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Review Article| Volume 30, ISSUE 3, P727-746, September 2010

First- and Second-Trimester Screening for Preeclampsia and Intrauterine Growth Restriction

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      References

        • McIntire D.D.
        • Bloom S.L.
        • Casey B.M.
        • et al.
        Birth weight in relation to morbidity and mortality among newborn infants.
        N Engl J Med. 1999; 340: 1234-1238
        • Kaufmann P.
        • Black S.
        • Huppertz B.
        Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia.
        Biol Reprod. 2003; 69: 1-7
        • Roberts J.M.
        • Cooper D.W.
        Pathogenesis and genetics of pre-eclampsia.
        Lancet. 2001; 357: 53-56
        • Caniggia I.
        • Winter J.
        • Lye S.J.
        • et al.
        Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia.
        Placenta. 2000; 21: S25-S30
        • Scifres C.M.
        • Nelson D.M.
        Intrauterine growth restriction, human placental development and trophoblast cell death.
        J Physiol. 2009; 587: 3453-3458
        • Burton G.J.
        • Woods A.W.
        • Jauniaux E.
        • et al.
        Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy.
        Placenta. 2009; 30: 473-482
        • Roberts J.M.
        • Taylor R.N.
        • Musci T.J.
        • et al.
        Preeclampsia: an endothelial cell disorder.
        Am J Obstet Gynecol. 1989; 161: 1200-1204
        • Hsu C.D.
        • Iriye B.
        • Johnson T.R.
        • et al.
        Elevated circulating thrombomodulin in severe preeclampsia.
        Am J Obstet Gynecol. 1993; 169: 148-149
        • Mills J.L.
        • DerSimonian R.
        • Raymond E.
        • et al.
        Prostacyclin and thromboxane changes predating clinical onset of preeclampsia: a multicenter prospective study.
        JAMA. 1999; 282: 356-362
        • Taylor R.N.
        • Crombleholme W.R.
        • Friedman S.A.
        • et al.
        High plasma cellular fibronectin levels correlate with biochemical and clinical features of preeclampsia but cannot be attributed to hypertension alone.
        Am J Obstet Gynecol. 1991; 165: 895-901
        • Vatten L.J.
        • Skjaerven R.
        Is pre-eclampsia more than one disease?.
        BJOG. 2004; 111: 298-302
        • Moldenhauer J.S.
        • Stanek J.
        • Warshak C.
        • et al.
        The frequency and severity of placental findings in women with preeclampsia are gestational age dependent.
        Am J Obstet Gynecol. 2003; 189: 1173-1177
        • Egbor M.
        • Ansari T.
        • Morris N.
        • et al.
        Morphometric placental villous and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction.
        BJOG. 2006; 113: 580-589
        • Melchiorre K.
        • Wormald B.
        • Leslie K.
        • et al.
        First-trimester uterine artery Doppler indices in term and preterm pre-eclampsia.
        Ultrasound Obstet Gynecol. 2008; 32: 133-137
        • von Dadelszen P.
        • Magee L.A.
        • Roberts J.M.
        Subclassification of preeclampsia.
        Hypertens Pregnancy. 2003; 22: 143-148
      1. Schulz K.F. Grimes D.A. The Lancet handbook of essential concepts in clinical research. Elsevier, Philadelphia (PA)2006: 79
        • Jaeschke R.
        • Guyatt G.H.
        • Sackett D.L.
        Users' guides to the medical literature. III. How to use an article about a diagnostic test. B. What are the results and will they help me in caring for my patients? The Evidence-Based Medicine Working Group.
        JAMA. 1994; 271: 703-707
        • Villar J.
        • Say L.
        • Shennan A.
        • et al.
        Methodological and technical issues related to the diagnosis, screening, prevention, and treatment of pre-eclampsia and eclampsia.
        Int J Gynaecol Obstet. 2004; 85: S28-S41
      2. Lindheimer M.D. Roberts J.M. Cunningham F.G. Chesley's hypertensive disorders in pregnancy. 3rd edition. Elsevier, Oxford (UK)2009
        • Lang T.A.
        • Secic M.
        How to report statistics in medicine.
        American College of Physicians, Philadelphia1997
      3. Riegelman R.K. Hirsch R. Studying a study and testing a test. 2nd edition. Little, Brown and Co, Boston1987
        • Farag K.
        • Hassan I.
        • Ledger W.L.
        Prediction of preeclampsia: can it be achieved?.
        Obstet Gynecol Surv. 2004; 59 ([quiz: 485]): 464-482
        • Conde-Agudelo A.
        • Villar J.
        • Lindheimer M.
        World Health Organization systematic review of screening tests for preeclampsia.
        Obstet Gynecol. 2004; 104: 1367-1391
        • Pilalis A.
        • Souka A.P.
        • Antsaklis P.
        • 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: 135-140
        • 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 (e1–7): 330
        • 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. 2008; 178: 701-711
        • Conde-Agudelo A.
        • Lindheimer M.
        Use of Doppler ultrasonography to predict pre-eclampsia.
        CMAJ. 2008; 179 ([author reply: 53–4]): 53
        • Pretorius D.H.
        • Nelson T.R.
        • Baergen R.N.
        • et al.
        Imaging of placental vasculature using three-dimensional ultrasound and color power Doppler: a preliminary study.
        Ultrasound Obstet Gynecol. 1998; 12: 45-49
        • Konje J.C.
        • Huppertz B.
        • Bell S.C.
        • et al.
        3-dimensional colour power angiography for staging human placental development.
        Lancet. 2003; 362: 1199-1201
        • Hafner E.
        • Metzenbauer M.
        • Höfinger D.
        • et al.
        Comparison between three-dimensional placental volume at 12 weeks and uterine artery impedance/notching at 22 weeks in screening for pregnancy-induced hypertension, pre-eclampsia and fetal growth restriction in a low-risk population.
        Ultrasound Obstet Gynecol. 2006; 27: 652-657
        • Rizzo G.
        • Capponi A.
        • Pietrolucci M.E.
        • et al.
        Effects of maternal cigarette smoking on placental volume and vascularization measured by 3-dimensional power Doppler ultrasonography at 11 + 0 to 13 + 6 weeks of gestation.
        Am J Obstet Gynecol. 2009; 200 (e1–5): 415
        • Matijevic R.
        • Kurjak A.
        The assessment of placental blood vessels by three-dimensional power Doppler ultrasound.
        J Perinat Med. 2002; 30: 26-32
        • Merce L.T.
        • Barco M.J.
        • Bau S.
        Reproducibility of the study of placental vascularization by three-dimensional power Doppler.
        J Perinat Med. 2004; 32: 228-233
        • Tuuli M.G.
        • Houser M.
        • Odibo L.
        • et al.
        Validation of placental vascular sonobiopsy for obtaining representative placental vascular indices by three-dimensionalpower Doppler ultrasonography.
        Placenta. 2010; 31: 192-196
        • Merce L.T.
        • Barco M.J.
        • Bau S.
        • et al.
        Assessment of placental vascularization by three-dimensional power Doppler “vascular biopsy” in normal pregnancies.
        Croat Med J. 2005; 46: 765-771
        • Noguchi J.
        • Hata K.
        • Tanaka H.
        • et al.
        Placental vascular sonobiopsy using three-dimensional power Doppler ultrasound in normal and growth restricted fetuses.
        Placenta. 2009; 30: 391-397
        • Guiot C.
        • Gaglioti P.
        • Oberto M.
        • et al.
        Is three-dimensional power Doppler ultrasound useful in the assessment of placental perfusion in normal and growth-restricted pregnancies?.
        Ultrasound Obstet Gynecol. 2008; 31: 171-176
        • Raine-Fenning N.J.
        • Welsh A.W.
        • Jones N.W.
        • et al.
        Methodological considerations for the correct application of quantitative three-dimensional power Doppler angiography.
        Ultrasound Obstet Gynecol. 2008; 32 ([author reply: 117–8]): 115-117
        • Raine-Fenning N.J.
        • Nordin N.M.
        • Ramnarine K.V.
        • et al.
        Determining the relationship between three-dimensional power Doppler data and true blood flow characteristics: an in-vitro flow phantom experiment.
        Ultrasound Obstet Gynecol. 2008; 32: 540-550
        • Raine-Fenning N.J.
        • Nordin N.M.
        • Ramnarine K.V.
        • et al.
        Evaluation of the effect of machine settings on quantitative three-dimensional power Doppler angiography: an in-vitro flow phantom experiment.
        Ultrasound Obstet Gynecol. 2008; 32: 551-559
        • Schulten-Wijman M.J.
        • Struijk P.C.
        • Brezinka C.
        • et al.
        Evaluation of volume vascularization index and flow index: a phantom study.
        Ultrasound Obstet Gynecol. 2008; 32: 560-564
        • Viero S.
        • Chaddha V.
        • Alkazaleh F.
        • et al.
        Prognostic value of placental ultrasound in pregnancies complicated by absent end-diastolic flow velocity in the umbilical arteries.
        Placenta. 2004; 25: 735-741
        • Toal M.
        • Chan C.
        • Fallah S.
        • et al.
        Usefulness of a placental profile in high-risk pregnancies.
        Am J Obstet Gynecol. 2007; 196 (e1–7): 363
        • Redman C.W.
        Current topic: pre-eclampsia and the placenta.
        Placenta. 1991; 12: 301-308
        • Thomas R.L.
        • Blakemore K.J.
        Evaluation of elevations in maternal serum alpha-fetoprotein: a review.
        Obstet Gynecol Surv. 1990; 45: 269-283
        • Costa S.L.
        • Proctor L.
        • Dodd J.M.
        • et al.
        Screening for placental insufficiency in high-risk pregnancies: is earlier better?.
        Placenta. 2008; 29: 1034-1040
        • Cindrova-Davies T.
        • Spasic-Boskovic O.
        • Jauniaux E.
        • et al.
        Nuclear factor-kappa B, p38, and stress-activated protein kinase mitogen-activated protein kinase signaling pathways regulate proinflammatory cytokines and apoptosis in human placental explants in response to oxidative stress: effects of antioxidant vitamins.
        Am J Pathol. 2007; 170: 1511-1520
        • Hung T.H.
        • Charnock-Jones D.S.
        • Skepper J.N.
        • et al.
        Secretion of tumor necrosis factor-alpha from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation in vitro: a potential mediator of the inflammatory response in preeclampsia.
        Am J Pathol. 2004; 164: 1049-1061
        • Tjoa M.L.
        • Cindrova-Davies T.
        • Spasic-Boskovic O.
        • et al.
        Trophoblastic oxidative stress and the release of cell-free feto-placental DNA.
        Am J Pathol. 2006; 169: 400-404
        • Redman C.W.
        Platelets and the beginnings of preeclampsia.
        N Engl J Med. 1990; 323: 478-480
        • Bosio P.M.
        • Cannon S.
        • McKenna P.J.
        • et al.
        Plasma P-selectin is elevated in the first trimester in women who subsequently develop pre-eclampsia.
        BJOG. 2001; 108: 709-715
        • Morris R.K.
        • Cnossen J.S.
        • Langejans M.
        • et al.
        Serum screening with Down's syndrome markers to predict pre-eclampsia and small for gestational age: systematic review and meta-analysis.
        BMC Pregnancy Childbirth. 2008; 8: 33
        • Ito N.
        • Nomura S.
        • Iwase A.
        • et al.
        ADAMs, a disintegrin and metalloproteinases, mediate shedding of oxytocinase.
        Biochem Biophys Res Commun. 2004; 314: 1008-1013
        • Iba K.
        • Albrechtsen R.
        • Gilpin B.
        • et al.
        The cysteine-rich domain of human ADAM 12 supports cell adhesion through syndecans and triggers signaling events that lead to beta1 integrin-dependent cell spreading.
        J Cell Biol. 2000; 149: 1143-1156
        • Laigaard J.
        • Sørensen T.
        • Placing S.
        • et al.
        Reduction of the disintegrin and metalloprotease ADAM12 in preeclampsia.
        Obstet Gynecol. 2005; 106: 144-149
        • Spencer K.
        • Cowans N.J.
        • Stamatopoulou A.
        ADAM12s in maternal serum as a potential marker of pre-eclampsia.
        Prenat Diagn. 2008; 28: 212-216
        • Cowans N.J.
        • Spencer K.
        First-trimester ADAM12 and PAPP-A as markers for intrauterine fetal growth restriction through their roles in the insulin-like growth factor system.
        Prenat Diagn. 2007; 27: 264-271
        • Poon L.C.
        • Chelemen T.
        • Granvillano O.
        • et al.
        First-trimester maternal serum a disintegrin and metalloprotease 12 (ADAM12) and adverse pregnancy outcome.
        Obstet Gynecol. 2008; 112: 1082-1090
        • Nicolaides K.H.
        • Bindra R.
        • Turan O.M.
        • 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: 13-17
        • Chafetz I.
        • Kuhnreich I.
        • Sammar M.
        • et al.
        First-trimester placental protein 13 screening for preeclampsia and intrauterine growth restriction.
        Am J Obstet Gynecol. 2007; 197 (e1–7): 35
        • Sekizawa A.
        • Sekizawa A.
        • Purwosunu Y.
        • et al.
        PP13 mRNA expression in trophoblasts from preeclamptic placentas.
        Reprod Sci. 2009; 16: 408-413
        • Cowans N.J.
        • Spencer K.
        • Meiri H.
        First-trimester maternal placental protein 13 levels in pregnancies resulting in adverse outcomes.
        Prenat Diagn. 2008; 28: 121-125
        • Romero R.
        • Kusanovic J.P.
        • Than N.G.
        • et al.
        First-trimester maternal serum PP13 in the risk assessment for preeclampsia.
        Am J Obstet Gynecol. 2008; 199 (e1–11): 122
        • Gonen R.
        • Shahar R.
        • Grimpel Y.I.
        • et al.
        Placental protein 13 as an early marker for pre-eclampsia: a prospective longitudinal study.
        BJOG. 2008; 115: 1465-1472
        • Huppertz B.
        • Sammar M.
        • Chefetz I.
        • et al.
        Longitudinal determination of serum placental protein 13 during development of preeclampsia.
        Fetal Diagn Ther. 2008; 24: 230-236
        • Akolekar R.
        • Syngelaki A.
        • Beta J.
        • et al.
        Maternal serum placental protein 13 at 11–13 weeks of gestation in preeclampsia.
        Prenat Diagn. 2009; 29: 1103-1108
        • Maynard S.
        • Epstein F.H.
        • Karumanchi S.A.
        Preeclampsia and angiogenic imbalance.
        Annu Rev Med. 2008; 59: 61-78
        • Powers R.W.
        • Roberts J.M.
        • Cooper K.M.
        • et al.
        Maternal serum soluble fms-like tyrosine kinase 1 concentrations are not increased in early pregnancy and decrease more slowly postpartum in women who develop preeclampsia.
        Am J Obstet Gynecol. 2005; 193: 185-191
        • Maynard S.E.
        • Min J.Y.
        • Merchan J.
        • et al.
        Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia.
        J Clin Invest. 2003; 111: 649-658
        • Sugimoto H.
        • Hamano Y.
        • Charytan D.
        • et al.
        Neutralization of circulating vascular endothelial growth factor (VEGF) by anti-VEGF antibodies and soluble VEGF receptor 1 (sFlt-1) induces proteinuria.
        J Biol Chem. 2003; 278: 12605-12608
        • Taylor R.N.
        • Grimwood J.
        • Taylor R.S.
        • et al.
        Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies.
        Am J Obstet Gynecol. 2003; 188: 177-182
        • 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: 303-309
        • Thadhani R.
        • Mutter W.P.
        • Wolf M.
        • et al.
        First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia.
        J Clin Endocrinol Metab. 2004; 89: 770-775
        • Teixeira P.G.
        • Cabral A.C.
        • Andrade S.P.
        • et al.
        Placental growth factor (PlGF) is a surrogate marker in preeclamptic hypertension.
        Hypertens Pregnancy. 2008; 27: 65-73
        • Lam C.
        • Lim K.H.
        • Karumanchi S.A.
        Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia.
        Hypertension. 2005; 46: 1077-1085
        • Moore Simas T.A.
        • Crawford S.L.
        • Solitro M.J.
        • et al.
        Angiogenic factors for the prediction of preeclampsia in high-risk women.
        Am J Obstet Gynecol. 2007; 197 (e1–8): 244
        • Akolekar R.
        • Zaragoza E.
        • Poon L.C.
        • et al.
        Maternal serum placental growth factor at 11 + 0 to 13 + 6 weeks of gestation in the prediction of pre-eclampsia.
        Ultrasound Obstet Gynecol. 2008; 32: 732-739
        • Kusanovic J.P.
        • Romero R.
        • Chaiworapongsa T.
        • et al.
        A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia.
        J Matern Fetal Neonatal Med. 2009; 22: 1021-1038
        • Savvidou M.D.
        • Akolekar R.
        • Zaragoza E.
        • et al.
        First trimester urinary placental growth factor and development of pre-eclampsia.
        BJOG. 2009; 116: 643-647
        • Rana S.
        • Karumanchi S.A.
        • Levine R.J.
        • et al.
        Sequential changes in antiangiogenic factors in early pregnancy and risk of developing preeclampsia.
        Hypertension. 2007; 50: 137-142
        • Signore C.
        • Mills J.L.
        • Qian C.
        • et al.
        Circulating soluble endoglin and placental abruption.
        Prenat Diagn. 2008; 28: 852-858
        • Baumann M.U.
        • Bersinger N.A.
        • Mohaupt M.G.
        • et al.
        First-trimester serum levels of soluble endoglin and soluble fms-like tyrosine kinase-1 as first-trimester markers for late-onset preeclampsia.
        Am J Obstet Gynecol. 2008; 199 (e1–6): 266
        • Hsu-Lin S.
        • Berman C.L.
        • Furie B.C.
        • et al.
        A platelet membrane protein expressed during platelet activation and secretion. Studies using a monoclonal antibody specific for thrombin-activated platelets.
        J Biol Chem. 1984; 259: 9121-9126
        • Larsen E.
        • Celi A.
        • Gilbert G.E.
        • et al.
        PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes.
        Cell. 1989; 59: 305-312
        • Halim A.
        • Kanayama N.
        • el Maradny E.
        • et al.
        Plasma P selectin (GMP-140) and glycocalicin are elevated in preeclampsia and eclampsia: their significances.
        Am J Obstet Gynecol. 1996; 174: 272-277
        • Banzola I.
        • Farina A.
        • Concu M.
        • et al.
        Performance of a panel of maternal serum markers in predicting preeclampsia at 11–15 weeks' gestation.
        Prenat Diagn. 2007; 27: 1005-1010
        • Spencer K.
        • Yu C.K.
        • Rembouskos G.
        • et al.
        First trimester sex hormone-binding globulin and subsequent development of preeclampsia or other adverse pregnancy outcomes.
        Hypertens Pregnancy. 2005; 24: 303-311
        • Williams M.A.
        • Farrand A.
        • Mittendorf R.
        • et al.
        Maternal second trimester serum tumor necrosis factor-alpha-soluble receptor p55 (sTNFp55) and subsequent risk of preeclampsia.
        Am J Epidemiol. 1999; 149: 323-329
        • Serin I.S.
        • Ozçelik B.
        • Basbug M.
        • et al.
        Predictive value of tumor necrosis factor alpha (TNF-alpha) in preeclampsia.
        Eur J Obstet Gynecol Reprod Biol. 2002; 100: 143-145
        • Schipper E.J.
        • Bolte A.C.
        • Schalkwijk C.G.
        • et al.
        TNF-receptor levels in preeclampsia–results of a longitudinal study in high-risk women.
        J Matern Fetal Neonatal Med. 2005; 18: 283-287
        • Leal A.M.
        • Poon L.C.
        • Frisova V.
        • et al.
        First-trimester maternal serum tumor necrosis factor receptor-1 and pre-eclampsia.
        Ultrasound Obstet Gynecol. 2009; 33: 135-141
        • Wolf M.
        • Sandler L.
        • Muñoz K.
        • et al.
        First trimester insulin resistance and subsequent preeclampsia: a prospective study.
        J Clin Endocrinol Metab. 2002; 87: 1563-1568
        • D'Anna R.
        • Baviera G.
        • Corrado F.
        • et al.
        Adiponectin and insulin resistance in early- and late-onset pre-eclampsia.
        BJOG. 2006; 113: 1264-1269
        • Moses E.K.
        • Lade J.A.
        • Guo G.
        • et al.
        A genome scan in families from Australia and New Zealand confirms the presence of a maternal susceptibility locus for pre-eclampsia, on chromosome 2.
        Am J Hum Genet. 2000; 67: 1581-1585
        • Harrison G.A.
        • Humphrey K.E.
        • Jones N.
        • et al.
        A genomewide linkage study of preeclampsia/eclampsia reveals evidence for a candidate region on 4q.
        Am J Hum Genet. 1997; 60: 1158-1167
        • Farina A.
        • Sekizawa A.
        • De Sanctis P.
        • et al.
        Gene expression in chorionic villous samples at 11 weeks' gestation from women destined to develop preeclampsia.
        Prenat Diagn. 2008; 28: 956-961
        • Founds S.A.
        • Conley Y.P.
        • Lyons-Weiler J.F.
        • et al.
        Altered global gene expression in first trimester placentas of women destined to develop preeclampsia.
        Placenta. 2009; 30: 15-24
        • Alberry M.S.
        • Maddocks D.G.
        • Hadi M.A.
        • et al.
        Quantification of cell free fetal DNA in maternal plasma in normal pregnancies and in pregnancies with placental dysfunction.
        Am J Obstet Gynecol. 2009; 200 (e1–6): 98
        • Caramelli E.
        • Rizzo N.
        • Concu M.
        • et al.
        Cell-free fetal DNA concentration in plasma of patients with abnormal uterine artery Doppler waveform and intrauterine growth restriction–a pilot study.
        Prenat Diagn. 2003; 23: 367-371
        • Holzgreve W.
        • Ghezzi F.
        • Di Naro E.
        • et al.
        Disturbed feto-maternal cell traffic in preeclampsia.
        Obstet Gynecol. 1998; 91: 669-672
        • Lo Y.M.
        • Leung T.N.
        • Tein M.S.
        • et al.
        Quantitative abnormalities of fetal DNA in maternal serum in preeclampsia.
        Clin Chem. 1999; 45: 184-188
        • DiFederico E.
        • Genbacev O.
        • Fisher S.J.
        Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall.
        Am J Pathol. 1999; 155: 293-301
        • Cotter A.M.
        • Martin C.M.
        • O'leary J.J.
        • et al.
        Increased fetal DNA in the maternal circulation in early pregnancy is associated with an increased risk of preeclampsia.
        Am J Obstet Gynecol. 2004; 191: 515-520
        • Crowley A.
        • Martin C.
        • Fitzpatrick P.
        • et al.
        Free fetal DNA is not increased before 20 weeks in intrauterine growth restriction or pre-eclampsia.
        Prenat Diagn. 2007; 27: 174-179
        • NCI-NHGRI Working Group on Replication in Association Studies
        • Manolio T.
        • Chanock S.J.
        • et al.
        Replicating genotype-phenotype associations.
        Nature. 2007; 447: 655-660
        • Poon L.C.
        • Maiz N.
        • Valencia C.
        • et al.
        First-trimester maternal serum pregnancy-associated plasma protein-A and pre-eclampsia.
        Ultrasound Obstet Gynecol. 2009; 33: 23-33
        • Plasencia W.
        • Maiz N.
        • Poon L.
        • et al.
        Uterine artery Doppler at 11 + 0 to 13 + 6 weeks and 21 + 0 to 24 + 6 weeks in the prediction of pre-eclampsia.
        Ultrasound Obstet Gynecol. 2008; 32: 138-146
        • Sibai B.
        • Dekker G.
        • Kupferminc M.
        Pre-eclampsia.
        Lancet. 2005; 365: 785-799
        • Espinoza J.
        • Romero R.
        • Nien J.K.
        • et al.
        Identification of patients at risk for early onset and/or severe preeclampsia with the use of uterine artery Doppler velocimetry and placental growth factor.
        Am J Obstet Gynecol. 2007; 196 (e1–13): 326
        • Poon L.C.
        • Kametas N.A.
        • Maiz N.
        • et al.
        First-trimester prediction of hypertensive disorders in pregnancy.
        Hypertension. 2009; 53: 812-818
        • Poon L.C.
        • Karagiannis G.
        • Leal A.
        • et al.
        Hypertensive disorders in pregnancy: screening by uterine artery Doppler imaging and blood pressure at 11–13 weeks.
        Ultrasound Obstet Gynecol. 2009; 34: 497-502