2,183
Views
112
CrossRef citations to date
0
Altmetric
Original Article

Late-onset preeclampsia is associated with an imbalance of angiogenic and anti-angiogenic factors in patients with and without placental lesions consistent with maternal underperfusion

, , , , , , , & show all
Pages 498-507 | Received 14 May 2011, Accepted 23 May 2011, Published online: 25 Aug 2011

References

  • Romero R, Lockwood C, Oyarzun E, Hobbins JC. Toxemia: new concepts in an old disease. Semin Perinatol 1988;12:302–323.
  • von Dadelszen P, Menzies J, Magee LA. The complications of hypertension in pregnancy. Minerva Med 2005;96:287–302.
  • Sibai BM. Hypertensive disorders of pregnancy: the United States perspective. Curr Opin Obstet Gynecol 2008;20:102–106.
  • Berg CJ, Mackay AP, Qin C, Callaghan WM. Overview of maternal morbidity during hospitalization for labor and delivery in the United States: 1993-1997 and 2001-2005. Obstet Gynecol 2009;113:1075–1081.
  • Khan KS, Wojdyla D, Say L, Gülmezoglu AM, Van Look PF. WHO analysis of causes of maternal death: a systematic review. Lancet 2006;367:1066–1074.
  • Kuklina EV, Ayala C, Callaghan WM. Hypertensive disorders and severe obstetric morbidity in the United States. Obstet Gynecol 2009;113:1299–1306.
  • Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005;308:1592–1594.
  • Roberts JM, Gammill HS. Preeclampsia: recent insights. Hypertension 2005;46:1243–1249.
  • Robertson WB, Brosens I, Dixon G. Maternal uterine vascular lesions in the hypertensive complications of pregnancy. Perspect Nephrol Hypertens 1976;5:115–127.
  • Pijnenborg R, Anthony J, Davey DA, 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.
  • Romero R, Kusanovic JP, Chaiworapongsa T, Hassan SS. Placental bed disorders in preterm labor, preterm PROM, spontaneous abortion and abruptio placentae. Best Pract Res Clin Obstet Gynaecol 2011;25:313–327.
  • Silasi M, Cohen B, Karumanchi SA, Rana S. Abnormal placentation, angiogenic factors, and the pathogenesis of preeclampsia. Obstet Gynecol Clin North Am 2010;37:239–253.
  • Brosens I, Pijnenborg R, Vercruysse L, Romero R. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 2011;204:193–201.
  • Roberts JM, Hubel CA. The two stage model of preeclampsia: variations on the theme. Placenta 2009;30 Suppl A:S32–S37.
  • Gammill HS, Roberts JM. Emerging concepts in preeclampsia investigation. Front Biosci 2007;12:2403–2411.
  • Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK. Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 1989;161:1200–1204.
  • Roberts JM, Taylor RN, Goldfien A. Endothelial cell activation as a pathogenetic factor in preeclampsia. Semin Perinatol 1991;15:86–93.
  • Vaisbuch E, Romero R, Mazaki-Tovi S, Erez O, Kim SK, Chaiworapongsa T, Gotsch F, et al. Retinol binding protein 4—a novel association with early-onset preeclampsia. J Perinat Med 2010;38:129–139.
  • Mazaki-Tovi S, Romero R, Vaisbuch E, Kusanovic JP, Erez O, Gotsch F, Chaiworapongsa T, et al. Maternal serum adiponectin multimers in preeclampsia. J Perinat Med 2009;37:349–363.
  • Nien JK, Mazaki-Tovi S, Romero R, Erez O, Kusanovic JP, Gotsch F, Pineles BL, et al. Adiponectin in severe preeclampsia. J Perinat Med 2007;35:503–512.
  • Arias F, Romero R, Joist H, Kraus FT. Thrombophilia: a mechanism of disease in women with adverse pregnancy outcome and thrombotic lesions in the placenta. J Matern Fetal Med 1998;7:277–286.
  • Chaiworapongsa T, Yoshimatsu J, Espinoza J, Kim YM, Berman S, Edwin S, Yoon BH, Romero R. Evidence of in vivo generation of thrombin in patients with small-for-gestational-age fetuses and pre-eclampsia. J Matern Fetal Neonatal Med 2002;11:362–367.
  • Erez O, Hoppensteadt D, Romero R, Espinoza J, Goncalves L, Nien JK, Kusanovic JP, et al. Preeclampsia is associated with low concentrations of protein Z. J Matern Fetal Neonatal Med 2007;20:661–667.
  • Erez O, Romero R, Hoppensteadt D, Than NG, Fareed J, Mazaki-Tovi S, Espinoza J, et al. Tissue factor and its natural inhibitor in pre-eclampsia and SGA. J Matern Fetal Neonatal Med 2008;21:855–869.
  • Erez O, Romero R, Vaisbuch E, Mazaki-Tovi S, Kusanovic JP, Chaiworapongsa T, Than NG, et al. Maternal anti-protein Z antibodies in pregnancies complicated by pre-eclampsia, SGA and fetal death. J Matern Fetal Neonatal Med 2009;22:662–671.
  • Erez O, Romero R, Kim SS, Kim JS, Kim YM, Wildman DE, Than NG, et al. Over-expression of the thrombin receptor (PAR-1) in the placenta in preeclampsia: a mechanism for the intersection of coagulation and inflammation. J Matern Fetal Neonatal Med 2008;21:345–355.
  • Soto E, Romero R, Richani K, Espinoza J, Chaiworapongsa T, Nien JK, Edwin SS, et al. Preeclampsia and pregnancies with small-for-gestational age neonates have different profiles of complement split products. J Matern Fetal Neonatal Med 2010;23:646–657.
  • Lynch AM, Salmon JE. Dysregulated complement activation as a common pathway of injury in preeclampsia and other pregnancy complications. Placenta 2010;31:561–567.
  • Derzsy Z, Prohászka Z, Rigó J Jr, Füst G, Molvarec A. Activation of the complement system in normal pregnancy and preeclampsia. Mol Immunol 2010;47:1500–1506.
  • Lynch AM, Murphy JR, Gibbs RS, Levine RJ, Giclas PC, Salmon JE, Holers VM. The interrelationship of complement-activation fragments and angiogenesis-related factors in early pregnancy and their association with pre-eclampsia. BJOG 2010;117:456–462.
  • Rampersad R, Barton A, Sadovsky Y, Nelson DM. The C5b-9 membrane attack complex of complement activation localizes to villous trophoblast injury in vivo and modulates human trophoblast function in vitro. Placenta 2008;29:855–861.
  • Lynch AM, Murphy JR, Byers T, Gibbs RS, Neville MC, Giclas PC, Salmon JE, Holers VM. Alternative complement pathway activation fragment Bb in early pregnancy as a predictor of preeclampsia. Am J Obstet Gynecol 2008;198:385.e1–385.e9.
  • Gervasi MT, Chaiworapongsa T, Pacora P, Naccasha N, Yoon BH, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001;185:792–797.
  • Redman CW, Sacks GP, Sargent IL. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999;180:499–506.
  • Sacks GP, Studena K, Sargent K, Redman CW. 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.
  • Than NG, Romero R, Erez O, Kusanovic JP, Tarca AL, Edwin SS, Kim JS, et al. A role for mannose-binding lectin, a component of the innate immune system in pre-eclampsia. Am J Reprod Immunol 2008;60:333–345.
  • Kim YM, Romero R, Oh SY, Kim CJ, Kilburn BA, Armant DR, Nien JK, et al. Toll-like receptor 4: a potential link between “danger signals,” the innate immune system, and preeclampsia? Am J Obstet Gynecol 2005;193:921–927.
  • Chaiworapongsa T, Romero R, Yoshimatsu J, Espinoza J, Kim YM, Park K, Kalache K, et al. Soluble adhesion molecule profile in normal pregnancy and pre-eclampsia. J Matern Fetal Neonatal Med 2002;12:19–27.
  • Romero R, Vizoso J, Emamian M, Duffy T, Riely C, Halford T, Oyarzun E, et al. Clinical significance of liver dysfunction in pregnancy-induced hypertension. Am J Perinatol 1988;5:146–151.
  • Romero R, Mazor M, Lockwood CJ, Emamian M, Belanger KP, Hobbins JC, Duffy T. Clinical significance, prevalence, and natural history of thrombocytopenia in pregnancy-induced hypertension. Am J Perinatol 1989;6:32–38.
  • Luttun A, Carmeliet P. Soluble VEGF receptor Flt1: the elusive preeclampsia factor discovered? J Clin Invest 2003;111:600–602.
  • Myatt L. Role of placenta in preeclampsia. Endocrine 2002;19:103–111.
  • Conrad KP, Benyo DF. Placental cytokines and the pathogenesis of preeclampsia. Am J Reprod Immunol 1997;37:240–249.
  • Sibai B, Romero R, Klebanoff MA, Rice MM, Caritis S, Lindheimer MD, Van Dorsten JP, et al.; Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. Maternal plasma concentrations of the soluble tumor necrosis factor receptor 2 are increased prior to the diagnosis of preeclampsia. Am J Obstet Gynecol 2009;200:630.e1–630.e8.
  • Haeger M, Unander M, Andersson B, Tarkowski A, Arnestad JP, Bengtsson A. Increased release of tumor necrosis factor-alpha and interleukin-6 in women with the syndrome of hemolysis, elevated liver enzymes, and low platelet count. Acta Obstet Gynecol Scand 1996;75:695–701.
  • Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, von Dadelszen P. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 2006;27:56–61.
  • Sargent IL, Germain SJ, Sacks GP, Kumar S, Redman CW. Trophoblast deportation and the maternal inflammatory response in pre-eclampsia. J Reprod Immunol 2003;59:153–160.
  • Huppertz B, Frank HG, Reister F, Kingdom J, Korr H, Kaufmann P. Apoptosis cascade progresses during turnover of human trophoblast: analysis of villous cytotrophoblast and syncytial fragments in vitro. Lab Invest 1999;79:1687–1702.
  • 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.
  • Sedeek M, Gilbert JS, LaMarca BB, Sholook M, Chandler DL, Wang Y, Granger JP. Role of reactive oxygen species in hypertension produced by reduced uterine perfusion in pregnant rats. Am J Hypertens 2008;21:1152–1156.
  • Raijmakers MT, Peters WH, Steegers EA, Poston L. NAD(P)H oxidase associated superoxide production in human placenta from normotensive and pre-eclamptic women. Placenta 2004;25 Suppl A:S85–S89.
  • Mellembakken JR, Aukrust P, Olafsen MK, Ueland T, Hestdal K, Videm V. Activation of leukocytes during the uteroplacental passage in preeclampsia. Hypertension 2002;39:155–160.
  • Clark CJ, Boswell F, Greer IA, Lyall F. Treatment of endothelial cells with serum from women with preeclampsia: effect on neutrophil adhesion. J Soc Gynecol Investig 1997;4:27–33.
  • Walther T, Wallukat G, Jank A, Bartel S, Schultheiss HP, Faber R, Stepan H. Angiotensin II type 1 receptor agonistic antibodies reflect fundamental alterations in the uteroplacental vasculature. Hypertension 2005;46:1275–1279.
  • Parrish MR, Wallace K, Tam Tam KB, Herse F, Weimer A, Wenzel K, Wallukat G, et al. Hypertension in Response to AT1-AA: Role of Reactive Oxygen Species in Pregnancy-Induced Hypertension. Am J Hypertens 2011;24:835–840.
  • Dechend R, Gratze P, Wallukat G, Shagdarsuren E, Plehm R, Bräsen JH, Fiebeler A, et al. Agonistic autoantibodies to the AT1 receptor in a transgenic rat model of preeclampsia. Hypertension 2005;45:742–746.
  • Than NG, Abdul Rahman O, Magenheim R, Nagy B, Fule T, Hargitai B, Sammar M, et al. Placental protein 13 (galectin-13) has decreased placental expression but increased shedding and maternal serum concentrations in patients presenting with preterm pre-eclampsia and HELLP syndrome. Virchows Arch 2008;453:387–400.
  • Than NG, Erez O, Wildman DE, Tarca AL, Edwin SS, Abbas A, Hotra J, et al. Severe preeclampsia is characterized by increased placental expression of galectin-1. J Matern Fetal Neonatal Med 2008;21:429–442.
  • Romero R, Kusanovic JP, Than NG, Erez O, Gotsch F, Espinoza J, Edwin S, et al. First-trimester maternal serum PP13 in the risk assessment for preeclampsia. Am J Obstet Gynecol 2008;199:122.e1–122.e11.
  • Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res 2004;95:884–891.
  • Bujold E, Blackwell SC, Hendler I, Berman S, Sorokin Y, Gauthier RJ. Modified Bishop’s score and induction of labor in patients with a previous cesarean delivery. Am J Obstet Gynecol 2004;191:1644–1648.
  • Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, 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.
  • Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, 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.
  • Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res 2005;57:1R–7R.
  • Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642–649.
  • Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, et al.; CPEP Study Group. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006;355:992–1005.
  • Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med 2008;21:9–23.
  • Ahmed A, Whittle MJ, Khaliq A. Differential expression of placenta growth factor (PlGF) and vascular endothelial growth factor (VEGF) in abnormal placentation. J Soc Gynecol Investig 1997;4
  • Lindheimer MD, Romero R. Emerging roles of antiangiogenic and angiogenic proteins in pathogenesis and prediction of preeclampsia. Hypertension 2007;50:35–36.
  • Bdolah Y, Karumanchi SA, Sachs BP. Recent advances in understanding of preeclampsia. Croat Med J 2005;46:728–736.
  • Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee Kim Y, Gonçalves LF, 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;190:1541–7; discussion 1547.
  • Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004;350:672–683.
  • Tidwell SC, Ho HN, Chiu WH, Torry RJ, Torry DS. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001;184:1267–1272.
  • Aggarwal PK, Jain V, Sakhuja V, Karumanchi SA, Jha V. Low urinary placental growth factor is a marker of pre-eclampsia. Kidney Int 2006;69:621–624.
  • Crispi F, Domínguez C, Llurba E, Martín-Gallán P, Cabero L, Gratacós 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.
  • Levine RJ, Qian C, Maynard SE, Yu KF, Epstein FH, Karumanchi SA. Serum sFlt1 concentration during preeclampsia and mid trimester blood pressure in healthy nulliparous women. Am J Obstet Gynecol 2006;194:1034–1041.
  • Muller PR, James AH, Murtha AP, Yonish B, Jamison MG, Dekker G. Circulating angiogenic factors and abnormal uterine artery Doppler velocimetry in the second trimester. Hypertens Pregnancy 2006;25:183–192.
  • Wathén KA, Tuutti E, Stenman UH, Alfthan H, Halmesmäki E, Finne P, Ylikorkala O, Vuorela P. Maternal serum-soluble vascular endothelial growth factor receptor-1 in early pregnancy ending in preeclampsia or intrauterine growth retardation. J Clin Endocrinol Metab 2006;91:180–184.
  • Masuyama H, Suwaki N, Nakatsukasa H, Masumoto A, Tateishi Y, Hiramatrsu Y. Circulating angiogenic factors in preeclampsia, gestational proteinuria, and preeclampsia superimposed on chronic glomerulonephritis. Am J Obstet Gynecol 2006;194:551–556.
  • Robinson CJ, Johnson DD, Chang EY, Armstrong DM, Wang W. Evaluation of placenta growth factor and soluble Fms-like tyrosine kinase 1 receptor levels in mild and severe preeclampsia. Am J Obstet Gynecol 2006;195:255–259.
  • Robinson CJ, Johnson DD. Soluble endoglin as a second-trimester marker for preeclampsia. Am J Obstet Gynecol 2007;197:174.e1–174.e5.
  • Espinoza J, Romero R, Nien JK, Gomez R, Kusanovic JP, Gonçalves LF, Medina L, 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;196:326.e1–326.13.
  • Moore Simas TA, Crawford SL, Solitro MJ, Frost SC, Meyer BA, Maynard SE. Angiogenic factors for the prediction of preeclampsia in high-risk women. Am J Obstet Gynecol 2007;197:244.e1–244.e8.
  • Staff AC, Braekke K, Johnsen GM, Karumanchi SA, Harsem NK. Circulating concentrations of soluble endoglin (CD105) in fetal and maternal serum and in amniotic fluid in preeclampsia. Am J Obstet Gynecol 2007;197:176.e1–176.e6.
  • Rana S, Karumanchi SA, Levine RJ, Venkatesha S, Rauh-Hain JA, Tamez H, Thadhani R. Sequential changes in antiangiogenic factors in early pregnancy and risk of developing preeclampsia. Hypertension 2007;50:137–142.
  • Stepan H, Unversucht A, Wessel N, Faber R. Predictive value of maternal angiogenic factors in second trimester pregnancies with abnormal uterine perfusion. Hypertension 2007;49:818–824.
  • Schlembach D, Wallner W, Sengenberger R, Stiegler E, Mörtl M, Beckmann MW, Lang U. Angiogenic growth factor levels in maternal and fetal blood: correlation with Doppler ultrasound parameters in pregnancies complicated by pre-eclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 2007;29:407–413.
  • Vatten LJ, Eskild A, Nilsen TI, Jeansson S, Jenum PA, Staff AC. Changes in circulating level of angiogenic factors from the first to second trimester as predictors of preeclampsia. Am J Obstet Gynecol 2007;196:239.e1–239.e6.
  • Unal ER, Robinson CJ, Johnson DD, Chang EY. Second-trimester angiogenic factors as biomarkers for future-onset preeclampsia. Am J Obstet Gynecol 2007;197:211.e1–211.e4.
  • Crispi F, Llurba E, Domínguez C, Martín-Gallán P, Cabero L, Gratacós E. 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.
  • De Vivo A, Baviera G, Giordano D, Todarello G, Corrado F, D’anna R. Endoglin, PlGF and sFlt-1 as markers for predicting pre-eclampsia. Acta Obstet Gynecol Scand 2008;87:837–842.
  • Diab AE, El-Behery MM, Ebrahiem MA, Shehata AE. Angiogenic factors for the prediction of pre-eclampsia in women with abnormal midtrimester uterine artery Doppler velocimetry. Int J Gynaecol Obstet 2008;102:146–151.
  • Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic JP, Gotsch F, et al. The change in concentrations of angiogenic and anti-angiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age. J Matern Fetal Neonatal Med 2008;21:279–287.
  • Lim JH, Kim SY, Park SY, Yang JH, Kim MY, Ryu HM. Effective prediction of preeclampsia by a combined ratio of angiogenesis-related factors. Obstet Gynecol 2008;111:1403–1409.
  • Sibai BM, Koch MA, Freire S, Pinto e Silva JL, Rudge MV, Martins-Costa S, Bartz J, et al. Serum inhibin A and angiogenic factor levels in pregnancies with previous preeclampsia and/or chronic hypertension: are they useful markers for prediction of subsequent preeclampsia? Am J Obstet Gynecol 2008;199:268.e1–268.e9.
  • Stepan H, Geipel A, Schwarz F, Krämer T, Wessel N, Faber R. Circulatory soluble endoglin and its predictive value for preeclampsia in second-trimester pregnancies with abnormal uterine perfusion. Am J Obstet Gynecol 2008;198:175.e1–175.e6.
  • Kusanovic JP, Romero R, Chaiworapongsa T, Erez O, Mittal P, Vaisbuch E, Mazaki-Tovi S, 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.
  • Wang A, Rana S, Karumanchi SA. Preeclampsia: the role of angiogenic factors in its pathogenesis. Physiology (Bethesda) 2009;24:147–158.
  • Chedraui P, Lockwood CJ, Schatz F, Buchwalder LF, Schwager G, Guerrero C, Escobar GS, Hidalgo L. Increased plasma soluble fms-like tyrosine kinase 1 and endoglin levels in pregnancies complicated with preeclampsia. J Matern Fetal Neonatal Med 2009;22:565–570.
  • Powers RW, Jeyabalan A, Clifton RG, Van Dorsten P, Hauth JC, Klebanoff MA, Lindheimer MD, et al.; Eunice Kennedy Shriver National Institute of Child Health Human Development Maternal-Fetal Medicine Units Network. Soluble fms-Like tyrosine kinase 1 (sFlt1), endoglin and placental growth factor (PlGF) in preeclampsia among high risk pregnancies. PLoS ONE 2010;5:e13263.
  • Aggarwal PK, Chandel N, Jain V, Jha V. The relationship between circulating endothelin-1, soluble fms-like tyrosine kinase-1 and soluble endoglin in preeclampsia. J Hum Hypertens 2011.
  • Haddad R, Romero R, Gould BR, Tromp G, Gotsch F, Edwin SS, Zingg HH. Angiogenesis gene expression in mouse uterus during the common pathway of parturition. Am J Obstet Gynecol 2008;198:539.e1–539.e8.
  • Chaiworapongsa T, Romero R, Tarca AL, Kusanovic JP, Gotsch F, Mittal P, Kim SK, et al. A decrease in maternal plasma concentrations of sVEGFR-2 precedes the clinical diagnosis of preeclampsia. Am J Obstet Gynecol 2010;202:550.e1–550.10.
  • Akolekar R, Zaragoza E, Poon LC, Pepes S, Nicolaides KH. 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.
  • Akolekar R, Syngelaki A, Sarquis R, Zvanca M, Nicolaides KH. Prediction of early, intermediate and late pre-eclampsia from maternal factors, biophysical and biochemical markers at 11-13 weeks. Prenat Diagn 2011;31:66–74.
  • Thadhani R, Mutter WP, Wolf M, Levine RJ, Taylor RN, Sukhatme VP, Ecker J, Karumanchi SA. 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 PG, Cabral AC, Andrade SP, Reis ZS, da Cruz LP, Pereira JB, Martins BO, Rezende CA. Placental growth factor (PlGF) is a surrogate marker in preeclamptic hypertension. Hypertens Pregnancy 2008;27:65–73.
  • Torry DS, Wang HS, Wang TH, Caudle MR, Torry RJ. Preeclampsia is associated with reduced serum levels of placenta growth factor. Am J Obstet Gynecol 1998;179:1539–1544.
  • Lyall F. The Placenta in Preeclampsia. 2011;1st:246–252.
  • Kumazaki K, Nakayama M, Suehara N, Wada Y. Expression of vascular endothelial growth factor, placental growth factor, and their receptors Flt-1 and KDR in human placenta under pathologic conditions. Hum Pathol 2002;33:1069–1077.
  • Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, Goncalves LF, Edwin S, et al. 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. J Matern Fetal Neonatal Med 2008;21:25–40.
  • Chaiworapongsa T, Romero R, Kusanovic JP, Mittal P, Kim SK, Gotsch F, Than NG, et al. Plasma soluble endoglin concentration in pre-eclampsia is associated with an increased impedance to flow in the maternal and fetal circulations. Ultrasound Obstet Gynecol 2010;35:155–162.
  • Gilbert JS, Babcock SA, Granger JP. Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 2007;50:1142–1147.
  • Makris A, Thornton C, Thompson J, Thomson S, Martin R, Ogle R, Waugh R, et al. Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int 2007;71:977–984.
  • Gilbert JS, Gilbert SA, Arany M, Granger JP. Hypertension produced by placental ischemia in pregnant rats is associated with increased soluble endoglin expression. Hypertension 2009;53:399–403.
  • von Dadelszen P, Magee LA, Roberts JM. Subclassification of preeclampsia. Hypertens Pregnancy 2003;22:143–148.
  • Vatten LJ, Skjaerven R. Is pre-eclampsia more than one disease? BJOG 2004;111:298–302.
  • Valensise H, Vasapollo B, Gagliardi G, Novelli GP. Early and late preeclampsia: two different maternal hemodynamic states in the latent phase of the disease. Hypertension 2008;52:873–880.
  • MacKay AP, Berg CJ, Atrash HK. Pregnancy-related mortality from preeclampsia and eclampsia. Obstet Gynecol 2001;97:533–538.
  • Odegård RA, Vatten LJ, Nilsen ST, Salvesen KA, Austgulen R. Preeclampsia and fetal growth. Obstet Gynecol 2000;96:950–955.
  • Mbah AK, Alio AP, Marty PJ, Bruder K, Whiteman VE, Salihu HM. Pre-eclampsia in the first pregnancy and subsequent risk of stillbirth in black and white gravidas. Eur J Obstet Gynecol Reprod Biol 2010;149:165–169.
  • Kenneth L, Hall DR, Gebhardt S, Grové D. Late onset preeclampsia is not an innocuous condition. Hypertens Pregnancy 2010;29:262–270.
  • Hauth JC, Ewell MG, Levine RJ, Esterlitz JR, Sibai B, Curet LB, Catalano PM, Morris CD. Pregnancy outcomes in healthy nulliparas who developed hypertension. Calcium for Preeclampsia Prevention Study Group. Obstet Gynecol 2000;95:24–28.
  • Tan KH, Kwek K, Yeo GS. Epidemiology of pre-eclampsia and eclampsia at the KK Women’s and Children’s Hospital, Singapore. Singapore Med J 2006;47:48–53.
  • Hutcheon JA, Lisonkova S, Joseph KS. Epidemiology of pre-eclampsia and the other hypertensive disorders of pregnancy. Best Pract Res Clin Obstet Gynaecol 2011.
  • Schutte JM, Steegers EA, Schuitemaker NW, Santema JG, de Boer K, Pel M, Vermeulen G, et al.; Netherlands Maternal Mortality Committee. Rise in maternal mortality in the Netherlands. BJOG 2010;117:399–406.
  • Wikström AK, Larsson A, Eriksson UJ, Nash P, Nordén-Lindeberg S, Olovsson M. Placental growth factor and soluble FMS-like tyrosine kinase-1 in early-onset and late-onset preeclampsia. Obstet Gynecol 2007;109:1368–1374.
  • 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;189:1173–1177.
  • Sebire NJ, Goldin RD, Regan L. Term preeclampsia is associated with minimal histopathological placental features regardless of clinical severity. J Obstet Gynaecol 2005;25:117–118.
  • van der Merwe JL, Hall DR, Wright C, Schubert P, Grové D. Are early and late preeclampsia distinct subclasses of the disease–what does the placenta reveal? Hypertens Pregnancy 2010;29:457–467.
  • Masuyama H, Segawa T, Sumida Y, Masumoto A, Inoue S, Akahori Y, Hiramatsu Y. Different profiles of circulating angiogenic factors and adipocytokines between early- and late-onset pre-eclampsia. BJOG 2010;117:314–320.
  • ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. Obstet Gynecol 2002;99:159–167
  • Sibai BM, Ewell M, Levine RJ, Klebanoff MA, Esterlitz J, Catalano PM, Goldenberg RL, 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.
  • Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163–168.
  • Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation—a workshop report. Placenta 2005;26 Suppl A:S114–S117.
  • Mayhew TM. Taking tissue samples from the placenta: an illustration of principles and strategies. Placenta 2008;29:1–14.
  • Wolf M, Shah A, Lam C, Martinez A, Smirnakis KV, Epstein FH, Taylor RN, et al. Circulating levels of the antiangiogenic marker sFLT-1 are increased in first versus second pregnancies. Am J Obstet Gynecol 2005;193:16–22.
  • Srinivas SK, Morrison AC, Andrela CM, Elovitz MA. Allelic variations in angiogenic pathway genes are associated with preeclampsia. Am J Obstet Gynecol 2010;202:45.e1–445.11.
  • Muy-Rivera M, Vadachkoria S, Woelk GB, Qiu C, Mahomed K, Williams MA. Maternal plasma VEGF, sVEGF-R1, and PlGF concentrations in preeclamptic and normotensive pregnant Zimbabwean women. Physiol Res 2005;54:611–622.
  • Park CW, Park JS, Shim SS, Jun JK, Yoon BH, 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.
  • Ohkuchi A, Hirashima C, Matsubara S, Suzuki H, Takahashi K, Arai F, Watanabe T, et al. Alterations in placental growth factor levels before and after the onset of preeclampsia are more pronounced in women with early onset severe preeclampsia. Hypertens Res 2007;30:151–159.
  • Ogge G, Chaiworapongsa T, Kusanovic JP, Yeo L, Kim CJ, Hassan S, Romero R. Evidence that placental lesions are more frequent in early-onset than in late-onset preeclampsia. Reproductive Science 2011; 18
  • Teasdale F. Histomorphometry of the human placenta in maternal preeclampsia. Am J Obstet Gynecol 1985;152:25–31.
  • Kingdom J. Adriana and Luisa Castellucci Award Lecture 1997. Placental pathology in obstetrics: adaptation or failure of the villous tree? Placenta 1998;19:347–351.
  • 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.
  • Krebs C, Macara LM, Leiser R, Bowman AW, Greer IA, Kingdom JC. 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.
  • Benirschke K, Kaufmann P. 2000. Architecture of Normal Villous Trees. In: Benirschke, K, Kaufmann, P. Pathology of the human placental (pp). 121–173. New York: Springer-Verlag New York, Inc..
  • Egbor M, Ansari T, Morris N, Green CJ, Sibbons PD. Morphometric placental villous and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction. BJOG 2006;113:580–589.
  • Shore VH, Wang TH, Wang CL, Torry RJ, Caudle MR, Torry DS. Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 1997;18:657–665.
  • Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, et al. 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.
  • Chaiworapongsa T, Romero R, Gotsch F, Kusanovic JP, Mittal P, Kim SK, Erez O, et al. Acute pyelonephritis during pregnancy changes the balance of angiogenic and anti-angiogenic factors in maternal plasma. J Matern Fetal Neonatal Med 2010;23:167–178.
  • Rajakumar A, Michael HM, Rajakumar PA, Shibata E, Hubel CA, Karumanchi SA, Thadhani R, et al. 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.
  • Redman CW, Sargent IL. Immunology of pre-eclampsia. Am J Reprod Immunol 2010;63:534–543.
  • Redline RW, Boyd T, Campbell V, Hyde S, Kaplan C, Khong TY, Prashner HR, Waters BL; Society for Pediatric Pathology, Perinatal Section, Maternal Vascular Perfusion Nosology Committee. Maternal vascular underperfusion: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2004;7:237–249.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.