Plasma soluble endoglin concentration in pre-eclampsia is associated with an increased impedance to flow in the maternal and fetal circulations

Ultrasound in Obstetrics and Gynecology

Volumn 35, Issue 2, 2010, Pages 155-162

  Chaiworapongsa, T ^a,b   Romero, R ^a,b   Kusanovic, J P ^a,b   Mittal, P ^a,b   Kim, S K ^a   Gotsch, F ^a   Than, N G ^a   Mazaki Tovi, S ^a,b   Vaisbuch, E ^a,b   Erez, O ^a,b   Yeo, L ^a,b   Hassan, S S ^a,b   Sorokin, Y ^a,b  

^a HUTZEL HOSPITAL   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Pre eclampsia; Soluble endoglin; Umbilical artery Doppler velocimetry; Uterine artery Doppler velocimetry

Indexed keywords

BIOLOGICAL MARKER; CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; LEUKOCYTE ANTIGEN;

ADOLESCENT; ADULT; ARTICLE; BLOOD; BLOOD FLOW; BLOOD FLOW VELOCITY; CROSS-SECTIONAL STUDY; ECHOGRAPHY; FEMALE; FETOMATERNAL TRANSFUSION; FETUS ECHOGRAPHY; GESTATIONAL AGE; HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; PREECLAMPSIA; PREGNANCY; RETROSPECTIVE STUDY; UMBILICAL ARTERY; UTERINE ARTERY;

ADOLESCENT; ADULT; ANTIGENS, CD; BIOLOGICAL MARKERS; BLOOD FLOW VELOCITY; CROSS-SECTIONAL STUDIES; FEMALE; GESTATIONAL AGE; HUMANS; MATERNAL-FETAL EXCHANGE; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, CELL SURFACE; REGIONAL BLOOD FLOW; RETROSPECTIVE STUDIES; ULTRASONOGRAPHY, PRENATAL; UMBILICAL ARTERIES; UTERINE ARTERY; YOUNG ADULT;

EID: 76349093612     PISSN: 09607692     EISSN: 14690705     Source Type: Journal    
DOI: 10.1002/uog.7491     Document Type: Article

References (51)

1. Redman CW, Sargent IL. Placental stress and pre-eclampsia: a revised view. Placenta 2009; 30 (Suppl A): S38-S42.
2. Roberts JM, Hubel CA. The two stage model of preeclampsia: variations on the theme. Placenta 2008; 30 (Suppl A): S32-S37.
3. Sibai BM. Hypertensive disorders of pregnancy: the United States perspective. Curr Opin Obstet Gynecol 2008; 20: 102-106.
4. Romero R, Lockwood C, Oyarzun E, Hobbins JC. Toxemia: new concepts in an old disease. Semin Perinatol 1988; 12: 302-323.
5. 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.
6. Voigt HJ, Becker V. Doppler flow measurements and histomorphology of the placental bed in uteroplacental insufficiency. J PerinatMed 1992; 20: 139-147.
7. Olofsson P, Laurini RN, 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.
8. 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.
9. Conrad KP, Benyo DF. Placental cytokines and the pathogenesis of preeclampsia. Am J Reprod Immunol 1997; 37: 240-249.
10. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, von DP. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 2006; 27: 56-61.
11. 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.
12. 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.
13. 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.
14. 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.
15. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA. Excess placental soluble fmslike tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003; 111: 649-658.
16. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350: 672-683.
17. Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Mee KY, Goncalves 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: 1541-1547.
18. Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Kim MR, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, Mazor M. Plasma soluble vascular endothelial growth factor receptor1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005; 17: 3-18.
19. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, Gotsch F, Erez O, Mazaki-Tovi S, Gomez R, Edwin S, Chaiworapongsa T, Levine RJ, Karumanchi SA. 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.
20. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D'Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12: 642-649. (Pubitemid 43865232)
21. Levine RJ, Lam C, Qian C, Yu KF,Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, Karumanchi SA. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl JMed 2006; 355: 992-1005.
22. ten Dijke P, Goumans MJ, Pardali E. Endoglin in angiogenesis and vascular diseases. Angiogenesis 2008; 11: 79-89.
23. Stepan H, Geipel A, Schwarz F, Kramer 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: 175-176.
24. Savvidou MD, Noori M, Anderson JM, Hingorani AD, Nicolaides KH. Maternal endothelial function and serum concentrations of placental growth factor and soluble endoglin in women with abnormal placentation. Ultrasound Obstet Gynecol 2008; 32: 871-876.
25. Baumann MU, Bersinger NA, Mohaupt MG, Raio L, Gerber S, Surbek DV. 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: 266.e1-266.e6.
26. Hirashima C, Ohkuchi A, Matsubara S, Suzuki H, Takahashi K, Usui R, Suzuki M. Alteration of serum soluble endoglin levels after the onset of preeclampsia is more pronounced in women with early-onset. Hypertens Res 2008; 31: 1541-1548.
27. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996; 87: 163-168.
28. 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.
29. von Dadelszen P, Magee LA, Roberts JM. Subclassification of preeclampsia. Hypertens Pregnancy 2003; 22: 143-148.
30. Harrington KF, 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-S20.
31. 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.
32. Bower S, Schuchter K, Campbell S. Doppler ultrasound screening as part of routine antenatal scanning: prediction of preeclampsia and intrauterine growth retardation. Br J Obstet Gynaecol 1993; 100: 989-994.
33. Arduini D, Rizzo G. Normal values of pulsatility index from fetal vessels: a cross-sectional study on 1556 healthy fetuses. J PerinatMed 1990; 18: 165-172.
34. Trudinger BJ, Cook CM, Giles WB, 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.
35. Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, Goncalves LF, Edwin S, Kusanovic JP, Erez O, Than NG, Hassan SS, Romero R. 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.
36. Schlembach D, Wallner W, Sengenberger R, Stiegler E, Mortl 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.
37. Papageorghiou AT, Leslie K. Uterine artery Doppler in the prediction of adverse pregnancy outcome. Curr Opin Obstet Gynecol 2007; 19: 103-109.
38. Espinoza J, Romero R, Nien JK, Gomez R, Kusanovic JP, Goncalves LF, Medina L, Edwin S, Hassan S, Carstens M, Gonzalez R. 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.e13.
39. 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.
40. 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.
41. Egbor M, Ansari T, Morris N, Green CJ, Sibbons PD. Morphometric placental villous and vascular abnormalities in earlyand late-onset pre-eclampsia with and without fetal growth restriction. BJOG 2006; 113: 580-589.
42. 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.
43. Li Z, Zhang Y, Ying MJ, Kapoun AM, Shao Q, Kerr I, Lam A, O'Young G, Sannajust F, Stathis P, Schreiner G, Karumanchi SA, Protter AA, Pollitt NS. Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 2007; 50: 686-692.
44. 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.
45. Savvidou MD, Yu CK, Harland LC, Hingorani AD, Nicolaides KH. 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.
46. Espinoza J, Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Nien JK, Kusanovic JP, Erez O, Bujold E, Goncalves LF, Gomez R, Edwin S. Unexplained fetal death: another antiangiogenic state. J Matern Fetal Neonatal Med 2007; 20: 495-507.
47. Espinoza J, Romero R, Nien JK, Kusanovic JP, Richani K, Gomez R, Kim CJ, Mittal P, Gotsh F, Erez O, Chaiworapongsa T, Hassan S. A role of the anti-angiogenic factor sVEGFR-1 in the 'mirror syndrome' (Ballantyne's syndrome). J Matern Fetal Neonatal Med 2006; 19: 607-613.
48. Kusanovic JP, Romero R, Espinoza J, Nien JK, Kim CJ, Mittal P, Edwin S, Erez O, Gotsch F, Mazaki-Tovi S, Than NG, Soto E, Camacho N, Gomez R, Quintero R, Hassan SS. Twintotwin transfusion syndrome: an antiangiogenic state? Am J Obstet Gynecol 2008; 198: 382.e1-e.8.
49. Yinon Y, Nevo O, Xu J, Many A, Rolfo A, Todros T, Post M, Caniggia I. Severe intrauterine growth restriction pregnancies have increased placental endoglin levels: hypoxic regulation via transforming growth factor-beta 3. Am J Pathol 2008; 172: 77-85.
50. Munaut C, Lorquet S, Pequeux C, Blacher S, Berndt S, Frankenne F, Foidart JM. Hypoxia is responsible for soluble vascular endothelial growth factor receptor-1 (VEGFR-1) but not for soluble endoglin induction in villous trophoblast. Hum Reprod 2008; 23: 1407-1415.
51. Gotsch F, Kim YM, Kim CJ, Edwin S, Holtra J, Tarca AL, Chaiworapongsa T, Kusanovic JP, Mor G, Redman C, Romero R. A link between inflammation/infection and anti-angiogenic state in preeclampsia : inflammatory mediators mimic effect of hypoxia on trophoblast by increasing sFlt-1 and decreasing placental growth factor production. International Society for the Study of Hypertension in Pregnancy 2009 World Congress XVI, Washington, DC, USA, 2008; 46.