381
Views
6
CrossRef citations to date
0
Altmetric
Reviews

Recent developments and persisting challenges in the prevention and treatment of venous thromboembolism in patients with hematological malignancies

ORCID Icon, , , &
Pages 1277-1291 | Received 25 Oct 2019, Accepted 02 Jan 2020, Published online: 21 Jan 2020

References

  • Khorana AA, Kuderer NM, Culakova E, et al. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood. 2008;111:4902–4907.
  • Walker AJ, Card TR, West J, et al. Incidence of venous thromboembolism in patients with cancer - a cohort study using linked United Kingdom databases. Eur J Cancer. 2013;49:1404–1413.
  • Lee AYY, 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. 2003;349:146–153.
  • Raskob GE, van Es N, Verhamme P, et al. Edoxaban for the treatment of cancer-associated venous thromboembolism. N Engl J Med. 2018;378:615–624.
  • Khorana AA, Noble S, Lee AYY, et al. Role of direct oral anticoagulants in the treatment of cancer-associated venous thromboembolism: guidance from the SSC of the ISTH. J Thromb Haemost. 2018;16:1891–1894.
  • Agnelli G, George DJ, Kakkar AK, et al. Semuloparin for thromboprophylaxis in patients receiving chemotherapy for cancer. N Engl J Med. 2012;366:601–609.
  • Pelzer U, Opitz B, Deutschinoff G, 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. 2015;33:2028–2034.
  • Carrier M, Abou-Nassar K, Mallick R, et al. Apixaban to prevent venous thromboembolism in patients with cancer. N Engl J Med. 2019;380:711–719.
  • Mulder FI, Candeloro M, Kamphuisen PW, et al. The Khorana score for prediction of venous thromboembolism in cancer patients: a systematic review and meta-analysis. Haematologica. 2019;104:1277–1287.
  • Prandoni P, Lensing AWA, Piccioli A, et al. Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood. 2002;100:3484–3488.
  • Ruíz-Giménez N, Suárez C, González R, et al.; RIETE Investigators. Predictive variables for major bleeding events in patients presenting with documented acute venous thromboembolism. Findings from the RIETE Registry. Thromb Haemost. 2008;100:26–31.
  • Prandoni P, Trujillo-Santos J, Surico T, et al.; for the RIETE Investigators. Recurrent thromboembolism and major bleeding during oral anticoagulant therapy in patients with solid cancer: findings from the RIETE registry. Haematologica. 2008;93:1432–1434.
  • Trujillo-Santos J, Nieto JA, Tiberio G, et al. Predicting recurrences or major bleeding in cancer patients with venous thromboembolism. Findings from the RIETE Registry. Thromb Haemost. 2008;100:435–439.
  • Streiff MB, Milentijevic D, McCrae K, et al. Effectiveness and safety of anticoagulants for the treatment of venous thromboembolism in patients with cancer. Am J Hematol. 2018;93:664–671.
  • Kamphuisen PW, Beyer-Westendorf J. Bleeding complications during anticoagulant treatment in patients with cancer. Thromb Res. 2014;133:S49–S55.
  • Farge D, Frere C, Connors JM, et al. 2019 international clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer. Lancet Oncol. 2019;20:e566–e581.
  • Kearon C, Akl EA, Ornelas J, et al. Antithrombotic therapy for VTE disease: CHEST guideline and expert panel report. Chest. 2016;149:315–352.
  • Posch F, Königsbrügge O, Zielinski C, et al. Treatment of venous thromboembolism in patients with cancer: a network meta-analysis comparing efficacy and safety of anticoagulants. Thromb Res. 2015;136:582–589.
  • Key NS, Khorana AA, Kuderer NM, et al. Venous thromboembolism prophylaxis and treatment in patients with cancer: ASCO clinical practice guideline update. J Clin Oncol. Forthcoming. 2019.
  • Ay C, Kamphuisen PW, Agnelli G. Antithrombotic therapy for prophylaxis and treatment of venous thromboembolism in patients with cancer: review of the literature on current practice and emerging options. ESMO Open 2017;2:e000188.
  • Meyer G. Low-molecular weight heparin or direct oral anticoagulants for the treatment of cancer associated thrombosis. Are we at the crossroad? Thromb Res. 2019;173:156–157.
  • Vedovati MC, Giustozzi M, Bonitta G, et al. Efficacy and safety of anticoagulant agents in patients with venous thromboembolism and cancer: a network meta-analysis. Thromb Res. 2018;170:175–180.
  • Zakai NA, Walker RF, MacLehose RF, et al. Impact of anticoagulant choice on hospitalized bleeding risk when treating cancer-associated venous thromboembolism. J Thromb Haemost. 2018;16:2403–2412.
  • Agnelli G, Gussoni G, Bianchini C, 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.
  • Di Nisio M, Porreca E, Candeloro M, et al. Primary prophylaxis for venous thromboembolism in ambulatory cancer patients receiving chemotherapy. Cochrane Database Syst Rev. 2016;2016:CD008500.
  • Burnett AE, Mahan CE, Vazquez SR, et al. Guidance for the practical management of the direct oral anticoagulants (DOACs) in VTE treatment. J Thromb Thrombolysis. 2016;41:206–232.
  • van Es N, Coppens M, Schulman S, et al. Direct oral anticoagulants compared with vitamin K antagonists for acute venous thromboembolism: evidence from phase 3 trials. Blood. 2014;124:1968–1975.
  • Riva N, Ageno W. Use of the direct oral anticoagulants for the treatment of venous thromboembolism. Hematol Oncol Clin North Am. 2016;30:1035–1051.
  • Steffel J, Verhamme P, Potpara TS, et al. ESC Scientific Document Group. The 2018 European Heart Rhythm Association Practical Guide on the use of non-vitamin K antagonist oral anticoagulants in patients with atrial fibrillation. Eur Heart J. 2018;39:1330–1393.
  • Crowther M, Cuker A. How can we reverse bleeding in patients on direct oral anticoagulants? Kardiol Pol. 2019;77:3–11.
  • Ebner M, Birschmann I, Peter A, et al. Limitations of specific coagulation tests for direct oral anticoagulants: a critical analysis. J Am Heart Assoc. 2018;7:e009807.
  • Ruff CT, Giugliano RP, Antman EM. Management of bleeding with non–vitamin K antagonist oral anticoagulants in the era of specific reversal agents. Circulation 2016;134:248–261.
  • Ruff CT, Giugliano RP, Braunwald E, et al. Comparison of the efficacy and safety of new oral anticoagulants with warfarin in patients with atrial fibrillation: a meta-analysis of randomised trials. Lancet. 2014;383:955–962.
  • Schaefer JK, McBane RD, Wysokinski WE. How to choose appropriate direct oral anticoagulant for patient with nonvalvular atrial fibrillation. Ann Hematol. 2016;95:437–449.
  • Konstantinides SV, Meyer G, Becattini C, et al. 2019 ESC Guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS). Eur Heart J. 2019;ehz405.
  • Gómez-Outes A, Terleira-Fernández AI, Lecumberri R, et al. Direct oral anticoagulants in the treatment of acute venous thromboembolism: a systematic review and meta-analysis. Thromb Res. 2014;134:774–782.
  • Agnelli G, Buller HR, Cohen A, et al. Oral apixaban for the treatment of acute venous thromboembolism. N Engl J Med. 2013;369:799–808.
  • Schulman S, Kearon C, Kakkar AK, et al. Dabigatran versus Warfarin in the treatment of acute venous thromboembolism. N Engl J Med. 2009;361:2342–2352.
  • Investigators E, Bauersachs R, Berkowitz SD, et al. Oral rivaroxaban for symptomatic venous thromboembolism. N Engl J Med. 2010;363:2499–2510.
  • Büller HR, Décousus H, Grosso MA, et al. Hokusai-VTE Investigators. Edoxaban versus warfarin for the treatment of symptomatic venous thromboembolism. N Engl J Med. 2013;369:1406–1415.
  • Khorana AA, Soff GA, Kakkar AK, et al. Rivaroxaban for thromboprophylaxis in high-risk ambulatory patients with cancer. N Engl J Med. 2019;380:720–728.
  • Young AM, Marshall A, Thirlwall J, et al. Comparison of an oral factor Xa inhibitor with low molecular weight heparin in patients with cancer with venous thromboembolism: results of a randomized trial (SELECT-D). J Clin Oncol. 2018;36:2017–2023.
  • McBane RD, Wysokinski WE, Le-Rademacher JG, et al. Apixaban and dalteparin in active malignancy-associated venous thromboembolism: the ADAM VTE trial. J Thromb Haemost. Forthcoming. 2019.
  • Mulder FI, van Es N, Kraaijpoel N, et al. Edoxaban for treatment of venous thromboembolism in patient groups with different types of cancer: results from the Hokusai VTE Cancer study. Thromb Res. 2020;185:13–19.
  • Li A, Garcia DA, Lyman GH, et al. Direct oral anticoagulant (DOAC) versus low-molecular-weight heparin (LMWH) for treatment of cancer associated thrombosis (CAT): a systematic review and meta-analysis. Thromb Res. 2019;173:158–163.
  • Wang T, Zwicker JI, Ay C, et al. The use of direct oral anticoagulants for primary thromboprophylaxis in ambulatory cancer patients: guidance from the SSC of the ISTH. J Thromb Haemost. 2019;17:1772–1778.
  • Samuelson Bannow BT, Lee A, Khorana AA, et al. Management of cancer-associated thrombosis in patients with thrombocytopenia: guidance from the SSC of the ISTH. J Thromb Haemost. 2018;16:1246–1249.
  • Tufano A, Galderisi M, Esposito L, et al. Anticancer drug-related nonvalvular atrial fibrillation: challenges in management and antithrombotic strategies. Semin Thromb Hemost. 2018;44:388–396.
  • Chu G, Versteeg HH, Verschoor AJ, et al. Atrial fibrillation and cancer – an unexplored field in cardiovascular oncology. Blood Rev. 2019;35:59–67.
  • Kraaijpoel N, Carrier M. How I treat cancer-associated venous thromboembolism. Blood. 2019;133:291–298.
  • Short NJ, Connors JM. New oral anticoagulants and the cancer patient. Oncologist. 2014;19:82–93.
  • Patel HK, Khorana AA. Anticoagulation in cancer patients: a summary of pitfalls to avoid. Curr Oncol Rep. 2019;21:18.
  • Caruso V, Di Castelnuovo A, Meschengieser S, et al. Thrombotic complications in adult patients with lymphoma: a meta-analysis of 29 independent cohorts including 18 018 patients and 1149 events. Blood. 2010;115:5322–5328.
  • Santi RM, Ceccarelli M, Bernocco E, et al. Khorana score and histotype predicts incidence of early venous thromboembolism in non-Hodgkin lymphomas: a pooled-data analysis of 12 clinical trials of fondazione italiana linfomi (FIL). Thromb Haemost. 2017;117:1615–1621.
  • Mahajan A, Wun T, Chew H, et al. Lymphoma and venous thromboembolism: influence on mortality. Thromb Res. 2014;133:S23–S8.
  • Lund JL, Østgård LS, Prandoni P, et al. Incidence, determinants and the transient impact of cancer treatments on venous thromboembolism risk among lymphoma patients in Denmark. Thromb Res. 2015;136:917–923.
  • Borchmann S, Müller H, Hude I, et al. Thrombosis as a treatment complication in Hodgkin lymphoma patients: a comprehensive analysis of three prospective randomized German Hodgkin Study Group (GHSG) trials. Ann Oncol. 2019;30:1329–1334.
  • Katkish LA, Rangaraju S, Rector TS, et al. Incidence of unprovoked venous thromboembolic events in patients with chronic lymphocytic leukemia. Leuk Lymphoma 2018;59:509–511.
  • Rupa-Matysek J, Gil L, Kaźmierczak M, et al. Prediction of venous thromboembolism in newly diagnosed patients treated for lymphoid malignancies: validation of the Khorana Risk Score. Med Oncol. 2018;35:5.
  • Mohren M, Markmann I, Jentsch-Ullrich K, et al. Increased risk of thromboembolism in patients with malignant lymphoma: a single-centre analysis. Br J Cancer 2005;92:1349–1351.
  • Antic D, Milic N, Nikolovski S, et al. Development and validation of multivariable predictive model for thromboembolic events in lymphoma patients. Am J Hematol. 2016;91:1014–1019.
  • Antic D, Milic N, Mihaljevic B, et al. External validation and revision of thrombosis lymphoma/throly/score. Blood. 2018;132:140.
  • Sanfilippo KM, Luo S, Wang T, et al. Predicting venous thromboembolism in multiple myeloma: development and validation of the IMPEDE VTE score. Am J Hematol. 2019;94:1176–1184.
  • Swan D, Rocci A, Bradbury C, et al. Venous thromboembolism in multiple myeloma – choice of prophylaxis, role of direct oral anticoagulants and special considerations. Br J Haematol. 2018;183:538–556.
  • Palumbo A, Rajkumar SV, Dimopoulos MA, et al.; on behalf of the International Myeloma Working Group. Prevention of thalidomide- and lenalidomide-associated thrombosis in myeloma. Leukemia 2008;22:414–423.
  • Palumbo A, Rajkumar SV, San Miguel JF, et al. International myeloma working group consensus statement for the management, treatment, and supportive care of patients with myeloma not eligible for standard autologous stem-cell transplantation. J Clin Oncol. 2014;32:587–600.
  • Pegourie B, Karlin L, Benboubker L, et al.; for the IFM Group. Apixaban for the prevention of thromboembolism in immunomodulatory-treated myeloma patients: Myelaxat, a phase 2 pilot study. Am J Hematol. 2019;94:635–640.
  • Cornell R. Prospective study of apixaban for primary prevention of venous thromboembolism in patients with multiple myeloma receiving immunomodulatory therapy. Front Oncol. 2019;9:45.
  • Storrar NPF, Mathur A, Johnson PRE, et al. Safety and efficacy of apixaban for routine thromboprophylaxis in myeloma patients treated with thalidomide- and lenalidomide-containing regimens. Br J Haematol. 2019;185:142–144.
  • Fotiou D, Gavriatopoulou M, Ntanasis-Stathopoulos I, et al. Updates on thrombotic events associated with multiple myeloma. Expert Rev Hematol. 2019;12:355–365.
  • Kekre N, Connors JM. Venous thromboembolism incidence in hematologic malignancies. Blood Rev. 2019;33:24–32.
  • Barbui T, Finazzi G, Falanga A. Myeloproliferative neoplasms and thrombosis. Blood. 2013;122:2176–2184.
  • De Stefano V, Finazzi G. Barbui T. Antithrombotic therapy for venous thromboembolism in myeloproliferative neoplasms. Blood Cancer J. 2018;8:65.
  • Cohen H, Hunt BJ, Efthymiou M, et al.; on behalf of the RAPS Trial Investigators. Direct oral anticoagulants use in antiphospholipid syndrome: are these drugs an effective and safe alternative to warfarin? A systematic review of the literature: comment. Curr Rheumatol Rep. 2017;19:74.
  • Ordi-Ros J, Sáez-Comet L, Pérez-Conesa M, et al. Rivaroxaban versus vitamin k antagonist in antiphospholipid syndrome: a randomized noninferiority trial. Ann Intern Med. 2019;171:685.
  • Carrier M, Khorana AA, Zwicker JI, et al.; on behalf of the subcommittee on Haemostasis and Malignancy for the SSC of the ISTH. 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.
  • Samuelson Bannow BT, Walter RB, Gernsheimer TB, et al. Patients treated for acute VTE during periods of treatment-related thrombocytopenia have high rates of recurrent thrombosis and transfusion-related adverse outcomes. J Thromb Thrombolysis. 2017;44:442–447.
  • Samuelson Bannow BR, Lee AYY, Khorana AA, et al. Management of anticoagulation for cancer-associated thrombosis in patients with thrombocytopenia: a systematic review. Res Pract Thromb Haemost. 2018;2:664–669.
  • Mantha S, Miao Y, Wills J, et al. Enoxaparin dose reduction for thrombocytopenia in patients with cancer: a quality assessment study. J Thromb Thrombolysis. 2017;43:514–518.
  • Gerber DE, Segal JB, Levy MY, et al. The incidence of and risk factors for venous thromboembolism (VTE) and bleeding among 1514 patients undergoing hematopoietic stem cell transplantation: implications for VTE prevention. Blood. 2008;112:504–510.
  • Khanal N, Bociek RG, Chen B, et al. Venous thromboembolism in patients with hematologic malignancy and thrombocytopenia. Am J Hematol. 2016;91:E468–E472.
  • Caruso V, Iacoviello L, Di Castelnuovo A, et al. Venous thrombotic complications in adults undergoing induction treatment for acute lymphoblastic leukemia: results from a meta-analysis. J Thromb Haemost. 2007;5:621–623.
  • Ahrari A, Al-Ani F, Wang YP, et al. Treatment of venous thromboembolism in acute leukemia: a systematic review. Thromb Res. 2019;178:1–6.
  • Zahid MF, Murad MH, Litzow MR, et al. Venous thromboembolism following hematopoietic stem cell transplantation - a systematic review and meta-analysis. Ann Hematol. 2016;95:1457–1464.
  • Napolitano M, Valore L, Saccullo G, et al. Management of venous thromboembolism (VTE) in patients with acute leukemia: results from a multicenter study. Blood. 2014;124:3688–3688.
  • Ku GH, White RH, Chew HK, et al. Venous thromboembolism in patients with acute leukemia: incidence, risk factors, and effect on survival. Blood. 2009;113:3911–3917.
  • Vu K, Luong NV, Hubbard J, et al. A retrospective study of venous thromboembolism in acute leukemia patients treated at the university of Texas MD Anderson cancer center. Cancer Med. 2015;4:27–35.
  • Kekre N, Kim HT, Ho VT, et al. Venous thromboembolism is associated with graft- versus -host disease and increased non-relapse mortality after allogeneic hematopoietic stem cell transplantation. Haematologica. 2017;102:1185–1191.
  • Gangaraju R, Chen Y, Hageman L, et al. Risk of venous thromboembolism in patients with non‐Hodgkin lymphoma surviving blood or marrow transplantation. Cancer. 2019;125:4498–4508.
  • Houghton DE, Key NS, Zakai NA, et al. Analysis of anticoagulation strategies for venous thromboembolism during severe thrombocytopenia in patients with hematologic malignancies: a retrospective cohort. Leuk Lymphoma. 2017;58:2573–2581.
  • Dawwas GK, Brown J, Dietrich E, et al. Effectiveness and safety of apixaban versus rivaroxaban for prevention of recurrent venous thromboembolism and adverse bleeding events in patients with venous thromboembolism: a retrospective population-based cohort analysis. Lancet Haematol. 2019;6:e20–e28.
  • López-López JA, Sterne JAC, Thom HHZ, et al. Oral anticoagulants for prevention of stroke in atrial fibrillation: systematic review, network meta-analysis, and cost effectiveness analysis. BMJ. 2017;359:j5058.
  • Lutsey PL, Zakai NA, MacLehose RF, et al. Risk of hospitalised bleeding in comparisons of oral anticoagulant options for the primary treatment of venous thromboembolism. Br J Haematol. 2019;185:903–911.
  • Castellucci LA, Cameron C, Le Gal G, et al. Clinical and safety outcomes associated with treatment of acute venous thromboembolism. JAMA. 2014;312:1122.
  • Cohen AT, Hamilton M, Mitchell SA, et al. Comparison of the novel oral anticoagulants apixaban, dabigatran, edoxaban, and rivaroxaban in the initial and long-term treatment and prevention of venous thromboembolism: systematic review and network meta-analysis. PLoS One. 2015;10:e0144856.
  • Tritschler T, Castellucci LA. It’s time for head-to-head trials with direct oral anticoagulants. Thromb Res. 2019;180:64–69.
  • Aryal MR, Gosain R, Donato A, et al. Systematic review and meta-analysis of the efficacy and safety of apixaban compared to rivaroxaban in acute VTE in the real world. Blood Adv. 2019;3:2381–2387.
  • Decousus H, Bourmaud A, Fournel P, et al. Cancer-associated thrombosis in patients with implanted ports: a prospective multicenter French cohort study (ONCOCIP). Blood. 2018;132:707–716.
  • Lavau-Denes S, Lacroix P, Maubon A, et al. Prophylaxis of catheter-related deep vein thrombosis in cancer patients with low-dose warfarin, low molecular weight heparin, or control: a randomized, controlled, phase III study. Cancer Chemother Pharmacol. 2013;72:65–73.
  • Muñoz FJ, Mismetti P, Poggio R, et al. Clinical outcome of patients with upper-extremity deep vein thrombosis. Chest. 2008;133:143–148.
  • Kahale LA, Tsolakian IG, Hakoum MB, et al. Anticoagulation for people with cancer and central venous catheters. Cochrane Database Syst Rev. 2018;2018:CD006468.
  • Farge D, Bounameaux H, Brenner B, et al. International clinical practice guidelines including guidance for direct oral anticoagulants in the treatment and prophylaxis of venous thromboembolism in patients with cancer. Lancet Oncol. 2016;17:e452–e466.
  • Zwicker JI, Rojan A, Campigotto F, et al. Pattern of frequent but nontargeted pharmacologic thromboprophylaxis for hospitalized patients with cancer at academic medical centers: a prospective, cross-sectional, multicenter study. J Clin Oncol. 2014;32:1792–1796.
  • Burleigh E, Wang C, Foster D, et al. Thromboprophylaxis in medically ill patients at risk for venous thromboembolism. Am J Health Syst Pharm. 2006;63:S23–S29.
  • Figueroa R, Alfonso A, López-Picazo J, et al. Insights into venous thromboembolism prevention in hospitalized cancer patients: lessons from a prospective study. PLoS One. 2018;13:e0200220.
  • Sorigue M, Miljkovic MD. Atrial fibrillation and stroke risk in patients with cancer: a primer for oncologists. J Oncol Pract. 2019;15:641–650.
  • Delluc A, Wang TF, Yap ES, et al. Anticoagulation of cancer patients with non-valvular atrial fibrillation receiving chemotherapy: guidance from the SSC of the ISTH. J Thromb Haemost. 2019;17:1247–1252.
  • Zamorano JL, Lancellotti P, Rodriguez Muñoz D, et al. 2016 ESC Position Paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines. Eur Heart J. 2016;37:2768–2801.
  • Schulman S, Zondag M, Linkins L, et al. Recurrent venous thromboembolism in anticoagulated patients with cancer: management and short-term prognosis. J Thromb Haemost. 2015;13:1010–1018.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.