Circulating Angiogenic Factors and the Risk of Preeclampsia

doi:10.1056/NEJMoa031884

Volume 350:672-683		February 12, 2004		Number 7

Circulating Angiogenic Factors and the Risk of Preeclampsia

Richard J. Levine, M.D., M.P.H., Sharon E. Maynard, M.D., Cong Qian, M.S., Kee-Hak Lim, M.D., Lucinda J. England, M.D., M.S.P.H., Kai F. Yu, Ph.D., Enrique F. Schisterman, Ph.D., Ravi Thadhani, M.D., M.P.H., Benjamin P. Sachs, M.B., B.S., D.P.H., Franklin H. Epstein, M.D., Baha M. Sibai, M.D., Vikas P. Sukhatme, M.D., Ph.D., and S. Ananth Karumanchi, M.D.

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ABSTRACT

Background The cause of preeclampsia remains unclear. Limiteddata suggest that excess circulating soluble fms-like tyrosinekinase 1 (sFlt-1), which binds placental growth factor (PlGF)and vascular endothelial growth factor (VEGF), may have a pathogenicrole.

Methods We performed a nested case–control study withinthe Calcium for Preeclampsia Prevention trial, which involvedhealthy nulliparous women. Each woman with preeclampsia wasmatched to one normotensive control. A total of 120 pairs ofwomen were randomly chosen. Serum concentrations of angiogenicfactors (total sFlt-1, free PlGF, and free VEGF) were measuredthroughout pregnancy; there were a total of 655 serum specimens.The data were analyzed cross-sectionally within intervals ofgestational age and according to the time before the onset ofpreeclampsia.

Results During the last two months of pregnancy in the normotensivecontrols, the level of sFlt-1 increased and the level of PlGFdecreased. These changes occurred earlier and were more pronouncedin the women in whom preeclampsia later developed. The sFlt-1level increased beginning approximately five weeks before theonset of preeclampsia. At the onset of clinical disease, themean serum level in the women with preeclampsia was 4382 pgper milliliter, as compared with 1643 pg per milliliter in controlswith fetuses of similar gestational age (P<0.001). The PlGFlevels were significantly lower in the women who later had preeclampsiathan 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 beforethe onset of preeclampsia, coincident with the increase in thesFlt-1 level. Alterations in the levels of sFlt-1 and free PlGFwere greater in women with an earlier onset of preeclampsiaand in women in whom preeclampsia was associated with a small-for-gestational-ageinfant.

Conclusions Increased levels of sFlt-1 and reduced levels ofPlGF predict the subsequent development of preeclampsia.

Source Information

From the Division of Epidemiology, Statistics, and Prevention Research, National Institute of Child Health and Human Development, Department of Health and Human Services, Bethesda, Md. (R.J.L., L.J.E., K.F.Y., E.F.S.); the Departments of Medicine (S.E.M., F.H.E., V.P.S., S.A.K.) and Obstetrics and Gynecology (K.-H.L., B.P.S., S.A.K.), Beth Israel Deaconess Medical Center and Harvard Medical School, Boston; Allied Technology Group, Rockville, Md. (C.Q.); the Harvard School of Public Health, Boston (B.P.S.); the Departments of Medicine and Obstetrics, Massachusetts General Hospital and Harvard Medical School, Boston (R.T.); and the Department of Obstetrics and Gynecology, University of Cincinnati College of Medicine, Cincinnati (B.M.S.).

Drs. Levine and Karumanchi contributed equally to the article.

Address reprint requests to Dr. Levine at the National Institute of Child Health and Human Development, Bldg. 6100, Rm. 7B03, Bethesda, MD 20892, or at levinerj{at}mail.nih.gov, or to Dr. Karumanchi at Beth Israel Deaconess Medical Center, 330 Brookline Ave., Dana 517, Boston, MA 02215, or at sananth{at}bidmc.harvard.edu.

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Circulating Angiogenic Factors and Preeclampsia
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N Engl J Med 2004; 350:2003-2004, May 6, 2004. Correspondence

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Cohen, A., Lim, K.-H., Lee, Y., Rana, S., Karumanchi, S. A., Brown, F. (2007). Circulating Levels of the Antiangiogenic Marker Soluble FMS-Like Tyrosine Kinase 1 Are Elevated in Women With Pregestational Diabetes and Preeclampsia: Angiogenic markers in preeclampsia and preexisting diabetes. Diabetes Care 30: 375-377 [Full Text]
Zhou, C. C., Ahmad, S., Mi, T., Xia, L., Abbasi, S., Hewett, P. W., Sun, C., Ahmed, A., Kellems, R. E., Xia, Y. (2007). Angiotensin II Induces Soluble fms-Like Tyrosine Kinase-1 Release via Calcineurin Signaling Pathway in Pregnancy. Circ. Res. 100: 88-95 [Abstract] [Full Text]
Williams, P. J., Gumaa, K., Scioscia, M., Redman, C. W., Rademacher, T. W. (2007). Inositol Phosphoglycan P-Type in Preeclampsia: A Novel Marker?. Hypertension 49: 84-89 [Abstract] [Full Text]
Luft, F. C. (2006). Soluble endoglin (sEng) joins the soluble fms-like tyrosine kinase (sFlt) receptor as a pre-eclampsia molecule. Nephrol Dial Transplant 21: 3052-3054 [Full Text]
Allen, J. A., Adlakha, A., Bergethon, P. R. (2006). Reversible Posterior Leukoencephalopathy Syndrome After Bevacizumab/FOLFIRI Regimen for Metastatic Colon Cancer.. Arch Neurol 63: 1475-1478 [Abstract] [Full Text]
Nevo, O., Soleymanlou, N., Wu, Y., Xu, J., Kingdom, J., Many, A., Zamudio, S., Caniggia, I. (2006). Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R1085-R1093 [Abstract] [Full Text]

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