The DOI matches its Crossref record; 38 of the 39 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
DeLong, E. R., DeLong, D. M., & Clarke-Pearson, D. L. (1988) · Biometrics · doi:10.2307/2531595 · Cited by 22,649
Maynard, S. E., Min, J.-Y., Merchan, J., Lim, K.-H., Li, J., Mondal, S., Libermann, T. A., Morgan, J. P., Sellke, F. W., Stillman, I. E., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17189 · Cited by 4,101
Self-citationCirculating angiogenic factors and the risk of preeclampsia
Levine, R. J., Maynard, S. E., Qian, C., Lim, K.-H., England, L. J., Yu, K. F., Schisterman, E. F., Thadhani, R., Sachs, B. P., Epstein, F. H., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa031884 · Cited by 3,720
Self-citationCirculating angiogenic factors and the risk of preeclampsia*
(2004) · Obstetrics and Gynecology · doi:10.1097/00006250-200405000-00028 · Cited by 2,623
Soluble Endoglin and Other Circulating Antiangiogenic Factors in Preeclampsia
Levine, R. J., Lam, C., Qian, C., Yu, K. F., Maynard, S. E., Sachs, B. P., Sibai, B. M., Epstein, F. H., Romero, R. J., Thadhani, R., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa055352 · Cited by 1,823
Kendall, R. L., & Thomas, K. A. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.22.10705 · Cited by 1,419
Eremina, V., Sood, M. M., Haigh, J. J., Nagy, A., Lajoie, G., Ferrara, N., Gerber, H. P., Kikkawa, Y., Miner, J. H., & Quaggin, S. E. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17423 · Cited by 1,308
Soluble Endoglin and Other Circulating Antiangiogenic Factors in Preeclampsia
(2006) · New England Journal of Medicine · doi:10.1056/nejmx060063 · Cited by 1,237
ACOG Practice Bulletin No. 33: Diagnosis and Management of Preeclampsia and Eclampsia
ACOG Committee on Obstetric Practice (2002) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01747-1 · Cited by 1,180
Wallis, A. B., Saftlas, A. F., Hsia, J., & Atrash, H. K. (2008) · American Journal of Hypertension · doi:10.1038/ajh.2008.20 · Cited by 759
Cited by
Sorted by citations
Rana (2019) · doi:10.1161/circresaha.118.313276 · Cited by 2,095
Brown, M. A., Magee, L. A., Kenny, L. C., Karumanchi, S. A., McCarthy, F. P., Saito, S., Hall, D. R., Warren, C. E., Adoyi, G., & Ishaku, S. (2018) · Hypertension · doi:10.1161/hypertensionaha.117.10803 · Cited by 2,089
“Measurement of angiogenic factors may play a role in this regard in the future but is still at a research stage.(56)”
BackgroundSelf-citationPredictive Value of the sFlt-1:PlGF Ratio in Women with Suspected Preeclampsia
Zeisler, H., Llurba, E., Chantraine, F., Vatish, M., Staff, A. C., Sennström, M., Olovsson, M., Brennecke, S. P., Stepan, H., Allegranza, D., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1414838 · Cited by 1,872
Mol, B. W., Roberts, C. T., Thangaratinam, S., Magee, L. A., de Groot, C. J. M., & Hofmeyr, G. J. (2015) · The Lancet · doi:10.1016/s0140-6736(15)00070-7 · Cited by 1,667
Tranquilli, A. L., Dekker, G., Magee, L. A., Roberts, J. M., Sibai, B. M., Steyn, W., Zeeman, G. G., & Brown, M. A. (2014) · Pregnancy Hypertension · doi:10.1016/j.preghy.2014.02.001 · Cited by 1,419
Pre-eclampsia: pathogenesis, novel diagnostics and therapies
Phipps, E. A., Thadhani, R., Benzing, T. R., & Karumanchi, S. A. (2019) · Nature Reviews Nephrology · doi:10.1038/s41581-019-0119-6 · Cited by 1,328
Magee, L. A., Brown, M. A., Hall, D. R., Gupte, S., Hennessy, A., Karumanchi, S. A., Kenny, L. C., McCarthy, F., Myers, J., Poon, L. C., et al. (2022) · Pregnancy Hypertension · doi:10.1016/j.preghy.2021.09.008 · Cited by 1,134
“…has high negative predictive value in ruling out: development of proteinuric pre-eclampsia within 7 days, adverse maternal outcomes within 14 days [46], or delivery with pre-eclampsia within 14 days [37 – 38] when suspected pre-eclampsia is primarily related to hypertension (but not when FGR is a…”
BackgroundBrown, M. A., Magee, L. A., Kenny, L. C., Karumanchi, S. A., McCarthy, F. P., Saito, S., Hall, D. R., Warren, C., Adoyi, G., & Ishaku, S. (2018) · Pregnancy Hypertension · doi:10.1016/j.preghy.2018.05.004 · Cited by 1,117
“Measurement of angiogenic factors may play a role in this regard in the future but is still at a research stage(56).”
BackgroundChappell, L. C., Cluver, C. A., Kingdom, J. C., & Tong, S. (2021) · The Lancet · doi:10.1016/s0140-6736(20)32335-7 · Cited by 1,013
Diagnostic Accuracy of Placental Growth Factor in Women With Suspected Preeclampsia
Chappell, L. C., Duckworth, S., Seed, P. T., Griffin, M., Myers, J., Mackillop, L. H., Simpson, N., Waugh, J. J. S., Anumba, D. O. C., Kenny, L. C., et al. (2013) · Circulation · doi:10.1161/circulationaha.113.003215 · Cited by 501
“Mild preeclampsia 25 (9) 24 (18) 40 (20)”
Tracking placental development in health and disease
Aplin, J., Myers, J., Timms, K., & Westwood, M. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0372-6 · Cited by 401
Verlohren, S., Herraı̀z, I., Lapaire, O., Schlembach, D., Zeisler, H., Calda, P., Sabrià, J., Markfeld-Erol, F., Galindo, A., Schoofs, K., et al. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.01787 · Cited by 375
“blood pressure and proteinuria, the sFlt-1/PlGF ratio is able to improve prediction of adverse preeclampsia-related outcomes.(9)”
BackgroundRana, S., Burke, S. D., & Karumanchi, S. A. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.10.022 · Cited by 366
“2).(136) This ratio alone outperformed standard clinical diagnostic measures including blood pressure, proteinuria, and uric acid.”
BackgroundSOMANZ guidelines for the management of hypertensive disorders of pregnancy 2014
Lowe, S. A., Bowyer, L., Lust, K., McMahon, L. P., Morton, M., North, R. A., Paech, M., & Said, J. M. (2015) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/ajo.12399 · Cited by 299
Removal of Soluble Fms-Like Tyrosine Kinase-1 by Dextran Sulfate Apheresis in Preeclampsia
Thadhani, R., Hagmann, H., Schaarschmidt, W., Roth, B., Cingoez, T., Karumanchi, S. A., Wenger, J., Lucchesi, K. J., Tamez, H. E., Lindner, T. H., et al. (2015) · Journal of the American Society of Nephrology · doi:10.1681/asn.2015020157 · Cited by 283
Tomimatsu, T., Mimura, K., Matsuzaki, S., Endo, M., Kumasawa, K., & Kimura, T. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174246 · Cited by 290
“In pregnant women with suspected preeclampsia, the severity of the maternal antiangiogenic state predicted preeclampsia-related adverse complications more accurately than the highest systolic blood pressure, a hallmark of the diagnostic criteria for preeclampsia [110,111].”
BackgroundEarly Prediction of Preeclampsia
Poon, L. C., & Nicolaides, K. H. (2014) · Obstetrics and Gynecology International · doi:10.1155/2014/297397 · Cited by 286
“In such high-risk pregnancies, measurement of serum PlGF or soluble fms-like tyrosine kinase-1 (sFlt-1) to PlGF ratio is highly accurate in identifying the target group [111–116].”
BackgroundStepan, H., Herraı̀z, I., Schlembach, D., Verlohren, S., Brennecke, S. P., Chantraine, F., Klein, E. E., Lapaire, O., Llurba, E., Ramoni, A., et al. (2015) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.14799 · Cited by 274
Sircar, M., Thadhani, R., & Karumanchi, S. A. (2015) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0000000000000105 · Cited by 260
Pathophysiology and epidemiology of peripartum cardiomyopathy
Hilfiker‐Kleiner, D., & Sliwa, K. S. (2014) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2014.37 · Cited by 253
Romero, R., Erez, O., Hüttemann, M., Maymon, E., Panaitescu, B., Conde-Agudelo, A., Pacora, P., Yoon, B. H., & Grossman, L. I. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.06.003 · Cited by 253
Preeclampsia: Pathogenesis, Prevention, and Long-Term Complications
Jim, B., & Karumanchi, S. A. (2017) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2017.05.011 · Cited by 257
Stepan, H., Galindo, A., Hund, M., Schlembach, D., Sillman, J., Surbek, D., & Vatish, M. (2023) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.26032 · Cited by 245
Combining Biomarkers to Predict Pregnancy Complications and Redefine Preeclampsia
Stepan, H., Hund, M., & Andraczek, T. (2020) · Hypertension · doi:10.1161/hypertensionaha.119.13763 · Cited by 252
Verlohren, S., Brennecke, S. P., Galindo, A., Karumanchi, S. A., Mirković, L., Schlembach, D., Stepan, H., Vatish, M., Zeisler, H., & Rana, S. (2021) · Pregnancy Hypertension · doi:10.1016/j.preghy.2021.12.003 · Cited by 253
RNAi modulation of placental sFLT1 for the treatment of preeclampsia
Turanov, A. A., Lo, A. S., Hassler, M. R., Makris, A., Ashar-Patel, A., Alterman, J. F., Coles, A. H., Haraszti, R. Á., Roux, L., Godinho, B. M. D. C., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4297 · Cited by 217
Epidemiology and Mechanisms of De Novo and Persistent Hypertension in the Postpartum Period
Goel, A., Maski, M. R., Bajracharya, S., Wenger, J., Zhang, D., Salahuddin, S., Shahul, S. S., Thadhani, R., Seely, E. W., Karumanchi, S. A., et al. (2015) · Circulation · doi:10.1161/circulationaha.115.015721 · Cited by 208
Preeclampsia: Novel Mechanisms and Potential Therapeutic Approaches
Armaly, Z., Jadaon, J. E., Jabbour, A. R., & Abassi, Z. A. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00973 · Cited by 217
“The imbalance between the proangiogenic VEGF and PlGF, and the antiangiogenic sFlt-1 and sEng plays a central role in the pathogenesis of placental hypoxia, as both VEGF and PlGF are essential for fetal and placental angiogenesiss (Lam et al., 2005; Sison et al., 2010; Bertuccio et al., 2011; Powe et al., 2011; Rana e…”
BackgroundAgrawal, S., Cerdeira, A. S., Redman, C. W. G., & Vatish, M. (2017) · Hypertension · doi:10.1161/hypertensionaha.117.10182 · Cited by 186
Dröge, L. A., Perschel, F. H., Stütz, N., Gafron, A., Frank, L., Busjahn, A., Henrich, W., & Verlohren, S. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15146 · Cited by 169
A placenta clinic approach to the diagnosis and management of fetal growth restriction
Kingdom, J. C., Audette, M. C., Hobson, S. R., Windrim, R. C., & Morgen, E. K. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.11.575 · Cited by 167
Angiogenic Factors in Preeclampsia: From Diagnosis to Therapy
Karumanchi, S. A. (2016) · Hypertension · doi:10.1161/hypertensionaha.116.06421 · Cited by 163
“To demonstrate clinical use of these biomarkers, we led a large clinical study to evaluate the role of angiogenic biomarkers in the prediction of preeclampsia-related adverse outcomes among women evaluated at our institution for suspected preeclampsia.(74) We demonstrated that the plasma sFlt1/PlGF ratio on presentati…”
Cerdeira, A. S., O’Sullivan, J. M., Ohuma, E. O., Harrington, D. J., Szafranski, P., Black, R., Mackillop, L. H., Impey, L. W. M., Greenwood, C. E. L., James, T. J., et al. (2019) · Hypertension · doi:10.1161/hypertensionaha.119.12739 · Cited by 162
“Missing data for 1;2 and 1 patients respectively.(4,7,8,11,12,15,16,19) Missing data for 1 patient.”
BackgroundClinical characterization and outcomes of preeclampsia with normal angiogenic profile
Rana, S., Schnettler, W. T., Powe, C. E., Wenger, J., Salahuddin, S., Cerdeira, A. S., Verlohren, S., Perschel, F. H., Arany, Z. P., Lim, K.-H., et al. (2013) · Hypertension in Pregnancy · doi:10.3109/10641955.2013.784788 · Cited by 158
“Study Population This is a part of an ongoing prospective cohort study on pregnant patients who presented to obstetrical triage at Beth Israel Deaconess Medical Center (BIDMC), Boston, MA, as described elsewhere (20).”
BackgroundMethodInfluentialTomimatsu, T., Mimura, K., Endo, M., Kumasawa, K., & Kimura, T. (2016) · Hypertension Research · doi:10.1038/hr.2016.152 · Cited by 158
Tsiakkas, A., Duvdevani, N., Wright, A., Wright, D. E., & Nicolaides, K. H. (2015) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.14811 · Cited by 152
Khosla, K., Heimberger, S., Nieman, K. M., Tung, A., Shahul, S. S., Staff, A. C., & Rana, S. (2021) · Hypertension · doi:10.1161/hypertensionaha.121.16506 · Cited by 156
First‐trimester maternal factors and biomarker screening for preeclampsia
Poon, L. C., & Nicolaides, K. H. (2014) · Prenatal Diagnosis · doi:10.1002/pd.4397 · Cited by 152
Cabiddu, G., Castellino, S., Gernone, G., Santoro, D., Moroni, G. L., Giannattasio, M., Gregorini, G. A., Giacchino, F., Attini, R., Loi, V., et al. (2016) · Journal of Nephrology · doi:10.1007/s40620-016-0285-6 · Cited by 153
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 149
“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 148
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 146
Maternal cardiac metabolism in pregnancy
Liu, L. X., & Arany, Z. P. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu009 · Cited by 144
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
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
“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 148
“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 149
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
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
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 153
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 138
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
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
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 136
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 137
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 135
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 145
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
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
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
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
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 118
“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 120
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 118
“[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 149
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
Verlohren, S., Melchiorre, K., Khalil, A. A., & Thilaganathan, B. (2014) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.13310 · Cited by 110
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
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 112
“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 106
“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
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 123
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 105
“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
“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
“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 97
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 105
“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 94
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
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 91
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
“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 90
“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 90
“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
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
Preeclampsia and Kidney Disease: Deciphering Cause and Effect
Kattah, A. G. (2020) · Current Hypertension Reports · doi:10.1007/s11906-020-01099-1 · Cited by 90
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 84
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 82
Verlohren, S., & Dröge, L.-A. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.09.046 · Cited by 84
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 82
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
“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
“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 80
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 83
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
“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 79
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 82
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
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 77
“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
“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
Metadata
- 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 › Clinical Neurology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
