Hyperthyroidism and venous thrombosis: A casual or causal association? A systematic literature review

Clinical and Applied Thrombosis/Hemostasis

Volumn 17, Issue 4, 2011, Pages 387-392

  Franchini, Massimo ^a   Lippi, Giuseppe ^a   Targher, Giovanni ^b  

^a UNIVERSITY HOSPITAL OF PARMA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

Author keywords

coagulation; Graves' disease; hyperthyroidism; venous thrombosis

Indexed keywords

ACTIVATED PROTEIN C; BLOOD CLOTTING FACTOR 5 LEIDEN; BLOOD CLOTTING FACTOR 8; FIBRINOGEN; LUPUS ANTICOAGULANT; METHYLENETETRAHYDROFOLATE REDUCTASE (NADPH2); ORAL CONTRACEPTIVE AGENT; PROTHROMBIN;

ANGIOCARDIOGRAPHY; ANTICOAGULATION; ANTIPHOSPHOLIPID SYNDROME; ASYMPTOMATIC DISEASE; BUDD CHIARI SYNDROME; CARDIOVASCULAR RISK; CONSCIOUSNESS DISORDER; DEEP VEIN THROMBOSIS; DIABETES MELLITUS; DISEASE ASSOCIATION; GENE MUTATION; GRAVES DISEASE; HEADACHE; HEART ATRIUM FIBRILLATION; HUMAN; HYPERHOMOCYSTEINEMIA; HYPERTHYROIDISM; INTRACRANIAL HYPERTENSION; LUNG EMBOLISM; NEUROPATHY; OBESITY; OCCLUSIVE CEREBROVASCULAR DISEASE; ORAL CONTRACEPTION; PNEUMONIA; PRIORITY JOURNAL; PROTEIN C DEFICIENCY; RETROSPECTIVE STUDY; REVIEW; SJOEGREN SYNDROME; SMOKING; SUBACUTE THYROIDITIS; SYSTEMATIC REVIEW; THROMBOCYTOSIS; THROMBOPHILIA; THYROTOXICOSIS; VARICOSIS; VEIN THROMBOSIS; VENOUS THROMBOEMBOLISM;

ADOLESCENT; ADULT; AGED; FEMALE; HEMOSTASIS; HUMANS; HYPERTHYROIDISM; HYPOTHYROIDISM; MALE; MIDDLE AGED; VENOUS THROMBOSIS; YOUNG ADULT;

EID: 80052724936     PISSN: 10760296     EISSN: 19382723     Source Type: Journal    
DOI: 10.1177/1076029610364521     Document Type: Review

References (61)

1. Squizzato A., Romualdi E., Büller HR, Gerdes VEA. Thyroid dysfunction and effects on coagulation and fibrinolysis: a systematic review. J Clin Endocrinol Metab. 2007 ; 92 (7). 2415-2420. (Pubitemid 47037335)
2. Franchini M., Montagnana M., Manzato F., Vescovi PP Thyroid dysfunction and hemostasis: an issue still unresolved. Semin Thromb Hemost. 2009 ; 35 (3). 288-294.
3. Simone JV, Abildgaard CF, Schulman I. Blood coagulation in thyroid dysfunction. N Engl J Med. 1965 ; 273 (20). 1057-1061.
4. Myrup B., Bregengård C., Faber J. Primary haemostasis and thyroid disease. J Int Med. 1995 ; 238 (1). 59-63.
5. Hofbauer LC, Heufelder AE Coagulation disorders in thyroid diseases. Eur J Endocrinol. 1997 ; 136 (1). 1-7. (Pubitemid 27090671)
6. Squizzato A., Gerdes VEA, Ageno W., Büller HR The coagulation system in endocrine disorders: a narrative review. Intern Emerg Med. 2007 ; 28 (2). 76-83.
7. Marongiu F., Cauli C., Mariotti S. Thyroid, hemostasis and thrombosis. J Endocrinol Invest. 2004 ; 27 (11). 1065-1071.
8. Mariotti S., Cambuli VM Cardiovascular risk in elderly hypothyroid patients. Thyroid. 2007 ; 17 (11). 1067-1073. (Pubitemid 350207761)
9. Schutta HS, Williams EC, Baranski BG, Sutula TP Cerebral venous thrombosis with plasminogen deficiency. Stroke. 1991 ; 22 (3). 401-405.
10. Siegert CEH, Smelt AHM, de Bruin TWA. Superior sagittal sinus thrombosis and thyrotoxicosis. Possible association in two cases. Stroke. 1995 ; 26 (3). 496-497.
11. Silburn PA, Sandstrom PA, Staples C., Mowat P., Boyle RS Deep cerebral venous thrombosis presenting as an encephalitic illness. Postgrad Med J. 1996 ; 72 (848). 355-368.
12. Dulli DA, Luzzio CC, Williams EC, Schutta HS Cerebral venous thrombosis and activated protein C resistance. Stroke. 1996 ; 27 (10). 1731-1733. (Pubitemid 26332494)
13. De Schryver EL, Hoogenraad TU, Banga JD, Kappelle LJ Thyrotoxicosis, protein C deficiency and lupus anticoagulant in a case of cerebral sinus thrombosis. Neth J Med. 1999 ; 55 (4). 201-202. (Pubitemid 29438716)
14. Verberne HJ, Fliers E., Prummel MF, Stam J., Brandjes DP, Wiersinga WM Thyrotoxicosis as a predisposing factor for cerebral venous thrombosis. Thyroid. 2000 ; 10 (7). 607-610. (Pubitemid 30670622)
15. Dai A., Wasay M., Dubey N., Giglio P., Bakshi R. Superior sagittal sinus thrombosis secondary to hyperthyroidism. J Stroke Cerebrovasc Dis. 2000 ; 9 (2). 89-90.
16. Ra CS, Lui CC, Liang CL, Chen HJ, Kuo YL, Chen WF Superior sagittal sinus thrombosis induced by thyrotoxicosis. J Neurosurg. 2001 ; 94 (1). 130-132.
17. Maes J., Michotte A., Velkeniers B., Stadnik T., Jochmans K. Hyperthyroidism with increased factor VIII procoagulant protein as a predisposing factor for cerebral venous thrombosis. J Neurol Neurosurg Psychiatry. 2002 ; 73 (4). 458.
18. Molloy E., Cahill M., O'Hare AJ Cerebral venous sinus thrombosis precipitated by Graves' disease and factor V Leiden mutation. Ir Med J. 2003 ; 96 (2). 46-47. (Pubitemid 38111699)
19. Morimoto S., Nemoto M., Han A., et al. ''Economy class syndrome'' associated with diabetes and Graves disease [in Japanese]. Nippon Naika Gakkai Zasshi. 2003 ; 92 (10). 2020-2022.
20. Colleran KM, Ratliff DM, Burge MR Potential association of thyrotoxicosis with vitamin B and folate deficiencies, resulting in risk for hyperhomocysteinemia and subsequent thromboembolic events. Endocr Pract. 2003 ; 9 (4). 290-295.
21. Madronero-Vuelta AB, Sanahuja-Montesinos J., Bergua-Llop M., Aragua's-Arasanz C. Trombosis venosa cerebral asociada a tiroiditis subaguda de De Quervain en una paciente con la mutacio'n G20210A del gen de la protrombina. Rev Neurol. 2004 ; 39 (6). 533-535. (Pubitemid 39472011)
22. Karouache A., Mounach J., Bouraza A., et al. Cerebral thrombophlebitis revealing hyperthyroidism: two cases report and literature review. Rev Med Interne. 2004 ; 25 (12). 920-923. (Pubitemid 39611012)
23. Mouton S., Nighoghossian N., Berruyer M., et al. Hyperthyroidism and cerebral venous thrombosis. Eur Neurol. 2005 ; 54 (2). 78-80. (Pubitemid 41540648)
24. Werner D., Misfeld M., Regenfus M., Sievers HH, Graf B. Emergency coronary angiography with gadolinium in a patient with thyrotoxicosis, pulmonary embolism and persistent right atrial thrombi. Clin Res Cardiol. 2006 ; 95 (8). 418-421. (Pubitemid 44133992)
25. Kasuga K., Naruse S., Umeda M., Tanaka M., Fujita N. Case of cerebral venous thrombosis due to Graves' disease with increased factor VIII activity. Rinsho Shinkeigaku. 2006 ; 46 (4). 270-273. (Pubitemid 43854715)
26. Squizzato A., Vitale J., Gerdes VE, Romualdi E., Büller HR, Ageno W. Recurrent deep venous thrombosis during optimal anticoagulation and overt hyperthyroidism: a case report. Blood Coagul Fibrinolysis. 2007 ; 18 (8). 801-803. (Pubitemid 350059340)
27. Nagumo K., Fukushima T., Takahashi H., Sakakibara Y., Kojima S., Akikusa B. Thyroid crisis and protein C deficiency in a case of superior sagittal sinus thrombosis. Brain Nerve. 2007 ; 59 (3). 271-276. (Pubitemid 46449674)
28. Romualdi E., Squizzato A., Ageno W. Venous thrombosis: a possible complication of overt hyperthyroidism. Eur J Intern Med. 2008 ; 19 (5). 386-388.
29. Makino M., Honda H., Miyoshi F., et al. A fulminant case of renal vein thrombosis in a patient with autoimmune disorder and membranous nephropathy. Intern Med. 2008 ; 47 (10). 969-973. (Pubitemid 351936195)
30. Kim D., Young S., Chunilal S., Cutfield R. Possible association of venous thromboembolism and hyperthyroidism: 4 case reports and literature review. N Z Med J. 2008 ; 121 (1280). 53-57.
31. Pekdemir M., Yilmaz S., Ersel M., Sarisoy HT A rare cause of headache: cerebral venous sinus thrombosis due to hyperthyroidism. Am J Emerg Med. 2008 ; 26 (3). 383.e1-383.e2.
32. Strada L., Gandolfo C., Del Sette M. Cerebral sinus venous thrombosis in a subject with thyrotoxicosis and MTHFR gene polymorphism. Neurol Sci. 2008 ; 29 (5). 343-345.
33. Mouelhi L., Mekki H., Debbeche R., Salem M., Najjar T. Thrombosis in inflammatory bowel disease: mechanisms and risk factors. Tunis Med. 2009 ; 87 (5). 307-310.
34. Danescu LG, Badshah A., Danescu SC, et al. Venous thromboembolism in patients hospitalized with thyroid dysfunction. Clin Appl Thromb Hemost. 2009 ; 15 (6). 676-680.
35. Usami K., Kinoshita T., Tokumoto K., et al. Successful treatment of plasma exchange for severe cerebral venous thrombosis with thyrotoxicosis. J Stroke Cerebrovasc Dis. 2009 ; 18 (3). 239-243.
36. Farid NR, Griffiths BL, Collins JR, Marshall WH, Ingram DW Blood coagulation and fibrinolysis in thyroid disease. Thromb Haemost. 1976 ; 35 (2). 415-422.
37. Marongiu F., Conti M., Murtas ML, Mameli G., Sorano GG, Martino E. What causes the increase in platelet mean volume in thyroid pathological conditions ? Thromb Haemost. 1990 ; 63 (2). 323-324. (Pubitemid 20128207)
38. Franchini M., Lippi G., Manzato F., Vescovi PP Thyroid-associated autoimmune coagulation disorders. J Thromb Thrombolysis. 2010 ; 29 (1). 87-91.
39. Marshall JS, Weisberger AS, Levy RP Coexistent idiopathic thrombocytopenic purpura and hyperthyroidism. Ann Intern Med. 1967 ; 67 (2). 411-414.
40. Pinals RS, Tomar RH, Haas DC, Farah F. Graves' disease, myasthenia gravis and purpura. Ann Intern Med. 1977 ; 87 (2). 250.
41. Yamaguchi K., Ookubo Y., Matsuda H., Suzaki K., Fujushima H., Uzwa H. Idiopathic thrombocytopenic purpura subsequent to Graves' disease and insulin-dependent diabetes mellitus. Diab Res Clin Pract. 1987 ; 3 (4). 233-237. (Pubitemid 17092559)
42. Hofbauer LC, Spitzweg C., Schmauss S., Heufelder AE Graves disease associated with autoimmune thrombocytopenic purpura. Arch Intern Med. 1997 ; 157 (9). 1033-1036. (Pubitemid 27190894)
43. Cordiano I., Betterle C., Spadaccino CA, Soini B., Girolami A., Fabris F. Autoimmune thrombocytopenia (AITP) and thyroid autoimmune disease (TAD): overlapping syndromes ? Clin Exp Immunol. 1998 ; 113 (3). 373-378. (Pubitemid 28410561)
44. Marongiu F., Conti M., Murtas ML, et al. Anticardiolipin antibodies in Grave's disease: relationship with thrombin activity in vivo. Thromb Res. 1991 ; 64 (6). 745-749.
45. Paggi A., Caccavo D., Ferri GM, et al. Anticardiolipin antibodies in autoimmune thyroid disease. Clin Endocrinol. 1994 ; 40 (3). 329-333.
46. Hofbauer LC, Spitzweg C., Heufelder AE Graves' disease associated with the primary antiphospholipid syndrome. J Rheumatol. 1996 ; 23 (8). 1435-1437. (Pubitemid 26258770)
47. Takahashi A., Tamura A., Ishikawa O. Antiphospholipid antibody syndrome complicated by Graves' disease. J Dermatol. 2002 ; 29 (12). 776-780. (Pubitemid 36125339)
48. Homoncik M., Gessl A., Ferlitsch A., Jilma B., Vierhapper H. Altered platelet plug formation in hyperthyroidism and hypothyroidism. J Clin Endocrinol Metab. 2007 ; 92 (8). 3006-3012. (Pubitemid 47236363)
49. Loeliger EA, Esch B. The biological disappearance rate of prothrombin, factors VII, IX and X from plasma in hypothyroidism, hyperthyroidism and during fever. Thromb Diathes Haemorrh. 1963 ; 10 (2). 267-277.
50. Rogers JS, Shane SR, Jencks FS Factor VIII activity and thyroid function. Ann Intern Med. 1982 ; 97 (5). 713-716. (Pubitemid 13251644)
51. Rogers JS, Shane SR Factor VIII activity in normal volunteers receiving oral thyroid hormone. J Lab Clin Med. 1983 ; 102 (3). 444-449. (Pubitemid 13009619)
52. Palareti G., Biagi G., Legnani C., et al. Association of reduced factor VIII with impaired platelet reactivity to adrenalin and collagen after total thyroidectomy. Thromb Haemost. 1989 ; 62 (4). 1053-1056. (Pubitemid 20011488)
53. Michiels JJ, Schroyens W., Berneman Z., van der Planken M. Acquired von Willebrand syndrome type 1 in hypothyroidism: reversal after treatment with thyroxine. Clin Appl Thromb Hemost. 2001 ; 7 (2). 113-115. (Pubitemid 32242186)
54. Lippi G., Franchini M., Targher G., et al. Hyperthyroidism is associated with shortened APTT and increased fibrinogen values in a general population of unselected outpatients. J Thromb Thrombolysis. 2009 ; 28 (3). 362-365.
55. Dorr M., Robinson DM, Wallaschofski H., et al. Low serum thyrotropin is associated with high plasma fibrinogen. J Clin Endocrinol Metab. 2006 ; 91 (2). 530-534. (Pubitemid 43236922)
56. Coban E., Aydemir M. Levels of plasma fibrinogen and D-dimer in subjects with subclinical hyperthyroidism. Med Sci Monit. 2008 ; 14 (1). CR42 - CR46.
57. Erem C. Blood coagulation, fibrinolytic activity and lipid profile in subclinical thyroid disease: subclinical hyperthyroidism increases plasma factor X activity. Clin Endocrinol. 2006 ; 64 (3). 323-329.
58. Erem C., Ersoz H., Karti SS, et al. Blood coagulation and fibrinolysis in patients with hyperthyroidism. J Endocrinol Invest. 2002 ; 25 (4). 345-350. (Pubitemid 34436130)
59. Koster T., Blann AD, Briët E., Vandenbroucke JP, Rosendaal FR Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet. 1995 ; 345 (8843). 152-155.
60. Squizzato A., Gerdes VEA, Brandjes DPM, Buller HR, Stam J. Thyroid diseases and cerebrovascular disease. Stroke. 2005 ; 36 (10). 2302-2310. (Pubitemid 41429267)
61. Martinelli I. Unusual forms of venous thrombosis and thrombophilia. Pathophysiol Haemost Thromb. 2002 ; 32 (5-6). 343-345. (Pubitemid 37490567)