Download PDF
Hamostaseologie
DOI: 10.1055/a-2284-5855
Review Article

Cardio-Oncology: A New Discipline in Medicine and Its Relevance to Hematology

Andreas Spannbauer
1   Department of Cardiology, Medical University of Vienna, Vienna, Austria
,
Jutta Bergler-Klein
1   Department of Cardiology, Medical University of Vienna, Vienna, Austria
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

Cardio-oncology, a burgeoning subspecialty, addresses the complex interplay between cardiology and oncology, particularly in light of increased cardiovascular (CV) disease mortality in cancer patients. This review provides a comprehensive overview of cardio-oncology with a focus on the therapies used in hematological malignancies. We explore the bidirectional relationship between heart failure and cancer, emphasizing the need for collaborative care. The review discusses risk stratification, highlighting the importance of baseline CV risk assessment and personalized surveillance regimens. Primary and secondary prevention strategies, including pharmacological interventions, are outlined. The review also delves into the cardiotoxicity associated with hematological cancer therapies, focusing on anthracyclines, Bruton kinase inhibitors, BCR-ABL tyrosine kinase inhibitors, CAR-T cell therapy, immune checkpoint inhibitors, multiple myeloma treatments, and hematopoietic stem cell transplantation. We then highlight the high risk of venous and arterial thromboembolisms in cancer patients and the challenges of anticoagulation management in cardio-oncology. Finally, the review touches on the importance of long-term follow-up and appropriate screening in cancer survivors at high risk of CV morbidity and mortality, based on their CV risk profile and the type and dose of cardiotoxic therapies they received such as anthracyclines or high radiation doses.

Keywords

cardio-oncology - cardiotoxicity - thrombosis - prevention


Publication History

Received: 02 November 2023

Accepted: 28 March 2024

Article published online:
09 May 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Sturgeon KM, Deng L, Bluethmann SM. et al. A population-based study of cardiovascular disease mortality risk in US cancer patients. Eur Heart J 2019; 40 (48) 3889-3897
    CrossrefPubMedGoogle Scholar
  • 2 Herrmann J. From trends to transformation: where cardio-oncology is to make a difference. Eur Heart J 2019; 40 (48) 3898-3900
    CrossrefPubMedGoogle Scholar
  • 3 Armenian SH, Xu L, Ky B. et al. Cardiovascular Disease among survivors of adult-onset cancer: a community-based retrospective cohort study. J Clin Oncol 2016; 34 (10) 1122-1130
    CrossrefPubMedGoogle Scholar
  • 4 Lyon AR, López-Fernández T, Couch LS. et al; ESC Scientific Document Group. 2022 ESC Guidelines on cardio-oncology developed in collaboration with the European Hematology Association (EHA), the European Society for Therapeutic Radiology and Oncology (ESTRO) and the International Cardio-Oncology Society (IC-OS). Eur Heart J 2022; 43 (41) 4229-4361
    CrossrefPubMedGoogle Scholar
  • 5 Chao C, Xu L, Bhatia S. et al. Cardiovascular disease risk profiles in survivors of adolescent and young adult (AYA) cancer: the Kaiser Permanente AYA Cancer Survivors study. J Clin Oncol 2016; 34 (14) 1626-1633
    CrossrefPubMedGoogle Scholar
  • 6 Lau ES, Paniagua SM, Liu E. et al. Cardiovascular risk factors are associated with future cancer. JACC Cardiooncol 2021; 3 (01) 48-58
    CrossrefPubMedGoogle Scholar
  • 7 Aboumsallem JP, Moslehi J, de Boer RA. Reverse cardio-oncology: cancer development in patients with cardiovascular disease. J Am Heart Assoc 2020; 9 (02) e013754
    CrossrefPubMedGoogle Scholar
  • 8 Jaiswal V, Ang SP, Agrawal V. et al. Association between heart failure and the incidence of cancer: a systematic review and meta-analysis. Eur Heart J Open 2023; 3 (05) oead073
    CrossrefPubMedGoogle Scholar
  • 9 Jaiswal S, Natarajan P, Silver AJ. et al. Clonal hematopoiesis and risk of atherosclerotic cardiovascular disease. N Engl J Med 2017; 377 (02) 111-121
    CrossrefPubMedGoogle Scholar
  • 10 Mas-Peiro S, Hoffmann J, Fichtlscherer S. et al. Clonal haematopoiesis in patients with degenerative aortic valve stenosis undergoing transcatheter aortic valve implantation. Eur Heart J 2020; 41 (08) 933-939
    CrossrefPubMedGoogle Scholar
  • 11 Mas-Peiro S, Pergola G, Berkowitsch A. et al. Long-term risk associated with clonal hematopoiesis in patients with severe aortic valve stenosis undergoing TAVR. Clin Res Cardiol 2023; 112 (05) 585-593
    CrossrefPubMedGoogle Scholar
  • 12 Sikking MA, Stroeks SLVM, Waring OJ. et al. Clonal hematopoiesis of indeterminate potential from a heart failure specialist's point of view. J Am Heart Assoc 2023; 12 (15) e030603
    CrossrefPubMedGoogle Scholar
  • 13 Assmus B, Cremer S, Kirschbaum K. et al. Clonal haematopoiesis in chronic ischaemic heart failure: prognostic role of clone size for DNMT3A- and TET2-driver gene mutations. Eur Heart J 2021; 42 (03) 257-265
    CrossrefPubMedGoogle Scholar
  • 14 Fidler TP, Xue C, Yalcinkaya M. et al. The AIM2 inflammasome exacerbates atherosclerosis in clonal haematopoiesis. Nature 2021; 592 (7853) 296-301
    CrossrefPubMedGoogle Scholar
  • 15 Fuster JJ, MacLauchlan S, Zuriaga MA. et al. Clonal hematopoiesis associated with TET2 deficiency accelerates atherosclerosis development in mice. Science 2017; 355 (6327) 842-847
    CrossrefPubMedGoogle Scholar
  • 16 Nakao T, Natarajan P. Clonal hematopoiesis, multi-omics and coronary artery disease. Nat Cardiovasc Res 2022; 1 (11) 965-967
    CrossrefPubMedGoogle Scholar
  • 17 Svensson EC, Madar A, Campbell CD. et al. TET2-Driven clonal hematopoiesis and response to canakinumab: an exploratory analysis of the CANTOS randomized clinical trial. JAMA Cardiol 2022; 7 (05) 521-528
    CrossrefPubMedGoogle Scholar
  • 18 Lyon AR, Dent S, Stanway S. et al. Baseline cardiovascular risk assessment in cancer patients scheduled to receive cardiotoxic cancer therapies: a position statement and new risk assessment tools from the Cardio-Oncology Study Group of the Heart Failure Association of the European Society of Cardiology in collaboration with the International Cardio-Oncology Society. Eur J Heart Fail 2020; 22 (11) 1945-1960
    CrossrefPubMedGoogle Scholar
  • 19 Sanfilippo KM, Keller J, Gage BF. et al. Statins are associated with reduced mortality in multiple myeloma. J Clin Oncol 2016; 34 (33) 4008-4014
    CrossrefPubMedGoogle Scholar
  • 20 Afzal A, Fiala MA, Gage BF, Wildes TM, Sanfilippo K. Statins reduce mortality in multiple myeloma: a population-based US study. Clin Lymphoma Myeloma Leuk 2020; 20 (12) e937-e943
    CrossrefPubMedGoogle Scholar
  • 21 Yang J, Li C, Shen Y. et al. Impact of statin use on cancer-specific mortality and recurrence: a meta-analysis of 60 observational studies. Medicine (Baltimore) 2020; 99 (14) e19596
    CrossrefPubMedGoogle Scholar
  • 22 Kim J, Choi E-A, Han Y-E. et al. Association between statin use and all-cause mortality in cancer survivors, based on the Korean health insurance service between 2002 and 2015. Nutr Metab Cardiovasc Dis 2020; 30 (03) 434-440
    CrossrefPubMedGoogle Scholar
  • 23 Ren Q-W, Yu S-Y, Teng TK. et al. Statin associated lower cancer risk and related mortality in patients with heart failure. Eur Heart J 2021; 42 (32) 3049-3059
    CrossrefPubMedGoogle Scholar
  • 24 Neilan TG, Quinaglia T, Onoue T. et al. Atorvastatin for anthracycline-associated cardiac dysfunction: the STOP-CA randomized clinical trial. JAMA 2023; 330 (06) 528-536
    CrossrefPubMedGoogle Scholar
  • 25 Williams B, Mancia G, Spiering W. et al; ESC Scientific Document Group. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur Heart J 2018; 39 (33) 3021-3104
    CrossrefPubMedGoogle Scholar
  • 26 Protani M, Coory M, Martin JH. Effect of obesity on survival of women with breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat 2010; 123 (03) 627-635
    CrossrefPubMedGoogle Scholar
  • 27 Speck RM, Courneya KS, Mâsse LC, Duval S, Schmitz KH. An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. J Cancer Surviv 2010; 4 (02) 87-100
    CrossrefPubMedGoogle Scholar
  • 28 Mazzoni A-S, Helgesen Bjørke AC, Stenling A. et al. The role of long-term physical activity in relation to cancer-related health outcomes: a 12-month follow-up of the Phys-Can RCT. Integr Cancer Ther 2023; 22: 15 347354231178869
    PubMedGoogle Scholar
  • 29 Armenian SH, Yang D, Teh JB. et al. Prediction of cardiovascular disease among hematopoietic cell transplantation survivors. Blood Adv 2018; 2 (14) 1756-1764
    CrossrefPubMedGoogle Scholar
  • 30 van Nimwegen FA, Schaapveld M, Janus CPM. et al. Cardiovascular disease after Hodgkin lymphoma treatment: 40-year disease risk. JAMA Intern Med 2015; 175 (06) 1007-1017
    CrossrefPubMedGoogle Scholar
  • 31 Arcari A, Rigacci L, Tucci A. et al. A Fondazione Italiana Linfomi cohort study of R-COMP vs R-CHOP in older patients with diffuse large B-cell lymphoma. Blood Adv 2023; 7 (15) 4160-4169
    CrossrefPubMedGoogle Scholar
  • 32 Fridrik MA, Jaeger U, Petzer A. et al. Cardiotoxicity with rituximab, cyclophosphamide, non-pegylated liposomal doxorubicin, vincristine and prednisolone compared to rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisolone in frontline treatment of patients with diffuse large B-cell lymphoma: a randomised phase-III study from the Austrian Cancer Drug Therapy Working Group [Arbeitsgemeinschaft Medikamentöse Tumortherapie AGMT](NHL-14). Eur J Cancer 2016; 58: 112-121
    CrossrefPubMedGoogle Scholar
  • 33 Li L, Chen R, Zhou D. et al. The efficacy and cardiac toxicity of different-dose pegylated liposomal doxorubicin in elderly patients with diffuse large B lymphoma. Cancer Med 2023; 12 (04) 4184-4194
    CrossrefPubMedGoogle Scholar
  • 34 Lu B, Shen L, Ma Y. et al. Cardiovascular adverse events associated with cyclophosphamide, pegylated liposomal doxorubicin, vincristine, and prednisone with or without rituximab ((R)-CDOP) in non-Hodgkin's lymphoma: a systematic review and meta-analysis. Front Pharmacol 2022; 13: 1060668
    CrossrefPubMedGoogle Scholar
  • 35 Rigacci L, Annibali O, Kovalchuk S. et al; Fondazione Italiana Linfomi (FIL). Nonpeghylated liposomal doxorubicin combination regimen (R-COMP) for the treatment of lymphoma patients with advanced age or cardiac comorbidity. Hematol Oncol 2020; 38 (04) 478-486
    CrossrefPubMedGoogle Scholar
  • 36 Sancho J-M, Fernández-Alvarez R, Gual-Capllonch F. et al. R-COMP versus R-CHOP as first-line therapy for diffuse large B-cell lymphoma in patients ≥60 years: Results of a randomized phase 2 study from the Spanish GELTAMO group. Cancer Med 2021; 10 (04) 1314-1326
    CrossrefPubMedGoogle Scholar
  • 37 Buonadonna A, Scalone S, Lombardi D. et al. Prospective, multicenter phase II trial of non-pegylated liposomal doxorubicin combined with ifosfamide in first-line treatment of advanced/metastatic soft tissue sarcomas. Cancers (Basel) 2023; 15 (20) 5036
    CrossrefPubMedGoogle Scholar
  • 38 Fiegl M, Mlineritsch B, Hubalek M, Bartsch R, Pluschnig U, Steger GG. Single-agent pegylated liposomal doxorubicin (PLD) in the treatment of metastatic breast cancer: results of an Austrian observational trial. BMC Cancer 2011; 11: 373
    CrossrefPubMedGoogle Scholar
  • 39 Luminari S, Viel E, Ferreri AJM. et al. Nonpegylated liposomal doxorubicin combination regimen in patients with diffuse large B-cell lymphoma and cardiac comorbidity. Results of the HEART01 phase II trial conducted by the Fondazione Italiana Linfomi. Hematol Oncol 2018; 36 (01) 68-75
    CrossrefPubMedGoogle Scholar
  • 40 Gyöngyösi M, Lukovic D, Zlabinger K. et al. Liposomal doxorubicin attenuates cardiotoxicity via induction of interferon-related DNA damage resistance. Cardiovasc Res 2020; 116 (05) 970-982
    PubMedGoogle Scholar
  • 41 Oliveira GH, Al-Kindi SG, Guha A, Dey AK, Rhea IB, deLima MJ. Cardiovascular risk assessment and management of patients undergoing hematopoietic cell transplantation. Bone Marrow Transplant 2021; 56 (03) 544-551
    CrossrefPubMedGoogle Scholar
  • 42 Ranchoux B, Günther S, Quarck R. et al. Chemotherapy-induced pulmonary hypertension: role of alkylating agents. Am J Pathol 2015; 185 (02) 356-371
    CrossrefPubMedGoogle Scholar
  • 43 Jiang D, Song Z, Hu Y, Dong F, Zhao R. Risk of bleeding associated with BTK inhibitor monotherapy: a systematic review and meta-analysis of randomized controlled trials. Expert Rev Clin Pharmacol 2022; 15 (08) 987-996
    CrossrefPubMedGoogle Scholar
  • 44 Byrd JC, Hillmen P, Ghia P. et al. Acalabrutinib versus ibrutinib in previously treated chronic lymphocytic leukemia: results of the first randomized phase III trial. J Clin Oncol 2021; 39 (31) 3441-3452
    Google Scholar
  • 45 Ghia P, Pluta A, Wach M. et al. ASCEND: phase III, randomized trial of acalabrutinib versus idelalisib plus rituximab or bendamustine plus rituximab in relapsed or refractory chronic lymphocytic leukemia. J Clin Oncol 2020; 38 (25) 2849-2861
    CrossrefPubMedGoogle Scholar
  • 46 Sharman JP, Egyed M, Jurczak W. et al. Acalabrutinib with or without obinutuzumab versus chlorambucil and obinutuzmab for treatment-naive chronic lymphocytic leukaemia (ELEVATE TN): a randomised, controlled, phase 3 trial. Lancet 2020; 395 (10232): 1278-1291
    CrossrefPubMedGoogle Scholar
  • 47 Brown JR, Eichhorst B, Hillmen P. et al. Zanubrutinib or ibrutinib in relapsed or refractory chronic lymphocytic leukemia. N Engl J Med 2023; 388 (04) 319-332
    CrossrefPubMedGoogle Scholar
  • 48 Kittai A, Skarbnik A, Miranda M. et al. A matching-adjusted indirect comparison (MAIC) of the efficacy and safety of acalabrutinib (acala) versus zanubrutinib (zanu) in relapsed or refractory chronic lymphocytic leukemia (RR CLL). JCO 2023; 41: 7540-7540
    CrossrefPubMedGoogle Scholar
  • 49 Mendez-Ruiz A, Lossos IS, Cohen MG. Bleeding risk with antiplatelets and Bruton's tyrosine kinase inhibitors in patients with percutaneous coronary intervention. J Soc Cardiovasc Angiogr Interv 2023; 2 (03) 100608
    PubMedGoogle Scholar
  • 50 Bergler-Klein J. Real-life insight into ibrutinib cardiovascular events: defining the loose ends. J Am Coll Cardiol 2019; 74 (13) 1679-1681
    CrossrefPubMedGoogle Scholar
  • 51 Awan FT, Addison D, Alfraih F. et al. International consensus statement on the management of cardiovascular risk of Bruton's tyrosine kinase inhibitors in CLL. Blood Adv 2022; 6 (18) 5516-5525
    CrossrefPubMedGoogle Scholar
  • 52 Caldeira D, Alves D, Costa J, Ferreira JJ, Pinto FJ. Ibrutinib increases the risk of hypertension and atrial fibrillation: systematic review and meta-analysis. PLoS One 2019; 14 (02) e0211228
    CrossrefPubMedGoogle Scholar
  • 53 Jeon Y-W, Lee S-E, Kim S-H. et al. Six-year follow-up of dasatinib-related pulmonary arterial hypertension (PAH) for chronic myeloid leukemia in single center. Blood 2013; 122: 4017
    CrossrefPubMedGoogle Scholar
  • 54 Moslehi JJ. Cardiovascular toxic effects of targeted cancer therapies. N Engl J Med 2016; 375 (15) 1457-1467
    CrossrefPubMedGoogle Scholar
  • 55 Moslehi JJ, Deininger M. Tyrosine kinase inhibitor-associated cardiovascular toxicity in chronic myeloid leukemia. J Clin Oncol 2015; 33 (35) 4210-4218
    CrossrefPubMedGoogle Scholar
  • 56 Cortes JE, Kim D-W, Pinilla-Ibarz J. et al; PACE Investigators. A phase 2 trial of ponatinib in Philadelphia chromosome-positive leukemias. N Engl J Med 2013; 369 (19) 1783-1796
    CrossrefPubMedGoogle Scholar
  • 57 Barber MC, Mauro MJ, Moslehi J. Cardiovascular care of patients with chronic myeloid leukemia (CML) on tyrosine kinase inhibitor (TKI) therapy. Hematology (Am Soc Hematol Educ Program) 2017; 2017 (01) 110-114
    CrossrefPubMedGoogle Scholar
  • 58 Herrmann J, Yang EH, Iliescu CA. et al. Vascular toxicities of cancer therapies: the old and the new–an evolving avenue. Circulation 2016; 133 (13) 1272-1289
    CrossrefPubMedGoogle Scholar
  • 59 Ganatra S, Dani SS, Yang EH, Zaha VG, Nohria A. Cardiotoxicity of T-cell antineoplastic therapies: JACC: CardioOncology Primer. JACC Cardiooncol 2022; 4 (05) 616-623
    CrossrefPubMedGoogle Scholar
  • 60 Lee DW, Santomasso BD, Locke FL. et al. ASTCT consensus grading for cytokine release syndrome and neurologic toxicity associated with immune effector cells. Biol Blood Marrow Transplant 2019; 25 (04) 625-638
    CrossrefPubMedGoogle Scholar
  • 61 Neelapu SS, Locke FL, Bartlett NL. et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med 2017; 377 (26) 2531-2544
    CrossrefPubMedGoogle Scholar
  • 62 Schuster SJ, Svoboda J, Chong EA. et al. Chimeric antigen receptor T cells in refractory B-cell lymphomas. N Engl J Med 2017; 377 (26) 2545-2554
    CrossrefPubMedGoogle Scholar
  • 63 Apel A, Ofran Y, Wolach O. et al. Safety and efficacy of blinatumomab: a real world data. Ann Hematol 2020; 99 (04) 835-838
    CrossrefPubMedGoogle Scholar
  • 64 Jung S-H, Lee SR, Yang D-H. et al. Efficacy and safety of blinatumomab treatment in adult Korean patients with relapsed/refractory acute lymphoblastic leukemia on behalf of the Korean Society of Hematology ALL Working Party. Ann Hematol 2019; 98 (01) 151-158
    CrossrefPubMedGoogle Scholar
  • 65 Kantarjian H, Stein A, Gökbuget N. et al. Blinatumomab versus chemotherapy for advanced acute lymphoblastic leukemia. N Engl J Med 2017; 376 (09) 836-847
    CrossrefPubMedGoogle Scholar
  • 66 Topp MS, Kufer P, Gökbuget N. et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol 2011; 29 (18) 2493-2498
    CrossrefPubMedGoogle Scholar
  • 67 Patel NP, Dalal PJ, Meng Z. et al. Myocardial strain is associated with adverse cardiac events in patients treated with chimeric antigen receptor (CAR) T-cell therapy. Eur J Haematol 2024; 112 (01) 102-110
    CrossrefPubMedGoogle Scholar
  • 68 Alvi RM, Frigault MJ, Fradley MG. et al. Cardiovascular events among adults treated with chimeric antigen receptor T-cells (CAR-T). J Am Coll Cardiol 2019; 74 (25) 3099-3108
    CrossrefPubMedGoogle Scholar
  • 69 Ng CT, Gonzalez Bonilla HM, Chang I. et al. CAR-T therapy in lymphoma patients with coexisting cardiomyopathy or cardiac lymphomatous involvement. JACC Case Rep 2023; 15: 101840
    CrossrefPubMedGoogle Scholar
  • 70 Lee DH, Kumar A, Mohammed T. et al. Cardiac events after standard of care idecabtagene vicleucel for relapsed and refractory multiple myeloma. Blood Adv 2023; 7 (16) 4247-4257
    CrossrefPubMedGoogle Scholar
  • 71 Ghosh AK, Chen DH, Guha A, Mackenzie S, Walker JM, Roddie C. CAR T cell therapy-related cardiovascular outcomes and management: systemic disease or direct cardiotoxicity?. JACC Cardiooncol 2020; 2 (01) 97-109
    CrossrefPubMedGoogle Scholar
  • 72 Mahmood SS, Riedell PA, Feldman S. et al. Biomarkers and cardiovascular outcomes in chimeric antigen receptor T-cell therapy recipients. Eur Heart J 2023; 44 (22) 2029-2042
    CrossrefPubMedGoogle Scholar
  • 73 Guo M, Wang X, Xiao S. et al. Preliminary assessment of cardiotoxicity in chimeric antigen receptor T cell therapy: a systematic review and meta-analysis. Clin Exp Med 2023; 23 (06) 2041-2050
    CrossrefPubMedGoogle Scholar
  • 74 Hatic H, Sampat D, Goyal G. Immune checkpoint inhibitors in lymphoma: challenges and opportunities. Ann Transl Med 2021; 9 (12) 1037-1037
    CrossrefPubMedGoogle Scholar
  • 75 Wang DY, Salem JE, Cohen JV. et al. Fatal toxic effects associated with immune checkpoint inhibitors: a systematic review and meta-analysis. JAMA Oncol 2018; 4 (12) 1721-1728
    CrossrefPubMedGoogle Scholar
  • 76 Salem J-E, Manouchehri A, Moey M. et al. Cardiovascular toxicities associated with immune checkpoint inhibitors: an observational, retrospective, pharmacovigilance study. Lancet Oncol 2018; 19 (12) 1579-1589
    CrossrefPubMedGoogle Scholar
  • 77 Moslehi JJ, Salem J-E, Sosman JA, Lebrun-Vignes B, Johnson DB. Increased reporting of fatal immune checkpoint inhibitor-associated myocarditis. Lancet 2018; 391 (10124): 933-933
    CrossrefPubMedGoogle Scholar
  • 78 Mahmood SS, Fradley MG, Cohen JV. et al. Myocarditis in patients treated with immune checkpoint inhibitors. J Am Coll Cardiol 2018; 71 (16) 1755-1764
    CrossrefPubMedGoogle Scholar
  • 79 Johnson DB, Balko JM, Compton ML. et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med 2016; 375 (18) 1749-1755
    CrossrefPubMedGoogle Scholar
  • 80 Chen C, Chen T, Liang J. et al. Cardiotoxicity induced by immune checkpoint inhibitors: a pharmacovigilance study from 2014 to 2019 based on FAERS. Front Pharmacol 2021; 12: 616505
    CrossrefPubMedGoogle Scholar
  • 81 Anquetil C, Salem JE, Lebrun-Vignes B. et al. Immune checkpoint inhibitor-associated myositis: expanding the spectrum of cardiac complications of the immunotherapy revolution. Circulation 2018; 138 (07) 743-745
    CrossrefPubMedGoogle Scholar
  • 82 Fazel M, Jedlowski PM. Severe myositis, myocarditis, and myasthenia gravis with elevated anti-striated muscle antibody following single dose of ipilimumab-nivolumab therapy in a patient with metastatic melanoma. Case Reports Immunol 2019; 2019: 2539493
    CrossrefPubMedGoogle Scholar
  • 83 Dolladille C, Ederhy S, Sassier M. et al. Immune checkpoint inhibitor rechallenge after immune-related adverse events in patients with cancer. JAMA Oncol 2020; 6 (06) 865-871
    CrossrefPubMedGoogle Scholar
  • 84 D'Souza M, Nielsen D, Svane IM. et al. The risk of cardiac events in patients receiving immune checkpoint inhibitors: a nationwide Danish study. Eur Heart J 2021; 42 (16) 1621-1631
    CrossrefPubMedGoogle Scholar
  • 85 Laenens D, Yu Y, Santens B. et al. Incidence of cardiovascular events in patients treated with immune checkpoint inhibitors. J Clin Oncol 2022; 40 (29) 3430-3438
    CrossrefPubMedGoogle Scholar
  • 86 Drobni ZD, Alvi RM, Taron J. et al. Association between immune checkpoint inhibitors with cardiovascular events and atherosclerotic plaque. Circulation 2020; 142 (24) 2299-2311
    CrossrefPubMedGoogle Scholar
  • 87 Calabretta R, Hoeller C, Pichler V. et al. Immune checkpoint inhibitor therapy induces inflammatory activity in large arteries. Circulation 2020; 142 (24) 2396-2398
    CrossrefPubMedGoogle Scholar
  • 88 Zhang L, Awadalla M, Mahmood SS. et al. Cardiovascular magnetic resonance in immune checkpoint inhibitor-associated myocarditis. Eur Heart J 2020; 41 (18) 1733-1743
    CrossrefPubMedGoogle Scholar
  • 89 Gevaert SA, Halvorsen S, Sinnaeve PR. et al. Evaluation and management of cancer patients presenting with acute cardiovascular disease: a Clinical Consensus Statement of the Acute CardioVascular Care Association (ACVC) and the ESC council of Cardio-Oncology-part 2: acute heart failure, acute myocardial diseases, acute venous thromboembolic diseases, and acute arrhythmias. Eur Heart J Acute Cardiovasc Care 2022; 11 (11) 865-874
    CrossrefPubMedGoogle Scholar
  • 90 Waxman AJ, Clasen S, Hwang W-T. et al. Carfilzomib-associated cardiovascular adverse events: a systematic review and meta-analysis. JAMA Oncol 2018; 4 (03) e174519
    CrossrefPubMedGoogle Scholar
  • 91 Siegel D, Martin T, Nooka A. et al. Integrated safety profile of single-agent carfilzomib: experience from 526 patients enrolled in 4 phase II clinical studies. Haematologica 2013; 98 (11) 1753-1761
    CrossrefPubMedGoogle Scholar
  • 92 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 2020; 38 (05) 496-520
    CrossrefPubMedGoogle Scholar
  • 93 Laugaard Lorenzen E, Christian Rehammar J, Jensen M-B, Ewertz M, Brink C. Radiation-induced risk of ischemic heart disease following breast cancer radiotherapy in Denmark, 1977-2005. Radiother Oncol 2020; 152: 103-110
    CrossrefPubMedGoogle Scholar
  • 94 Gangaraju R, Chen Y, Hageman L. et al. Prediction of coronary heart disease events in blood or marrow transplantation recipients. JACC Cardiooncol 2023; 5 (04) 504-517
    CrossrefPubMedGoogle Scholar
  • 95 Vasbinder A, Hoeger CW, Catalan T. et al. Cardiovascular events after hematopoietic stem cell transplant: incidence and risk factors. JACC Cardiooncol 2023; 5 (06) 821-832
    CrossrefPubMedGoogle Scholar
  • 96 Timp JF, Braekkan SK, Versteeg HH, Cannegieter SC. Epidemiology of cancer-associated venous thrombosis. Blood 2013; 122 (10) 1712-1723
    CrossrefPubMedGoogle Scholar
  • 97 Grilz E, Posch F, Nopp S. et al. Relative risk of arterial and venous thromboembolism in persons with cancer vs. persons without cancer-a nationwide analysis. Eur Heart J 2021; 42 (23) 2299-2307
    CrossrefPubMedGoogle Scholar
  • 98 Mulder FI, Horváth-Puhó E, van Es N. et al. Venous thromboembolism in cancer patients: a population-based cohort study. Blood 2021; 137 (14) 1959-1969
    CrossrefPubMedGoogle Scholar
  • 99 van Es N, Le Gal G, Otten H-M. et al. Screening for occult cancer in patients with unprovoked venous thromboembolism: a systematic review and meta-analysis of individual patient data. Ann Intern Med 2017; 167 (06) 410-417
    CrossrefPubMedGoogle Scholar
  • 100 Mulder FI, Carrier M, van Doormaal F. et al. Risk scores for occult cancer in patients with unprovoked venous thromboembolism: results from an individual patient data meta-analysis. J Thromb Haemost 2020; 18 (10) 2622-2628
    CrossrefPubMedGoogle Scholar
  • 101 Ay C, Pabinger I, Cohen AT. Cancer-associated venous thromboembolism: burden, mechanisms, and management. Thromb Haemost 2017; 117 (02) 219-230
    Article in Thieme ConnectPubMedGoogle Scholar
  • 102 Gussoni G, Frasson S, La Regina M, Di Micco P, Monreal M. RIETE Investigators. Three-month mortality rate and clinical predictors in patients with venous thromboembolism and cancer. Findings from the RIETE registry. Thromb Res 2013; 131 (01) 24-30
    CrossrefPubMedGoogle Scholar
  • 103 Sørensen HT, Pedersen L, van Es N, Büller HR, Horváth-Puhó E. Impact of venous thromboembolism on the mortality in patients with cancer: a population-based cohort study. Lancet Reg Health Eur 2023; 34: 100739
    CrossrefPubMedGoogle Scholar
  • 104 Caroti KS, Becattini C, Carrier M. et al. Rivaroxaban versus apixaban for treatment of cancer-associated venous thromboembolism in patients at lower risk of bleeding. TH Open 2023; 7 (03) e206-e216
    Article in Thieme ConnectPubMedGoogle Scholar
  • 105 Schrag D, Uno H, Rosovsky R. et al; CANVAS Investigators. Direct oral anticoagulants vs low-molecular-weight heparin and recurrent VTE in patients with cancer: a randomized clinical trial. JAMA 2023; 329 (22) 1924-1933
    CrossrefPubMedGoogle Scholar
  • 106 López-Fernández T, Martín-García A, Roldán Rabadán I. et al; Expert reviewers. Atrial fibrillation in active cancer patients: expert position paper and recommendations. Rev Esp Cardiol (Engl Ed) 2019; 72 (09) 749-759
    PubMedGoogle Scholar
  • 107 Tsoukalas N, Brito-Dellan N, Font C. et al; MASCC Hemostasis Study Group. Complexity and clinical significance of drug-drug interactions (DDIs) in oncology: challenging issues in the care of patients regarding cancer-associated thrombosis (CAT). Support Care Cancer 2022; 30 (10) 8559-8573
    CrossrefPubMedGoogle Scholar
  • 108 Liu M, Qiu X, Sun Y. et al. Intensify standardized anticoagulation for cancer-associated pulmonary embolism: from single-center real-world data. Clin Ther 2023; 45 (12) 1236-1243
    CrossrefPubMedGoogle Scholar
  • 109 Holmes CE, Ades S, Gilchrist S. et al. Successful model for guideline implementation to prevent cancer-associated thrombosis: venous thromboembolism prevention in the ambulatory cancer clinic. JCO Oncol Pract 2020; 16 (09) e868-e874
    CrossrefPubMedGoogle Scholar
  • 110 Martin KA, Molsberry R, Khan SS, Linder JA, Cameron KA, Benson III A. Preventing venous thromboembolism in oncology practice: Use of risk assessment and anticoagulation prophylaxis. Res Pract Thromb Haemost 2020; 4 (07) 1211-1215
    CrossrefPubMedGoogle Scholar
  • 111 Martin KA, Cameron KA, Lyleroehr MJ, Linder JA, O'Brien M, Hirschhorn LR. Venous thromboembolism prevention in cancer care: implementation strategies to address underuse. Res Pract Thromb Haemost 2023; 7 (07) 102173
    CrossrefPubMedGoogle Scholar
  • 112 Bergqvist D, Agnelli G, Cohen AT. et al; ENOXACAN II Investigators. Duration of prophylaxis against venous thromboembolism with enoxaparin after surgery for cancer. N Engl J Med 2002; 346 (13) 975-980
    CrossrefPubMedGoogle Scholar
  • 113 Key NS, Khorana AA, Kuderer NM. et al. Venous Thromboembolism prophylaxis and treatment in patients with cancer: ASCO guideline update. J Clin Oncol 2023; 41 (16) 3063-3071
    CrossrefPubMedGoogle Scholar
  • 114 Becattini C, Pace U, Pirozzi F. et al. Rivaroxaban vs placebo for extended antithrombotic prophylaxis after laparoscopic surgery for colorectal cancer. Blood 2022; 140 (08) 900-908
    CrossrefPubMedGoogle Scholar
  • 115 Guntupalli SR, Brennecke A, Behbakht K. et al. Safety and efficacy of apixaban vs enoxaparin for preventing postoperative venous thromboembolism in women undergoing surgery for gynecologic malignant neoplasm: a randomized clinical trial. JAMA Netw Open 2020; 3 (06) e207410
    CrossrefPubMedGoogle Scholar
  • 116 Khorana AA, Kuderer NM, Culakova E, Lyman GH, Francis CW. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood 2008; 111 (10) 4902-4907
    CrossrefPubMedGoogle Scholar
  • 117 Carrier M, Abou-Nassar K, Mallick R. et al; AVERT Investigators. Apixaban to prevent venous thromboembolism in patients with cancer. N Engl J Med 2019; 380 (08) 711-719
    CrossrefPubMedGoogle Scholar
  • 118 Khorana AA, Soff GA, Kakkar AK. et al; CASSINI Investigators. Rivaroxaban for thromboprophylaxis in high-risk ambulatory patients with cancer. N Engl J Med 2019; 380 (08) 720-728
    CrossrefPubMedGoogle Scholar
  • 119 Wang T-F, Baumann Kreuziger L, Leader A. et al. Characteristics and outcomes of patients on concurrent direct oral anticoagulants and targeted anticancer therapies-TacDOAC registry: communication from the ISTH SSC Subcommittee on Hemostasis and Malignancy. J Thromb Haemost 2021; 19 (08) 2068-2081
    CrossrefPubMedGoogle Scholar
  • 120 Bolek H, Ürün Y. Cancer-associated thrombosis and drug-drug interactions of antithrombotic and antineoplastic agents. Cancer 2023; 129 (20) 3216-3229
    CrossrefPubMedGoogle Scholar
  • 121 Navi BB, Reiner AS, Kamel H. et al. Arterial thromboembolic events preceding the diagnosis of cancer in older persons. Blood 2019; 133 (08) 781-789
    CrossrefPubMedGoogle Scholar
  • 122 Navi BB, Reiner AS, Kamel H. et al. Risk of arterial thromboembolism in patients with cancer. J Am Coll Cardiol 2017; 70 (08) 926-938
    CrossrefPubMedGoogle Scholar
  • 123 Mitrovic M, Pantic N, Sabljic N. et al. Arterial thrombosis in patients with acute myeloid leukemia: incidence and risk factors. Cancers (Basel) 2023; 15 (11) 3060
    CrossrefPubMedGoogle Scholar
  • 124 Mulder FI, Horváth-Puhó E, van Es N. et al. Arterial thromboembolism in cancer patients: a Danish population-based cohort study. JACC Cardiooncol 2021; 3 (02) 205-218
    PubMedGoogle Scholar
  • 125 Ay C, Grilz E, Nopp S. et al. Atrial fibrillation and cancer: prevalence and relative risk from a nationwide study. Res Pract Thromb Haemost 2022; 7 (01) 100026
    CrossrefPubMedGoogle Scholar
  • 126 Leader A, Mendelson Cohen N, Afek S. et al. Arterial thromboembolism in patients with AF and CHA2DS2-VASc score 0-2 with and without cancer. JACC Cardiooncol 2023; 5 (02) 174-185
    CrossrefPubMedGoogle Scholar
  • 127 Shabtaie SA, Tan NY, Ward RC. et al. Left atrial appendage occlusion in patients with atrial fibrillation and cancer. JACC Cardiooncol 2023; 5 (02) 203-212
    CrossrefPubMedGoogle Scholar
  • 128 Xu Y, Cole K, Collins E, Moledina A, Mallity C, Carrier M. Anticoagulation for the prevention of arterial thrombosis in ambulatory cancer patients: systematic review and meta-analysis. JACC Cardiooncol 2023; 5 (04) 520-532
    CrossrefPubMedGoogle Scholar
  • 129 Brenner B, Bikdeli B, Tzoran I. et al; RIETE Investigators. Arterial ischemic events are a major complication in cancer patients with venous thromboembolism. Am J Med 2018; 131 (09) 1095-1103
    CrossrefPubMedGoogle Scholar
  • 130 Spaccarotella C, Esposito G, Indolfi C. To anticoagulate or not to anticoagulate to prevent arterial thrombosis during systemic cancer therapy. JACC Cardiooncol 2023; 5 (04) 533-535
    CrossrefPubMedGoogle Scholar
  • 131 Cardinale D, Colombo A, Lamantia G. et al. Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy. J Am Coll Cardiol 2010; 55 (03) 213-220
    CrossrefPubMedGoogle Scholar
  • 132 Velusamy R, Nolan M, Murphy A, Thavendiranathan P, Marwick TH. Screening for coronary artery disease in cancer survivors: JACC: CardioOncology State-of-the-Art Review. JACC Cardiooncol 2023; 5 (01) 22-38
    CrossrefPubMedGoogle Scholar
  • 133 Zheng H, Zhan H. Cardio-oncology guidelines and strength of the evidence. JACC Cardiooncol 2023; 5 (01) 149-152
    CrossrefPubMedGoogle Scholar
  • 134 Poenou G, Heestermans M, Lafaie L. et al. Inhibition of factor XI: a new era in the treatment of venous thromboembolism in cancer patients?. Int J Mol Sci 2023; 24 (19) 14433
    CrossrefPubMedGoogle Scholar