CC BY-NC-ND 4.0 · South Asian J Cancer 2021; 10(03): 195-210
DOI: 10.1055/s-0041-1731907
Cardio-Oncology

Bradyarrhythmias in Cardio-Oncology

Marta Fonseca
1   Division of Cardiology, Cardiac-Oncology Service, Bart’s Heart Centre, St Bartholomew’s Hospital West Smithfield, London, United Kingdom
2   Hatter Cardiovascular Institute, Institute of Cardiovascular Science UCL, University College London Hospital, London, United Kingdom
,
3   UCLA Cardio-Oncology Program, Division of Cardiology, Department of Medicine, University of California, Los Angeles, Los Angeles, California, United States
,
Duc Do
3   UCLA Cardio-Oncology Program, Division of Cardiology, Department of Medicine, University of California, Los Angeles, Los Angeles, California, United States
,
Shouvik Haldar
4   Division of Cardiology, Heart Rhythm Centre, The Royal Brompton and Harefield Hospitals, Guys & St Thomas’ NHS Foundation Trust, London, United Kingdom
5   National Heart and Lung Institute, Imperial College, London, United Kingdom
,
Shelby Kutty
6   The Helen B. Taussig Heart Center, The Johns Hopkins Hospital and Johns Hopkins University, Baltimore, Maryland, United States
,
Eric H. Yang
3   UCLA Cardio-Oncology Program, Division of Cardiology, Department of Medicine, University of California, Los Angeles, Los Angeles, California, United States
,
Arjun K. Ghosh#
1   Division of Cardiology, Cardiac-Oncology Service, Bart’s Heart Centre, St Bartholomew’s Hospital West Smithfield, London, United Kingdom
2   Hatter Cardiovascular Institute, Institute of Cardiovascular Science UCL, University College London Hospital, London, United Kingdom
,
Avirup Guha#
7   Harrington Heart and Vascular Institute, Case Western Reserve University, Cleveland, Ohio, United States
8   Division of Cardiology, Department of Medicine, Augusta University, Augusta, Georgia, United States
9   Division of Cardiology-Oncology Program, The Ohio State University, Columbus, Ohio, United States
› Institutsangaben
Funding None.

Abstract

The relationship between bradyarrhythmias and cancer therapies has not been well described but is increasingly recognized. There have been extensive advances in oncological pharmacotherapy, with several new classes of drugs available including targeted agents, immune checkpoint inhibitors and CAR T cell therapy. This increasing repertoire of available drugs has revolutionized overall prognosis and survival of cancer patients but the true extent of their cardiovascular toxicity is only beginning to be understood. Previous studies and published reviews have traditionally focused on conventional chemotherapies and in arrhythmias in general, particularly tachyarrhythmias. The number of patients with both cancer and cardiovascular problems is increasing globally and oncologists and cardiologists need to be adept at managing arrythmia based scenarios. Greater collaboration between the two specialties including studies with prospective data collection in Cardio-Oncology are much needed to fill in knowledge gaps in this arena. This case-based review summarizes current available evidence of cancer treatment-related bradyarrhythmia incidence (including its different subtypes), possible mechanisms and outcomes. Furthermore, we propose a stepwise surveillance and management protocol for patients with suspected bradyarrhythmia related to cancer treatment.

# Joint senior authors.




Publikationsverlauf

Artikel online veröffentlicht:
15. Oktober 2021

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  • References

  • 1 Elazhary S, Alawyat HA. Bradycardia associated with antithymocyte globulin treatment of a pediatric patient with sickle cell disease: a case report and literature review. Hematol Transfus Cell Ther 2020; (e-pub ahead of print). doi: DOI: 10.1016/j.htct.2020.08.018.
  • 2 Ando M, Yokozawa T, Sawada J. et al Cardiac conduction abnormalities in patients with breast cancer undergoing high-dose chemotherapy and stem cell transplantation. Bone Marrow Transplant 2000; 25 (02) 185-189
  • 3 Ramireddy K, Kane KM, Adhar GC. Acquired episodic complete heart block after high-dose chemotherapy with cyclophosphamide and thiotepa. Am Heart J 1994; 127 (03) 701-704
  • 4 Agarwal N, Burkart TA. Transient, high-grade atrioventricular block from high-dose cyclophosphamide. Tex Heart Inst J 2013; 40 (05) 626-627
  • 5 Haddad D, Guha A, Awan F, Daoud EG, Baliga R. Arrhythmias in cancer and cancer treatment: a review. In: Encyclopedia of Cardiovascular Research and Medicine Vol 1. Elsevier 2018: 162-181
  • 6 Tamargo J, Caballero R, Delpón E. Cancer chemotherapy and cardiac arrhythmias: a review. Drug Saf 2015; 38 (02) 129-152
  • 7 Kilickap S, Barista I, Akgul E, Aytemir K, Aksoy S, Tekuzman G. Early and late arrhythmogenic effects of doxorubicin. South Med J 2007; 100 (03) 262-265
  • 8 Darling HS. Cisplatin induced bradycardia. Int J Cardiol 2015; 182: 304-306
  • 9 Kucharz J, Michalowska-Kaczmarczyk A, Zygulska AL. et al Bradycardia as a rare symptom of cisplatin cardiotoxicity: a case report. Oncol Lett 2016; 11 (03) 2297-2299
  • 10 Schlumbrecht MP, Hehr K. Cisplatin-induced bradycardia and the importance of the QT interval. J Oncol Pharm Pract 2015; 21 (02) 157-160
  • 11 Altundağ O, Çelik I, Kars A. Recurrent asymptomatic bradycardia episodes after cisplatin infusion. Ann Pharmacother 2001; 35 (05) 641-642
  • 12 Talapatra K, Rajesh I, Rajesh B, Selvamani B, Subhashini J. Transient asymptomatic bradycardia in patients on infusional 5-fluorouracil. J Cancer Res Ther 2007; 3 (03) 169-171
  • 13 Stewart T, Pavlakis N, Ward M. Cardiotoxicity with 5-fluorouracil and capecitabine: more than just vasospastic angina. Intern Med J 2010; 40 (04) 303-307
  • 14 Khan MA, Masood N, Husain N, Ahmad B, Aziz T, Naeem A. A retrospective study of cardiotoxicities induced by 5-fluouracil (5-FU) and 5-FU based chemotherapy regimens in Pakistani adult cancer patients at Shaukat Khanum Memorial Cancer Hospital & Research Center. J Pak Med Assoc 2012; 62 (05) 430-434
  • 15 Kosmas C, Kallistratos MS, Kopterides P. et al Cardiotoxicity of fluoropyrimidines in different schedules of administration: a prospective study. J Cancer Res Clin Oncol 2008; 134 (01) 75-82
  • 16 Cil T, Kaplan MA, Altintas A, Pasa S, Isikdogan A. Cytosine-arabinoside induced bradycardia in patient with non-Hodgkin lymphoma: a case report. Leuk Lymphoma 2007; 48 (06) 1247-1249
  • 17 McGuire W, Rowinsky E, Rosenhein N. et al Taxol: a unique antineoplastic agent with significant activity in advanced ovarian epithelial neoplasms. Int J Gynaecol Obstet 1990; 31 (03) 298
  • 18 Huang CH, Chen WJ, Wu CC, Chen YC, Lee YT. Complete atrioventricular block after arsenic trioxide treatment in an acute promyelocytic leukemic patient. Pacing Clin Electrophysiol 1999; 22 (6 Pt 1) 965-967
  • 19 Shridhar PL. Interleukin-2 induced atrioventricular dissociation. Int J Collaborative Res Internal Med Public Health 2016; 8 (08) 510-511
  • 20 Foran JM, Rohatiner AZS, Cunningham D. et al European phase II study of rituximab (chimeric anti-CD20 monoclonal antibody) for patients with newly diagnosed mantle-cell lymphoma and previously treated mantle-cell lymphoma, immunocytoma, and small B-cell lymphocytic lymphoma. J Clin Oncol 2000; 18 (02) 317-324
  • 21 Ko Ko NL, Minaskeian N, El Masry HZ. A case of irreversible bradycardia after rituximab therapy for diffuse large B-cell lymphoma. Cardiooncology 2020; 6 (01) 22
  • 22 Cervera Grau JM, Esquerdo Galiana G, Belso Candela A, Llorca Ferrándiz C, Juárez Marroquí A, Maciá Escalante S. Complete atrioventricular block induced by rituximab in monotherapy in an aged patient with non-Hodgkin’s diffuse large B-cell lymphoma. Clin Transl Oncol 2008; 10 (05) 298-299
  • 23 Berenson JR, Jagannath S, Barlogie B. et al Safety of prolonged therapy with bortezomib in relapsed or refractory multiple myeloma. Cancer 2005; 104 (10) 2141-2148
  • 24 Enrico O, Gabriele B, Nadia C. et al Unexpected cardiotoxicity in haematological bortezomib treated patients. Br J Haematol 2007; 138 (03) 396-397
  • 25 Rajkumar SV, Gertz MA, Lacy MQ. et al Thalidomide as initial therapy for early-stage myeloma. Leukemia 2003; 17 (04) 775-779
  • 26 Fahdi IE, Gaddam V, Saucedo JF. et al Bradycardia during therapy for multiple myeloma with thalidomide. Am J Cardiol 2004; 93 (08) 1052-1055
  • 27 Hinterseer M, Becker A, Kääb S, Lang N, Näbauer M, Steinbeck G. Thalidomide-induced symptomatic third-degree atrioventricular block. Clin Res Cardiol 2006; 95 (09) 474-476
  • 28 Ou S-HI, Tang Y, Polli A, Wilner KD, Schnell P. Factors associated with sinus bradycardia during crizotinib treatment: a retrospective analysis of two large-scale multinational trials (PROFILE 1005 and 1007). Cancer Med 2016; 5 (04) 617-622
  • 29 Morcos PN, Bogman K, Hubeaux S. et al Effect of alectinib on cardiac electrophysiology: results from intensive electrocardiogram monitoring from the pivotal phase II NP28761 and NP28673 studies. Cancer Chemother Pharmacol 2017; 79 (03) 559-568
  • 30 Lorlatinib. FDA package insert. Published 2018. Available at: https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/ 210868s000lbl.pdf. Accessed February 15, 2021
  • 31 Ponatinib. FDA package insert. Published 2012. Available at: https://www.accessdata.fda.gov/drugsatfda_docs/label/2014/ 203469s009lbl.pdf. Accessed February 15, 2021
  • 32 Nilotinib. FDA package insert. Published 2017. Available at: https://www.accessdata.fda.gov/drugsatfda_docs/label/2017/ 022068s026lbl.pdf. Accessed February 15, 2021
  • 33 Ball S, Ghosh RK, Wongsaengsak S. et al Cardiovascular toxicities of immune checkpoint inhibitors: JACC Review Topic of the Week. J Am Coll Cardiol 2019; 74 (13) 1714-1727
  • 34 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 (08) 1059-1068
  • 35 Escudier M, Cautela J, Malissen N. et al Clinical features, management, and outcomes of immune checkpoint inhibitor-related cardiotoxicity. Circulation 2017; 136 (21) 2085-2087
  • 36 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
  • 37 Atallah-Yunes SA, Kadado AJ, Kaufman GP, Hernandez-Montfort J. Immune checkpoint inhibitor therapy and myocarditis: a systematic review of reported cases. J Cancer Res Clin Oncol 2019; 145 (06) 1527-1557
  • 38 Zlotoff DA, Hassan MZO, Zafar A. et al Electrocardiographic features of immune checkpoint inhibitor associated myocarditis. J Immunother Cancer 2021; 9 (03) e002007
  • 39 Mahmood SS, Chen CL, Shapnik N, Krishnan U, Singh HS, Makker V. Myocarditis with tremelimumab plus durvalumab combination therapy for endometrial cancer: a case report. Gynecol Oncol Rep 2018; 25: 74-77
  • 40 Katsume Y, Isawa T, Toi Y. et al Complete atrioventricular block associated with pembrolizumab-induced acute myocarditis: the need for close cardiac monitoring. Intern Med 2018; 57 (21) 3157-3162
  • 41 Yanase T, Moritoki Y, Kondo H, Ueyama D, Akita H, Yasui T. Myocarditis and myasthenia gravis by combined nivolumab and ipilimumab immunotherapy for renal cell carcinoma: a case report of successful management. Urol Case Rep 2020; 34: 101508
  • 42 Safi M, Ahmed H, Al-Azab M. et al PD-1/PDL-1 inhibitors and cardiotoxicity; molecular, etiological and management outlines. J Adv Res 2020; 29: 45-54
  • 43 Lyon AR, Yousaf N, Battisti NML, Moslehi J, Larkin J. Immune checkpoint inhibitors and cardiovascular toxicity. Lancet Oncol 2018; 19 (09) e447-e458
  • 44 Nishimura H, Okazaki T, Tanaka Y. et al Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001; 291 (5502) 319-322
  • 45 Okazaki T, Tanaka Y, Nishio R. et al Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat Med 2003; 9 (12) 1477-1483
  • 46 Love VA, Grabie N, Duramad P, Stavrakis G, Sharpe A, Lichtman A. CTLA-4 ablation and interleukin-12 driven differentiation synergistically augment cardiac pathogenicity of cytotoxic T lymphocytes. Circ Res 2007; 101 (03) 248-257
  • 47 Grabie N, Gotsman I, DaCosta R. et al Endothelial programmed death-1 ligand 1 (PD-L1) regulates CD8+ T-cell mediated injury in the heart. Circulation 2007; 116 (18) 2062-2071
  • 48 Johnson DB, Balko JM, Compton ML. et al Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med 2016; 375 (18) 1749-1755
  • 49 Desai MY, Windecker S, Lancellotti P. et al Prevention, diagnosis, and management of radiation-associated cardiac disease: JACC Scientific Expert Panel. J Am Coll Cardiol 2019; 74 (07) 905-927
  • 50 Desai MY, Jellis CL, Kotecha R, Johnston DR, Griffin BP. Radiation-associated cardiac disease: a practical approach to diagnosis and management. JACC Cardiovasc Imaging 2018; 11 (08) 1132-1149
  • 51 Adams MJ, Lipsitz SR, Colan SD. et al Cardiovascular status in long-term survivors of Hodgkin’s disease treated with chest radiotherapy. J Clin Oncol 2004; 22 (15) 3139-3148
  • 52 Orzan F, Brusca A, Gaita F, Giustetto C, Figliomeni MC, Libero L. Associated cardiac lesions in patients with radiation-induced complete heart block. Int J Cardiol 1993; 39 (02) 151-156
  • 53 Cohen SI, Bharati S, Glass J, Lev M. Radiotherapy as a cause of complete atrioventricular block in Hodgkin’s disease. An electrophysiological-pathological correlation. Arch Intern Med 1981; 141 (05) 676-679
  • 54 Slama MS, Le Guludec D, Sebag C. et al Complete atrioventricular block following mediastinal irradiation: a report of six cases. Pacing Clin Electrophysiol 1991; 14 (07) 1112-1118
  • 55 Heidenreich PA, Kapoor JR. Radiation induced heart disease: systemic disorders in heart disease. Heart 2009; 95 (03) 252-258
  • 56 Tzivoni D, Ratzkowski E, Biran S, Brook JG, Stern S. Complete heart block following therapeutic irradiation of the left side of the chest. Chest 1977; 71 (02) 231-234
  • 57 Donnellan E, Jellis CL, Griffin BP. Radiation-associated cardiac disease: from molecular mechanisms to clinical management. Curr Treat Options Cardiovasc Med 2019; 21 (05) 22
  • 58 Tapio S. Pathology and biology of radiation-induced cardiac disease. J Radiat Res (Tokyo) 2016; 57 (05) 439-448
  • 59 Boerma M, Sridharan V, Mao XW. et al Effects of ionizing radiation on the heart. Mutat Res 2016; 770 (Pt B) 319-327
  • 60 Scripture CD, Figg WD. Drug interactions in cancer therapy. Nat Rev Cancer 2006; 6 (07) 546-558
  • 61 Campen CJ, Vogel WH, Shah PJ. Managing drug interactions in cancer therapy: a guide for the advanced practitioner. J Adv Pract Oncol 2017; 8 (06) 609-620
  • 62 Stoll P, Kopittke L. Potential drug-drug interactions in hospitalized patients undergoing systemic chemotherapy: a prospective cohort study. Int J Clin Pharm 2015; 37 (03) 475-484
  • 63 van Leeuwen RWF, Brundel DHS, Neef C. et al Prevalence of potential drug-drug interactions in cancer patients treated with oral anticancer drugs. Br J Cancer 2013; 108 (05) 1071-1078
  • 64 Lam MSH, Ignoffo RJ. A guide to clinically relevant drug interactions in oncology. J Oncol Pharm Pract 2003; 9 (2-3) 45-85
  • 65 Kennedy C, Brewer L, Williams D. Drug interactions. Med (United Kingdom) 2016; 44 (07) 422-426
  • 66 Kheshti R, Aalipour M, Namazi S. A comparison of five common drug-drug interaction software programs regarding accuracy and comprehensiveness. J Res Pharm Pract 2016; 5 (04) 257-263
  • 67 Roblek T, Vaupotic T, Mrhar A, Lainscak M. Drug-drug interaction software in clinical practice: a systematic review. Eur J Clin Pharmacol 2015; 71 (02) 131-142
  • 68 Marcath LA, Xi J, Hoylman EK, Kidwell KM, Kraft SL, Hertz DL. Comparison of nine tools for screening drug-drug interactions of oral oncolytics. J Oncol Pract 2018; 14 (06) e368-e374
  • 69 Wolters Kluwer. Lexi-Interact Online. Published 2021. Available at: https/ www.uptodate.com/drug-interactions/ Accessed February 7, 2021
  • 70 Corporation IBM. Micromedex. Published 2021. Available at: https/ www.micromedexsolutions.com
  • 71 Kaur A, Yu SS, Lee AJ, Chiao TB. Thalidomide-induced sinus bradycardia. Ann Pharmacother 2003; 37 (7-8) 1040-1043
  • 72 Yamaguchi T. Syncope and sinus bradycardia from combined use of thalidomide and beta-blocker. Pharmacoepidemiol Drug Saf 2008; 17 (10) 1033-1035
  • 73 Rogala BG, Charpentier MM, Nguyen MK, Landolf KM, Hamad L, Gaertner KM. Oral anticancer therapy: management of drug interactions. J Oncol Pract 2019; 15 (02) 81-90
  • 74 Haouala A, Widmer N, Duchosal MA, Montemurro M, Buclin T, Decosterd LA. Drug interactions with the tyrosine kinase inhibitors imatinib, dasatinib, and nilotinib. Blood 2011; 117 (08) e75-e87
  • 75 Pembrolizumab Label FDA. Published 2014. Available at: http://www.accessdata.fda.gov/drugsatfda_docs/label/2014/ 125514lbl.pdf. Accessed February 15, 2021
  • 76 Ipilimumab Label FDA. Published 2011. Available at: https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/ 125377s094lbl.pdf. Accessed February 15, 2021
  • 77 Nivolumab Label FDA. Published 2014. Available at: https://www.accessdata.fda.gov/drugsatfda_docs/label/2019/ 125554s070lbl.pdf. Accessed February 15, 2021
  • 78 Khan A, Riaz S, Carhart Jr R. Pembrolizumab-induced mobitz type 2 second-degree atrioventricular block. Case Rep Cardiol 2020; 2020: 8428210
  • 79 Reddy N, Moudgil R, Lopez-Mattei JC. et al Progressive and reversible conduction disease with checkpoint inhibitors. Can J Cardiol 2017; 33 (10) 1335.e13-1335.e15
  • 80 Giancaterino S, Abushamat F, Duran J, Lupercio F, DeMaria A, Hsu JC. Complete heart block and subsequent sudden cardiac death from immune checkpoint inhibitor-associated myocarditis. HeartRhythm Case Rep 2020; 6 (10) 761-764
  • 81 AbbVie Inc. and Genentech USA I. Management of potential VENCLEXTA drug interactions. Published 2021. Available at: https://www.venclextahcp.com/cll/dosing/drug-interactions.html. Accessed April 4, 2021
  • 82 Kusumoto FM, Schoenfeld MH, Barrett C. et al 2018 ACC/AHA/HRS guideline on the evaluation and management of patients with bradycardia and cardiac conduction delay: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Rhythm Society. Circulation 2019; 140 (08) e382-e482
  • 83 Brignole M, Auricchio A, Baron-Esquivias G. et al ESC Committee for Practice Guidelines (CPG), Document Reviewers. 2013 ESC Guidelines on cardiac pacing and cardiac resynchronization therapy: the Task Force on cardiac pacing and resynchronization therapy of the European Society of Cardiology (ESC). Developed in collaboration with the European Heart Rhythm Association (EHRA). Eur Heart J 2013; 34 (29) 2281-2329
  • 84 Herrmann J. Adverse cardiac effects of cancer therapies: cardiotoxicity and arrhythmia. Nat Rev Cardiol 2020; 17 (08) 474-502
  • 85 Guglin M, Aljayeh M, Saiyad S, Ali R, Curtis AB. Introducing a new entity: chemotherapy-induced arrhythmia. Europace 2009; 11 (12) 1579-1586
  • 86 Buza V, Rajagopalan B, Curtis AB. Cancer treatment-induced arrhythmias: focus on chemotherapy and targeted therapies. Circ Arrhythm Electrophysiol 2017; 10 (08) 1-12
  • 87 Tshuma N, Glynn N, Evanson J, Powles T, Drake WM. Hypothalamitis and severe hypothalamic dysfunction associated with anti-programmed cell death ligand 1 antibody treatment. Eur J Cancer 2018; 104: 247-249
  • 88 Bukamur HS, Mezughi H, Karem E, Shahoub I, Shweihat Y. Nivolumab-induced third degree atrioventricular block in a patient with stage IV squamous cell lung carcinoma. Cureus 2019; 11 (06) e4869
  • 89 Prevel R, Colin G, Calès V, Renault PA, Mazieres J. Bloc atrio-ventriculaire de grade III compliquant une myocardite au décours d’un traitement par anti-PD1: observation d’un cas et revue de la littérature. Rev Med Interne 2020; 41 (04) 284-288
  • 90 Tan JL, Mugwagwa AN, Cieslik L, Joshi R. Nivolumab-induced myocarditis complicated by complete atrioventricular block in a patient with metastatic non-small cell lung cancer. BMJ Case Rep 2019; 12 (07) e229963
  • 91 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 (02) 155-158
  • 92 Samara Y, Yu CL, Dasanu CA. Acute autoimmune myocarditis and hepatitis due to ipilimumab monotherapy for malignant melanoma. J Oncol Pharm Pract 2019; 25 (04) 966-968
  • 93 Hardy T, Yin M, Chavez JA. et al Acute fatal myocarditis after a single dose of anti-PD-1 immunotherapy, autopsy findings: a case report. Cardiovasc Pathol 2020; 46: 107202
  • 94 Szuchan C, Elson L, Alley E. et al Checkpoint inhibitor-induced myocarditis and myasthenia gravis in a recurrent/metastatic thymic carcinoma patient: a case report. Eur Heart J Case Rep 2020; 4 (03) 1-8
  • 95 Lee DH, Armanious M, Huang J, Jeong D, Druta M, Fradley MG. Case of pembrolizumab-induced myocarditis presenting as torsades de pointes with safe re-challenge. J Oncol Pharm Pract 2020; 26 (06) 1544-1548
  • 96 Agrawal N, Khunger A, Vachhani P. et al Cardiac toxicity associated with immune checkpoint inhibitors: case series and review of the literature. Case Rep Oncol 2019; 12 (01) 260-276
  • 97 Brahmer JR, Lacchetti C, Schneider BJ. et al National Comprehensive Cancer Network. 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) 1714-1768
  • 98 Thompson JA, Schneider BJ, Brahmer J. et al NCCN guidelines insights: management of immunotherapy-related toxicities, version 1.2020. J Natl Compr Canc Netw 2020; 18 (03) 230-241
  • 99 Adams MJ, Lipshultz SE, Schwartz C, Fajardo LF, Coen V, Constine LS. Radiation-associated cardiovascular disease: manifestations and management. Semin Radiat Oncol 2003; 13 (03) 346-356
  • 100 Shen W-K, Sheldon RS, Benditt DG. et al 2017 ACC/AHA/HRS guideline for the evaluation and management of patients with syncope: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Rhythm Society. J Am Coll Cardiol 2017; 70 (05) e39-e110