Incidence, risk factors, and management of bleeding in patients receiving anticoagulants for the treatment of cancer-associated thrombosis.
Anticoagulants
Bleeding
Cancer-associated thrombosis
Direct oral anticoagulants
Low-molecular-weight heparin
Journal
Supportive care in cancer : official journal of the Multinational Association of Supportive Care in Cancer
ISSN: 1433-7339
Titre abrégé: Support Care Cancer
Pays: Germany
ID NLM: 9302957
Informations de publication
Date de publication:
Apr 2022
Apr 2022
Historique:
received:
08
08
2021
accepted:
26
09
2021
pubmed:
8
10
2021
medline:
23
2
2022
entrez:
7
10
2021
Statut:
ppublish
Résumé
Updated clinical practice guidelines recommend the long-term use of low-molecular-weight heparins or direct oral anticoagulants as the preferred option for the treatment of cancer-associated thrombosis (CAT), using a personalized approach matching the right drug to the right patient. In most cases, the benefit of anticoagulant therapy outweighs the risk. However, the long-term use of anticoagulants is associated with a non-negligible risk of bleeding, which constitutes a rare but serious adverse effect. Bleeding complications have been reported to be overall 2 to 3 times more frequent in cancer patients with CAT receiving anticoagulation than in non-cancer patients, with a reported incidence of major bleeding ranging from 2.4 to 16.0% in randomized controlled trials (RCT). In the absence of validated risk assessment model to predict the risk of bleeding in these patients, a careful evaluation of each individual profile, with adequate selection of the most appropriate anticoagulant for each individual patient, is warranted for overcoming management challenges, taking in account the numerous factors which may potentiate the overall bleeding risk in these complex patients, such as advanced or metastatic disease, older age, anemia, thrombocytopenia, renal impairment, liver dysfunction, and concomitant anticancer therapies. The purpose of this review is to call for awareness on bleeding complications as a major safety issue of CAT treatment and to summarize data from recent RCT and real-world studies on the incidence and risk factors for bleeding in this unique and challenging population to further help clinicians in decision-making.
Identifiants
pubmed: 34617159
doi: 10.1007/s00520-021-06598-8
pii: 10.1007/s00520-021-06598-8
doi:
Substances chimiques
Anticoagulants
0
Heparin, Low-Molecular-Weight
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2919-2931Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Timp JF, Braekkan SK, Versteeg HH, Cannegieter SC (2013) Epidemiology of cancer-associated venous thrombosis. Blood 122:1712–1723
pubmed: 23908465
Mulder FI, Horvath-Puho E, van Es N, van Laarhoven HWM, Pedersen L, Moik F, Ay C, Buller HR, Sorensen HT (2021) Venous thromboembolism in cancer patients: a population-based cohort study. Blood 137:1959–1969
pubmed: 33171494
Meyer G, Marjanovic Z, Valcke J, Lorcerie B, Gruel Y, Solal-Celigny P, Le Maignan C, Extra JM, Cottu P, Farge D (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 162:1729–1735
pubmed: 12153376
Lee AY, Levine MN, Baker RI, Bowden C, Kakkar AK, Prins M, Rickles FR, Julian JA, Haley S, Kovacs MJ, Gent M, Comparison R, of Low-Molecular-Weight Heparin versus Oral Anticoagulant Therapy for the Prevention of Recurrent Venous Thromboembolism in Patients with Cancer I, (2003) 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
pubmed: 12853587
Hull RD, Pineo GF, Brant RF, Mah AF, Burke N, Dear R, Wong T, Cook R, Solymoss S, Poon MC, Raskob G, Investigators LT (2006) Long-term low-molecular-weight heparin versus usual care in proximal-vein thrombosis patients with cancer. Am J Med 119:1062–1072
pubmed: 17145251
Deitcher SR, Kessler CM, Merli G, Rigas JR, Lyons RM, Fareed J, Investigators O (2006) Secondary prevention of venous thromboembolic events in patients with active cancer: enoxaparin alone versus initial enoxaparin followed by warfarin for a 180-day period. Clin Appl Thromb Hemost 12:389–396
pubmed: 17000884
Lee AYY, Kamphuisen PW, Meyer G, Bauersachs R, Janas MS, Jarner MF, Khorana AA, Investigators C (2015) Tinzaparin vs warfarin for treatment of acute venous thromboembolism in patients with active cancer: a randomized clinical trial. JAMA 314:677–686
pubmed: 26284719
Raskob GE, van Es N, Verhamme P, Carrier M, Di Nisio M, Garcia D, Grosso MA, Kakkar AK, Kovacs MJ, Mercuri MF, Meyer G, Segers A, Shi M, Wang TF, Yeo E, Zhang G, Zwicker JI, Weitz JI, Buller HR, Hokusai VTECI (2018) Edoxaban for the Treatment of Cancer-Associated Venous Thromboembolism. N Engl J Med 378:615–624
pubmed: 29231094
Young AM, Marshall A, Thirlwall J, Chapman O, Lokare A, Hill C, Hale D, Dunn JA, Lyman GH, Hutchinson C, MacCallum P, Kakkar A, Hobbs FDR, Petrou S, Dale J, Poole CJ, Maraveyas A, Levine M (2018) 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 36:2017–2023
pubmed: 29746227
McBane RD 2nd, Wysokinski WE, Le-Rademacher JG, Zemla T, Ashrani A, Tafur A, Perepu U, Anderson D, Gundabolu K, Kuzma C, Perez Botero J, Leon Ferre RA, Henkin S, Lenz CJ, Houghton DE, Vishnu P, Loprinzi CL (2020) Apixaban and dalteparin in active malignancy-associated venous thromboembolism: the ADAM VTE trial. J Thromb Haemost 18:411–421
pubmed: 31630479
Agnelli G, Becattini C, Meyer G, Munoz A, Huisman MV, Connors JM, Cohen A, Bauersachs R, Brenner B, Torbicki A, Sueiro MR, Lambert C, Gussoni G, Campanini M, Fontanella A, Vescovo G, Verso M, Caravaggio I (2020) Apixaban for the Treatment of Venous Thromboembolism Associated with Cancer. N Engl J Med 382:1599–1607
pubmed: 32223112
Farge D, Frere C, Connors JM, Ay C, Khorana AA, Munoz A, Brenner B, Kakkar A, Rafii H, Solymoss S, Brilhante D, Monreal M, Bounameaux H, Pabinger I, Douketis J (2019) 2019 international clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer. Lancet Oncol 20:e566–e581
pubmed: 31492632
National Comprehensive Cancer Network (2020) Guideline on Cancer‐Associated Venous Thromboembolic Disease (Version 1.2020) https://www.nccn.org/professionals/physician_gls/pdf/vte.pdf February 13, 2021
Sanchez O, Benhamou Y, Bertoletti L, Constant J, Couturaud F, Delluc A, Elias A, Fischer AM, Frappe P, Gendron N, Girard P, Godier A, Gut-Gobert C, Laporte S, Mahe I, Mauge L, Meneveau N, Meyer G, Mismetti P, Parent F, Pernod G, Quere I, Revel MP, Roy PM, Salaun PY, Smadja DM, Sevestre MA (2019) Recommendations of good practice for the management of thromboembolic venous disease in adults. Short version. Rev Mal Respir 36:249–283
pubmed: 30799126
Lyman GH, Carrier M, Ay C, Di Nisio M, Hicks LK, Khorana AA, Leavitt AD, Lee AYY, Macbeth F, Morgan RL, Noble S, Sexton EA, Stenehjem D, Wiercioch W, Kahale LA, Alonso-Coello P (2021) American Society of Hematology 2021 guidelines for management of venous thromboembolism: prevention and treatment in patients with cancer. Blood Adv 5:927–974
pubmed: 33570602
pmcid: 7903232
Key NS, Khorana AA, Kuderer NM, Bohlke K, Lee AYY, Arcelus JI, Wong SL, Balaban EP, Flowers CR, Francis CW, Gates LE, Kakkar AK, Levine MN, Liebman HA, Tempero MA, Lyman GH, Falanga A (2020) Venous thromboembolism prophylaxis and treatment in patients with cancer: ASCO Clinical Practice Guideline Update. J Clin Oncol 38:496–520
pubmed: 31381464
Prandoni P, Lensing AW, Piccioli A, Bernardi E, Simioni P, Girolami B, Marchiori A, Sabbion P, Prins MH, Noventa F, Girolami A (2002) Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 100:3484–3488
pubmed: 12393647
Schulman S, Kearon C (2005) Definition of major bleeding in clinical investigations of antihemostatic medicinal products in non-surgical patients. J Thromb Haemost 3:692–694
pubmed: 15842354
Kaatz S, Ahmad D, Spyropoulos AC, Schulman S (2015) Definition of clinically relevant non-major bleeding in studies of anticoagulants in atrial fibrillation and venous thromboembolic disease in non-surgical patients: communication from the SSC of the ISTH. J Thromb Haemost 13:2119–2126
pubmed: 26764429
Kahale LA, Hakoum MB, Tsolakian IG, Matar CF, Terrenato I, Sperati F, Barba M, Yosuico VE, Schunemann H, Akl EA (2018) Anticoagulation for the long-term treatment of venous thromboembolism in people with cancer. Cochrane Database Syst Rev 6: CD006650
Kamphuisen PW, Lee AYY, Meyer G, Bauersachs R, Janas MS, Jarner MF, Khorana AA, Investigators C (2018) Clinically relevant bleeding in cancer patients treated for venous thromboembolism from the CATCH study. J Thromb Haemost 16:1069–1077
pubmed: 29573330
Mulder FI, Bosch FTM, Young AM, Marshall A, McBane RD, Zemla TJ, Carrier M, Kamphuisen PW, Bossuyt PMM, Buller HR, Weitz JI, Middeldorp S, van Es N (2020) Direct oral anticoagulants for cancer-associated venous thromboembolism: a systematic review and meta-analysis. Blood 136:1433–1441
pubmed: 32396939
Giustozzi M, Agnelli G, Del Toro-Cervera J, Klok FA, Rosovsky RP, Martin AC, Herold J, Tzoran I, Szmit S, Bertoletti L, Becattini C, Huisman MV (2020) Direct oral anticoagulants for the treatment of acute venous thromboembolism associated with cancer: a systematic review and meta-analysis. Thromb Haemost 120:1128–1136
pubmed: 32365386
Tao E, Luo YL, Tao Z, Wan L (2020) A meta-analysis of bridging anticoagulation between low molecular weight heparin and heparin. Medicine (Baltimore) 99:e18729
Moik F, Posch F, Zielinski C, Pabinger I, Ay C (2020) Direct oral anticoagulants compared to low-molecular-weight heparin for the treatment of cancer-associated thrombosis: updated systematic review and meta-analysis of randomized controlled trials. Res Pract Thromb Haemost 4:550–561
pubmed: 32548553
pmcid: 7292654
Trujillo-Santos J, Nieto JA, Ruíz-Gamietea Á, López-Jiménez L, García-Bragado F, Quintavalla R, Monreal M (2010) Bleeding complications associated with anticoagulant therapy in patients with cancer. Thromb Res 125:S58–S61
pubmed: 20434007
Moustafa F, Giorgi Pierfranceschi M, Di Micco P, Bucherini E, Lorenzo A, Villalobos A, Nieto JA, Valero B, Samperiz AL, Monreal M, Investigators R (2017) Clinical outcomes during anticoagulant therapy in fragile patients with venous thromboembolism. Res Pract Thromb Haemost 1:172–179
pubmed: 30046687
pmcid: 6058265
Angelini DE, Radivoyevitch T, McCrae KR, Khorana AA (2019) Bleeding incidence and risk factors among cancer patients treated with anticoagulation. Am J Hematol 94:780–785
pubmed: 31006890
Francis CW, Kessler CM, Goldhaber SZ, Kovacs MJ, Monreal M, Huisman MV, Bergqvist D, Turpie AG, Ortel TL, Spyropoulos AC, Pabinger I, Kakkar AK (2015) Treatment of venous thromboembolism in cancer patients with dalteparin for up to 12 months: the DALTECAN Study. J Thromb Haemost 13:1028–1035
pubmed: 25827941
Jara-Palomares L, Solier-Lopez A, Elias-Hernandez T, Asensio-Cruz M, Blasco-Esquivias I, Marin-Barrera L, de la Borbolla-Artacho MR, Praena-Fernandez JM, Montero-Romero E, Navarro-Herrero S, Serrano-Gotarredona MP, Sanchez-Diaz JM, Palacios C, Otero R (2017) Tinzaparin in cancer associated thrombosis beyond 6months: TiCAT study. Thromb Res 157:90–96
pubmed: 28719850
Mahe I, Plaisance L, Chapelle C, Laporte S, Planquette B, Bertoletti L, Couturaud F, Falvo N, Falchero L, Mahe I, Helfer H, Chidiac J, Meyer G (2020) Long-term treatment of cancer-associated thrombosis (CAT) beyond 6 months in the medical practice: USCAT, a 432-Patient Retrospective Non-Interventional Study. Cancers (Basel) 12
Mahe I, Chidiac J, Bertoletti L, Font C, Trujillo-Santos J, Peris M, Perez Ductor C, Nieto S, Grandone E, Monreal M, investigators R, (2017) The clinical course of venous thromboembolism may differ according to cancer site. Am J Med 130:337–347
pubmed: 27884650
Porfidia A, Giordano M, Sturiale CL, D’Arrigo S, Donadini MP, Olivi A, Ageno W, Pola R (2020) Risk of intracranial bleeding in patients with primary brain cancer receiving therapeutic anticoagulation for venous thromboembolism: a meta-analysis. Brain Behav 10:e01638
pubmed: 32314875
pmcid: 7303369
Trujillo-Santos J, Nieto JA, Tiberio G, Piccioli A, Di Micco P, Prandoni P, Monreal M, Registry R (2008) Predicting recurrences or major bleeding in cancer patients with venous thromboembolism. Findings from the RIETE. Registry Thromb Haemost 100:435–439
pubmed: 18766259
Zwicker JI, Karp Leaf R, Carrier M (2016) A meta-analysis of intracranial hemorrhage in patients with brain tumors receiving therapeutic anticoagulation. J Thromb Haemost 14:1736–1740
pubmed: 27306689
Leader A, Hamulyak EN, Carney BJ, Avrahami M, Knip JJ, Rozenblatt S, Beenen LFM, Yust-Katz S, Icht O, Coppens M, Raanani P, Middeldorp S, Buller HR, Zwicker JI, Spectre G (2020) Intracranial hemorrhage with direct oral anticoagulants in patients with brain metastases. Blood Adv 4:6291–6297
pubmed: 33351124
pmcid: 7756985
Moik F, Pabinger I, Ay C (2020) How I treat cancer-associated thrombosis. ESMO Open 5:e000610
pubmed: 31958288
Lalla RV, Bowen J, Barasch A, Elting L, Epstein J, Keefe DM, McGuire DB, Migliorati C, Nicolatou-Galitis O, Peterson DE, Raber-Durlacher JE, Sonis ST, Elad S, Mucositis guidelines leadership group of the multinational association of supportive care in C, International Society of Oral O (2014) MASCC/ISOO clinical practice guidelines for the management of mucositis secondary to cancer therapy. Cancer 120:1453–1461
Wang Y, Abu-Sbeih H, Mao E, Ali N, Ali FS, Qiao W, Lum P, Raju G, Shuttlesworth G, Stroehlein J, Diab A (2018) Immune-checkpoint inhibitor-induced diarrhea and colitis in patients with advanced malignancies: retrospective review at MD Anderson. J Immunother Cancer 6:37
pubmed: 29747688
pmcid: 5946546
Som A, Mandaliya R, Alsaadi D, Farshidpour M, Charabaty A, Malhotra N, Mattar MC (2019) Immune checkpoint inhibitor-induced colitis: a comprehensive review. World J Clin Cases 7:405–418
pubmed: 30842952
pmcid: 6397821
Bapatla A, Tariq T, Haider MB, Mohamad B (2021) Atezolizumab, a PD-L1 inhibitor: an association of bleeding gastric ulcer with its use. Cureus 13:e15637
pubmed: 34150414
pmcid: 8208334
Kuperman A, Lopez-Reyes R, Bosco LJ, Lorenzo A, Jose B, Farge Bancel D, Alfonso M, Lumbierres M, Stemer G, Monreal Bosch M, Braester A, Investigators R (2018) Anemia and bleeding in patients receiving anticoagulant therapy for venous thromboembolism. J Thromb Thrombolysis 45:360–368
pubmed: 29383557
National Comprehensive Cancer Network (2012) Guideline on cancer and chemotherapy-induced anemia (Version 2.2012) https://www.nccn.org/professionals/physician_gls/pdf/growthfactors.pdf . February 13, 2021
Dicato M, Plawny L, Diederich M (2010) Anemia in cancer. Ann Oncol 21 Suppl 7: vii167-172
Di Micco P, Ruiz-Gimenez N, Nieto JA, Aujesky D, del Molino F, Valle R, Barron M, Maestre A, Monreal M, investigators R, (2013) Platelet count and outcome in patients with acute venous thromboembolism. Thromb Haemost 110:1025–1034
pubmed: 23925476
Mones JV, Soff G (2019) Management of thrombocytopenia in cancer patients cancer treatment and research 179:139–150
pubmed: 31317485
Samuelson Bannow BT, Lee A, Khorana AA, Zwicker JI, Noble S, Ay C, Carrier M (2018) Management of cancer-associated thrombosis in patients with thrombocytopenia: guidance from the SSC of the ISTH. J Thromb Haemost 16:1246–1249
pubmed: 29737593
Liebman HA (2014) Thrombocytopenia in cancer patients. Thromb Res 133(Suppl 2):S63-69
pubmed: 24862148
Launay-Vacher V, Oudard S, Janus N, Gligorov J, Pourrat X, Rixe O, Morere JF, Beuzeboc P, Deray G, Renal I, Cancer Medications Study G (2007) Prevalence of renal insufficiency in cancer patients and implications for anticancer drug management: the renal insufficiency and anticancer medications (IRMA) study. Cancer 110:1376–1384
Yoshida E, Fujimura Y, Ikeda Y, Takeda I, Yamamoto Y, Nishikawa K, Miyataka K, Oonuki M, Kawasaki T, Katayama M et al (1995) Impaired high-shear-stress-induced platelet aggregation in patients with chronic renal failure undergoing haemodialysis. Br J Haematol 89:861–867
pubmed: 7772523
Dager WE, Kiser TH (2010) Systemic anticoagulation considerations in chronic kidney disease. Adv Chronic Kidney Dis 17:420–427
pubmed: 20727512
Remuzzi G, Marchesi D, Livio M, Cavenaghi AE, Mecca G, Donati MB, de Gaetano G (1978) Altered platelet and vascular prostaglandin-generation in patients with renal failure and prolonged bleeding times. Thromb Res 13:1007–1015
pubmed: 373157
Woodruff S, Feugere G, Abreu P, Heissler J, Ruiz MT, Jen F (2016) 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 42:494–504
pubmed: 27344439
pmcid: 5040733
Bauersachs R, Lee AYY, Kamphuisen PW, Meyer G, Janas MS, Jarner MF, Khorana AA, Investigators C (2018) Renal impairment, recurrent venous thromboembolism and bleeding in cancer patients with acute venous thromboembolism-analysis of the CATCH Study. Thromb Haemost 118: 914-921
Projean D, Lalonde S, Morin J, Nogues E, Seguin A, Vincent A, Lafrance JP, Masson V, Kassis J, Fafard J, Lordkipanidze M (2018) Study of the bioaccumulation of tinzaparin in renally impaired patients when given at prophylactic doses—the STRIP study. Thromb Res 174:48–50
pubmed: 30554045
Krens SD, Lassche G, Jansman FGA, Desar IME, Lankheet NAG, Burger DM, van Herpen CML, van Erp NP (2019) Dose recommendations for anticancer drugs in patients with renal or hepatic impairment. Lancet Oncol 20:e200–e207
pubmed: 30942181
Barnett K, Mercer SW, Norbury M, Watt G, Wyke S, Guthrie B (2012) Epidemiology of multimorbidity and implications for health care, research, and medical education: a cross-sectional study. The Lancet 380:37–43
Nightingale G, Hajjar E, Swartz K, Andrel-Sendecki J, Chapman A (2015) Evaluation of a pharmacist-led medication assessment used to identify prevalence of and associations with polypharmacy and potentially inappropriate medication use among ambulatory senior adults with cancer. J Clin Oncol 33:1453–1459
pubmed: 25800766
Vanassche T, Verhamme P, Wells PS, Segers A, Ageno W, Brekelmans MPA, Chen CZ, Cohen AT, Grosso MA, Medina AP, Mercuri MF, Winters SM, Zhang G, Weitz JI, Raskob GE, Buller HR (2018) Impact of age, comorbidity, and polypharmacy on the efficacy and safety of edoxaban for the treatment of venous thromboembolism: An analysis of the randomized, double-blind Hokusai-VTE trial. Thromb Res 162:7–14
pubmed: 29248859
Bellesoeur A, Thomas-Schoemann A, Allard M, Smadja D, Vidal M, Alexandre J, Goldwasser F, Blanchet B (2018) Pharmacokinetic variability of anticoagulants in patients with cancer-associated thrombosis: clinical consequences. Crit Rev Oncol Hematol 129:102–112
pubmed: 30097228
Lee JY, Oh IY, Lee JH, Kim SY, Kwon SS, Yang HJ, Kim YK, Bang SM (2020) The increased risk of bleeding due to drug-drug interactions in patients administered direct oral anticoagulants. Thromb Res 195:243–249
pubmed: 32823239
Hanigan S, Das J, Pogue K, Barnes GD, Dorsch MP (2020) The real world use of combined P-glycoprotein and moderate CYP3A4 inhibitors with rivaroxaban or apixaban increases bleeding. J Thromb Thrombolysis 49:636–643
pubmed: 31925665
Sychev D, Mirzaev K, Cherniaeva M, Kulikova M, Bochkov P, Shevchenko R, Gorbatenkova S, Golovina O, Ostroumova O, Bahteeva D, Rytkin E (2020) Drug-drug interaction of rivaroxaban and calcium channel blockers in patients aged 80 years and older with nonvalvular atrial fibrillation. Drug Metab Pers Ther 35
Testa S, Prandoni P, Paoletti O, Morandini R, Tala M, Dellanoce C, Giorgi-Pierfranceschi M, Betti M, Danzi GB, Pan A, Palareti G (2020) Direct oral anticoagulant plasma levels’ striking increase in severe COVID-19 respiratory syndrome patients treated with antiviral agents: The Cremona experience. J Thromb Haemost 18:1320–1323
pubmed: 32329231
Corsini A, Ferri N, Proietti M, Boriani G (2020) Edoxaban and the issue of drug-drug interactions: from pharmacology to clinical practice. Drugs 80:1065–1083
pubmed: 32504376
Santini D, Citarella F, Vincenzi B, Russano M, Tonini G, Stellato M (2019) Cabozantinib and apixaban: an hitherto unreported interaction. Exp Hematol Oncol 8:22
pubmed: 31528502
pmcid: 6737677
Beyth RJ, Quinn LM, Landefeld CS (1998) Prospective evaluation of an index for predicting the risk of major bleeding in outpatients treated with warfarin. Am J Med 105:91–99
pubmed: 9727814
Kearon C, Ginsberg JS, Kovacs MJ, Anderson DR, Wells P, Julian JA, MacKinnon B, Weitz JI, Crowther MA, Dolan S, Turpie AG, Geerts W, Solymoss S, van Nguyen P, Demers C, Kahn SR, Kassis J, Rodger M, Hambleton J, Gent M, Extended low-intensity anticoagulation for thrombo-embolism I, (2003) comparison of low-intensity warfarin therapy with conventional-intensity warfarin therapy for long-term prevention of recurrent venous thromboembolism. N Engl J Med 349:631–639
pubmed: 12917299
Kuijer PM, Hutten BA, Prins MH, Buller HR (1999) Prediction of the risk of bleeding during anticoagulant treatment for venous thromboembolism. Arch Intern Med 159:457–460
pubmed: 10074953
Pisters R, Lane DA, Nieuwlaat R, de Vos CB, Crijns HJ, Lip GY (2010) A novel user-friendly score (HAS-BLED) to assess 1-year risk of major bleeding in patients with atrial fibrillation: the Euro Heart Survey. Chest 138:1093–1100
pubmed: 20299623
Decousus H, Tapson VF, Bergmann JF, Chong BH, Froehlich JB, Kakkar AK, Merli GJ, Monreal M, Nakamura M, Pavanello R, Pini M, Piovella F, Spencer FA, Spyropoulos AC, Turpie AG, Zotz RB, Fitzgerald G, Anderson FA (2011) Factors at admission associated with bleeding risk in medical patients: findings from the IMPROVE investigators. Chest 139:69–79
pubmed: 20453069
Ruiz-Gimenez N, Suarez C, Gonzalez R, Nieto JA, Todoli JA, Samperiz AL, Monreal M, Investigators R (2008) Predictive variables for major bleeding events in patients presenting with documented acute venous thromboembolism. Findings from the RIETE Registry Thromb Haemost 100:26–31
pubmed: 18612534
Klok FA, Hosel V, Clemens A, Yollo WD, Tilke C, Schulman S, Lankeit M, Konstantinides SV (2016) Prediction of bleeding events in patients with venous thromboembolism on stable anticoagulation treatment. Eur Respir J 48:1369–1376
pubmed: 27471209
Klok FA, Niemann C, Dellas C, Hasenfuss G, Konstantinides S, Lankeit M (2016) Performance of five different bleeding-prediction scores in patients with acute pulmonary embolism. J Thromb Thrombolysis 41:312–320
pubmed: 26091712
Kearon C, Akl EA, Ornelas J, Blaivas A, Jimenez D, Bounameaux H, Huisman M, King CS, Morris TA, Sood N, Stevens SM, Vintch JRE, Wells P, Woller SC, Moores L (2016) Antithrombotic therapy for VTE disease: CHEST Guideline and Expert Panel Report. Chest 149:315–352
pubmed: 26867832
Carrier M, Blais N, Crowther M, Kavan P, Le Gal G, Moodley O, Shivakumar S, Tagalakis V, Wu C, Lee AYY (2018) Treatment algorithm in cancer-associated thrombosis: Canadian expert consensus. Curr Oncol 25:329–337
pubmed: 30464682
pmcid: 6209545
Pernod G, Joly M, Sonnet B (2020) Direct oral anticoagulant (DOAC) versus low-molecular-weight heparin (LMWH) for the treatment of cancer-associated thrombosis (which agent for which patient). JMV-Journal de Médecine Vasculaire 45: 6S17–16S23
Piran S, Schulman S (2019) Treatment of bleeding complications in patients on anticoagulant therapy. Blood 133:425–435
pubmed: 30559261
Majeed A, Goldhaber SZ, Kakkar A, Kearon C, Eriksson H, Kreuzer J, Feuring M, Hantel S, Friedman J, Schellong S, Schulman S (2016) Bleeding events with dabigatran or warfarin in patients with venous thromboembolism. Thromb Haemost 115:291–298
pubmed: 26403199
Atiq F, van den Bemt PM, Leebeek FW, van Gelder T, Versmissen J (2015) A systematic review on the accumulation of prophylactic dosages of low-molecular-weight heparins (LMWHs) in patients with renal insufficiency. Eur J Clin Pharmacol 71:921–929
pubmed: 26071276
pmcid: 4500846
Bertoletti L, Ollier E, Duvillard C, Delavenne X, Beyens MN, De Magalhaes E, Bellet F, Basset T, Mismetti P, Laporte S (2017) Direct oral anticoagulants: current indications and unmet needs in the treatment of venous thromboembolism. Pharmacol Res 118:33–42
pubmed: 27350265
Al-Samkari H, Connors JM (2018) The role of direct oral anticoagulants in treatment of cancer-associated thrombosis. Cancers (Basel) 10:271