Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-05-18T11:10:38.171Z Has data issue: false hasContentIssue false
  • English
  • Français

ANGIOGENIC IMBALANCES IN THE PATHOGENESIS OF PREGNANCY COMPLICATIONS

Published online by Cambridge University Press:  17 September 2014

JIMMY ESPINOZA
JIMMY ESPINOZA*
Affiliation:
Department of Obstetrics and Gynecology, Baylor College of Medicine and Texas Children's Hospital Pavilion for Women, Houston, TX
*
Dr Jimmy Espinoza, MD, Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Baylor College of Medicine and TCH Pavilion for Women, 6651 Main Street, Suite 1020, Houston TX 77030. Email: jimmy.espinoza@bcm.edu
Get access Rights & Permissions [Opens in a new window]

Extract

Endothelial cell proliferation and survival require continuous low levels of vascular endothelial growth factor (VEGF). The bioavailability of this angiogenic factor appears to be regulated by anti-angiogenic factors, including the soluble form of VEGF receptor 1 (sFlt-1) in the non-pregnant and pregnant states. During pregnancy a VEGF antagonist (sFlt-1) and other anti-angiogenic factors, including soluble endoglin (s-Eng), are produced by the human placenta and released into the maternal circulation; an excess of these anti-angiogenic factors can lead into angiogenic imbalances and pregnancy complications. This is important because regulation of VEGF action on angiogenic balances appears to be essential for a successful pregnancy.

Type
Review Article
Information
Fetal and Maternal Medicine Review , Volume 25 , Issue 1 , February 2014 , pp. 42 - 58
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1.Luttun, A, Carmeliet, P. Soluble VEGF receptor Flt1: the elusive preeclampsia factor discovered? J Clin Invest 2003; 111 (5): 600–2.CrossRefGoogle ScholarPubMed
2.Barleon, B, Reusch, P, Totzke, F, Herzog, C, Keck, C, Martiny-Baron, G, et al.Soluble VEGFR-1 secreted by endothelial cells and monocytes is present in human serum and plasma from healthy donors. Angiogenesis 2001; 4 (2): 143–54.CrossRefGoogle ScholarPubMed
3.Clark, DE, Smith, SK, He, Y, Day, KA, Licence, DR, Corps, AN, et al.A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod 1998; 59 (6): 1540–48.CrossRefGoogle ScholarPubMed
4.Levine, RJ, Maynard, SE, Qian, C, Lim, KH, England, LJ, Yu, KF, et al.Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350 (7): 672–83.CrossRefGoogle ScholarPubMed
5.Levine, RJ, Karumanchi, SA. Circulating angiogenic factors in preeclampsia. Clin Obstet Gynecol 2005; 48 (2): 372–86.CrossRefGoogle ScholarPubMed
6.Maynard, SE, Min, JY, Merchan, J, Lim, KH, Li, J, Mondal, S, 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 (5): 649–58.CrossRefGoogle ScholarPubMed
7.Venkatesha, S, Toporsian, M, Lam, C, Hanai, J, Mammoto, T, Kim, YM, et al.Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12 (6): 642–9.CrossRefGoogle Scholar
8.Ferrara, N, Gerber, HP, LeCouter, J. The biology of VEGF and its receptors. Nat Med 2003; 9 (6): 669–76.CrossRefGoogle ScholarPubMed
9.Ferrara, N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004; 25 (4): 581–611.CrossRefGoogle ScholarPubMed
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 (6, Pt 1): 1539–44.CrossRefGoogle ScholarPubMed
11.Koga, K, Osuga, Y, Yoshino, O, Hirota, Y, Ruimeng, X, Hirata, T, et al.Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003; 88 (5): 2348–51.CrossRefGoogle ScholarPubMed
12.Krauss, T, Pauer, HU, Augustin, HG. Prospective analysis of placenta growth factor (PlGF) concentrations in the plasma of women with normal pregnancy and pregnancies complicated by preeclampsia. Hypertens Pregnancy 2004; 23 (1): 101–11.CrossRefGoogle ScholarPubMed
13.Chaiworapongsa, T, Romero, R, Kim, YM, Kim, GJ, Kim, MR, Espinoza, J, 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 (1): 3–18.CrossRefGoogle Scholar
14.Redman, CW, Sargent, IL. Latest advances in understanding preeclampsia. Science 2005; 308 (5728): 1592–94.CrossRefGoogle ScholarPubMed
15.Bdolah, Y, Karumanchi, SA, Sachs, BP. Recent advances in understanding of preeclampsia. Croat Med J 2005; 46 (5): 728–36.Google ScholarPubMed
16.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 (1): 255–9.CrossRefGoogle ScholarPubMed
17.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 (1): 201–7.CrossRefGoogle ScholarPubMed
18.Levine, RJ, Lam, C, Qian, C, Yu, KF, Maynard, SE, Sachs, BP, et al.Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006; 355 (10): 992–1005.CrossRefGoogle ScholarPubMed
19.Boutsikou, T, Malamitsi-Puchner, A, Economou, E, Boutsikou, M, Puchner, KP, Hassiakos, D. Soluble vascular endothelial growth factor receptor-1 in intrauterine growth restricted fetuses and neonates. Early Hum Dev 2006; 82 (4): 235–9.CrossRefGoogle ScholarPubMed
20.Wallner, W, Sengenberger, R, Strick, R, Strissel, PL, Meurer, B, Beckmann, MW, et al.Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clin Sci (Lond) 2007; 112 (1): 51–7.CrossRefGoogle ScholarPubMed
21.Espinoza, J, Romero, R, Nien, JK, Kusanovic, JP, Richani, K, Gomez, R, 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 (10): 607–13.CrossRefGoogle ScholarPubMed
22.Rana, S, Venkatesha, S, DePaepe, M, Chien, EK, Paglia, M, Karumanchi, SA. Cytomegalovirus-induced mirror syndrome associated with elevated levels of circulating antiangiogenic factors. Obstet Gynecol 2007; 109 (2, Pt2): 549–52.CrossRefGoogle ScholarPubMed
23.Kusanovic, JP, Romero, R, Espinoza, J, Nien, JK, Kim, CJ, Mittal, P, et al.Twin-to-twin transfusion syndrome: an antiangiogenic state? Am J Obstet Gynecol 2008; 198 (4): 382–8.CrossRefGoogle ScholarPubMed
24.Espinoza, J, Chaiworapongsa, T, Romero, R, Kim, YM, Kim, GJ, Nien, JK, et al.Unexplained fetal death: another anti-angiogenic state. J Matern Fetal Neonatal Med 2007; 20 (7): 495–507.CrossRefGoogle ScholarPubMed
25.Espinoza, J, Uckele, JE, Starr, RA, Lorenz, RP, Bronsteen, RA, Berry, SM. Insights into angiogenic imbalances during pregnancy. Obstet Gynecol 2009; 114: 437–440.CrossRefGoogle ScholarPubMed
26.Zhou, Y, McMaster, M, Woo, K, Janatpour, M, Perry, J, Karpanen, T, et al.Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol 2002; 160 (4): 1405–23.CrossRefGoogle ScholarPubMed
27.Tsatsaris, V, Goffin, F, Munaut, C, Brichant, JF, Pignon, MR, Noel, A, et al.Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 2003; 88 (11): 5555–63.CrossRefGoogle ScholarPubMed
28.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 (3): 621–4.CrossRefGoogle ScholarPubMed
29.Signore, C, Mills, JL, Qian, C, Yu, K, Lam, C, Epstein, FH, et al.Circulating angiogenic factors and placental abruption. Obstet Gynecol 2006; 108 (2): 338–44.CrossRefGoogle ScholarPubMed
30.Stepan, H, Faber, R. Elevated sFlt1 level and preeclampsia with parvovirus-induced hydrops. N Engl J Med 2006; 354 (17): 1857–58.CrossRefGoogle ScholarPubMed
31.Kallen, B. Maternal morbidity and mortality in in-vitro fertilization. Best Pract Res Clin Obstet Gynaecol 2008; 22 (3): 549–58.CrossRefGoogle ScholarPubMed
32.Kallen, B, Finnstrom, O, Nygren, KG, Otterblad, OP, Wennerholm, UB. In vitro fertilisation in Sweden: obstetric characteristics, maternal morbidity and mortality. BJOG 2005; 112 (11): 1529–35.CrossRefGoogle ScholarPubMed
33.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 (6): 1142–47.CrossRefGoogle ScholarPubMed
34.Lyall, F, Greer, IA, Boswell, F, Fleming, R. Suppression of serum vascular endothelial growth factor immunoreactivity in normal pregnancy and in pre-eclampsia. Br J Obstet Gynaecol 1997; 104 (2): 223–228.CrossRefGoogle ScholarPubMed
35.Kupferminc, MJ, Daniel, Y, Englender, T, Baram, A, Many, A, Jaffa, AJ, et al.Vascular endothelial growth factor is increased in patients with preeclampsia. Am J Reprod Immunol 1997; 38 (4): 302–306.CrossRefGoogle ScholarPubMed
36.McKeeman, GC, Ardill, JE, Caldwell, CM, Hunter, AJ, 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 (4): 1240–1246.CrossRefGoogle ScholarPubMed
37.Chaiworapongsa, T, Romero, R, Espinoza, J, Bujold, E, Mee, KY, Goncalves, LF, et al.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 (6): 1541–47.CrossRefGoogle ScholarPubMed
38.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 (5, Pt 2): 1R–7R.CrossRefGoogle ScholarPubMed
39.Levine, RJ, Thadhani, R, Qian, C, Lam, C, Lim, KH, Yu, KF, et al.Urinary placental growth factor and risk of preeclampsia. JAMA 2005; 293 (1): 77–85.CrossRefGoogle ScholarPubMed
40.Rajakumar, A, Michael, HM, Rajakumar, PA, Shibata, E, Hubel, CA, Karumanchi, SA, 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 (7): 563–73.CrossRefGoogle ScholarPubMed
41.Shibata, E, Rajakumar, A, Powers, RW, Larkin, RW, Gilmour, C, Bodnar, LM, et al.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 (8): 4895–4903.CrossRefGoogle Scholar
42.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 (1): 33–9.CrossRefGoogle ScholarPubMed
43.Steegers, EA, von Dadelszen, P, Duvekot, JJ, Pijnenborg, R. Pre-eclampsia. Lancet 2010; 376 (9741): 631–44.CrossRefGoogle ScholarPubMed
44.von Dadelszen, P, Magee, LA, Roberts, JM. Subclassification of preeclampsia. Hypertens Pregnancy 2003; 22 (2): 143–8.CrossRefGoogle ScholarPubMed
45.Dekker, GA, Sibai, BM. Etiology and pathogenesis of preeclampsia: current concepts. Am J Obstet Gynecol 1998; 179 (5): 1359–75.CrossRefGoogle ScholarPubMed
46.Austgulen, R, Isaksen, CV, Chedwick, L, Romundstad, P, Vatten, L, Craven, C. Pre-eclampsia: associated with increased syncytial apoptosis when the infant is small-for-gestational-age. J Reprod Immunol 2004; 61 (1): 39–50.CrossRefGoogle ScholarPubMed
47.Crocker, IP, Cooper, S, Ong, SC, Baker, PN. Differences in apoptotic susceptibility of cytotrophoblasts and syncytiotrophoblasts in normal pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am J Pathol 2003; 162 (2): 637–43.CrossRefGoogle ScholarPubMed
48.Leung, DN, Smith, SC, To, KF, Sahota, DS, Baker, PN. Increased placental apoptosis in pregnancies complicated by preeclampsia. Am J Obstet Gynecol 2001; 184 (6): 1249–50.CrossRefGoogle ScholarPubMed
49.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 (2): 153–60.CrossRefGoogle ScholarPubMed
50.Johansen, M, Redman, CW, Wilkins, T, Sargent, IL. Trophoblast deportation in human pregnancy – its relevance for pre-eclampsia. Placenta 1999; 20 (7): 531–9.CrossRefGoogle ScholarPubMed
51.Knight, M, Redman, CW, Linton, EA, Sargent, IL. Shedding of syncytiotrophoblast microvilli into the maternal circulation in pre-eclamptic pregnancies. Br J Obstet Gynaecol 1998; 105 (6): 632–40.CrossRefGoogle ScholarPubMed
52.Chua, S, Wilkins, T, Sargent, I, Redman, C. Trophoblast deportation in pre-eclamptic pregnancy. Br J Obstet Gynaecol 1991; 98 (10): 973–9.CrossRefGoogle ScholarPubMed
53.Makris, A, Thornton, C, Thompson, J, Thomson, S, Martin, R, Ogle, R, et al.Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int 2007; 71 (10): 977–84.CrossRefGoogle ScholarPubMed
54.Nagamatsu, T, Fujii, T, Kusumi, M, Zou, L, Yamashita, T, Osuga, Y, 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 (11): 4838–45.CrossRefGoogle ScholarPubMed
55.Nevo, O, Soleymanlou, N, Wu, Y, Xu, J, Kingdom, J, Many, A, et al.Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol 2006; 291 (4): R1085–R93.CrossRefGoogle ScholarPubMed
56.Chaiworapongsa, T, Espinoza, J, Gotsch, F, Kim, YM, Kim, GJ, Goncalves, LF, 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 (1): 25–40.CrossRefGoogle ScholarPubMed
57.Soto, E, Romero, R, Kusanovic, JP, Ogge, G, Hussein, Y, Yeo, L, et al.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. J Matern Fetal Neonatal Med 2011; 25: 498–507.CrossRefGoogle Scholar
58.Espinoza, J, Uckele, JE, Starr, RA, Seubert, DE, Espinoza, AF, Berry, SM. Angiogenic imbalances: the obstetric perspective. Am J Obstet Gynecol 2010; 203 (1): 17–18.CrossRefGoogle ScholarPubMed
59.Rajakumar, A, Cerdeira, AS, Rana, S, Zsengeller, Z, Edmunds, L, Jeyabalan, A, et al.Transcriptionally active syncytial aggregates in the maternal circulation may contribute to circulating soluble fms-like tyrosine kinase 1 in preeclampsia. Hypertension 2012; 59 (2): 256–64.CrossRefGoogle ScholarPubMed
60.Rana, S, Schnettler, WT, Powe, C, Wenger, J, Salahuddin, S, Cerdeira, AS, et al.Clinical characterization and outcomes of preeclampsia with normal angiogenic profile. Hypertens Pregnancy 2013; 32 (2): 189–201.CrossRefGoogle ScholarPubMed
61.Malamitsi-Puchner, A, Boutsikou, T, Economou, E, Sarandakou, A, Makrakis, E, Hassiakos, D, et al.Vascular endothelial growth factor and placenta growth factor in intrauterine growth-restricted fetuses and neonates. Mediators Inflamm 2005; 2005 (5): 293–7.CrossRefGoogle ScholarPubMed
62.Girardi, G, Yarilin, D, Thurman, JM, Holers, VM, Salmon, JE. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006; 203 (9): 2165–75.CrossRefGoogle ScholarPubMed
63.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 (1): 40–7.CrossRefGoogle ScholarPubMed
64.Sandrim, VC, Palei, AC, Cavalli, RC, Araujo, FM, Ramos, ES, Duarte, G, et al.Vascular endothelial growth factor genotypes and haplotypes are associated with pre-eclampsia but not with gestational hypertension. Mol Hum Reprod 2009; 15 (2): 115–20.CrossRefGoogle Scholar
65.Tjoa, ML, van Vugt, JM, Mulders, MA, Schutgens, RB, Oudejans, CB, van Wijk, IJ. Plasma placenta growth factor levels in midtrimester pregnancies. Obstet Gynecol 2001; 98 (4): 600–7.Google ScholarPubMed
66.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 (6): 1267–72.CrossRefGoogle ScholarPubMed
67.Chappell, LC, Seed, PT, Briley, A, Kelly, FJ, Hunt, BJ, Charnock-Jones, DS, et al.A longitudinal study of biochemical variables in women at risk of preeclampsia. Am J Obstet Gynecol 2002; 187 (1): 127–36.CrossRefGoogle ScholarPubMed
68.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 (1): 177–82.CrossRefGoogle ScholarPubMed
69.Polliotti, BM, Fry, AG, Saller, DN, Mooney, RA, Cox, C, Miller, RK. Second-trimester maternal serum placental growth factor and vascular endothelial growth factor for predicting severe, early-onset preeclampsia. Obstet Gynecol 2003; 101 (6): 1266–74.Google ScholarPubMed
70.Parra, M, Rodrigo, R, Barja, P, Bosco, C, Fernandez, V, Munoz, H, et al.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 (4): 1486–91.CrossRefGoogle ScholarPubMed
71.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 (3): 244–8.Google Scholar
72.Ohkuchi, A, Hirashima, C, Matsubara, S, Suzuki, H, Takahashi, K, Arai, F, 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 (2): 151–9.CrossRefGoogle ScholarPubMed
73.Poon, LC, Zaragoza, E, Akolekar, R, Anagnostopoulos, E, Nicolaides, KH. Maternal serum placental growth factor (PlGF) in small for gestational age pregnancy at 11(+0) to 13(+6) weeks of gestation. Prenat Diagn 2008; 28 (12): 1110–15.CrossRefGoogle Scholar
74.Erez, O, Romero, R, Espinoza, J, Fu, W, Todem, D, Kusanovic, JP, 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 (5): 279–87.CrossRefGoogle ScholarPubMed
75.Poon, LC, Kametas, NA, Maiz, N, Akolekar, R, Nicolaides, KH. First-trimester prediction of hypertensive disorders in pregnancy. Hypertension 2009; 53 (5): 812–18.CrossRefGoogle ScholarPubMed
76.Thadhani, R, Mutter, WP, Wolf, M, Levine, RJ, Taylor, RN, Sukhatme, VP, et al.First trimester placental growth factor and soluble fms-like tyrosine kinase 1 and risk for preeclampsia. J Clin Endocrinol Metab 2004; 89 (2): 770–5.CrossRefGoogle ScholarPubMed
77.Rana, S, Karumanchi, SA, Levine, RJ, Venkatesha, S, Rauh-Hain, JA, Tamez, H, et al.Sequential changes in antiangiogenic factors in early pregnancy and risk of developing preeclampsia. Hypertension 2007; 50 (1): 137–42.CrossRefGoogle ScholarPubMed
78.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 (3): 266.CrossRefGoogle ScholarPubMed
79.Romero, R, Nien, JK, Espinoza, J, Todem, D, Fu, W, Chung, H, 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 (1): 9–23.Google Scholar
80.Schmidt, M, Dogan, C, Birdir, C, Kuhn, U, Gellhaus, A, Kimmig, R, et al.Placental growth factor: a predictive marker for preeclampsia? Gynakol Geburtshilfliche Rundsch 2009; 49 (2): 94–99.CrossRefGoogle ScholarPubMed
81.Espinoza, J, Romero, R, Nien, JK, Gomez, R, Kusanovic, JP, Goncalves, LF. 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 (4): 326.e1–13.CrossRefGoogle ScholarPubMed
82.Espinoza, J. Recent biomarkers for the identification of patients at risk for preeclampsia: the role of uteroplacental ischemia. Expert Opin Med Diagn 2012; 6 (2): 109–20.CrossRefGoogle ScholarPubMed
83.Rasmussen, S, Irgens, LM. Fetal growth and body proportion in preeclampsia. Obstet Gynecol 2003; 101 (3): 575–83.Google ScholarPubMed
84.Aardema, MW, Saro, MC, Lander, M, De Wolf, BT, Oosterhof, H, Aarnoudse, JG. Second trimester Doppler ultrasound screening of the uterine arteries differentiates between subsequent normal and poor outcomes of hypertensive pregnancy: two different pathophysiological entities? Clin Sci (Lond) 2004; 106 (4): 377–82.CrossRefGoogle ScholarPubMed
85.Harrington, K, Cooper, D, Lees, C, Hecher, K, Campbell, S. Doppler ultrasound of the uterine arteries: the importance of bilateral notching in the prediction of pre-eclampsia, placental abruption or delivery of a small-for-gestational-age baby. Ultrasound Obstet Gynecol 1996; 7 (3): 182–88.CrossRefGoogle ScholarPubMed
86.Albaiges, G, Missfelder-Lobos, H, Lees, C, Parra, M, Nicolaides, KH. One-stage screening for pregnancy complications by color Doppler assessment of the uterine arteries at 23 weeks’ gestation. Obstet Gynecol 2000; 96 (4): 559–64.Google Scholar
87.Papageorghiou, AT, Yu, CK, Cicero, S, Bower, S, Nicolaides, KH. Second-trimester uterine artery Doppler screening in unselected populations: a review. J Matern Fetal Neonatal Med 2002; 12 (2): 78–88.CrossRefGoogle ScholarPubMed
88.Papageorghiou, AT, Yu, CK, Bindra, R, Pandis, G, Nicolaides, KH. Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol 2001; 18 (5): 441–449.CrossRefGoogle ScholarPubMed
89.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 (4): 1173–1177.CrossRefGoogle ScholarPubMed
90.Ogge, G, Chaiworapongsa, T, Romero, R, Hussein, Y, Kusanovic, JP, Yeo, L, et al.Placental lesions associated with maternal underperfusion are more frequent in early-onset than in late-onset preeclampsia*. J Perinat Med 2011; 39 (6): 641–52.CrossRefGoogle Scholar
91.Bolin, M, Wiberg-Itzel, E, Wikstrom, AK, Goop, M, Larsson, A, Olovsson, M, et al.Angiopoietin-1/angiopoietin-2 ratio for prediction of preeclampsia. Am J Hypertens 2009; 22 (8): 891–895.CrossRefGoogle ScholarPubMed
92.Kusanovic, JP, Romero, R, Chaiworapongsa, T, Erez, O, Mittal, P, Vaisbuch, E, 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 (11): 1021–38.CrossRefGoogle ScholarPubMed
93.Poon, LC, Maiz, N, Valencia, C, Plasencia, W, Nicolaides, KH. First-trimester maternal serum pregnancy-associated plasma protein-A and pre-eclampsia. Ultrasound Obstet Gynecol 2009; 33 (1): 23–33.CrossRefGoogle ScholarPubMed
94.Chaiworapongsa, T, Romero, R, Savasan, ZA, Kusanovic, JP, Ogge, G, Soto, E, et al.Maternal plasma concentrations of angiogenic/anti-angiogenic factors are of prognostic value in patients presenting to the obstetrical triage area with the suspicion of preeclampsia. J Matern Fetal Neonatal Med 2011; 24 (10): 1187–207.CrossRefGoogle Scholar
95.Stepan, H, Schaarschmidt, W, Jank, A, Verlohren, S, Kratzsch, J. Use of angiogenic factors (sFlt-1/PlGF ratio) to confirm the diagnosis of preeclampsia in clinical routine: first experience. Z Geburtshilfe Neonatol 2010; 214 (6): 234–38.CrossRefGoogle ScholarPubMed
96.Rana, S, Powe, CE, Salahuddin, S, Verlohren, S, Perschel, FH, Levine, RJ, et al.Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia. Circulation 2012; 125 (7): 911–9.Google Scholar
97.Verlohren, S, Herraiz, I, Lapaire, O, Schlembach, D, Zeisler, H, Calda, P, et al.New gestational phase-specific cutoff values for the use of the soluble fms-like tyrosine kinase-1/placental growth factor ratio as a diagnostic test for preeclampsia. Hypertension 2013; 63 (2): 346–52.CrossRefGoogle Scholar
98.Lindheimer, MD, Kanter, D. Interpreting abnormal proteinuria in pregnancy: the need for a more pathophysiological approach. Obstet Gynecol 2010; 115 (2, Pt 1): 365–75.CrossRefGoogle ScholarPubMed
99.Benton, SJ, Hu, Y, Xie, F, Kupfer, K, Lee, SW, Magee, LA, et al.Angiogenic factors as diagnostic tests for preeclampsia: a performance comparison between two commercial immunoassays. Am J Obstet Gynecol 2011; 205 (5): 469–8.CrossRefGoogle ScholarPubMed
100.Sunderji, S, Gaziano, E, Wothe, D, Rogers, LC, Sibai, B, Karumanchi, SA, et al.Automated assays for sVEGF R1 and PlGF as an aid in the diagnosis of preterm preeclampsia: a prospective clinical study. Am J Obstet Gynecol 2010; 202 (1): 40–7.CrossRefGoogle ScholarPubMed
101.Verlohren, S, Herraiz, I, Lapaire, O, Schlembach, D, Moertl, M, Zeisler, H, et al.The sFlt-1/PlGF ratio in different types of hypertensive pregnancy disorders and its prognostic potential in preeclamptic patients. Am J Obstet Gynecol 2012; 206 (1): 58.CrossRefGoogle ScholarPubMed
102.Knudsen, UB, Kronborg, CS, von Dadelszen, P, Kupfer, K, Lee, S, Vittinghus, E, et al.A single rapid point-of-care placental growth factor determination as an aid in the diagnosis of preeclampsia. Pregnancy Hypertens 2012; 2: 8–15.Google Scholar
103.Chappell, LC, Duckworth, S, Seed, PT, Griffin, M, Myers, J, Mackillop, L, et al.Diagnostic accuracy of placental growth factor in women with suspected preeclampsia: a prospective multicenter study. Circulation 2013; 128 (19): 2121–31.CrossRefGoogle ScholarPubMed
104.Espinoza, J, Kusanovic, JP, Bahado-Singh, R, Gervasi, MT, Romero, R, Lee, W, et al.Should bilateral uterine artery notching be used in the risk assessment for preeclampsia, small-for-gestational-age, and gestational hypertension? J Ultrasound Med 2010; 29 (7): 1103–15.CrossRefGoogle ScholarPubMed
105.O’driscoll, DT. A fluid retention syndrome associated with severe iso-immunization to the rhesus factor. J Obstet Gynaecol Br Emp 1956; 63 (3): 372–74.Google Scholar
106.Goodlin, RC. Impending fetal death in utero due to isoimmunization. Obstet Gynecol 1957; 10 (3): 299–302.Google Scholar
107.Scott, JS. Pregnancy toxaemia associated with hydrops foetalis, hydatidiform mole and hydramnios. J Obstet Gynaecol Br Emp 1958; 65 (5): 689–701.CrossRefGoogle ScholarPubMed
108.Cohen, A. Maternal syndrome in Rh iso-immunization: report of a case. J Obstet Gynaecol Br Emp 1960; 67: 325–27.CrossRefGoogle ScholarPubMed
109.Hirsch, MR, Mark, MS. Pseudotoxemia and erythroblastosis. Report of a case. Obstet Gynecol 1964; 24: 47–8.Google Scholar
110.John, AH, Duncan, AS. The Maternal Syndrome associated with hydrops foetalis. J Obstet Gynaecol Br Commonw 1964; 71: 61–5.CrossRefGoogle ScholarPubMed
111.Quagliarello, JR, Passalaqua, AM, Greco, MA, Zinberg, S, Young, BK. Ballantyne's triple edema syndrome: prenatal diagnosis with ultrasound and maternal renal biopsy findings. Am J Obstet Gynecol 1978; 132 (5): 580–81.CrossRefGoogle ScholarPubMed
112.Duthie, SJ, Walkinshaw, SA. Parvovirus associated fetal hydrops: reversal of pregnancy-induced proteinuric hypertension by in utero fetal transfusion. Br J Obstet Gynaecol 1995; 102 (12): 1011–13.CrossRefGoogle ScholarPubMed
113.Carbillon, L, Oury, JF, Guerin, JM, Azancot, A, Blot, P. Clinical biological features of Ballantyne syndrome and the role of placental hydrops. Obstet Gynecol Surv 1997; 52 (5): 310–14.CrossRefGoogle ScholarPubMed
114.Ordorica, SA, Marks, F, Frieden, FJ, Hoskins, IA, Young, BK. Aneurysm of the vein of Galen: a new cause for Ballantyne syndrome. Am J Obstet Gynecol 1990; 162 (5): 1166–67.CrossRefGoogle ScholarPubMed
115.Midgley, DY, Harding, K. The Mirror syndrome. Eur J Obstet Gynecol Reprod Biol 2000; 88 (2): 201–2.CrossRefGoogle ScholarPubMed
116.Finamore, PS, Kontopoulos, E, Price, M, Giannina, G, Smulian, JC. Mirror syndrome associated with sacrococcygeal teratoma: a case report. J Reprod Med 2007; 52 (3): 225–7.Google ScholarPubMed
117.Dorman, SL, Cardwell, MS. Ballantyne syndrome caused by a large placental chorioangioma. Am J Obstet Gynecol 1995; 173 (5): 1632–33.CrossRefGoogle ScholarPubMed
118.Barker, G, Boyd, RD, D’Souza, SW, Donnai, P, Fox, H, Sibley, CP. Placental water content and distribution. Placenta 1994; 15 (1): 47–56.CrossRefGoogle ScholarPubMed
119.Kovalovszki, L, Villanyi, E, Benko, G. Placental villous edema: a possible cause of antenatal hypoxia. Acta Paediatr Hung 1990; 30 (2): 209–15.Google Scholar
120.Naeye, RL, Maisels, MJ, Lorenz, RP, Botti, JJ. The clinical significance of placental villous edema. Pediatrics 1983; 71 (4): 588–94.CrossRefGoogle ScholarPubMed
121.Alvarez, H, Sala, MA, Benedetti, WL. Intervillous space reduction in the edematous placenta. Am J Obstet Gynecol 1972; 112 (6): 819–20.CrossRefGoogle ScholarPubMed
122.Stepan, H, Faber, R. Cytomegalovirus-induced mirror syndrome associated with elevated levels of angiogenic factors. Obstet Gynecol 2007; 109 (5): 1205–6.CrossRefGoogle ScholarPubMed
123.Koga, K, Osuga, Y, Tajima, T, Hirota, Y, Igarashi, T, Fujii, T, et al.Elevated serum soluble fms-like tyrosine kinase 1 (sFlt1) level in women with hydatidiform mole. Fertil Steril 2009; 94 (1): 305–8.CrossRefGoogle Scholar
124.Soto-Wright, V, Bernstein, M, Goldstein, DP, Berkowitz, RS. The changing clinical presentation of complete molar pregnancy. Obstet Gynecol 1995; 86 (5): 775–9.CrossRefGoogle ScholarPubMed
125.Jauniaux, E. Partial moles: from postnatal to prenatal diagnosis. Placenta 1999; 20 (5–6): 379–88.CrossRefGoogle ScholarPubMed
126.Prasannan-Nair, C, Reynolds, SF, Budden, G. Partial molar pregnancy with severe pre-eclampsia at 19 weeks’ gestation. J Obstet Gynaecol 2006; 26 (8): 817.CrossRefGoogle Scholar
127.Stefos, T, Plachouras, N, Mari, G, Cosmi, E, Lolis, D. A case of partial mole and atypical type I triploidy associated with severe HELLP syndrome at 18 weeks’ gestation. Ultrasound Obstet Gynecol 2002; 20 (4): 403–4.CrossRefGoogle ScholarPubMed
128.Sherer, DM, Dalloul, M, Stimphil, R, Hellmann, M, Khoury-Collado, F, Osho, J, et al.Acute onset of severe hemolysis, elevated liver enzymes, and low platelet count syndrome in a patient with a partial hydatidiform mole at 17 weeks gestation. Am J Perinatol 2006; 23 (3): 163–6.CrossRefGoogle Scholar
129.Jank, A, Kratzsch, J, Stepan, H. Effect of terminated fetal circulation on maternal angiogenic factors in severe early preeclampsia. Hypertens Pregnancy 2012.CrossRefGoogle Scholar
130.Benirschke, K, Kaufmann, P, Baergen, R. Molar pregnancies. In: Benirschke, K, Kaufmann, P, Baergen, R (eds.) Pathology of the Human Placenta. New York, NY: Springer, 2006; 797–836.Google Scholar
131.Qiao, S, Nagasaka, T, Nakashima, N. Numerous vessels detected by CD34 in the villous stroma of complete hydatidiform moles. Int J Gynecol Pathol 1997; 16 (3): 233–8.CrossRefGoogle ScholarPubMed
132.Sibai, BM, Stella, CL. Diagnosis and management of atypical preeclampsia-eclampsia. Am J Obstet Gynecol 2009; 200 (5): 481–7.CrossRefGoogle ScholarPubMed
133.Burton, GJ, Charnock-Jones, DS, Jauniaux, E. Regulation of vascular growth and function in the human placenta. Reproduction 2009; 138 (6): 895–902.Google Scholar
134.Espinoza, J, Espinoza, AF. Pre-eclampsia: a maternal manifestation of a fetal adaptive response? Ultrasound Obstet Gynecol 2011; 38 (4): 367–70.CrossRefGoogle ScholarPubMed
135.Espinoza, J, Espinoza, AF, Power, GG. High fetal plasma adenosine concentration: a role for the fetus in preeclampsia? Am J Obstet Gynecol 2011; 205 (5): 485.e24-7.CrossRefGoogle Scholar
136.Jeyabalan, A, McGonigal, S, Gilmour, C, Hubel, CA, Rajakumar, A. Circulating and placental endoglin concentrations in pregnancies complicated by intrauterine growth restriction and preeclampsia. Placenta 2008; 29 (6): 555–63.CrossRefGoogle ScholarPubMed
137.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 (5, Pt 1): 760–5.CrossRefGoogle ScholarPubMed
138.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 (3): 161–8.Google Scholar
139.Aardema, MW, Oosterhof, H, Timmer, A, van, R, I, Aarnoudse, JG. 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 (5): 405–11.CrossRefGoogle ScholarPubMed
140.Madazli, R, Somunkiran, A, Calay, Z, Ilvan, S, Aksu, MF. 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 (5): 510–16.CrossRefGoogle ScholarPubMed
141.Voigt, HJ, Becker, V. Doppler flow measurements and histomorphology of the placental bed in uteroplacental insufficiency. J Perinat Med 1992; 20 (2): 139–47.CrossRefGoogle ScholarPubMed
142.Espinoza, J, Romero, R, Mee, KY, Kusanovic, JP, Hassan, S, Erez, O, et al.Normal and abnormal transformation of the spiral arteries during pregnancy. J Perinat Med 2006; 34 (6): 447–58.Google Scholar
143.Pijnenborg, R, Vercruysse, L, Hanssens, M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006; 27 (9–10): 939–58.CrossRefGoogle ScholarPubMed
144.Kosaka, K, Fujiwara, H, Yoshioka, S, Fujii, S. Vascular endothelial growth factor production by circulating immune cells is elevated in ovarian hyperstimulation syndrome. Hum Reprod 2007; 22 (6): 1647–51.CrossRefGoogle ScholarPubMed
145.Pau, E, Alonso-Muriel, I, Gomez, R, Novella, E, Ruiz, A, Garcia-Velasco, JA, et al.Plasma levels of soluble vascular endothelial growth factor receptor-1 may determine the onset of early and late ovarian hyperstimulation syndrome. Hum Reprod 2006; 21 (6): 1453–60.CrossRefGoogle ScholarPubMed
146.Gomez, R, Simon, C, Remohi, J, Pellicer, A. Administration of moderate and high doses of gonadotropins to female rats increases ovarian vascular endothelial growth factor (VEGF) and VEGF receptor-2 expression that is associated to vascular hyperpermeability. Biol Reprod 2003; 68 (6): 2164–71.CrossRefGoogle ScholarPubMed
147.Gomez, R, Simon, C, Remohi, J, Pellicer, A. Vascular endothelial growth factor receptor-2 activation induces vascular permeability in hyperstimulated rats, and this effect is prevented by receptor blockade. Endocrinology 2002; 143 (11): 4339–48.CrossRefGoogle ScholarPubMed
148.Luttun, A, Tjwa, M, Carmeliet, P. Placental growth factor (PlGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann N Y Acad Sci 2002; 979: 80–93.CrossRefGoogle ScholarPubMed
149.Li, Z, Zhang, Y, Ying, MJ, Kapoun, AM, Shao, Q, Kerr, I, et al.Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 2007; 50 (4): 686–92.CrossRefGoogle Scholar
150.Thadhani, R, Kisner, T, Hagmann, H, Bossung, V, Noack, S, Schaarschmidt, W, et al.Pilot study of extracorporeal removal of soluble fms-like tyrosine kinase-1 in preeclampsia. Circulation 2011; 124 (8): 940–50.Google Scholar