Circulating angiogenic factors and the risk of preeclampsia
Open accessAbstract
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.
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There is excessive production of sVEGFR-1 and soluble endoglin in the uterus of preeclamptic patients proportional to the severity of the disease.
“There is excessive production of sVEGFR-1 and soluble endoglin in the uterus of preeclamptic patients(121) proportional to the severity of the disease (151–153)”
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 [151]
Cites
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 · see citing works
Self-citationYang, 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 2,681 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Zhou, Y., Damsky, C. H., & Fisher, S. J. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119388 · Cited by 937 · see citing works
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 639 · see citing works
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 · see citing works
Self-citationWalker, J. J. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02800-2 · Cited by 519 · see citing works
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 461 · see citing works
Taylor, R. N., Grimwood, J., Taylor, R. S., McMaster, M., Fisher, S. J., & North, R. A. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2003.111 · Cited by 410 · see citing works
Koga, K., Osuga, Y., Yoshino, O., Hirota, Y., Ruimeng, X., Hirata, T., Takeda, S., Yano, T., Tsutsumi, O., & Taketani, Y. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021942 · Cited by 403 · see citing works
Birth-Weight-for-Gestational-Age Patterns by Race, Sex, and Parity in the United States Population
Zhang, J. (1995) · Obstetrics and Gynecology · doi:10.1016/0029-7844(95)00142-e · Cited by 297 · see citing works
Preeclampsia is associated with reduced serum levels of placenta growth factor
Torry, D. S., Wang, H., Wang, T., Caudle, M. R., & Torry, R. J. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70021-3 · Cited by 286 · see citing works
Excessive placental secretion of neurokinin B during the third trimester causes pre-eclampsia
Page, N., Woods, R. J., Gardiner, S. M., Lomthaisong, K., Gladwell, R. T., Butlin, D., Manyonda, I., & Lowry, P. J. (2000) · Nature · doi:10.1038/35015579 · Cited by 250 · see citing works
Disturbed Feto-Maternal Cell Traffic in Preeclampsia
Holzgreve, W., GHEZZI, F., NARO, E. D., GÄNSHIRT, D., MAYMON, E., & HAHN, S. (1998) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(98)00068-4 · Cited by 247 · see citing works
Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia
Tidwell, S., Ho, H., Chiu, W.-H., Torry, R. J., & Torry, D. S. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.113129 · Cited by 231 · see citing works
Polliotti, B. (2003) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(03)00338-7 · Cited by 225 · see citing works
Glomerular endotheliosis in normal pregnancy and pre-eclampsia
Strevens, H., Wide‐Swensson, D., Hansen, A., Horn, T. D., Ingemarsson, I., Larsen, S., Willner, J., & Olsen, S. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2003.02162.x · Cited by 176 · see citing works
Cockell, A., Learmont, J. G., Smárason, A. K., Redman, C. W. G., Sargent, I. L., & Poston, L. (1997) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1997.tb11052.x · Cited by 171 · see citing works
Plasma placenta growth factor levels in midtrimester pregnancies
Tjoa, M. L. (2001) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01497-1 · Cited by 103 · see citing works
Expression and Function of Placenta Growth Factor: Implications for Abnormal Placentation
Torry, D., Mukherjea, D., Arroyo, J. A., & Torry, R. J. (2003) · Journal of the Society for Gynecologic Investigation · doi:10.1016/s1071-5576(03)00048-0 · Cited by 102 · see citing works
Decreased Maternal Serum Placenta Growth Factor in Early Second Trimester and Preeclampsia
Su, Y. N., Lee, C., Cheng, W., Shau, W. Y., Chow, S. N., & Hsieh, F. J. (2001) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(01)01341-2 · Cited by 89 · see citing works
Trial of calcium for preeclampsia prevention (CPEP): Rationale, design, and methods
Levine, R. J., Esterlitz, J., Raymond, E. G., DerSimonian, R., Hauth, J. C., Curet, L. B., Sibai, B. M., Catalano, P. M., Morris, C. D., Clemens, J. D., et al. (1996) · Controlled Clinical Trials · doi:10.1016/s0197-2456(96)00106-7 · Cited by 74 · see citing works
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Vascular Endothelial Growth Factor: Basic Science and Clinical Progress
Ferrara, N. (2004) · Endocrine Reviews · doi:10.1210/er.2003-0027 · Cited by 3,707 · see citing works
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 · see citing works
Rana (2019) · doi:10.1161/circresaha.118.313276 · Cited by 2,095 · see citing works
Self-citationBrown, 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 · see citing works
Self-citationPreterm labor: One syndrome, many causes
Romero, R., Dey, S. K., & Fisher, S. J. (2014) · Science · doi:10.1126/science.1251816 · Cited by 1,984 · see citing works
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 · see citing works
Self-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 1,820 · see citing works
Sibai, B. M., Dekker, G., & Kupferminc, M. J. (2005) · The Lancet · doi:10.1016/s0140-6736(05)17987-2 · Cited by 1,815 · see citing works
Self-citationSoluble 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 1,804 · see citing works
Self-citationShibuya, M. (2011) · Genes & Cancer · doi:10.1177/1947601911423031 · Cited by 1,778 · see citing works
Perkins, N. J., & Schisterman, E. F. (2006) · American Journal of Epidemiology · doi:10.1093/aje/kwj063 · Cited by 1,753 · see citing works
Self-citationThe 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 1,674 · see citing works
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 1,619 · see citing works
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 · see citing works
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 1,500 · see citing works
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 1,343 · see citing works
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 1,255 · see citing works
Self-citationPre-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 · see citing works
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 1,089 · see citing works
Self-citationSignal 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 1,057 · see citing works
Endothelial cells and VEGF in vascular development
Coultas, L., Chawengsaksophak, K., & Rossant, J. (2005) · Nature · doi:10.1038/nature04479 · Cited by 1,016 · see citing works
Chappell, L. C., Cluver, C. A., Kingdom, J. C., & Tong, S. (2021) · The Lancet · doi:10.1016/s0140-6736(20)32335-7 · Cited by 977 · see citing works
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 972 · see citing works
Self-citationPre-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 · see citing works
Takahashi, H., & Shibuya, M. (2005) · Clinical Science · doi:10.1042/cs20040370 · Cited by 950 · see citing works
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 919 · see citing works
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 · see citing works
Placental Origins of Preeclampsia
Huppertz, B. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.107607 · Cited by 899 · see citing works
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 · see citing works
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 838 · see citing works
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 · see citing works
Shibuya, M. (2012) · The Journal of Biochemistry · doi:10.1093/jb/mvs136 · Cited by 796 · see citing works
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 785 · see citing works
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 773 · see citing works
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 · see citing works
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 731 · see citing works
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 722 · see citing works
Self-citationInflammation, 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 · see citing works
Roberts, J. M., & Gammill, H. S. (2005) · Hypertension · doi:10.1161/01.hyp.0000188408.49896.c5 · Cited by 693 · see citing works
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 686 · see citing works
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 675 · see citing works
Self-citationPreeclampsia 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 · see citing works
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 · see citing works
Self-citationPreeclampsia: 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 633 · see citing works
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 623 · see citing works
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 613 · see citing works
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 580 · see citing works
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 570 · see citing works
Self-citationGilbert, 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 553 · see citing works
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 552 · see citing works
Self-citationRelaxin 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 · see citing works
Ahmad, S., & Ahmed, A. (2004) · Circulation Research · doi:10.1161/01.res.0000147365.86159.f5 · Cited by 516 · see citing works
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 515 · see citing works
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 507 · see citing works
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 · see citing works
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 495 · see citing works
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 491 · see citing works
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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 · see citing works
Angiogenic Factors and Preeclampsia
Maynard, S. E., & Karumanchi, S. A. (2011) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2010.10.004 · Cited by 482 · see citing works
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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 470 · see citing works
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 465 · see citing works
Ness, R. B., & Sibai, B. M. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.07.049 · Cited by 460 · see citing works
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Jeyabalan, A. (2013) · Nutrition Reviews · doi:10.1111/nure.12055 · Cited by 440 · see citing works
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 437 · see citing works
Gu, Y., Lewis, D. F., & Wang, Y. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1550 · Cited by 434 · see citing works
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 433 · see citing works
Roberts, J. M., & Escudero, C. (2012) · Pregnancy Hypertension · doi:10.1016/j.preghy.2012.01.001 · Cited by 430 · see citing works
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 429 · see citing works
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 427 · see citing works
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 · see citing works
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 421 · see citing works
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 411 · see citing works
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 406 · see citing works
Self-citationGupta, A. K., Hasler, P., Holzgreve, W., Gebhardt, G., & Hahn, S. (2005) · Human Immunology · doi:10.1016/j.humimm.2005.11.003 · Cited by 403 · see citing works
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 394 · see citing works
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 · see citing works
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 386 · see citing works
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 · see citing works
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 · see citing works
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 381 · see citing works
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 375 · see citing works
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 · see citing works
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 373 · see citing works
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 · see citing works
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 · see citing works
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 366 · see citing works
Noori, M., Donald, A. E., Angelakopoulou, A., Hingorani, A. D., & Williams, D. J. (2010) · Circulation · doi:10.1161/circulationaha.109.895458 · Cited by 361 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Self-citationPlacental growth factor and pre-eclampsia
Chau, K., Hennessy, A., & Makris, A. (2017) · Journal of Human Hypertension · doi:10.1038/jhh.2017.61 · Cited by 352 · see citing works
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 351 · see citing works
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 351 · see citing works
Self-citationPilot 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 347 · see citing works
Self-citationVascular 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 346 · see citing works
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 342 · see citing works
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 342 · see citing works
- 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
- 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
- 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 › Psychiatry and Mental health › 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
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