Fibrinolytic defects and recurrent miscarriage: A systematic review and meta-analysis

Obstetrics and Gynecology

Volumn 109, Issue 5, 2007, Pages 1146-1155

  Sotiriadis, Alexandros ^a   Makrigiannakis, Antonis ^a   Stefos, Theodor ^a   Paraskevaidis, Evangelos ^a   Kalantaridou, Sophia N ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 ANTIPLASMIN; ALPHA 2 MACROGLOBULIN; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 12; KALLIKREIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEASE NEXIN I; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE RECEPTOR;

BLOOD CLOTTING DISORDER; BLOOD CLOTTING FACTOR 12 DEFICIENCY; ENZYME RELEASE; FEMALE; FIBRINOLYSIS; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; GENOTYPE; HOMOZYGOSITY; HUMAN; PREVALENCE; PRIORITY JOURNAL; RECURRENT ABORTION; REVIEW; SPONTANEOUS ABORTION; SYSTEMATIC REVIEW;

ABORTION, HABITUAL; CASE-CONTROL STUDIES; CHILD; FACTOR XII; FACTOR XII DEFICIENCY; FACTOR XIII; FEMALE; FIBRINOLYSIS; GESTATIONAL AGE; HUMANS; ODDS RATIO; PLASMINOGEN ACTIVATOR INHIBITOR 1; POLYMORPHISM, GENETIC; PREGNANCY;

EID: 34247642244     PISSN: 00297844     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.AOG.0000260873.94196.d6     Document Type: Review

References (59)

1. Management of recurrent pregnancy loss. ACOG Practice Bulletin No. 24. American College of Obstetricians and Gynecologists. Int J Gynaecol Obstet 2002;78:179-90.
2. Quenby S, Farquharson RG, Dawood F, Hughes AM, Topping J. Recurrent miscarriage and long-term thrombosis risk: a case-control study. Hum Reprod 2005;20:1729-32.
3. Rey E, Kahn SR, David M, Shrier I. Thrombophilic disorders and fetal loss: a meta-analysis. Lancet 2003;361:901-8.
4. Gris JC, Schved JF, Neveu S, Mares P, Aguilar-Martinez P, Dupaigne D. Impaired fibrinolytic capacity and early recurrent spontaneous abortion. BMJ 1990;300:1500.
5. Lala PK, Chakraborty C. Factors regulating trophoblast migration and invasiveness: possible derangements contributing to pre-eclampsia and fetal injury. Placenta 2003;24:575-87.
6. Kluft C, Dooijewaard G, Emeis JJ. Role of the contact system in fibrinolysis. Semin Thromb Hemost 1987;13:50-68.
7. Miles LA, Greengard JS, Griffin JH. A comparison of the abilities of plasma kallikrein, beta-Factor XIIa, Factor XIa and urokinase to activate plasminogen. Thromb Res 1983;29:407-17.
8. Saksela O, Rifkin DB. Cell-associated plasminogen activation: regulation and physiological functions. Annu Rev Cell Biol 1988;4:93-126.
9. Anteby EY, Greenfield C, Natanson-Yaron S, Goldman-Wohl D, Hamani Y, Khudyak V, et al. Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 2004;10:229-35.
10. Bauer S, Pollheimer J, Hartmann J, Husslein P, Aplin JD, Knofler M. Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J Clin Endocrinol Metab 2004;89:812-22.
11. Graham CH. Effect of transforming growth factor-beta on the plasminogen activator system in cultured first trimester human cytotrophoblasts. Placenta 1997;18:137-43.
12. Xia Y, Wen HY, Kellems RE. Angiotensin II inhibits human trophoblast invasion through AT1 receptor activation. J Biol Chem 2002;277:24601-8.
13. Fitzpatrick TE, Graham CH. Stimulation of plasminogen activator inhibitor-1 expression in immortalized human trophoblast cells cultured under low levels of oxygen. Exp Cell Res 1998;245:155-62.
14. von dem Borne PA, Meijers JC, Bouma BN. Feedback activation of factor XI by thrombin in plasma results in additional formation of thrombin that protects fibrin clots from fibrinolysis. Blood 1995;86:3035-42.
15. Bereczky Z, Katona E, Muszbek L. Fibrin stabilization (factor XIII), fibrin structure and thrombosis. Pathophysiol Haemost Thromb 2003;33:430-7.
16. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000;283:2008-12.
17. Jennings I, Kitchen S, Woods TA, Preston FE, Greaves M. Potentially clinically important inaccuracies in testing for the lupus anticoagulant: an analysis of results from three surveys of the UK National External Quality Assessment Scheme (NEQAS) for Blood Coagulation. Thromb Haemost 1997;77:934-7.
18. Royal College of Obstetricians and Gynaecologists. The investigation and treatment of couples with recurrent miscarriage. Clinical Green Top Guideline No. 17. 2003. Available at: http://www.rcog.org.uk/resources/Public/pdf/ Recurrent_Miscarriage_No17.pdf. Retrieved February 20, 2007.
19. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557-60.
20. Lau J, Ioannidis JP, Schmid CH. Quantitative synthesis in systematic reviews. Ann Intern Med 1997;127:820-6.
21. Anwar R, Gallivan L, Edmonds SD, Markham AF. Genotype/phenotype correlations for coagulation factor XIII: specific normal polymorphisms are associated with high or low factor XIII specific activity. Blood 1999;93:897-905.
22. Gris JC, Ripart-Neveu S, Maugard C, Tailland ML, Brun S, Courtieu C, et al. Respective evaluation of the prevalence of haemostasis abnormalities in unexplained primary early recurrent miscarriages. The Nimes Obstetricians and Haematologists (NOHA) Study. Thromb Haemost 1997;77:1096-103.
23. Barbosa HC, Carvalho EC, Barini R, Siqueira LH, Costa DS, Annichino-Bizzacchi Tyr204Phe and Val34Leu polymorphisms in two Brazilian ethnic groups and in patients with recurrent miscarriages. Fertil Steril 2004;82:1455-7.
24. Pauer HU, Burfeind P, Kostering H, Emons G, Hinney B. Factor XII deficiency is strongly associated with primary recurrent abortions. Fertil Steril 2003;80:590-4.
25. Walch K, Riener EK, Tempfer CB, Endler G, Huber JC, Unfried G. The C46T polymorphism of the coagulation factor XII gene and idiopathic recurrent miscarriage. BJOG 2005;112:1434-6.
26. Wolf CE, Haubelt H, Pauer HU, Hinney B, Krome-Cesar C, Legler TJ, et al. Recurrent pregnancy loss and its relation to FV Leiden, FII G20210A and polymorphisms of plasminogen activator and plasminogen activator inhibitor. Pathophysiol Haemost Thromb 2003;33:134-7.
27. Buchholz T, Lohse P, Rogenhofer N, Kosian E, Pihusch R, Thaler CJ. Polymorphisms in the ACE and PAI-1 genes are associated with recurrent spontaneous miscarriages. Hum Reprod 2003;18:2473-7.
28. Dossenbach-Glaninger A, van TM, Dossenbach M, Oberkanins C, Moritz A, Krugluger W, et al. Plasminogen activator inhibitor 1 4G/5G polymorphism and coagulation factor XIII Val34Leu polymorphism: impaired fibrinolysis and early pregnancy loss. Clin Chem 2003;49:1081-6.
29. Coulam CB, Jeyendran RS, Fishel LA, Roussev R. Multiple thrombophilic gene mutations rather than specific gene mutations are risk factors for recurrent miscarriage. Am J Reprod Immunol 2006;55:360-8.
30. Glueck CJ, Wang P, Bornovali S, Goldenberg N, Sieve L. Polycystic ovary syndrome, the G1691A factor V Leiden mutation, and plasminogen activator inhibitor activity: associations with recurrent pregnancy loss. Metabolism 2003;52:1627-32.
31. Iinuma Y, Sugiura-Ogasawara M, Makino A, Ozaki Y, Suzumori N, Suzumori K. Coagulation factor XII activity, but not an associated common genetic polymorphism (46C/T), is linked to recurrent miscarriage. Fertil Steril 2002;77:353-6.
32. Braulke I, Pruggmayer M, Melloh P, Hinney B, Kostering H, Gunther E. Factor XII (Hageman) deficiency in women with habitual abortion: new subpopulation of recurrent aborters? Fertil Steril 1993;59:98-101.
33. Lopez Ramirez Y, Vivenes M, Miller A, Pulido A, Lopez Mora J, Arocha-Pinango CL, et al. Prevalence of the coagulation factor XIII polymorphism Val34Leu in women with recurrent miscarriage. Clin Chim Acta 2006;374:69-74.
34. Schubring C, Grulich-Henn J, Burkhard P, Kloss HR, Selmayr E, Muller-Berghaus G. Fibrinolysis and factor XIII in women with spontaneous abortion. Eur J Obstet Gynecol Reprod Biol 1990;35:215-21.
35. Ogasawara MS, Aoki K, Katano K, Ozaki Y, Suzumori K. Factor XII but not protein C, protein S, antithrombin III, or factor XIII is a predictor of recurrent miscarriage. Fertil Steril 2001;75:916-9.
36. Ogasawara MS, Iinuma Y, Aoki K, Katano K, Ozaki Y, Suzumori K. Low-dose aspirin is effective for treatment of recurrent miscarriage in patients with decreased coagulation factor XII. Fertil Steril 2001;76:203-4.
37. Robertson L, Wu O, Langhorne P, Twaddle S, Clark P, Lowe GD, et al. Thrombophilia in pregnancy: a systematic review. Br J Haematol 2006;132:171-96.
38. Girolami A, Randi ML, Gavasso S, Lombardi AM, Spiezia F. The occasional venous thromboses seen in patients with severe (homozygous) FXII deficiency are probably due to associated risk factors: a study of prevalence in 21 patients and review of the literature. J Thromb Thrombolysis 2004;17:139-43.
39. Girolami A, Morello M, Girolami B, Lombardi AM, Bertolo C. Myocardial infarction and arterial thrombosis in severe (homozygous) FXII deficiency: no apparent causative relation. Clin Appl Thromb Hemost 2005;11:49-53.
40. Girolami A, Zocca N, Girolami B, Lombardi AM, Fabris F. Pregnancies and oral contraceptive therapy in severe (homozygons) FXII deficiency: a study in 12 patients and review of the literature. J Thromb Thrombolysis 2004;18:209-12.
41. Zito F, Lowe GD, Rumley A, McMahon AD, Humphries SE; WOSCOPS Study Group West of Scotland Coronary Prevention Study. Association of the factor XII 46C>T polymorphism with risk of coronary heart disease (CHD) in the WOSCOPS study. Atherosclerosis 2002;165:153-8.
42. Endler G, Exner M, Mannhalter C, Meier S, Ruzicka K, Handler S, et al. A common C->T polymorphism at nt 46 in the promoter region of coagulation factor XII is associated with decreased factor XII activity. Thromb Res 2001;101:255-60.
43. Kohler HP, Futers TS, Grant PJ. FXII (46C->T) polymorphism and in vivo generation of FXII activity-gene frequencies and relationship in patients with coronary artery disease. Thromb Haemost 1999;81:745-7.
44. Endler G, Mannhalter C, Sunder-Plassmann H, Lalouschek W, Kapiotis S, Exner M, et al. Homozygosity for the C->T polymorphism at nucleotide 46 in the 5= untranslated region of the factor XII gene protects from development of acute coronary syndrome. Br J Haematol 2001;115:1007-9.
45. Roldan V, Corral J, Marin F, Pineda J, Vicente V, Gonzalez-Conejero R. Synergistic association between hypercholesterolemia and the C46T factor XII polymorphism for developing premature myocardial infarction. Thromb Haemost 2005;94:1294-9.
46. Feinberg RF, Kao LC, Haimowitz JE, Queenan JT Jr, Wun TC, Strauss JF, et al. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts. Lab Invest 1989;61:20-6.
47. Burzotta F, Di Castelnuovo A, Amore C, D'Orazio A, Di Bitondo R, Donati MB, et al. 4G/5G promoter PAI-1 gene polymorphism is associated with plasmatic PAI-1 activity in Italians: a model of gene-environment interaction. Thromb Haemost 1998;79:354-8.
48. Kolben M, Lopens A, Blaser J, Ulm K, Schmitt M, Schneider KT, et al. Proteases and their inhibitors are indicative in gestational disease. Eur J Obstet Gynecol Reprod Biol 1996;68:59-65.
49. Yamada N, Arinami T, Yamakawa-Kobayashi K, Watanabe H, Sohda S, Hamada H, et al. The 4G/5G polymorphism of the plasminogen activator inhibitor-1 gene is associated with severe preeclampsia. J Hum Genet 2000;45:138-41.
50. Glueck CJ, Phillips H, Cameron D, Wang P, Fontaine RN, Moore SK, et al. The 4G/4G polymorphism of the hypofibrinolytic plasminogen activator inhibitor type 1 gene: an independent risk factor for serious pregnancy complications. Metabolism 2000;49:845-52.
51. Glueck CJ, Kupferminc MJ, Fontaine RN, Wang P, Weksler BB, Eldor A. Genetic hypofibrinolysis in complicated pregnancies. Obstet Gynecol 2001;97:44-8.
52. Belo L, Santos-Silva A, Rumley A, Lowe G, Pereira-Leite L, Quintanilha A, et al. Elevated tissue plasminogen activator as a potential marker of endothelial dysfunction in pre-eclampsia: correlation with proteinuria. BJOG 2002;109:1250-5.
53. Glueck CJ, Pranikoff J, Aregawi D, Haque M, Zhu B, Tracy T, et al. The factor V Leiden mutation, high factor VIII, and high plasminogen activator inhibitor activity: etiologies for sporadic miscarriage. Metabolism 2005;54:1345-9.
54. Glueck CJ, Fontaine RN, Gruppo R, Stroop D, Sieve-Smith L, Tracy T, et al. The plasminogen activator inhibitor-1 gene, hypofibrinolysis, and osteonecrosis. Clin Orthop Relat Res 1999:133-46.
55. Balogh I, Szoke G, Karpati L, Wartiovaara U, Katona E, Komaromi I, et al. Val34Leu polymorphism of plasma factor XIII: biochemistry and epidemiology in familial thrombophilia. Blood 2000;96:2479-86.
56. Aflalo ED, Sod-Moriah UA, Potashnik G, Har-Vardi I. Expression of plasminogen activators in preimplantation rat embryos developed in vivo and in vitro. Reprod Biol Endocrinol 2005;3:7.
57. Meijers JC, Tekelenburg WL, Bouma BN, Bertina RM, Rosendaal FR. High levels of coagulation factor XI as a risk factor for venous thrombosis. N Engl J Med 2000;342:696-701.
58. Bouma BN, Meijers JC. Role of blood coagulation factor XI in downregulation of fibrinolysis. Curr Opin Hematol 2000;7:266-72.
59. Daya S. Characteristics of good causation studies. Semin Reprod Med 2003;21:73-83.