Journal of Thrombosis and Thrombolysis

, Volume 30, Issue 1, pp 67–78 | Cite as

Venous thromboembolism and cancer: a systematic review

  • Celso Arrais Rodrigues
  • Renata Ferrarotto
  • Roberto Kalil Filho
  • Yana A. S. Novis
  • Paulo M. G. Hoff
Article

Abstract

Venous thromboembolism (VTE) is a serious and potentially fatal disorder, which is often associated with a significant impact on the quality of life and on the clinical outcome of cancer patients. The pathophysiology of the association between thrombosis and cancer is complex: malignancy is associated with a baseline hypercoagulable state due to many factors including release of inflammatory cytokines, activation of the clotting system, expression of hemostatic proteins on tumor cells, inhibition of natural anticoagulants, and impaired fibrinolysis. Several risk factors, related to the patient, the disease, and the therapeutic interventions, have been identified as contributing to the occurrence of VTE. There is convincing evidence to recommend the use of heparins or fondaparinux for prevention of VTE in selected cancer patients, and, especially in some particular types of malignancies and cancer treatments. Management of VTE in patients with cancer is more challenging and bleeding complications associated with the use of anticoagulants are significantly higher in cancer patients than in those without malignancy. Important issues that need to be considered in all cases are interference with anticancer therapy, inconvenience of treatment, and impact on quality of life.

Keywords

Venous thromboembolism Cancer Thromboprophylaxis Anticoagulation 

References

  1. 1.
    Trousseau A (1865) Phlegmasia alba dolens, 2nd edn. JB Balliere et Fils, ParisGoogle Scholar
  2. 2.
    Khorana AA, Ahrendt SA, Ryan CK et al (2007) Tissue factor expression, angiogenesis, and thrombosis in pancreatic cancer. Clin Cancer Res 13:2870–2875PubMedGoogle Scholar
  3. 3.
    Lee AY, Levine MN (2003) Venous thromboembolism and cancer: risks and outcomes. Circulation 107:I17–I21PubMedGoogle Scholar
  4. 4.
    White RH, Chew HK, Zhou H et al (2005) Incidence of venous thromboembolism in the year before the diagnosis of cancer in 528,693 adults. Arch Intern Med 165:1782–1787PubMedGoogle Scholar
  5. 5.
    Prandoni P, Piccioli A (1997) Venous thromboembolism and cancer: a two-way clinical association. Front Biosci 2:e12–e20PubMedGoogle Scholar
  6. 6.
    Bick RL (1978) Alterations of hemostasis associated with malignancy: etiology, pathophysiology, diagnosis and management. Semin Thromb Hemost 5:1–26PubMedGoogle Scholar
  7. 7.
    Kakkar AK, Levine M, Pinedo HM et al (2003) Venous thrombosis in cancer patients: insights from the FRONTLINE survey. Oncologist 8:381–388PubMedGoogle Scholar
  8. 8.
    Levitan N, Dowlati A, Remick SC et al (1999) Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data. Medicine (Baltimore) 78:285–291Google Scholar
  9. 9.
    Sorensen HT, Mellemkjaer L, Olsen JH et al (2000) Prognosis of cancers associated with venous thromboembolism. N Engl J Med 343:1846–1850PubMedGoogle Scholar
  10. 10.
    Stein PD, Beemath A, Meyers FA et al (2006) Incidence of venous thromboembolism in patients hospitalized with cancer. Am J Med 119:60–68PubMedGoogle Scholar
  11. 11.
    Blom JW, Doggen CJ, Osanto S et al (2005) Malignancies, prothrombotic mutations, and the risk of venous thrombosis. JAMA 293:715–722PubMedGoogle Scholar
  12. 12.
    Huber O, Bounameaux H, Borst F et al (1992) Postoperative pulmonary embolism after hospital discharge. An underestimated risk. Arch Surg 127:310–313PubMedGoogle Scholar
  13. 13.
    Kakkar AK, Haas S, Wolf H et al (2005) Evaluation of perioperative fatal pulmonary embolism and death in cancer surgical patients: the MC-4 cancer substudy. Thromb Haemost 94:867–871PubMedGoogle Scholar
  14. 14.
    Khorana AA, Francis CW, Culakova E et al (2006) Thromboembolism in hospitalized neutropenic cancer patients. J Clin Oncol 24:484–490PubMedGoogle Scholar
  15. 15.
    Prandoni P, Falanga A, Piccioli A (2005) Cancer and venous thromboembolism. Lancet Oncol 6:401–410PubMedGoogle Scholar
  16. 16.
    Baron JA, Gridley G, Weiderpass E et al (1998) Venous thromboembolism and cancer. Lancet 351:1077–1080PubMedGoogle Scholar
  17. 17.
    Sorensen HT, Mellemkjaer L, Steffensen FH et al (1998) The risk of a diagnosis of cancer after primary deep venous thrombosis or pulmonary embolism. N Engl J Med 338:1169–1173PubMedGoogle Scholar
  18. 18.
    Murchison JT, Wylie L, Stockton DL (2004) Excess risk of cancer in patients with primary venous thromboembolism: a national, population-based cohort study. Br J Cancer 91:92–95PubMedGoogle Scholar
  19. 19.
    Johnson MJ, Sproule MW, Paul J (1999) The prevalence and associated variables of deep venous thrombosis in patients with advanced cancer. Clin Oncol (R Coll Radiol) 11:105–110Google Scholar
  20. 20.
    Sproul E (1938) Carcinoma and venous thrombosis: the frequency of association of carcinoma in the body or tail of the pancreas with multiple venous thrombosis. Am J Cancer 34:566–585Google Scholar
  21. 21.
    Ambrus JL, Ambrus CM, Pickern J et al (1975) Hematologic changes and thromboembolic complications in neoplastic disease and their relationship to metastasis. J Med 6:433–458PubMedGoogle Scholar
  22. 22.
    Sorensen HT, Pedersen L, Mellemkjaer L et al (2005) The risk of a second cancer after hospitalisation for venous thromboembolism. Br J Cancer 93:838–841PubMedGoogle Scholar
  23. 23.
    Schulman S, Lindmarker P (2000) Incidence of cancer after prophylaxis with warfarin against recurrent venous thromboembolism. Duration of Anticoagulation Trial. N Engl J Med 342:1953–1958PubMedGoogle Scholar
  24. 24.
    Tagalakis V, Tamim H, Blostein M et al (2007) Use of warfarin and risk of urogenital cancer: a population-based, nested case-control study. Lancet Oncol 8:395–402PubMedGoogle Scholar
  25. 25.
    Lazo-Langner A, Goss GD, Spaans JN et al (2007) The effect of low-molecular-weight heparin on cancer survival. A systematic review and meta-analysis of randomized trials. J Thromb Haemost 5:729–737PubMedGoogle Scholar
  26. 26.
    Altinbas M, Coskun HS, Er O et al (2004) A randomized clinical trial of combination chemotherapy with and without low-molecular-weight heparin in small cell lung cancer. J Thromb Haemost 2:1266–1271PubMedGoogle Scholar
  27. 27.
    Kakkar AK, Levine MN, Kadziola Z et al (2004) Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol 22:1944–1948PubMedGoogle Scholar
  28. 28.
    Klerk CP, Smorenburg SM, Otten HM et al (2005) The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol 23:2130–2135PubMedGoogle Scholar
  29. 29.
    Lee A, Levine M (2005) Treatment of venous thromboembolism in cancer patients. Cancer Control 12(Suppl 1):17–21PubMedGoogle Scholar
  30. 30.
    Edgington TS, Mackman N, Brand K et al (1991) The structural biology of expression and function of tissue factor. Thromb Haemost 66:67–79PubMedGoogle Scholar
  31. 31.
    Nemerson Y (1995) Tissue factor: then and now. Thromb Haemost 74:180–184PubMedGoogle Scholar
  32. 32.
    Lopez-Pedrera C, Barbarroja N, Dorado G et al (2006) Tissue factor as an effector of angiogenesis and tumor progression in hematological malignancies. Leukemia 20:1331–1340PubMedGoogle Scholar
  33. 33.
    Varki A (2007) Trousseau’s syndrome: multiple definitions and multiple mechanisms. Blood 110:1723–1729PubMedGoogle Scholar
  34. 34.
    Czaykowski P, Hui D (2007) Chemotherapy in small bowel adenocarcinoma: 10-year experience of the British Columbia Cancer Agency. Clin Oncol (R Coll Radiol) 19:143–149Google Scholar
  35. 35.
    Miller KD, Sweeney CJ, Sledge GW Jr (2001) Redefining the target: chemotherapeutics as antiangiogenics. J Clin Oncol 19:1195–1206PubMedGoogle Scholar
  36. 36.
    Baz R, Li L, Kottke-Marchant K et al (2005) The role of aspirin in the prevention of thrombotic complications of thalidomide and anthracycline-based chemotherapy for multiple myeloma. Mayo Clin Proc 80:1568–1574PubMedGoogle Scholar
  37. 37.
    Zangari M, Elice F, Fink L et al (2007) Thrombosis in multiple myeloma. Expert Rev Anticancer Ther 7:307–315PubMedGoogle Scholar
  38. 38.
    Sousou T, Khorana A (2009) Identifying cancer patients at risk for venous thromboembolism. Hamostaseologie 29:121–124PubMedGoogle Scholar
  39. 39.
    Yusuf SW, Razeghi P, Yeh ET (2008) The diagnosis and management of cardiovascular disease in cancer patients. Curr Probl Cardiol 33:163–196PubMedGoogle Scholar
  40. 40.
    Agnelli G, Bolis G, Capussotti L et al (2006) A clinical outcome-based prospective study on venous thromboembolism after cancer surgery: the @RISTOS project. Ann Surg 243:89–95PubMedGoogle Scholar
  41. 41.
    Lin J, Wakefield TW, Henke PK (2006) Risk factors associated with venous thromboembolic events in patients with malignancy. Blood Coagul Fibrinolysis 17:265–270PubMedGoogle Scholar
  42. 42.
    Chew HK, Wun T, Harvey D et al (2006) Incidence of venous thromboembolism and its effect on survival among patients with common cancers. Arch Intern Med 166:458–464PubMedGoogle Scholar
  43. 43.
    Rodriguez AO, Wun T, Chew H et al (2007) Venous thromboembolism in ovarian cancer. Gynecol Oncol 105:784–790PubMedGoogle Scholar
  44. 44.
    Fotopoulou C, duBois A, Karavas AN et al (2008) Incidence of venous thromboembolism in patients with ovarian cancer undergoing platinum/paclitaxel-containing first-line chemotherapy: an exploratory analysis by the Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group. J Clin Oncol 26:2683–2689PubMedGoogle Scholar
  45. 45.
    Chew HK, Wun T, Harvey DJ et al (2007) Incidence of venous thromboembolism and the impact on survival in breast cancer patients. J Clin Oncol 25:70–76PubMedGoogle Scholar
  46. 46.
    Alcalay A, Wun T, Khatri V et al (2006) Venous thromboembolism in patients with colorectal cancer: incidence and effect on survival. J Clin Oncol 24:1112–1118PubMedGoogle Scholar
  47. 47.
    Chew HK, Davies AM, Wun T et al (2008) The incidence of venous thromboembolism among patients with primary lung cancer. J Thromb Haemost 6:601–608PubMedGoogle Scholar
  48. 48.
    Ramacciotti E, Wolosker N, Puech-Leao P et al (2003) Prevalence of factor V Leiden, FII G20210A, FXIII Val34Leu and MTHFR C677T polymorphisms in cancer patients with and without venous thrombosis. Thromb Res 109:171–174PubMedGoogle Scholar
  49. 49.
    Kennedy M, Andreescu AC, Greenblatt MS et al (2005) Factor V Leiden, prothrombin 20210A and the risk of venous thrombosis among cancer patients. Br J Haematol 128:386–388PubMedGoogle Scholar
  50. 50.
    Kröger K, Weiland D, Ose C et al (2006) Risk factors for venous thromboembolic events in cancer patients. Ann Oncol 17:297–303PubMedGoogle Scholar
  51. 51.
    Samama MM (2000) An epidemiologic study of risk factors for deep vein thrombosis in medical outpatients: the Sirius study. Arch Intern Med 160:3415–3420PubMedGoogle Scholar
  52. 52.
    Prandoni P, Lensing AW, Cogo A et al (1996) The long-term clinical course of acute deep venous thrombosis. Ann Intern Med 125:1–7PubMedGoogle Scholar
  53. 53.
    Sallah S, Wan JY, Nguyen NP (2002) Venous thrombosis in patients with solid tumors: determination of frequency and characteristics. Thromb Haemost 87:575–579PubMedGoogle Scholar
  54. 54.
    Heit JA, Silverstein MD, Mohr DN et al (2000) Risk factors for deep vein thrombosis and pulmonary embolism: a population-based case–control study. Arch Intern Med 160:809–815PubMedGoogle Scholar
  55. 55.
    Heit JA, O’Fallon WM, Petterson TM et al (2002) Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study. Arch Intern Med 162:1245–1248PubMedGoogle Scholar
  56. 56.
    Goldschmidt N, Linetsky E, Shalom E et al (2003) High incidence of thromboembolism in patients with central nervous system lymphoma. Cancer 98:1239–1242PubMedGoogle Scholar
  57. 57.
    Blom JW, Vanderschoot JP, Oostindier MJ et al (2006) Incidence of venous thrombosis in a large cohort of 66,329 cancer patients: results of a record linkage study. J Thromb Haemost 4:529–535PubMedGoogle Scholar
  58. 58.
    Pritchard KI, Paterson AH, Paul NA et al (1996) Increased thromboembolic complications with concurrent tamoxifen and chemotherapy in a randomized trial of adjuvant therapy for women with breast cancer National Cancer Institute of Canada Clinical Trials Group Breast Cancer Site Group. J Clin Oncol 14:2731–2737PubMedGoogle Scholar
  59. 59.
    Palumbo A, Rajkumar SV, Dimopoulos MA et al (2008) Prevention of thalidomide- and lenalidomide-associated thrombosis in myeloma. Leukemia 22:414–423PubMedGoogle Scholar
  60. 60.
    Khorana AA, Francis CW, Culakova E et al (2007) Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost 5:632–634PubMedGoogle Scholar
  61. 61.
    Fisher B, Dignam J, Wolmark N et al (1997) Tamoxifen and chemotherapy for lymph node-negative, estrogen receptor-positive breast cancer. J Natl Cancer Inst 89:1673–1682PubMedGoogle Scholar
  62. 62.
    Deitcher SR, Gomes MP (2004) The risk of venous thromboembolic disease associated with adjuvant hormone therapy for breast carcinoma: a systematic review. Cancer 101:439–449PubMedGoogle Scholar
  63. 63.
    Coombes RC, Hall E, Gibson LJ et al (2004) A randomized trial of exemestane after two to three years of tamoxifen therapy in postmenopausal women with primary breast cancer. N Engl J Med 350:1081–1092PubMedGoogle Scholar
  64. 64.
    Rajkumar SV, Gertz MA, Lacy MQ et al (2003) Thalidomide as initial therapy for early-stage myeloma. Leukemia 17:775–779PubMedGoogle Scholar
  65. 65.
    Rajkumar SV, Blood E, Vesole D, Fonseca R, Greipp PR, Eastern Cooperative Oncology Group (2006) Phase III clinical trial of thalidomide plus dexamethasone compared with dexamethasone alone in newly diagnosed multiple myeloma: a clinical trial coordinated by the Eastern Cooperative Oncology Group. J Clin Oncol 24(3):431–436PubMedGoogle Scholar
  66. 66.
    Rajkumar SV, Rosiñol L, Hussein M, Catalano J, Jedrzejczak W, Lucy L, Olesnyckyj M, Yu Z, Knight R, Zeldis JB, Bladé J (2008) Multicenter, randomized, double-blind, placebo-controlled study of thalidomide plus dexamethasone compared with dexamethasone as initial therapy for newly diagnosed multiple myeloma. J Clin Oncol 26(13):2171–2177PubMedGoogle Scholar
  67. 67.
    Kabbinavar F, Hurwitz HI, Fehrenbacher L et al (2003) Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21:60–65PubMedGoogle Scholar
  68. 68.
    Menon SP, Rajkumar SV, Lacy M, Falco P, Palumbo A (2008) Thromboembolic events with lenalidomide-based therapy for multiple myeloma. Cancer 112(7):1522–1528PubMedGoogle Scholar
  69. 69.
    Hurwitz H, Fehrenbacher L, Novotny W et al (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350:2335–2342PubMedGoogle Scholar
  70. 70.
    Scappaticci FA, Skillings JR, Holden SN et al (2007) Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab. J Natl Cancer Inst 99:1232–1239PubMedGoogle Scholar
  71. 71.
    Moore MJ, Goldstein D, Hamm J, Figer A, Hecht JR, Gallinger S, Au HJ, Murawa P, Walde D, Wolff RA, Campos D, Lim R, Ding K, Clark G, Voskoglou-Nomikos T, Ptasynski M, Parulekar W, National Cancer Institute of Canada Clinical Trials Group (2007) Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 25:1960–1966PubMedGoogle Scholar
  72. 72.
    Duvic M, Talpur R, Ni X et al (2007) Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 109:31–39PubMedGoogle Scholar
  73. 73.
    Verso M, Agnelli G (2003) Venous thromboembolism associated with long-term use of central venous catheters in cancer patients. J Clin Oncol 21:3665–3675PubMedGoogle Scholar
  74. 74.
    Verso M, Agnelli G, Bertoglio S et al (2005) Enoxaparin for the prevention of venous thromboembolism associated with central vein catheter: a double-blind, placebo-controlled, randomized study in cancer patients. J Clin Oncol 23:4057–4062PubMedGoogle Scholar
  75. 75.
    Lee AY, Levine MN, Butler G et al (2006) Incidence, risk factors, and outcomes of catheter-related thrombosis in adult patients with cancer. J Clin Oncol 24:1404–1408PubMedGoogle Scholar
  76. 76.
    Bohlius J, Wilson J, Seidenfeld J et al (2006) Recombinant human erythropoietins and cancer patients: updated meta-analysis of 57 studies including 9353 patients. J Natl Cancer Inst 98:708–714PubMedCrossRefGoogle Scholar
  77. 77.
    Khorana AA, Kuderer NM, Culakova E et al (2008) Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 111:4902–4907PubMedGoogle Scholar
  78. 78.
    Westin SN, Skinner EN, Jonsson Funk M et al (2007) Incidence of symptomatic deep venous thrombosis with epoetin alfa or darbepoetin alfa treatment of anemia in patients with ovarian or primary peritoneal cancer. Gynecol Oncol 105:414–417PubMedGoogle Scholar
  79. 79.
    Khorana AA, Francis CW, Culakova E et al (2005) Risk factors for chemotherapy-associated venous thromboembolism in a prospective observational study. Cancer 104:2822–2829PubMedGoogle Scholar
  80. 80.
    Simanek R. Vormittag R, Alguel G, Ay C, Dunkler D, Quehenberger P, Zielinski C, Jaeger U, Pabinger I (2007) A high platelet coung independently predicts venous thromboembolism in cancer patients. J Thromb Haemost 5:abstract PT497Google Scholar
  81. 81.
    Falanga A, Levine MN, Consonni R et al (1998) The effect of very-low-dose warfarin on markers of hypercoagulation in metastatic breast cancer: results from a randomized trial. Thromb Haemost 79:23–27PubMedGoogle Scholar
  82. 82.
    Sallah S, Husain A, Sigounas V et al (2004) Plasma coagulation markers in patients with solid tumors and venous thromboembolic disease receiving oral anticoagulation therapy. Clin Cancer Res 10:7238–7243PubMedGoogle Scholar
  83. 83.
    Ay C, Simanek R, Vormittag R et al (2008) High plasma levels of soluble P-selectin are predictive of venous thromboembolism in cancer patients: results from the Vienna Cancer and Thrombosis Study (CATS). Blood 112:2703–2708PubMedGoogle Scholar
  84. 84.
    Leizorovicz A, Cohen AT, Turpie AG et al (2004) Randomized, placebo-controlled trial of dalteparin for the prevention of venous thromboembolism in acutely ill medical patients. Circulation 110:874–879PubMedGoogle Scholar
  85. 85.
    Cohen AT, Davidson BL, Gallus AS et al (2006) Efficacy and safety of fondaparinux for the prevention of venous thromboembolism in older acute medical patients: randomised placebo controlled trial. BMJ 332:325–329PubMedGoogle Scholar
  86. 86.
    Geerts WH, Pineo GF, Heit JA et al (2004) Prevention of venous thromboembolism: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest 126:338S–400SPubMedGoogle Scholar
  87. 87.
    Nicolaides AN, Fareed J, Kakkar AK, Breddin HK, Goldhaber SZ, Hull R, Kakkar VV, Michiels JJ, Myers K, Samama M, Sasahara A, Kalodiki E (2006) Prevention and treatment of venous thromboembolism. International Consensus Statement (guidelines according to scientific evidence). Int Angiol 25(2):101–161Google Scholar
  88. 88.
    Hull RD, Pineo GF, Brant RF et al (2006) Long-term low-molecular-weight heparin versus usual care in proximal-vein thrombosis patients with cancer. Am J Med 119:1062–1072PubMedGoogle Scholar
  89. 89.
    Lyman GH, Khorana AA, Falanga A et al (2007) American Society of Clinical Oncology guideline: recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer. J Clin Oncol 25:5490–5505PubMedGoogle Scholar
  90. 90.
    Mandala M, Falanga A, Roila F (2008) Management of venous thromboembolism in cancer patients: ESMO clinical recommendations. Ann Oncol 19(suppl 2):ii126–ii127PubMedGoogle Scholar
  91. 91.
    Mandala M, Falanga A, Piccioli A et al (2006) Venous thromboembolism and cancer: guidelines of the Italian Association of Medical Oncology (AIOM). Crit Rev Oncol Hematol 59:194–204PubMedGoogle Scholar
  92. 92.
    Wagman LD, Baird MF, Bennett CL et al (2006) Venous thromboembolic disease: clinical practice guidelines in oncology. J Natl Compr Canc Netw 4:838–869PubMedGoogle Scholar
  93. 93.
    Samama MM, Cohen AT, Darmon JY et al (1999) A comparison of enoxaparin with placebo for the prevention of venous thromboembolism in acutely ill medical patients: Prophylaxis in Medical Patients with Enoxaparin Study Group. N Engl J Med 341:793–800PubMedGoogle Scholar
  94. 94.
    Alikhan R, Cohen AT, Combe S et al (2004) Risk factors for venous thromboembolism in hospitalized patients with acute medical illness: analysis of the MEDENOX Study. Arch Intern Med 164:963–968PubMedGoogle Scholar
  95. 95.
    Gärdlund B (1996) Randomised, controlled trial of low-dose heparin for prevention of fatal pulmonary embolism in patients with infectious diseases: The Heparin Prophylaxis Study Group. Lancet 347:1357–1361PubMedGoogle Scholar
  96. 96.
    Mismetti P, Laporte-Simitsidis S, Tardy B et al (2000) Prevention of venous thromboembolism in internal medicine with unfractionated or low-molecular weight heparins: a meta-analysis of randomized clinical trials. Thromb Haemost 83:14–19PubMedGoogle Scholar
  97. 97.
    Levine M, Hirsh J, Gent M et al (1994) Double blind randomised trial of a very-low-dose warfarin for prevention of thromboembolism in stage IV breast cancer. Lancet 343:886–889PubMedGoogle Scholar
  98. 98.
    Deheinzelin D, Braga AL, Martins LC et al (2006) Incorrect use of thromboprophylaxis for venous thromboembolism in medical and surgical patients: results of a multicentric, observational and cross-sectional study in Brazil. J Thromb Haemost 4(6):1266–1270PubMedGoogle Scholar
  99. 99.
    Lee AY (2009) Treatment of venous thromboembolism in cancer patients. Best Pract Res Clin Haematol 22:93–101PubMedGoogle Scholar
  100. 100.
    Baglin TP, Keeling DM, Watson HG (2006) Guidelines on oral anticoagulation (warfarin): third edition—2005 update. Br J Haematol 132:277–285PubMedGoogle Scholar
  101. 101.
    Palareti G, Legnani C, Lee A et al (2000) A comparison of the safety and efficacy of oral anticoagulation for the treatment of venous thromboembolic disease in patients with or without malignancy. Thromb Haemost 84:805–810PubMedGoogle Scholar
  102. 102.
    Prandoni P, Lensing AW, Piccioli A et al (2002) Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 100:3484–3488PubMedGoogle Scholar
  103. 103.
    Hutten BA, Prins MH, Gent M et al (2000) 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 18:3078–3083PubMedGoogle Scholar
  104. 104.
    Meyer G, Marjanovic Z, Valcke J et al (2002) Comparison of low-molecular-weight heparin and warfarin for the secondary prevention of venous thromboembolism in patients with cancer: a randomized controlled study. Arch Intern Med 162:1729–1735PubMedGoogle Scholar
  105. 105.
    Segal JB, Streiff MB, Hofmann LV et al (2007) Management of venous thromboembolism: a systematic review for a practice guideline. Ann Intern Med 146:211–222PubMedGoogle Scholar
  106. 106.
    Buller HR, Agnelli G, Hull RD et al (2004) Antithrombotic therapy for venous thromboembolic disease: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest 126:401S–428SPubMedGoogle Scholar
  107. 107.
    Kearon C, Kahn SR, Agnelli G et al (2008) Antithrombotic therapy for venous thromboembolic disease: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 133:454S–545SPubMedGoogle Scholar
  108. 108.
    Hirsh J, Bauer KA, Donati MB et al (2008) Parenteral anticoagulants: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 133:141S–159SPubMedGoogle Scholar
  109. 109.
    Buller HR, Davidson BL, Decousus H et al (2003) Subcutaneous fondaparinux versus intravenous unfractionated heparin in the initial treatment of pulmonary embolism. N Engl J Med 349:1695–1702PubMedGoogle Scholar
  110. 110.
    Warkentin TE, Greinacher A, Koster A et al (2008) Treatment and prevention of heparin-induced thrombocytopenia: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Edition). Chest 133:340S–380SPubMedGoogle Scholar
  111. 111.
    Noble SI, Shelley MD, Coles B et al (2008) Management of venous thromboembolism in patients with advanced cancer: a systematic review and meta-analysis. Lancet Oncol 9:577–584PubMedGoogle Scholar
  112. 112.
    Louzada ML, Majeed H, Wells PS (2009) Efficacy of low-molecular-weight-heparin versus vitamin K antagonists for long term treatment of cancer-associated venous thromboembolism in adults: a systematic review of randomized controlled trials. Thromb Res 123:837–844PubMedGoogle Scholar
  113. 113.
    Decousus H, Leizorovicz A, Parent F et al (1998) A clinical trial of vena caval filters in the prevention of pulmonary embolism in patients with proximal deep vein thrombosis: Prevention du Risque d’Embolie Pulmonaire par Interruption Cave Study Group. N Engl J Med 338:409–415PubMedGoogle Scholar
  114. 114.
    PREPIC Study Group (2005) Eight-year follow-up of patients with permanent vena cava filters in the prevention of pulmonary embolism: The PREPIC (Prevention du Risque d’Embolie Pulmonaire par Interruption Cave) randomized study. Circulation 112:416–422Google Scholar
  115. 115.
    Khorana AA, Rao MV (2007) Approaches to risk-stratifying cancer patients for venous thromboembolism. Thromb Res 120(Suppl 2):S41–S50PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Celso Arrais Rodrigues
    • 1
  • Renata Ferrarotto
    • 1
  • Roberto Kalil Filho
    • 2
  • Yana A. S. Novis
    • 1
  • Paulo M. G. Hoff
    • 1
  1. 1.Centro de OncologiaHospital Sirio LibanêsSão PauloBrazil
  2. 2.Centro de CardiologiaHospital Sirio LibanêsSão PauloBrazil

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