Venous thrombosis: Understanding the paradoxes of recurrence

Journal of Thrombosis and Haemostasis

Volumn 11, Issue SUPPL.1, 2013, Pages 161-169

  Cannegieter, S C ^a   van Hylckama Vlieg, A ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Prognosis; Recurrence; Risk; Risk factors; Venous thrombosis

Indexed keywords

D DIMER;

ANTICOAGULANT THERAPY; BLOOD CLOTTING; BODY MASS; CLINICAL DECISION MAKING; CLINICAL PRACTICE; DISEASE ASSOCIATION; ENTERITIS; GENE MUTATION; HUMAN; MORTALITY; PRIORITY JOURNAL; RECURRENCE RISK; RECURRENT DISEASE; REVIEW; RISK FACTOR; SEX DIFFERENCE; SMOKING; THROMBOPHILIA; TIME; VEIN THROMBOSIS;

PROGNOSIS; RECURRENCE; RISK; RISK FACTORS; VENOUS THROMBOSIS;

HUMANS; RECURRENCE; RISK FACTORS; VENOUS THROMBOSIS;

EID: 84880637476     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12263     Document Type: Review

References (69)

1. Kearon C, Akl EA, Comerota AJ, Prandoni P, Bounameaux H, Goldhaber SZ, Nelson ME, Wells PS, Gould MK, Dentali F, Crowther M, Kahn SR, American College of Chest Physicians. 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-94S.
2. Prandoni P, Noventa F, Ghirarduzzi A, Pengo V, Bernardi E, Pesavento R, Iotti M, Tormene D, Simioni P, Pagnan A. The risk of recurrent venous thromboembolism after discontinuing anticoagulation in patients with acute proximal deep vein thrombosis or pulmonary embolism. A prospective cohort study in 1, 626 patients. Haematologica 2007; 92: 199-205.
3. Christiansen SC, Cannegieter SC, Koster T, Vandenbroucke JP, Rosendaal FR. Thrombophilia, clinical factors, and recurrent venous thrombotic events. JAMA 2005; 293: 2352-61.
4. Hansson P-O, Sorbo J, Eriksson H. Recurrent venous thromboembolism after deep vein thrombosis. Arch Intern Med 2000; 160: 769-74.
5. Keeling D. Duration of anticoagulation: decision making based on absolute risk. Blood Rev 2006; 20: 173-8.
6. Linkins LA, Choi PT, Douketis JD. Clinical impact of bleeding in patients taking oral anticoagulant therapy for venous thromboembolism: a meta-analysis. Ann Intern Med 2003; 139: 893-900.
7. Dahabreh IJ, Kent DM. Index event bias as an explanation for the paradoxes of recurrence risk research. JAMA 2011; 305: 822-3.
8. Rich JD, Cannon CP, Murphy SA, Qin J, Giugliano RP, Braunwald E. Prior aspirin use and outcomes in acute coronary syndromes. J Am Coll Cardiol 2010; 56: 1376-85.
9. Gruberg L, Weissman NJ, Waksman R, Fuchs S, Deible R, Pinnow EE, Ahmed LM, Kent KM, Pichard AD, Suddath WO, Satler LF, Lindsay J Jr. The impact of obesity on the short-term and long-term outcomes after percutaneous coronary intervention: the obesity paradox? J Am Coll Cardiol 2002; 39: 578-84.
10. Barbash GI, Reiner J, White HD, Wilcox RG, Armstrong PW, Sadowski Z, Morris D, Aylward P, Woodlief LH, Topol EJ. Evaluation of paradoxic beneficial effects of smoking in patients receiving thrombolytic therapy for acute myocardial infarction: mechanism of the "smoker's paradox" from the GUSTO-I trial, with angiographic insights: Global Utilization of Streptokinase and Tissue- Plasminogen Activator for Occluded Coronary Arteries. J Am Coll Cardiol 1995; 26: 1222-9.
11. Smits LJ, van Kuijk SM, Leffers P, Peeters LL, Prins MH, Sep SJ. Index event bias-a numerical example. J Clin Epidemiol 2013; 66: 192-6.
12. Baglin T. Unraveling the thrombophilia paradox: from hypercoagulability to the prothrombotic state. J Thromb Haemost 2010; 8: 228-33.
13. Christiansen SC, Lijfering WM, Helmerhorst FM, Rosendaal FR, Cannegieter SC. Sex difference in risk of recurrent venous thrombosis and the risk profile for a second event. J Thromb Haemost 2010; 8: 2159-68.
14. Eischer L, Eichinger S, Kyrle PA. Age at first venous thromboembolism and risk of recurrence: a prospective cohort study. Medicine (Baltimore) 2009; 88: 366-70.
15. Marchiori A, Mosena L, Prins MH, Prandoni P. The risk of recurrent venous thromboembolism among heterozygous carriers of factor V Leiden or prothrombin G20210A mutation. A systematic review of prospective studies. Haematologica 2007; 92: 1107-14.
16. Rosendaal FR. Venous thrombosis: a multicausal disease. Lancet 1999; 353: 1167-73.
17. Iorio A, Kearon C, Filippucci E, Marcucci M, Macura A, Pengo V, Siragusa S, Palareti G. Risk of recurrence after a first episode of symptomatic venous thromboembolism provoked by a transient risk factor: a systematic review. Arch Intern Med 2010; 170: 1710-6.
18. Le Gal G, Kovacs MJ, Carrier M, Do K, Kahn SR, Wells PS, Anderson DA, Chagnon I, Solymoss S, Crowther M, Righini M, Lacut K, White RH, Vickars L, Rodger M. Risk of recurrent venous thromboembolism after a first oestrogen-associated episode. Data from the REVERSE cohort study. Thromb Haemost 2010; 104: 498-503.
19. White RH, Chan WS, Zhou H, Ginsberg JS. Recurrent venous thromboembolism after pregnancy-associated versus unprovoked thromboembolism. Thromb Haemost 2008; 100: 246-52.
20. Rothman KJ, Greenland S, Lash TL. Modern Epidemiology. Philadelphia, PA: Lippincott, Williams, Wilkins, 2008.
21. Marchetti M, Pistorio A, Barosi G. Extended anticoagulation for prevention of recurrent venous thromboembolism in carriers of factor V Leiden-cost-effectiveness analysis. Thromb Haemost 2000; 84: 752-7.
22. Vink R, Kraaijenhagen RA, Levi M, Buller HR. Individualized duration of oral anticoagulant therapy for deep vein thrombosis based on a decision model. J Thromb Haemost 2003; 1: 2523-30.
23. Ho WK, Hankey GJ, Quinlan DJ, Eikelboom JW. Risk of recurrent venous thromboembolism in patients with common thrombophilia: a systematic review. Arch Intern Med 2006; 166: 729-36.
24. van den Belt AG, Sanson BJ, Simioni P, Prandoni P, Büller HR, Girolami A, Prins MH. Recurrence of venous thromboembolism in patients with familial thrombophilia. Arch Intern Med 1997; 157: 2227-32.
25. De Stefano V, Simioni P, Rossi E, Tormene D, Za T, Pagnan A, Leone G. The risk of recurrent venous thromboembolism in patients with inherited deficiency of natural anticoagulants antithrombin, protein C and protein S. Haematologica 2006; 91: 695-708.
26. Brouwer JL, Lijfering WM, Ten Kate MK, Kluin-Nelemans HC, Veeger NJ, van der Meer J. High long-term absolute risk of recurrent venous thromboembolism in patients with hereditary deficiencies of protein S, protein C or antithrombin. Thromb Haemost 2009; 101: 93-9.
27. Vossen CY, Walker ID, Svensson P, Souto JC, Scharrer I, Preston FE, Palareti G, Pabinger I, van der Meer FJ, Makris M, Fontcuberta J, Conard J, Rosendaal FR. Recurrence rate after a first venous thrombosis in patients with familial thrombophilia. Arterioscler Thromb Vasc Biol 2005; 25: 1992-7.
28. Baglin T, Luddington R, Brown K, Baglin C. Incidence of recurrent venous thromboembolism in relation to clinical and thrombophilic risk factors: prospective cohort study. Lancet 2003; 362: 523-6.
29. Engbers MJ, van Hylckama Vlieg A, Rosendaal FR. Venous thrombosis in the elderly: incidence, risk factors and risk groups. J Thromb Haemost 2010; 8: 2105-12.
30. Heit JA, Silverstein MD, Mohr DN, Petterson TM, Lohse CM, O'Fallon WM, Melton LJ 3rd. The epidemiology of venous thromboembolism in the community. Thromb Haemost 2001; 86: 452-63.
31. Kyrle PA, Minar E, Bialonczyk C, Hirschl M, Weltermann A, Eichinger S. The risk of recurrent venous thromboembolism in men and women. N Engl J Med 2004; 350: 2558-63.
32. Kim TM, Kim JS, Han SW, Hong YS, Kim I, Ha J, Kim SJ, Chung JW, Park JH, Lee D, Park S, Kim BK, Kim NK, Yoon SS. Clinical predictors of recurrent venous thromboembolism: a single institute experience in Korea. Thromb Res 2009; 123: 436-43.
33. Murin S, Romano PS, White RH. Comparison of outcomes after hospitalization for deep venous thrombosis or pulmonary embolism. Thromb Haemost 2002; 88: 407-14.
34. Hutten BA, Prins MH, Gent M, Ginsberg J, Tijssen JG, Buller HR. Incidence of recurrent thromboembolic and bleeding complications among patients with venous thromboembolism in relation to both malignancy and achieved international normalized ratio: a retrospective analysis. J Clin Oncol 2000; 18: 3078-83.
35. Prandoni P, Lensing AW, Piccioli A, Bernardi E, Simioni P, Girolami B, Marchiori A, Sabbion P, Prins MH, Noventa F, Girolami A. Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 2002; 100: 3484-8.
36. Heit JA, Silverstein MD, Mohr DN, Petterson TM, O'Fallon WM, Melton LJ III. Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case-control study. Arch Intern Med 2000; 160: 809-15.
37. Douketis JD, Foster GA, Crowther MA, Prins MH, Ginsberg JS. Clinical risk factors and timing of recurrent venous thromboembolism during the initial 3 months of anticoagulant therapy. Arch Intern Med 2000; 160: 3431-6.
38. Cushman M, Tsai AW, White RH, Heckbert SR, Rosamond WD, Enright P, Folsom AR. Deep vein thrombosis and pulmonary embolism in two cohorts: the longitudinal investigation of thromboembolism etiology. Am J Med 2004; 117: 19-25.
39. de Godoy JM, de Godoy MF, Braile DM. Recurrent thrombosis in patients with deep vein thrombosis and/or venous thromboembolism associated with anticardiolipin antibodies. Angiology 2006; 57: 79-83.
40. Khamashta MA, Cuadrado MJ, Mujic F, Taub NA, Hunt BJ, Hughes GR. The management of thrombosis in the antiphospholipid-antibody syndrome. N Engl J Med 1995; 332: 993-7.
41. Schulman S, Svenungsson E, Granqvist S. Anticardiolipin antibodies predict early recurrence of thromboembolism and death among patients with venous thromboembolism following anticoagulant therapy. Duration of Anticoagulation Study Group. Am J Med 1998; 104: 332-8.
42. Novacek G, Weltermann A, Sobala A, Tilg H, Petritsch W, Reinisch W, Mayer A, Haas T, Kaser A, Feichtenschlager T, Fuchssteiner H, Knoflach P, Vogelsang H, Miehsler W, Platzer R, Tillinger W, Jaritz B, Schmid A, Blaha B, Dejaco C, et al. Inflammatory bowel disease is a risk factor for recurrent venous thromboembolism. Gastroenterology 2010; 139: 779-87.
43. Laczkovics C, Grafenhofer H, Kaider A, Quehenberger P, Simanek R, Mannhalter C, Lechner K, Pabinger I. Risk of recurrence after a first venous thromboembolic event in young women. Haematologica 2007; 92: 1201-7.
44. Eichinger S, Hron G, Bialonczyk C, Hirschl M, Minar E, Wagner O, Heinze G, Kyrle PA. Overweight, obesity, and the risk of recurrent venous thromboembolism. Arch Intern Med 2008; 168: 1678-83.
45. Romualdi E, Squizzato A, Ageno W. Abdominal obesity and the risk of recurrent deep vein thrombosis. Thromb Res 2007; 119: 687-90.
46. Bates SM, Greer IA, Middeldorp S, Veenstra DL, Prabulos AM, Vandvik PO, American College of Chest Physicians. VTE, thrombophilia, antithrombotic therapy, and pregnancy: Antithrombotic Therapy and Prevention of Thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest 2012;141(Suppl 2):e691S-736S
47. Stegeman BH, Timp JF, Flinterman LE, Helmerhorst FM, Rosendaal FR, Cannegieter SC, van Hylckama Vlieg A. Recurrent venous thrombosis in premenopausal women: effect of hormonal contraceptive use. Abstract for the 2013 ISTH congress.
48. Verhovsek M, Douketis JD, Yi Q, Shrivastava S, Tait RC, Baglin T, Poli D, Lim W. Systematic review: D-dimer to predict recurrent disease after stopping anticoagulant therapy for unprovoked venous thromboembolism. Ann Intern Med 2008; 149: 481-90.
49. Bruinstroop E, Klok FA, Van De Ree MA, Oosterwijk FL, Huisman MV. Elevated D-dimer levels predict recurrence in patients with idiopathic venous thromboembolism: a meta-analysis. J Thromb Haemost 2009; 7: 611-8.
50. Eichinger S, Minar E, Bialonczyk C, Minar E, Kollars M, Kyrle PA. D-dimer levels and risk of recurrent venous thromboembolism. JAMA 2003; 290: 1071-4.
51. Hron G, Kollars M, Binder BR, Eichinger S, Kyrle PA. Identification of patients at low risk for recurrent venous thromboembolism by measuring thrombin generation. JAMA 2006; 296: 397-402.
52. Eichinger S, Hron G, Kollars M, Kyrle PA. Prediction of recurrent venous thromboembolism by endogenous thrombin potential and D-dimer. Clin Chem 2008; 54: 2042-8.
53. Tripodi A, Legnani C, Chantarangkul V, Cosmi B, Palareti G, Mannucci PM. High thrombin generation measured in the presence of thrombomodulin is associated with an increased risk of recurrent venous thromboembolism. J Thromb Haemost 2008; 6: 1327-33.
54. Besser M, Baglin C, Luddington R, van Hylckama Vlieg A, Baglin T. High rate of unprovoked recurrent venous thrombosis is associated with high thrombin-generating potential in a prospective cohort study. J Thromb Haemost 2008; 6: 1720-5.
55. Prandoni P, Lensing AW, Prins MH, Bernardi E, Marchiori A, Bagatella P, Frulla M, Mosena L, Tormene D, Piccioli A, Simioni P, Girolami A. Residual venous thrombosis as a predictive factor of recurrent venous thromboembolism. Ann Intern Med 2002; 137: 955-60.
56. Young L, Ockelford P, Milne D, Rolfe-Vyson V, McKelvie S, Harper P. Post-treatment residual thrombus increases the risk of recurrent deep vein thrombosis and mortality. J Thromb Haemost 2006;4:1919-24.
57. Siragusa S, Malato A, Anastasio R, Cigna V, Milio G, Amato C, Bellisi M, Attanzio MT, Cormaci O, Pellegrino M, Dolce A, Casuccio A, Bajardi G, Mariani G. Residual vein thrombosis to establish duration of anticoagulation after a first episode of deep vein thrombosis: the "DACUS" study. Blood 2008; 112: 511-5.
58. Cosmi B, Legnani C, Cini M, Guazzaloca G, Palareti G. D-dimer levels in combination with residual venous obstruction and the risk of recurrence after anticoagulation withdrawal for a first idiopathic deep vein thrombosis. Thromb Haemost 2005; 94: 969-74.
59. Emmerich J, Fiessinger JN. Residual venous thrombosis and recurrent thromboembolism. Ann Intern Med 2003; 139: 303.; author reply 304.
60. Douketis JD, Crowther MA, Foster GA, Ginsberg JS. Does the location of thrombosis determine the risk of disease recurrence in patients with proximal deep vein thrombosis? Am J Med 2001; 110: 515-9.
61. Laporte S, Tardy B, Quenet S, Buchmuller-Cordier A, Chabaud S, Epinat M, Decousus H, Mismetti P. The location of deep vein thrombosis as a predictive factor for recurrence and cancer discovery after proximal deep vein thrombosis. Haematologica 2003; 88: ELT08.
62. McRae S, Tran H, Schulman S, Ginsberg J, Kearon C. Effect of patient's sex on risk of recurrent venous thromboembolism: a meta-analysis. Lancet 2006; 368: 371-8.
63. Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrøm J. Incidence and mortality of venous thrombosis a population-based study. J Thromb Haemost 2007; 5: 692-9.
64. Kyrle PA, Minar E, Hirschl M, Bialonczyk C, Stain M, Schneider B, Weltermann A, Speiser W, Lechner K, Eichinger S. High plasma levels of factor VIII and the risk of recurrent venous thromboembolism. N Engl J Med 2000; 343: 457-62.
65. Legnani C, Benilde C, Michela C, Mirella F, Giuliana G, Gualtiero P. High plasma levels of factor VIII and risk of recurrence of venous thromboembolism. Br J Haematol 2004; 124: 504-10.
66. Weltermann A, Eichinger S, Bialonczyk C, Minar E, Hirschl M, Quehenberger P, Schönauer V, Kyrle PA. The risk of recurrent venous thromboembolism among patients with high factor IX levels. J Thromb Haemost 2003; 1: 28-32.
67. Rodger MA, Kahn SR, Wells PS, Anderson DA, Chagnon I, Le Gal G, Solymoss S, Crowther M, Perrier A, White R, Vickars L, Ramsay T, Betancourt MT, Kovacs MJ. Identifying unprovoked thromboembolism patients at low risk for recurrence who can discontinue anticoagulant therapy. CMAJ 2008; 179: 417-26.
68. Eichinger S, Heinze G, Jandeck LM, Kyrle PA. Risk assessment of recurrence in patients with unprovoked deep vein thrombosis or pulmonary embolism: the Vienna prediction model. Circulation 2010; 121: 1630-6.
69. Tosetto A, Iorio A, Marcucci M, Baglin T, Cushman M, Eichinger S, Palareti G, Poli D, Tait RC, Douketis J. Predicting disease recurrence in patients with previous unprovoked venous thromboembolism: a proposed prediction score (DASH). J Thromb Haemost 2012; 10: 1019-25.