google Scholar
Howley, HE, Walker, M, Rodger, MA. A systematic review of the association between factor V Leiden or prothrombin gene variant and intrauterine growth restriction. Am J Obstet Gynecol 2005;192(3):694–708.Google Scholar
Alfirevic, Z, Roberts, D, Martlew, V. How strong is the association between maternal thrombophilia and adverse pregnancy outcome? A systematic review. Eur J Obstet Gynecol Reprod Biol 2002;101(1):6–14.Google Scholar
Chakravarty, EF, Khanna, D, Chung, L. Pregnancy outcomes in systemic sclerosis, primary pulmonary hypertension, and sickle cell disease. Obstet Gynecol 2008;111(4):927–34.Google Scholar
Kujovich, JL. Thrombophilia and pregnancy complications. Am J Obstet Gynecol 2004;191(2):412–24.Google Scholar
Luewan, S, Srisupundit, K, Tongsong, T. Outcomes of pregnancies complicated by beta-thalassemia/hemoglobin E disease. Int J Gynaecol Obstet 2009;104(3):203–5.Google Scholar
Kingdom, JC, Drewlo, S. Is heparin a placental anticoagulant in high-risk pregnancies? Blood 2001;118(18):4780–8.Google Scholar
Mortola, JP, Frappell, PB, Aguero, L, Armstrong, K. Birth weight and altitude: a study in Peruvian communities. J Pediatr 2000;136(3):324–9.Google Scholar
Stein, AD, Lumey, LH. The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: the Dutch Famine Birth Cohort Study. Hum Biol 2000;72(4):641–54.Google Scholar
Khashan, AS, Henriksen, TB, Mortensen, PB, et al. The impact of maternal celiac disease on birthweight and preterm birth: a Danish population-based cohort study. Hum Reprod 2010;25(2):528–34.Google Scholar
Anjum, N, Baker, PN, Robinson, NJ, Aplin, JD. Maternal celiac disease autoantibodies bind directly to syncytiotrophoblast and inhibit placental tissue transglutaminase activity. Reprod Biol Endocrinol 2009;7:16.Google Scholar
Proud, J, Grant, AM. Third trimester placental grading by ultrasonography as a test of fetal wellbeing. Br Med J (Clin Res Ed) 1987;294(6588):1641–4.Google Scholar
Cooley, SM, Donnelly, JC, Walsh, T, et al. The impact of ultrasonographic placental architecture on antenatal course, labor and delivery in a low-risk primigravid population. J Matern Fetal Neonatal Med 2010;24(3):493–7.Google Scholar
McCowan, LM, Dekker, GA, Chan, E, et al. Spontaneous preterm birth and small for gestational age infants in women who stop smoking early in pregnancy: prospective cohort study. BMJ 2009;338:b1081.Google Scholar
Royal College of Obstetricians and Gynaecologists. Alcohol consumption and the outcomes of pregnancy. RCOG Statement No. 5. March 2006.Google Scholar
Meyer-Leu, Y, Lemola, S, Daeppen, JB, Deriaz, O, Gerber, S. Association of moderate alcohol use and binge drinking during pregnancy with neonatal health. Alcohol Clin Exp Res 2011;35(9):1669–77.Google Scholar
Mills, JL, Graubard, BI, Harley, EE, Rhoads, GG, Berendes, HW. Maternal alcohol consumption and birth weight. How much drinking during pregnancy is safe? JAMA 1984;252(14):1875–9.Google Scholar
Richardson, S, Browne, ML, Rasmussen, SA, et al. Associations between periconceptional alcohol consumption and craniosynostosis, omphalocele, and gastroschisis. Birth Defects Res A Clin Mol Teratol 2011;91(7):623–30.Google Scholar
Gundogan, F, Elwood, G, Longato, L, et al. Impaired placentation in fetal alcohol syndrome. Placenta 2008;29(2):148–57.Google Scholar
Smith, LM, Lagasse, LL, Derauf, C, et al. Prenatal methamphetamine use and neonatal neurobehavioral outcome. Neurotoxicol Teratol 2008;30(1):20–8.Google Scholar
Naeye, RL, Blanc, W, Leblanc, W, Khatamee, MA. Fetal complications of maternal heroin addiction: abnormal growth, infections, and episodes of stress. J Pediatr 1973;83(6):1055–61.Google Scholar
Bada, HS, Das, A, Bauer, CR, et al. Low birth weight and preterm births: etiologic fraction attributable to prenatal drug exposure. J Perinatol 2005;25(10):631–7.Google Scholar
Toh, S, Mitchell, AA, Louik, C, et al. Antidepressant use during pregnancy and the risk of preterm delivery and fetal growth restriction. J Clin Psychopharmacol 2009;29(6):555–60.Google Scholar
Wen, SW, Zhou, J, Yang, Q, et al. Maternal exposure to folic acid antagonists and placenta-mediated adverse pregnancy outcomes. CMAJ 2008;179(12):1263–8.Google Scholar
Sassoon, DA, Castro, LC, Davis, JL, Hobel, CJ. Perinatal outcome in triplet versus twin gestations. Obstet Gynecol 1990;75(5):817–20.Google Scholar
Zhu, BP, Rolfs, RT, Nangle, BE, Horan, JM. Effect of the interval between pregnancies on perinatal outcomes. N Engl J Med 1999;340(8):589–94.Google Scholar
Khashan, AS, Baker, PN, Kenny, LC. Preterm birth and reduced birthweight in first and second teenage pregnancies: a register-based cohort study. BMC Pregnancy Childbirth 2010;10:36.Google Scholar
Lee, KS, Ferguson, RM, Corpuz, M, Gartner, LM. Maternal age and incidence of low birth weight at term: a population study. Am J Obstet Gynecol 1988;158(1):84–9.Google Scholar
Ananth, CV, Kaminsky, L, Getahun, D, Kirby, RS, Vintzileos, AM. Recurrence of fetal growth restriction in singleton and twin gestations. J Matern Fetal Neonatal Med 2009;22(8):654–61.Google Scholar
Snijders, RJ, Sherrod, C, Gosden, CM, Nicolaides, KH. Fetal growth retardation: associated malformations and chromosomal abnormalities. Am J Obstet Gynecol 1993;168(2):547–55.Google Scholar
Khoury, MJ, Erickson, JD, Cordero, JF, McCarthy, BJ. Congenital malformations and intrauterine growth retardation: a population study. Pediatrics 1988;82(1):83–90.Google Scholar
Rochelson, B, Kaplan, C, Guzman, E, et al. A quantitative analysis of placental vasculature in the third-trimester fetus with autosomal trisomy. Obstet Gynecol 1990;75(1):59–63.Google Scholar
Fujimoto, A, Wilson, MG. Growth retardation in Wolf-Hirschhorn syndrome. Hum Genet 1990;84(3):296–7.Google Scholar
Wollmann, HA, Kirchner, T, Enders, H, Preece, MA, Ranke, MB. Growth and symptoms in Silver-Russell syndrome: review on the basis of 386 patients. Eur J Pediatr 1995;154(12):958–68.Google Scholar
Raynor, BD, Richards, D. Growth retardation in fetuses with gastroschisis. J Ultrasound Med 1997;16(1):13–16.Google Scholar
Alexander, GR, Kogan, M, Martin, J, Papiernik, E. What are the fetal growth patterns of singletons, twins, and triplets in the United States? Clin Obstet Gynecol 1998;41(1):114–25.Google Scholar
Kent, EM, Breathnach, FM, Gillan, JE, et al. Placental cord insertion and birthweight discordance in twin pregnancies: results of the national prospective ESPRiT study. Am J Obstet Gynecol 2011;205(4):376.e1–7.Google Scholar
Yinon, Y, Mazkereth, R, Rosentzweig, N, et al. Growth restriction as a determinant of outcome in preterm discordant twins. Obstet Gynecol 2005;105(1):80–4.Google Scholar
Abdel-Fattah, SA, Bhat, A, Illanes, S, Bartha, JL, Carrington, D. TORCH test for fetal medicine indications: only CMV is necessary in the United Kingdom. Prenat Diagn 2005;25(11):1028–31.Google Scholar
Umbers, AJ, Boeuf, P, Clapham, C, et al. Placental malaria-associated inflammation disturbs the insulin-like growth factor axis of fetal growth regulation. J Infect Dis 2011;203(4):561–9.Google Scholar
McCarthy, FP, Giles, ML, Rowlands, S, Purcell, KJ, Jones, CA. Antenatal interventions for preventing the transmission of cytomegalovirus (CMV) from the mother to fetus during pregnancy and adverse outcomes in the congenitally infected infant. Cochrane Database Syst Rev 2011;(3):CD008371.Google Scholar
Germain, M, Krohn, MA, Hillier, SL, Eschenbach, DA. Genital flora in pregnancy and its association with intrauterine growth retardation. J Clin Microbiol 1994;32(9):2162–8.Google Scholar
Baboonian, C, Smith, DA, Shapland, D, et al. Placental infection with Chlamydia pneumoniae and intrauterine growth restriction. Cardiovasc Res 2003;60(1):165–9.Google Scholar
Lausman, AMF, Walker, M, Kingdom, J. Screening, diagnosis and management of intrauterine growth restriction. J Obstet Gynaecol Can 2012;34(1):17–28.Google Scholar
Rijhsinghani, A, Yankowitz, J, Strauss, RA, et al. Risk of preeclampsia in second-trimester triploid pregnancies. Obstet Gynecol 1997;90(6):884–8.Google Scholar
Abdel-Fattah, SA, Bhat, A, Illanes, S, Bartha, JL, Carrington, D. TORCH test for fetal medicine indications: only CMV is necessary in the United Kingdom. Prenat Diagn 2005;25(11):1028–31.Google Scholar
Rosenthal, GL, Wilson, PD, Permutt, T, Boughman, JA, Ferencz, C. Birth weight and cardiovascular malformations: a population-based study. The Baltimore-Washington Infant Study. Am J Epidemiol 1991;133(12):1273–81.Google Scholar
Ellis, C, Pymar, H, Windrim, R, Keating, S, Kingdom, J. A puzzling intrauterine death: non-compaction of the fetal ventricular myocardium presenting with reversed end-diastolic flow velocity in the umbilical arteries. J Obstet Gynaecol Can 2005;27(7):695–8.Google Scholar
Franco, C, Walker, M, Robertson, J, et al. Placental infarction and thrombophilia. Obstet Gynecol 2011;117(4):929–34.Google Scholar
Reeves, S, Bernstein, I. Effects of maternal tobacco-smoke exposure on fetal growth and neonatal size. Expert Rev Obstet Gynecol 2008;3(6):719–30.Google Scholar
Gulmezoglu, M, de Onis, M, Villar, J. Effectiveness of interventions to prevent or treat impaired fetal growth. Obstet Gynecol Surv 1997;52(2):139–49.Google Scholar
Dolan-Mullen, P, Ramirez, G, Groff, JY. A meta-analysis of randomized trials of prenatal smoking cessation interventions. Am J Obstet Gynecol 1994;171(5):1328–34.Google Scholar
Mitani, M, Matsuda, Y, Makino, Y, Akizawa, Y, Ohta, H. Clinical features of fetal growth restriction complicated later by preeclampsia. J Obstet Gynaecol Res 2009;35(5):882–7.Google Scholar
Proctor, LK, Toal, M, Keating, S, et al. Placental size and the prediction of severe early-onset intrauterine growth restriction in women with low pregnancy-associated plasma protein-A. Ultrasound Obstet Gynecol 2009;34(3):274–82.Google Scholar
Toal, M, Keating, S, Machin, G, et al. Determinants of adverse perinatal outcome in high-risk women with abnormal uterine artery Doppler images. Am J Obstet Gynecol 2008;198(3):330e1–7.Google Scholar
Manning, FA. Fetal biophysical profile: a critical appraisal. Clin Obstet Gynecol 2002;45(4):975–85.Google Scholar
Nicolaides, KH, Peters, MT, Vyas, S, et al. Relation of rate of urine production to oxygen tension in small-for-gestational-age fetuses. Am J Obstet Gynecol 1990;162(2):387–91.Google Scholar
Dayal, AK, Manning, FA, Berck, DJ, et al. Fetal death after normal biophysical profile score: an eighteen-year experience. Am J Obstet Gynecol 1999;181(5 Pt 1):1231–6.Google Scholar
Grivell, RM, Alfirevic, Z, Gyte, GM, Devane, D. Antenatal cardiotocography for fetal assessment. Cochrane Database Syst Rev 2010;(1):CD007863.Google Scholar
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):1254–8.Google Scholar
Maulik, D, Mundy, D, Heitmann, E. Evidence-based approach to umbilical artery Doppler fetal surveillance in high-risk pregnancies: an update. Clin Obstet Gynecol 2010;53(4):869–78.Google Scholar
Krebs, C, Macara, LM, Leiser, R, et al. Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree. Am J Obstet Gynecol 1996;175(6):1534–42.Google Scholar
Saleemuddin, A, Tantbirojn, P, Sirois, K, et al. Obstetric and perinatal complications in placentas with fetal thrombotic vasculopathy. Pediatr Dev Pathol 2010;13(6):459–64.Google Scholar
Cruz-Martinez, R, Figueras, F, Benavides-Serralde, A, et al. Sequence of changes in myocardial performance index in relation with aortic isthmus and ductus venosus Doppler in fetuses with early-onset intrauterine growth restriction. Ultrasound Obstet Gynecol 2011;38(2):179–84.Google Scholar
Skoll, MA, Fouron, JC, Sonesson, SE, et al. Doppler velocimetric indices from the abdominal and placental ends of the umbilical artery of growth-restricted fetuses. J Clin Ultrasound 1997;25(8):421–4.Google Scholar
Baschat, AA, Viscardi RM, Hussey-Gardner B, Hashmi N, Harman C. Infant neurodevelopment following fetal growth restriction: relationship with antepartum surveillance parameters. Ultrasound Obstet Gynecol 2009;33(1):44–50.Google Scholar
Baschat, AA, Cosmi, E, Bilardo, CM, et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol 2007;109(2 Pt 1):253–61.Google Scholar
Hecher, K, Campbell, S, Doyle, P, Harrington, K, Nicolaides, K. Assessment of fetal compromise by Doppler ultrasound investigation of the fetal circulation. Arterial, intracardiac, and venous blood flow velocity studies. Circulation 1995;91(1):129–38.Google Scholar
Mari, G, Hanif, F, Kruger, M, et al. Middle cerebral artery peak systolic velocity: a new Doppler parameter in the assessment of growth-restricted fetuses. Ultrasound Obstet Gynecol 2007;29(3):310–16.Google Scholar
Cruz-Martinez, R, Figueras, F, Hernandez-Andrade, E, Oros, D, Gratacos E. Fetal brain Doppler to predict cesarean delivery for nonreassuring fetal status in term small-for-gestational-age fetuses. Obstet Gynecol 2011;117(3):618–26.Google Scholar
Francisco, RP, Miyadahira, S, Zugaib, M. Predicting pH at birth in absent or reversed end-diastolic velocity in the umbilical arteries. Obstet Gynecol 2006;107(5):1042–8.Google Scholar
Boers, KE, Vijgen, SM, Bijlenga, D, et al. Induction versus expectant monitoring for intrauterine growth restriction at term: randomised equivalence trial (DIGITAT). BMJ 2010;341:c7087.Google Scholar
Hershkovitz, R, Kingdom, JC, Geary, M, Rodeck, CH. 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):209–12.Google Scholar
Walker, MG, Hindmarsh, PC, Geary, M, Kingdom, JC. Sonographic maturation of the placenta at 30 to 34 weeks is not associated with second trimester markers of placental insufficiency in low-risk pregnancies. J Obstet Gynaecol Can 2010;32(12):1134–9.Google Scholar
Group, GRIT Study. A randomised trial of timed delivery for the compromised preterm fetus: short term outcomes and Bayesian interpretation. BJOG 2003;110(1):27–32.Google Scholar
Thornton, JG, Hornbuckle, J, Vail, A, Spiegelhalter, DJ, Levene, M. Infant wellbeing at 2 years of age in the Growth Restriction Intervention Trial (GRIT): multicentred randomised controlled trial. Lancet 2004;364(9433):513–20.Google Scholar
Bujold, E, Morency, AM, Roberge, S, et al. Acetylsalicylic acid for the prevention of preeclampsia and intra-uterine growth restriction in women with abnormal uterine artery Doppler: a systematic review and meta-analysis. J Obstet Gynaecol Can 2009;31(9):818–26.Google Scholar
Dodd, JM, McLeod, A, Windrim, RC, Kingdom, J. Antithrombotic therapy for improving maternal or infant health outcomes in women considered at risk of placental dysfunction. Cochrane Database Syst Rev 2010;(6):CD006780.Google Scholar
Kingdom, JC, Walker, M, Proctor, LK, et al. Unfractionated heparin for second trimester placental insufficiency: a pilot randomized trial. J Thromb Haemost 2011;9(8):1483–92.Google Scholar
Lees, C, Valensise, H, Black, R, et al. The efficacy and fetal-maternal cardiovascular effects of transdermal glyceryl trinitrate in the prophylaxis of pre-eclampsia and its complications: a randomized double-blind placebo-controlled trial. Ultrasound Obstet Gynecol 1998;12(5):334–8.Google Scholar
Winer, N, Branger, B, Azria, E, et al. L-Arginine treatment for severe vascular fetal intrauterine growth restriction: a randomized double-bind controlled trial. Clin Nutr 2009;28(3):243–8.Google Scholar
von Dadelszen, P, Dwinnell, S, Magee, LA, et al. Sildenafil citrate therapy for severe early-onset intrauterine growth restriction. BJOG 2011;118(5):624–8.Google Scholar
Simchen, MJ, Alkazaleh, F, Adamson, SL, et al. The fetal cardiovascular response to antenatal steroids in severe early-onset intrauterine growth restriction. Am J Obstet Gynecol 2004;190(2):296–304.Google Scholar
Say, L, Gulmezoglu, AM, Hofmeyr, GJ. Maternal oxygen administration for suspected impaired fetal growth. Cochrane Database Syst Rev 2003;(1):CD000137.Google Scholar
Thadhani, R, Kisner, T, Hagmann, H, et al. Pilot study of extracorporeal removal of soluble Fms-like tyrosine kinase 1 in preeclampsia. Circulation 2011;124(8):940–50.Google Scholar
Royal College of Obstetricians and Gynaecologists. Reducing the Risk of Thrombosis and Embolism during Pregnancy and the Puerperium (Green-top 37a). London, RCOG, 2009.
Moldenhauer, JS, Stanek, J, Warshak, C, Khoury, J, Sibai, B. The frequency and severity of placental findings in women with preeclampsia are gestational age dependent. Am J Obstet Gynecol 2003;189(4):1173–7.Google Scholar
Toal, M, Chan, C, Fallah, S, et al. Usefulness of a placental profile in high-risk pregnancies. Am J Obstet Gynecol 2007;196(4):363e1–7.Google Scholar
Ray, JG, Vermeulen, MJ, Schull, MJ, Redelmeier, DA. Cardiovascular health after maternal placental syndromes (CHAMPS): population-based retrospective cohort study. Lancet 2005;366(9499):1797–803.Google Scholar
Staff, AC, Dechend, R, Pijnenborg, R. Learning from the placenta: acute atherosis and vascular remodeling in preeclampsia – novel aspects for atherosclerosis and future cardiovascular health. Hypertension 2010;56(6):1026–34.Google Scholar
Lausman, AY, Kingdom, JC, Bradley, TJ, Slorach, C, Ray, JG. Subclinical atherosclerosis in association with elevated placental vascular resistance in early pregnancy. Atherosclerosis 2009;206(1):33–5.Google Scholar
Yinon, Y, Kingdom, JC, 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):1846–53.Google Scholar

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Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

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Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

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