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Thromb Haemost 2016; 116(04): 618-625
DOI: 10.1160/TH16-04-0302
Theme Issue Article
Schattauer GmbH

Clinical practice guidelines for prophylaxis of venous thomboembolism in cancer patients

Corinne Frere
1   Assistance Publique Hôpitaux de Marseille, Timone Hospital, Service d’Hematologie biologique, Marseille; Aix-Marseille Université, INSERM UMRS 1076, VRCM, Marseille, France
,
Dominique Farge
2   Assistance Publique-Hôpitaux de Paris, Saint-Louis Hospital, Internal Medicine: Autoimmune and and Vascular Diseases Unit, UF 04, Paris; INSERM UMRS 1160, Paris 7 Diderot University, Sorbonne Paris Cité, Paris, France
› Author Affiliations
Further Information

Publication History

Received: 17 April 2016

Accepted after minor revision: 12 August 2016

Publication Date:
20 November 2017 (online)

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Summary

Symptomatic venous thromboembolism (VTE) occurs 4-7 times more frequently in cancer patients as compared to non-cancer patients. A significant number of risk factors, which can be subcategorised as patient-, cancer- or treatment-related, have been shown to influence the risk of VTE during malignancy and further incorporated in risk-assessment models. Safe and efficient thromboprophylaxis regimens allow substantial decreased in VTE rates, since VTE is most often a largely preventable disease, but thromboprophylaxis remains underused in cancer compared to non-cancer patients. If thromboprophylaxis is warranted in cancer patients undergoing surgery or hospitalised for acute medical illness or with a lower mobility in the absence of contraindications to anticoagulants, its benefit remains controversial in outpatients and may be limited to locally advanced or metastatic pancreatic or lung cancer treated with chemotherapy. The International Initiative on Thrombosis and Cancer-CME free mobile app (ios and android), based on the International Clinical Practice Guidelines (CPG), facilitates their implementation and dissemination of knowledge worldwide so as to improve VTE treatment and prophylaxis in cancer patients.

Keywords

Venous thromboembolism - prophylaxis - anticoagulants - current clinical practice guidelines - risk assessment
 

  • References

  • 1 Timp JF. et al. Epidemiology of cancer-associated venous thrombosis. Blood 2013; 122: 1712-1723.
    CrossrefPubMedGoogle Scholar
  • 2 Khorana AA. et al. Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost 2007; 05: 632-634.
    CrossrefPubMedGoogle Scholar
  • 3 Khorana AA. et al. Health care costs associated with venous thromboembolism in selected high-risk ambulatory patients with solid tumors undergoing chemotherapy in the United States. Clin Outcomes Res CEOR 2013; 05: 101-108.
    PubMedGoogle Scholar
  • 4 Falanga A, Zacharski L.. Deep vein thrombosis in cancer: the scale of the problem and approaches to management. Ann Oncol Off J Eur Soc Med Oncol ESMO 2005; 16: 696-701.
    CrossrefPubMedGoogle Scholar
  • 5 Farge-Bancel D. et al Implementing thrombosis guidelines in cancer patients: a review. Rambam Maimonides Med J 2014; 05: e0041.
    CrossrefPubMedGoogle Scholar
  • 6 Mandalà M. et al Management of venous thromboembolism (VTE) in cancer patients: ESMO Clinical Practice Guidelines. Ann Oncol Off J Eur Soc Med Oncol ESMO 2011; 22 (06) vi 85-92.
    PubMedGoogle Scholar
  • 7 Mandalà M. et al Venous thromboembolism and cancer: guidelines of the Italian Association of Medical Oncology (AIOM). Crit Rev Oncol Hematol 2006; 59: 194-204.
    CrossrefPubMedGoogle Scholar
  • 8 Farge D. et al. 2008 French national guidelines for the treatment of venous thromboembolism in patients with cancer: report from the working group. Crit Rev Oncol Hematol 2010; 73: 31-46.
    CrossrefPubMedGoogle Scholar
  • 9 Debourdeau P. et al. 2008 SOR guidelines for the prevention and treatment of thrombosis associated with central venous catheters in patients with cancer: report from the working group. Ann Oncol Off J Eur Soc Med Oncol ESMO 2009; 20: 1459-1471.
    CrossrefPubMedGoogle Scholar
  • 10 Noble SIR. et al. Management of venous thromboembolism in patients with advanced cancer: a systematic review and meta-analysis. Lancet Oncol 2008; 09: 577-584.
    CrossrefPubMedGoogle Scholar
  • 11 Watson HG. et al. Guideline on aspects of cancer-related venous thrombosis. Br J Haematol 2015; 170: 640-648.
    CrossrefPubMedGoogle Scholar
  • 12 Khorana AA. et al. Guidance for the prevention and treatment of cancer-associated venous thromboembolism. J Thromb Thrombolysis 2016; 41: 81-91.
    CrossrefPubMedGoogle Scholar
  • 13 Easaw JC. et al. Canadian consensus recommendations on the management of venous thromboembolism in patients with cancer. Part 1: prophylaxis. Curr Oncol Tor Ont 2015; 22: 133-143.
    PubMedGoogle Scholar
  • 14 Easaw JC. et al. Canadian consensus recommendations on the management of venous thromboembolism in patients with cancer. Part 2: treatment. Curr Oncol Tor Ont 2015; 22: 144-155.
    PubMedGoogle Scholar
  • 15 Lyman GH. et al. American Society of Clinical Oncology guideline: recommendations for venous thromboembolism prophylaxis and treatment in patients with cancer. J Clin Oncol Off J Am Soc Clin Oncol 2007; 25: 5490-5505.
    CrossrefPubMedGoogle Scholar
  • 16 Lyman GH. et al. Venous Thromboembolism Prophylaxis and Treatment in Patients With Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update. J Clin Oncol. 2013 JCO.2013.49.1118.
    PubMedGoogle Scholar
  • 17 Lyman GH. et al. Venous Thromboembolism Prophylaxis and Treatment in Patients With Cancer: American Society of Clinical Oncology Clinical Practice Guideline Update 2014. J Clin Oncol. 2015 JCO.2014.59.7351.
    PubMedGoogle Scholar
  • 18 Geerts WH. et al. Prevention of venous thromboembolism: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th Ed). Chest 2008; 133: 381S-453S.
    CrossrefPubMedGoogle Scholar
  • 19 Kearon C. 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: e419S-94S.
    CrossrefPubMedGoogle Scholar
  • 20 Kearon C. et al. Antithrombotic Therapy for VTE Disease: CHEST Guideline and Expert Panel Report. Chest 2016; 149: 315-352.
    CrossrefPubMedGoogle Scholar
  • 21 Di Nisio M. et al Prevention of venous thromboembolism in hospitalized medical cancer patients: guidance from the SSC of the ISTH. J Thromb Haemost 2014; 12: 1746-1749.
    CrossrefPubMedGoogle Scholar
  • 22 Carrier M. et al. Management of challenging cases of patients with cancer-associated thrombosis including recurrent thrombosis and bleeding: guidance from the SSC of the ISTH. J Thromb Haemost 2013; 11: 1760-1765.
    CrossrefPubMedGoogle Scholar
  • 23 Zwicker JI. et al. Catheter-associated deep vein thrombosis of the upper extremity in cancer patients: guidance from the SSC of the ISTH. J Thromb Haemost 2014; 12: 796-800.
    CrossrefPubMedGoogle Scholar
  • 24 NCC Guidelines for Cancer-Associated Venous Thromboembolic disease [Internet]. 2016 [cited 2016 Jan 1]. Available from: https://www.nccn.org/store/login/login.aspx?ReturnURL=http://www.nccn.org/professionals/physician_gls/pdf/vte.pdf
    PubMedGoogle Scholar
  • 25 Streiff MB, Holmstrom B, Ashrani A. et al. Cancer-Associated Venous Thromboembolic Disease, Version 1.2015. J Natl Compr Cancer Netw 2015; 13: 1079-1095.
    CrossrefPubMedGoogle Scholar
  • 26 Farge D. et al. International clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer. J Thromb Haemost 2013; 11: 56-70.
    CrossrefPubMedGoogle Scholar
  • 27 Debourdeau P. et al. International clinical practice guidelines for the treatment and prophylaxis of thrombosis associated with central venous catheters in patients with cancer. J Thromb Haemost 2013; 11: 71-80.
    CrossrefPubMedGoogle Scholar
  • 28 Heit JA.. Epidemiology of venous thromboembolism. Nat Rev Cardiol 2015; 12: 464-474.
    CrossrefPubMedGoogle Scholar
  • 29 Connolly GC, Francis CW.. Cancer-associated thrombosis. Hematol Educ Program Am Soc Hematol Am Soc Hematol Educ Program 2013; 2013: 684-691.
    PubMedGoogle Scholar
  • 30 Streiff MB.. Association between cancer types, cancer treatments, and venous thromboembolism in medical oncology patients. Clin Adv Hematol Oncol 2013; 11: 349-357.
    PubMedGoogle Scholar
  • 31 Khorana AA. et al. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 2008; 111: 4902-4907.
    CrossrefPubMedGoogle Scholar
  • 32 Ay C. et al. Prediction of venous thromboembolism in cancer patients. Blood 2010; 116: 5377-5382.
    CrossrefPubMedGoogle Scholar
  • 33 Kakkar AK, Williamson RC.. Prevention of venous thromboembolism in cancer patients. Semin Thromb Hemost 1999; 25: 239-243.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 34 Kakkar AK. et al. Evaluation of perioperative fatal pulmonary embolism and death in cancer surgical patients: the MC-4 cancer substudy. Thromb Haemost 2005; 94: 867-871.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 Trinh VQ. et al. Venous thromboembolism after major cancer surgery: temporal trends and patterns of care. JAMA Surg 2014; 149: 43-49.
    CrossrefPubMedGoogle Scholar
  • 36 Kim JYS. et al. Surgical duration and risk of venous thromboembolism. JAMA Surg 2015; 150: 110-117.
    CrossrefPubMedGoogle Scholar
  • 37 Einstein MH. et al. Venous thromboembolism prevention in gynecologic cancer surgery: a systematic review. Gynecol Oncol 2007; 105: 813-819.
    CrossrefPubMedGoogle Scholar
  • 38 Mismetti P. et al. Meta-analysis of low molecular weight heparin in the prevention of venous thromboembolism in general surgery. Br J Surg 2001; 88: 913-930.
    CrossrefPubMedGoogle Scholar
  • 39 Efficacy and safety of enoxaparin versus unfractionated heparin for prevention of deep vein thrombosis in elective cancer surgery: a double-blind randomized multicentre trial with venographic assessment. ENOXACAN Study Group. Br J Surg 1997; 84: 1099-1103.
    CrossrefPubMedGoogle Scholar
  • 40 Akl EA. et al. Low molecular weight heparin versus unfractionated heparin for perioperative thromboprophylaxis in patients with cancer. Cochrane Database Syst Rev 2014; 06: CD009447.
    PubMedGoogle Scholar
  • 41 Bergqvist D. et al. Low molecular weight heparin started before surgery as prophylaxis against deep vein thrombosis: 2500 versus 5000 XaI units in 2070 patients. Br J Surg 1995; 82: 496-501.
    CrossrefPubMedGoogle Scholar
  • 42 Bergqvist D. et al. Duration of prophylaxis against venous thromboembolism with enoxaparin after surgery for cancer. N Engl J Med 2002; 346: 975-980.
    CrossrefPubMedGoogle Scholar
  • 43 Kakkar VV. et al. Extended prophylaxis with bemiparin for the prevention of venous thromboembolism after abdominal or pelvic surgery for cancer: the CAN-BESURE randomized study. J Thromb Haemost 2010; 08: 1223-1229.
    CrossrefPubMedGoogle Scholar
  • 44 Vedovati MC. et al. A randomized study on 1-week versus 4-week prophylaxis for venous thromboembolism after laparoscopic surgery for colorectal cancer. Ann Surg 2014; 259: 665-669.
    CrossrefPubMedGoogle Scholar
  • 45 Samama MM. 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 1999; 341: 793-800.
    CrossrefPubMedGoogle Scholar
  • 46 Leizorovicz A. et al. Randomized, placebo-controlled trial of dalteparin for the prevention of venous thromboembolism in acutely ill medical patients. Circulation 2004; 110: 874-879.
    CrossrefPubMedGoogle Scholar
  • 47 Cohen AT. et al. Efficacy and safety of fondaparinux for the prevention of venous thromboembolism in older acute medical patients: randomised placebo controlled trial. Br Med J 2006; 332: 325-329.
    CrossrefPubMedGoogle Scholar
  • 48 Carrier M. et al. Lack of evidence to support thromboprophylaxis in hospitalized medical patients with cancer. Am J Med 2014; 127: 82-86. e1
    CrossrefPubMedGoogle Scholar
  • 49 Haas S. et al. Heparin based prophylaxis to prevent venous thromboembolic events and death in patients with cancer – a subgroup analysis of CERTIFY. BMC Cancer 2011; 11: 316.
    CrossrefPubMedGoogle Scholar
  • 50 Caruso V. et al. Thrombotic complications in childhood acute lymphoblastic leukemia: a meta-analysis of 17 prospective studies comprising 1752 pediatric patients. Blood 2006; 108: 2216-2222.
    CrossrefPubMedGoogle Scholar
  • 51 Mitchell L. et al. Validation of a predictive model for identifying an increased risk for thromboembolism in children with acute lymphoblastic leukemia: results of a multicentre cohort study. Blood 2010; 115: 4999-5004.
    CrossrefPubMedGoogle Scholar
  • 52 Spencer FA. et al. Venous thromboembolism in the outpatient setting. Arch Intern Med 2007; 167: 1471-1475.
    CrossrefPubMedGoogle Scholar
  • 53 Khorana AA. et al. Incidence and predictors of venous thromboembolism (VTE) among ambulatory high-risk cancer patients undergoing chemotherapy in the United States. Cancer 2013; 119: 648-655.
    CrossrefPubMedGoogle Scholar
  • 54 Bohlius J. et al. Recombinant human erythropoietins and cancer patients: updated meta-analysis of 57 studies including 9353 patients. J Natl Cancer Inst 2006; 98: 708-714.
    CrossrefPubMedGoogle Scholar
  • 55 Khorana AA. et al. Blood transfusions, thrombosis, and mortality in hospitalized patients with cancer. Arch Intern Med 2008; 168: 2377-2381.
    CrossrefPubMedGoogle Scholar
  • 56 Kakkar AK. et al. Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS). J Clin Oncol Off J Am Soc Clin Oncol 2004; 22: 1944-1948.
    CrossrefPubMedGoogle Scholar
  • 57 Agnelli G. et al. Semuloparin for Thromboprophylaxis in Patients Receiving Chemotherapy for Cancer. N Engl J Med 2012; 366: 601-609.
    CrossrefPubMedGoogle Scholar
  • 58 Agnelli G. et al. Nadroparin for the prevention of thromboembolic events in ambulatory patients with metastatic or locally advanced solid cancer receiving chemotherapy: a randomised, placebo-controlled, double-blind study. Lancet Oncol 2009; 10: 943-949.
    CrossrefPubMedGoogle Scholar
  • 59 Maraveyas A, Waters J, Roy R. et al. Gemcitabine versus gemcitabine plus dalteparin thromboprophylaxis in pancreatic cancer. Eur J Cancer Oxf Engl 1990 2012; 48: 1283-1292.
    PubMedGoogle Scholar
  • 60 Pelzer U. et al. Efficacy of Prophylactic Low-Molecular Weight Heparin for Ambulatory Patients With Advanced Pancreatic Cancer: Outcomes From the CONKO-004 Trial. J Clin Oncol Off J Am Soc Clin Oncol 2015; 33: 2028-2034.
    CrossrefPubMedGoogle Scholar
  • 61 Haas SK. et al. Low-molecular-weight heparin versus placebo for the prevention of venous thromboembolism in metastatic breast cancer or stage III/IV lung cancer. Clin Appl Thromb Off J Int Acad Clin Appl Thromb 2012; 18: 159-165.
    PubMedGoogle Scholar
  • 62 Macbeth F. et al. Randomized Phase III Trial of Standard Therapy Plus Low Molecular Weight Heparin in Patients With Lung Cancer: FRAGMATIC Trial. J Clin Oncol 2016; 34: 488-494.
    PubMedGoogle Scholar
  • 63 Akl EA. et al. Parenteral anticoagulation in ambulatory patients with cancer. Cochrane Database Syst Rev 2014; 12: CD006652.
    PubMedGoogle Scholar
  • 64 Di Nisio M. et al Primary prophylaxis for venous thromboembolism in ambulatory cancer patients receiving chemotherapy. Cochrane Database Syst Rev 2014; 08: CD008500.
    PubMedGoogle Scholar
  • 65 Palumbo A. et al. Prevention of thalidomide- and lenalidomide-associated thrombosis in myeloma. Leukemia 2008; 22: 414-423.
    CrossrefPubMedGoogle Scholar
  • 66 Palumbo A. et al. Aspirin, warfarin, or enoxaparin thromboprophylaxis in patients with multiple myeloma treated with thalidomide: a phase III, open-label, randomized trial. J Clin Oncol Off J Am Soc Clin Oncol 2011; 29: 986-993.
    CrossrefPubMedGoogle Scholar
  • 67 Kakkar AK. et al. Venous thrombosis in cancer patients: insights from the FRONTLINE survey. Oncologist 2003; 08: 381-388.
    CrossrefPubMedGoogle Scholar
  • 68 Kahn SR. et al. Multicentre evaluation of the use of venous thromboembolism prophylaxis in acutely ill medical patients in Canada. Thromb Res 2007; 119: 145-155.
    CrossrefPubMedGoogle Scholar
  • 69 Tapson VF. et al. Venous thromboembolism prophylaxis in acutely ill hospitalized medical patients: findings from the International Medical Prevention Registry on Venous Thromboembolism. Chest 2007; 132: 936-945.
    CrossrefPubMedGoogle Scholar
  • 70 Kucher N. et al. Clinical predictors of prophylaxis use prior to the onset of acute venous thromboembolism in hospitalized patients SWIss Venous ThromboEmbolism Registry (SWIVTER). J Thromb Haemost 2008; 06: 2082-2087.
    CrossrefPubMedGoogle Scholar
  • 71 Zwicker JI. et al. Pattern of frequent but nontargeted pharmacologic thrombo-prophylaxis for hospitalized patients with cancer at academic medical centres: a prospective, cross-sectional, multicentre study. J Clin Oncol Off J Am Soc Clin Oncol 2014; 32: 1792-1796.
    CrossrefPubMedGoogle Scholar
  • 72 Panizo E. et al. Factors influencing the use of thromboprophylaxis in cancer outpatients in clinical practice: A prospective study. Thromb Res 2015; 136: 1145-1148.
    CrossrefPubMedGoogle Scholar
  • 73 Cohen AT. et al. Rivaroxaban for thromboprophylaxis in acutely ill medical patients. N Engl J Med 2013; 368: 513-523.
    CrossrefPubMedGoogle Scholar
  • 74 Levine MN. et al. A randomized phase II trial of apixaban for the prevention of thromboembolism in patients with metastatic cancer. J Thromb Haemost 2012; 10: 807-814.
    CrossrefPubMedGoogle Scholar