Login Register Cart 0
Current Cardiology Reviews

Current Cardiology Reviews

Editor-in-Chief

ISSN (Print): 1573-403X
ISSN (Online): 1875-6557

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Cardiotoxicity of Biological Therapies in Cancer Patients: An In-depth Review

Author(s): Luai Madanat*, Ruby Gupta, Paul Weber, Navneet Kumar, Rohit Chandra, Hycienth Ahaneku, Yatharth Bansal, Joseph Anderson, Abhay Bilolikar and Ishmael Jaiyesimi

Volume 19, Issue 3, 2023

Published on: 03 January, 2023

Article ID: e310522205428 Pages: 11

DOI: 10.2174/1573403X18666220531094800

Price: $65

Become a Editorial Board Member
Become a Reviewer
Become a Editor
Become a Section Editor

Abstract

Cardiotoxicity from chemotherapy regimens has been long reported. However, the understanding of cardiac side effects of biological therapies is rapidly evolving. With cancer patients achieving higher life expectancy due to the use of personalized medicine and novel targeted anticancer agents, the occurrence of cardiotoxicity is becoming more significant. Novel biological therapies include anti-HER2 antibodies, tyrosine kinase inhibitors, bruton kinase inhibitors, antivascular endothelial growth factors, proteasome inhibitors, immunomodulator drugs, and immune checkpoint inhibitors. Potential cardiovascular toxicities linked to these anticancer agents include hypertension, arrhythmias, QT prolongation, myocardial ischemia and infarction, left ventricular dysfunction, congestive heart failure, and thromboembolism. Cardiac biomarkers, electrocardiography, echocardiography and magnetic resonance imaging are common diagnostic modalities used for early detection of these complications and timely intervention. This review discusses the various types of cardiotoxicities caused by novel anticancer biologic agents, their molecular and pathophysiological mechanisms, risk factors, and diagnostic and management strategies that can be used to prevent, minimize, and treat them.

Keywords: Cardiotoxicity, anticancer drugs, targeted therapies, biological therapies, immune checkpoint inhibitors, cardiooncology.

[1]
Bellinger AM, Arteaga CL, Force T, et al. Cardio-oncology: How new targeted cancer therapies and precision medicine can inform cardiovascular discovery. Circulation 2015; 132(23): 2248-58.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.115.010484] [PMID: 26644247]
[2]
Dazzi H, Kaufmann K, Follath F. Anthracycline-induced acute cardiotoxicity in adults treated for leukaemia. Analysis of the clinico-pathological aspects of documented acute anthracycline-induced cardiotoxicity in patients treated for acute leukaemia at the University Hospital of Zurich, Switzerland, between 1990 and 1996. Ann Oncol 2001; 12(7): 963-6.
[http://dx.doi.org/10.1023/A:1011196910325] [PMID: 11521803]
[3]
Pai VB, Nahata MC. Cardiotoxicity of chemotherapeutic agents: Incidence, treatment and prevention. Drug Saf 2000; 22(4): 263-302.
[http://dx.doi.org/10.2165/00002018-200022040-00002] [PMID: 10789823]
[4]
Maurea N, Coppola C, Piscopo G, et al. Pathophysiology of cardiotoxicity from target therapy and angiogenesis inhibitors. J Cardiovasc Med 2016; 17: 19-26.
[http://dx.doi.org/10.2459/JCM.0000000000000377]
[5]
Felker GM, Thompson RE, Hare JM, et al. Underlying causes and long-term survival in patients with initially unexplained cardiomyopathy. N Engl J Med 2000; 342(15): 1077-84.
[http://dx.doi.org/10.1056/NEJM200004133421502] [PMID: 10760308]
[6]
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: The Task Force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur Heart J 2016; 37(36): 2768-801.
[http://dx.doi.org/10.1093/eurheartj/ehw211] [PMID: 27567406]
[7]
Ganatra S, Neilan TG. Immune checkpoint inhibitor-associated myocarditis. Oncologist 2018; 23(8): 879-86.
[http://dx.doi.org/10.1634/theoncologist.2018-0130] [PMID: 29802219]
[8]
Tokunaga R, Zhang W, Naseem M, et al. CXCL9, CXCL10, CXCL11/CXCR3 axis for immune activation - A target for novel cancer therapy. Cancer Treat Rev 2018; 63: 40-7.
[http://dx.doi.org/10.1016/j.ctrv.2017.11.007] [PMID: 29207310]
[9]
Kokubo H, Miyagawa-Tomita S, Tomimatsu H, et al. Targeted disruption of hesr2 results in atrioventricular valve anomalies that lead to heart dysfunction. Circ Res 2004; 95(5): 540-7.
[http://dx.doi.org/10.1161/01.RES.0000141136.85194.f0] [PMID: 15297376]
[10]
Veronese ML, Mosenkis A, Flaherty KT, et al. Mechanisms of hypertension associated with BAY 43-9006. J Clin Oncol 2006; 24(9): 1363-9.
[http://dx.doi.org/10.1200/JCO.2005.02.0503] [PMID: 16446323]
[11]
Chen MH, Kerkelä R, Force T. Mechanisms of cardiac dysfunction associated with tyrosine kinase inhibitor cancer therapeutics. Circulation 2008; 118(1): 84-95.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.776831] [PMID: 18591451]
[12]
Gressett SM, Shah SR. Intricacies of bevacizumab-induced toxicities and their management. Ann Pharmacother 2009; 43(3): 490-501.
[http://dx.doi.org/10.1345/aph.1L426] [PMID: 19261963]
[13]
Patel V, Balakrishnan K, Bibikova E, et al. Comparison of acalabrutinib, a selective bruton tyrosine kinase inhibitor, with ibrutinib in chronic lymphocytic leukemia cells. Clin Cancer Res 2017; 23(14): 3734-43.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-1446] [PMID: 28034907]
[14]
Lub S, Maes K, Menu E, De Bruyne E, Vanderkerken K, Van Valckenborgh E. Novel strategies to target the ubiquitin pro-teasome system in multiple myeloma. Oncotarget 2016; 7(6): 6521-37.
[http://dx.doi.org/10.18632/oncotarget.6658] [PMID: 26695547]
[15]
Wu P, Oren O, Gertz MA, Yang EH. Proteasome inhibitor-related cardiotoxicity: Mechanisms, diagnosis, and management. Curr Oncol Rep 2020; 22(7): 66.
[http://dx.doi.org/10.1007/s11912-020-00931-w] [PMID: 32514632]
[16]
Quach H, Ritchie D, Stewart AK, et al. Mechanism of action of immunomodulatory drugs (IMiDS) in multiple myeloma. Leukemia 2010; 24(1): 22-32.
[http://dx.doi.org/10.1038/leu.2009.236] [PMID: 19907437]
[17]
Ribas A, Wolchok JD. Cancer immunotherapy using check-point blockade. Science 2018; 359(6382): 1350-5.
[http://dx.doi.org/10.1126/science.aar4060] [PMID: 29567705]
[18]
Eigentler TK, Hassel JC, Berking C, et al. Diagnosis, monitoring and management of immune-related adverse drug reactions of anti-PD-1 antibody therapy. Cancer Treat Rev 2016; 45: 7-18.
[http://dx.doi.org/10.1016/j.ctrv.2016.02.003] [PMID: 26922661]
[19]
Herbst RS, Soria JC, Kowanetz M, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014; 515(7528): 563-7.
[http://dx.doi.org/10.1038/nature14011] [PMID: 25428504]
[20]
Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366(26): 2443-54.
[http://dx.doi.org/10.1056/NEJMoa1200690] [PMID: 22658127]
[21]
Ding W, LaPlant BR, Call TG, et al. Pembrolizumab in patients with CLL and Richter transformation or with relapsed CLL. Blood 2017; 129(26): 3419-27.
[http://dx.doi.org/10.1182/blood-2017-02-765685] [PMID: 28424162]
[22]
Weber JS, Kähler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipili-mumab. J Clin Oncol 2012; 30(21): 2691-7.
[http://dx.doi.org/10.1200/JCO.2012.41.6750] [PMID: 22614989]
[23]
Johnson DB, Chandra S, Sosman JA. Immune checkpoint inhibitor toxicity in. JAMA 2018; 320(16): 1702-3.
[http://dx.doi.org/10.1001/jama.2018.13995] [PMID: 30286224]
[24]
Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med 2018; 378(2): 158-68.
[http://dx.doi.org/10.1056/NEJMra1703481] [PMID: 29320654]
[25]
Heery CR, Coyne GHOS, Madan RA, et al. Phase I open-label, multiple ascending dose trial of MSB0010718C, an anti-PD-L1 monoclonal antibody, in advanced solid malignan-cies. J Clin Oncol 2014; 32(15): 3064.
[http://dx.doi.org/10.1200/jco.2014.32.15_suppl.3064]
[26]
Geisler BP, Raad RA, Esaian D, Sharon E, Schwartz DR. Apical ballooning and cardiomyopathy in a melanoma patient treated with ipilimumab: A case of takotsubo-like syndrome. J Immunother Cancer 2015; 3(1): 4.
[http://dx.doi.org/10.1186/s40425-015-0048-2] [PMID: 25705383]
[27]
Läubli H, Balmelli C, Bossard M, Pfister O, Glatz K, Zippelius A. Acute heart failure due to autoimmune myocarditis under pembrolizumab treatment for metastatic melanoma. J Immunother Cancer 2015; 3(1): 11.
[http://dx.doi.org/10.1186/s40425-015-0057-1] [PMID: 25901283]
[28]
Tajmir-Riahi A, Bergmann T, Schmid M, Agaimy A, Schuler G, Heinzerling L. Life-threatening autoimmune cardiomyopathy reproducibly induced in a patient by checkpoint inhibitor therapy. J Immunother 2018; 41(1): 35-8.
[http://dx.doi.org/10.1097/CJI.0000000000000190] [PMID: 29077601]
[29]
Behling J, Kaes J, Münzel T, Grabbe S, Loquai C. New-onset third-degree atrioventricular block because of autoimmune-induced myositis under treatment with anti-programmed cell death-1 (nivolumab) for metastatic melanoma. Melanoma Res 2017; 27(2): 155-8.
[http://dx.doi.org/10.1097/CMR.0000000000000314] [PMID: 27977496]
[30]
Reuben A, Petaccia de Macedo M, McQuade J, et al. Compar-ative immunologic characterization of autoimmune giant cell myocarditis with ipilimumab. OncoImmunology 2017; 6(12): e1361097.
[http://dx.doi.org/10.1080/2162402X.2017.1361097] [PMID: 29209563]
[31]
Lyon AR, Yousaf N, Battisti NML, Moslehi J, Larkin J. Immune checkpoint inhibitors and cardiovascular toxicity. Lancet Oncol 2018; 19(9): e447-58.
[http://dx.doi.org/10.1016/S1470-2045(18)30457-1] [PMID: 30191849]
[32]
Roth ME, Muluneh B, Jensen BC, Madamanchi C, Lee CB. Left ventricular dysfunction after treatment with ipilimumab for metastatic melanoma. Am J Ther 2016; 23(6): e1925-8.
[http://dx.doi.org/10.1097/MJT.0000000000000430] [PMID: 26885708]
[33]
Anderson RD, Brooks M. Apical takotsubo syndrome in a patient with metastatic breast carcinoma on novel immunotherapy. Int J Cardiol 2016; 222: 760-1.
[http://dx.doi.org/10.1016/j.ijcard.2016.07.291] [PMID: 27521552]
[34]
Salem JE, Manouchehri A, Moey M, et al. Cardiovascular toxicities associated with immune checkpoint inhibitors: An observational, retrospective, pharmacovigilance study. Lancet Oncol 2018; 19(12): 1579-89.
[http://dx.doi.org/10.1016/S1470-2045(18)30608-9] [PMID: 30442497]
[35]
Tajiri K, Ieda M. Cardiac Complications in immune check-point inhibition therapy. Front Cardiovasc Med 2019; 6: 3.
[http://dx.doi.org/10.3389/fcvm.2019.00003] [PMID: 30729114]
[36]
Mahmood SS, Fradley MG, Cohen JV, et al. Myocarditis in patients treated with immune checkpoint inhibitors. J Am Coll Cardiol 2018; 71(16): 1755-64.
[http://dx.doi.org/10.1016/j.jacc.2018.02.037] [PMID: 29567210]
[37]
Johnson DB, Balko JM, Compton ML, et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med 2016; 375(18): 1749-55.
[http://dx.doi.org/10.1056/NEJMoa1609214] [PMID: 27806233]
[38]
Voskens CJ, Goldinger SM, Loquai C, et al. The price of tumor control: An analysis of rare side effects of anti-CTLA-4 therapy in metastatic melanoma from the ipilimumab network. PLoS One 2013; 8(1): e53745.
[http://dx.doi.org/10.1371/journal.pone.0053745] [PMID: 23341990]
[39]
Upadhrasta S, Elias H, Patel K, Zheng L. Managing cardiotoxicity associated with immune checkpoint inhibitors. Chronic Dis Transl Med 2019; 5(1): 6-14.
[http://dx.doi.org/10.1016/j.cdtm.2019.02.004] [PMID: 30993259]
[40]
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): 1721-8.
[http://dx.doi.org/10.1001/jamaoncol.2018.3923] [PMID: 30242316]
[41]
Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: Correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235(4785): 177-82.
[http://dx.doi.org/10.1126/science.3798106] [PMID: 3798106]
[42]
Gonzalez-Angulo AM, Litton JK, Broglio KR, et al. High risk of recurrence for patients with breast cancer who have human epidermal growth factor receptor 2-positive, node-negative tumors 1 cm or smaller. J Clin Oncol 2009; 27(34): 5700-6.
[http://dx.doi.org/10.1200/JCO.2009.23.2025] [PMID: 19884543]
[43]
Azim H, Azim HA Jr, Escudier B. Trastuzumab versus lapatinib: The cardiac side of the story. Cancer Treat Rev 2009; 35(7): 633-8.
[http://dx.doi.org/10.1016/j.ctrv.2009.06.007] [PMID: 19640652]
[44]
Ewer MS, Vooletich MT, Durand JB, et al. Reversibility of trastuzumab-related cardiotoxicity: New insights based on clinical course and response to medical treatment. J Clin Oncol 2005; 23(31): 7820-6.
[http://dx.doi.org/10.1200/JCO.2005.13.300] [PMID: 16258084]
[45]
Bowles EJ, Wellman R, Feigelson HS, et al. Risk of heart failure in breast cancer patients after anthracycline and trastuzumab treatment: A retrospective cohort study. J Natl Cancer Inst 2012; 104(17): 1293-305.
[http://dx.doi.org/10.1093/jnci/djs317] [PMID: 22949432]
[46]
Perez EA, Romond EH, Suman VJ, et al. Four-year follow-up of trastuzumab plus adjuvant chemotherapy for operable human epidermal growth factor receptor 2-positive breast cancer: Joint analysis of data from NCCTG N9831 and NSABP B-31. J Clin Oncol 2011; 29(25): 3366-73.
[http://dx.doi.org/10.1200/JCO.2011.35.0868] [PMID: 21768458]
[47]
Tan-Chiu E, Yothers G, Romond E, et al. Assessment of cardiac dysfunction in a randomized trial comparing doxorubicin and cyclophosphamide followed by paclitaxel, with or without trastuzumab as adjuvant therapy in node-positive, human epidermal growth factor receptor 2-overexpressing breast cancer: NSABP B-31. J Clin Oncol 2005; 23(31): 7811-9.
[http://dx.doi.org/10.1200/JCO.2005.02.4091] [PMID: 16258083]
[48]
Slamon DJ, Leyland-Jones B, Shak S, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001; 344(11): 783-92.
[http://dx.doi.org/10.1056/NEJM200103153441101] [PMID: 11248153]
[49]
Seidman A, Hudis C, Pierri MK, et al. Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin Oncol 2002; 20(5): 1215-21.
[http://dx.doi.org/10.1200/JCO.2002.20.5.1215] [PMID: 11870163]
[50]
Piotrowski G, Gawor R, Stasiak A, Gawor Z, Potemski P, Banach M. Cardiac complications associated with trastuzumab in the setting of adjuvant chemotherapy for breast cancer overexpressing human epidermal growth factor receptor type 2 - a prospective study. Arch Med Sci 2012; 8(2): 227-35.
[http://dx.doi.org/10.5114/aoms.2012.28549] [PMID: 22661994]
[51]
Onitilo AA, Engel JM, Stankowski RV. Cardiovascular toxici-ty associated with adjuvant trastuzumab therapy: Prevalence, patient characteristics, and risk factors. Ther Adv Drug Saf 2014; 5(4): 154-66.
[http://dx.doi.org/10.1177/2042098614529603] [PMID: 25083270]
[52]
Senkus E, Jassem J. Cardiovascular effects of systemic cancer treatment. Cancer Treat Rev 2011; 37(4): 300-11.
[http://dx.doi.org/10.1016/j.ctrv.2010.11.001] [PMID: 21126826]
[53]
Valachis A, Nearchou A, Polyzos NP, Lind P. Cardiac toxicity in breast cancer patients treated with dual HER2 blockade. Int J Cancer 2013; 133(9): 2245-52.
[http://dx.doi.org/10.1002/ijc.28234] [PMID: 23629633]
[54]
Swain SM, Ewer MS, Cortés J, et al. Cardiac tolerability of pertuzumab plus trastuzumab plus docetaxel in patients with HER2-positive metastatic breast cancer in CLEOPATRA: A randomized, double-blind, placebo-controlled phase III study. Oncologist 2013; 18(3): 257-64.
[http://dx.doi.org/10.1634/theoncologist.2012-0448] [PMID: 23475636]
[55]
Alhussein MM, Mokbel A, Cosman T, et al. Pertuzumab cardiotoxicity in patients with her2-positive cancer: A sys-tematic review and meta-analysis. CJC Open 2021; 3(11): 1372-82.
[http://dx.doi.org/10.1016/j.cjco.2021.06.019] [PMID: 34901806]
[56]
Girardi F, Franceschi E, Brandes AA. Cardiovascular safety of VEGF-targeting therapies: Current evidence and handling strategies. Oncologist 2010; 15(7): 683-94.
[http://dx.doi.org/10.1634/theoncologist.2009-0235] [PMID: 20547589]
[57]
Perez EA, Koehler M, Byrne J, Preston AJ, Rappold E, Ewer MS. Cardiac safety of lapatinib: Pooled analysis of 3689 patients enrolled in clinical trials. Mayo Clin Proc 2008; 83(6): 679-86.
[http://dx.doi.org/10.1016/S0025-6196(11)60896-3] [PMID: 18533085]
[58]
Blackwell KL, Burstein HJ, Storniolo AM, et al. Randomized study of Lapatinib alone or in combination with trastuzumab in women with ErbB2-positive, trastuzumab-refractory metastatic breast cancer. J Clin Oncol 2010; 28(7): 1124-30.
[http://dx.doi.org/10.1200/JCO.2008.21.4437] [PMID: 20124187]
[59]
Figueroa-Magalhães MC, Jelovac D, Connolly R, Wolff AC. Treatment of HER2-positive breast cancer. Breast 2014; 23(2): 128-36.
[http://dx.doi.org/10.1016/j.breast.2013.11.011] [PMID: 24360619]
[60]
Verma S, Miles D, Gianni L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012; 367(19): 1783-91.
[http://dx.doi.org/10.1056/NEJMoa1209124] [PMID: 23020162]
[61]
Iqbal N, Iqbal N. Imatinib: A breakthrough of targeted therapy in cancer. Chemother Res Pract 2014; 2014: 357027.
[http://dx.doi.org/10.1155/2014/357027] [PMID: 24963404]
[62]
Atallah E, Durand JB, Kantarjian H, Cortes J. Congestive heart failure is a rare event in patients receiving imatinib therapy. Blood 2007; 110(4): 1233-7.
[http://dx.doi.org/10.1182/blood-2007-01-070144] [PMID: 17449798]
[63]
Highlights of prescribing information. Available from: https://www.novartis.us/sites/www.novartis.us/files/gleevec_tabs.p df (Accessed on May 21, 2022).
[64]
Baker SJ, Reddy EP. Targeted inhibition of kinases in cancer therapy. Mt Sinai J Med 2010; 77(6): 573-86.
[http://dx.doi.org/10.1002/msj.20220] [PMID: 21105121]
[65]
Brave M, Goodman V, Kaminskas E, et al. Sprycel for chron-ic myeloid leukemia and Philadelphia chromosome-positive acute lymphoblastic leukemia resistant to or intolerant of imatinib mesylate. Clin Cancer Res 2008; 14(2): 352-9.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-4175] [PMID: 18223208]
[66]
Saglio G, Kim DW, Issaragrisil S, et al. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med 2010; 362(24): 2251-9.
[http://dx.doi.org/10.1056/NEJMoa0912614] [PMID: 20525993]
[67]
Larson RA, Hochhaus A, Hughes TP, et al. Nilotinib vs imatinib in patients with newly diagnosed Philadelphia chromosome-positive chronic myeloid leukemia in chronic phase: ENESTnd 3-year follow-up. Leukemia 2012; 26(10): 2197-203.
[http://dx.doi.org/10.1038/leu.2012.134] [PMID: 22699418]
[68]
Shibuya M. Vascular Endothelial Growth Factor (VEGF) and Its Receptor (VEGFR) signaling in angiogenesis: A crucial target for anti- and pro-angiogenic therapies. Genes Cancer 2011; 2(12): 1097-105.
[http://dx.doi.org/10.1177/1947601911423031] [PMID: 22866201]
[69]
Kazazi-Hyseni F, Beijnen JH, Schellens JH. Bevacizumab. Oncologist 2010; 15(8): 819-25.
[http://dx.doi.org/10.1634/theoncologist.2009-0317] [PMID: 20688807]
[70]
Yeh ETH, Tong AT, Lenihan DJ, et al. Cardiovascular complications of cancer therapy: Diagnosis, pathogenesis, and management. Circulation 2004; 109(25): 3122-31.
[http://dx.doi.org/10.1161/01.CIR.0000133187.74800.B9] [PMID: 15226229]
[71]
Economopoulou P, Kotsakis A, Kapiris I, Kentepozidis N. Cancer therapy and cardiovascular risk: Focus on bevacizumab. Cancer Manag Res 2015; 7: 133-43.
[http://dx.doi.org/10.2147/CMAR.S77400] [PMID: 26082660]
[72]
Scappaticci FA, Skillings JR, Holden SN, et al. Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab. J Natl Cancer Inst 2007; 99(16): 1232-9.
[http://dx.doi.org/10.1093/jnci/djm086] [PMID: 17686822]
[73]
Ranpura V, Hapani S, Chuang J, Wu S. Risk of cardiac ischemia and arterial thromboembolic events with the angiogenesis inhibitor bevacizumab in cancer patients: A meta-analysis of randomized controlled trials. Acta Oncol 2010; 49(3): 287-97.
[http://dx.doi.org/10.3109/02841860903524396] [PMID: 20156114]
[74]
Marisi G, Cucchetti A, Ulivi P, et al. Ten years of sorafenib in hepatocellular carcinoma: Are there any predictive and/or prognostic markers? World J Gastroenterol 2018; 24(36): 4152-63.
[http://dx.doi.org/10.3748/wjg.v24.i36.4152] [PMID: 30271080]
[75]
Escudier B, Eisen T, Stadler WM, et al. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356(2): 125-34.
[http://dx.doi.org/10.1056/NEJMoa060655] [PMID: 17215530]
[76]
Llovet JM, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359(4): 378-90.
[http://dx.doi.org/10.1056/NEJMoa0708857] [PMID: 18650514]
[77]
Coelho RC, Reinert T, Campos F, et al. Sunitinib treatment in patients with advanced renal cell cancer: The Brazilian National Cancer Institute (INCA) experience. Int Braz J Urol 2016; 42(4): 694-703.
[http://dx.doi.org/10.1590/S1677-5538.IBJU.2015.0226] [PMID: 27564279]
[78]
Chu TF, Rupnick MA, Kerkela R, et al. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet 2007; 370(9604): 2011-9.
[http://dx.doi.org/10.1016/S0140-6736(07)61865-0] [PMID: 18083403]
[79]
Curigliano G, Cardinale D, Suter T, et al. Cardiovascular toxicity induced by chemotherapy, targeted agents and radiotherapy: ESMO Clinical Practice Guidelines. Ann Oncol 2012; 23(7): 155-66.
[http://dx.doi.org/10.1093/annonc/mds293]
[80]
Mitchell J, Lenihan D. Management of cancer-therapy-induced LV dysfunction: Can the guidelines help?. American College of Cardiology 2018.
[81]
Lee CS, Rattu MA, Kim SS. A review of a novel, Bruton’s tyrosine kinase inhibitor, ibrutinib. J Oncol Pharm Pract 2016; 22(1): 92-104.
[http://dx.doi.org/10.1177/1078155214561281] [PMID: 25425007]
[82]
Danilov AV, Persky DO. Incorporating acalabrutinib, a selec-tive next-generation Bruton tyrosine kinase inhibitor, into clinical practice for the treatment of haematological malignancies. Br J Haematol 2021; 193(1): 15-25.
[http://dx.doi.org/10.1111/bjh.17184] [PMID: 33216986]
[83]
Tam CS, Opat S, Simpson D, et al. Zanubrutinib for the treatment of relapsed or refractory mantle cell lymphoma. Blood Adv 2021; 5(12): 2577-85.
[http://dx.doi.org/10.1182/bloodadvances.2020004074] [PMID: 34152395]
[84]
Tang CPS, McMullen J, Tam C. Cardiac side effects of Bruton Tyrosine Kinase (BTK) inhibitors. Leuk Lymphoma 2018; 59(7): 1554-64.
[http://dx.doi.org/10.1080/10428194.2017.1375110] [PMID: 28901789]
[85]
Brown JR, Moslehi J, O’Brien S, et al. Characterization of atrial fibrillation adverse events reported in ibrutinib randomized controlled registration trials. Haematologica 2017; 102(10): 1796-805.
[http://dx.doi.org/10.3324/haematol.2017.171041] [PMID: 28751558]
[86]
Mato AR, Nabhan C, Barr PM, et al. Outcomes of CLL patients treated with sequential kinase inhibitor therapy: A real world experience. Blood 2016; 128(18): 2199-205.
[http://dx.doi.org/10.1182/blood-2016-05-716977] [PMID: 27601462]
[87]
Leong DP, Caron F, Hillis C, et al. The risk of atrial fibrillation with ibrutinib use: A systematic review and meta-analysis. Blood 2016; 128(1): 138-40.
[http://dx.doi.org/10.1182/blood-2016-05-712828] [PMID: 27247135]
[88]
Baptiste F, Cautela J, Ancedy Y, et al. High incidence of atrial fibrillation in patients treated with ibrutinib. Open Heart 2019; 6(1): e001049.
[http://dx.doi.org/10.1136/openhrt-2019-001049] [PMID: 31168393]
[89]
Salem JE, Manouchehri A, Bretagne M, et al. Cardiovascular Toxicities Associated With Ibrutinib. J Am Coll Cardiol 2019; 74(13): 1667-78.
[http://dx.doi.org/10.1016/j.jacc.2019.07.056] [PMID: 31558250]
[90]
Dickerson T, Wiczer T, Waller A, et al. Hypertension and incident cardiovascular events following ibrutinib initiation. Blood 2019; 134(22): 1919-28.
[http://dx.doi.org/10.1182/blood.2019000840] [PMID: 31582362]
[91]
Highlights of prescribing information. 2019. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2019/213217s000lbl.pdf
[92]
Richardson PG, Barlogie B, Berenson J, et al. A phase 2 study of bortezomib in relapsed, refractory myeloma. N Engl J Med 2003; 348(26): 2609-17.
[http://dx.doi.org/10.1056/NEJMoa030288] [PMID: 12826635]
[93]
Groen K, van de Donk N, Stege C, Zweegman S, Nijhof IS. Carfilzomib for relapsed and refractory multiple myeloma. Cancer Manag Res 2019; 11: 2663-75.
[http://dx.doi.org/10.2147/CMAR.S150653] [PMID: 31037034]
[94]
Dasanu CA. Complete heart block secondary to bortezomib use in multiple myeloma. J Oncol Pharm Pract 2011; 17(3): 282-4.
[http://dx.doi.org/10.1177/1078155210367839] [PMID: 20406745]
[95]
Foley PW, Hamilton MS, Leyva F. Myocardial scarring fol-lowing chemotherapy for multiple myeloma detected using late gadolinium hyperenhancement cardiovascular magnetic resonance. J Cardiovasc Med 2010; 11: 386-8.
[http://dx.doi.org/10.2459/JCM.0b013e32832f3ff2]
[96]
Subedi A, Sharma LR, Shah BK. Bortezomib-induced acute congestive heart failure: A case report and review of literature. Ann Hematol 2014; 93(10): 1797-9.
[http://dx.doi.org/10.1007/s00277-014-2026-z] [PMID: 24599584]
[97]
Richardson PG, Sonneveld P, Schuster MW, et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 2005; 352(24): 2487-98.
[http://dx.doi.org/10.1056/NEJMoa043445] [PMID: 15958804]
[98]
Xiao Y, Yin J, Wei J, Shang Z. Incidence and risk of cardio-toxicity associated with bortezomib in the treatment of cancer: A systematic review and meta-analysis. PLoS One 2014; 9(1): e87671.
[http://dx.doi.org/10.1371/journal.pone.0087671] [PMID: 24489948]
[99]
Stewart AK, Rajkumar SV, Dimopoulos MA, et al. Carfilzomib, lenalidomide, and dexamethasone for relapsed multiple myeloma. N Engl J Med 2015; 372(2): 142-52.
[http://dx.doi.org/10.1056/NEJMoa1411321] [PMID: 25482145]
[100]
Dimopoulos MA, Moreau P, Palumbo A, et al. Carfilzomib and dexamethasone versus bortezomib and dexamethasone for patients with relapsed or refractory multiple myeloma (ENDEAVOR): A randomised, phase 3, open-label, multicentre study. Lancet Oncol 2016; 17(1): 27-38.
[http://dx.doi.org/10.1016/S1470-2045(15)00464-7] [PMID: 26671818]
[101]
Mikhael J, Ismaila N, Cheung MC, et al. Treatment of multiple myeloma: ASCO and CCO joint clinical practice guideline. J Clin Oncol 2019; 37(14): 1228-63.
[http://dx.doi.org/10.1200/JCO.18.02096] [PMID: 30932732]
[102]
Dimopoulos MA, Eleutherakis-Papaiakovou V. Adverse effects of thalidomide administration in patients with neo-plastic diseases. Am J Med 2004; 117(7): 508-15.
[http://dx.doi.org/10.1016/j.amjmed.2004.03.040] [PMID: 15464708]
[103]
Dimopoulos MA, Chen C, Spencer A, et al. Long-term follow-up on overall survival from the MM-009 and MM-010 phase III trials of lenalidomide plus dexamethasone in patients with relapsed or refractory multiple myeloma. Leukemia 2009; 23(11): 2147-52.
[http://dx.doi.org/10.1038/leu.2009.147] [PMID: 19626046]
[104]
Carrier M, Le Gal G, Tay J, Wu C, Lee AY. Rates of venous thromboembolism in multiple myeloma patients undergoing immunomodulatory therapy with thalidomide or lenalidomide: A systematic review and meta-analysis. J Thromb Haemost 2011; 9(4): 653-63.
[http://dx.doi.org/10.1111/j.1538-7836.2011.04215.x] [PMID: 21255254]
[105]
Miguel JS, Weisel K, Moreau P, et al. Pomalidomide plus low-dose dexamethasone versus high-dose dexamethasone alone for patients with relapsed and refractory multiple myeloma (MM-003): A randomised, open-label, phase 3 trial. Lancet Oncol 2013; 14(11): 1055-66.
[http://dx.doi.org/10.1016/S1470-2045(13)70380-2] [PMID: 24007748]
[106]
Palumbo A, Rajkumar SV, Dimopoulos MA, et al. Prevention of thalidomide- and lenalidomide-associated thrombosis in myeloma. Leukemia 2008; 22(2): 414-23.
[http://dx.doi.org/10.1038/sj.leu.2405062] [PMID: 18094721]
[107]
Mitchell J, Lenihan DJ. Management of cancer-therapy-induced LV dysfunction: Can the guidelines help?. ACC 2018.
[108]
Armenian SH, Lacchetti C, Barac A, et al. Prevention and monitoring of cardiac dysfunction in survivors of adult cancers: American society of clinical oncology clinical practice guideline. J Clin Oncol 2017; 35(8): 893-911.
[http://dx.doi.org/10.1200/JCO.2016.70.5400] [PMID: 27918725]
[109]
Ky B, Putt M, Sawaya H, et al. Early increases in multiple biomarkers predict subsequent cardiotoxicity in patients with breast cancer treated with doxorubicin, taxanes, and trastuzumab. J Am Coll Cardiol 2014; 63(8): 809-16.
[http://dx.doi.org/10.1016/j.jacc.2013.10.061] [PMID: 24291281]
[110]
Plummer C, Michael A, Shaikh G, et al. Expert recommendations on the management of hypertension in patients with ovarian and cervical cancer receiving bevacizumab in the UK. Br J Cancer 2019; 121(2): 109-16.
[http://dx.doi.org/10.1038/s41416-019-0481-y] [PMID: 31182765]
[111]
Balanescu DV, Donisan T, Palaskas NL, Iliescu C. Emerging concerns in cardio-oncology: Immune checkpoint inhibitor cardiotoxicity. 2019. Available from: https://www.acc.org/latest-in-cardiology/articles/2019/06/21/08/45/emerging-concerns-in-cardio-oncology
[112]
Escudier M, Cautela J, Malissen N, et al. Clinical features, management, and outcomes of immune checkpoint inhibitor-related cardiotoxicity. Circulation 2017; 136(21): 2085-7.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.117.030571] [PMID: 29158217]
[113]
Awadalla M, Mahmood SS, Groarke JD, et al. Global longitudinal strain and cardiac events in patients with immune checkpoint inhibitor-related myocarditis. Global longitudinal strain and cardiac events in patients with immune checkpoint inhibitor-related myocarditis. J Am Coll Cardiol 2020; 75(5): 467-78.
[http://dx.doi.org/10.1016/j.jacc.2019.11.049] [PMID: 32029128]
[114]
Ferreira VM, Schulz-Menger J, Holmvang G, et al. Cardiovascular magnetic resonance in nonischemic myocardial inflammation: Expert recommendations. J Am Coll Cardiol 2018; 72(24): 3158-76.
[http://dx.doi.org/10.1016/j.jacc.2018.09.072] [PMID: 30545455]
[115]
Zhang L, Awadalla M, Mahmood SS, et al. Cardiovascular magnetic resonance in immune checkpoint inhibitor-associated myocarditis. Eur Heart J 2020; 41(18): 1733-43.
[http://dx.doi.org/10.1093/eurheartj/ehaa051] [PMID: 32112560]
[116]
Aquaro GD, Perfetti M, Camastra G, et al. Cardiac MR with late gadolinium enhancement in acute myocarditis with preserved systolic function: ITAMY study. J Am Coll Cardiol 2017; 70(16): 1977-87.
[http://dx.doi.org/10.1016/j.jacc.2017.08.044] [PMID: 29025554]
[117]
Zhang L, Reynolds KL, Lyon AR, Palaskas N, Neilan TG. The evolving immunotherapy landscape and the epidemiology, diagnosis, and management of cardiotoxicity: Primer. JACC CardioOncol 2021; 3(1): 35-47.
[http://dx.doi.org/10.1016/j.jaccao.2020.11.012] [PMID: 33842895]
[118]
Brahmer JR, Lacchetti C, Schneider BJ, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American society of clinical oncology clinical practice guideline. J Clin Oncol 2018; 36(17): 1714-68.
[http://dx.doi.org/10.1200/JCO.2017.77.6385] [PMID: 29442540]
[119]
Weber JS, Hodi FS, Wolchok JD, et al. Safety profile of nivolumab monotherapy: A pooled analysis of patients with advanced melanoma. J Clin Oncol 2017; 35(7): 785-92.
[http://dx.doi.org/10.1200/JCO.2015.66.1389] [PMID: 28068177]
[120]
Arbour KC, Mezquita L, Long N, et al. Impact of baseline steroids on efficacy of programmed cell death-1 and programmed death-ligand 1 blockade in patients with non-small-cell lung cancer. J Clin Oncol 2018; 36(28): 2872-8.
[http://dx.doi.org/10.1200/JCO.2018.79.0006] [PMID: 30125216]
[121]
Faje AT, Lawrence D, Flaherty K, et al. High-dose glucocorticoids for the treatment of ipilimumab-induced hypophysitis is associated with reduced survival in patients with melanoma. Cancer 2018; 124(18): 3706-14.
[http://dx.doi.org/10.1002/cncr.31629] [PMID: 29975414]
[122]
Downey SG, Klapper JA, Smith FO, et al. Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin Cancer Res 2007; 13(22 Pt 1): 6681-8.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-0187] [PMID: 17982122]
[123]
Esfahani K, Buhlaiga N, Thébault P, Lapointe R, Johnson NA, Miller WH Jr. Alemtuzumab for immune-related myocarditis due to PD-1 therapy. N Engl J Med 2019; 380(24): 2375-6.
[http://dx.doi.org/10.1056/NEJMc1903064] [PMID: 31189042]
[124]
Tay RY, Blackley E, McLean C, et al. Successful use of equine anti-thymocyte globulin (ATGAM) for fulminant myocarditis secondary to nivolumab therapy. Br J Cancer 2017; 117(7): 921-4.
[http://dx.doi.org/10.1038/bjc.2017.253] [PMID: 28797029]
[125]
Kwon HJ, Coté TR, Cuffe MS, Kramer JM, Braun MM. Case reports of heart failure after therapy with a tumor necrosis factor antagonist. Ann Intern Med 2003; 138(10): 807-11.
[http://dx.doi.org/10.7326/0003-4819-138-10-200305200-00008] [PMID: 12755552]
[126]
Mir H, Alhussein M, Alrashidi S, et al. Cardiac complications associated with checkpoint inhibition: A systematic review of the literature in an important emerging area. Can J Cardiol 2018; 34(8): 1059-68.
[http://dx.doi.org/10.1016/j.cjca.2018.03.012] [PMID: 29980467]

Rights & Permissions Print Cite
Article Metrics
Pdf icon 96
Html icon 2
Find your institution