Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia
Open accessAbstract
BACKGROUND: An imbalance in circulating angiogenic factors plays a central role in the pathogenesis of preeclampsia. METHODS AND RESULTS: We prospectively studied 616 women who were evaluated for suspected preeclampsia. We measured plasma levels of antiangiogenic soluble fms-like tyrosine kinase 1 (sFlt1) and proangiogenic placental growth factor (PlGF) at presentation and examined for an association between the sFlt1/PlGF ratio and subsequent adverse maternal and perinatal outcomes within 2 weeks. The median sFlt1/PlGF ratio at presentation was elevated in participants who experienced any adverse outcome compared with those who did not (47.0 [25th-75th percentile, 15.5-112.2] versus 10.8 [25th-75th percentile, 4.1-28.6]; P<0.0001). Among those presenting at <34 weeks (n=167), the results were more striking (226.6 [25th-75th percentile, 50.4-547.3] versus 4.5 [25th-75th percentile, 2.0-13.5]; P<0.0001), and the risk was markedly elevated when the highest sFlt1/PlGF ratio tertile was compared with the lowest (odds ratio, 47.8; 95% confidence interval, 14.6-156.6). Among participants presenting at <34 weeks, the addition of sFlt1/PlGF ratio to hypertension and proteinuria significantly improved the prediction for subsequent adverse outcomes (area under the curve, 0.93 for hypertension, proteinuria, and sFlt1/PlGF versus 0.84 for hypertension and proteinuria alone; P=0.001). Delivery occurred within 2 weeks of presentation in 86.0% of women with an sFlt1/PlGF ratio ≥85 compared with 15.8% of women with an sFlt1/PlGF ratio <85 (hazard ratio, 15.2; 95% confidence interval, 8.0-28.7). CONCLUSIONS: In women with suspected preeclampsia presenting at <34 weeks, circulating sFlt1/PlGF ratio predicts adverse outcomes occurring within 2 weeks. The accuracy of this test is substantially better than that of current approaches and may be useful in risk stratification and management. Additional studies are warranted to validate these findings.
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The increase of sVEGFR-1 causes a parallel decrease of maternal plasma concentrations of PlGF in preeclampsia.
“The increase of sVEGFR-1 causes a parallel decrease of maternal plasma concentrations of PIGF in preeclampsia(119, 143–150).”
From Metformin, the Aspirin of the 21st Century: Its Role in Gestational Diabetes Mellitus, Prevention of Preeclampsia and Cancer, and the Promotion of Longevity (2017) · cites this paper as [146]
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Placental Growth Factor Administration Abolishes Placental Ischemia-Induced Hypertension
Spradley, F. T., Tan, A. Y., Joo, W. S., Daniels, G., Kussie, P. H., Karumanchi, S. A., & Granger, J. P. (2016) · Hypertension · doi:10.1161/hypertensionaha.115.06783 · Cited by 145 · see citing works
“predicting the development of preeclampsia and its related complications.(34) Indeed, among high-risk individuals, this”
BackgroundAdvances in the pathophysiology of pre-eclampsia and related podocyte injury
Craici, I. M., Wagner, S. J., Weissgerber, T. L., Grande, J. P., & Garovic, V. D. (2014) · Kidney International · doi:10.1038/ki.2014.17 · Cited by 146 · see citing works
Chaiworapongsa, T., Romero, R. J., Korzeniewski, S. J., Kusanovic, J. P., Soto, E., Lam, J., Dong, Z., Than, N. G., Yeo, L., Hernandez‐Andrade, E. A., et al. (2013) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2013.01.016 · Cited by 144 · see citing works
Maternal cardiac metabolism in pregnancy
Liu, L. X., & Arany, Z. P. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu009 · Cited by 144 · see citing works
Zeisler, H., Llurba, E., Chantraine, F., Vatish, M., Staff, A. C., Sennström, M., Olovsson, M. H., Brennecke, S. P., Stepan, H., Allegranza, D., et al. (2018) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.19178 · Cited by 144 · see citing works
Circulating Angiogenic Factor Levels in Hypertensive Disorders of Pregnancy
Thadhani, R., Lemoine, E. R., Rana, S., Costantine, M. M., Calsavara, V. F., Boggess, K., Wylie, B. J., Simas, T. A. M., Louis, J. M., Espinoza, J., et al. (2022) · NEJM Evidence · doi:10.1056/evidoa2200161 · Cited by 149 · see citing works
“Often, when these measures become significantly altered, end-organ damage has already ensued.(9,10) Furthermore, frequent testing, prolonged hospitalizations, and unclear diagnoses cause significant stress to pregnant women.”
BackgroundMethodInfluentialNeutrophil NETs in reproduction: from infertility to preeclampsia and the possibility of fetal loss
Hahn, S., Giaglis, S., Hoesli, I. M., & Hasler, P. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00362 · Cited by 142 · see citing works
“These may include the imbalance of placentally produced angiogenic factors (Powe et al., 2011; Rana et al., 2012), or the dysregulation of inflammatory cytokine networks (Rusterholz et al., 2007; Granne et al., 2011).”
BackgroundAssociation Between Hypertensive Disorders of Pregnancy and Later Risk of Cardiomyopathy
Behrens, I., Basit, S., Lykke, J. A., Ranthe, M. F., Wohlfahrt, J., Bundgaard, H., Melbye, M., & Boyd, H. A. (2016) · JAMA · doi:10.1001/jama.2016.1869 · Cited by 144 · see citing works
Diagnosis of acute neurological emergencies in pregnant and post-partum women
Edlow, J. A., Caplan, L. R., O’Brien, K., & Tibbles, C. D. (2013) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70306-x · Cited by 141 · see citing works
Bian, X.-M., Biswas, A., Huang, X., Lee, K. J., Li, T. K. T., Masuyama, H., Ohkuchi, A., Park, J. S., Saito, S., Tan, K. H., et al. (2019) · Hypertension · doi:10.1161/hypertensionaha.119.12760 · Cited by 141 · see citing works
Herraı̀z, I., Llurba, E., Verlohren, S., Galindo, A., & on behalf of the Spanish Group for the Study of Angiogenic Markers in Preeclampsia (2017) · Fetal Diagnosis and Therapy · doi:10.1159/000477903 · Cited by 140 · see citing works
The Promise of Angiogenic Markers for the Early Diagnosis and Prediction of Preeclampsia
Hagmann, H., Thadhani, R., Benzing, T. R., Karumanchi, S. A., & Stepan, H. (2012) · Clinical Chemistry · doi:10.1373/clinchem.2011.169094 · Cited by 136 · see citing works
Pre-eclampsia part 2: prediction, prevention and management
Chaiworapongsa, T., Chaemsaithong, P., Korzeniewski, S. J., Yeo, L., & Romero, R. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.103 · Cited by 132 · see citing works
Maternal Vascular Malperfusion and Adverse Perinatal Outcomes in Low-Risk Nulliparous Women
Wright, E., Audette, M. C., Ye, X. Y., Keating, S. J., Hoffman, B., Lye, S. J., Shah, P. S., & Kingdom, J. C. (2017) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000002264 · Cited by 133 · see citing works
Thrombotic microangiopathies of pregnancy: Differential diagnosis
Gupta, M., Feinberg, B. B., & Burwick, R. M. (2018) · Pregnancy Hypertension · doi:10.1016/j.preghy.2018.02.007 · Cited by 135 · see citing works
Angiogenic Factors in Diagnosis, Management, and Research in Preeclampsia
Rana, S., Karumanchi, S. A., & Lindheimer, M. D. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.02293 · Cited by 131 · see citing works
The renin–angiotensin–aldosterone system in pre-eclampsia: the delicate balance between good and bad
Verdonk, K., Visser, W. E., van den Meiracker, A. H., & Danser, A. H. J. (2013) · Clinical Science · doi:10.1042/cs20130455 · Cited by 130 · see citing works
EASL Clinical Practice Guidelines on the management of liver diseases in pregnancy
Williamson, C., Nana, M., Poon, L. C., Kupčinskas, L., Painter, R. C., Taliani, G., Heneghan, M. A., Marschall, H., & Beuers, U. H. (2023) · Journal of Hepatology · doi:10.1016/j.jhep.2023.03.006 · Cited by 137 · see citing works
G-Protein-Coupled Receptor Kinase 2 and Hypertension
Santulli, G., Trimarco, B., & Iaccarino, G. (2013) · High Blood Pressure & Cardiovascular Prevention · doi:10.1007/s40292-013-0001-8 · Cited by 123 · see citing works
Ukah, U. V., Silva, D. A. D., Payne, B. A., Magee, L. A., Hutcheon, J. A., Brown, H. L., Ansermino, J. M., Lee, T., & von Dadelszen, P. (2017) · Pregnancy Hypertension · doi:10.1016/j.preghy.2017.11.006 · Cited by 122 · see citing works
Tsiakkas, A., Saiid, Y., Wright, A., Wright, D., & Nicolaides, K. H. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.02.016 · Cited by 119 · see citing works
Recent Advances in the Understanding of the Pathophysiology of Preeclampsia
Warrington, J. P., George, E. M., Palei, A. C., Spradley, F. T., & Granger, J. P. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.00588 · Cited by 120 · see citing works
Rayman, M. P., Searle, E., Kelly, L. A., Johnsen, S., Bodman-Smith, K. B., Bath, S. C., Mao, J., & Redman, C. W. G. (2014) · British Journal Of Nutrition · doi:10.1017/s0007114514000531 · Cited by 117 · see citing works
“the concentration of sFlt-1((12,59)), the data for PlGF and the ratio of sFlt-1:PlGF are also presented.”
BackgroundAndrietti, S., Silva, M. D. L., Wright, A., Wright, D. E., & Nicolaides, K. H. (2015) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.15812 · Cited by 116 · see citing works
Herraı̀z, I., Simon, E. D. S., Gómez‐Arriaga, P. I., Martínez-Moratalla, J. M., García-Burguillo, A., Jiménez, E., & Galindo, A. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160819009 · Cited by 114 · see citing works
“[60] used this cut-off point to predict adverse pregnancy outcomes showing that, in cases evaluated under 34 weeks of gestation,”
Devuyst, O., Ahn, C., Barten, T. R. M., Brosnahan, G., Cadnapaphornchai, M. A., Chapman, A. B., Gall, É. C.-L., Drenth, J. P. H., Gansevoort, R. T., Harris, P. C., et al. (2025) · Kidney International · doi:10.1016/j.kint.2024.07.009 · Cited by 142 · see citing works
Korzeniewski, S. J., Romero, R. J., Chaiworapongsa, T., Chaemsaithong, P., Kim, C. J., Kim, Y. M., Kim, J.-S., Yoon, B. H., Hassan, S. S., & Yeo, L. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.11.015 · Cited by 112 · see citing works
Verlohren, S., Melchiorre, K., Khalil, A. A., & Thilaganathan, B. (2014) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.13310 · Cited by 110 · see citing works
Boyd, H. A., Basit, S., Behrens, I., Leirgul, E., Bundgaard, H., Wohlfahrt, J., Melbye, M., & Øyen, N. (2017) · Circulation · doi:10.1161/circulationaha.116.024600 · Cited by 109 · see citing works
Yung, H. W., Colleoni, F., Dommett, E., Cindrová‐Davies, T., Kingdom, J. C., Murray, A. J., & Burton, G. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907548116 · Cited by 110 · see citing works
“Measurement of these proteins in maternal blood is now central to the clinical diagnosis of the disease (10, 11).”
BackgroundPlacental growth factor (PlGF): a key to optimizing fetal growth
Vrachnis, N., Kalampokas, E., Sifakis, S., Vitoratos, N., Kalampokas, T., Botsis, D., & Iliodromiti, Z. (2013) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2013.766694 · Cited by 105 · see citing works
“Moreover, a study concluded that in women with suspected preeclampsia presenting at 534 weeks, an elevated circulating sFlt1/PlGF ratio predicts adverse outcomes occurring within 2 weeks [72].”
BackgroundHu, X., Ao, J., Li, X., Zhang, H., Wu, J., & Cheng, W. (2018) · Clinical Epigenetics · doi:10.1186/s13148-018-0482-3 · Cited by 103 · see citing works
Poon, L. C., Magee, L. A., Verlohren, S., Shennan, A. H., von Dadelszen, P., Sheiner, E., Hadar, E., Visser, G. H. A., Costa, F. D. S., Kapur, A., et al. (2021) · International Journal of Gynecology & Obstetrics · doi:10.1002/ijgo.13763 · Cited by 118 · see citing works
Rana, S., Hacker, M. R., Modest, A. M., Salahuddin, S., Lim, K.-H., Verlohren, S., Perschel, F. H., & Karumanchi, S. A. (2012) · Hypertension · doi:10.1161/hypertensionaha.112.195065 · Cited by 103 · see citing works
“These findings are similar to those in our study evaluating the role of sFlt-1/PlGF ratio in singleton pregnancy.(21) Interestingly, in our study, normotensive women carrying twins had approximately 2-fold-higher circulating sFlt-1 and 3-fold-higher sFlt-1/PlGF ratio (Table 3 and Table 4) than did normotensive women w…”
MethodResultInfluentialRecent advances in the diagnosis and management of pre-eclampsia
Duhig, K. E., & Shennan, A. H. (2015) · F1000Prime Reports · doi:10.12703/p7-24 · Cited by 101 · see citing works
“In 2012, Rana and colleagues [30] demonstrated that, in women presenting with suspected pre-eclampsia, the median sFlt-1/PlGF ratio at presentation was elevated in participants who experienced any adverse outcome compared with those who did not (47.”
BackgroundHerraı̀z, I., Dröge, L. A., Gómez‐Montes, E., Henrich, W., Galindo, A., & Verlohren, S. (2014) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000000367 · Cited by 98 · see citing works
“Regarding the prognosis, there is a positive correlation between the sFlt-1/PlGF ratio and the likelihood of complications.(8,9) Nevertheless, the heterogeneity of placental disorders cannot be fully explained by means of a simplistic angiogenic imbalance approach.”
New Developments in the Pathogenesis of Preeclampsia
Naljayan, M. V., & Karumanchi, S. A. (2013) · Advances in Chronic Kidney Disease · doi:10.1053/j.ackd.2013.02.003 · Cited by 94 · see citing works
Biomarkers and the Prediction of Adverse Outcomes in Preeclampsia
Lim, S., Li, W., Kemper, J., Nguyen, A., Mol, B. W., & Reddy, M. (2020) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000004149 · Cited by 99 · see citing works
“17,23,32,36,39,46 Sixteen studies assessed the relationship between biomarkers and small for gestational age or fetal growth restriction (Appendix 12, available online at http://links.lww.com/AOG/C100).”
InfluentialSoluble Endoglin As a Marker for Preeclampsia, Its Severity, and the Occurrence of Adverse Outcomes
Leaños‐Miranda, A., Navarro-Romero, C. S., Sillas-Pardo, L. J., Ramírez-Valenzuela, K. L., Isordia‐Salas, I., & Jiménez-Trejo, L. M. (2019) · Hypertension · doi:10.1161/hypertensionaha.119.13348 · Cited by 89 · see citing works
Complement in Pregnancy: A Delicate Balance
Denny, K. J., Woodruff, T. M., Taylor, S. M., & Callaway, L. K. (2012) · American Journal of Reproductive Immunology · doi:10.1111/aji.12000 · Cited by 90 · see citing works
Angiogenic balance (sFlt-1/PlGF) and preeclampsia
Lecarpentier, É., & Tsatsaris, V. (2016) · Annales d Endocrinologie · doi:10.1016/j.ando.2016.04.007 · Cited by 89 · see citing works
Chaiworapongsa, T., Romero, R. J., Korzeniewski, S. J., Cortez, J. M., Pappas, A., Tarca, A. L., Chaemsaithong, P., Dong, Z., Yeo, L., & Hassan, S. S. (2013) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2013.806905 · Cited by 88 · see citing works
“Other than our first retrospective study of angiogenic/anti-angiogenic factors in the obstetrical triage area [106], three studies reported an association between maternal plasma angiogenic/ anti-angiogenic factor concentrations in women who presented to the obstetrical triage area with suspected PE and adverse matern…”
BackgroundResultZeisler, H., Llurba, E., Chantraine, F., Vatish, M., Staff, A. C., Sennström, M., Olovsson, M. H., Brennecke, S. P., Stepan, H., Allegranza, D., et al. (2016) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000001525 · Cited by 86 · see citing works
“001).(9) In another study of 388 women with normal pregnancy outcomes and 164 women with preeclampsia, women with an sFlt-1-to-PlGF ratio above 655.”
BackgroundGray, K. J., Saxena, R., & Karumanchi, S. A. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.11.562 · Cited by 87 · see citing works
“In the clinic, recent evidence supports the utility of the sFLT1 and PlGF for predicting adverse maternal and perinatal outcomes for preterm patients, ruling out preeclampsia in patients with suspected disease, and predicting which high-risk patients are at low risk for severe adverse outcomes.(38-50)”
Sequential plasma angiogenic factors levels in women with suspected preeclampsia
Baltajian, K., Bajracharya, S., Salahuddin, S., Berg, A. H., Geahchan, C., Wenger, J. B., Thadhani, R., Karumanchi, S. A., & Rana, S. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.01.168 · Cited by 88 · see citing works
Chaiworapongsa, T., Romero, R. J., Whitten, A. E., Korzeniewski, S. J., Chaemsaithong, P., Hernandez‐Andrade, E. A., Yeo, L., & Hassan, S. S. (2015) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2015.1048431 · Cited by 80 · see citing works
Preeclampsia and Kidney Disease: Deciphering Cause and Effect
Kattah, A. G. (2020) · Current Hypertension Reports · doi:10.1007/s11906-020-01099-1 · Cited by 86 · see citing works
A machine-learning–based algorithm improves prediction of preeclampsia-associated adverse outcomes
Schmidt, L. J., Rieger, O., Neznansky, M., Hackelöer, M., Dröge, L. A., Henrich, W., Higgins, D., & Verlohren, S. (2022) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2022.01.026 · Cited by 81 · see citing works
Gestational Hypertension and Preeclampsia: Are They the Same Disease?
Melamed, N., Ray, J. G., Hladunewich, M., Cox, B., & Kingdom, J. C. (2014) · Journal of Obstetrics and Gynaecology Canada · doi:10.1016/s1701-2163(15)30545-4 · Cited by 81 · see citing works
Verlohren, S., & Dröge, L.-A. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.09.046 · Cited by 83 · see citing works
Placental Disease and the Maternal Syndrome of Preeclampsia: Missing Links?
Tannetta, D., & Sargent, I. L. (2013) · Current Hypertension Reports · doi:10.1007/s11906-013-0395-7 · Cited by 80 · see citing works
Sibiude, J., Guibourdenche, J., Dionne, M.-D., Ray, C. L., Anselem, O., Serreau, R., Goffinet, F., & Tsatsaris, V. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050208 · Cited by 79 · see citing works
“A prospective study has recently suggested that the sFLT/PlGF ratio appears better than previous markers for the prediction of adverse outcomes [25].”
BackgroundSaffer, C. S., Olson, G., Boggess, K., Beyerlein, R., Eubank, C., & Sibai, B. M. (2013) · Pregnancy Hypertension · doi:10.1016/j.preghy.2013.01.004 · Cited by 79 · see citing works
“While the pathophysiology of preeclampsia is not yet fully understood, there is growing evidence associating angiogenic proteins in screening, diagnosing and predicting the clinical course of the condition [6–15].”
BackgroundMethodDröge, L.-A., Herraı̀z, I., Zeisler, H., Schlembach, D., Stepan, H., Küssel, L., Henrich, W., Galindo, A., & Verlohren, S. (2014) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.14760 · Cited by 79 · see citing works
Alfredo Perales, M., Delgado⋈, J. L., de la Calle, M., García‐Hernández, J. A., Escudero, A. I., Maza, J. M. C., Sarabia, M. D., Laíz, B., Duque, M., Navarro, M., et al. (2016) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.17373 · Cited by 81 · see citing works
Caillon, H., Tardif, C., Dumontet, E., Winer, N., & Masson, D. (2017) · Annals of Laboratory Medicine · doi:10.3343/alm.2018.38.2.95 · Cited by 78 · see citing works
“Interestingly, the sFlt-1/ PlGF ratio appears to show better performance than single markers in predicting the risk of PE [10, 11].”
BackgroundInfluence of the sFlt-1/PlGF Ratio on Clinical Decision-Making in Women with Suspected Preeclampsia
Klein, E., Schlembach, D., Ramoni, A., Langer, E., Bahlmann, F., Grill, S., Schaffenrath, H., van der Does, R., Messinger, D., Verhagen-Kamerbeek, W. D. J., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156013 · Cited by 77 · see citing works
Angiogenic and antiangiogenic factors in preeclampsia
Helmo, F. R., Lopes, A. M. M., Carneiro, A. C. D. M., Campos, C. G., Silva, P. B., Monteiro, M. L. G. D. R., Rocha, L. P., dos Reis, M. A., Etchebehere, R. M., Machado, J. R., et al. (2017) · Pathology - Research and Practice · doi:10.1016/j.prp.2017.10.021 · Cited by 78 · see citing works
Angiogenic biomarkers in triage and risk for preeclampsia with severe features
Rana, S., Salahuddin, S., Mueller, A., Berg, A. H., Thadhani, R., & Karumanchi, S. A. (2018) · Pregnancy Hypertension · doi:10.1016/j.preghy.2018.05.008 · Cited by 77 · see citing works
Vasoactive agents for the prediction of early- and late-onset preeclampsia in a high-risk cohort
Villa, P., Hämäläinen, E. K., Mäki, A., Räikkönen, K., Pesonen, A., Taipale, P., Kajantie, E., & Laivuori, H. M. (2013) · BMC Pregnancy and Childbirth · doi:10.1186/1471-2393-13-110 · Cited by 76 · see citing works
“Rana and coworkers [18], studied angiogenic factors in 616 women with a suspected preeclampsia, and found that in early-onset (<34 weeks) disease sFlt-1/PlGF ratio predicts adverse outcome occurring within two weeks.”
BackgroundHund, M., Allegranza, D., Schoedl, M., Dilba, P., Verhagen-Kamerbeek, W. D. J., & Stepan, H. (2014) · BMC Pregnancy and Childbirth · doi:10.1186/1471-2393-14-324 · Cited by 77 · see citing works
“In women with suspected preeclampsia, the sFlt-1/PlGF ratio may also help to identify those women who will develop a preeclampsiarelated pregnancy complication [35].”
Background
- Authors
- Rana, S., Powe, C. E., Salahuddin, S., Verlohren, S., Perschel, F. H., Levine, R. J., Lim, K.-H., Wenger, J. B., Thadhani, R., & Karumanchi, S. A.
- Affiliations
- National Institutes of Health (US)
- ORCID
- Venue
- Circulation
- Published
- 2012-02-21
- Volume
- 125
- Issue
- 7
- Pages
- 911-919
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- PMC
- PMC3319742
- OpenAlex
- W2134502189
- Cited by
- 668
- References
- 39
- Citations by year
- 2026: 30 · 2025: 51 · 2024: 40 · 2023: 46 · 2022: 50 · 2021: 52 · 2020: 49 · 2019: 48 · 2018: 49 · 2017: 48 · 2016: 49 · 2015: 42 · 2014: 49 · 2013: 41 · 2012: 20
- FWCI
- 58.66
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Psychiatry and Mental health › Neurological Complications and Syndromes
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- preeclampsia, angiogenic factors, soluble fms-like tyrosine kinase-1, placental growth factor, sFlt-1/PlGF ratio, adverse maternal outcomes, perinatal outcomes, early-onset preeclampsia, proteinuria, hypertension, adverse outcome prediction, preterm birth, placental insufficiency, endothelial dysfunction, maternal morbidity
- MeSH terms
- Placenta Growth Factor, Adult, Female, Humans, Pre-Eclampsia, Pregnancy, Pregnancy Proteins, Prospective Studies, Risk, ROC Curve, Systole, Logistic Models, Vascular Endothelial Growth Factor Receptor-1
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