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
Preterm premature rupture of the membranes
Mercer, B. (2003) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(02)02366-9 · Cited by 742
Romero, R. J., Nien, J. K., Espinoza, J., Todem, D., Fu, W., Chung, H., Kusanovic, J. P., Gotsch, F., Erez, O., Mazaki‐Tovi, S., et al. (2008) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050701830480 · Cited by 683
von Dadelszen, P., Payne, B. A., Li, J., Ansermino, J. M., Pipkin, F. B., Côté, A., Douglas, M. J., Gruslin, A., Hutcheon, J. A., Joseph, K. S., et al. (2010) · The Lancet · doi:10.1016/s0140-6736(10)61351-7 · Cited by 593
Sibai, B. M., Mercer, B. M., Schiff, E., & Friedman, S. A. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(94)90104-x · Cited by 458
An automated method for the determination of the sFlt-1/PIGF ratio in the assessment of preeclampsia
Verlohren, S., Galindo, A., Schlembach, D., Zeisler, H., Herraı̀z, I., Moertl, M. G., Pape, J., Dudenhausen, J. W., Denk, B., & Stepan, H. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.09.016 · Cited by 433
Vitamins C and E to Prevent Complications of Pregnancy-Associated Hypertension
Roberts, J. M., Myatt, L., Spong, C. Y., Thom, E. A., Hauth, J. C., Leveno, K. J., Pearson, G. D., Wapner, R. J., Varner, M. W., Thorp, J. M., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa0908056 · Cited by 402
Fisher, K. A., Luger, A., Spargo, B. H., & Lindheimer, M. D. (1981) · Medicine · doi:10.1097/00005792-198107000-00002 · Cited by 374
Noori, M., Donald, A. E., Angelakopoulou, A., Hingorani, A. D., & Williams, D. J. (2010) · Circulation · doi:10.1161/circulationaha.109.895458 · Cited by 364
Chaiworapongsa, T., Romero, R., Kim, Y. M., Kim, G. J., Kim, M. R., Espinoza, J., Bujold, E., Gonçalves, L., Gomez, R., Edwin, S., et al. (2005) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050400028816 · Cited by 359
Pilot Study of Extracorporeal Removal of Soluble Fms-Like Tyrosine Kinase 1 in Preeclampsia
Thadhani, R., Kisner, T., Hagmann, H., Boßung, V., Noack, S., Schaarschmidt, W., Jank, A., Kribs, A., Cornely, O. A., Kreyssig, C., et al. (2011) · Circulation · doi:10.1161/circulationaha.111.034793 · Cited by 355
Diagnosis and management of atypical preeclampsia-eclampsia
Sibai, B. M., & Stella, C. L. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.07.048 · Cited by 353
Odendaal, H. J., Pattinson, R., Bam, R. H., Grove, D., & Tj, K. (1990) · PubMed · Cited by 285
Kusanovic, J. P., Romero, R. J., Chaiworapongsa, T., Erez, O., Mittal, P., Vaisbuch, E., Mazaki‐Tovi, S., Gotsch, F., Edwin, S. S., Gómez, R., et al. (2009) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767050902994754 · Cited by 281
Li, Z., Zhang, Y., Jing, Y., Kapoun, A. M., Shao, Q., Kerr, I., Lam, A., O’Young, G., Sannajust, F. J., Stathis, P., et al. (2007) · Hypertension · doi:10.1161/hypertensionaha.107.092098 · Cited by 263
Lu, F., Longo, M., Tamayo, E. H., Maner, W. L., Al-Hendy, A. A., Anderson, G. D., Hankins, G. D. V., & Saade, G. R. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2006.12.024 · Cited by 229
VEGF and TGF-β are required for the maintenance of the choroid plexus and ependyma
Maharaj, A. S. R., Walshe, T. E., Saint‐Geniez, M., Venkatesha, S., Maldonado, A. E., Himes, N. C., Matharu, K., Karumanchi, S. A., & D'Amore, P. A. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20072041 · Cited by 193
Neonatal outcome after preterm delivery for preeclampsia
Friedman, S. A., Schiff, E., Kao, L., & Sibai, B. M. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)91412-9 · Cited by 182
Sunderji, S., Gaziano, E. P., Wothe, D. D., Rogers, L. C., Sibai, B. M., Karumanchi, S. A., & Hodges-Savola, C. A. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.07.025 · Cited by 132
Can antenatal clinical and biochemical markers predict the development of severe preeclampsia?
Stamilio, D. M., Sehdev, H. M., Morgan, M. A., PROPERT, K. J., & Macones, G. A. (2000) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2000.103890 · Cited by 128
Ahmed, A. (2011) · Thrombosis Research · doi:10.1016/s0049-3848(11)70020-2 · Cited by 127
Menzies, J., Magee, L. A., MacNab, Y. C., Ansermino, J. M., Li, J., Douglas, M. J., Gruslin, A., Kyle, P. M., Lee, S. K., Moore, M. P., et al. (2007) · Hypertension in Pregnancy · doi:10.1080/10641950701521742 · Cited by 114
Preterm Premature Rupture of the Membranes
Mercer, B. M. (2003) · Obstetrics and Gynecology · doi:10.1097/00006250-200301000-00033 · Cited by 109
Ganzevoort, W., Rep, A., de Vries, J. I. P., Bonsel, G. J., & Wolf, H. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2006.02.012 · Cited by 107
Preterm Premature Rupture of the Membranes
Mercer, B. M. (2008) · The Global Library of Women s Medicine · doi:10.3843/glowm.10120 · Cited by 72
Williams, K. P., & Galerneau, F. (2002) · Journal of Obstetrics and Gynaecology Canada · doi:10.1016/s1701-2163(16)30193-1 · Cited by 63
Prediction of Adverse Maternal Outcomes in Preeclampsia
von Dadelszen, P., Payne, B. A., Li, J., Ansermino, J. M., Pipkin, F. B., Côté, A., Douglas, M. J., Gruslin, A., Hutcheon, J. A., Joseph, K. S., et al. (2012) · Obstetric Anesthesia Digest · doi:10.1097/01.aoa.0000410808.61878.a4 · Cited by 36
Prognostic Role of Uterine Artery Doppler in Patients with Preeclampsia
Meler, E., Figueras, F., Mula, R., Crispi, F., Benassar, M., Gómez, O., & Gratacós, E. (2009) · Fetal Diagnosis and Therapy · doi:10.1159/000258048 · Cited by 34
Schneider, E., Gleixner, A., Hänel, R., Leyhe, Y., Kleinschmidt, C. K., Beck, G., Steinberg, M., Denk, B., & Gassner, D. (2009) · Zeitschrift für Geburtshilfe und Neonatologie · doi:10.1055/s-0029-1216308 · Cited by 15
Flagged first, then by citations
1 of the 39 references couldn’t be matched to a known paper.
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
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