The pattern and magnitude of “in vivo thrombin generation” differ in women with preeclampsia and in those with SGA fetuses without preeclampsia

References

• Beller FK, Ebert C. The coagulation and fibrinolytic enzyme system in pregnancy and in the puerperium. Eur J Obstet Gynecol Reprod Biol. 1982;13:177–197.
   PubMed Web of Science ®Google Scholar
• Stirling Y, Woolf L, North WR, et al. Haemostasis in normal pregnancy. Thromb Haemost. 1984;52:176–182.
   PubMed Web of Science ®Google Scholar
• Bellart J, Gilabert R, Angles A, et al. Tissue factor levels and high ratio of fibrinopeptide A:D-dimer as a measure of endothelial procoagulant disorder in pre-eclampsia. Br J Obstet Gynaecol. 1999;106:594–597.
   PubMedGoogle Scholar
• Chaiworapongsa T, Espinoza J, Yoshimatsu J, et al. Activation of coagulation system in preterm labor and preterm premature rupture of membranes. J Matern Fetal Neonatal Med. 2002;11:368–373.
   PubMedGoogle Scholar
• Rosenkranz A, Hiden M, Leschnik B, et al. Calibrated automated thrombin generation in normal uncomplicated pregnancy. Thromb Haemost. 2008;99:331–337.
   PubMed Web of Science ®Google Scholar
• Hellgren M, Blomback M. Studies on blood coagulation and fibrinolysis in pregnancy, during delivery and in the puerperium. I. Normal condition. Gynecol Obstet Invest. 1981;12:141–154.
   PubMed Web of Science ®Google Scholar
• Donohoe S, Quenby S, Mackie I, et al. Fluctuations in levels of antiphospholipid antibodies and increased coagulation activation markers in normal and heparin-treated antiphospholipid syndrome pregnancies. Lupus. 2002;11:11–20.
   PubMed Web of Science ®Google Scholar
• Bremme KA. Haemostatic changes in pregnancy. Best Pract Res Clin Haematol. 2003;16:153–168.
   PubMed Web of Science ®Google Scholar
• Brenner B. Haemostatic changes in pregnancy. Thromb Res. 2004;114:409–414.
   PubMed Web of Science ®Google Scholar
• Clark P, Brennand J, Conkie JA, et al. Activated protein C sensitivity, protein C, protein S and coagulation in normal pregnancy. Thromb Haemost. 1998;79:1166–1170.
   PubMed Web of Science ®Google Scholar
• Faught W, Garner P, Jones G, et al. Changes in protein C and protein S levels in normal pregnancy. Am J Obstet Gynecol. 1995;172:147–150.
   PubMed Web of Science ®Google Scholar
• Oruc S, Saruc M, Koyuncu FM, et al. Changes in the plasma activities of protein C and protein S during pregnancy. Aust N Z J Obstet Gynaecol. 2000;40:448–450.
   PubMed Web of Science ®Google Scholar
• Lefkowitz JB, Clarke SH, Barbour LA. Comparison of protein S functional and antigenic assays in normal pregnancy. Am J Obstet Gynecol. 1996;175:657–660.
   PubMed Web of Science ®Google Scholar
• Mahieu B, Jacobs N, Mahieu S, et al. Haemostatic changes and acquired activated protein C resistance in normal pregnancy. Blood Coagul Fibrinolysis: Int J Haemost Thromb. 2007;18:685–688.
   PubMed Web of Science ®Google Scholar
• Mimuro S, Lahoud R, Beutler L, et al. Changes of resistance to activated protein C in the course of pregnancy and prevalence of factor V mutation. Aust N Z J Obstet Gynaecol. 1998;38:200–204.
   PubMed Web of Science ®Google Scholar
• Cumming AM, Tait RC, Fildes S, et al. Development of resistance to activated protein C during pregnancy. Br J Haematol. 1995;90:725–727.
   PubMed Web of Science ®Google Scholar
• Biezenski JJ, Moore HC. Fibrinolysis in normal pregnancy. J Clin Pathol. 1958;11:306–310.
   PubMed Web of Science ®Google Scholar
• Naidoo SS, Hathorn M, Gillman T. Fibrinolytic and antifibrinolytic activity in pregnancy. J Clin Pathol. 1960;13:224–225.
   PubMed Web of Science ®Google Scholar
• Thorsen S. The inhibition of tissue plasminogen activator and urokinase-induced fibrinolysis by some natural proteinase inhibitors and by plasma and serum from normal and pregnant subjects. Scand J Clin Lab Invest. 1973;31:51–59.
   Google Scholar
• Kleiner GJ, Greston WM. Current concepts of defibrination in the pregnant woman. J Reprod Med. 1976;17:309–317.
   PubMed Web of Science ®Google Scholar
• Arias F, Andrinopoulos G, Zamora J. Whole-blood fibrinolytic activity in normal and hypertensive pregnancies and its relation to the placental concentration of urokinase inhibitor. Am J Obstet Gynecol. 1979;133:624–629.
   PubMed Web of Science ®Google Scholar
• Kruithof EK, Tran-Thang C, Gudinchet A, et al. Fibrinolysis in pregnancy: a study of plasminogen activator inhibitors. Blood. 1987;69:460–466.
   PubMed Web of Science ®Google Scholar
• Ishii A, Yamada S, Yamada R, et al. t-PA activity in peripheral blood obtained from pregnant women. J Perinat Med. 1994;22:113–117.
   PubMed Web of Science ®Google Scholar
• Wright JG, Cooper P, Astedt B, et al. Fibrinolysis during normal human pregnancy: complex inter-relationships between plasma levels of tissue plasminogen activator and inhibitors and the euglobulin clot lysis time. Br J Haematol. 1988;69:253–258.
   PubMed Web of Science ®Google Scholar
• Brosens I, Renaer M. On the pathogenesis of placental infarcts in pre-eclampsia. J Obstet Gynaecol Br Commonw. 1972;79:794–799.
   PubMedGoogle Scholar
• Robertson WB, Brosens I, Dixon G. Uteroplacental vascular pathology. Eur J Obstet Gynecol Reprod Biol. 1975;5:47–65.
   PubMedGoogle Scholar
• Pijnenborg R, Anthony J, Davey DA, et al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol. 1991;98:648–655.
   PubMedGoogle Scholar
• Gersell DJ. Selected vascular lesions of the placenta. Clin Lab Med. 1995;15:611–629.
   PubMed Web of Science ®Google Scholar
• Sikkema JM, Franx A, Bruinse HW, et al. Placental pathology in early onset pre-eclampsia and intra-uterine growth restriction in women with and without thrombophilia. Placenta. 2002;23:337–342.
   PubMed Web of Science ®Google Scholar
• Rolschau J. Infarctions and intervillous thrombosis in placenta, and their association with intrauterine growth retardation. Acta Obstet Gynecol Scand Suppl. 1978;72:22–27.
   PubMedGoogle Scholar
• Arias F, Romero R, Joist H, et al. Thrombophilia: a mechanism of disease in women with adverse pregnancy outcome and thrombotic lesions in the placenta. J Matern Fetal Med. 1998;7:277–286.
   PubMedGoogle Scholar
• Mitra SC, Seshan SV, Riachi LE. Placental vessel morphometry in growth retardation and increased resistance of the umbilical artery Doppler flow. J Matern Fetal Med. 2000;9:282–286.
   PubMedGoogle Scholar
• Sugimura M, Ohashi R, Kobayashi T, et al. Intraplacental coagulation in intrauterine growth restriction: cause or result? Semin Thromb Hemost. 2001;27:107–113.
   PubMed Web of Science ®Google Scholar
• Ornoy A, Crone K, Altshuler G. Pathological features of the placenta in fetal death. Arch Pathol Lab Med. 1976;100:367–371.
   PubMed Web of Science ®Google Scholar
• Preston FE, Rosendaal FR, Walker ID, et al. Increased fetal loss in women with heritable thrombophilia. Lancet. 1996;348:913–916.
   PubMed Web of Science ®Google Scholar
• Kim YM, Bujold E, Chaiworapongsa T, et al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol. 2003;189:1063–1069.
   PubMed Web of Science ®Google Scholar
• Elovitz MA, Baron J, Phillippe M. The role of thrombin in preterm parturition. Am J Obstet Gynecol. 2001;185:1059–1063.
   PubMed Web of Science ®Google Scholar
• Arias F, Rodriquez L, Rayne SC, et al. Maternal placental vasculopathy and infection: two distinct subgroups among patients with preterm labor and preterm ruptured membranes. Am J Obstet Gynecol. 1993;168:585–591.
   PubMed Web of Science ®Google Scholar
• Moldenhauer JS, Stanek J, Warshak C, et al. The frequency and severity of placental findings in women with preeclampsia are gestational age dependent. Am J Obstet Gynecol. 2003;189:1173–1177.
   PubMed Web of Science ®Google Scholar
• Chaiworapongsa T, Yoshimatsu J, Espinoza J, et al. Evidence of in vivo generation of thrombin in patients with small-for-gestational-age fetuses and pre-eclampsia. J Matern Fetal Neonatal Med. 2002;11:362–367.
   PubMedGoogle Scholar
• Hemker HC, Giesen P, AlDieri R, et al. The calibrated automated thrombogram (CAT): a universal routine test for hyper- and hypocoagulability. Pathophysiol Haemost Thromb. 2002;32:249–253.
   PubMed Web of Science ®Google Scholar
• Kovac MK, Lalic-Cosic SZ, Dmitrovic JM, et al. Thrombin generation, D-dimer and protein S in uncomplicated pregnancy. Clin Chem Lab Med. 2015;53:1975–1979.
   PubMed Web of Science ®Google Scholar
• Rice NT, Szlam F, Varner JD, et al. Differential contributions of intrinsic and extrinsic pathways to thrombin generation in adult, maternal and cord plasma samples. PLoS One. 2016;11:e0154127.
   PubMed Web of Science ®Google Scholar
• Bulletins–Obstetrics ACoP. ACOG practice bulletin. Diagnosis and management of preeclampsia and eclampsia. Obstet Gynecol. 2002;99:159–167.
   PubMed Web of Science ®Google Scholar
• Alexander GR, Himes JH, Kaufman RB, et al. A United States national reference for fetal growth. Obstet Gynecol. 1996;87:163–168.
   PubMed Web of Science ®Google Scholar
• Redline RW, Heller D, Keating S, et al. Placental diagnostic criteria and clinical correlation–a workshop report. Placenta. 2005;26 Suppl A:S114–S117.
   PubMed Web of Science ®Google Scholar
• Levi M. Disseminated intravascular coagulation. Crit Care Med. 2007;35:2191–2195.
   PubMed Web of Science ®Google Scholar
• McLean KC, Bernstein IM, Brummel-Ziedins KE. Tissue factor-dependent thrombin generation across pregnancy. Am J Obstet Gynecol. 2012;207:135 e131–136.
   Web of Science ®Google Scholar
• Lawson JH, Kalafatis M, Stram S, et al. A model for the tissue factor pathway to thrombin. I. An empirical study. J Biol Chem. 1994;269:23357–23366.
   PubMed Web of Science ®Google Scholar
• Butenas S, van 't Veer C, Mann KG. Evaluation of the initiation phase of blood coagulation using ultrasensitive assays for serine proteases. J Biol Chem. 1997;272:21527–21533.
   PubMed Web of Science ®Google Scholar
• Brummel KE, Paradis SG, Butenas S, et al. Thrombin functions during tissue factor-induced blood coagulation. Blood. 2002;100:148–152.
   PubMed Web of Science ®Google Scholar
• Butenas S, Mann KG. Blood coagulation. Biochemistry Mosc. 2002;67:3–12.
   PubMed Web of Science ®Google Scholar
• Butenas S, Bouchard BA, Brummel-Ziedins KE, et al. Tissue factor activity in whole blood. Blood. 2005;105:2764–2770.
   PubMed Web of Science ®Google Scholar
• Butenas S, Orfeo T, Brummel-Ziedins KE, et al. Tissue factor in thrombosis and hemorrhage. Surgery. 2007;142:S2–S14.
   PubMed Web of Science ®Google Scholar
• Hockin MF, Jones KC, Everse SJ, et al. A model for the stoichiometric regulation of blood coagulation. J Biol Chem. 2002;277:18322–18333.
   PubMed Web of Science ®Google Scholar
• Bellart J, Gilabert R, Miralles RM, et al. Endothelial cell markers and fibrinopeptide A to D-dimer ratio as a measure of coagulation and fibrinolysis balance in normal pregnancy. Gynecol Obstet Invest. 1998;46:17–21.
   PubMed Web of Science ®Google Scholar
• Walker MC, Garner PR, Keely EJ, et al. Changes in activated protein C resistance during normal pregnancy. Am J Obstet Gynecol. 1997;177:162–169.
   PubMed Web of Science ®Google Scholar
• Yuen PM, Yin JA, Lao TT. Fibrinopeptide A levels in maternal and newborn plasma. Eur J Obstet Gynecol Reprod Biol. 1989;30:239–244.
   PubMed Web of Science ®Google Scholar
• de Boer K, ten Cate JW, Sturk A, et al. Enhanced thrombin generation in normal and hypertensive pregnancy. Am J Obstet Gynecol. 1989;160:95–100.
   PubMed Web of Science ®Google Scholar
• Sorensen JD, Secher NJ, Jespersen J. Perturbed (procoagulant) endothelium and deviations within the fibrinolytic system during the third trimester of normal pregnancy. A possible link to placental function. Acta Obstet Gynecol Scand. 1995;74:257–261.
   PubMed Web of Science ®Google Scholar
• Kuczynski J, Uszynski W, Zekanowska E, et al. Tissue factor (TF) and tissue factor pathway inhibitor (TFPI) in the placenta and myometrium. Eur J Obstet Gynecol Reprod Biol. 2002;105:15–19.
   PubMed Web of Science ®Google Scholar
• Lockwood CJ, Krikun G, Schatz F. The decidua regulates hemostasis in human endometrium. Semin Reprod Endocrinol. 1999;17:45–51.
   PubMedGoogle Scholar
• Erlich J, Parry GC, Fearns C, et al. Tissue factor is required for uterine hemostasis and maintenance of the placental labyrinth during gestation. Proc Natl Acad Sci USA. 1999;96:8138–8143.
   PubMed Web of Science ®Google Scholar
• Lockwood CJ, Krikun G, Schatz F. Decidual cell-expressed tissue factor maintains hemostasis in human endometrium. Ann N Y Acad Sci. 2001;943:77–88.
   PubMed Web of Science ®Google Scholar
• Omsjo IH, Oian P, Maltau JM, et al. Thromboplastin activity in amniotic fluid. Gynecol Obstet Invest. 1985;19:1–5.
   PubMed Web of Science ®Google Scholar
• Creter D. Amnioplastin: new reagent for coagulation tests. Lancet. 1977;2:251.
   PubMed Web of Science ®Google Scholar
• Lockwood CJ, Bach R, Guha A, et al. Amniotic fluid contains tissue factor, a potent initiator of coagulation. Am J Obstet Gynecol. 1991;165:1335–1341.
   PubMed Web of Science ®Google Scholar
• Reinthaller A, Mursch-Edlmayr G, Tatra G. Thrombin–antithrombin III complex levels in normal pregnancy with hypertensive disorders and after delivery. Br J Obstet Gynaecol. 1990;97:506–510.
   PubMedGoogle Scholar
• Uszynski M. Generation of thrombin in blood plasma of non-pregnant and pregnant women studied through concentration of thrombin–antithrombin III complexes. Eur J Obstet Gynecol Reprod Biol. 1997;75:127–131.
   PubMed Web of Science ®Google Scholar
• Reber G, Amiral J, de Moerloose P. Modified antithrombin III levels during normal pregnancy and relationship with prothrombin fragment F1 + 2 and thrombin-antithrombin complexes. Thromb Res. 1998;91:45–47.
   PubMed Web of Science ®Google Scholar
• Andersson T, Lorentzen B, Hogdahl H, et al. Thrombin-inhibitor complexes in the blood during and after delivery. Thromb Res. 1996;82:109–117.
   PubMed Web of Science ®Google Scholar
• Erez O, Gotsch F, Mazaki-Tovi S, et al. Evidence of maternal platelet activation, excessive thrombin generation, and high amniotic fluid tissue factor immunoreactivity and functional activity in patients with fetal death. J Maternal–Fetal Neonatal Med. 2009;22:672–687.
   PubMed Web of Science ®Google Scholar
• Elovitz MA, Saunders T, Ascher-Landsberg J, et al. Effects of thrombin on myometrial contractions in vitro and in vivo. Am J Obstet Gynecol. 2000;183:799–804.
   PubMed Web of Science ®Google Scholar
• Erez O, Romero R, Hoppensteadt D, et al. Tissue factor and its natural inhibitor in pre-eclampsia and SGA. J Maternal–Fetal Neonatal Med. 2008;21:855–869.
   PubMed Web of Science ®Google Scholar
• Williams VK, Griffiths AB, Carbone S, et al. Fibrinogen concentration and factor VIII activity in women with preeclampsia. Hypertens Pregnancy. 2007;26:415–421.
   PubMed Web of Science ®Google Scholar
• Hayashi M, Inoue T, Hoshimoto K, et al. Characterization of five marker levels of the hemostatic system and endothelial status in normotensive pregnancy and pre-eclampsia. Eur J Haematol. 2002;69:297–302.
   PubMed Web of Science ®Google Scholar
• Abdel Gader AM, Al-Mishari AA, Awadalla SA, et al. Total and free tissue factor pathway inhibitor in pregnancy hypertension. Int J Gynaecol Obstet. 2006;95:248–253.
   PubMed Web of Science ®Google Scholar
• Erez O, Hoppensteadt D, Romero R, et al. Preeclampsia is associated with low concentrations of protein Z. J Maternal–Fetal Neonatal Med. 2007;20:661–667.
   PubMed Web of Science ®Google Scholar
• Erez O, Espinoza J, Chaiworapongsa T, et al. A link between a hemostatic disorder and preterm PROM: a role for tissue factor and tissue factor pathway inhibitor. J Maternal–Fetal Neonatal Med. 2008;21:732–744.
   PubMed Web of Science ®Google Scholar
• Erez O, Romero R, Vaisbuch E, et al. High tissue factor activity and low tissue factor pathway inhibitor concentrations in patients with preterm labor. J Maternal–Fetal Neonatal Med. 2010;23:23–33.
   PubMed Web of Science ®Google Scholar
• Kusanovic JP, Espinoza J, Romero R, et al. Plasma protein Z concentrations in pregnant women with idiopathic intrauterine bleeding and in women with spontaneous preterm labor. J Matern Fetal Neonatal Med. 2007;20:453–463.
   PubMed Web of Science ®Google Scholar
• Macey MG, Bevan S, Alam S, et al. Platelet activation and endogenous thrombin potential in pre-eclampsia. Thromb Res. 2010;125:e76–e81.
   PubMed Web of Science ®Google Scholar
• Gardiner C, Tannetta DS, Simms CA, et al. Syncytiotrophoblast microvesicles released from pre-eclampsia placentae exhibit increased tissue factor activity. PLoS One. 2011;6:e26313.
   PubMed Web of Science ®Google Scholar
• Rafik Hamad R, Curvers J, Berntorp E, et al. Increased thrombin generation in women with a history of preeclampsia. Thromb Res. 2009;123:580–586.
   PubMed Web of Science ®Google Scholar
• Mastrolia SA, Novack L, Thachil J, et al. LMWH in the prevention of preeclampsia and fetal growth restriction in women without thrombophilia. A systematic review and meta-analysis. Thromb Haemost. 2016;116: 868–878.
   PubMed Web of Science ®Google Scholar