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The Journal of Maternal-Fetal & Neonatal Medicine Volume 22, 2009 - Issue 8
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Original Article

Evidence of maternal platelet activation, excessive thrombin generation, and high amniotic fluid tissue factor immunoreactivity and functional activity in patients with fetal death

Offer Erez Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USACorrespondence[email protected]
, MD,
Francesca Gotsch Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA
,
Shali Mazaki-Tovi Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Edi Vaisbuch Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Juan Pedro Kusanovic Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Chong Jai Kim Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of Pathology, Wayne State University, Detroit, Michigan, USA
,
Tinnakorn Chaiworapongsa Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Deborah Hoppensteadt Department of Pathology, Loyola University Health System, Maywood, Illinois, USA
,
Jawed Fareed Department of Pathology, Loyola University Health System, Maywood, Illinois, USA
,
Nandor G. Than Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA
,
Chia-Ling Nhan-Chang Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Lami Yeo Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Percy Pacora Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA
,
Moshe Mazor Department of OB/GYN, Soroka Medical Center, Beer Sheva University of the Negev, Beer-Sheva, Israel
,
Sonia S. Hassan Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
,
Pooja Mittal Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA
&
Roberto Romero Perinatology Research Branch, NICHD, NIH, DHHS, Bethesda, Maryland, USA; Department of OB/GYN, Wayne State University, Detroit, Michigan, USA; Center for Molecular Medicine and Genetics, Wayne State University, Detroit, Michigan, USACorrespondence[email protected]
, MD show all
Pages 672-687 | Received 10 Oct 2008, Accepted 09 Feb 2009, Published online: 19 Aug 2009

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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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Offer Erez, Maha Othman, Anat Rabinovich, Elad Leron, Francesca Gotsch & Jecko Thachil. (2022) DIC in Pregnancy – Pathophysiology, Clinical Characteristics, Diagnostic Scores, and Treatments. Journal of Blood Medicine 13, pages 21-44.
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Rachel Gomez-Tolub, Anat Rabinovich, Eric Kachko, Neta Benshalom-Tirosh, Dan Tirosh, Jecko Thachil, Limor Besser, Nandor Gabor Than & Offer Erez. (2022) Placental abruption as a trigger of DIC in women with HELLP syndrome: a population-based study. The Journal of Maternal-Fetal & Neonatal Medicine 35:17, pages 3259-3269.
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Ali Alhousseini, Roberto Romero, Neta Benshalom-Tirosh, Dereje Gudicha, Percy Pacora, Dan Tirosh, Doron Kabiri, Lami Yeo, Jecko Thachil, Chaur-Dong Hsu, Sonia S. Hassan & Offer Erez. (2022) Nonovert disseminated intravascular coagulation (DIC) in pregnancy: a new scoring system for the identification of patients at risk for obstetrical hemorrhage requiring blood product transfusion. The Journal of Maternal-Fetal & Neonatal Medicine 35:2, pages 242-257.
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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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Offer Erez, Roberto Romero, Edi Vaisbuch, Juan Pedro Kusanovic, Shali Mazaki-Tovi, Tinnakorn Chaiworapongsa, Francesca Gotsch, Pooja Mittal, Samuel S. Edwin, Chia-Ling Nhan-Chang, Nandor Gabor Than, Chong Jai Kim, Sun Kwon Kim, Lami Yeo, Moshe Mazor & Sonia S. Hassan. (2018) The pattern and magnitude of “in vivo thrombin generation” differ in women with preeclampsia and in those with SGA fetuses without preeclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 31:13, pages 1671-1680.
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Offer Erez, Roberto Romero, Edi Vaisbuch, Nandor Gabor Than, Juan Pedro Kusanovic, Shali Mazaki-Tovi, Francesca Gotsch, Pooja Mittal, Zhong Dong, Tinnakorn Chaiworapongsa, Chong Jai Kim, Chia-Ling Nhan-Chang, Sun Kwon Kim, Lami Yeo, Moshe Mazor & Sonia S. Hassan. (2018) Tissue factor activity in women with preeclampsia or SGA: a potential explanation for the excessive thrombin generation in these syndromes. The Journal of Maternal-Fetal & Neonatal Medicine 31:12, pages 1568-1577.
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Yeon Mee Kim, Piya Chaemsaithong, Roberto Romero, Majid Shaman, Chong Jai Kim, Jung-Sun Kim, Faisal Qureshi, Suzanne M. Jacques, Ahmed I. Ahmed, Tinnakorn Chaiworapongsa, Sonia S. Hassan, Lami Yeo & Steven J. Korzeniewski. (2015) Placental lesions associated with acute atherosis. The Journal of Maternal-Fetal & Neonatal Medicine 28:13, pages 1554-1562.
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Luca Spiezia, Silvia Visentin, Claudia Radu, Maria Bon, Barry Woodhams, Erich Cosmi & Paolo Simioni. (2013) Association between increased FVIIa-antithrombin complex/FVIIa ratio and pre-eclampsia. The Journal of Maternal-Fetal & Neonatal Medicine 26:13, pages 1352-1354.
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Vanessa Topping, Roberto Romero, Nandor Gabor Than, Adi L. Tarca, Zhonghui Xu, Sun Young Kim, Bing Wang, Lami Yeo, Chong Jai Kim, Sonia S. Hassan & Jung-Sun Kim. (2013) Interleukin-33 in the human placenta. The Journal of Maternal-Fetal & Neonatal Medicine 26:4, pages 327-338.
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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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Amir A Kuperman, Ron Hoffman & Benjamin Brenner. (2010) Managing thrombophilia during pregnancy. Expert Review of Obstetrics & Gynecology 5:3, pages 371-381.
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Offer Erez, Roberto Romero, Edi Vaisbuch, Juan Pedro Kusanovic, Shali Mazaki-Tovi, Tinnakorn Chaiworapongsa, Francesca Gotsch, Jawed Fareed, Debra Hoppensteadt, Nandor Gabor Than, Bo Hyun Yoon, Sam Edwin, Zhong Dong, Jimmy Espinoza, Moshe Mazor & Sonia S. Hassan. (2010) High tissue factor activity and low tissue factor pathway inhibitor concentrations in patients with preterm labor. The Journal of Maternal-Fetal & Neonatal Medicine 23:1, pages 23-33.
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Articles from other publishers (33)

Offer Erez, Francesca Gotsch, Eunjung Jung, Tinnakorn Chaiworapongsa, Dereje W. Gudicha, Manaphat Suksai, Dahiana M. Gallo, Piya Chaemsaithong, Mariachiara Bosco, Malek Al Qasem, Arun Meyyazhagan, Nandor Gabor Than & Roberto Romero. (2023) Perturbations in kinetics of the thrombin generation assay identify women at risk of preeclampsia in the first trimester and provide the rationale for a preventive approach. American Journal of Obstetrics and Gynecology 228:5, pages 580.e1-580.e17.
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Elise Schapkaitz, Elena Libhaber, Barry F. Jacobson, Marketa Toman, Annika Gerber & Harry R. Büller. (2022) Evaluation of markers of fibrinolysis and coagulation in pregnant women with human immunodeficiency virus. Thrombosis Research 217, pages 1-8.
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Toshiaki IBA, Theodore E. WARKENTIN, Jean M. CONNORS & Jerrold H. LEVY. (2022) Therapeutic strategies in patients with coagulopathy and disseminated intravascular coagulation: awareness of the phase-dependent characteristics. Minerva Medica 112:6.
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Ryan Wang, Chloe Getrajdman, Daniel Blech, Sarp Aksel, Samuel Bender & Daniel Katz. (2021) Atypical Hemolytic-Uremic Syndrome Following Obstetric Hemorrhage in the Setting of Fetal Demise and Placenta Accreta: A Case Report. A&A Practice 15:5, pages e01476.
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Lauren H. Theilen, Heather D. Campbell, Sunni L. Mumford, Alexandra C. Purdue-Smithe, Lindsey A. Sjaarda, Neil J. Perkins, Jeannie G. Radoc, Robert M. Silver & Enrique F. Schisterman. (2020) Platelet activation and placenta-mediated adverse pregnancy outcomes: an ancillary study to the Effects of Aspirin in Gestation and Reproduction trial. American Journal of Obstetrics and Gynecology 223:5, pages 741.e1-741.e12.
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Salvatore Andrea Mastrolia & Irene Cetin. 2020. Female Reproductive Dysfunction. Female Reproductive Dysfunction 411 430 .
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Maha Othman, Amparo Santamaría Ortiz, María Cerdá, Offer Erez, Adrian Minford, Deborah Obeng‐Tuudah, Marc Blondon, Ingrid Bistervels, Saskia Middeldorp & Rezan Abdul‐Kadir. (2019) Thrombosis and hemostasis health in pregnancy: Registries from the International Society on Thrombosis and Haemostasis. Research and Practice in Thrombosis and Haemostasis 3:4, pages 607-614.
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Anat Rabinovich, Rezan Abdul‐Kadir, Jecko Thachil, Toshiaki Iba, Maha Othman & Offer Erez. (2019) DIC in obstetrics: Diagnostic score, highlights in management, and international registry‐communication from the DIC and Women's Health SSCs of the International Society of Thrombosis and Haemostasis. Journal of Thrombosis and Haemostasis 17:9, pages 1562-1566.
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Dana A. Muin, Helmuth Haslacher, Vanessa Koller, Herbert Kiss, Anke Scharrer & Alex Farr. (2018) Impact of fetal maceration grade on risk of maternal disseminated intravascular coagulation after intrauterine fetal death – A retrospective cohort study. Scientific Reports 8:1.
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Tinnakorn Chaiworapongsa, Roberto Romero, Offer Erez, Adi L. Tarca, Agustin Conde-Agudelo, Piya Chaemsaithong, Chong Jai Kim, Yeon Mee Kim, Jung-Sun Kim, Bo Hyun Yoon, Sonia S. Hassan, Lami Yeo & Steven J. Korzeniewski. (2017) The prediction of fetal death with a simple maternal blood test at 24-28 weeks: a role for angiogenic index-1 (PlGF/sVEGFR-1 ratio). American Journal of Obstetrics and Gynecology 217:6, pages 682.e1-682.e13.
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Jean F. Regal, Richard M. Burwick & Sherry D. Fleming. (2017) The Complement System and Preeclampsia. Current Hypertension Reports 19:11.
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Warren Stevens, Tiffany Shih, Devin Incerti, Thanh G.N. Ton, Henry C. Lee, Desi Peneva, George A. Macones, Baha M. Sibai & Anupam B. Jena. (2017) Short-term costs of preeclampsia to the United States health care system. American Journal of Obstetrics and Gynecology 217:3, pages 237-248.e16.
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Offer Erez. (2017) Disseminated intravascular coagulation in pregnancy – Clinical phenotypes and diagnostic scores. Thrombosis Research 151, pages S56-S60.
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Salvatore Andrea Mastrolia, Moshe Mazor, Gershon Holcberg, Elad Leron, Ofer Beharier, Giuseppe Loverro & Offer Erez. (2017) The physiologic anticoagulant and anti-inflammatory role of heparins and their utility in the prevention of pregnancy complications. Thrombosis and Haemostasis 113:06, pages 1236-1246.
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Offer Erez, Salvatore Andrea Mastrolia & Jecko Thachil. (2015) Disseminated intravascular coagulation in pregnancy: insights in pathophysiology, diagnosis and management. American Journal of Obstetrics and Gynecology 213:4, pages 452-463.
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Mahmood H. Khichi, Wanda P. Parsons & Linda A. Winters-Miner. 2015. Practical Predictive Analytics and Decisioning Systems for Medicine. Practical Predictive Analytics and Decisioning Systems for Medicine 558 602 .
Salvatore Andrea Mastrolia, Moshe Mazor, Giuseppe Loverro, Vered Klaitman & Offer Erez. (2014) Placental vascular pathology and increased thrombin generation as mechanisms of disease in obstetrical syndromes. PeerJ 2, pages e653.
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Gabor Szalai, Yi Xu, Roberto Romero, Tinnakorn Chaiworapongsa, Zhonghui Xu, Po Jen Chiang, Hyunyoung Ahn, Birgitta Sundell, Olesya Plazyo, Yang Jiang, Mary Olive, Bing Wang, Suzanne M. Jacques, Faisal Qureshi, Adi L. Tarca, Offer Erez, Zhong Dong, Zoltan Papp, Sonia S. Hassan, Edgar Hernandez-Andrade & Nandor Gabor Than. (2014) In Vivo Experiments Reveal the Good, the Bad and the Ugly Faces of sFlt-1 in Pregnancy. PLoS ONE 9:11, pages e110867.
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Offer Erez, Lena Novack, Ruthy Beer-Weisel, Doron Dukler, Fernanda Press, Alexander Zlotnik, Nandor Gabor Than, Aaron Tomer & Moshe Mazor. (2014) DIC Score in Pregnant Women – A Population Based Modification of the International Society on Thrombosis and Hemostasis Score. PLoS ONE 9:4, pages e93240.
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Nazli Hossain & Michael J. Paidas. (2013) Disseminated intravascular coagulation. Seminars in Perinatology 37:4, pages 257-266.
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Jianzhong An, Magarya S. Waitara, Michelle Bordas, Vidhyalakshmi Arumugam, Raymond G. HoffmannBrian G. PetrichUma Sinha, Paula E. North & Rashmi Sood. (2013) Heparin rescues factor V Leiden–associated placental failure independent of anticoagulation in a murine high-risk pregnancy model. Blood 121:11, pages 2127-2134.
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Jennifer Kerns & Jody Steinauer. (2013) Management of postabortion hemorrhage. Contraception 87:3, pages 331-342.
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Elizabeth Vargis, Naoko Brown, Kent Williams, Ayman Al-Hendy, Bibhash C. Paria, Jeff Reese & Anita Mahadevan-Jansen. (2012) Detecting Biochemical Changes in the Rodent Cervix During Pregnancy Using Raman Spectroscopy. Annals of Biomedical Engineering 40:8, pages 1814-1824.
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Donald J. Dudley. 2011. Stillbirth: Prediction, Prevention and Management. Stillbirth: Prediction, Prevention and Management 229 241 .
Galit Sarig, Adi J. Klil-Drori, Dafna Chap-Marshak, Benjamin Brenner & Arieh Drugan. (2011) Activation of coagulation in amniotic fluid during normal human pregnancy. Thrombosis Research.
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G. GIRARDI. (2011) Role of tissue factor in feto‐maternal development: a xiphos. Journal of Thrombosis and Haemostasis 9:2, pages 250-256.
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Giovanna Ogge, Tinnakorn Chaiworapongsa, Roberto Romero, Youssef Hussein, Juan Pedro Kusanovic, Lami Yeo, Chong Jai Kim & Sonia S. Hassan. (2011) Placental lesions associated with maternal underperfusion are more frequent in early-onset than in late-onset preeclampsia. Journal of Perinatal Medicine 39:6.
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