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Research Article

Plasma concentrations of angiogenic/anti-angiogenic factors have prognostic value in women presenting with suspected preeclampsia to the obstetrical triage area: a prospective study

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Pages 132-144 | Received 15 Apr 2013, Accepted 16 May 2013, Published online: 08 Aug 2013

References

  • Romero R, Lockwood C, Oyarzun E, Hobbins JC. Toxemia: new concepts in an old disease. Semin Perinatol 1988;12:302–23
  • Di Renzo GC. The great obstetrical syndromes. J Matern Fetal Neonatal Med 2009;22:633–5
  • Romero R. Prenatal medicine: the child is the father of the man. Prenat Neonat Med 1996;1:8–11
  • 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
  • Gervasi MT, Chaiworapongsa T, Pacora P, et al. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001;185:792–7
  • Redman CW, Sacks GP, Sargent IL. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999;180:499–506
  • Redman CW, Sargent IL. Preeclampsia and the systemic inflammatory response. Semin Nephrol 2004;24:565–70
  • Roberts JM. Endothelial dysfunction in preeclampsia. Semin Reprod Endocrinol 1998;16:5–15
  • Roberts JM. Objective evidence of endothelial dysfunction in preeclampsia. Am J Kidney Dis 1999;33:992–7
  • Chaiworapongsa T, Romero R, Yoshimatsu J, et al. Soluble adhesion molecule profile in normal pregnancy and pre-eclampsia. J Matern Fetal Neonatal Med 2002;12:19–27
  • Petrozella L, Mahendroo M, Timmons B, et al. Endothelial microparticles and the antiangiogenic state in preeclampsia and the postpartum period. Am J Obstet Gynecol 2012;207:140–6
  • Cunningham FG, Pritchard JA. Hematologic considerations of pregnancy-induced hypertension. Semin Perinatol 1978;2:29–38
  • Weenink GH, Treffers PE, Vijn P, et al. Antithrombin III levels in preeclampsia correlate with maternal and fetal morbidity. Am J Obstet Gynecol 1984;148:1092–7
  • Chaiworapongsa T, Yoshimatsu J, Espinoza J, et al. Evidence of in vivo generation of thrombin in patients with small-for-gestational-age fetuses and pre-eclampsia. J Matern Fetal Neonatal Med 2002;11:362–7
  • de Boer K, ten Cate JW, Sturk A, et al. Enhanced thrombin generation in normal and hypertensive pregnancy. Am J Obstet Gynecol 1989;160:95–100
  • Erez O, Romero R, Kim SS, 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;21:345–55
  • Dekker G. Prothrombotic mechanisms in preeclampsia. Thromb Res 2005;115:17–21
  • Erez O, Romero R, Hoppensteadt D, et al. Tissue factor and its natural inhibitor in pre-eclampsia and SGA. J Matern Fetal Neonatal Med 2008;21:855–69
  • 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;4:246 A
  • Zhou Y, McMaster M, Woo K, 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;160:1405–23
  • Tsatsaris V, Goffin F, Munaut C, et al. Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J Clin Endocrinol Metab 2003;88:5555–63
  • Maynard SE, Min JY, Merchan J, 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;111:649–58
  • Koga K, Osuga Y, Yoshino O, et al. Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J Clin Endocrinol Metab 2003;88:2348–51
  • Levine RJ, Maynard SE, Qian C, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004;350:672–83
  • Chaiworapongsa T, Romero R, Espinoza J, 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;190:1541–7
  • Nagamatsu T, Fujii T, Kusumi 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;145:4838–45
  • Ahmad S, Ahmed A. Antiangiogenic effect of soluble vascular endothelial growth factor receptor-1 in placental angiogenesis. Endothelium 2005;12:89–95
  • Chaiworapongsa T, Romero R, Kim YM, 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
  • Venkatesha S, Toporsian M, Lam C, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006;12:642–9
  • Levine RJ, Lam C, Qian C, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006;355:992–1005
  • Vatten LJ, Eskild A, Nilsen TI, et al. Changes in circulating level of angiogenic factors from the first to second trimester as predictors of preeclampsia. Am J Obstet Gynecol 2007;196:239–6
  • Romero R, Nien JK, Espinoza J, 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
  • Erez O, Romero R, Espinoza J, 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;21:279–87
  • Stepan H. Angiogenic factors and pre-eclampsia: an early marker is needed. Clin Sci (Lond) 2009;116:231–2
  • Kusanovic JP, Romero R, Chaiworapongsa T, 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;22:1021–38
  • Chaiworapongsa T, Romero R, Kusanovic JP, 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;35:155–62
  • Ogge G, Chaiworapongsa T, Romero R, et al. Placental lesions associated with maternal underperfusion are more frequent in early-onset than in late-onset preeclampsia. J Perinat Med 2011;39:641–52
  • Weed S, Bastek JA, Anton L, et al. Examining the correlation between placental and serum placenta growth factor in preeclampsia. Am J Obstet Gynecol 2012;207:140–6
  • Weissgerber TL, Roberts JM, Jeyabalan A, et al. Haptoglobin phenotype, angiogenic factors, and preeclampsia risk. Am J Obstet Gynecol 2012;206:358
  • Soto E, Romero R, Kusanovic JP, 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 2012;25:498–507
  • Martin JN, Jr, Rinehart BK, May WL, et al. The spectrum of severe preeclampsia: comparative analysis by HELLP (hemolysis, elevated liver enzyme levels, and low platelet count) syndrome classification. Am J Obstet Gynecol 1999;180:1373–84
  • Romero R, Mazor M, Lockwood CJ, et al. Clinical significance, prevalence, and natural history of thrombocytopenia in pregnancy-induced hypertension. Am J Perinatol 1989;6:32–8
  • Romero R, Vizoso J, Emamian M, et al. Clinical significance of liver dysfunction in pregnancy-induced hypertension. Am J Perinatol 1988;5:146–51
  • Belfort M, Van VT, White GL, et al. Low maternal middle cerebral artery Doppler resistance indices can predict future development of preeclampsia. Ultrasound Obstet Gynecol 2012;40:406--11
  • Kobayashi T, Terao T. Preeclampsia as chronic disseminated intravascular coagulation. Study of two parameters: thrombin-antithrombin III complex and D-dimers. Gynecol Obstet Invest 1987;24:170–8
  • Lindheimer MD, Taler SJ, Cunningham FG. Hypertension in pregnancy. J Am Soc Hypertens 2010;4:68–78
  • Melchiorre K, Thilaganathan B. Maternal cardiac function in preeclampsia. Curr Opin Obstet Gynecol 2011;23:440–7
  • Parrish MR, Laye MR, Wood T, et al. Impedance cardiography facilitates differentiation of severe and superimposed preeclampsia from other hypertensive disorders. Hypertens Pregnancy 2012;31:327--40
  • Riskin-Mashiah S, Belfort MA, Saade GR, Herd AJ. Side-to-side differences in transcranial Doppler parameters in normotensive and preeclamptic pregnant women. Am J Obstet Gynecol 2004;190:194–8
  • Barton JR, Sibai BM. Gastrointestinal complications of pre-eclampsia. Semin Perinatol 2009;33:179–88
  • Weinstein L. Syndrome of hemolysis, elevated liver enzymes, and low platelet count: a severe consequence of hypertension in pregnancy. Am J Obstet Gynecol 1982;142:159–67
  • MacKenna J, Dover NL, Brame RG. Preeclampsia associated with hemolysis, elevated liver enzymes, and low platelets–an obstetric emergency? Obstet Gynecol 1983;62:751–4
  • Martin JN, Jr, Blake PG, Perry KG, Jr, et al. The natural history of HELLP syndrome: patterns of disease progression and regression. Am J Obstet Gynecol 1991;164:1500–9
  • de Boer K, Buller HR, ten Cate JW, Treffers PE. Coagulation studies in the syndrome of haemolysis, elevated liver enzymes and low platelets. Br J Obstet Gynaecol 1991;98:42–7
  • Patten IS, Rana S, Shahul S, et al. Cardiac angiogenic imbalance leads to peripartum cardiomyopathy. Nature 2012;485:333–8
  • Hinchey J, Chaves C, Appignani B, et al. A reversible posterior leukoencephalopathy syndrome. N Engl J Med 1996;334:494–500
  • Oehm E, Hetzel A, Els T, et al. Cerebral hemodynamics and autoregulation in reversible posterior leukoencephalopathy syndrome caused by pre-/eclampsia. Cerebrovasc Dis 2006;22:204–8
  • Melchiorre K, Sutherland GR, Baltabaeva A, et al. Maternal cardiac dysfunction and remodeling in women with preeclampsia at term. Hypertension 2011;57:85–93
  • Reuwer AQ, Reuwer PJ, van der Post JA, et al. Prolactin fragmentation by trophoblastic matrix metalloproteinases as a possible contributor to peripartum cardiomyopathy and pre-eclampsia. Med Hypotheses 2010;74:348–52
  • Escher G, Mohaupt M. Role of aldosterone availability in preeclampsia. Mol Aspects Med 2007;28:245–54
  • 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;25:313–27
  • Ananth CV, Vintzileos AM. Ischemic placental disease: epidemiology and risk factors. Eur J Obstet Gynecol Reprod Biol 2011;159:77–82
  • Drewlo S, Czikk M, Baczyk D, et al. Glial cell missing-1 mediates over-expression of tissue inhibitor of metalloproteinase-4 in severe pre-eclamptic placental villi. Hum Reprod 2011;26:1025–34
  • ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Number 33, January 2002. American College of Obstetricians and Gynecologists. Int J Gynaecol Obstet 2002;77:67–75
  • Hirashima C, Ohkuchi A, Takahashi K, et al. Gestational hypertension as a subclinical preeclampsia in view of serum levels of angiogenesis-related factors. Hypertens Res 2011;34:212–7
  • Liu CM, Cheng PJ, Chang SD. Maternal complications and perinatal outcomes associated with gestational hypertension and severe preeclampsia in Taiwanese women. J Formos Med Assoc 2008;107:129–38
  • Walker RL, Hemmelgarn B, Quan H. Incidence of gestational hypertension in the Calgary Health Region from 1995 to 2004. Can J Cardiol 2009;25:e284–e287
  • Homer CS, Brown MA, Mangos G, Davis GK. Non-proteinuric pre-eclampsia: a novel risk indicator in women with gestational hypertension. J Hypertens 2008;26:295–302
  • donald-Wallis C, Lawlor DA, Heron J, et al. Relationships of risk factors for pre-eclampsia with patterns of occurrence of isolated gestational proteinuria during normal term pregnancy. PLoS One 2011;6:e22115
  • Morikawa M, Yamada T, Minakami H. Outcome of pregnancy in patients with isolated proteinuria. Curr Opin Obstet Gynecol 2009;21:491–5
  • Holston AM, Qian C, Yu KF, et al. Circulating angiogenic factors in gestational proteinuria without hypertension. Am J Obstet Gynecol 2009;200:392–10
  • Ohkuchi A, Hirashima C, Matsubara S, et al. Serum sFlt1:PlGF ratio, PlGF, and soluble endoglin levels in gestational proteinuria. Hypertens Pregn 2009;28:95–108
  • Morikawa M, Yamada T, Yamada T, et al. Pregnancy outcome of women who developed proteinuria in the absence of hypertension after mid-gestation. J Perinat Med 2008;36:419–24
  • Sibai BM, Stella CL. Diagnosis and management of atypical preeclampsia-eclampsia. Am J Obstet Gynecol 2009;200:481–7
  • Aarnoudse JG, Houthoff HJ, Weits J, et al. A syndrome of liver damage and intravascular coagulation in the last trimester of normotensive pregnancy. A clinical and histopathological study. Br J Obstet Gynaecol 1986;93:145–55
  • Goodlin RC. Severe pre-eclampsia: another great imitator. Am J Obstet Gynecol 1976;125:747–53
  • Bailey DJ, Walton SM. Routine investigations might be useful in pre-eclampsia, but not in gestational hypertension. Aust N Z J Obstet Gynaecol 2005;45:144–7
  • Saudan P, Brown MA, Buddle ML, Jones M. Does gestational hypertension become pre-eclampsia? Br J Obstet Gynaecol 1998;105:1177–84
  • Milne F, Redman C, Walker J, et al. Assessing the onset of pre-eclampsia in the hospital day unit: summary of the pre-eclampsia guideline (PRECOG II). Br Med J 2009;339:b3129
  • Sibai BM. Evaluation and management of severe preeclampsia before 34 weeks' gestation. Am J Obstet Gynecol 2011;205:191–8
  • Sibai BM. Diagnosis and management of gestational hypertension and preeclampsia. Obstet Gynecol 2003;102:181–92
  • Anumba DO, Lincoln K, Robson SC. Predictive value of clinical and laboratory indices at first assessment in women referred with suspected gestational hypertension. Hypertens Pregnancy 2010;29:163–79
  • Thangaratinam S, Ismail KM, Sharp S, et al. Accuracy of serum uric acid in predicting complications of pre-eclampsia: a systematic review. BJOG 2006;113:369–78
  • Menzies J, Magee LA, MacNab YC, et al. Current CHS and NHBPEP criteria for severe preeclampsia do not uniformly predict adverse maternal or perinatal outcomes. Hypertens Pregnancy 2007;26:447–62
  • Bell SC, Halligan AW, Martin A, et al. The role of observer error in antenatal dipstick proteinuria analysis. Br J Obstet Gynaecol 1999;106:1177–80
  • Bellomo G, Venanzi S, Saronio P, et al. Prognostic significance of serum uric acid in women with gestational hypertension. Hypertension 2011;58:704–8
  • van der Tuuk K, Koopmans CM, Groen H, et al. Prediction of progression to a high risk situation in women with gestational hypertension or mild pre-eclampsia at term. Aust N Z J Obstet Gynaecol 2011;51:339–46
  • Thornton CE, Makris A, Ogle RF, et al. Role of proteinuria in defining pre-eclampsia: clinical outcomes for women and babies. Clin Exp Pharmacol Physiol 2010;37:466–70
  • Paula LG, da Costa BE, Poli-de-Figueiredo CE, Antonello IC. Does uric acid provide information about maternal condition and fetal outcome in pregnant women with hypertension? Hypertens Pregn 2008;27:413–20
  • Martin JN, Jr, May WL, Magann EF, et al. Early risk assessment of severe preeclampsia: admission battery of symptoms and laboratory tests to predict likelihood of subsequent significant maternal morbidity. Am J Obstet Gynecol 1999;180:1407–14
  • Haddad B, Barton JR, Livingston JC, et al. Risk factors for adverse maternal outcomes among women with HELLP (hemolysis, elevated liver enzymes, and low platelet count) syndrome. Am J Obstet Gynecol 2000;183:444–8
  • Cavkaytar S, Ugurlu EN, Karaer A, et al. Are clinical symptoms more predictive than laboratory parameters for adverse maternal outcome in HELLP syndrome? Acta Obstet Gynecol Scand 2007;86:648–51
  • Witlin AG, Saade GR, Mattar F, Sibai BM. Risk factors for abruptio placentae and eclampsia: analysis of 445 consecutively managed women with severe preeclampsia and eclampsia. Am J Obstet Gynecol 1999;180:1322–9
  • Ganzevoort W, Rep A, Bonsel GJ, et al. Dynamics and incidence patterns of maternal complications in early-onset hypertension of pregnancy. BJOG 2007;114:741–50
  • Oney T, Meyer-Sabellek W. Variability of arterial blood pressure in normal and hypertensive pregnancy. J Hypertens Suppl 1990;8:S77–S81
  • Lindheimer MD, Kanter D. Interpreting abnormal proteinuria in pregnancy: the need for a more pathophysiological approach. Obstet Gynecol 2010;115:365–75
  • Nisell H, Palm K, Wolff K. Prediction of maternal and fetal complications in preeclampsia. Acta Obstet Gynecol Scand 2000;79:19–23
  • Sibai BM, Barton JR. Expectant management of severe preeclampsia remote from term: patient selection, treatment, and delivery indications. Am J Obstet Gynecol 2007;196:514–9
  • Odendaal HJ, Pattinson RC, du TR. Fetal and neonatal outcome in patients with severe pre-eclampsia before 34 weeks. S Afr Med J 1987;71:555–8
  • Ganzevoort W, Rep A, de Vries JI, et al. Prediction of maternal complications and adverse infant outcome at admission for temporizing management of early-onset severe hypertensive disorders of pregnancy. Am J Obstet Gynecol 2006;195:495–503
  • Gazmararian JA, Petersen R, Jamieson DJ, et al. Hospitalizations during pregnancy among managed care enrollees. Obstet Gynecol 2002;100:94–100
  • Bacak SJ, Callaghan WM, Dietz PM, Crouse C. Pregnancy-associated hospitalizations in the United States, 1999-2000. Am J Obstet Gynecol 2005;192:592–7
  • Callaghan WM, MacKay AP, Berg CJ. Identification of severe maternal morbidity during delivery hospitalizations, United States, 1991–2003. Am J Obstet Gynecol 2008;199:133–8
  • Liu S, Heaman M, Sauve R, et al. An analysis of antenatal hospitalization in Canada, 1991–2003. Matern Child Health J 2007;11:181–7
  • Brooten D, Kaye J, Poutasse SM, et al. Frequency, timing, and diagnoses of antenatal hospitalizations in women with high-risk pregnancies. J Perinatol 1998;18:372–6
  • Chaiworapongsa T, Romero R, Savasan ZA, 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;24:1187–207
  • Stoll BJ, Hansen NI, Bell EF, et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics 2010;126:443–56
  • Clark RH. The epidemiology of respiratory failure in neonates born at an estimated gestational age of 34 weeks or more. J Perinatol 2005;25:251–7
  • Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 1978;92:529–34
  • Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;163:1723–9
  • DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988;44:837–45
  • Rana S, Powe CE, Salahuddin S, et al. Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia. Circulation 2012;125:911–9
  • Pencina MJ, D'Agostino RB Sr. Thoroughly modern risk prediction? Sci Transl Med 2012;4:131fs10
  • von Dadelszen P, Payne B, Li J, et al. Prediction of adverse maternal outcomes in pre-eclampsia: development and validation of the fullPIERS model. Lancet 2011;377:219–27
  • Sibiude J, Guibourdenche J, Dionne MD, et al. Placental growth factor for the prediction of adverse outcomes in patients with suspected preeclampsia or intrauterine growth restriction. PLoS One 2012;7:e50208
  • Moore AG, Young H, Keller JM, et al. Angiogenic biomarkers for prediction of maternal and neonatal complications in suspected preeclampsia. J Matern Fetal Neonatal Med 2012;25:2651–7
  • Cook NR. Use and misuse of the receiver operating characteristic curve in risk prediction. Circulation 2007;115:928–35
  • Hlatky MA, Greenland P, Arnett DK, et al. Criteria for evaluation of novel markers of cardiovascular risk: a scientific statement from the American Heart Association. Circulation 2009;119:2408–16
  • Cook NR. Statistical evaluation of prognostic versus diagnostic models: beyond the ROC curve. Clin Chem 2008;54:17–23
  • Molvarec A, Szarka A, Walentin S, et al. Circulating angiogenic factors determined by electrochemiluminescence immunoassay in relation to the clinical features and laboratory parameters in women with pre-eclampsia. Hypertens Res 2010;33:892–8
  • Ohkuchi A, Hirashima C, Suzuki H, et al. Evaluation of a new and automated electrochemiluminescence immunoassay for plasma sFlt-1 and PlGF levels in women with preeclampsia. Hypertens Res 2010;33:422–7
  • Schiettecatte J, Russcher H, Anckaert E, et al. Multicenter evaluation of the first automated Elecsys sFlt-1 and PlGF assays in normal pregnancies and preeclampsia. Clin Biochem 2010;43:768–70
  • Verlohren S, Galindo A, Schlembach D, et al. An automated method for the determination of the sFlt-1/PIGF ratio in the assessment of preeclampsia. Am J Obstet Gynecol 2010;202:161

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