Cited by 3,720Pregnancy and preeclampsia studiesNeurological Complications and SyndromesAngiogenesis and VEGF in Cancer

The DOI matches its Crossref record; 24 of the 24 references it cites were found in a registry or an index.

Circulating Angiogenic Factors and the Risk of Preeclampsia

Open access

Levine, Richard J., Maynard, Sharon E., Qian, Cong, Lim, Kee-Hak, England, Lucinda J., Yu, Kai F., Schisterman, Enrique F., Thadhani, Ravi, Sachs, Benjamin P., Epstein, Franklin H., Sibai, Baha M., Sukhatme, Vikas P., Karumanchi, S. Ananth·2004·New England Journal of Medicine

DOI 10.1056/nejmoa031884

Open this paper in CoChat — free account Open PDF

Abstract

BACKGROUND: The cause of preeclampsia remains unclear. Limited data suggest that excess circulating soluble fms-like tyrosine kinase 1 (sFlt-1), which binds placental growth factor (PlGF) and vascular endothelial growth factor (VEGF), may have a pathogenic role. METHODS: We performed a nested case-control study within the Calcium for Preeclampsia Prevention trial, which involved healthy nulliparous women. Each woman with preeclampsia was matched to one normotensive control. A total of 120 pairs of women were randomly chosen. Serum concentrations of angiogenic factors (total sFlt-1, free PlGF, and free VEGF) were measured throughout pregnancy; there were a total of 655 serum specimens. The data were analyzed cross-sectionally within intervals of gestational age and according to the time before the onset of preeclampsia. RESULTS: During the last two months of pregnancy in the normotensive controls, the level of sFlt-1 increased and the level of PlGF decreased. These changes occurred earlier and were more pronounced in the women in whom preeclampsia later developed. The sFlt-1 level increased beginning approximately five weeks before the onset of preeclampsia. At the onset of clinical disease, the mean serum level in the women with preeclampsia was 4382 pg per milliliter, as compared with 1643 pg per milliliter in controls with fetuses of similar gestational age (P<0.001). The PlGF levels were significantly lower in the women who later had preeclampsia than in the controls beginning at 13 to 16 weeks of gestation (mean, 90 pg per milliliter vs. 142 pg per milliliter, P=0.01), with the greatest difference occurring during the weeks before the onset of preeclampsia, coincident with the increase in the sFlt-1 level. Alterations in the levels of sFlt-1 and free PlGF were greater in women with an earlier onset of preeclampsia and in women in whom preeclampsia was associated with a small-for-gestational-age infant. CONCLUSIONS: Increased levels of sFlt-1 and reduced levels of PlGF predict the subsequent development of preeclampsia.

Integrity signals

Registry

Crossref · 10.1056/nejmoa031884

Cites

24 of 24 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia
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-citation
A Randomized Trial of Bevacizumab, an Anti–Vascular Endothelial Growth Factor Antibody, for Metastatic Renal Cancer
Yang, J. C., Haworth, L. R., Sherry, R. M., Hwu, P., Schwartzentruber, D. J., Topalian, S. L., Steinberg, S. M., Chen, H. X., & Rosenberg, S. A. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa021491 · Cited by 2,704
Phase II, Randomized Trial Comparing Bevacizumab Plus Fluorouracil (FU)/Leucovorin (LV) With FU/LV Alone in Patients With Metastatic Colorectal Cancer
Kabbinavar, F. F., Hurwitz, H. I., Fehrenbacher, L., Meropol, N. J., Novotny, W. F., Liebérman, G., Griffing, S., & Bergsland, E. K. (2002) · Journal of Clinical Oncology · doi:10.1200/jco.2003.10.066 · Cited by 1,711
Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases
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
Pathogenesis and genetics of pre-eclampsia
Roberts, J., & Cooper, D. (2001) · The Lancet · doi:10.1016/s0140-6736(00)03577-7 · Cited by 1,279
Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome?
Zhou, Y., Damsky, C. H., & Fisher, S. J. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119388 · Cited by 937
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
Zhou, Y., McMaster, M., Woo, K., Janatpour, M. J., Perry, J., Kärpänen, T., Alitalo, K. K., Damsky, C. H., & Fisher, S. J. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)62567-9 · Cited by 643
Trial of Calcium to Prevent Preeclampsia
Levine, R. J., Hauth, J. C., Curet, L. B., Sibai, B. M., Catalano, P. M., Morris, C. D., DerSimonian, R., Esterlitz, J. R., Raymond, E. G., Bild, D. E., et al. (1997) · New England Journal of Medicine · doi:10.1056/nejm199707103370201 · Cited by 634
Self-citation
Pre-eclampsia
Walker, J. J. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02800-2 · Cited by 519
Overexpression of the Soluble Vascular Endothelial Growth Factor Receptor in Preeclamptic Patients: Pathophysiological Consequences
Tsatsaris, V., Goffin, F., Munaut, C., Brichant, J.-F., Pignon, M.-R., Noël, A., Schaaps, J., CABROL, D., Frankenne, F., & Foidart, J. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030528 · Cited by 465

Flagged first, then by citations

Show all 24 references

Sorted by citations

Vascular Endothelial Growth Factor: Basic Science and Clinical Progress
Ferrara, N. (2004) · Endocrine Reviews · doi:10.1210/er.2003-0027 · Cited by 3,788
VEGF receptor signalling ? in control of vascular function
Olsson, A.-K., Dimberg, A., Kreuger, J., & Claesson-Welsh, L. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1911 · Cited by 3,122
Untitled work
Rana (2019) · doi:10.1161/circresaha.118.313276 · Cited by 2,095
Self-citation
Hypertensive Disorders of Pregnancy: ISSHP Classification, Diagnosis, and Management Recommendations for International Practice
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
Self-citation
Preterm labor: One syndrome, many causes
Romero, R., Dey, S. K., & Fisher, S. J. (2014) · Science · doi:10.1126/science.1251816 · Cited by 1,984
Soluble endoglin contributes to the pathogenesis of preeclampsia
Venkatesha, S., Toporsian, M., Lam, C., Hanai, J.-I., Mammoto, T., Kim, Y. M., Bdolah, Y., Lim, K.-H., Yuan, H.-T., Libermann, T. A., et al. (2006) · Nature Medicine · doi:10.1038/nm1429 · Cited by 1,855
Self-citation
Predictive 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
Pre-eclampsia
Sibai, B. M., Dekker, G., & Kupferminc, M. J. (2005) · The Lancet · doi:10.1016/s0140-6736(05)17987-2 · Cited by 1,852
Self-citation
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
Self-citation
Vascular Endothelial Growth Factor (VEGF) and Its Receptor (VEGFR) Signaling in Angiogenesis: A Crucial Target for Anti- and Pro-Angiogenic Therapies
Shibuya, M. (2011) · Genes & Cancer · doi:10.1177/1947601911423031 · Cited by 1,844
The Inconsistency of “Optimal” Cutpoints Obtained using Two Criteria based on the Receiver Operating Characteristic Curve
Perkins, N. J., & Schisterman, E. F. (2006) · American Journal of Epidemiology · doi:10.1093/aje/kwj063 · Cited by 1,794
Self-citation
The effects of oxidative stress on female reproduction: a review
Agarwal, A. K., Aponte, A., Premkumar, B. J., Shaman, A. A., & Gupta, S. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-49 · Cited by 1,721
Pre-eclampsia
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
The “Great Obstetrical Syndromes” are associated with disorders of deep placentation
Brosens, I., Pijnenborg, R., Vercruysse, L., & Romero, R. (2011) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.08.009 · Cited by 1,568
VEGF Inhibition and Renal Thrombotic Microangiopathy
Eremina, V., Jefferson, J. A., Kowalewska, J., Höchster, H. S., Haas, M., Weisstuch, J., Richardson, C., Kopp, J. B., Kabir, M. G., Backx, P. H., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0707330 · Cited by 1,518
The International Federation of Gynecology and Obstetrics ( FIGO ) initiative on pre‐eclampsia: A pragmatic guide for first‐trimester screening and prevention
Poon, L. C., Shennan, A. H., Hyett, J. A., Kapur, A., Hadar, E., Divakar, H., McAuliffe, F. M., Costa, F. D. S., von Dadelszen, P., McIntyre, D. H., et al. (2019) · International Journal of Gynecology & Obstetrics · doi:10.1002/ijgo.12802 · Cited by 1,430
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 1,315
Self-citation
Pre-eclampsia: pathophysiology and clinical implications
Burton, G. J., Redman, C. W., Roberts, J. M., & Moffett, A. (2019) · BMJ · doi:10.1136/bmj.l2381 · Cited by 1,250
The hypertensive disorders of pregnancy: ISSHP classification, diagnosis & management recommendations for international practice
Brown, 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
Self-citation
Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis
Shibuya, M., & Claesson, L. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.11.012 · Cited by 1,083
Endothelial cells and VEGF in vascular development
Coultas, L., Chawengsaksophak, K., & Rossant, J. (2005) · Nature · doi:10.1038/nature04479 · Cited by 1,016
Pre-eclampsia
Chappell, 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
Preeclampsia, a Disease of the Maternal Endothelium
Powe, C. E., Levine, R. J., & Karumanchi, S. A. (2011) · Circulation · doi:10.1161/circulationaha.109.853127 · Cited by 987
Self-citation
Pre-eclampsia part 1: current understanding of its pathophysiology
Chaiworapongsa, T., Chaemsaithong, P., Yeo, L., & Romero, R. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.102 · Cited by 956
The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions
Takahashi, H., & Shibuya, M. (2005) · Clinical Science · doi:10.1042/cs20040370 · Cited by 990
Properties of the Glomerular Barrier and Mechanisms of Proteinuria
Haraldsson, B. S., Nystrom, J. C., & Deen, W. M. (2008) · Physiological Reviews · doi:10.1152/physrev.00055.2006 · Cited by 941
Revisiting biomarker discovery by plasma proteomics
Geyer, P. E., Holdt, L. M., Teupser, D., & Mann, M. (2017) · Molecular Systems Biology · doi:10.15252/msb.20156297 · Cited by 917
Placental Origins of Preeclampsia
Huppertz, B. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.107607 · Cited by 899
Inflammation and Pregnancy
Challis, J. R., Lockwood, C. J., Myatt, L., Norman, J. E., Strauss, J. F., & Petraglia, F. (2009) · Reproductive Sciences · doi:10.1177/1933719108329095 · Cited by 893
The biology of vascular endothelial growth factors
Tammela, T., Enholm, B., Alitalo, K. K., & Paavonen, K. (2005) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.12.002 · Cited by 859
The Placenta: A Multifaceted, Transient Organ
Burton, G. J., & Fowden, A. L. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0066 · Cited by 833
Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases
Shibuya, M. (2012) · The Journal of Biochemistry · doi:10.1093/jb/mvs136 · Cited by 820
Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface
Red‐Horse, K., Zhou, Y., Genbačev, O., Prakobphol, A., Foulk, R. A., McMaster, M., & Fisher, S. J. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200422991 · Cited by 796
VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature
Kamba, T., Tam, B. Y. Y., Hashizume, H., Haskell, A., Sennino, B., Mancuso, M. R., Norberg, S. M., O’Brien, S., Davis, R. B., Gowen, L. C., et al. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00133.2005 · Cited by 788
Matrix Metalloproteinases, Vascular Remodeling, and Vascular Disease
Wang, X. L., & Khalil, R. A. (2017) · Advances in pharmacology · doi:10.1016/bs.apha.2017.08.002 · Cited by 758
VEGFs and receptors involved in angiogenesis versus lymphangiogenesis
Lohela, M. K., Bry, M., Tammela, T., & Alitalo, K. K. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.12.012 · Cited by 751
Pathogenesis of Preeclampsia
Young, B. C., Levine, R. J., & Karumanchi, S. A. (2010) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-121808-102149 · Cited by 734
Self-citation
Inflammation, Immunity, and Hypertensive End-Organ Damage
McMaster, W. G., Kirabo, A., Madhur, M. S., & Harrison, D. G. (2015) · Circulation Research · doi:10.1161/circresaha.116.303697 · Cited by 708
Preeclampsia: Recent Insights
Roberts, J. M., & Gammill, H. S. (2005) · Hypertension · doi:10.1161/01.hyp.0000188408.49896.c5 · Cited by 693
Corneal avascularity is due to soluble VEGF receptor-1
Ambati, B. K., Nozaki, M., Singh, N., Takeda, A., Jani, P. D., Suthar, T., Albuquerque, R., Richter, E. R., Sakurai, E., Newcomb, M. T., et al. (2006) · Nature · doi:10.1038/nature05249 · Cited by 703
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
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
Self-citation
Preeclampsia and the Risk of End-Stage Renal Disease
Vikse, B. E., Irgens, L. M., Leivestad, T., Skjærven, R., & Iversen, B. M. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0706790 · Cited by 673
Angiogenic factors and the risk of adverse outcomes in women with suspected preeclampsia
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. (2012) · Circulation · doi:10.1161/circulationaha.111.054361 · Cited by 668
Self-citation
Preeclampsia: Updates in Pathogenesis, Definitions, and Guidelines
Phipps, E., Prasanna, D., Brima, W., & Jim, B. (2016) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.12081115 · Cited by 651
Differential Roles of Vascular Endothelial Growth Factor Receptor-1 and Receptor-2 in Angiogenesis
Shibuya, M. (2006) · BMB Reports · doi:10.5483/bmbrep.2006.39.5.469 · Cited by 630
The two-stage placental model of preeclampsia: An update
Staff, A. C. (2019) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2019.07.004 · Cited by 640
RETIRED: Diagnosis, Evaluation, and Management of the Hypertensive Disorders of Pregnancy
Magee, L. A., Helewa, M. E., Rey, É., Cardew, S., Côté, A., Douglas, M. J., Firoz, T., Gibson, P., Gruslin, A., Lange, I. R., et al. (2008) · Journal of Obstetrics and Gynaecology Canada · doi:10.1016/s1701-2163(16)32776-1 · Cited by 581
Cardiac angiogenic imbalance leads to peripartum cardiomyopathy
Patten, I. S., Rana, S., Shahul, S. S., Rowe, G. C., Jang, C., Liu, L., Hacker, M. R., Rhee, J. S., Mitchell, J., Mahmood, F. U., et al. (2012) · Nature · doi:10.1038/nature11040 · Cited by 577
Self-citation
Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction
Gilbert, J. S., Ryan, M. J., LaMarca, B. B., Sedeek, M. H., Murphy, S., & Granger, J. P. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01113.2007 · Cited by 561
Preeclampsia: The Role of Angiogenic Factors in Its Pathogenesis
Wang, A., Rana, S., & Karumanchi, S. A. (2009) · Physiology · doi:10.1152/physiol.00043.2008 · Cited by 561
Self-citation
Relaxin family peptides and their receptors
Bathgate, R. A. D., Halls, M. L., van der Westhuizen, E. T., Callander, G. E., Kocan, M., & Summers, R. J. (2013) · Physiological Reviews · doi:10.1152/physrev.00001.2012 · Cited by 534
Elevated Placental Soluble Vascular Endothelial Growth Factor Receptor-1 Inhibits Angiogenesis in Preeclampsia
Ahmad, S., & Ahmed, A. (2004) · Circulation Research · doi:10.1161/01.res.0000147365.86159.f5 · Cited by 524
Biology and therapeutic targeting of vascular endothelial growth factor A
Pérez, L., & Ferrara, N. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00631-w · Cited by 527
Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction
Girardi, G., Yarilin, D. A., Thurman, J. M., Holers, V. M., & Salmon, J. E. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20061022 · Cited by 509
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
Monocytes and Macrophages in Pregnancy and Pre-Eclampsia
Faas, M. M., Spaans, F., & de Vos, P. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00298 · Cited by 506
Targeting Proteins for Destruction by the Ubiquitin System: Implications for Human Pathobiology
Schwartz, A. L., & Ciechanover, A. J. (2008) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.051208.165340 · Cited by 498
Prospective Study of Infantile Hemangiomas: Demographic, Prenatal, and Perinatal Characteristics
Haggstrom, A. N., Drolet, B. A., Baselga, E., Chamlin, S. L., Garzón, M. C., Horii, K. A., Lucky, A. W., Mancini, A. J., Metry, D. W., Newell, B. D., et al. (2007) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2006.12.003 · Cited by 484
Angiogenic Factors and Preeclampsia
Maynard, S. E., & Karumanchi, S. A. (2011) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2010.10.004 · Cited by 494
Self-citation
Diagnosis, evaluation, and management of the hypertensive disorders of pregnancy
Magee, L. A., Pels, A., Helewa, M. E., Rey, É., & von Dadelszen, P. (2014) · Pregnancy Hypertension · doi:10.1016/j.preghy.2014.01.003 · Cited by 489
Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice
Zhou, C. C., Zhang, Y., Irani, R. A., Zhang, H., Mi, T., Popek, E. J., Hicks, J. M., Ramin, S. M., Kellems, R. E., & Xia, Y. (2008) · Nature Medicine · doi:10.1038/nm.1856 · Cited by 476
First-Trimester Prediction of Hypertensive Disorders in Pregnancy
Poon, L. C., Kametas, N. A., Maíz, N., Akolekar, R., & Nicolaides, K. H. (2009) · Hypertension · doi:10.1161/hypertensionaha.108.127977 · Cited by 472
Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia
Ness, R. B., & Sibai, B. M. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.07.049 · Cited by 469
Self-citation
Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis
Shibuya, M. (2006) · Angiogenesis · doi:10.1007/s10456-006-9055-8 · Cited by 457
Epidemiology of preeclampsia: impact of obesity
Jeyabalan, A. (2013) · Nutrition Reviews · doi:10.1111/nure.12055 · Cited by 456
IFPA Senior Award Lecture: Making sense of pre-eclampsia – Two placental causes of preeclampsia?
Redman, C. W. G., Sargent, I. L., & Staff, A. C. (2014) · Placenta · doi:10.1016/j.placenta.2013.12.008 · Cited by 446
Placental Productions and Expressions of Soluble Endoglin, Soluble fms-Like Tyrosine Kinase Receptor-1, and Placental Growth Factor in Normal and Preeclamptic Pregnancies
Gu, Y., Lewis, D. F., & Wang, Y. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1550 · Cited by 435
Pre-eclampsia: its pathogenesis and pathophysiolgy
Gathiram, P., & Moodley, J. (2016) · Cardiovascular journal of South Africa/Cardiovascular journal of Southern Africa · doi:10.5830/cvja-2016-009 · Cited by 444
The placenta in preeclampsia
Roberts, J. M., & Escudero, C. (2012) · Pregnancy Hypertension · doi:10.1016/j.preghy.2012.01.001 · Cited by 430
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
Vascular endothelial growth factor signaling in health and disease: from molecular mechanisms to therapeutic perspectives
Lee, C., Kim, M., Kumar, A., Lee, H., Yang, Y., & Kim, Y. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02249-0 · Cited by 452
Uterine artery Doppler at 11 + 0 to 13 + 6 weeks in the prediction of pre‐eclampsia
Plasencia, W., Maiz, N., Bonino, S., Kaihura, C., & Nicolaides, K. H. (2007) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.5157 · Cited by 425
Negative Regulation of Soluble Flt-1 and Soluble Endoglin Release by Heme Oxygenase-1
Cudmore, M., Ahmad, S., Al‐Ani, B., Fujisawa, T., Coxall, H., Chudasama, K., Devey, L. R., Wigmore, S. J., Abbas‐Hanif, A., Hewett, P. W., et al. (2007) · Circulation · doi:10.1161/circulationaha.106.660134 · Cited by 425
Syncytiotrophoblast stress in preeclampsia: the convergence point for multiple pathways
Redman, C. W. G., Staff, A. C., & Roberts, J. M. (2021) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.09.047 · Cited by 419
Circulating Angiogenic Factors in the Pathogenesis and Prediction of Preeclampsia
Lam, C. S., Lim, K.-H., & Karumanchi, S. A. (2005) · Hypertension · doi:10.1161/01.hyp.0000187899.34379.b0 · Cited by 408
Self-citation
Induction of Neutrophil Extracellular DNA Lattices by Placental Microparticles and IL-8 and Their Presence in Preeclampsia
Gupta, A. K., Hasler, P., Holzgreve, W., Gebhardt, G., & Hahn, S. (2005) · Human Immunology · doi:10.1016/j.humimm.2005.11.003 · Cited by 412
Molecular Evidence of Placental Hypoxia in Preeclampsia
Soleymanlou, N., Jurišica, I., Nevo, O., Ietta, F., Zhang, X., Zamudio, S., Post, M., & Caniggia, I. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0078 · Cited by 400
Oxidative stress: Normal pregnancy versus preeclampsia
Chiarello, D. I., Abad, C., Rojas, D., Toledo, F., Vázquez, C. M., Mate, A., Sobrevía, L., & Marı́n, R. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.12.005 · Cited by 394
Placental trophoblast cell differentiation: Physiological regulation and pathological relevance to preeclampsia
Ji, L., Brkić, J., Liu, M., Fu, G., Peng, C., & Wang, Y. (2012) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2012.12.008 · Cited by 394
Liver disease in pregnancy
Joshi, D., James, A., Quaglia, A., Westbrook, R. H., & Heneghan, M. A. (2010) · The Lancet · doi:10.1016/s0140-6736(09)61495-1 · Cited by 385
Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia
Kanasaki, K., Palmsten, K., Sugimoto, H., Ahmad, S., Hamano, Y., Xie, L., Parry, S., Augustin, H. G., Gattone, V. H., Folkman, J., et al. (2008) · Nature · doi:10.1038/nature06951 · Cited by 381
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 394
Redefining Preeclampsia Using Placenta-Derived Biomarkers
Staff, A. C., Benton, S. J., von Dadelszen, P., Roberts, J. M., Taylor, R. N., Powers, R. W., Jones, D. S., & Redman, C. W. G. (2013) · Hypertension · doi:10.1161/hypertensionaha.111.00250 · Cited by 383
New Gestational Phase–Specific Cutoff Values for the Use of the Soluble fms-Like Tyrosine Kinase-1/Placental Growth Factor Ratio as a Diagnostic Test for Preeclampsia
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
Preeclampsia, biomarkers, syncytiotrophoblast stress, and placental capacity
Redman, C. W. G., & Staff, A. C. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.08.003 · Cited by 382
Hypertension in Pregnancy and Later Cardiovascular Risk
Romundstad, P., Magnussen, E. B., Smith, G. D., & VATTEN, L. J. (2010) · Circulation · doi:10.1161/circulationaha.110.943407 · Cited by 372
Pre‐eclampsia‐like syndrome induced by severe COVID‐19: a prospective observational study
Mendoza, M., García-Ruiz, I., Maíz, N., Rodó, C., García‐Manau, P., Serrano, B., Lopez‐Martinez, R., Balcells, J., Fernández‐Hidalgo, N., Carreras, E., et al. (2020) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.16339 · Cited by 372
Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model
Kumasawa, K., Ikawa, M., Kidoya, H., Hasuwa, H., Saito‐Fujita, T., Morioka, Y., Takakura, N., Kimura, T., & Okabe, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011293108 · Cited by 373
Prospective Study of Placental Angiogenic Factors and Maternal Vascular Function Before and After Preeclampsia and Gestational Hypertension
Noori, M., Donald, A. E., Angelakopoulou, A., Hingorani, A. D., & Williams, D. J. (2010) · Circulation · doi:10.1161/circulationaha.109.895458 · Cited by 364
Spontaneous Coronary Artery Dissection Associated With Pregnancy
Tweet, M. S., Hayes, S. N., Codsi, E., Gulati, R., Rose, C. H., & Best, P. J. M. (2017) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.05.055 · Cited by 360
Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia
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
Increased Preeclampsia Risk and Reduced Aortic Compliance With In Vitro Fertilization Cycles in the Absence of a Corpus Luteum
von Versen‐Höynck, F., Schaub, A. M., Chi, Y.-Y., Chiu, K.-H., Liu, J., Lingis, M., Williams, R. S., Rhoton-Vlasak, A. S., Nichols, W. W., Fleischmann, R. R., et al. (2019) · Hypertension · doi:10.1161/hypertensionaha.118.12043 · Cited by 354
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
Self-citation
Placental growth factor and pre-eclampsia
Chau, K., Hennessy, A., & Makris, A. (2017) · Journal of Human Hypertension · doi:10.1038/jhh.2017.61 · Cited by 370
Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1
Nevo, O., Soleymanlou, N., Wu, Y., Xu, J., Kingdom, J. C., Many, A., Zamudio, S., & Caniggia, I. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00794.2005 · Cited by 361
Imbalances in circulating angiogenic factors in the pathophysiology of preeclampsia and related disorders
Rana, 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
Self-citation
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
Self-citation
Vascular adaptation in pregnancy and endothelial dysfunction in preeclampsia
Boeldt, D. S., & Bird, I. M. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0340 · Cited by 360
Elevated Blood Pressure in Pregnancy and Subsequent Chronic Disease Risk
Männistö, T. I., Mendola, P., Vääräsmäki, M., Järvelin, M., Hartikainen, A., Pouta, A. M., & Suvanto, E. T. J. (2013) · Circulation · doi:10.1161/circulationaha.112.128751 · Cited by 344
Mechanisms of VEGF (Vascular Endothelial Growth Factor) Inhibitor–Associated Hypertension and Vascular Disease
Pandey, A. K., Singhi, E. K., Arroyo, J. P., Ikizler, T. A., Gould, E. R., Brown, J. D., Beckman, J. A., Harrison, D. G., & Moslehi, J. J. (2017) · Hypertension · doi:10.1161/hypertensionaha.117.10271 · Cited by 346

Authors: 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., Sibai, B. M., Sukhatme, V. P., & Karumanchi, S. A.
Affiliations: National Institutes of Health (US)
Beth Israel Deaconess Medical Center (US)
Allied Technology (United States) (US)
Harvard University (US)
University of Cincinnati (US)
ORCID: Qian, Cong
England, Lucinda J.
Schisterman, Enrique F.
Thadhani, Ravi
Sachs, Benjamin P.
Sukhatme, Vikas P.
Karumanchi, S. Ananth
Venue: New England Journal of Medicine
Publisher: Massachusetts Medical Society
Published: 2004-02-12
Volume: 350
Issue: 7
Pages: 672-683
ISSN: 0028-4793 (ISSN-L)
1533-4406
DOI: 10.1056/nejmoa031884
OpenAlex: W2081255404
Cited by: 3,720
References: 24
Citations by year: 2026: 148 · 2025: 165 · 2024: 142 · 2023: 152 · 2022: 207 · 2021: 180 · 2020: 170 · 2019: 182 · 2018: 185 · 2017: 229 · 2016: 201 · 2015: 171 · 2014: 193 · 2013: 199 · 2012: 185
FWCI: 122.15
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: New England Journal of Medicine (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Clinical Neurology › Neurological Complications and Syndromes
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: preeclampsia, soluble fms-like tyrosine kinase-1, placental growth factor, vascular endothelial growth factor, angiogenic factors, serum biomarkers, preeclampsia risk prediction, small for gestational age, nulliparous women
MeSH terms: Placenta Growth Factor, Adult, Cross-Sectional Studies, Female, Gestational Age, Humans, Pre-Eclampsia, Pregnancy, Pregnancy Proteins, Risk Factors, Biomarkers, Body Mass Index, Logistic Models, Odds Ratio, Case-Control Studies, Statistics, Nonparametric, Vascular Endothelial Growth Factor Receptor-1, Vascular Endothelial Growth Factor A

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

Circulating Angiogenic Factors and the Risk of Preeclampsia

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks