Ischemic stroke and inherited thrombophilias

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Abstract

In this review the impact of the most common thrombophilias on the risk of ischemic stroke and atherothrombosis is thoroughly analyzed. The functional role of different β-fibrinogen genotypes was reviewed and their correlations with ischemic cerebrovascular diseases, brachiocephalic artery atherosclerosis and arterial hypertension are evaluated. In addition, associations of stroke with key genetic factors such as the Leyden mutation (factor V), mutations in the genes of prothrombin, PAI-1 (plasminogen activator inhibitor), glycoprotein IIIa, etc. are assessed. Results of the authors’ own works on the occurrence of various inherited thrombophilias in a group of 43 patients with ischemic stroke of undefined origin are presented.

About the authors

Natalia V. Pizova

Yaroslavl' State Medical University

Author for correspondence.
Email: pizova@yandex.ru
Россия, Yaroslavl'

References

  1. Jackson S.P. Arterial thrombosis-insidious, unpredictable and deadly. Nature Medicine. 2011; 17(11): 1423–1436. doi: 10.1038/nm.2515. PMID: 22064432.
  2. Roger V.L., Go A.S., Lloyd-Jones D.M. et al. Heart Disease and Stroke Statistics-2011 Update A Report From the American Heart Association. Circulation. 2011; 123(4): E18–E209. doi: 10.1161/CIR.0b013e3182009701. PMID: 21160056.
  3. ISTH Steering Committee for World Thrombosis Day. Thrombosis: a major contributor to the global disease burden. J Thromb Haemost. 2014; 12(10): 1580-1590. doi: 10.1160/TH14-08-0671. PMID: 25300294.
  4. Lozano R., Naghavi M., Foreman K. et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012; 380: 2095–2128. doi: 10.1016/S0140-6736(12)61728-0. PMID: 23245604
  5. Simons L.A., Simons J. A Comparison of Risk Factors for Coronary Heart Disease and Ischaemic Stroke. Heart Lung and Circulation. 2012; 21(3): 198–199. doi: 10.1016/j.hlc.2011.11.007. PMID: 22197633.
  6. Bokarev I.N., Bokarev M.I. [Thrombophilia, vein thrombosis and their treatments]. Klinicheskaia meditsina. 2002; 5: 4-8 (In Russ.).
  7. Domashenko M.A., Tanashyan M.M., Kistenev B.A. et al. [Coagulopathy and repeated ischemic disorders of cerebral circulation]. Atmosfera. Nervnyye bolezni. 2005; 3: 36-40 (In Russ.).
  8. Zorilova I.V., Illarioshkin S.N., Efimov V.S. et al. [Hereditary thrombophilia as a risk factor of ischemic stroke in young patients]. Insul’t: prilozheniye k Zhurnalu nevrologii i psikhiatrii im. S. S. Korsakova. 2006; 18: 17-25 (In Russ.).
  9. Kissela B.M., Khoury J.C., Alwell K. et al. Age at stroke: temporal trends in stroke incidence in a large, biracial population. Neurology. 2012; 79: 1781–1787. doi: 10.1212/WNL.0b013e318270401d. PMID: 23054237.
  10. Guercini F., Acciarresi M., Agnelli G et al. Cryptogenic stroke: time to determine aetiology. J Thromb Haemost. 2008; 6(4): 549–554. doi: 10.1111/j.1538-7836.2008.02903.x. PMID: 18208534.
  11. Sacco R.L., Ellenberg J.H., Mohr J.P. et al. Infarcts of undetermined cause: the NINCDS Stroke Data Bank. Ann Neurol. 1989; 25(4): 382–390. doi: 10.1002/ana.410250410. PMID: 2712533.
  12. Palomeras S.E., Fossas F.P., Cano O.A.T. et al. Cryptogenic infarct. A follow-up period of 1 year study. Neurologia. 2009; 24(5): 304–308. PMID: 19642032.
  13. Dobrynina L. A., Kalashnikova L. A., Patrusheva N. L. et al. [Polymorphic mutations in 5,10-methylenetetrahydrofolatereductase, prothrombin and clotting factor V in young patients with stroke]. Klinicheskaia meditsina. 2012; 3: 37-40 (In Russ).
  14. Hart R.G., Diener H.C., Connolly S.J. Embolic strokes of undetermined source: support for a new clinical construct—authors' reply. Lancet Neurol. 2014; 13(10): 967. doi: 10.1016/S1474-4422(14)70197-8. PMID: 25231516.
  15. Furie B., Furie B.C. Mechanisms of thrombus formation. New England Journal of Medicine. 2008; 359(9): 938–949. doi: 10.1056/NEJMra0801082. PMID: 18753650.
  16. Borissoff J.I., Spronk H.M.H., ten Cate H. Mechanisms of Disease the Hemostatic System As A Modulator of Atherosclerosis. New England Journal of Medicine. 2011; 364(18): 1746–1760. doi: 10.1093/cvr/cvp066. PMID: 19228706.
  17. Loeffen R., Spronk H.M., ten Cate H. The impact of blood coagulability on atherosclerosis and cardiovascular disease. J Thromb Haemost. 2012; 10(7): 1207–1216. doi: 10.1111/j.1538-7836.2012.04782.x. PMID: 22578148.
  18. Lippi G., Franchini M., Targher G. Arterial thrombus formation in cardiovascular disease. Nat Rev Cardiol. 2011; 8(9): 502–512. doi: 10.1038/nrcardio.2011.91. PMID: 21727917.
  19. Marlar R. Report on the diagnosis and treatment of homozygous protein C deficiency. Report of the Working Party on Homozygous Protein C Deficiency of the ICTH-Subcommittee on Protein C and Protein S. Thromb. Haemost. 1989; 61: 529–531. PMID: 2529664
  20. Boekholdt S.M., Kramer M.H. Arterial thrombosis and the role of thrombophilia. Semin Thromb Hemost. 2007; 33(6): 588–96. doi: 10.1055/s-2007-985755. PMID: 17768691.
  21. Siegerink B., Govers-Riemslag J.W.P., Rosendaal F.R. et al. Intrinsic Coagulation Activation and the Risk of Arterial Thrombosis in Young Women Results From the Risk of Arterial Thrombosis in Relation to Oral Contraceptives (RATIO) Case-Control Study. Circulation. 2010; 122(18): 1854–1861. doi: 10.1161/CIRCULATIONAHA.110.943738. PMID: 20956210.
  22. Govers-Riemslag J.W., Smid M., Cooper J.A. et al. The plasma kallikrein-kinin system and risk of cardiovascular disease in men. J Thromb Haemost. 2007; 5(9): 1896–1903. doi: 10.1111/j.1538-7836.2007.02687.x. PMID: 17723129.
  23. The British Committee of Standards in Haematology. Guidelines on the investigation and management of thrombophilia. J Clin Pathol. 1990; 43: 703—709. PMID: 2212062.
  24. Nachman R.L., Silverstein R. Hypercoagulable states. Ann Intern Med. 1993; 119: 819—827. PMID: 8379603.
  25. Jordan F.L.J., Nandorff A. The familial tendency in thromboembolic disease. Acta Med Scand. 1956; 156: 267-75. PMID: 13394174.
  26. Momot A. P. [The problem of thrombophilia in clinical practice]. Rossiyskiy zhurnal detskoy gematologii i onkologii. 2015; 1: 36-48. doi: 10.17650/2311-1267-2015-1-36-48 (In Russ).
  27. Vorob’yev A.I. [Hypercoagulable states in the clinic internal medicine]. Moskovskiy doktor. Vestnik Moskovskogo gorodskogo nauchnogo obshchestva terapevtov. 2009; 3(92): 1, 4–5 (In Russ).
  28. Egeberg O. Inherited antithrombin deficiency causing thrombophilia. Thromb. Diath. Haemorgh. 1965; 13: 516–530. PMID: 14347873.
  29. Kozlovskaya N.L. [Thrombophilic conditions]. Klinich. farmakologiya i terapiya. 2003; 12(1): 74-79 (In Russ.).
  30. Patrushev L.I. [Thrombophilic conditions and modern methods for their diagnostics]. Rus med zhurnal. 1998; 6(3): 181—185 (In Russ.).
  31. Kozlovskaya N.L., Bobrova L.A. [Inherited thrombophilia and kidneys]. Klinicheskaya nefrologiya. 2009; 3: 23–4 (In Russ.).
  32. Okorokov A.N. Diagnostika bolezney vnutrennikh organov: T. 5. diagnostika bolezney sistemy krovi. diagnostika bolezney pochek. [Diagnosis in internal medicine: Vol.5. Diagnosis blood disorders. Diagnosis kidney disease]. Moscow: Meditsinskaya literatura; 2003 (In Russ.).
  33. Patrushev L.I. [Genetic mechanisms of inherited hemostasis disorders]. Biokhimiya. 2002; 67: 40-55 (In Russ.).
  34. Reshetnyak T.M., Patrushev L.I., Stukacheva E.A. et al. [Leiden, G20210A mutations in prothrombin gene and antiphospholipid antibodies in systemic lupus erythematosus and antiphospholipid syndrome]. Ter. arkhiv. 2000; 5: 34-38. PMID: 11109617 (In Russ.).
  35. Owen W.G., Esmon C.T. Functional properties of an endothelial cofactor for thrombin-catalized activation of protein C. J. Biol. Chem. 1981; 256: 5532–5535. PMID: 6894592.
  36. Dahlbäck B. Advances in understanding pathogenic mechanisms of thrombophilic disorders. Blood. 2008; 112(1): 19-27. doi: 10.1182/blood-2008-01-077909. PMID: 18574041.
  37. Kim R.J., Becker R.C. Association between factor V Leiden, pro-thrombin G20210A, and methylenetetrahydrofolate reductase C677T mutations and events of the arterial circulatory system: a meta-analysis of published studies. Am Heart J. 2003; 146: 948-957. doi: 10.1016/S0002-8703(03)00519-2. PMID: 14660985.
  38. Ye Z., Liu E.H.C., Higgins J.P.T. et al. Seven haemostatic gene polymorphisms in coronary disease: meta-analysis of 66,155 cases and 91,307 controls. The Lancet. 2006; 367: 651-658. doi: 10.1016/S0140-6736(06)68263-9. PMID: 16503463.
  39. Moster M. Coagulopathies and arterial stroke. Journal of Neuro-Ophthalmology. 2003; 23(1): 63-71. PMID: 12616091.
  40. Bonduel M., Sciuccati G., Hepner M. et al. Prethrombotic disorders in children with arterial ischemic stroke and sinovenous thrombosis. Arch Neurol. 1999; 56: 967-971. PMID: 10448802.
  41. Szolnoki Z., Somogyvari F., Kondacs A. et al. Evaluation of the roles of the Leiden V mutation and ACE I/D polymorphism in subtypes of ischemic stroke. J.Neurol. 2001; 248(9): 756-761. PMID: 11596779.
  42. Ridker P.M., Hennekens C.H., Stampfer M.J. et al. Prospective study of endogenous tissue plasminogen activator and risk of stroke. Lancet. 1994; 343(8903): 940-943. PMID: 7909008.
  43. Smith F.B., Lee A.J., Fowkes F.G. et al. Hemostatic factors as predictors of ischemic heart disease and stroke in the Edinburgh Artery Study. Arterioscler Thromb Vasc Biol. 1997; 17(11): 3321-3325. PMID: 9409328.
  44. Johansson L., Jansson J.H., Boman K. et al. Tissue plasminogen activator, plasminogen activator inhibitor-1, and tissue plasminogen activator/plasminogen activator inhibitor-1 complex as risk factors for the development of a first stroke. Stroke. 2000; 31(1): 26-32. PMID: 10625711.
  45. Zunker P., Schick A., Padró T. et al. Tissue plasminogen activator and plasminogen activator inhibitor in patients with acute ischemic stroke: relation to stroke etiology. Neurol Res. 1999; 21(8): 727-732. PMID: 10596380.
  46. Munts A.G., van Genderen P.J., Dippel D.W. et al. Coagulation disorders in young adults with acute cerebral ischaemia. J Neurol. 1998; 245(1): 21-25. PMID: 9457624.
  47. Kenet G., Sadetzki S., Murad H. et al. Factor V leiden and antiphospholipid antibodies are significant risk factors for ischemic stroke in children. Stroke. 2000; 31: 1283-1288. PMID: 10835445.
  48. Carod-Artal F.J., Nunes S.V., Portugal D, et al. Ischemic stroke subtypes and thrombophilia in young and elderly Brazilian stroke patients admitted to a rehabilitation hospital. Stroke. 2005; 36(9): 2012-2014. doi: 10.1161/01.STR.0000177881.34840.cf. PMID: 16109904.
  49. Austin H., Chimowitz M.I., Hill H.A. et al. Cryptogenic stroke in relation to genetic variation in clotting factors and other genetic polymorphisms among young men and women. Stroke. 2002; 33(12): 2762-2768. PMID: 12468767.
  50. Taylor F.B. Jr. Protein S, C4b binding protein, and the hypercoagulable state. J Lab Clin Med. 1992; 119(6): 596-597. PMID: 1534344.
  51. Schäfer H.P., von Felten A. Protein-S deficiency in young patients with thrombotic brain infarction. Schweiz Med Wochenschr. 1989; 119(16): 489-492. PMID: 2524095.
  52. Green D., Otoya J., Oriba H. et al. Protein S deficiency in middle-aged women with stroke. Neurology. 1992; 42(5): 1029-1033. PMID: 1533705.
  53. Girolami A., Simioni P., Lazzaro A.R. et al. Severe arterial cerebral thrombosis in a patient with protein S deficiency (moderately reduced total and markedly reduced free protein S): a family study. Thromb Haemost. 1989; 61(1): 144-147. PMID: 2526383.
  54. Sie P., Boneu B., Biermé R. et al. Arterial thrombosis and protein S deficiency. Thromb Haemost. 1989; 62(3): 1040. PMID: 2531937.
  55. Wiesel M.L., Borg J.Y., Grunebaum L. et al. Influence of protein S deficiency on the arterial thrombosis risk. Presse Med. 1991; 20(22): 1023-1027. PMID: 1829220.
  56. Douay X., Lucas C., Caron C. et al. Antithrombin, protein C and protein S levels in 127 consecutive young adults with ischemic stroke. Acta Neurol Scand. 1998; 98(2): 124-127. PMID: 9724011.
  57. Mayer S.A., Sacco R.L., Hurlet-Jensen A. et al. Free protein S deficiency in acute ischemic stroke. A case-control study. Stroke. 1993; 24(2): 224-227. PMID: 8421823.
  58. Scarabin P.Y., Arveiler D., Amouyel P. et al. Plasma fibrinogen explains much of the difference in risk of coronary heart disease between France and Northern Ireland. The PRIME study. Atherosclerosis. 2003; 166: 103-109. PMID: 12482556.
  59. Heinrich J., Balleisen L., Schulte H. et al. Fibrinogen and factor VII in the prediction of coronary risk: results from the PROCAM study in healthy men. Arterioscler Thromb. 1994; 14: 54-59. PMID: 8274478.
  60. Meade T.W., Mellows S., Brozovic M. et al. Haemostatic function and ischaemic heart disease: principal results of the Northwick Park Heart Study. Lancet. 1986; 2: 533-537. PMID: 2875280.
  61. De Maat M.P., Kastelein J.J., Jukema J.W. et al. -455G/A polymorphism of the b-fibrinogen gene is associated with the progression of coronary atherosclerosis in symptomatic men: proposed role for an acute-phasereaction pattern of fibrinogen. REGRESS group. Arterioscler Thromb Vasc Biol. 1998; 18: 265-271. PMID: 9484992.
  62. Kessler C., Spitzer C., Stauske D. et al. The apolipoprotein E and-fibrinogen G/A-455 gene polymorphisms are associated with ischemic stroke involving large-vessel disease. Arterioscler Thromb Vasc Biol. 1997; 17: 2880-2884. PMID: 9409270.
  63. Nishiuma S., Kario K., Yakushijin K. et al. Genetic variation in the promoter region of the beta-fibrinogen gene is associated with ischemic stroke in a Japanese population. Blood Coagul Fibrinolysis. 1998; 9: 373-379. PMID: 9690809.
  64. Martiskainen M., Pohjasvaara T., Mikkelsson J. et al. Fibrinogen gene promoter 455-A allele as a risk factor for lacunar stroke. Stroke. 2003; 34: 886-891. doi: 10.1161/01.STR.0000060029.23872.55. PMID: 12637691.
  65. Bots M.L., Elwood P.C., Salonen J.T. et al. Level of fibrinogen and risk of fatal and non-fatal stroke. EUROSTROKE: a collaborative study among research centres in Europe. J Epidemiol Community Health. 2002; 56(1): 14-18. PMID: 11815639.
  66. Lalouschek W., Aull S., Series W. et al. The prothrombin G20210A mutation and factor V Leiden mutation in patients with cerebrovascular disease. Blood. 1998; 92(2): 704-705. PMID: 9657778.
  67. Bentolila S., Ripoll L., Drouet L. et al. Thrombophilia due to 20210 G-->A prothrombin polymorphism and cerebral ischemia in the young. Stroke. 1997; 28(9): 1846-1847. PMID: 9303036.
  68. Aznar J., Mira Y., Vayá A. et al. Factor V Leiden and prothrombin G20210A mutations in young adults with cryptogenic ischemic stroke. Thromb Haemost. 2004; 91(5): 1031-1034. doi: 10.1160/TH03-11-0690. PMID: 15116266.
  69. Margaglione M., D’Andrea G., Giuliani N. et al. Inherited prothrombotic conditions and premature ischemic stroke: sex difference in the association with factor V Leiden. Arterioscler Thromb Vasc Biol. 1999; 19: 1751-1756. PMID: 10397694.
  70. Casas J.P., Hingorani A.D., Bautista L.E. at al. Meta-analysis of Genetic Studies in Ischemic Stroke: Thirty-two Genes Involving Approximately 18,000 Cases and 58,000 Controls. Archives of Neurology. 2004; 61: 1652-1661. doi: 10.1001/archneur.61.11.1652. PMID: 15534175.
  71. Lalouschek W., Schillinger M., Hsieh K. et al. Matched case-control study on factor V Leiden and the prothrombin G20210A mutation in patients with ischemic stroke/transient ischemic attack up to the age of 60 years. Stroke. 2005; 36(7): 1405-1409. doi: 10.1161/01.STR.0000170635.45745.b8. PMID: 15947254.
  72. Slooter A.J., Rosendaal F.R., Tanis B.C. et al. Prothrombotic conditions, oral contraceptives, and the risk of ischemic stroke. J Thromb Haemost. 2005; 3: 1213-1217. doi: 10.1111/j.1538-7836.2005.01442.x. PMID: 15946211.
  73. Bezzi G., Bolzani W., Compagnoni V. et al. Factor V Leiden mutation and patent foramen ovale in ischemic stroke. Neurol Sci. 2002; 23: 229-231. doi: 10.1007/s100720200046. PMID: 12522679.
  74. Pezzini A., Grassi M., Zotto E.D. et al. Do common prothrombotic mutations influence the risk of cerebral ischaemia in patients with patent foramen ovale? Systematic review and meta-analysis. Thromb Haemost. 2009; 101: 813-817. PMID: 19404532.
  75. Poort S.R., Rosendaal F.R., Reitsma P.H. et al. A common genetic variation in the 3'-untranslated region of the prothrombin gene is associated with elevated plasma prothrombin levels and an increase in venous thrombosis. Blood. 1996; 88: 3698-3703. PMID: 8916933.
  76. De Stefano V., Chiusolo P., Paciaroni K. et al. Prothrombin G20210A mutant genotype is a risk factor for cerebrovascular ischemic disease in young patients. Blood. 1998; 91: 3562-3565. PMID: 9572989.
  77. Nowak-Göttl U., Sträter R., Heinecke A. et al. Lipoprotein (a) and genetic polymorphisms of clotting factor V, prothrombin, and methylenetetrahydrofolate reductase are risk factors of spontaneous ischemic stroke in childhood. Blood. 1999;94(11): 3678-3682. PMID: 10572079.
  78. Kozlova T.V. [The significance of genetic disorders in the system of hemocoagulation and hyperhomocysteinemia as a causative factor of cerebrovascular complications in patients with atrial fibrillation]. Nevrologicheskiy vestnik. 2005; XXXVII(1-2): 26-31 (In Russ.).
  79. Feinberg W.M., Macy E., Cornell E.S. et al. Plasmin-alpha2-antiplasmin complex in patients with atrial fibrillation. Stroke Prevention in Atrial Fibrillation Investigators. Thromb Haemost. 1999; 82: 100-103. PMID: 10456461.
  80. Kucukarabaci B., Gunes H.V., Ozdemir G. at al. Investigation of Association between Plasminogen Activator Inhibitor Type-1 (PAI-1) Gene 4G/5G Polymorphism Frequency and Plasma PAI-1 Enzyme Activity in Patients with Acute Stroke. Genetic Testing. 2008; 12: 443-451. doi: 10.1089/gte.2008.0025. PMID: 18662099.
  81. Slavik L., Krcova V., Hlusi A. et al. Molecular pathophysiology of thrombotic states and their impact to laboratory diagnostics. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2009; 153: 19-25. PMID: 19365521.
  82. Wiklund P.G., Nilsson L., Ardnor S.N. et al. Plasminogen Activator Inhibitor-1 4G/5G Polymorphism and Risk of Stroke: Replicated Findings in Two Nested Case-Control Studies Based on Independent Cohorts. Stroke. 2005; 36: 1661-1665. doi: 10.1161/01.STR.0000174485.10277.24. PMID: 16020771.
  83. Xu X., Li J., Sheng W. et al. Meta-Analysis of Genetic Studies from Journals Published in China of Ischemic Stroke in the Han Chinese Population. Cerebrovascular Diseases. 2008; 26: 48-62. doi: 10.1159/000135653. PMID: 18511872.
  84. Davidenkova E.F., Kolosova N.P., Liberman I. Mediko-geneticheskoye konsul’tirovaniye v sisteme profilaktiki ishemicheskoy bolezni serdtsa i insul’tov. [Genetic counseling for preventing ischemic heart disease and stroke]. Leningrad: Meditsina. 1979; 199 (In Russ.).
  85. Tsantes A.E., Nikolopoulos G.K., Bagos P.G. at al. Plasminogen activator inhibitor-1 4G/5G polymorphism and risk of ischemic stroke: a meta-analysis. Blood Coagulation & Fibrinolysis. 2007; 18: 497-504. doi: 10.1097/MBC.0b013e3281ec4eee. PMID: 17581326.
  86. Hoyekstra T., Geleijnse D.M., Kluft K. et al. [4G/4G genotype of PAI-1 gene is associated with risk of stroke in elderly]. Stroke: Rossiyskoye izdaniye. Nauchno-prakticheskiy meditsinskiy zhurnal. 2004; 2: 74-83 (In Russ.).
  87. Carter A.M., Catto A.J., Bamford J.M. et al. Association of the platelet glycoprotein IIb HPA-3 polymorphism with survival after ischemic stroke. Stroke. 1999; 30: 2606-2611. PMID: 10582985.
  88. Ridker P.M., Hennekens C.H., Schmitz C. et al. PlA1/A2 polymorphism of platelet glycoprotein IIIa and risks of myocardial infarction, stroke and venous thrombosis. Lancet. 1997; 349: 385-388. doi: 10.1016/S0140-6736(97)80010-4. PMID: 9033464.
  89. Slowik A., Dziedzic T., Turaj W. et al. A2 alelle of GpIIIa gene is a risk factor for stroke caused by large-vessel disease in males. Stroke. 2004; 35: 1589-1593. doi: 10.1161/01.STR.0000132194.24663.3d. PMID: 15178823.
  90. Slovik A., Dziyedzik T., Turay V. et al. [The GpIIIa A2 allele is a risk factor of stroke caused by atherosclerosis of the main arteries in men]. Stroke “(Insul’t)". 2005; 7 (In Russ.).
  91. Pizova N.V. Nasledstvennyye trombofilii i insul’t. [Inherited thrombophilia and stroke]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. 2013: 8(113): 76-81 (In Russ).
  92. Favaloro E.J., McDonald D, Lippi G. Laboratory investigation of thrombophilia: the good, the bad, and the ugly. Semin Thromb Hemost. 2009; 35(7): 695-710. doi: 10.1055/s-0029-1242723. PMID: 20013536.
  93. Pernod G., Biron-Andreani C., Morange P.E. et al. French Group on hemostasis, thrombosis, French Society of Vascular Medicine. Recommendations on testing for thrombophilia in venous thromboembolic disease: a French consensus guideline. J Mal Vasc. 2009; 34(3): 156-203. PMID: 19645086.
  94. Baglin T., Gray E., Greaves M., Hunt B.J. et al. Clinical guidelines for testing for heritable thrombophilia. Br J Haematol. 2010; 149(2): 209-220. doi: 10.1111/j.1365-2141.2009.08022.x. PMID: 20128794.
  95. Nicolaides A., Hull R.D., Fareed J. Thrombophilia. Clin Apl Thromb Hemost. 2013; 19(2): 177-187. doi: 10.1177/1076029612474840m. PMID: 23529489.
  96. De Stefano V., Rossi E. Testing for inherited thrombophilia and consequences for antithrombotic prophylaxis in patients with venous thromboembolism and their relatives. A review of the Guidelines from Scientific Societies and Working Groups. Thromb Haemost. 2013; 110(4): 697-705. doi: 10.1160/TH13-01-0011. PMID: 23846575.
  97. Kearon C., Akl E.A., Comerota A.J., Prandoni P. et al. Antithrombotic therapy for VTE disease: Antithrombotic Therapy and Prevention of Thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2012; 141 (suppl 2): e419S-e494S. doi: 10.1378/chest.11-2301. PMID: 22315268.
  98. National Institute for Health and Clinical Excellence: Guidance. In: Venous thromboembolic diseases: the management of venous thromboembolic diseases and the role of thrombophilia testing. London, National Institute for Health and Clinical Excellence: Guidance; 2012. PMID: 23638495.
  99. Hicks L.K., Bering H., Carson K.R., et al. The ASH Choosing Wisely®campaign: five hematologic tests and treatments to question. Blood. 2013; 122(24): 3879-3883. doi: 10.1182/asheducation-2013.1.9. PMID: 24319155
  100. Favaloro E.J. The futility of thrombophilia testing. Clin Chem Lab Med. 2014; 52(4): 499-503. doi: 10.1515/cclm-2013-0560. PMID: 23940063.
  101. Franchini M. The utility of thrombophilia Testing. Clin Chem Lab Med. 2014; 52(4): 495-497. doi: 10.1515/cclm-2013-0559. PMID: 23945127.
  102. Stevens S.M. Role of thrombophilia testing: con. J Thromb Thrombolysis. 2015; 39(3): 379-391. doi: 10.1007/s11239-015-1170-1. PMID: 25609384.
  103. Moll S. Thrombophilia: clinical-practical aspects. J Thromb Thrombolyis. 2015; 39(3): 367-378. doi: 10.1007/s11239-015-1197-3. PMID: 25724822.

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