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

Alexander R Lyon, Susan Dent, Susannah Stanway, Helena Earl, Christine Brezden-Masley, Alain Cohen-Solal, Carlo G Tocchetti, Javid J Moslehi, John D Groarke, Jutta Bergler-Klein, Vincent Khoo, Li Ling Tan, Markus S Anker, Stephan von Haehling, Christoph Maack, Radek Pudil, Ana Barac, Paaladinesh Thavendiranathan, Bonnie Ky, Tomas G Neilan, Yury Belenkov, Stuart D Rosen, Zaza Iakobishvili, Aaron L Sverdlov, Ludhmila A Hajjar, Ariane V S Macedo, Charlotte Manisty, Fortunato Ciardiello, Dimitrios Farmakis, Rudolf A de Boer, Hadi Skouri, Thomas M Suter, Daniela Cardinale, Ronald M Witteles, Michael G Fradley, Joerg Herrmann, Robert F Cornell, Ashutosh Wechelaker, Michael J Mauro, Dragana Milojkovic, Hugues de Lavallade, Frank Ruschitzka, Andrew J S Coats, Petar M Seferovic, Ovidiu Chioncel, Thomas Thum, Johann Bauersachs, M Sol Andres, David J Wright, Teresa López-Fernández, Chris Plummer, Daniel Lenihan, Alexander R Lyon, Susan Dent, Susannah Stanway, Helena Earl, Christine Brezden-Masley, Alain Cohen-Solal, Carlo G Tocchetti, Javid J Moslehi, John D Groarke, Jutta Bergler-Klein, Vincent Khoo, Li Ling Tan, Markus S Anker, Stephan von Haehling, Christoph Maack, Radek Pudil, Ana Barac, Paaladinesh Thavendiranathan, Bonnie Ky, Tomas G Neilan, Yury Belenkov, Stuart D Rosen, Zaza Iakobishvili, Aaron L Sverdlov, Ludhmila A Hajjar, Ariane V S Macedo, Charlotte Manisty, Fortunato Ciardiello, Dimitrios Farmakis, Rudolf A de Boer, Hadi Skouri, Thomas M Suter, Daniela Cardinale, Ronald M Witteles, Michael G Fradley, Joerg Herrmann, Robert F Cornell, Ashutosh Wechelaker, Michael J Mauro, Dragana Milojkovic, Hugues de Lavallade, Frank Ruschitzka, Andrew J S Coats, Petar M Seferovic, Ovidiu Chioncel, Thomas Thum, Johann Bauersachs, M Sol Andres, David J Wright, Teresa López-Fernández, Chris Plummer, Daniel Lenihan

Abstract

This position statement from the Heart Failure Association of the European Society of Cardiology Cardio-Oncology Study Group in collaboration with the International Cardio-Oncology Society presents practical, easy-to-use and evidence-based risk stratification tools for oncologists, haemato-oncologists and cardiologists to use in their clinical practice to risk stratify oncology patients prior to receiving cancer therapies known to cause heart failure or other serious cardiovascular toxicities. Baseline risk stratification proformas are presented for oncology patients prior to receiving the following cancer therapies: anthracycline chemotherapy, HER2-targeted therapies such as trastuzumab, vascular endothelial growth factor inhibitors, second and third generation multi-targeted kinase inhibitors for chronic myeloid leukaemia targeting BCR-ABL, multiple myeloma therapies (proteasome inhibitors and immunomodulatory drugs), RAF and MEK inhibitors or androgen deprivation therapies. Applying these risk stratification proformas will allow clinicians to stratify cancer patients into low, medium, high and very high risk of cardiovascular complications prior to starting treatment, with the aim of improving personalised approaches to minimise the risk of cardiovascular toxicity from cancer therapies.

Keywords: Cardio-oncology; Cardiotoxicity; Heart failure; Risk factors; Risk prediction.

© 2020 The Authors. European Journal of Heart Failure published by John Wiley & Sons Ltd on behalf of European Society of Cardiology.

Figures

Figure 1
Figure 1
Examples of five different patients and primary or secondary prevention based on the history of pre-existing cardiovascular (CV) disease and/or prior cardiotoxicity from treatment of a previous malignancy.
Figure 2
Figure 2
The different risk factors which contribute to baseline cardiovascular (CV) risk in a cancer patient scheduled to receive a cardiotoxic cancer treatment, and a checklist of the clinical history and investigations required at baseline prior to starting a cardiotoxic cancer therapy. *Cardiac biomarkers (troponin and natriuretic peptides) should be measured where available. BNP, brain natriuretic peptide; ECG, electrocardiogram; HbA1c, glycated haemoglobin; NT-proBNP, N-terminal pro-brain natriuretic peptide.

References

    1. Zamorano JL, Lancellotti P, Rodriguez Munoz D, Aboyans V, Asteggiano R, Galderisi M, Habib G, Lenihan DJ, Lip GY, Lyon AR, Lopez Fernandez T, Mohty D, Piepoli MF, Tamargo J, Torbicki A, Suter TM; ESC Scientific Document Group. 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;37:2768–2801.
    1. Lancellotti P, Suter TM, Lopez-Fernandez T, Galderisi M, Lyon AR, Van der Meer P, Cohen Solal A, Zamorano JL, Jerusalem G, Moonen M, Aboyans V, Bax JJ, Asteggiano R. Cardio-oncology services: rationale, organization, and implementation: a report from the ESC Cardio-Oncology Council. Eur Heart J 2019;40:1756–1763.
    1. Pareek N, Cevallos J, Moliner P, Shah M, Tan LL, Chambers V, Baksi AJ, Khattar RS, Sharma R, Rosen SD, Lyon AR. Activity and outcomes of a cardio-oncology service in the United Kingdom – a five-year experience. Eur J Heart Fail 2018;20:1721–1731.
    1. Armenian SH, Lacchetti C, Barac A, Carver J, Constine LS, Denduluri N, Dent S, Douglas PS, Durand JB, Ewer M, Fabian C, Hudson M, Jessup M, Jones LW, Ky B, Mayer EL, Moslehi J, Oeffinger K, Ray K, Ruddy K, Lenihan D. Prevention and monitoring of cardiac dysfunction in survivors of adult cancers: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol 2017;35:893–911.
    1. Plana JC, Galderisi M, Barac A, Ewer MS, Ky B, Scherrer-Crosbie M, Ganame J, Sebag IA, Agler DA, Badano LP, Banchs J, Cardinale D, Carver J, Cerqueira M, DeCara JM, Edvardsen T, Flamm SD, Force T, Griffin BP, Jerusalem G, Liu JE, Magalhaes A, Marwick T, Sanchez LY, Sicari R, Villarraga HR, Lancellotti P. Expert consensus for multimodality imaging evaluation of adult patients during and after cancer therapy: a report from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 2014;15:1063–1093.
    1. Curigliano G, Cardinale D, Suter T, Plataniotis G, de Azambuja E, Sandri MT, Criscitiello C, Goldhirsch A, Cipolla C, Roila F; ESMO Guidelines Working Group. Cardiovascular toxicity induced by chemotherapy, targeted agents and radiotherapy: ESMO Clinical Practice Guidelines. Ann Oncol 2012;23 Suppl 7:vii155–166.
    1. Lyon AR, Yousaf N, Battisti NML, Moslehi J, Larkin J. Immune checkpoint inhibitors and cardiovascular toxicity. Lancet Oncol 2018;19:e447–e458.
    1. Mahmood SS, Fradley MG, Cohen JV, Nohria A, Reynolds KL, Heinzerling LM, Sullivan RJ, Damrongwatanasuk R, Chen CL, Gupta D, Kirchberger MC, Awadalla M, Hassan MZ, Moslehi JJ, Shah SP, Ganatra S, Thavendiranathan P, Lawrence DP, Groarke JD, Neilan TG. Myocarditis in patients treated with immune checkpoint inhibitors. J Am Coll Cardiol 2018;71:1755–1764.
    1. Alvi RM, Frigault MJ, Fradley MG, Jain MD, Mahmood SS, Awadalla M, Lee DH, Zlotoff DA, Zhang L, Drobni ZD, Hassan MZ, Bassily E, Rhea I, Ismail-Khan R, Mulligan CP, Banerji D, Lazaryan A, Shah BD, Rokicki A, Raje N, Chavez JC, Abramson J, Locke FL, Neilan TG. Cardiovascular events among adults treated with chimeric antigen receptor T-cells (CAR-T). J Am Coll Cardiol 2019;74:3099–3108.
    1. Wang L, Tan TC, Halpern EF, Neilan TG, Francis SA, Picard MH, Fei H, Hochberg EP, Abramson JS, Weyman AE, Kuter I, Scherrer-Crosbie M. Major cardiac events and the value of echocardiographic evaluation in patients receiving anthracycline-based chemotherapy. Am J Cardiol 2015;116:442–446.
    1. Salz T, Zabor EC, de Nully Brown P, Dalton SO, Raghunanthan NJ, Matasar MJ, Steingart R, Vickers AJ, Svenssen Munksgaard P, Oeffinger KC, Johansen C. Preexisting cardiovascular risk and subsequent heart failure among non-Hodgkin lymphoma survivors. J Clin Oncol 2017;35:3837–3843.
    1. Pinder MC, Duan Z, Goodwin JS, Hortobagyi GN, Giordano SH. Congestive heart failure in older women treated with adjuvant anthracycline chemotherapy for breast cancer. J Clin Oncol 2007;25:3808–3815.
    1. Cardinale D, Sandri MT, Martinoni A, Tricca LabTech A, Civelli M, Lamantia G, Cinieri S, Martinelli G, Cipolla CM, Fiorentini C. Left ventricular dysfunction predicted by early troponin I release after high-dose chemotherapy. J Am Coll Cardiol 2000;36:517–522.
    1. Cardinale D, Sandri MT, Colombo A, Colombo N, Boeri M, Lamantia G, Civelli M, Peccatori F, Martinelli G, Fiorentini C, Cipolla CM. Prognostic value of troponin I in cardiac risk stratification of cancer patients undergoing high-dose chemotherapy. Circulation 2004;109:2749–2754.
    1. Ky B, Putt M, Sawaya H, French B, Januzzi JL Jr, Sebag IA, Plana JC, Cohen V, Banchs J, Carver JR, Wiegers SE, Martin RP, Picard MH, Gerszten RE, Halpern EF, Passeri J, Kuter I, Scherrer-Crosbie M. Early increases in multiple biomarkers predict subsequent cardiotoxicity in patients with breast cancer treated with doxorubicin, taxanes, and trastuzumab. J Am Coll Cardiol 2014;63:809–816.
    1. Lenihan DJ, Stevens PL, Massey M, Plana JC, Araujo DM, Fanale MA, Fayad LE, Fisch MJ, Yeh ET. The utility of point-of-care biomarkers to detect cardiotoxicity during anthracycline chemotherapy: a feasibility study. J Card Fail 2016;22:433–438.
    1. De Iuliis F, Salerno G, Taglieri L, De Biase L, Lanza R, Cardelli P, Scarpa S. Serum biomarkers evaluation to predict chemotherapy-induced cardiotoxicity in breast cancer patients. Tumour Biol 2016;37:3379–3387.
    1. Von Hoff DD, Layard MW, Basa P, Davis HL Jr, Von Hoff AL, Rozencweig M, Muggia FM. Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med 1979;91:710–717.
    1. Swain SM, Whaley FS, Ewer MS. Congestive heart failure in patients treated with doxorubicin: a retrospective analysis of three trials. Cancer 2003;97:2869–2879.
    1. Hequet O, Le QH, Moullet I, Pauli E, Salles G, Espinouse D, Dumontet C, Thieblemont C, Arnaud P, Antal D, Bouafia F, Coiffier B. Subclinical late cardiomyopathy after doxorubicin therapy for lymphoma in adults. J Clin Oncol 2004;22:1864–1871.
    1. Szmit S, Jurczak W, Zaucha JM, Drozd-Sokolowska J, Spychalowicz W, Joks M, Długosz-Danecka M, Torbicki A. Pre-existing arterial hypertension as a risk factor for early left ventricular systolic dysfunction following (R)-CHOP chemotherapy in patients with lymphoma. J Am Soc Hypertens 2014;8:791–799.
    1. Mulrooney DA, Yeazel MW, Kawashima T, Mertens AC, Mitby P, Stovall M, Donaldson SS, Green DM, Sklar CA, Robison LL, Leisenring WM. Cardiac outcomes in a cohort of adult survivors of childhood and adolescent cancer: retrospective analysis of the Childhood Cancer Survivor Study cohort. BMJ 2009;339:b4606.
    1. van Nimwegen FA, Schaapveld M, Janus CP, Krol AD, Petersen EJ, Raemaekers JM, Kok WE, Aleman BM, van Leeuwen FE. Cardiovascular disease after Hodgkin lymphoma treatment: 40-year disease risk. JAMA Intern Med 2015;175:1007–1017.
    1. Gianni L, Dombernowsky P, Sledge G, Martin M, Amadori D, Arbuck SG, Ravdin P, Brown M, Messina M, Tuck D, Weil C, Winograd B. Cardiac function following combination therapy with paclitaxel and doxorubicin: an analysis of 657 women with advanced breast cancer. Ann Oncol 2001;12:1067–1073.
    1. Volkova M, Russell R. Anthracycline cardiotoxicity: prevalence, pathogenesis and treatment. Curr Cardiol Rev 2011;7:214–220.
    1. Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Bronnum D, Correa C, Cutter D, Gagliardi G, Gigante B, Jensen MB, Nisbet A, Peto R, Rahimi K, Taylor C, Hall P. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med 2013;368:987–998.
    1. van der Pal HJ, van Dalen EC, van Delden E, van Dijk IW, Kok WE, Geskus RB, Sieswerda E, Oldenburger F, Koning CC, van Leeuwen F, Caron HN, Kremer LC. High risk of symptomatic cardiac events in childhood cancer survivors. J Clin Oncol 2012;30:1429–1437.
    1. Barrett-Lee PJ, Dixon JM, Farrell C, Jones A, Leonard R, Murray N, Palmieri C, Plummer CJ, Stanley A, Verrill MW. Expert opinion on the use of anthracyclines in patients with advanced breast cancer at cardiac risk. Ann Oncol 2009;20:816–827.
    1. Guenancia C, Lefebvre A, Cardinale D, Yu AF, Ladoire S, Ghiringhelli F, Zeller M, Rochette L, Cottin Y, Vergely C. Obesity as a risk factor for anthracyclines and trastuzumab cardiotoxicity in breast cancer: a systematic review and meta-analysis. J Clin Oncol 2016;34:3157–3165.
    1. Kotwinski P, Smith G, Cooper J, Sanders J, Ma L, Teis A, Kotwinski D, Mythen M, Pennell DJ, Jones A, Montgomery H; Breast cancer Early disease: Toxicity from Therapy with Epirubicin Regimens–Cardiac Assessment and Risk Evaluation (BETTER-CARE) Study Investigators. Body surface area and baseline blood pressure predict subclinical anthracycline cardiotoxicity in women treated for early breast cancer. PLoS One 2016;11:e0165262.
    1. Serrano C, Cortes J, De Mattos-Arruda L, Bellet M, Gomez P, Saura C, Pérez J, Vidal M, Muñoz-Couselo E, Carreras MJ, Sánchez-Ollé G, Tabernero J, Baselga J, Di Cosimo S. Trastuzumab-related cardiotoxicity in the elderly: a role for cardiovascular risk factors. Ann Oncol 2012;23:897–902.
    1. Ezaz G, Long JB, Gross CP, Chen J. Risk prediction model for heart failure and cardiomyopathy after adjuvant trastuzumab therapy for breast cancer. J Am Heart Assoc 2014;3:e000472.
    1. Chavez-MacGregor M, Zhang N, Buchholz TA, Zhang Y, Niu J, Elting L, Smith BD, Hortobagyi GN, Giordano SH. Trastuzumab-related cardiotoxicity among older patients with breast cancer. J Clin Oncol 2013;31:4222–4228.
    1. Gunaldi M, Duman BB, Afsar CU, Paydas S, Erkisi M, Kara IO, Sahin B. Risk factors for developing cardiotoxicity of trastuzumab in breast cancer patients: an observational single-centre study. J Oncol Pharm Pract 2016;22:242–247.
    1. Romond EH, Jeong JH, Rastogi P, Swain SM, Geyer CE Jr, Ewer MS, Rathi V, Fehrenbacher L, Brufsky A, Azar CA, Flynn PJ, Zapas JL, Polikoff J, Gross HM, Biggs DD, Atkins JN, Tan-Chiu E, Zheng P, Yothers G, Mamounas EP, Wolmark N . Seven-year follow-up assessment of cardiac function in NSABP B-31, a randomized trial comparing doxorubicin and cyclophosphamide followed by paclitaxel (ACP) with ACP plus trastuzumab as adjuvant therapy for patients with node-positive, human epidermal growth factor receptor 2-positive breast cancer. J Clin Oncol 2012;30:3792–3799.
    1. Perez EA, Suman VJ, Davidson NE, Sledge GW, Kaufman PA, Hudis CA, Martino S, Gralow JR, Dakhil SR, Ingle JN, Winer EP, Gelmon KA, Gersh BJ, Jaffe AS, Rodeheffer RJ. Cardiac safety analysis of doxorubicin and cyclophosphamide followed by paclitaxel with or without trastuzumab in the North Central Cancer Treatment Group N9831 Adjuvant Breast Cancer trial. J Clin Oncol 2008;26:1231–1238.
    1. Nowsheen S, Aziz K, Park JY, Lerman A, Villarraga HR, Ruddy KJ, Herrmann J. Trastuzumab in female breast cancer patients with reduced left ventricular ejection fraction. J Am Heart Assoc 2018;7:e008637.
    1. Cardinale D, Colombo A, Torrisi R, Sandri MT, Civelli M, Salvatici M, Lamantia G, Colombo N, Cortinovis S, Dessanai MA, Nolè F, Veglia F, Cipolla CM. Trastuzumab-induced cardiotoxicity: clinical and prognostic implications of troponin I evaluation. J Clin Oncol 2010;28:3910–3916.
    1. Zardavas D, Suter TM, Van Veldhuisen DJ, Steinseifer J, Noe J, Lauer S, Al-Sakaff N, Piccart-Gebhart MJ, de Azambuja E. Role of troponins I and T and N-terminal prohormone of brain natriuretic peptide in monitoring cardiac safety of patients with early-stage human epidermal growth factor receptor 2-positive breast cancer receiving trastuzumab: a Herceptin adjuvant study cardiac marker substudy. J Clin Oncol 2017;35:878–884.
    1. Seidman A, Hudis C, Pierri MK, Shak S, Paton V, Ashby M, Murphy M, Stewart SJ, Keefe D. Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin Oncol 2002;20:1215–1221.
    1. Tarantini L, Cioffi G, Gori S, Tuccia F, Boccardi L, Bovelli D, Lestuzzi C, Maurea N, Oliva S, Russo G, Faggiano P; Italian Cardio-Oncologic Network. Trastuzumab adjuvant chemotherapy and cardiotoxicity in real-world women with breast cancer. J Card Fail 2012;18:113–119.
    1. Jawa Z, Perez RM, Garlie L, Singh M, Qamar R, Khandheria BK, Jahangir A, Shi Y. Risk factors of trastuzumab-induced cardiotoxicity in breast cancer: a meta-analysis. Medicine (Baltimore) 2016;95:e5195.
    1. Adamo V, Ricciardi GR, Adamo B, Ferraro G, Franchina T, Rossello R, Zanghì M, Cicero G, Rizzo S, Caristi N, Russo A. The risk of toxicities from trastuzumab, alone or in combination, in an elderly breast cancer population. Oncology 2014;86:16–21.
    1. Slamon D, Eiermann W, Robert N, Pienkowski T, Martin M, Press M, Mackey J, Glaspy J, Chan A, Pawlicki M, Pinter T, Valero V, Liu MC, Sauter G, von Minckwitz G, Visco F, Bee V, Buyse M, Bendahmane B, Tabah-Fisch I, Lindsay MA, Riva A, Crown J; Breast Cancer International Research Group. Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med 2011;365:1273–1283.
    1. Suter TM, Procter M, van Veldhuisen DJ, Muscholl M, Bergh J, Carlomagno C, Perren T, Passalacqua R, Bighin C, Klijn JG, Ageev FT, Hitre E, Groetz J, Iwata H, Knap M, Gnant M, Muehlbauer S, Spence A, Gelber RD, Piccart-Gebhart MJ. Trastuzumab-associated cardiac adverse effects in the herceptin adjuvant trial. J Clin Oncol 2007;25:3859–3865.
    1. Guglin M, Hartlage G, Reynolds C, Chen R, Patel V. Trastuzumab-induced cardiomyopathy: not as benign as it looks? A retrospective study. J Card Fail 2009;15:651–657.
    1. Huszno J, Les D, Sarzyczny-Slota D, Nowara E. Cardiac side effects of trastuzumab in breast cancer patients – single centere experiences. Contemp Oncol (Pozn) 2013;17:190–195.
    1. Ewer MS, Suter TM, Lenihan DJ, Niculescu L, Breazna A, Demetri GD, Motzer RJ. Cardiovascular events among 1090 cancer patients treated with sunitinib, interferon, or placebo: a comprehensive adjudicated database analysis demonstrating clinically meaningful reversibility of cardiac events. Eur J Cancer 2014;50:2162–2170.
    1. Hurley PJ, Konety S, Cao Q, Oertli C, Vankina S, Blaes AH. Frequency and risk factors for tyrosine kinase inhibitor-associated cardiotoxicity. J Clin Oncol 2016;34(15 Suppl):6596.
    1. Schmidinger M, Zielinski CC, Vogl UM, Bojic A, Bojic M, Schukro C, Ruhsam M, Hejna M, Schmidinger H. Cardiac toxicity of sunitinib and sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol 2008;26:5204–5212.
    1. Chu TF, Rupnick MA, Kerkela R, Dallabrida SM, Zurakowski D, Nguyen L, Woulfe K, Pravda E, Cassiola F, Desai J, George S, Harris DM, Ismail NS, Chen JH, Schoen FJ, van den Abbeele AD, Demetri GD, Force T, Chen MH, Morgan JA. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet 2007;370:2011–2019.
    1. Di Lorenzo G, Autorino R, Bruni G, Carteni G, Ricevuto E, Tudini M, Ficorella C, Romano C, Aieta M, Giordano A, Giuliano M, Gonnella A, De Nunzio C, Rizzo M, Montesarchio V, Ewer M, De Placido S. Cardiovascular toxicity following sunitinib therapy in metastatic renal cell carcinoma: a multicenter analysis. Ann Oncol 2009;20:1535–1542.
    1. Hall PS, Harshman LC, Srinivas S, Witteles RM. The frequency and severity of cardiovascular toxicity from targeted therapy in advanced renal cell carcinoma patients. JACC Heart Fail 2013;1:72–78.
    1. Hamnvik OP, Choueiri TK, Turchin A, McKay RR, Goyal L, Davis M, Kaymakcalan MD, Williams JS. Clinical risk factors for the development of hypertension in patients treated with inhibitors of the VEGF signaling pathway. Cancer 2015;121:311–319.
    1. Kozloff M, Yood MU, Berlin J, Flynn PJ, Kabbinavar FF, Purdie DM, Ashby MA, Dong W, Sugrue MM, Grothey A; Investigators of the BRiTE Study. Clinical outcomes associated with bevacizumab-containing treatment of metastatic colorectal cancer: the BRiTE observational cohort study. Oncologist 2009;14:862–870.
    1. Scappaticci FA, Skillings JR, Holden SN, Gerber HP, Miller K, Kabbinavar F, Bergsland E, Ngai J, Holmgren E, Wang J, Hurwitz H. Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab. J Natl Cancer Inst 2007;99:1232–1239.
    1. Touyz RM, Herrmann J. Cardiotoxicity with vascular endothelial growth factor inhibitor therapy. NPJ Precis Oncol 2018;2:13.
    1. Neiman V, Gottfried M, Hammers HJ, Eisenberger MA, Carducci MA, Sinibaldi VJ, Rosenbaum E, Sarid D, Gez E, Peer A, Neumann A, Kovel S, Sella A, Mermershtain W, Rouvinov K, Berger R, Kejzman D. Clinicopathologic factors associated with the development of sunitinib-induced hypertension (HTN) in patients (pts) with metastatic renal cell carcinoma (mRCC). J Clin Oncol 2014;32(15 Suppl):508 (abstr).
    1. Dahlen T, Edgren G, Lambe M, Hoglund M, Bjorkholm M, Sandin F, Själander A, Richter J, Olsson-Strömberg U, Ohm L, Bäck M, Stenke L; Swedish CML Group and the Swedish CML Register Group. Cardiovascular events associated with use of tyrosine kinase inhibitors in chronic myeloid leukemia: a population-based cohort study. Ann Intern Med 2016;165:161–166.
    1. Lipton JH, Chuah C, Guerci-Bresler A, Rosti G, Simpson D, Assouline S, Etienne G, Nicolini FE, le Coutre P, Clark RE, Stenke L, Andorsky D, Oehler V, Lustgarten S, Rivera VM, Clackson T, Haluska FG, Baccarani M, Cortes JE, Guilhot F, Hochhaus A, Hughes T, Kantarjian HM, Shah NP, Talpaz M, Deininger MW; EPIC investigators. Ponatinib versus imatinib for newly diagnosed chronic myeloid leukaemia: an international, randomised, open-label, phase 3 trial. Lancet Oncol 2016;17:612–621.
    1. Aghel N, Lipton JH, Atenafu EG, Kim DD, Delgado DH. Cardiovascular events after exposure to nilotinib in chronic myeloid leukemia: long-term follow-up. Clin Lymphoma Myeloma Leuk 2017;17:870–878.e1.
    1. Hochhaus A, Saglio G, Hughes TP, Larson RA, Kim DW, Issaragrisil S, le Coutre PD, Etienne G, Dorlhiac-Llacer PE, Clark RE, Flinn IW, Nakamae H, Donohue B, Deng W, Dalal D, Menssen HD, Kantarjian HM. Long-term benefits and risks of frontline nilotinib vs imatinib for chronic myeloid leukemia in chronic phase: 5-year update of the randomized ENESTnd trial. Leukemia 2016;30:1044–1054.
    1. Castagnetti F, Breccia M, Gugliotta G, Martino B, D’Adda M, Stagno F, Carella AM, Avanzini P, Tiribelli M, Trabacchi E, Visani G, Gobbi M, Salvucci M, Levato L, Binotto G, Capalbo SF, Bochicchio MT, Soverini S, Cavo M, Martinelli G, Alimena G, Pane F, Saglio G, Rosti G, Baccarani M; GIMEMA CML Working Party. Nilotinib 300 mg twice daily: an academic single-arm study of newly diagnosed chronic phase chronic myeloid leukemia patients. Haematologica 2016;101:1200–1207.
    1. Chen JH, Lenihan DJ, Phillips SE, Harrell SL, Cornell RF. Cardiac events during treatment with proteasome inhibitor therapy for multiple myeloma. Cardiooncology 2017;3:4.
    1. . Lenalidomide: risk of thrombosis and thromboembolism. February 2011. (3 June 2020).
    1. Cornell RF, Ky B, Weiss BM, Dahm CN, Gupta DK, Du L, Carver JR, Cohen AD, Engelhardt BG, Garfall AL, Goodman SA, Harrell SL, Kassim AA, Jadhav T, Jagasia M, Moslehi J, O’Quinn R, Savona MR, Slosky D, Smith A, Stadtmauer EA, Vogl DT, Waxman A, Lenihan D. Prospective study of cardiac events during proteasome inhibitor therapy for relapsed multiple myeloma. J Clin Oncol 2019;37:1946–1955.
    1. Libourel EJ, Sonneveld P, van der Holt B, de Maat MP, Leebeek FW. High incidence of arterial thrombosis in young patients treated for multiple myeloma: results of a prospective cohort study. Blood 2010;116:22–26.
    1. Danhof S, Schreder M, Rasche L, Strifler S, Einsele H, Knop S. ‘Real-life’ experience of preapproval carfilzomib-based therapy in myeloma – analysis of cardiac toxicity and predisposing factors. Eur J Haematol 2016;97:25–32.
    1. Cardinale D, Colombo A, Bacchiani G, Tedeschi I, Meroni CA, Veglia F, Civelli M, Lamantia G, Colombo N, Curigliano G, Fiorentini C, Cipolla CM. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation 2015;131:1981–1988.
    1. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M, Baselga J, Norton L. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001;344:783–792.
    1. Cameron D, Piccart-Gebhart MJ, Gelber RD, Procter M, Goldhirsch A, de Azambuja E, Castro G Jr, Untch M, Smith I, Gianni L, Baselga J, al-Sakaff N, Lauer S, McFadden E, Leyland-Jones B, Bell R, Dowsett M, Jackisch C; Herceptin Adjuvant (HERA) Trial Study Team. 11 years’ follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive early breast cancer: final analysis of the HERceptin Adjuvant (HERA) trial. Lancet 2017;389:1195–1205.
    1. Motzer RJ, McCann L, Deen K. Pazopanib versus sunitinib in renal cancer. N Engl J Med 2013;369:1970.
    1. Cortes JE, Kim DW, Pinilla-Ibarz J, le Coutre PD, Paquette R, Chuah C, Nicolini FE, Apperley JF, Khoury HJ, Talpaz M, DeAngelo DJ, Abruzzese E, Rea D, Baccarani M, Müller MC, Gambacorti-Passerini C, Lustgarten S, Rivera VM, Haluska FG, Guilhot F, Deininger MW, Hochhaus A, Hughes TP, Shah NP, Kantarjian HM. Ponatinib efficacy and safety in Philadelphia chromosome-positive leukemia: final 5-year results of the phase 2 PACE trial. Blood 2018;132:393–404.
    1. Giles FJ, Mauro MJ, Hong F, Ortmann CE, McNeill C, Woodman RC, Hochhaus A, le Coutre PD, Saglio G. Rates of peripheral arterial occlusive disease in patients with chronic myeloid leukemia in the chronic phase treated with imatinib, nilotinib, or non-tyrosine kinase therapy: a retrospective cohort analysis. Leukemia 2013;27:1310–1315.
    1. Caocci G, Mulas O, Bonifacio M, Abruzzese E, Galimberti S, Orlandi EM, Iurlo A, Annunziata M, Luciano L, Castagnetti F, Gozzini A, Stagno F, Binotto G, Pregno P, Albano F, Martino B, Fozza C, Scaffidi L, Trawinska MM, Baratè C, Elena C, Cattaneo D, Scalzulli E, la Nasa G, Foà R, Breccia M. Recurrent arterial occlusive events in patients with chronic myeloid leukemia treated with second- and third-generation tyrosine kinase inhibitors and role of secondary prevention. Int J Cardiol 2019;288:124–127.
    1. Fox LC, Cummins KD, Costello B, Yeung D, Cleary R, Forsyth C, Tatarczuch M, Burbury K, Motorna O, Shortt J, Fleming S, McQuillan A, Schwarer A, Harrup R, Holmes A, Ratnasingam S, Chan KL, Hsu WH, Ashraf A, Putt F, Grigg A. The incidence and natural history of dasatinib complications in the treatment of chronic myeloid leukemia. Blood Adv 2017;1:802–811.
    1. Shah NP, Wallis N, Farber HW, Mauro MJ, Wolf RA, Mattei D, Guha M, Rea D, Peacock A. Clinical features of pulmonary arterial hypertension in patients receiving dasatinib. Am J Hematol 2015;90:1060–1064.
    1. Moslehi JJ, Deininger M. Tyrosine kinase inhibitor-associated cardiovascular toxicity in chronic myeloid leukemia. J Clin Oncol 2015;33:4210–4218.
    1. Xiao Y, Yin J, Wei J, Shang Z. Incidence and risk of cardiotoxicity associated with bortezomib in the treatment of cancer: a systematic review and meta-analysis. PLoS One 2014;9:e87671.
    1. Gogas HJ, Flaherty KT, Dummer R, Ascierto PA, Arance A, Mandala M, Liszkay G, Garbe C, Schadendorf D, Krajsova I, Gutzmer R, Sileni VC, Dutriaux C, de Groot JW, Yamazaki N, Loquai C, Gollerkeri A, Pickard MD, Robert C. Adverse events associated with encorafenib plus binimetinib in the COLUMBUS study: incidence, course and management. Eur J Cancer 2019;119:97–106.
    1. Mincu RI, Mahabadi AA, Michel L, Mrotzek SM, Schadendorf D, Rassaf T, Totzeck M. Cardiovascular adverse events associated with BRAF and MEK inhibitors: a systematic review and meta-analysis. JAMA Netw Open 2019;2:e198890.
    1. Keating NL, O’Malley AJ, Freedland SJ, Smith MR. Diabetes and cardiovascular disease during androgen deprivation therapy: observational study of veterans with prostate cancer. J Natl Cancer Inst 2010;102:39–46.
    1. Keating NL, O’Malley AJ, Smith MR. Diabetes and cardiovascular disease during androgen deprivation therapy for prostate cancer. J Clin Oncol 2006;24:4448–4456.
    1. Gandaglia G, Sun M, Popa I, Schiffmann J, Abdollah F, Trinh QD, Saad F, Graefen M, Briganti A, Montorsi F, Karakiewicz PI. The impact of androgen-deprivation therapy (ADT) on the risk of cardiovascular (CV) events in patients with non-metastatic prostate cancer: a population-based study. BJU Int 2014;114:E82–E89.
    1. Herrmann J, Lerman A, Sandhu NP, Villarraga HR, Mulvagh SL, Kohli M. Evaluation and management of patients with heart disease and cancer: cardio-oncology. Mayo Clin Proc 2014;89:1287–1306.
    1. Piepoli MF, Hoes AW, Agewall S, Albus C, Brotons C, Catapano AL, Cooney MT, Corrà U, Cosyns B, Deaton C, Graham I, Hall MS, Hobbs FD, Løchen ML, Löllgen H, Marques-Vidal P, Perk J, Prescott E, Redon J, Richter DJ, Sattar N, Smulders Y, Tiberi M, van der Worp HB, van Dis I, Verschuren WM, ESC Scientific Document Group. 2016 European Guidelines on cardiovascular disease prevention in clinical practice: the Sixth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of 10 societies and by invited experts) developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR). Eur Heart J 2016;37: 2315–2381.
    1. Martinez-Quintana E, Miranda-Garcia C, Gopar-Gopar S, Saiz-Udaeta B, Rodriguez-Gonzalez F. Transient apical ballooning syndrome during dobutamine stress echocardiography. Clin Investig Arterioscler 2014;26:200–203.
    1. Hippisley-Cox J, Coupland C, Brindle P. Development and validation of QRISK3 risk prediction algorithms to estimate future risk of cardiovascular disease: prospective cohort study. BMJ 2017;357:j2099.
    1. Bhatia N, Santos M, Jones LW, Beckman JA, Penson DF, Morgans AK, Moslehi J. Cardiovascular effects of androgen deprivation therapy for the treatment of prostate cancer: ABCDE steps to reduce cardiovascular disease in patients with prostate cancer. Circulation 2016;133:537–541.

Source: PubMed

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