Fetal death: A condition with a dissociation in the concentrations of soluble vascular endothelial growth factor receptor-2 between the maternal and fetal compartments

Journal of Maternal-Fetal and Neonatal Medicine

Volumn 23, Issue 9, 2010, Pages 960-972

  Chaiworapongsa, Tinnakorn ^a,b   Kusanovic, Juan Pedro ^a,b,c   Savasan, Zeynep Alpay ^a,b,c   Mazaki Tovi, Shali ^a,b,c   Kim, Sun Kwon ^a,b   Vaisbuch, Edi ^a,b,c   Tarca, Adi L ^a,d   Mittal, Pooja ^a,b,c   Ogge, Giovanna ^a,b   Madan, Ichchha ^a,b,c   Dong, Zhong ^a,c   Yeo, Lami ^a,b,c   Hassan, Sonia S ^a,b,c   Romero, Roberto ^a,b,c  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b Wayne State University ^*

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

^d Wayne State University   (United States)

Author keywords

Amniotic fluid; angiogenesis; angiogenic factor; congenital anomaly; intrauterine demise; maternal plasma; preeclampsia; sKDR; stillbirth; unexplained fetal death, sVEGF R2

Indexed keywords

VASCULOTROPIN RECEPTOR 2;

ADOLESCENT; ADULT; AFRICAN AMERICAN; AMNIOCENTESIS; AMNION FLUID ANALYSIS; ARTICLE; BIRTH WEIGHT; BLOOD ANALYSIS; BLOOD SAMPLING; CAUCASIAN; CHILDBIRTH; CHROMOSOME ABERRATION; CIGARETTE SMOKING; CONGENITAL MALFORMATION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FETUS; FETUS DEATH; GESTATIONAL AGE; HISPANIC; HUMAN; MAJOR CLINICAL STUDY; MATERNAL BLOOD; NULLIPARA; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; SOLUTIO PLACENTAE;

EID: 77955899231     PISSN: 14767058     EISSN: 14764954     Source Type: Journal    
DOI: 10.3109/14767050903410664     Document Type: Article

References (79)

1. Silver RM. Fetal death. Obstet Gynecol 2007;109:153-167.
2. Fretts RC. Etiology and prevention of stillbirth. Am J Obstet Gynecol 2005;193:1923-1935.
3. Smith GC, Fretts RC. Stillbirth. Lancet 2007;370:1715-1725.
4. Silver RM, Varner MW, Reddy U, Goldenberg R, Pinar H, Conway D, Bukowski R, Carpenter M, Hogue C, Willinger M, et al. Work-up of stillbirth: a review of the evidence. Am J Obstet Gynecol 2007;196:433-444.
5. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380:439-442.
6. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996;380:435-439.
7. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-676.
8. Shibuya M. Vascular endothelial growth factor-dependent and -independent regulation of angiogenesis. BMB Rep 2008;41:278-286.
9. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995;376:62-66.
10. 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.
11. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 2003;188:177-182.
12. Reuvekamp A, Velsing-Aarts FV, Poulina IE, Capello JJ, Duits AJ. Selective deficit of angiogenic growth factors characterises pregnancies complicated by pre-eclampsia. Br J Obstet Gynaecol 1999;106:1019-1022.
13. 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.
14. Tsatsaris V, Goffin F, Munaut C, Brichant JF, Pignon MR, Noel A, Schaaps JP, Cabrol D, Frankenne F, Foidart JM. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 2003;88:5555-5563.
15. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, 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.
16. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, et al. 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. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642-649. (Pubitemid 43865232)
19. Levine RJ, Lam C, Qian C, Yu KF, Maynard SE, Sachs BP, Sibai BM, Epstein FH, Romero R, Thadhani R, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006;355:992-1005.
20. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, Kusanovic JP, Gotsch F, Erez O, Mazaki-Tovi S, 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.
21. Chaiworapongsa T, Romero R, Gotsch F, Espinoza J, Nien JK, Goncalves L, Edwin S, Kim YM, Erez O, Kusanovic JP, et al. Low maternal concentrations of soluble vascular endothelial growth factor receptor-2 in preeclampsia and small for gestational age. J Matern Fetal Neonatal Med 2008;21:41-52.
22. Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic JP, Gotsch F, Edwin S, Nien JK, Chaiworapongsa T, et al. The change in concentrations of angiogenic and antiangiogenic 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.
23. 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;196:239-246.
24. 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.
25. Wikstrom AK, Larsson A, Eriksson UJ, Nash P, Norden- 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.
26. Unal ER, Robinson CJ, Johnson DD, Chang EY. Secondtrimester angiogenic factors as biomarkers for future-onset preeclampsia. Am J Obstet Gynecol 2007;197:211-214.
27. 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.
28. Crispi F, Llurba E, Dominguez C, Martin-Gallan P, Cabero L, Gratacos E. Predictive value of angiogenic factors and uterine artery Doppler for early- versus late-onset preeclampsia and intrauterine growth restriction. Ultrasound Obstet Gynecol 2008;31:303-309.
29. 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.
30. Chaiworapongsa T, Espinoza J, Gotsch F, Kim YM, Kim GJ, Goncalves LF, Edwin S, Kusanovic JP, Erez O, Than NG, 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.
31. Signore C, Mills JL, Qian C, Yu K, Lam C, Epstein FH, Karumanchi SA, Levine RJ. Circulating angiogenic factors and placental abruption. Obstet Gynecol 2006;108:338-344.
32. Espinoza J, Romero R, Nien JK, Kusanovic JP, Richani K, Gomez R, Kim CJ, Mittal P, Gotsh F, Erez O, et al. 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.
33. Kusanovic JP, Romero R, Espinoza J, Nien JK, Kim CJ, Mittal P, Edwin S, Erez O, Gotsch F, Mazaki-Tovi S, et al. Twin-to-twin transfusion syndrome: an antiangiogenic state? Am J Obstet Gynecol 2008;198:382-388.
34. Espinoza J, Chaiworapongsa T, Romero R, Kim YM, Kim GJ, Nien JK, Kusanovic JP, Erez O, Bujold E, Goncalves LF, et al. Unexplained fetal death: another anti-angiogenic state. J Matern Fetal Neonatal Med 2007;20:495-507.
35. Ebos JM, Bocci G, Man S, Thorpe PE, Hicklin DJ, Zhou D, Jia X, Kerbel RS. A naturally occurring soluble form of vascular endothelial growth factor receptor 2 detected in mouse and human plasma. Mol Cancer Res 2004;2:315-326.
36. Lin P, Sankar S, Shan S, Dewhirst MW, Polverini PJ, Quinn TQ, Peters KG. Inhibition of tumor growth by targeting tumor endothelium using a soluble vascular endothelial growth factor receptor. Cell Growth Differ 1998;9:49-58.
37. McLeod DS, Taomoto M, Cao J, Zhu Z, Witte L, Lutty GA. Localization of VEGF receptor-2 (KDR/Flk-1) and effects of blocking it in oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 2002;43:474-482.
38. Tas F, Duranyildiz D, Oguz H, Camlica H, Yasasever V, Topuz E. Circulating serum levels of angiogenic factors and vascular endothelial growth factor receptors 1 and 2 in melanoma patients. Melanoma Res 2006;16:405-411.
39. Cortelezzi A, Fracchiolla NS, Mazzeo LM, Silvestris I, Pomati M, Somalvico F, Bertolini F, Mancuso P, Pruneri GC, Gianelli U, et al. Endothelial precursors and mature endothelial cells are increased in the peripheral blood of myelodysplastic syndromes. Leuk Lymphoma 2005;46:1345-1351.
40. Aref S, El SM, Goda T, Fouda M, Al AH, Abdalla D. Soluble VEGF/sFLt1 ratio is an independent predictor of AML patient out come. Hematology 2005;10:131-134.
41. Faderl S, Do KA, JohnsonMM, Keating M, O'brien S, Jilani I, Ferrajoli A, Ravandi-Kashani F, Aguilar C, Dey A, et al. Angiogenic factors may have a different prognostic role in adult acute lymphoblastic leukemia. Blood 2005;106:4303-4307.
42. Robak E, Sysa-Jedrzejewska A, Robak T. Vascular endothelial growth factor and its soluble receptors VEGFR-1 and VEGFR-2 in the serum of patients with systemic lupus erythematosus. Mediators Inflamm 2003;12:293-298.
43. Srikiatkhachorn A, Ajariyakhajorn C, Endy TP, Kalayanarooj S, Libraty DH, Green S, Ennis FA, Rothman AL. Virusinduced decline in soluble vascular endothelial growth receptor 2 is associated with plasma leakage in dengue hemorrhagic Fever. J Virol 2007;81:1592-1600.
44. Chaiworapongsa T, Romero R, Gotsch F, Kusanovic JP, Mittal P, Kim SK, Erez O, Vaisbuch E, Mazaki-Tovi S, Kim CJ, et al. Acute pyelonephritis during pregnancy changes the balance of angiogenic and anti-angiogenic factors in maternal plasma. J Matern Fetal Neonatal Med 2009; July 16, [E-Pub ahead of print].
45. Chaiworapongsa T, Romero R, Tarca A, Kusanovic JP, Gotsch F, Mittal P, Erez O, Vaisbuch E, Mazaki-Tovi S, Dong Z, et al. A decrease in Maternal Plasma Concentrations of sVEGFR-2 precedes the clinical diagnosis of preeclampsia. Reprod Sci 2009;16:264A.
46. Kim SY, Park SY, Kim JW, Kim YM, Yang JH, Kim MY, Ahn HK, Shin JS, Kim JO, Ryu HM. Circulating endothelial progenitor cells, plasma VEGF VEGFR-1 and VEGFR-2 levels in preeclampsia. Am J Obstet Gynecol 2005;193:S74.
47. Wallner W, Sengenberger R, Strick R, Strissel PL, Meurer B, Beckmann MW, Schlembach D. Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clin Sci (Lond) 2007;112:51-57.
48. Burgos H. Angiogenic and growth factors in human amniochorion and placenta. Eur J Clin Invest 1983;13:289-296.
49. Tranquilli AL, Giannubilo SR, Bezzeccheri V, Ciavattini A, Scagnoli C, Mazzanti L. Amniotic levels of nitric oxide and vascular endothelial growth factor in pregnancy with subsequent intrauterine fetal death. Eur J Obstet Gynecol Reprod Biol 2004;114:162-165. (Pubitemid 38622076)
50. 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.
51. 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. (Pubitemid 30100498)
52. Staff AC, Braekke K, Harsem NK, Lyberg T, Holthe MR. 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.
53. Daneshmand SS, Cheung CY, Brace RA. Regulation of amniotic fluid volume by intramembranous absorption in sheep: role of passive permeability and vascular endothelial growth factor. Am J Obstet Gynecol 2003;188:786-793.
54. Astern J, Gowin-Rown J, Kendal-wright C. The expression of vascular endothelial growth factor and its receptors in primary human amniotic epithelial celss (AEC). Reprod Sci 2009;16:116A.
55. Cheung CY. Vascular endothelial growth factor activation of intramembranous absorption: a critical pathway for amniotic fluid volume regulation. J Soc Gynecol Investig 2004;11:63-74.
56. Yoon BH, Romero R, Moon JB, Shim SS, Lam M, Kim G, Jun JK. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2001;185:1130-1136. (Pubitemid 33097376)
57. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163-168.
58. Gonzalez RP, Gomez RM, Castro RS, Nien JK, Merino PO, Etchegaray AB, Carstens MR, Medina LH, Viviani PG, Rojas IT. [A national birth weight distribution curve according to gestational age in Chile from 1993 to 2000]. Rev Med Chil 2004;132:1155-1165.
59. Rana S, Rauh-Hain A, Karumanchi A, Thadhani R. Firsttrimester serum angiogenic factors and the risk of intrauterine fetal demise. Am J Obstet Gynecol 2007;197:S12.
60. Roberts JM. Endothelial dysfunction in preeclampsia. Semin Reprod Endocrinol 1998;16:5-15.
61. Johnson MR, Anim-Nyame N, Johnson P, Sooranna SR, Steer PJ. Does endothelial cell activation occur with intrauterine growth restriction? BJOG 2002;109:836-839.
62. Chaiworapongsa T, Romero R, Yoshimatsu J, Espinoza J, Kim YM, 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.
63. Roberts JM, Von Versen-Hoeynck F. Maternal fetal/placental interactions and abnormal pregnancy outcomes. Hypertension 2007;49:15-16.
64. Czabanka M, Peter C, Martin E, Walther A. Microcirculatory endothelial dysfunction during endotoxemia - insights into pathophysiology, pathologic mechanisms and clinical relevance. Curr Vasc Pharmacol 2007;5:266-275.
65. Quinton AE, Cook CM, Peek MJ. The relationship between cigarette smoking, endothelial function and intrauterine growth restriction in human pregnancy. BJOG 2008;115: 780-784.
66. Schouten M, Wiersinga WJ, Levi M, van der PT. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 2008;83:536-545.
67. Kanagalingam MG, Nelson SM, Freeman DJ, Ferrell WR, Cherry L, Lowe GD, Greer IA, Sattar N. Vascular dysfunction and alteration of novel and classic cardiovascular risk factors in mothers of growth restricted offspring. Atherosclerosis 2009;205:244-250.
68. Swendeman S, Mendelson K, Weskamp G, Horiuchi K, Deutsch U, Scherle P, Hooper A, Rafii S, Blobel CP. VEGFA stimulates ADAM17-dependent shedding of VEGFR2 and crosstalk between VEGFR2 and ERK signaling. Circ Res 2008;103:916-918.
69. Garton KJ, Gough PJ, Raines EW. Emerging roles for ectodomain shedding in the regulation of inflammatory responses. J Leukoc Biol 2006;79:1105-1116.
70. Higashiyama S, Nanba D. ADAM-mediated ectodomain shedding of HB-EGF in receptor cross-talk. Biochim Biophys Acta 2005;1751:110-117.
71. Bauvois B. Transmembrane proteases in cell growth and invasion: new contributors to angiogenesis? Oncogene 2004;23:317-329.
72. Jayasinghe C, Simiantonaki N, Michel-Schmidt R, Kirkpatrick CJ. Hypoxia-induced reduction of sVEGFR-2 levels in human colonic microvascular endothelial cells in vitro: comparative study with HUVEC. Int J Mol Med 2009;23:49-55.
73. Jayasinghe C, Simiantonaki N, Michel-Schmidt R, Kirkpatrick CJ. Comparative study of human colonic tumor-derived endothelial cells (HCTEC) and normal colonic microvascular endothelial cells (HCMEC): hypoxia-induced sVEGFR-1 and sVEGFR-2 levels. Oncol Rep 2009;21:933-939.
74. Smith GC, Yu CK, Papageorghiou AT, Cacho AM, Nicolaides KH. Maternal uterine artery Doppler flow velocimetry and the risk of stillbirth. Obstet Gynecol 2007; 109:144-151.
75. Gardosi J, Mul T, Mongelli M, Fagan D. Analysis of birthweight and gestational age in antepartum stillbirths. Br J Obstet Gynaecol 1998;105:524-530.
76. Khong TY, Liddell HS, Robertson WB. Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol 1987;94:649-655.
77. Cheung CY. Vascular endothelial growth factor: possible role in fetal development and placental function. J Soc Gynecol Investig 1997;4:169-177.
78. Vuorela-Vepsalainen P, Alfthan H, Orpana A, Alitalo K, Stenman UH, Halmesmaki E. Vascular endothelial growth factor is bound in amniotic fluid and maternal serum. Hum Reprod 1999;14:1346-1351.
79. Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 1996;226:324-328.