Cancer, clots and consensus: New understanding of an old problem

Journal of Clinical Oncology

Volumn 27, Issue 29, 2009, Pages 4821-4826

  Lyman, Gary H ^a   Khorana, Alok A ^b  

^a DUKE CANCER INSTITUTE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT AGENT; ANTINEOPLASTIC AGENT; ANTIVITAMIN K; BEVACIZUMAB; DALTEPARIN; DEXAMETHASONE; ENOXAPARIN; FONDAPARINUX; HEPARIN; LENALIDOMIDE; LOW MOLECULAR WEIGHT HEPARIN; THALIDOMIDE; TINZAPARIN; WARFARIN;

ARTERY THROMBOSIS; BLEEDING; BLOOD CLOTTING; CANCER PATIENT; CANCER SURVIVAL; CLINICAL TRIAL; DEEP VEIN THROMBOSIS; HIGH RISK PATIENT; HUMAN; HYPERCOAGULABILITY; LOW DRUG DOSE; LUNG EMBOLISM; MULTIPLE CYCLE TREATMENT; MULTIPLE MYELOMA; PRIORITY JOURNAL; REVIEW; SOLID TUMOR; VEIN THROMBOSIS; VENOUS THROMBOEMBOLISM; EVIDENCE BASED MEDICINE; FEMALE; FORECASTING; MALE; MORTALITY; NEOPLASM; PATHOLOGY; PRACTICE GUIDELINE; PRIMARY PREVENTION; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL; RISK ASSESSMENT; STANDARD; SURVIVAL;

ANTICOAGULANTS; EVIDENCE-BASED MEDICINE; FEMALE; FORECASTING; HUMANS; MALE; NEOPLASMS; PRACTICE GUIDELINES AS TOPIC; PRIMARY PREVENTION; PROGNOSIS; PULMONARY EMBOLISM; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK ASSESSMENT; SURVIVAL ANALYSIS; VENOUS THROMBOSIS;

EID: 70350708358     PISSN: 0732183X     EISSN: None     Source Type: Journal    
DOI: 10.1200/JCO.2009.22.3032     Document Type: Review

References (105)

1. Khorana AA: Malignancy, thrombosis and Trousseau: The case for an eponym. J Thromb Haemost1:2463-2465, 2003
2. Brotman DJ, Deitcher SR, Lip GY, Matzdorff AC: Virchow's triad revisited. South Med J 97:213-214, 2004
3. Lyman GH, Bettigole RE, Robson E, et al: Fibrinogen kinetics in patients with neoplastic disease. Cancer Mar 41:1113-1122, 1978
4. Bluff JE, Brown NJ, Reed MW, et al: Tissue factor, angiogenesis and tumour progression. Breast Cancer Res 10:204, 2008
5. Winter PC: The pathogenesis of venous thromboembolism in cancer: Emerging links with tumour biology. Hematol Oncol 24:126-133, 2006
6. Bobek V, Kovarik J: Antitumor and antimetastatic effect of warfarin and heparins. Biomed Pharmacother 58:213-219, 2004
7. Hejna M, Raderer M, Zielinski CC: Inhibition of metastases by anticoagulants. J Natl Cancer Inst 91:22-36, 1999
8. ten Cate H, Falanga A: The pathophysiology of cancer and thrombosis: Summary and conclusions. Pathophysiol Haemost Thromb 36:212-214, 2008
9. Falanga A: The incidence and risk of venous thromboembolism associated with cancer and nonsurgical cancer treatment. Cancer Invest 27:105-115, 2009
10. Furie B, Furie BC: Mechanisms of thrombus formation. N Engl J Med 359:938-949, 2008
11. Boccaccio C, Comoglio P: Genetic link between cancer and thrombosis. J Clin Oncol 27:4827-4833, 2009
12. Kasthuri RS, Mackman N, Taubman MB: Role of tissue factor in cancer. J Clin Oncol 27:4834-4838, 2009
13. Varki A: Trousseau's syndrome: Multiple definitions and multiple mechanisms. Blood 110:1723-1729, 2007
14. Prandoni P, Lensing AW, Buller HR, et al: Deep-vein thrombosis and the incidence of subsequent symptomatic cancer. N Engl J Med 327:1128-1133, 1992
15. Ambrus JL, Ambrus CM, Mink IB, et al: Causes of death in cancer patients. J Med 6:61-64, 1975
16. Khorana AA, Francis CW, Culakova E, et al: Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost 5:632-634, 2007
17. Shen VS, Pollak EW: Fatal pulmonary embolism in cancer patients: Is heparin prophylaxis justified? South Med J 73:841-843, 1980
18. Bullano MF, Willey V, Hauch O, et al: Longitudinal evaluation of health plan cost per venous thromboembolism or bleed event in patients with a prior venous thromboembolism event during hospitalization. J Manag Care Pharm 11:663-673, 2005
19. Elting LS, Escalante CP, Cooksley C, et al: Outcomes and cost of deep venous thrombosis among patients with cancer. Arch Intern Med 164:1653-1661, 2004
20. Lyman GH, Khorana AA, Falanga A, et al: American Society of Clinical Oncology guideline: Recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer. J Clin Oncol 25:5490-5505, 2007
21. Khorana AA, Kuderer NM, Culakova E, et al: Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 111:4902-4907, 2008
22. Kuderer NM, Khorana AA, Lyman GH, et al: A meta-analysis and systematic review of the efficacy and safety of anticoagulants as cancer treatment: Impact on survival and bleeding complications. Cancer 110:1149-1161, 2007
23. General US: Call to Action to Prevent Deep Vein Thrombosis and Pulmonary Embolism 2008. http://www.surgeongeneral.gov/topics/deepvein/
24. Geerts WH, Bergqvist D, Pineo GF, et al: Prevention of venous thromboembolism: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (ed 8). Chest 133:381S-453S, 2008 (suppl)
25. Falanga A, Marchetti M: Venous thromboembolism in the hematologic malignancies. J Clin Oncol 27:4848-4857, 2009
26. Francis CW: Clinical practice. Prophylaxis for thromboembolism in hospitalized medical patients. N Engl J Med 356:1438-1444, 2007
27. Khorana AA, Francis CW, Culakova E, et al: Thromboembolism in hospitalized neutropenic cancer patients. J Clin Oncol 24:484-490, 2006
28. Stein PD, Beemath A, Meyers FA, et al: Incidence of venous thromboembolism in patients hospitalized with cancer. Am J Med Jan 119:60-68, 2006
29. Dentali F, Douketis JD, Gianni M, et al: Meta-analysis: Anticoagulant prophylaxis to prevent symptomatic venous thromboembolism in hospitalized medical patients. Ann Intern Med 146:278-288, 2007
30. Khorana AA, Francis CW, Culakova E, et al: Frequency, risk factors, and trends for venous thromboembolism among hospitalized cancer patients. Cancer 110:2339-2346, 2007
31. Khorana AA: The NCCN Clinical Practice Guidelines on Venous Thromboembolic Disease: Strategies for improving VTE prophylaxis in hospitalized cancer patients. Oncologist 12:1361-1370, 2007
32. Levitan N, Dowlati A, Remick SC, et al: Rates of initial and recurrent thromboembolic disease among patients with malignancy versus those without malignancy. Risk analysis using Medicare claims data. Medicine (Baltimore) 78:285-291, 1999
33. Khorana AA, Francis CW, Culakova E, et al: Risk factors for chemotherapyassociated venous thromboembolism in a prospective observational study. Cancer 104:2822-2829, 2005
34. Shivakumar SP, Anderson DR, Couban S: Catheter-associated thrombosis in patients with malignancy. J Clin Oncol 27:4858-4864, 2009
35. Gosselin MV, Rubin GD, Leung AN, et al: Unsuspected pulmonary embolism: Prospective detection on routine helical CT scans. Radiology 208:209-215, 1998
36. Storto ML, Di Credico A, Guido F, et al: Incidental detection of pulmonary emboli on routine MDCT of the chest. Am J Roentgenol 184:264-267, 2005
37. Sebastian AJ, Paddon AJ: Clinically unsuspected pulmonary embolism - an important secondary finding in oncology CT. Clin Radiol 61:81-85, 2006
38. O'Connell CL, Boswell WD, Duddalwar V, et al: Unsuspected pulmonary emboli in cancer patients: Clinical correlates and relevance. J Clin Oncol 24:4928-4932, 2006
39. Cavo M, Zamagni E, Cellini C, et al: Deep-vein thrombosis in patients with multiple myeloma receiving first-line thalidomide-dexamethasone therapy. Blood 100:2272-2273, 2002
40. Kabbinavar F, Hurwitz HI, Fehrenbacher L, et al: Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21:60-65, 2003
41. Kuenen BC, Levi M, Meijers JC, et al: Potential role of platelets in endothelial damage observed during treatment with cisplatin, gemcitabine, and the angiogenesis inhibitor SU5416. J Clin Oncol 21:2192-2198, 2003
42. Zangari M: Thrombotic events in patients with cancer receiving antiangiogenesis agents. J Clin Oncol 27:4865-4873, 2009
43. Nalluri SR, Chu D, Keresztes R, et al: Risk of venous thromboembolism with the angiogenesis inhibitor bevacizumab in cancer patients: A meta-analysis. JAMA 300:2277-2285, 2008
44. Scappaticci FA, Skillings JR, Holden SN, et al: Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab. J Natl Cancer Inst 99:1232-1239, 2007
45. Bohlius J, Wilson J, Seidenfeld J, et al: Recombinant human erythropoietins and cancer patients: Updated meta-analysis of 57 studies including 9353 patients. J Natl Cancer Inst 98:708-714, 2006
46. Khorana AA, Francis CW, Blumberg N, et al: Blood transfusions, thrombosis, and mortality in hospitalized patients with cancer. Arch Intern Med 168:2377-2381, 2008
47. Khorana AA, Connolly GC: Assessing risk of venous thromboembolism in the patient with cancer. J Clin Oncol 27:4839-4847, 2009
48. Alcalay A, Wun T, Khatri V, et al: Venous thromboembolism in patients with colorectal cancer: Incidence and effect on survival. J Clin Oncol 24:1112-1118, 2006
49. Chew HK, Wun T, Harvey D, et al: Incidence of venous thromboembolism and its effect on survival among patients with common cancers. Arch Intern Med 166:458-464, 2006
50. Chew HK, Wun T, Harvey DJ, et al: Incidence of venous thromboembolism and the impact on survival in breast cancer patients. J Clin Oncol 25:70-76, 2007
51. Sorensen HT, Mellemkjaer L, Olsen JH, et al: Prognosis of cancers associated with venous thromboembolism. N Engl J Med 343:1846-1850, 2000
52. Kuderer NM, Francis CW, Culakova E, et al: E. Venous thromboembolism represents a major risk factor for early all-cause mortality in patients receiving cancer chemotherapy. J Clin Oncol 26:506s, 2008 (abstr 9521)
53. Streiff MB: Diagnosis and initial treatment of venous thromboembolism in patients with cancer. J Clin Oncol 27:4889-4894, 2009
54. Prandoni P, Lensing AW, Piccioli A, et al: Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 100:3484-3488, 2002
55. Lee AY: Anticoagulation in the treatment of established venous thromboembolism in patients with cancer. J Clin Oncol 27:4895-4901, 2009
56. Francis CW: Prevention of venous thromboembolism in hospitalized patients with cancer. J Clin Oncol 27:4874-4880, 2009
57. Cohen AT, Davidson BL, Gallus AS, et al: Efficacy and safety of fondaparinux for the prevention of venous thromboembolism in older acute medical patients: Randomised placebo controlled trial. BMJ 332:325-329, 2006
58. Leizorovicz A, Cohen AT, Turpie AG, et al: Randomized, placebocontrolled trial of dalteparin for the prevention of venous thromboembolism in acutely ill medical patients. Circulation 110:874-879, 2004
59. Samama MM, Cohen AT, Darmon JY, et al: 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 341:793-800, 1999
60. Kakkar AK, Haas S, Wolf H, et al: Evaluation of perioperative fatal pulmonary embolism and death in cancer surgical patients: The MC-4 cancer substudy. Thromb Haemost 94:867-871, 2005
61. Kakkar A: Prevention of venous thromboembolism in the cancer surgical patient. J Clin Oncol 27:4881-4884, 2009
62. Leonardi MJ, McGory ML, Ko CY: A systematic review of deep venous thrombosis prophylaxis in cancer patients: implications for improving quality. Ann Surg Oncol 14:929-936, 2007
63. Rasmussen E, Wille-Jorgensen P, Jorgensen LN: Extended out-ofhospital low-molecular-weight heparin prophylaxis against venous thromboembolism in patients after cancer operations: A meta-analysis. ISTH 2005:abstract
64. Jorgensen LN, Lausen I, Rasmussen MS, et al: Prolonged thromboprophylaxis with low molecular weight heparin (tinzaparin) following major general surgery primarily for cancer: An individual patient data meta-analysis. J Thromb Haemost 2005 (suppl 1; abstr P1870)
65. Buller HR, Agnelli G, Hull RD, et al: Antithrombotic therapy for venous thromboembolic disease: The Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. Chest 126:401S-428S, 2004 (suppl)
66. Siragusa S, Cosmi B, Piovella F, et al: Low-molecular-weight heparins and unfractionated heparin in the treatment of patients with acute venous thromboembolism: Results of a meta-analysis. Am J Med 100:269-277, 1996
67. Hettiarachchi RJ, Smorenburg SM, Ginsberg J, et al: Do heparins do more than just treat thrombosis? The influence of heparins on cancer spread. Thromb Haemost 82:947-952, 1999
68. Conti S, Guercini F, Iorio A: Low-molecular-weight heparin and cancer survival: Review of the literature and pooled analysis of 1,726 patients treated for at least three months. Pathophysiol Haemost Thromb 33:197-201, 2003
69. Meyer G, Marjanovic Z, Valcke J, et al: Comparison of low-molecularweight heparin and warfarin for the secondary prevention of venous thromboembolism in patients with cancer: A randomized controlled study. Arch Intern Med 162:1729-1735, 2002
70. Deitcher SR, Kessler CM, Merli G, et al: Secondary prevention of venous thromboembolic events (VTE) in patients with active malignancy: A randomized study of enoxaparin sodium alone vs. initial enoxaparin sodium followed by warfarin for a 180-day period. J Thromb Haemost 2003;1 (suppl 1; abstr OC194)
71. Lee AY, Levine MN, Baker RI, et al: Low-molecular-weight heparin versus a coumarin for the prevention of recurrent venous thromboembolism in patients with cancer. N Engl J Med 349:146-153, 2003
72. Hull RD, Pineo GF, Brant RF, et al: Self-managed long-term low-molecularweight heparin therapy: The balance of benefits and harms. Am J Med 120:72-82, 2007
73. Rana P, Levine M: Prevention of thrombosis in ambulatory patients with cancer. J Clin Oncol 27:4885-4888, 2009
74. Levine M, Hirsh J, Gent M, et al: Double-blind randomised trial of a very-low-dose warfarin for prevention of thromboembolism in stage IV breast cancer. Lancet 343:886-889, 1994
75. Agnelli G, Gussoni G, Bianchini C, et al: A randomized double-blind placebocontrolled study on nadroparin for prophylaxis of thromboembolic events in cancer patients receiving chemotherapy: The PROTECHT Study. Blood 112:6, 2008 (abstr 984)
76. Haas S, Kakkar A, Kemkes-Matthes B, et al: Prevention of venous thromboembolism with low-molecular-weight heparin in patients with metastatic breast or lung cancer: Results of the TOPIC studies. J Thromb Haemost 2005 (abstr 0R059)
77. Kakkar AK, Levine MN, Kadziola Z, et al: Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: The fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol 22:1944-1948, 2004
78. Perry JR, Rogers L, Laperriere N, et al: PRODIGE: A phase III randomized placebo-controlled trial of thromboprophylaxis using dalteparin low molecular weight heparin (LMWH) in patients with newly diagnosed malignant glioma. J Clin Oncol 25(2011), 2007
79. Sideras K, Schaefer PL, Okuno SH, et al: Low-molecular-weight heparin in patients with advanced cancer: A phase 3 clinical trial. Mayo Clin Proc 81:758-767, 2006
80. Amin A, Stemkowski S, Lin J, et al: Thromboprophylaxis rates in US medical centers: Success or failure? J Thromb Haemost 5:1610-1616, 2007
81. Burleigh E, Wang C, Foster D, et al: Thromboprophylaxis in medically ill patients at risk for venous thromboembolism. Am J Health Syst Pharm 63:S23-S29, 2006 (suppl 6)
82. Kahn SR, Panju A, Geerts W, et al: Multicenter evaluation of the use of venous thromboembolism prophylaxis in acutely ill medical patients in Canada. Thromb Res 119:145-155, 2007
83. Kakkar AK, Levine M, Pinedo HM, et al: Venous thrombosis in cancer patients: Insights from the FRONTLINE survey. Oncologist 8:381-388, 2003
84. Seddighzadeh A, Shetty R, Goldhaber SZ: Venous thromboembolism in patients with active cancer. Thromb Haemost 98:656-661, 2007
85. Gerotziafas GT, Papageorgiou C, Hatmi M, et al: Clinical studies with anticoagulants to improve survival in cancer patients. Pathophysiol Haemost Thromb 36:204-211, 2008
86. Vestjens JH, Sassen S, Prins MH: Blood coagulation and cancer: Thrombosis and survival, clinical relevance and impact: An introduction. Pathophysiol Haemost Thromb 36:113-121, 2008
87. Castelli R, Porro F, Tarsia P: The heparins and cancer: Review of clinical trials and biological properties. Vasc Med 9:205-213, 2004
88. Cosgrove RH, Zacharski LR, Racine E, et al: Improved cancer mortality with low-molecular-weight heparin treatment: A review of the evidence. Semin Thromb Hemost 28:79-87, 2002
89. Kuderer NM, Ortel TL, Francis CW: Impact of venous thromboembolism and anticoagulation on cancer and cancer survival. J Clin Oncol 27:4902-4911, 2009
90. Zacharski LR, Henderson WG, Rickles FR, et al: Effect of warfarin anticoagulation on survival in carcinoma of the lung, colon, head and neck, and prostate: Final report of VA Cooperative study #75. Cancer 53:2046-2052, 1984
91. Chahinian AP, Propert KJ, Ware JH, et al: A randomized trial of anticoagulation with warfarin and of alternating chemotherapy in extensive small-cell lung cancer by the Cancer and Leukemia Group B. J Clin Oncol 7:993-1002, 1989
92. Maurer LH, Herndon JE Jr, Hollis DR, et al: Randomized trial of chemotherapy and radiation therapy with or without warfarin for limited-stage small-cell lung cancer: A Cancer and Leukemia Group B study. J Clin Oncol 15:3378-3387, 1997
93. Lebeau B, Chastang C, Brechot JM, et al: Subcutaneous heparin treatment increases survival in small cell lung cancer: "Petites Cellules" Group. Cancer 74:38-45, 1994
94. Lazo-Langner A, Goss GD, Spaans JN, et al: The effect of low-molecularweight heparin on cancer survival: A systematic review and meta-analysis of randomized trials. J Thromb Haemost 5:729-737, 2007
95. Tagalakis V, Blostein M, Robinson-Cohen C, et al: The effect of anticoagulants on cancer risk and survival: Systematic review. Cancer Treat Rev 33:358-368, 2007
96. Akl EA, van Doormaal FF, Barba M, et al: Parenteral anticoagulation may prolong the survival of patients with limited small cell lung cancer: A Cochrane systematic review. J Exp Clin Cancer Res 27:4, 2008
97. Altinbas M, Coskun HS, Er O, et al: A randomized clinical trial of combination chemotherapy with and without low-molecular-weight heparin in small cell lung cancer. J Thromb Haemost 2:1266-1271, 2004
98. Klerk CP, Smorenburg SM, Otten HM, et al: The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol 23:2130-2135, 2005
99. Wagman LD, Baird MF, Bennett CL, et al: Venous thromboembolic disease: NCCN Clinical practice guidelines in oncology. J Natl Compr Canc Netw 6:716-753, 2008
100. Debourdeau P, Farge-Bancel D, Bosquet L, et al: 2008 Standards, options: Recommendations for venous thromboembolic events (VTE) treatment and central venous catheter thrombosis (CVCT) management in cancer patients. Bull Cancer 95:750-761, 2008
101. Di Minno G, Tufano A: Venous thromboembolism in oncologic patients: Guidelines for prevention and therapy and areas of uncertainty. Tumori 92:1-15, 2006 (suppl)
102. Mandala M, Falanga A, Roila F: Management of venous thromboembolism in cancer patients: ESMO clinical recommendations. Ann Oncol 19:ii126-ii127, 2008 (suppl 2)
103. Khorana AA, Streiff MB, Farge D, et al: Venous thromboembolism prophylaxis and treatment in cancer: A consensus statement of major guidelines panels and call to action. J Clin Oncol 27:4919-4926, 2009
104. Levine M: New antithrombotic drugs: Potential for use in oncology. J Clin Oncol 27:4912-4918, 2009
105. Somerfield MR, Einhaus K, Hagerty KL, et al: American Society of Clinical Oncology clinical practice guidelines: Opportunities and challenges. J Clin Oncol 26:4022-4026, 2008