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Original Article

A prospective cohort study of the value of maternal plasma concentrations of angiogenic and anti-angiogenic factors in early pregnancy and midtrimester in the identification of patients destined to develop preeclampsia

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Pages 1021-1038 | Received 19 Feb 2009, Accepted 09 Apr 2009, Published online: 17 Mar 2010

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Dahiana M. Gallo, Wendy Fitzgerald, Roberto Romero, Nardhy Gomez-Lopez, Dereje W. Gudicha, Nándor Gábor Than, Mariachiara Bosco, Tinnakorn Chaiworapongsa, Eunjung Jung, Arun Meyyazhagan, Manaphat Suksai, Francesca Gotsch, Offer Erez, Adi L. Tarca & Leonid Margolis. (2023) Proteomic profile of extracellular vesicles in maternal plasma of women with fetal death. The Journal of Maternal-Fetal & Neonatal Medicine 36:1.
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Sun Kwon Kim, Sangeetha Vishweswaraiah, Jacqueline Macknis, Ali Yilmaz, Ashna Lalwani, Nitish K. Mishra, Chittibabu Guda, Dotun Ogunyemi, Uppala Radhakrishna & Ray O. Bahado-Singh. (2022) New-onset postpartum preeclampsia: epigenetic mechanism and prediction. The Journal of Maternal-Fetal & Neonatal Medicine 35:25, pages 7179-7187.
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Bogdan Panaitescu, Roberto Romero, Nardhy Gomez-Lopez, Percy Pacora, Offer Erez, Felipe Vadillo-Ortega, Lami Yeo, Sonia S. Hassan & Chaur-Dong Hsu. (2020) ELABELA plasma concentrations are increased in women with late-onset preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 33:1, pages 5-15.
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Nikolina Docheva, Roberto Romero, Piya Chaemsaithong, Adi L. Tarca, Gaurav Bhatti, Percy Pacora, Bogdan Panaitescu, Noppadol Chaiyasit, Tinnakorn Chaiworapongsa, Eli Maymon, Sonia S. Hassan & Offer Erez. (2019) The profiles of soluble adhesion molecules in the “great obstetrical syndromes”*. The Journal of Maternal-Fetal & Neonatal Medicine 32:13, pages 2113-2136.
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Kristina Kumer, Tanja Premru-Sršen, Vesna Fabjan-Vodušek, Nataša Tul, Teja Fabjan & Joško Osredkar. (2018) Peripheral arterial tonometry and angiogenic biomarkers in preeclampsia. Hypertension in Pregnancy 37:4, pages 197-203.
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Roberto Romero, Piya Chaemsaithong, Adi L. Tarca, Steven J. Korzeniewski, Eli Maymon, Percy Pacora, Bogdan Panaitescu, Noppadol Chaiyasit, Zhong Dong, Offer Erez, Sonia S. Hassan & Tinnakorn Chaiworapongsa. (2018) Maternal plasma-soluble ST2 concentrations are elevated prior to the development of early and late onset preeclampsia – a longitudinal study. The Journal of Maternal-Fetal & Neonatal Medicine 31:4, pages 418-432.
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Ana Jakovljevic, Mirjana Bogavac, Zagorka Lozanov-Crvenkovic, Mirjana Milosević-Tosic, Aleksandra Nikolic & Gorana Mitic. (2017) Early pregnancy angiogenic proteins levels and pregnancy related hypertensive disorders. The Journal of Maternal-Fetal & Neonatal Medicine 30:5, pages 534-539.
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Sebastian Kwiatkowski, Ewa Kwiatkowska, Rafał Rzepka, Andrzej Torbe & Barbara Dolegowska. (2016) Ischemic placental syndrome – prediction and new disease monitoring. The Journal of Maternal-Fetal & Neonatal Medicine 29:12, pages 2033-2039.
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Tinnakorn Chaiworapongsa, Roberto Romero, Amy E. Whitten, Steven J. Korzeniewski, Piya Chaemsaithong, Edgar Hernandez-Andrade, Lami Yeo & Sonia S. Hassan. (2016) The use of angiogenic biomarkers in maternal blood to identify which SGA fetuses will require a preterm delivery and mothers who will develop pre-eclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 29:8, pages 1214-1228.
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Tinnakorn Chaiworapongsa, Roberto Romero, Steven J. Korzeniewski, Piya Chaemsaithong, Edgar Hernandez-Andrade, James H. Segars, Alan H. DeCherney, M. Cathleen McCoy, Chong Jai Kim, Lami Yeo & Sonia S. Hassan. (2016) Pravastatin to prevent recurrent fetal death in massive perivillous fibrin deposition of the placenta (MPFD). The Journal of Maternal-Fetal & Neonatal Medicine 29:6, pages 855-862.
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Sara Zullino, Daniela Di Martino, Tamara Stampalija & Enrico Ferrazzi. (2016) New lenses to look at preeclampsia. Gynecological Endocrinology 32:2, pages 87-90.
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Piya Chaemsaithong, Roberto Romero, Adi L. Tarca, Steven J. Korzeniewski, Alyse G. Schwartz, Jezid Miranda, Ahmed I. Ahmed, Zhong Dong, Sonia S. Hassan, Lami Yeo & Tinnakorn Tinnakorn. (2015) Maternal plasma fetuin-A concentration is lower in patients who subsequently developed preterm preeclampsia than in uncomplicated pregnancy: a longitudinal study. The Journal of Maternal-Fetal & Neonatal Medicine 28:11, pages 1260-1269.
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Thushari I. Alahakoon, Weiyi Zhang, Brian J. Trudinger & Vincent W. Lee. (2014) Discordant clinical presentations of preeclampsia and intrauterine fetal growth restriction with similar pro- and anti-angiogenic profiles. The Journal of Maternal-Fetal & Neonatal Medicine 27:18, pages 1854-1859.
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Kedak Baltajian, Jonathan L. Hecht, Julia B. Wenger, Saira Salahuddin, Stefan Verlohren, Frank H. Perschel, Zsuzsanna K. Zsengeller, Ravi Thadhani, S. Ananth Karumanchi & Sarosh Rana. (2014) Placental lesions of vascular insufficiency are associated with anti-angiogenic state in women with preeclampsia. Hypertension in Pregnancy 33:4, pages 427-439.
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Tiffany A. Moore Simas, Sybil L. Crawford, Susanne Bathgate, Jing Yan, Laura Robidoux, Melissa Moore & Sharon E. Maynard. (2014) Angiogenic biomarkers for prediction of early preeclampsia onset in high-risk women. The Journal of Maternal-Fetal & Neonatal Medicine 27:10, pages 1038-1048.
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Ratko Delić, Mario Štefanović, Štefka Krivec & Vladimir Weber. (2014) Statistical regression model of standard and new laboratory markers and its usefulness in prediction of preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 27:4, pages 388-392.
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Allison L. Cohen, Julia B. Wenger, Tamarra James-Todd, Brooke M. Lamparello, Elizabeth Halprin, Shanti Serdy, Shuling Fan, Gary L. Horowitz, Kee-Hak Lim, Sarosh Rana, Tamara C. Takoudes, Jennifer A. Wyckoff, Ravi Thadhani, S. Ananth Karumanchi & Florence M. Brown. (2014) The association of circulating angiogenic factors and HbA1c with the risk of preeclampsia in women with preexisting diabetes. Hypertension in Pregnancy 33:1, pages 81-92.
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Hironori Takahashi, Michi Hisano, Haruhiko Sago, Atsuko Murashima & Koushi Yamaguchi. (2014) Hypoproteinemia in the second trimester among patients with preeclampsia prior to the onset of clinical symptoms. Hypertension in Pregnancy 33:1, pages 55-60.
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Tinnakorn Chaiworapongsa, Roberto Romero, Steven J. Korzeniewski, Josef M. Cortez, Athina Pappas, Adi L. Tarca, Piya Chaemsaithong, Zhong Dong, Lami Yeo & Sonia S. Hassan. (2014) Plasma concentrations of angiogenic/anti-angiogenic factors have prognostic value in women presenting with suspected preeclampsia to the obstetrical triage area: a prospective study. The Journal of Maternal-Fetal & Neonatal Medicine 27:2, pages 132-144.
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Tamara Stampalija, Tinnakorn Chaiworapongsa, Roberto Romero, Piya Chaemsaithong, Steven J. Korzeniewski, Alyse G. Schwartz, Enrico M. Ferrazzi, Zhong Dong & Sonia S. Hassan. (2013) Maternal plasma concentrations of sST2 and angiogenic/anti-angiogenic factors in preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 26:14, pages 1359-1370.
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Nikolaos Vrachnis, Emmanouil Kalampokas, Stavros Sifakis, Nikolaos Vitoratos, Theodoros Kalampokas, Demetrios Botsis & Zoe Iliodromiti. (2013) Placental growth factor (PlGF): a key to optimizing fetal growth. The Journal of Maternal-Fetal & Neonatal Medicine 26:10, pages 995-1002.
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Shin Young Kim, So Yeon Park, Mi Jin Kim, Bom Yi Lee, Jung Yeol Han & Hyun Mee Ryu. (2013) Preeclampsia is associated with an elevation of plasma sMet concentrations in the second trimester. The Journal of Maternal-Fetal & Neonatal Medicine 26:9, pages 860-865.
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Sarosh Rana, William T. Schnettler, Camille Powe, Julia Wenger, Saira Salahuddin, Ana Sofia Cerdeira, Stefan Verlohren, Frank H. Perschel, Zoltan Arany, Kee-Hak Lim, Ravi Thadhani & S. Ananth Karumanchi. (2013) Clinical characterization and outcomes of preeclampsia with normal angiogenic profile. Hypertension in Pregnancy 32:2, pages 189-201.
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Tamar Eshkoli, Gershon Holcberg, Bella Bronfenmacher, Alaa Amash, Mahmoud Huleihel & Offer Erez. (2013) Perfusion with magnesium sulfate increases sFlt-1 secretion only in the fetal side of placenta of women with preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 26:2, pages 116-122.
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Andreea G. Moore, Heather Young, Jennifer M. Keller, Linda R. Ojo, Jing Yan, Tiffany A. Moore Simas & Sharon E. Maynard. (2012) Angiogenic biomarkers for prediction of maternal and neonatal complications in suspected preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 25:12, pages 2651-2657.
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Jimmy Espinoza. (2012) The need to redefine preeclampsia. Expert Opinion on Medical Diagnostics 6:4, pages 347-357.
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L. M. Reyes, R. G. García, S. L. Ruiz, D. Broadhurst, G. Aroca, S. T. Davidge & P. López-Jaramillo. (2012) Angiogenic imbalance and plasma lipid alterations in women with preeclampsia from a developing country. Growth Factors 30:3, pages 158-166.
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Eleazar Soto, Roberto Romero, Juan Pedro Kusanovic, Giovanna Ogge, Youssef Hussein, Lami Yeo, Sonia S Hassan, Chong Jai Kim & Tinnakorn Chaiworapongsa. (2012) Late-onset preeclampsia is associated with an imbalance of angiogenic and anti-angiogenic factors in patients with and without placental lesions consistent with maternal underperfusion. The Journal of Maternal-Fetal & Neonatal Medicine 25:5, pages 498-507.
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Tinnakorn Chaiworapongsa, Roberto Romero, Zeynep Alpay Savasan, Juan Pedro Kusanovic, Giovanna Ogge, Eleazar Soto, Zhong Dong, Adi Tarca, Bhatti Gaurav & Sonia S. Hassan. (2011) Maternal plasma concentrations of angiogenic/anti-angiogenic factors are of prognostic value in patients presenting to the obstetrical triage area with the suspicion of preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 24:10, pages 1187-1207.
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Roberto Romero, Tinnakorn Chaiworapongsa, Offer Erez, Adi L. Tarca, Maria Teresa Gervasi, Juan Pedro Kusanovic, Pooja Mittal, Giovanna Ogge, Edi Vaisbuch, Shali Mazaki-Tovi, Zhong Dong, Sun Kwon Kim, Lami Yeo & Sonia S. Hassan. (2010) An imbalance between angiogenic and anti-angiogenic factors precedes fetal death in a subset of patients: results of a longitudinal study. The Journal of Maternal-Fetal & Neonatal Medicine 23:12, pages 1384-1399.
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Hisashi Masuyama & Yuji Hiramatsu. (2010) Angiogenic proteins and adipocytokines as markers for prediction of preeclampsia. Expert Review of Obstetrics & Gynecology 5:6, pages 717-725.
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Giovanna Oggé, Roberto Romero, Tinnakorn Chaiworapongsa, Maria Teresa Gervasi, Percy Pacora, Offer Erez, Juan Pedro Kusanovic, Edi Vaisbuch, Shali Mazaki-Tovi, Francesca Gotsch, Pooja Mittal, Yeon Mee Kim & Sonia S. Hassan. (2010) Leukocytes of pregnant women with small-for-gestational age neonates have a different phenotypic and metabolic activity from those of women with preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 23:6, pages 476-487.
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Ana Sofia Cerdeira & S. Ananth Karumanchi. (2010) Angiogenic proteins as aid in the diagnosis and prediction of preeclampsia. Scandinavian Journal of Clinical and Laboratory Investigation 70:sup242, pages 73-78.
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