The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation

References

• Robertson W B, Brosens I, Dixon G. Maternal uterine vascular lesions in the hypertensive complications of pregnancy. Perspect Nephrol Hypertens 1976; 5: 115–127
   PubMedGoogle Scholar
• Brosens I A. Morphological changes in the utero-placental bed in pregnancy hypertension. Clin Obstet Gynaecol 1977; 4: 573–593
   PubMed Web of Science ®Google Scholar
• Sheppard B L, Bonnar J. An ultrastructural study of utero-placental spiral arteries in hypertensive and normotensive pregnancy and fetal growth retardation. Br J Obstet Gynaecol 1981; 88: 695–705
   PubMedGoogle Scholar
• Khong T Y, De Wolf F, Robertson W B, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93: 1049–1059
   PubMedGoogle Scholar
• Pijnenborg R, Anthony J, Davey D A, Rees A, Tiltman A, Vercruysse L, van Assche A. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991; 98: 648–655
   PubMedGoogle Scholar
• Redman C W, Sargent I L. Latest advances in understanding preeclampsia. Science 2005; 308: 1592–1594
   PubMed Web of Science ®Google Scholar
• Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet 2005; 365: 785–799
   PubMed Web of Science ®Google Scholar
• Roberts J M, Gammill H S. Preeclampsia: Recent insights. Hypertension 2005; 46: 1243–1249
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Fisher S J. The placental problem: Linking abnormal cytotrophoblast differentiation to the maternal symptoms of preeclampsia. Reprod Biol Endocrinol 2004; 2: 53
   PubMedGoogle Scholar
• Brosens I A, Robertson W B, Dixon H G. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972; 1: 177–191
   PubMedGoogle Scholar
• Brosens I, Renaer M. On the pathogenesis of placental infarcts in pre-eclampsia. J Obstet Gynaecol Br Commonw 1972; 79: 794–799
   PubMedGoogle Scholar
• Berger M, Cavanagh D. Toxemia of pregnancy. The hypertensive effect of acute experimental placental ischemia. Am J Obstet Gynecol 1963; 87: 293–305
   PubMedGoogle Scholar
• Carbillon L, Challier J C, Alouini S, Uzan M, Uzan S. Uteroplacental circulation development: Doppler assessment and clinical importance. Placenta 2001; 22: 795–799
   PubMed Web of Science ®Google Scholar
• Campbell S, Pearce J M, Hackett G, Cohen-Overbeek T, Hernandez C. Qualitative assessment of uteroplacental blood flow: Early screening test for high-risk pregnancies. Obstet Gynecol 1986; 68: 649–653
   PubMed Web of Science ®Google Scholar
• Soleymanlou N, Jurisica I, Nevo O, Ietta F, Zhang X, Zamudio S, Post M, Caniggia I. Molecular evidence of placental hypoxia in preeclampsia. J Clin Endocrinol Metab 2005; 90: 4299–4308
   PubMed Web of Science ®Google Scholar
• Iwata M, Matsuzaki N, Shimizu I, Mitsuda N, Nakayama M, Suehara N. Prenatal detection of ischemic changes in the placenta of the growth-retarded fetus by Doppler flow velocimetry of the maternal uterine artery. Obstet Gynecol 1993; 82: 494–499
   PubMedGoogle Scholar
• Ochi H, Suginami H, Matsubara K, Taniguchi H, Yano J, Matsuura S. Micro-bead embolization of uterine spiral arteries and changes in uterine arterial flow velocity waveforms in the pregnant ewe. Ultrasound Obstet Gynecol 1995; 6: 272–276
   PubMed Web of Science ®Google Scholar
• Talbert D G. Uterine flow velocity waveform shape as an indicator of maternal and placental development failure mechanisms: A model-based synthesizing approach. Ultrasound Obstet Gynecol 1995; 6: 261–271
   PubMed Web of Science ®Google Scholar
• Voigt H J, Becker V. Doppler flow measurements and histomorphology of the placental bed in uteroplacental insufficiency. J Perinat Med 1992; 20: 139–147
   PubMed Web of Science ®Google Scholar
• Olofsson P, Laurini R N, Marsal K. A high uterine artery pulsatility index reflects a defective development of placental bed spiral arteries in pregnancies complicated by hypertension and fetal growth retardation. Eur J Obstet Gynecol Reprod Biol 1993; 49: 161–168
   PubMed Web of Science ®Google Scholar
• Lin S, Shimizu I, Suehara N, Nakayama M, Aono T. Uterine artery Doppler velocimetry in relation to trophoblast migration into the myometrium of the placental bed. Obstet Gynecol 1995; 85: 760–765
   PubMed Web of Science ®Google Scholar
• Sagol S, Ozkinay E, Oztekin K, Ozdemir N. The comparison of uterine artery Doppler velocimetry with the histopathology of the placental bed. Aust N Z J Obstet Gynaecol 1999; 39: 324–329
   PubMed Web of Science ®Google Scholar
• Guzin K, Tomruk S, Tuncay Y A, Naki M, Sezginsoy S, Zemheri E, Yucel N, Kanadikirik F. The relation of increased uterine artery blood flow resistance and impaired trophoblast invasion in pre-eclamptic pregnancies. Arch Gynecol Obstet 2005; 272: 283–288
   PubMedGoogle Scholar
• Madazli R, Somunkiran A, Calay Z, Ilvan S, Aksu M F. Histomorphology of the placenta and the placental bed of growth restricted foetuses and correlation with the Doppler velocimetries of the uterine and umbilical arteries. Placenta 2003; 24: 510–516
   PubMed Web of Science ®Google Scholar
• Aardema M W, Oosterhof H, Timmer A, van Rooy I, Aarnoudse J G. Uterine artery Doppler flow and uteroplacental vascular pathology in normal pregnancies and pregnancies complicated by pre-eclampsia and small for gestational age fetuses. Placenta 2001; 22: 405–411
   PubMed Web of Science ®Google Scholar
• Albaiges G, Missfelder-Lobos H, Lees C, Parra M, Nicolaides K H. One-stage screening for pregnancy complications by color Doppler assessment of the uterine arteries at 23 weeks' gestation. Obstet Gynecol 2000; 96: 559–564
   PubMed Web of Science ®Google Scholar
• Campbell S, Black R S, Lees C C, Armstrong V, Peacock J L. Doppler ultrasound of the maternal uterine arteries: Disappearance of abnormal waveforms and relation to birthweight and pregnancy outcome. Acta Obstet Gynecol Scand 2000; 79: 631–634
   PubMed Web of Science ®Google Scholar
• Chappell L, Bewley S. Pre-eclamptic toxaemia: The role of uterine artery Doppler. Br J Obstet Gynaecol 1998; 105: 379–382
   PubMedGoogle Scholar
• Fleischer A, Schulman H, Farmakides G, Bracero L, Grunfeld L, Rochelson B, Koenigsberg M. Uterine artery Doppler velocimetry in pregnant women with hypertension. Am J Obstet Gynecol 1986; 154: 806–813
   PubMed Web of Science ®Google Scholar
• North R A, Ferrier C, Long D, Townend K, Kincaid-Smith P. Uterine artery Doppler flow velocity waveforms in the second trimester for the prediction of preeclampsia and fetal growth retardation. Obstet Gynecol 1994; 83: 378–386
   PubMed Web of Science ®Google Scholar
• Papageorghiou A T, Yu C K, Bindra R, Pandis G, Nicolaides K H. Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol 2001; 18: 441–449
   PubMed Web of Science ®Google Scholar
• Todros T, Ferrazzi E, Arduini D, Bastonero S, Bezzeccheri V, Biolcati M, Bonazzi B, Gabrielli S, Pilu G L, Rizzo G. Performance of Doppler ultrasonography as a screening test in low risk pregnancies: Results of a multicentric study. J Ultrasound Med 1995; 14: 343–348
   PubMed Web of Science ®Google Scholar
• Zimmermann P, Eirio V, Koskinen J, Kujansuu E, Ranta T. Doppler assessment of the uterine and uteroplacental circulation in the second trimester in pregnancies at high risk for pre-eclampsia and/or intrauterine growth retardation: Comparison and correlation between different Doppler parameters. Ultrasound Obstet Gynecol 1997; 9: 330–338
   PubMed Web of Science ®Google Scholar
• Harrington K F, Campbell S, Bewley S, Bower S. Doppler velocimetry studies of the uterine artery in the early prediction of pre-eclampsia and intra-uterine growth retardation. Eur J Obstet Gynecol Reprod Biol 1991; 42(Suppl)S14–20
   PubMed Web of Science ®Google Scholar
• Bower S, Schuchter K, Campbell S. Doppler ultrasound screening as part of routine antenatal scanning: Prediction of pre-eclampsia and intrauterine growth retardation. Br J Obstet Gynaecol 1993; 100: 989–994
   PubMedGoogle Scholar
• Friedman S A, Schiff E, Emeis J J, Dekker G A, Sibai B M. Biochemical corroboration of endothelial involvement in severe preeclampsia. Am J Obstet Gynecol 1995; 172: 202–203
   PubMed Web of Science ®Google Scholar
• Roberts J M, Taylor R N, Goldfien A. Endothelial cell activation as a pathogenetic factor in preeclampsia. Semin Perinatol 1991; 15: 86–93
   PubMed Web of Science ®Google Scholar
• Conrad K P, Benyo D F. Placental cytokines and the pathogenesis of preeclampsia. Am J Reprod Immunol 1997; 37: 240–249
   PubMed Web of Science ®Google Scholar
• Greer I A, Lyall F, Perera T, Boswell F, Macara L M. Increased concentrations of cytokines interleukin-6 and interleukin-1 receptor antagonist in plasma of women with preeclampsia: A mechanism for endothelial dysfunction?. Obstet Gynecol 1994; 84: 937–940
   PubMed Web of Science ®Google Scholar
• Granger J P, Alexander B T, Llinas M T, Bennett W A, Khalil R A. Pathophysiology of preeclampsia: Linking placental ischemia/hypoxia with microvascular dysfunction. Microcirculation 2002; 9: 147–160
   PubMed Web of Science ®Google Scholar
• Hung T H, Charnock-Jones D S, Skepper J N, Burton G J. 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
   PubMed Web of Science ®Google Scholar
• Sargent I L, Germain S J, Sacks G P, Kumar S, Redman C W. Trophoblast deportation and the maternal inflammatory response in pre-eclampsia. J Reprod Immunol 2003; 59: 153–160
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Romero R, Yoshimatsu J, Espinoza J, Kim Y M, Park K, Kalache K, Edwin S, Bujold E, Gomez R. Soluble adhesion molecule profile in normal pregnancy and pre-eclampsia. J Matern Fetal Neonatal Med 2002; 12: 19–27
   PubMedGoogle Scholar
• Redman C W, Sacks G P, Sargent I L. Preeclampsia: An excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999; 180: 499–506
   PubMed Web of Science ®Google Scholar
• Gervasi M T, Chaiworapongsa T, Pacora P, Naccasha N, Yoon B H, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001; 185: 792–797
   PubMed Web of Science ®Google Scholar
• Redman C W, Sargent I L. Placental debris, oxidative stress and pre-eclampsia. Placenta 2000; 21: 597–602
   PubMed Web of Science ®Google Scholar
• Sacks G P, Studena K, Sargent K, Redman C W. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998; 179: 80–86
   PubMed Web of Science ®Google Scholar
• Mellembakken J R, Aukrust P, Olafsen M K, Ueland T, Hestdal K, Videm V. Activation of leukocytes during the uteroplacental passage in preeclampsia. Hypertension 2002; 39: 155–160
   PubMed Web of Science ®Google Scholar
• Dekker G A, Sibai B M. Etiology and pathogenesis of preeclampsia: Current concepts. Am J Obstet Gynecol 1998; 179: 1359–1375
   PubMed Web of Science ®Google Scholar
• Friedman S A, de Groot C J, Taylor R N, Golditch B D, Roberts J M. Plasma cellular fibronectin as a measure of endothelial involvement in preeclampsia and intrauterine growth retardation. Am J Obstet Gynecol 1994; 170: 838–841
   PubMed Web of Science ®Google Scholar
• Bretelle F, Sabatier F, Blann A, D'Ercole C, Boutiere B, Mutin M, Boubli L, Sampol J, Dignat-George F. Maternal endothelial soluble cell adhesion molecules with isolated small for gestational age fetuses: Comparison with pre-eclampsia. BJOG 2001; 108: 1277–1282
   PubMed Web of Science ®Google Scholar
• Johnson M R, Anim-Nyame N, Johnson P, Sooranna S R, Steer P J. Does endothelial cell activation occur with intrauterine growth restriction?. BJOG 2002; 109: 836–839
   PubMed Web of Science ®Google Scholar
• Sabatier F, Bretelle F, D'Ercole C, Boubli L, Sampol J, Dignat-George F. Neutrophil activation in preeclampsia and isolated intrauterine growth restriction. Am J Obstet Gynecol 2000; 183: 1558–1563
   PubMed Web of Science ®Google Scholar
• Ness R B, Sibai B M. Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. Am J Obstet Gynecol 2006; 195: 40–49
   PubMed Web of Science ®Google Scholar
• Luttun A, Carmeliet P. Soluble VEGF receptor Flt1: The elusive preeclampsia factor discovered?. J Clin Invest 2003; 111: 600–602
   PubMed Web of Science ®Google Scholar
• Ferrara N, Gerber H P, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003; 9: 669–676
   PubMed Web of Science ®Google Scholar
• Maynard S E, Min J Y, Merchan J, Lim K H, Li J, Mondal S, Libermann T A, Morgan J P, Sellke F W, Stillman I E, 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
   PubMed Web of Science ®Google Scholar
• Levine R J, Maynard S E, Qian C, Lim K H, England L J, Yu K F, Schisterman E F, Thadhani R, Sachs B P, Epstein F H, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350: 672–683
   PubMed Web of Science ®Google Scholar
• Hertig A, Berkane N, Lefevre G, Toumi K, Marti H P, Capeau J, Uzan S, Rondeau E. Maternal serum sFlt1 concentration is an early and reliable predictive marker of preeclampsia. Clin Chem 2004; 50: 1702–1703
   PubMed Web of Science ®Google Scholar
• McKeeman G C, Ardill J E, Caldwell C M, Hunter A J, McClure N. Soluble vascular endothelial growth factor receptor-1 (sFlt-1) is increased throughout gestation in patients who have preeclampsia develop. Am J Obstet Gynecol 2004; 191: 1240–1246
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Romero R, Kim Y M, Kim G J, Kim M R, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, et al. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005; 17: 3–18
   PubMed Web of Science ®Google Scholar
• Park C W, Park J S, Shim S S, Jun J K, Yoon B H, Romero R. An elevated maternal plasma, but not amniotic fluid, soluble fms-like tyrosine kinase-1 (sFlt-1) at the time of mid-trimester genetic amniocentesis is a risk factor for preeclampsia. Am J Obstet Gynecol 2005; 193: 984–989
   PubMed Web of Science ®Google Scholar
• Powers R W, Roberts J M, Cooper K M, Gallaher M J, Frank M P, Harger G F, Ness R B. 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
   PubMed Web of Science ®Google Scholar
• Wathen K A, Tuutti E, Stenman U H, Alfthan H, Halmesmaki E, Finne P, Ylikorkala O, Vuorela P. Maternal serum soluble vascular endothelial growth factor receptor-1 in early pregnancy ending in pre-eclampsia or intrauterine growth retardation. J Clin Endocrinol Metab 2006; 91: 180–184
   PubMed Web of Science ®Google Scholar
• Parra M, Rodrigo R, Barja P, Bosco C, Fernandez V, Munoz H, Soto-Chacon E. Screening test for preeclampsia through assessment of uteroplacental blood flow and biochemical markers of oxidative stress and endothelial dysfunction. Am J Obstet Gynecol 2005; 193: 1486–1491
   PubMed Web of Science ®Google Scholar
• Koga K, Osuga Y, Yoshino O, Hirota Y, Ruimeng X, Hirata T, Takeda S, Yano T, Tsutsumi O, Taketani Y. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003; 88: 2348–2351
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee K Y, Goncalves L F, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol 2004; 190: 1541–1547
   PubMed Web of Science ®Google Scholar
• Stepan H, Geide A, Faber R. Soluble fms-like tyrosine kinase 1. N Engl J Med 2004; 351: 2241–2242
   PubMed Web of Science ®Google Scholar
• Staff A C, Braekke K, Harsem N K, Lyberg T, Holthe M R. Circulating concentrations of sFlt1 (soluble fms-like tyrosine kinase 1) in fetal and maternal serum during pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 2005; 122: 33–39
   PubMed Web of Science ®Google Scholar
• Tsatsaris V, Goffin F, Munaut C, Brichant J F, Pignon M R, Noel A, Schaaps J P, Cabrol D, Frankenne F, Foidart J M. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: Pathophysiological consequences. J Clin Endocrinol Metab 2003; 88: 5555–5563
   PubMed Web of Science ®Google Scholar
• Gerber H P, McMurtrey A, Kowalski J, Yan M, Keyt B A, Dixit V, Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 1998; 273: 30 336–30 343
   Google Scholar
• Shibata E, Rajakumar A, Powers R W, Larkin R W, Gilmour C, Bodnar L M, Crombleholme W R, Ness R B, Roberts J M, Hubel C A. Soluble fms-like tyrosine kinase 1 is increased in preeclampsia but not in normotensive pregnancies with small-for-gestational-age neonates: Relationship to circulating placental growth factor. J Clin Endocrinol Metab 2005; 90: 4895–4903
   PubMed Web of Science ®Google Scholar
• Boutsikou T, Malamitsi-Puchner A, Economou E, Boutsikou M, Puchner K P, Hassiakos D. Soluble vascular endothelial growth factor receptor-1 in intrauterine growth restricted fetuses and neonates. Early Hum Dev 2006; 82: 235–239
   PubMed Web of Science ®Google Scholar
• Savvidou M D, Yu C K, Harland L C, Hingorani A D, Nicolaides K H. Maternal serum concentration of soluble fms-like tyrosine kinase 1 and vascular endothelial growth factor in women with abnormal uterine artery Doppler and in those with fetal growth restriction. Am J Obstet Gynecol 2006; 195: 1668–1673
   PubMed Web of Science ®Google Scholar
• Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. 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: 201–207
   PubMed Web of Science ®Google Scholar
• Wallner W, Sengenberger R, Strick R, Strissel P L, Meurer B, Beckmann M W, Schlembach D. Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clin Sci (Lond) 2007; 112: 51–57
   PubMed Web of Science ®Google Scholar
• Seeds J W. Impaired fetal growth: Definition and clinical diagnosis. Obstet Gynecol 1984; 64: 303–310
   PubMed Web of Science ®Google Scholar
• Alexander G R, Himes J H, Kaufman R B, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996; 87: 163–168
   PubMed Web of Science ®Google Scholar
• Sibai B M, Ewell M, Levine R J, Klebanoff M A, Esterlitz J, Catalano P M, Goldenberg R L, Joffe G. Risk factors associated with preeclampsia in healthy nulliparous women. The Calcium for Preeclampsia Prevention (CPEP) Study Group. Am J Obstet Gynecol 1997; 177: 1003–1010
   PubMed Web of Science ®Google Scholar
• Kurmanavicius J, Florio I, Wisser J, Hebisch G, Zimmermann R, Muller R, Huch R, Huch A. Reference resistance indices of the umbilical, fetal middle cerebral and uterine arteries at 24 – 42 weeks of gestation. Ultrasound Obstet Gynecol 1997; 10: 112–120
   PubMed Web of Science ®Google Scholar
• Arduini D, Rizzo G. Normal values of pulsatility index from fetal vessels: A cross-sectional study on 1556 healthy fetuses. J Perinat Med 1990; 18: 165–172
   PubMed Web of Science ®Google Scholar
• Trudinger B J, Cook C M, Giles W B, Ng S, Fong E, Connelly A, Wilcox W. Fetal umbilical artery velocity waveforms and subsequent neonatal outcome. Br J Obstet Gynaecol 1991; 98: 378–384
   PubMedGoogle Scholar
• Brar H S, Platt L D. Reverse end-diastolic flow velocity on umbilical artery velocimetry in high-risk pregnancies: An ominous finding with adverse pregnancy outcome. Am J Obstet Gynecol 1988; 159: 559–561
   PubMed Web of Science ®Google Scholar
• Karsdorp V H, van Vugt J M, van Geijn H P, Kostense P J, Arduini D, Montenegro N, Todros T. Clinical significance of absent or reversed end diastolic velocity waveforms in umbilical artery. Lancet 1994; 344: 1664–1668
   PubMed Web of Science ®Google Scholar
• Romero R. Prenatal medicine: The child is the father of the man. Prenat Neonatal Med 1996; 1: 8–11
   Google Scholar
• Goldenberg R L, Cliver S P. Small for gestational age and intrauterine growth restriction: Definitions and standards. Clin Obstet Gynecol 1997; 40: 704–714
   PubMed Web of Science ®Google Scholar
• Bakketeig L S. Current growth standards, definitions, diagnosis and classification of fetal growth retardation. Eur J Clin Nutr 1998; 52(Suppl 1)S1–4
   PubMedGoogle Scholar
• Bamberg C, Kalache K D. Prenatal diagnosis of fetal growth restriction. Semin Fetal Neonatal Med 2004; 9: 387–394
   PubMedGoogle Scholar
• Pearce J M, Campbell S. Intrauterine growth retardation. Birth Defects Orig Artic Ser 1985; 21: 109–130
   PubMedGoogle Scholar
• Trudinger B J, Giles W B, Cook C M. Flow velocity waveforms in the maternal uteroplacental and fetal umbilical placental circulations. Am J Obstet Gynecol 1985; 152: 155–163
   PubMed Web of Science ®Google Scholar
• Morrow R J, Adamson S L, Bull S B, Ritchie J W. Effect of placental embolization on the umbilical arterial velocity waveform in fetal sheep. Am J Obstet Gynecol 1989; 161: 1055–1060
   PubMed Web of Science ®Google Scholar
• Krebs C, Macara L M, Leiser R, Bowman A W, Greer I A, Kingdom J C. 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: 1534–1542
   PubMed Web of Science ®Google Scholar
• Lunell N O, Sarby B, Lewander R, Nylund L. Comparison of uteroplacental blood flow in normal and in intrauterine growth-retarded pregnancy. Measurements with Indium-113m and a computer-linked gamma camera. Gynecol Obstet Invest 1979; 10: 106–118
   PubMed Web of Science ®Google Scholar
• Konje J C, Howarth E S, Kaufmann P, Taylor D J. Longitudinal quantification of uterine artery blood volume flow changes during gestation in pregnancies complicated by intrauterine growth restriction. BJOG 2003; 110: 301–305
   PubMed Web of Science ®Google Scholar
• Lunell N O, Nylund L E, Lewander R, Sarby B. Uteroplacental blood flow in pre-eclampsia measurements with indium-113m and a computer-linked gamma camera. Clin Exp Hypertens B 1982; 1: 105–117
   PubMed Web of Science ®Google Scholar
• Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res 2004; 95: 884–891
   PubMed Web of Science ®Google Scholar
• Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, Kozuma S, Taketani Y. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: An implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 2004; 145: 4838–4845
   PubMed Web of Science ®Google Scholar
• Li H, Gu B, Zhang Y, Lewis D F, Wang Y. Hypoxia-induced increase in soluble Flt-1 production correlates with enhanced oxidative stress in trophoblast cells from the human placenta. Placenta 2005; 26: 210–217
   PubMed Web of Science ®Google Scholar
• Lash G E, Taylor C M, Trew A J, Cooper S, Anthony F W, Wheeler T, Baker P N. Vascular endothelial growth factor and placental growth factor release in cultured trophoblast cells under different oxygen tensions. Growth Factors 2002; 20: 189–196
   PubMed Web of Science ®Google Scholar
• Padavala S, Pope N, Baker P, Crocker I. An imbalance between vascular endothelial growth factor and its soluble receptor in placental villous explants of intrauterine growth-restricted pregnancies. J Soc Gynecol Investig 2006; 13: 40–47
   PubMedGoogle Scholar
• Kingdom J, Huppertz B, Seaward G, Kaufmann P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol 2000; 92: 35–43
   PubMed Web of Science ®Google Scholar
• Caniggia I, Winter J L. Adriana and Luisa Castellucci Award Lecture 2001. Hypoxia inducible factor-1: Oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies—a review. Placenta 2002; 23(Suppl A)S47–57
   PubMed Web of Science ®Google Scholar
• Rajakumar A, Brandon H M, Daftary A, Ness R, Conrad K P. Evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae. Placenta 2004; 25: 763–769
   PubMed Web of Science ®Google Scholar
• Kurdi W, Fayyad A, Thakur V, Harrington K. Delayed normalization of uterine artery Doppler waveforms is not a benign phenomenon. Eur J Obstet Gynecol Reprod Biol 2004; 117: 20–23
   PubMed Web of Science ®Google Scholar
• Harrington K, Goldfrad C, Carpenter R G, Campbell S. Transvaginal uterine and umbilical artery Doppler examination of 12 – 16 weeks and the subsequent development of pre-eclampsia and intrauterine growth retardation. Ultrasound Obstet Gynecol 1997; 9: 94–100
   PubMed Web of Science ®Google Scholar
• Lam C, Lim K H, Karumanchi S A. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension 2005; 46: 1077–1085
   PubMed Web of Science ®Google Scholar
• Muller P R, James A H, Murtha A P, Yonish B, Jamison M G, Dekker G. Circulating angiogenic factors and abnormal uterine artery Doppler velocimetry in the second trimester. Hypertens Pregnancy 2006; 25: 183–192
   PubMed Web of Science ®Google Scholar
• Huppertz B, Kingdom J, Caniggia I, Desoye G, Black S, Korr H, Kaufmann P. Hypoxia favours necrotic versus apoptotic shedding of placental syncytiotrophoblast into the maternal circulation. Placenta 2003; 24: 181–190
   PubMed Web of Science ®Google Scholar
• Matsubara K, Nagamatsu T, Fujii T, Kozuma S, Taketani Y. Lymphokine-activated killer cells induced from decidual lymphocytes reduce the angiogenic activity of trophoblasts by enhancing the release of soluble fms-like tyrosine kinase-1 from trophoblasts: An implication for the pathophysiology of preeclampsia. J Reprod Immunol 2005; 68: 27–37
   PubMedGoogle Scholar
• Eubank T D, Roberts R, Galloway M, Wang Y, Cohn D E, Marsh C B. GM-CSF induces expression of soluble VEGF receptor-1 from human monocytes and inhibits angiogenesis in mice. Immunity 2004; 21: 831–842
   PubMed Web of Science ®Google Scholar
• Geva E, Ginzinger D G, Zaloudek C J, Moore D H, Byrne A, Jaffe R B. Human placental vascular development: Vasculogenic and angiogenic (branching and nonbranching) transformation is regulated by vascular endothelial growth factor-A, angiopoietin-1, and angiopoietin-2. J Clin Endocrinol Metab 2002; 87: 4213–4224
   PubMed Web of Science ®Google Scholar
• Kearney J B, Kappas N C, Ellerstrom C, DiPaola F W, Bautch V L. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood 2004; 103: 4527–4535
   PubMed Web of Science ®Google Scholar
• Girardi G, Yarilin D, Thurman J M, Holers V M, Salmon J E. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006; 203: 2165–2175
   PubMed Web of Science ®Google Scholar
• Stepan H, Faber R, Wessel N, Wallukat G, Schultheiss H P, Walther T. Relation between circulating angiotensin II type 1 receptor agonistic autoantibodies and soluble fms-like tyrosine kinase 1 in the pathogenesis of preeclampsia. J Clin Endocrinol Metab 2006; 91: 2424–2427
   PubMedGoogle Scholar
• Kingdom J C, Burrell S J, Kaufmann P. Pathology and clinical implications of abnormal umbilical artery Doppler waveforms. Ultrasound Obstet Gynecol 1997; 9: 271–286
   PubMed Web of Science ®Google Scholar
• Sebire N J, Talbert D. ‘Cor placentale’: Placental intervillus/intravillus blood flow mismatch is the pathophysiological mechanism in severe intrauterine growth restriction due to uteroplacental disease. Med Hypotheses 2001; 57: 354–357
   PubMedGoogle Scholar
• Pardi G, Cetin I, Marconi A M, Bozzetti P, Buscaglia M, Makowski E L, Battaglia F C. Venous drainage of the human uterus: Respiratory gas studies in normal and fetal growth-retarded pregnancies. Am J Obstet Gynecol 1992; 166: 699–706
   PubMedGoogle Scholar
• Sibley C P, Pardi G, Cetin I, Todros T, Piccoli E, Kaufmann P, Huppertz B, Bulfamante G, Cribiu F M, Ayuk P, et al. Pathogenesis of intrauterine growth restriction (IUGR)—conclusions derived from a European Union Biomed 2 Concerted Action project ‘Importance of Oxygen Supply in Intrauterine Growth Restricted Pregnancies’—a workshop report. Placenta 2002; 23(Suppl A)S75–79
   Google Scholar
• Khaliq A, Dunk C, Jiang J, Shams M, Li X F, Acevedo C, Weich H, Whittle M, Ahmed A. Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: Molecular evidence for ‘placental hyperoxia’ in intrauterine growth restriction. Lab Invest 1999; 79: 151–170
   PubMed Web of Science ®Google Scholar
• Regnault T R, de Vrijer B, Galan H L, Davidsen M L, Trembler K A, Battaglia F C, Wilkening R B, Anthony R V. The relationship between transplacental O2 diffusion and placental expression of PlGF, VEGF and their receptors in a placental insufficiency model of fetal growth restriction. J Physiol 2003; 550: 641–656
   PubMed Web of Science ®Google Scholar
• Ahmed A, Dunk C, Ahmad S, Khaliq A. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen—a review. Placenta 2000; 21(Suppl A)S16–24
   PubMedGoogle Scholar
• Rajakumar A, Michael H M, Rajakumar P A, Shibata E, Hubel C A, Karumanchi S A, Thadhani R, Wolf M, Harger G, Markovic N. Extra-placental expression of vascular endothelial growth factor receptor-1 (Flt-1) and soluble Flt-1 (sFlt-1), by peripheral blood mononuclear cells (PBMCs) in normotensive and preeclamptic pregnant women. Placenta 2005; 26: 563–573
   PubMed Web of Science ®Google Scholar
• Vuorela P, Helske S, Hornig C, Alitalo K, Weich H, Halmesmaki E. Amniotic fluid—soluble vascular endothelial growth factor receptor-1 in preeclampsia. Obstet Gynecol 2000; 95: 353–357
   PubMed Web of Science ®Google Scholar
• Schlembach D, Beinder E. Angiogenic factors in preeclampsia. J Soc Gynecol Investig 2003; 10: 316A
   Google Scholar
• Tsao P N, Wei S C, Su Y N, Chou H C, Chen C Y, Hsieh W S. Excess soluble fms-like tyrosine kinase 1 and low platelet counts in premature neonates of preeclamptic mothers. Pediatrics 2005; 116: 468–472
   PubMed Web of Science ®Google Scholar
• Hirashima C, Ohkuchi A, Arai F, Takahashi K, Suzuki H, Watanabe T, Kario K, Matsubara S, Suzuki M. Establishing reference values for both total soluble Fms-like tyrosine kinase 1 and free placental growth factor in pregnant women. Hypertens Res 2005; 28: 727–732
   PubMed Web of Science ®Google Scholar