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Current Oncology Reports

, 21:18 | Cite as

Anticoagulation in Cancer Patients: a Summary of Pitfalls to Avoid

  • Harsh K. Patel
  • Alok A. KhoranaEmail author
Palliative Medicine (A Jatoi, Section Editor)
  • 128 Downloads
Part of the following topical collections:
  1. Topical Collection on Palliative Medicine

Abstract

Purpose of Review

Venous thromboembolism (VTE) is a leading cause of morbidity and mortality in cancer patients, and its management is often associated with complications including risk of recurrent VTE and bleeding. Here, we review the current data on pitfalls during anticoagulation in cancer patients and measures necessary to avoid them.

Recent Findings

Although low-molecular-weight heparin monotherapy has been the standard of treatment for several years, emerging data for direct oral anticoagulants (DOACs) are leading to new paradigms in treatment. Reports of recent randomized trials suggest a lower risk of recurrent thrombosis but higher risk of bleeding, particularly in gastrointestinal cancer patients, with DOACs. Careful patient selection and individualization of therapy based on risk of bleeding as well as recurrent VTE are keys.

Summary

Problems like bleeding, recurrence, thrombocytopenia, drug-drug interactions, renal impairment, nausea-vomiting along with concerns about adherence arise during anticoagulation in cancer patients. However, with adequate pre-treatment assessment, correct anticoagulant selection and proper monitoring during anticoagulation, these issues can be addressed safely and effectively.

Keywords

Cancer VTE Thromboembolism Anticoagulation Thromboprophylaxis Pitfalls Bleeding Thrombocytopenia Chemotherapy LMWH VKA DOAC Adherence Renal insufficiency Drug-drug interactions 

Notes

Compliance with Ethical Standards

Conflict of Interest

Harsh K. Patel declares that he has no conflict of interest.

Alok A. Khorana has received compensation from Bayer, Sanofi, Parexel, Halozyme Therapeutics, Pfizer, Seattle Genetics, Pharmacyclics, PharmaCyte Biotech, AngioDynamics, LEO Pharma, TriSalus, and Medscape/WebMD for service as a consultant; has received travel support from Bayer, Sanofi, Parexel, Janssen, Halozyme Therapeutics, Pfizer, Seattle Genetics, AngioDynamics, LEO Pharma, and Medscape/WebMD; and is the Co-Chair of the CASSINI Steering Committee, as well as the National Coordinator for the MARINER trial, both of which are funded by Janssen.

Human and Animal Rights and Informed Consent

All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines)

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Walker AJ, Card TR, West J, Crooks C, Grainge MJ. Incidence of venous thromboembolism in patients with cancer—a cohort study using linked United Kingdom databases. Eur J Cancer. 2013;49(6):1404–13.  https://doi.org/10.1016/J.EJCA.2012.10.021.CrossRefPubMedGoogle Scholar
  2. 2.
    Gussoni G, Frasson S, La Regina M, Di Micco P, Monreal M. Three-month mortality rate and clinical predictors in patients with venous thromboembolism and cancer. Findings from the RIETE registry. Thromb Res. 2013;131(1):24–30.  https://doi.org/10.1016/j.thromres.2012.10.007.CrossRefPubMedGoogle Scholar
  3. 3.
    Anderson LA, Moore SC, Gridley G, Stone BJ, Landgren O. Concomitant and antecedent deep venous thrombosis and cancer survival in male US veterans. Leuk Lymphoma. 2011;52(5):764–70.  https://doi.org/10.3109/10428194.2010.551572.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Khorana AA, Francis CW, Culakova E, Kuderer NM, Lyman GH. Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost. 2007;5:632–4.  https://doi.org/10.1111/j.1538-7836.2007.02374.x.CrossRefPubMedGoogle Scholar
  5. 5.
    Kourlaba G, Relakis J, Mylonas C, Kapaki V, Kontodimas S, Holm MV, et al. The humanistic and economic burden of venous thromboembolism in cancer patients. Blood Coagul Fibrinolysis. 2015;26(1):13–31.  https://doi.org/10.1097/MBC.0000000000000193.CrossRefPubMedGoogle Scholar
  6. 6.
    Cohoon KP, Ransom JE, Leibson CL, et al. Direct medical costs attributable to cancer-associated venous thromboembolism: a population-based longitudinal study. Am J Med. 2016;129(9):1000.e15–25.  https://doi.org/10.1016/j.amjmed.2016.02.030.CrossRefGoogle Scholar
  7. 7.
    Arora M, Wun T. Adverse impact of venous thromboembolism on patients with cancer. Semin Thromb Hemost. 2014;40(3):313–8.  https://doi.org/10.1055/s-0034-1370769.CrossRefPubMedGoogle Scholar
  8. 8.
    Khorana AA, Carrier M, Garcia DA, Lee AYY. Guidance for the prevention and treatment of cancer-associated venous thromboembolism. J Thromb Thrombolysis. 2016;41(1):81–91.  https://doi.org/10.1007/s11239-015-1313-4.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Lee AYY. Overview of VTE treatment in cancer according to clinical guidelines. Thromb Res. 2018;164(January):S162–7.  https://doi.org/10.1016/j.thromres.2018.01.002.CrossRefPubMedGoogle Scholar
  10. 10.
    Mandalà M, Falanga A, Roila F. Management of venous thromboembolism (VTE) in cancer patients: ESMO clinical practice guidelines. Ann Oncol. 2011;22(SUPPL. 6):85–92.  https://doi.org/10.1093/annonc/mdr392.CrossRefGoogle Scholar
  11. 11.
    Lyman GH, Bohlke K, Khorana AA, Kuderer NM, Lee AY, Arcelus JI, 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;33(6):654–6.  https://doi.org/10.1200/JCO.2014.59.7351.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Streiff MB, Bockenstedt PL, Cataland SR, Chesney C, Eby C, Fanikos J, et al. Venous thromboembolic disease: clinical practice guidelines in oncology. JNCCN J Natl Compr Cancer Netw. 2013;11(11):1402–29.  https://doi.org/10.6004/JNCCN.2013.0163.CrossRefGoogle Scholar
  13. 13.
    Farge D, Bounameaux H, Brenner B, Cajfinger F, Debourdeau P, Khorana AA, 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(10):452–66.  https://doi.org/10.1016/S1470-2045(16)30369-2.CrossRefGoogle Scholar
  14. 14.
    Posch F, Königsbrügge O, Zielinski C, Pabinger I, Ay C. Treatment of venous thromboembolism in patients with cancer: a network meta-analysis comparing efficacy and safety of anticoagulants. Thromb Res. 2015;136(3):582–9.  https://doi.org/10.1016/j.thromres.2015.07.011.CrossRefPubMedGoogle Scholar
  15. 15.
    • Khorana AA, Noble S, Lee AYY, et al. Role of direct oral anticoagulants in treatment of cancer-associated venous thromboembolism: guidance from the SSC of the ISTH. J Thromb Haemost. 2018;16:1891–4.  https://doi.org/10.1111/jth.14219 This guidance document from ISTH emphasizes an individualized approach to choice of anticoagulation in treatment of cancer-associated VTE. CrossRefPubMedGoogle Scholar
  16. 16.
    Menapace LA, McCrae KR, Khorana AA. Predictors of recurrent venous thromboembolism and bleeding on anticoagulation. Thromb Res. 2016;140:S93–8.  https://doi.org/10.1016/S0049-3848(16)30106-2.CrossRefPubMedGoogle Scholar
  17. 17.
    Streiff MB, Milentijevic D, McCrae K, Yannicelli D, Fortier J, Nelson WW, et al. Effectiveness and safety of anticoagulants for the treatment of venous thromboembolism in patients with cancer. Am J Hematol. 2018;93(5):664–71.  https://doi.org/10.1002/ajh.25059.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kamphuisen PW, Lee AYY, Meyer G, Bauersachs R, Janas MS, Jarner MF, et al. Clinically relevant bleeding in cancer patients treated for venous thromboembolism from the CATCH study. J Thromb Haemost. 2018;16(6):1069–77.  https://doi.org/10.1111/jth.14007.CrossRefPubMedGoogle Scholar
  19. 19.
    Farge D, Trujillo-Santos J, Debourdeau P, Bura-Riviere A, Rodriguez-Beltrán EM, Nieto JA, et al. Fatal events in cancer patients receiving anticoagulant therapy for venous thromboembolism. Medicine (Baltimore). 2015;94(32):e1235.  https://doi.org/10.1097/MD.0000000000001235.CrossRefGoogle Scholar
  20. 20.
    van der Wall SJ, Klok FA, den Exter PL, Barrios D, Morillo R, Cannegieter SC, et al. Continuation of low-molecular-weight heparin treatment for cancer-related venous thromboembolism: a prospective cohort study in daily clinical practice. J Thromb Haemost. 2017;15(1):74–9.  https://doi.org/10.1111/jth.13563.CrossRefPubMedGoogle Scholar
  21. 21.
    Mantia C, Uhlmann EJ, Puligandla M, Weber GM, Neuberg D, Zwicker JI. Predicting the higher rate of intracranial hemorrhage in glioma patients receiving therapeutic enoxaparin. Blood. 2017;129(25):3379–85.  https://doi.org/10.1182/blood-2017-02-767285.CrossRefPubMedGoogle Scholar
  22. 22.
    Lee AYY, Kamphuisen PW, Meyer G, Bauersachs R, Janas MS, Jarner MF, et al. Tinzaparin vs warfarin for treatment of acute venous thromboembolism in patients with active cancer. JAMA. 2015;314(7):677.  https://doi.org/10.1001/jama.2015.9243.CrossRefPubMedGoogle Scholar
  23. 23.
    Young AM, Marshall A, Thirlwall J, Chapman O, Lokare A, Hill C, 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(20):2017–23.  https://doi.org/10.1200/JCO.2018.78.8034.CrossRefPubMedGoogle Scholar
  24. 24.
    • Raskob GE, van Es N, Verhamme P, et al. Edoxaban for the treatment of cancer-associated venous thromboembolism. N Engl J Med. 2018;378(7):615–24.  https://doi.org/10.1056/NEJMoa1711948 The study was one of two randomized trials to evaluate the benefit of a DOAC, rivaroxaban, compared to dalteparin monotherapy in treatment. CrossRefPubMedGoogle Scholar
  25. 25.
    Ross JA, Miller MM, Rojas Hernandez CM. Comparative effectiveness and safety of direct oral anticoagulants (DOACs) versus conventional anticoagulation for the treatment of cancer-related venous thromboembolism: a retrospective analysis. Thromb Res. 2017;150:86–9.  https://doi.org/10.1016/j.thromres.2016.12.016.CrossRefPubMedGoogle Scholar
  26. 26.
    Kamphuisen PW, Beyer-Westendorf J. Bleeding complications during anticoagulant treatment in patients with cancer. Thromb Res. 2014;133(SUPPL. 2):S49–55.  https://doi.org/10.1016/S0049-3848(14)50009-6.CrossRefPubMedGoogle Scholar
  27. 27.
    Carrier M, Khorana AA, Zwicker JI, Noble S, Lee AYY. 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(9):1760–5.  https://doi.org/10.1111/jth.12338.CrossRefPubMedGoogle Scholar
  28. 28.
    Lee AYY, Peterson EA. Treatment of cancer-associated thrombosis. Blood. 2013;122(14):2310–8.  https://doi.org/10.1182/blood-2013-04-460162.CrossRefPubMedGoogle Scholar
  29. 29.
    Lee AYY, Levine MN, Baker RI, Bowden C, Kakkar AK, Prins M, 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(2):146–53.  https://doi.org/10.1056/nejmoa025313.CrossRefPubMedGoogle Scholar
  30. 30.
    Carrier M, Cameron C, Delluc A, Castellucci L, Khorana A, Lee AYY. Efficacy and safety of anticoagulant therapy for the treatment of acute cancer-associated thrombosis: a systematic review and meta-analysis. Thromb Res. 2014;134(6):1214–9.  https://doi.org/10.1016/j.thromres.2014.09.039.CrossRefPubMedGoogle Scholar
  31. 31.
    Kahale LA, Hakoum MB, Tsolakian IG, et al. Anticoagulation for the long-term treatment of venous thromboembolism in people with cancer (review). Cochrane Database Syst Rev. 2018;6:CD006650.  https://doi.org/10.1002/14651858.CD006650.pub5.www.cochranelibrary.com.CrossRefPubMedGoogle Scholar
  32. 32.
    Schulman S, How I. Treat How I treat recurrent venous thromboembolism in patients receiving anticoagulant therapy. Blood. 2017;129(25):3285–94.  https://doi.org/10.1182/blood-2017-03-742304.con.CrossRefPubMedGoogle Scholar
  33. 33.
    Kopolovic I, Lee AYY, Wu C. Management and outcomes of cancer-associated venous thromboembolism in patients with concomitant thrombocytopenia: a retrospective cohort study. Ann Hematol. 2015;94(2):329–36.  https://doi.org/10.1007/s00277-014-2198-6.CrossRefPubMedGoogle Scholar
  34. 34.
    Timp JF, Braekkan SK, Versteeg HH, Cannegieter SC. Epidemiology of cancer-associated venous thrombosis. Blood. 2013;122(10):1712–24.  https://doi.org/10.1182/blood-2013-04-460121.CrossRefPubMedGoogle Scholar
  35. 35.
    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;(April):1–6.  https://doi.org/10.1002/rth2.12111
  36. 36.
    • 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(6):1246–9.  https://doi.org/10.1111/jth.14015 This ISTH guidance article provides advice regarding thrombocytopenia in cancer VTE and its effective management. CrossRefPubMedGoogle Scholar
  37. 37.
    Launay-vacher V, Oudard S, Janus N, et al. Prevalence of renal insufficiency in cancer patients and implications for anticancer drug management. Cancer. 2007;110(6):1376–84.  https://doi.org/10.1002/cncr.22904.CrossRefPubMedGoogle Scholar
  38. 38.
    Janus N, Byloos E, Machiels J, et al. Cancer and renal insufficiency results of the BIRMA study. Br J Cancer. 2010;103(12):1815–21.  https://doi.org/10.1038/sj.bjc.6605979.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    • Bauersachs R, Lee AYY, Kamphuisen PW, et al. Renal Impairment, recurrent venous thromboembolism and bleeding in cancer patients with acute venous thromboembolism—analysis of the CATCH study. Thromb Haemost. 2018;118(5):914–21.  https://doi.org/10.1055/s-0038-1641150 This is one of few articles that focus on the incidence and outcomes of anticoagulating cancer patients with renal insufficiency derived from a large study cohort. CrossRefPubMedGoogle Scholar
  40. 40.
    Launay-Vacher V, Aapro M, De Castro G, et al. Renal effects of molecular targeted therapies in oncology: a review by the cancer and the kidney. Ann Oncol. 2015;26(8):1677–84.  https://doi.org/10.1093/annonc/mdv136.CrossRefPubMedGoogle Scholar
  41. 41.
    Jalal DI, Chonchol M, Targher G. Disorders of hemostasis associated with chronic kidney disease. Semin Thromb Hemost. 2010;36(1):34–40.CrossRefGoogle Scholar
  42. 42.
    Kooiman J, den Exter PL, Cannegieter SC, le Cessie S, del Toro J, Sahuquillo JC, et al. Impact of chronic kidney disease on the risk of clinical outcomes in patients with cancer-associated venous thromboembolism during anticoagulant treatment. J Thromb Haemost. 2013;11(11):1968–76.  https://doi.org/10.1111/jth.12411.CrossRefPubMedGoogle Scholar
  43. 43.
    Woodruff S, Feugà ¨r G, Abreu P, Heissler J, Ruiz MT, Jen F. A post hoc analysis of dalteparin versus oral anticoagulant (VKA) therapy for the prevention of recurrent venous thromboembolism (rVTE) in patients with cancer and renal impairment. J Thromb Thrombolysis. 2016;42(4):494–504.  https://doi.org/10.1007/s11239-016-1386-8.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Bauersachs RM. LMWH in cancer patients with renal impairment—better than warfarin? Thromb Res. 2016;140:S160–4.  https://doi.org/10.1016/S0049-3848(16)30116-5.CrossRefPubMedGoogle Scholar
  45. 45.
    Scotté F, Rey JB, Launay-Vacher V. Thrombosis, cancer and renal insufficiency: low molecular weight heparin at the crossroads. Support Care Cancer. 2012;20(12):3033–42.  https://doi.org/10.1007/s00520-012-1590-9.CrossRefPubMedGoogle Scholar
  46. 46.
    •• Riess H, Ay C, Bauersachs R, et al. Use of direct oral anticoagulants in patients with cancer: practical considerations for the management of patients with nausea or vomiting. Oncologist. 2018;23(7):822–39.  https://doi.org/10.1634/theoncologist.2017-0473 This consensus statement provides information regarding how best to manage DOAC therapy in patients with nausea and emesis. CrossRefPubMedGoogle Scholar
  47. 47.
    Khorana AA, Yannicelli D, McCrae KR, et al. Evaluation of US prescription patterns: are treatment guidelines for cancer-associated venous thromboembolism being followed? Thromb Res. 2016;145:51–3.  https://doi.org/10.1016/j.thromres.2016.07.013.CrossRefPubMedGoogle Scholar
  48. 48.
    • Khorana AA, McCrae KR, Milentijevic D, et al. Current practice patterns and patient persistence with anticoagulant treatments for cancer-associated thrombosis. Res Pract Thromb Haemost. 2017;1(1):14–22.  https://doi.org/10.1002/rth2.12002 This paper provides clinical practice information regarding persistence with anticoagulant therapy. CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Cajfinger F, Debourdeau P, Lamblin A, Benatar V, Falvo N, Benhamou Y, et al. Low-molecular-weight heparins for cancer-associated thrombosis: adherence to clinical practice guidelines and patient perception in TROPIQUE, a 409-patient prospective observational study. Thromb Res. 2016;144:85–92.  https://doi.org/10.1016/j.thromres.2016.06.005.CrossRefPubMedGoogle Scholar
  50. 50.
    Mahé I, Sterpu R, Bertoletti L, López-Jiménez L, Mellado Joan M, Trujillo-Santos J, et al. Long-term anticoagulant therapy of patients with venous thromboembolism. What are the practices? PLoS One. 2015;10(6):1–12.  https://doi.org/10.1371/journal.pone.0128741.CrossRefGoogle Scholar
  51. 51.
    Sevestre MA, Belizna C, Durant C, Bosson JL, Vedrine L, Cajfinger F, et al. Compliance with recommendations of clinical practice in the management of venous thromboembolism in cancer: the CARMEN study. J Mal Vasc. 2014;39(3):161–8.  https://doi.org/10.1016/j.jmv.2014.03.001.CrossRefPubMedGoogle Scholar
  52. 52.
    Noble S, Matzdorff A, Maraveyas A, Pisa G, Pisa G. Assessing patients’ anticoagulation preferences for the treatment of cancer-associated thrombosis using conjoint methodology. Haematologica. 2015;100(11):1486–92.  https://doi.org/10.3324/haematol.2015.127126.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kaatz S, Fu AC, AbuDagga A, LaMori J, Bookhart BK, Damaraju CV, et al. Association between anticoagulant treatment duration and risk of venous thromboembolism recurrence and bleeding in clinical practice. Thromb Res. 2014;134(4):807–13.  https://doi.org/10.1016/j.thromres.2014.07.027.CrossRefPubMedGoogle Scholar
  54. 54.
    Rahme E, Feugère G, Sirois C, Weicker S, Ramos E. Anticoagulant use in patients with cancer associated venous thromboembolism: a retrospective cohort study. Thromb Res. 2013;131(3):210–7.  https://doi.org/10.1016/j.thromres.2012.12.004.CrossRefPubMedGoogle Scholar
  55. 55.
    Delate T, Witt DM, Ritzwoller D, Weeks JC, Kushi L, Hornbrook MC, et al. Outpatient use of low molecular weight heparin monotherapy for first-line treatment of venous thromboembolism in advanced cancer. Oncologist. 2012;17:419–27.CrossRefGoogle Scholar
  56. 56.
    Spirk D, Ugi J, Korte W, Husmann M, Hayoz D, Baldi T, et al. Long-term anticoagulation treatment for acute venous thromboembolism in patients with and without cancer the SWIss venous ThromboEmbolism registry (SWIVTER) II. Thromb Haemost. 2011;105(6):962–7.  https://doi.org/10.1160/TH11-01-0002.CrossRefPubMedGoogle Scholar
  57. 57.
    Mahé I, Puget H, Buzzi JC, Lamuraglia M, Chidiac J, Strukov A, et al. Adherence to treatment guidelines for cancer-associated thrombosis: a French hospital-based cohort study. Support Care Cancer. 2016;24(8):3369–77.  https://doi.org/10.1007/s00520-016-3164-8.CrossRefPubMedGoogle Scholar
  58. 58.
    Ussai S, Petelin R, Giordano A, Malinconico M, Cirillo D, Pentimalli F. A pilot study on the impact of known drug-drug interactions in cancer patients. J Exp Clin Cancer Res. 2015;34(1):89.  https://doi.org/10.1186/s13046-015-0201-2.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Hata T, Kudo T, Sakai D, Takahashi H, Haraguchi N, Nishimura J, et al. Impact of capecitabine and S-1 on anticoagulant activity of warfarin in patients with gastrointestinal cancer. Cancer Chemother Pharmacol. 2016;78(2):389–96.  https://doi.org/10.1007/s00280-016-3080-0.CrossRefPubMedGoogle Scholar
  60. 60.
    Shah HR, Ledbetter L, Diasio R, Saif MW. A retrospective study of coagulation abnormalities in patients receiving concomitant capecitabine and warfarin. Clin Colorectal Cancer. 2006;5(5):354–8.  https://doi.org/10.3816/CCC.2006.n.006.CrossRefPubMedGoogle Scholar
  61. 61.
    Camidge R, Reigner B, Cassidy J, Grange S, Abt M, Weidekamm E, et al. Significant effect of capecitabine on the pharmacokinetics and pharmacodynamics of warfarin in patients with cancer. J Clin Oncol. 2005;23(21):4719–25.  https://doi.org/10.1200/JCO.2005.09.129.CrossRefPubMedGoogle Scholar
  62. 62.
    Yano R, Kurokawa T, Tsuyoshi H, et al. Transient elevation of international normalized ratio during cisplatin-based chemotherapy in patients who are taking warfarin. Ann Pharmacother. 2011;45(10).  https://doi.org/10.1345/aph.1Q290.
  63. 63.
    Burnett AE, Mahan CE, Vazquez SR, Oertel LB, Garcia DA, Ansell J. Guidance for the practical management of the direct oral anticoagulants (DOACs) in VTE treatment. J Thromb Thrombolysis. 2016;41(1):206–32.  https://doi.org/10.1007/s11239-015-1310-7.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Voigtlaender M, Langer F. Management of cancer-associated venous thromboembolism—a case-based practical approach. Vasa. 2018;47(2):77–89.  https://doi.org/10.1024/0301-1526/a000684.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Kansas City VA Medical CenterKansas CityUSA
  2. 2.Taussig Cancer Institute, Cleveland ClinicClevelandUSA

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