Cardiotoxicity of anticancer treatments: Epidemiology, detection, and management

CA Cancer Journal for Clinicians

Volumn 66, Issue 4, 2016, Pages 309-325

  Curigliano, Giuseppe ^a   Cardinale, Daniela ^a   Dent, Susan ^b   Criscitiello, Carmen ^a   Aseyev, Olexiy ^b   Lenihan, Daniel ^c   Cipolla, Carlo Maria ^a  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b OTTAWA REGIONAL CANCER CENTRE   (Canada)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

cancer treatment; cardiac dysfunction; cardio oncology; cardiotoxicity; hypertension; rhythm disturbances; vascular events

Indexed keywords

ALDOSTERONE ANTAGONIST; AMINO TERMINAL PRO BRAIN NATRIURETIC PEPTIDE; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTHRACYCLINE; ANTINEOPLASTIC AGENT; ANTINEOPLASTIC ANTIMETABOLITE; BEVACIZUMAB; BIOLOGICAL MARKER; BRAIN NATRIURETIC PEPTIDE; CARVEDILOL; CEDIRANIB; CYCLOPHOSPHAMIDE; DASATINIB; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENALAPRIL; EPIRUBICIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LOW MOLECULAR WEIGHT HEPARIN; NEBIVOLOL; NILOTINIB; PLACEBO; PROTEIN TYROSINE KINASE INHIBITOR; RAZOXANE; SORAFENIB; SUNITINIB; TELMISARTAN; TRASTUZUMAB; TROPONIN; UNINDEXED DRUG; VASCULOTROPIN INHIBITOR;

ATHEROSCLEROSIS; CANCER CHEMOTHERAPY; CANCER REGISTRY; CANCER SURVIVAL; CARDIOTOXICITY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR PARAMETERS; CLINICAL TRIAL (TOPIC); DISEASE ASSOCIATION; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; DRUG WITHDRAWAL; ECHOCARDIOGRAPHY; ENDOTHELIAL DYSFUNCTION; HEART FAILURE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE INJURY; HEART PROTECTION; HEART VENTRICLE ARRHYTHMIA; HEMATOLOGIC MALIGNANCY; HUMAN; HYPERTENSION; ISCHEMIA; MULTICENTER STUDY (TOPIC); MULTIPLE MYELOMA; MYOCARDIAL STRAIN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PATIENT MONITORING; PLEURA EFFUSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PULMONARY HYPERTENSION; QT PROLONGATION; RADIATION INJURY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK BENEFIT ANALYSIS; SOLID TUMOR; STRAIN ECHOCARDIOGRAPHY; THROMBOSIS; VENOUS THROMBOEMBOLISM; ARRHYTHMIAS, CARDIAC; CARDIOVASCULAR DISEASES; CHEMICALLY INDUCED; DRUG EFFECTS; HEART; MEDICAL EDUCATION; NEOPLASMS; NON PROFIT ORGANIZATION; RISK FACTOR; UNITED STATES;

AMERICAN CANCER SOCIETY; ANTHRACYCLINES; ANTINEOPLASTIC AGENTS; ARRHYTHMIAS, CARDIAC; CARDIOTOXICITY; CARDIOVASCULAR DISEASES; EDUCATION, MEDICAL, CONTINUING; HEART; HUMANS; HYPERTENSION; NEOPLASMS; RISK FACTORS; UNITED STATES;

EID: 84960970537     PISSN: 00079235     EISSN: 15424863     Source Type: Journal    
DOI: 10.3322/caac.21341     Document Type: Review

References (168)

1. Jemal A, Ward E, Thun M. Declining death rates reflect progress against cancer [serial online]. PLoS One. 2010;5:e9584.
2. Howlader N, Ries LAG, Mariotto AB, Reichman ME, Ruhl J, Cronin KA. Improved estimates of cancer-specific survival rates from population-based data. J Natl Cancer Inst. 2010;102:1584-1598.
3. Jemal A, Ward E, Hao Y, Thun M. Trends in the leading causes of death in the United States, 1970–2002. JAMA. 2005;294:1255-1259.
4. Dent S, Liu P, Brezden-Masley C, Lenihan D. Cancer and cardiovascular disease: the complex labyrinth [serial online]. J Oncol. 2015;2015:516450.
5. Bodai BI, Tuso P. Breast cancer survivorship: a comprehensive review of long-term medical issues and lifestyle recommendations. Perm J. 2015;19:48-79.
6. Siegel R, DeSantis C, Virgo K, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin. 2012;62:220-241.
7. Chen J, Long JB, Hurria A, Owusu C, Steingart RM, Gross CP. Incidence of heart failure or cardiomyopathy after adjuvant trastuzumab therapy for breast cancer. J Am Coll Cardiol. 2012;60:2504-2512.
8. 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;104:1293-1305.
9. Aleman BM, Moser EC, Nuver J, et al. Cardiovascular disease after cancer therapy. EJC Suppl. 2014;12:18-28.
10. Taunk NK, Haffty BG, Kostis JB, Goyal S. Radiation-induced heart disease: pathologic abnormalities and putative mechanisms [serial online]. Front Oncol. 2015;5:39.
11. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015;65:5-29.
12. Force T, Kolaja KL. Cardiotoxicity of kinase inhibitors: the prediction and translation of preclinical models to clinical outcomes. Nat Rev Drug Discov. 2011;10:111-126.
13. Ewer MS, Ewer SM. Cardiotoxicity of anticancer treatments [serial online]. Nat Rev Cardiol. 2015;12:620.
14. Ali MK, Ewer MS, Gibbs HR, Swafford J, Graff KL. Late doxorubicin-associated cardiotoxicity in children. The possible role of intercurrent viral infection. Cancer. 1994;74:182-188.
15. Hahn VS, Lenihan DJ, Ky B. Cancer therapy-induced cardiotoxicity: basic mechanisms and potential cardioprotective therapies [serial online]. J Am Heart Assoc. 2014;3:e000665.
16. Suter TM, Ewer MS. Cancer drugs and the heart: importance and management. Eur Heart J. 2013;34:1102-1111.
17. Procter M, Suter TM, de Azambuja E, et al. Longer-term assessment of trastuzumab-related cardiac adverse events in the Herceptin Adjuvant (HERA) trial. J Clin Oncol. 2010;28:3422-3428.
18. 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.
19. Yeh ET, Tong AT, Lenihan DJ, et al. Cardiovascular complications of cancer therapy: diagnosis, pathogenesis, and management. Circulation. 2004;109:3122-3131.
20. Armstrong GT, Kawashima T, Leisenring W, et al. Aging and risk of severe, disabling, life-threatening, and fatal events in the Childhood Cancer Survivor Study. J Clin Oncol. 2014;32:1218-1227.
21. Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009;53:2231-2247.
22. 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.
23. Von Hoff DD, Layard MW, Basa P, et al. Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med. 1979;91:710-717.
24. Wouters KA, Kremer LCM, Miller TL, Herman EH, Lipshultz SE. Protecting against anthracycline-induced myocardial damage: a review of the most promising strategies. Br J Haematol. 2005;131:561-578.
25. Zhang S, Liu X, Bawa-Khalfe T, et al. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat Med. 2012;18:1639-1642.
26. Martin M, Pienkowski T, Mackey J, et al. Adjuvant docetaxel for node-positive breast cancer. N Engl J Med. 2005;352:2302-2313.
27. Barrett-Lee PJ, Dixon JM, Farrell C, et al. Expert opinion on the use of anthracyclines in patients with advanced breast cancer at cardiac risk. Ann Oncol. 2009;20:816-827.
28. Crozier JA, Swaika A, Moreno-Aspitia A. Adjuvant chemotherapy in breast cancer: to use or not to use, the anthracyclines. World J Clin Oncol. 2014;5:529-538.
29. Harbeck N, Ewer MS, De Laurentiis M, Suter TM, Ewer SM. Cardiovascular complications of conventional and targeted adjuvant breast cancer therapy. Ann Oncol. 2011;22:1250-1258.
30. Chlebowski RT. Adriamycin (doxorubicin) cardiotoxicity: a review. West J Med. 1979;131:364-368.
31. Tjuljandin SA, Doig RG, Sobol MM, et al. Pharmacokinetics and toxicity of two schedules of high dose epirubicin. Cancer Res. 1990;50:5095-5101.
32. Anderlini P, Benjamin RS, Wong FC, et al. Idarubicin cardiotoxicity: a retrospective study in acute myeloid leukemia and myelodysplasia. J Clin Oncol. 1995;13:2827-2834.
33. Perez E. Paclitaxel in breast cancer. Oncologist. 1998;3:373-389.
34. Kenmotsu H, Tanigawara Y. Pharmacokinetics, dynamics and toxicity of docetaxel: why the Japanese dose differs from the Western dose. Cancer Sci. 2015;106:497-504.
35. Gottdiener JS, Appelbaum FR, Ferrans VJ, Deisseroth A, Ziegler J. Cardiotoxicity associated with high-dose cyclophosphamide therapy. Arch Intern Med. 1981;141:758-763.
36. Goldberg MA, Antin JH, Guinan EC, Rappeport JM. Cyclophosphamide cardiotoxicity: an analysis of dosing as a risk factor. Blood. 1986;68:1114-1118.
37. Kandylis K, Vassilomanolakis M, Tsoussis S, Efremidis AP. Ifosfamide cardiotoxicity in humans. Cancer Chemother Pharmacol. 1989;24:395-396.
38. Tascilar M, Loos WJ, Seynaeve C, Verweij J, Sleijfer S. The pharmacologic basis of ifosfamide use in adult patients with advanced soft tissue sarcomas. Oncologist. 2007;12:1351-1360.
39. Cancer Care Ontario. Ifosfamide: Drug Monograph. Cancer Care Ontario Drug Formulary-April 2014. Toronto, ON: Cancer Care Ontario; 2014.
40. Senturk T, Kanat O, Evrensel T, Aydinlar A. Capecitabine-induced cardiotoxicity mimicking myocardial infarction. Neth Heart J. 2009;17(7–8):277-280.
41. Schimmel KG, Richel DJ, van den Brink RB, Guchelaar HJ. Cardiotoxicity of cytotoxic drugs. Cancer Treat Rev. 2004;30:181-191.
42. Chanan-Khan A, Srinivasan S, Czuczman MS. Prevention and management of cardiotoxicity from antineoplastic therapy. J Support Oncol. 2004;2:251-256; discussion 259–261, 264–266.
43. Lebedinsky C, Gomez J, Park YC, et al. Trabectedin has a low cardiac risk profile: a comprehensive cardiac safety analysis. Cancer Chemother Pharmacol. 2011;68:1223-1231.
44. Brana I, Tabernero J. Cardiotoxicity. Ann Oncol. 2010;21(suppl 7):vii173-vii179.
45. 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;23:7820-7826.
46. Smith I, Procter M, Gelber RD, et al. Two-year follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer: a randomised controlled trial. Lancet. 2007;369:29-36.
47. 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;29:3366-3373.
48. Slamon D, Eiermann W, Robert N, et al. Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med. 2011;365:1273-1283.
49. Goldhirsch A, Gelber RD, Piccart-Gebhart MJ, et al. Two years versus 1 year of adjuvant trastuzumab for HER2-positive breast cancer (HERA): an open-label, randomised controlled trial. Lancet. 2013;382:1021-1028.
50. Baselga J, Perez EA, Pienkowski T, Bell R. Adjuvant trastuzumab: a milestone in the treatment of HER-2-positive early breast cancer. Oncologist. 2006;11(suppl 1):4-12.
51. Mackey JR, Clemons M, Cote MA, et al. Cardiac management during adjuvant trastuzumab therapy: recommendations of the Canadian Trastuzumab Working Group. Curr Oncol. 2008;15:24-35.
52. Romond EH, Perez EA, Bryant J, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med. 2005;353:1673-1684.
53. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med. 2005;353:1659-1672.
54. Romond EH, Jeong JH, Rastogi P, et al. 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.
55. Lenihan D, Suter T, Brammer M, Neate C, Ross G, Baselga J. Pooled analysis of cardiac safety in patients with cancer treated with pertuzumab. Ann Oncol. 2012;23:791-800.
56. Gianni L, Pienkowski T, Im YH, et al. Efficacy and safety of neoadjuvant pertuzumab and trastuzumab in women with locally advanced, inflammatory, or early HER2-positive breast cancer (NeoSphere): a randomised multicentre, open-label, phase 2 trial. Lancet Oncol. 2012;13:25-32.
57. Reynolds K, Sarangi S, Bardia A, Dizon DS. Precision medicine and personalized breast cancer: combination pertuzumab therapy. Pharmgenomics Pers Med. 2014;7:95-105.
58. Sevcikova K, Vertakova-Krakovska B, Spanik S. Neoadjuvant treatment in patients with HER2-positive breast cancer [serial online]. ISRN Oncol. 2013;2013:362467.
59. Chu TF, Rupnick MA, Kerkela R, et al. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet. 2007;370:2011-2019.
60. Cheng H, Force T. Molecular mechanisms of cardiovascular toxicity of targeted cancer therapeutics. Circ Res. 2010;106:21-34.
61. Chintalgattu V, Ai D, Langley RR, et al. Cardiomyocyte PDGFR-β signaling is an essential component of the mouse cardiac response to load-induced stress. J Clin Invest. 2010;120:472-484.
62. Kloner RA, Jennings RB. Consequences of brief ischemia: stunning, preconditioning, and their clinical implications: part 2. Circulation. 2001;104:3158-3167.
63. Cardinale D, Colombo A, Lamantia G, et al. Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy. J Am Coll Cardiol. 2010;55:213-220.
64. Aslam S, Eisen T. Vascular endothelial growth factor receptor tyrosine kinase inhibitors in metastatic renal cell cancer: latest results and clinical implications. Ther Adv Med Oncol. 2013;5:324-333.
65. Dewdney A, Cunningham D, Barbachano Y, Chau I. Correlation of bevacizumab-induced hypertension and outcome in the BOXER study, a phase II study of capecitabine, oxaliplatin (CAPOX) plus bevacizumab as peri-operative treatment in 45 patients with poor-risk colorectal liver-only metastases unsuitable for upfront resection. Br J Cancer. 2012;106:1718-1721.
66. Mir O, Coriat R, Cabanes L, et al. An observational study of bevacizumab-induced hypertension as a clinical biomarker of antitumor activity. Oncologist. 2011;16:1325-1332.
67. Fraeman KH, Nordstrom BL, Luo W, Landis SH, Shantakumar S. Incidence of new-onset hypertension in cancer patients: a retrospective cohort study [serial online]. Int J Hypertens. 2013;2013:379252.
68. Chen J, Lu Y, Zheng Y. Incidence and risk of hypertension with bevacizumab in non-small-cell lung cancer patients: a meta-analysis of randomized controlled trials. Drug Des Dev Ther. 2015;9:4751-4760.
69. Gampenrieder SP, Romeder F, Muß C, et al. Hypertension as a predictive marker for bevacizumab in metastatic breast cancer: results from a retrospective matched-pair analysis. Anticancer Res. 2014;34:227-233.
70. Azad NS, Posadas EM, Kwitkowski VE, et al. Combination targeted therapy with sorafenib and bevacizumab results in enhanced toxicity and antitumor activity. J Clin Oncol. 2008;26:3709-3714.
71. Larochelle P, Kollmannsberger C, Feldman RD, et al. Hypertension management in patients with renal cell cancer treated with anti-angiogenic agents. Curr Oncol. 2012;19:202-208.
72. George S, Reichardt P, Lechner T, Li S, Cohen DP, Demetri GD. Hypertension as a potential biomarker of efficacy in patients with gastrointestinal stromal tumor treated with sunitinib. Ann Oncol. 2012;23:3180-3187.
73. Sungyub L, Chamberlain RS. Hypertension risk among cancer patients treated with sunitinib: a meta-analysis and systematic review [serial online]. Targeted Oncol. targetedonc.com/publications/targeted-therapies-cancer/2015/June-2015/Hypertension-Risk-Among-Cancer-Patients-Treated-With-Sunitinib-A-Meta-analysis-and-Systematic-Review. Accessed September 18, 2015.
74. Funakoshi T, Latif A, Galsky MD. Risk of hypertension in cancer patients treated with sorafenib: an updated systematic review and meta-analysis. J Hum Hypertens. 2013;27:601-611.
75. Langenberg MH, Van Herpen CM, De Bono J, et al. Effective strategies for management of hypertension after vascular endothelial growth factor signaling inhibition therapy: results from a phase II randomized, factorial, double-blind study of cediranib in patients with advanced solid tumors. J Clin Oncol. 2009;27:6152-6159.
76. Castellano D, Capdevila J, Sastre J, et al. Sorafenib and bevacizumab combination targeted therapy in advanced neuroendocrine tumour: a phase II study of Spanish Neuroendocrine Tumour Group (GETNE0801). Eur J Cancer. 2013;49:3780-3787.
77. Kamba T, McDonald DM. Mechanisms of adverse effects of anti-VEGF therapy for cancer. Br J Cancer. 2007;96:1788-1795.
78. Li W, Croce K, Steensma DP, McDermott DF, Ben-Yehuda O, Moslehi J. Vascular and metabolic implications of novel targeted cancer therapies. J Am Coll Cardiol. 2015;66:1160-1178.
79. Moslehi JJ, Deininger M. Tyrosine kinase inhibitor-associated cardiovascular toxicity in chronic myeloid leukemia. J Clin Oncol. 2015;33:4210-4218.
80. Grandin EW, Ky B, Cornell RF, Carver J, Lenihan DJ. Patterns of cardiac toxicity associated with irreversible proteasome inhibition in the treatment of multiple myeloma. J Card Fail. 2015;21:138-144.
81. Atrash S, Tullos A, Panozzo S, et al. Cardiac complications in relapsed and refractory multiple myeloma patients treated with carfilzomib [serial online]. Blood Cancer J. 2015;5:e272.
82. Montani D, Bergot E, Gunther S, et al. Pulmonary arterial hypertension in patients treated by dasatinib. Circulation. 2012;125:2128-2137.
83. Giles FJ, Mauro MJ, Hong F, et al. 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.
84. Kim TD, Rea D, Schwarz M, et al. Peripheral artery occlusive disease in chronic phase chronic myeloid leukemia patients treated with nilotinib or imatinib. Leukemia. 2013;27:1316-1321.
85. Cesarman-Maus G, Braggio E, Fonseca R. Thrombosis in multiple myeloma (MM). Hematology. 2012;17(suppl 1):S177-S180.
86. Brell JM. Prolonged QTc interval in cancer therapeutic drug development: defining arrhythmic risk in malignancy. Prog Cardiovasc Dis. 2010;53:164-172.
87. Guglin M, Aljayeh M, Saiyad S, Ali R, Curtis AB. Introducing a new entity: chemotherapy-induced arrhythmia. Europace. 2009;11:1579-1586.
88. Farmakis D, Parissis J, Filippatos G. Insights into onco-cardiology: atrial fibrillation in cancer. J Am Coll Cardiol. 2014;63:945-953.
89. Heidenreich PA, Hancock SL, Lee BK, Mariscal CS, Schnittger I. Asymptomatic cardiac disease following mediastinal irradiation. J Am Coll Cardiol. 2003;42:743-749.
90. Darby SC, Ewertz M, McGale P, et al. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 2013;368:987-998.
91. Heidenreich PA, Hancock SL, Vagelos RH, Lee BK, Schnittger I. Diastolic dysfunction after mediastinal irradiation. Am Heart J. 2005;150:977-982.
92. 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(suppl 7):vii155-vii166.
93. Gagliardi G, Constine LS, Moiseenko V, et al. Radiation dose-volume effects in the heart. Int J Radiat Oncol. 2010;76:S77-S85.
94. Plana JC, Galderisi M, Barac A, et al. 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. J Am Soc Echocardiogr. 2014;27:911-939.
95. Thavendiranathan P, Grant AD, Negishi T, Plana JC, Popovíc ZB, Marwick TH. Reproducibility of echocardiographic techniques for sequential assessment of left ventricular ejection fraction and volumes: application to patients undergoing cancer chemotherapy. J Am Coll Cardiol. 2013;61:77-84.
96. Betriu A, Castaner A, Sanz GA, et al. Angiographic findings 1 month after myocardial infarction: a prospective study of 259 survivors. Circulation. 1982;65:1099-1105.
97. Daneault B, Genereux P, Kirtane AJ, et al. Comparison of 3-year outcomes after primary percutaneous coronary intervention in patients with left ventricular ejection fraction <40% versus ≥40% (from the HORIZONS-AMI trial). Am J Cardiol. 2013;111:12-20.
98. Smith LA, Cornelius VR, Plummer CJ, et al. Cardiotoxicity of anthracycline agents for the treatment of cancer: systematic review and meta-analysis of randomised controlled trials [serial online]. BMC Cancer. 2010;10:337.
99. Jensen BV, Skovsgaard T, Nielsen SL. Functional monitoring of anthracycline cardiotoxicity: a prospective, blinded, long-term observational study of outcome in 120 patients. Ann Oncol. 2002;13:699-709.
100. Ewer MS, Lenihan DJ. Left ventricular ejection fraction and cardiotoxicity: is our ear really to the ground? J Clin Oncol. 2008;26:1201-1203.
101. Cardinale D, Colombo A., Bacchiani G, et al. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation. 2015;131:1981-1989.
102. Nagueh SF, Appleton CP, Gillebert TC, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr. 2009;10:165-193.
103. Thavendiranathan P, Poulin F, Lim K-D, Plana JC, Woo A, Marwick TH. Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: a systematic review. J Am Coll Cardiol. 2014;63(25 pt A):2751-2768.
104. Drafts BC, Twomley KM, D'Agostino R, et al. Low to moderate dose anthracycline-based chemotherapy is associated with early noninvasive imaging evidence of subclinical cardiovascular disease. JACC Cardiovasc Imaging. 2013;6:877-885.
105. Fallah-Rad N, Walker JR, Wassef A, et al. The utility of cardiac biomarkers, tissue velocity and strain imaging, and cardiac magnetic resonance imaging in predicting early left ventricular dysfunction in patients with human epidermal growth factor receptor II-positive breast cancer treated with adjuvant trastuzumab therapy. J Am Coll Cardiol. 2011;57:2263-2270.
106. Negishi K, Negishi T, Haluska BA, Hare JL, Plana JC, Marwick TH. Use of speckle strain to assess left ventricular responses to cardiotoxic chemotherapy and cardioprotection. Eur Heart J Cardiovasc Imaging. 2014;15:324-331.
107. Ky B, Carver JR. Biomarker approach to the detection and cardioprotective strategies during anthracycline chemotherapy. Heart Fail Clin. 2011;7:323-331.
108. 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;63:809-816.
109. Daubert MA, Jeremias A. The utility of troponin measurement to detect myocardial infarction: review of the current findings. Vasc Health Risk Manag. 2010;6:691-699.
110. Cardinale D, Sandri MT, Colombo A, et al. Prognostic value of troponin I in cardiac risk stratification of cancer patients undergoing high-dose chemotherapy. Circulation. 2004;109:2749-2754.
111. Hequet O, Le QH, Moullet I, et al. Subclinical late cardiomyopathy after doxorubicin therapy for lymphoma in adults. J Clin Oncol. 2004;22:1864-1871.
112. Colombo A, Sandri MT, Salvatici M, Cipolla CM, Cardinale D. Cardiac complications of chemotherapy: role of biomarkers. Curr Treat Options Cardiovasc Med. 2014;16:313-313.
113. Lipshultz SE, Rifai N, Sallan SE, Lipsitz SR, Dalton V, Sacks DB. Predictive value of cardiac troponin T in pediatric patients at risk for myocardial injury. Circulation. 1997;96:2641-2648.
114. Cardinale D, Sandri MT, Martinoni A, et al. Left ventricular dysfunction predicted by early troponin I release after high-dose chemotherapy. J Am Coll Cardiol. 2000;36:517-522.
115. Cardinale D, Sandri MT, Martinoni A, et al. Myocardial injury revealed by plasma troponin I in breast cancer treatment with high dose chemotherapy. Ann Oncol. 2002;13:710-715.
116. Auner HW, Tinchon C, Linkesch W, Tiran A, Quehenberger F, Link H. Prolonged monitoring of troponin T for the detection of anthracycline cardiotoxicity in adults with hematological malignancies. Ann Hematol. 2003;82:218-222.
117. Sandri MT, Cardinale D, Zorzino L, et al. Minor increases in plasma troponin I predict decreased left ventricular ejection fraction after high-dose chemotherapy. Clin Chem. 2003;49:248-252.
118. Specchia G, Buquicchio C, Pansini N, Di Serio F, Liso V, Pastore D. Monitoring of cardiac function on the basis of serum troponin I levels in patients with acute leukemia treated with anthracyclines. J Lab Clin Med. 2005;145:212-220.
119. Kilickap S, Barista I, Akgul E, Aytemir K, Aksoyek S, Aksoy S. cTnT can be a useful marker for early detection of anthracycline cardiotoxicity. Ann Oncol. 2005;16:798-804.
120. Lee HS, Son CB, Shin SH, Kim YS. Clinical correlation between brain natriutetic peptide and anthracyclin-induced cardiac toxicity. Cancer Res Treat. 2008;40:121-126.
121. Schmidinger M, Zielinski CC, Vogl UM, Bojic A, Bojic M, Schukro C. Cardiac toxicity of sunitinib and sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol. 2008;26:5204-5212.
122. Cardinale D, Colombo A, Torrisi R, et al. Trastuzumab-induced cardiotoxicity: clinical and prognostic implications of troponin I evaluation. J Clin Oncol. 2010;28:3910-3916.
123. Morris PG, Chen C, Steingart RM, Fleisher M, et al. Troponin I and C-reactive protein are commonly detected in patients with breast cancer treated with dose-dense chemotherapy incorporating trastuzumab and lapatinib. Clin Cancer Res. 2011;17:3490-3499.
124. Sawaya H, Sebag IA, Plana JC, et al. Early detection and prediction of cardiotoxicity in chemotherapy-treated patients. Am J Cardiol. 2011;107:1375-1380.
125. Lipshultz SE, Miller TL, Scully RE, et al. Changes in cardiac biomarkers during doxorubicin treatment of pediatric patients With high-risk acute lymphoblastic leukemia: associations with long-term echocardiographic outcomes. J Clin Oncol. 2012;30:1042-1049.
126. Sawaya H, Sebag IA, Plana JC, et al. Assessment of echocardiography and biomarkers for the extended prediction of cardiotoxicity in patients treated with anthracyclines, taxanes, and trastuzumab. Circ Cardiovasc Imaging. 2012;5:596-603.
127. Geiger S, Stemmler HJ, Suhl P, et al. Anthracycline-induced cardiotoxicity: cardiac monitoring by continuous wave-Doppler ultrasound cardiac output monitoring and correlation to echocardiography. Onkologie. 2012;35:241-246.
128. Mornos C, Petrescu L. Early detection of anthracycline-mediated cardiotoxicity: the value of considering both global longitudinal left ventricular strain and twist. Can J Physiol Pharmacol. 2013;91:601-607.
129. Mavinkurve-Groothuis AM, Marcus KA, Pourier M, et al. Myocardial 2D strain echocardiography and cardiac biomarkers in children during and shortly after anthracycline therapy for acute lymphoblastic leukaemia: a prospective study. Eur Heart J Cardiovasc Imaging. 2013;14:562-569.
130. Mornos C, Manolis AJ, Cozma D, Kouremenos N, Zacharopoulou I, Ionac A. The value of left ventricular global longitudinal strain assessed by three-dimensional strain imaging in the early detection of anthracycline-mediated cardiotoxicity. Hellenic J Cardiol. 2014;55:235-244.
131. Ewer MS, Lippman SM. Type II chemotherapy-related cardiac dysfunction: time to recognize a new entity. J Clin Oncol. 2005;23:2900-2902.
132. Cardinale D, Salvatici M, Sandri MT. Role of biomarkers in cardioncology. Clin Chem Lab Med. 2011;49:1937-1948.
133. Christenson ES, James T, Agrawal V, Park BH. Use of biomarkers for the assessment of chemotherapy-induced cardiac toxicity. Clin Biochem. 2015;48(4-5):223-235.
134. Thakur A, Witteles RM. Cancer therapy-induced left ventricular dysfunction: interventions and prognosis. J Card Fail. 2014;20:155-158.
135. Stevens PL, Lenihan DJ. Cardiotoxicity due to chemotherapy: the role of biomarkers [serial online]. Curr Cardiol Rep. 2015;17:603.
136. Carver JR, Shapiro CL, Ng A, et al. American Society of Clinical Oncology clinical evidence review on the ongoing care of adult cancer survivors: cardiac and pulmonary late effects. J Clin Oncol. 2007;25:3991-4008.
137. Cardinale D, Colombo A, Sandri MT, et al. Prevention of high-dose chemotherapy-induced cardiotoxicity in high-risk patients by angiotensin-converting enzyme inhibition. Circulation. 2006;114:2474-2481.
138. Nakamae H, Tsumura K, Terada Y, et al. Notable effects of angiotensin II receptor blocker, valsartan, on acute cardiotoxic changes after standard chemotherapy with cyclophosphamide, doxorubicin, vincristine, and prednisolone. Cancer. 2005;104:2492-2498.
139. Cadeddu C, Piras A, Mantovani G, et al. Protective effects of the angiotensin II receptor blocker telmisartan on epirubicin-induced inflammation, oxidative stress, and early ventricular impairment. Am Heart J. 2010;160:487.e1–487.e7.
140. Akpek M, Ozdogru I, Sahin O, et al. Protective effects of spironolactone against anthracycline-induced cardiomyopathy. Eur J Heart Fail. 2015;17:81-89.
141. Kalay N, Basar E, Ozdogru I, et al. Protective effects of carvedilol against anthracycline-induced cardiomyopathy. J Am Coll Cardiol. 2006;48:2258-2262.
142. Kaya MG, Ozkan M, Gunebakmaz O, et al. Protective effects of nebivolol against anthracycline-induced cardiomyopathy: a randomized control study. Int J Cardiol. 2013;167:2306-2310.
143. Seicean S, Seicean A, Alan N, Plana JC, Budd GT, Marwick TH. Cardioprotective effect of β-adrenoceptor blockade in patients with breast cancer undergoing chemotherapy: follow-up study of heart failure Circ Heart Fail. 2013;6:420-426.
144. Bosch X, Rovira M, Sitges M, et al. Enalapril and carvedilol for preventing chemotherapy-induced left ventricular systolic dysfunction in patients with malignant hemopathies: the OVERCOME trial (preventiOn of left Ventricular dysfunction with Enalapril and caRvedilol in patients submitted to intensive ChemOtherapy for the treatment of Malignant hEmopathies). J Am Coll Cardiol. 2013;61:2355-2362.
145. Acar Z, Kale A, Turgut M, et al. Efficiency of atorvastatin in the protection of anthracycline-induced cardiomyopathy. J Am Coll Cardiol. 2011;58:988-989.
146. Seicean S, Seicean A, Plana JC, Budd GT, Marwick TH. Effect of statin therapy on the risk for incident heart failure in patients with breast cancer receiving anthracycline chemotherapy: an observational clinical cohort study. J Am Coll Cardiol. 2012;60:2384-2390.
147. Lipshultz SE, Rifai N, Dalton VM, et al. The effect of dexrazoxane on myocardial injury in doxorubicin-treated children with acute lymphoblastic leukemia. N Engl J Med. 2004;351:145-153.
148. Lipschultz SE, Scully RE, Lipsitz SR, et al. Assessment of dexrazoxane as a cardioprotectant in doxorubicin-treated children with high-risk acute lymphoblastic leukaemia: long-term follow-up of a prospective, randomized, multicentre trial. Lancet Oncol. 2010;11:950-961.
149. Sieswerda E, van Dalen EC, Postma A, Cheuk DK, Caron HN, Kremer LC. Medical interventions for treating anthracycline-induced symptomatic and asymptomatic cardiotoxicity during and after treatment for childhood cancer [serial online]. Cochrane Database Syst Rev. 2011;9:CD008011.
150. Hensley ML, Hagerty KL, Kewalramani T, et al. American Society of Clinical Oncology 2008 clinical practice guideline update: use of chemotherapy and radiation therapy protectants. J Clin Oncol. 2009;27:127-145.
151. Kalam K, Marwick TH. Role of cardioprotective therapy for prevention of cardiotoxicity with chemotherapy: a systematic review and meta-analysis. Eur J Cancer. 2013;49:2900-2909.
152. Cardinale D, Civelli M, Cipolla CM. Troponins in prediction of cardiotoxic effects [letter]. Ann Oncol 17:173, 2006; author reply 173–174.
153. Riad A, Bien S, Westermann D, et al. Pretreatment with statin attenuates the cardiotoxicity of doxorubicin in mice. Cancer Res. 2009;69:695-699.
154. Pituskin E, Haykowsky M, Mackey JR, et al. Rationale and design of the Multidisciplinary Approach to Novel Therapies in Cardiology Oncology Research Trial (MANTICORE 101-Breast): a randomized, placebo-controlled trial to determine whether conventional heart failure pharmacotherapy can prevent trastuzumab-mediated left ventricular remodeling among patients with HER2+ early breast cancer using cardiac MRI [serial online]. BMC Cancer. 2011;11:318.
155. Heck SL, Gulati G, Ree AH, et al. Rationale and design of the prevention of cardiac dysfunction during an Adjuvant Breast Cancer Therapy (PRADA) Trial. Cardiology. 2012;123:240-247.
156. Saini J, Rich MW, Lyss AP. Reversibility of severe left ventricular dysfunction due to doxorubicin cardiotoxicity. Report of three cases. Ann Intern Med. 1987;106:814-816.
157. Jensen BV, Nielsen SL, Skovsgaard T. Treatment with angiotensin-converting-enzyme inhibitor for epirubicin-induced dilated cardiomyopathy. Lancet. 1996;347:297-299.
158. Fazio S, Calmieri EA, Ferravate B, Bone F, Biondi B, Sacca L. Doxorubicin-induced cardiomyopathy treated with carvedilol. Clin Cardiol. 1998;21:777-779.
159. Noori A, Lindenfeld J, Wolfel E, Ferguson D, Bristow MR, Lowes BD. Beta-blockade in Adriamycin-induced cardiomyopathy. J Card Fail. 2000;6:115-119.
160. Mukai Y, Yoshida T, Nakaike R, et al. Five cases of anthracycline-induced cardiomyopathy effectively treated with carvedilol. Intern Med. 2004;43:1087-1088.
161. Tallaj JA, Franco V, Rayburn BK, et al. Response of doxorubicin-induced cardiomyopathy to the current management strategy of heart failure. J Heart Lung Transplant. 2005;24:2196-2201.
162. Tabet JY, Meurin P, Ben Driss A, et al. Beta-blockade intolerance in anthracycline-induced cardiomyopathy. Int J Cardiol. 2006;106:132-134.
163. OncologyPRO, European Society for Medical Oncology. QT Prolongation-All Kinase Inhibitors. oncologypro.esmo.org/Guidelines-Practice/Drug-Drug-Interactions-with-Kinase-Inhibitors/Types-of-Drug-Drug-Interactions/QT-Prolongation. Accessed November 14, 2015.
164. 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(suppl 7):vii155-vii166.
165. McDonagh TA, Blue L, Clark AL, et al. European Society of Cardiology Heart Failure Association standards for delivering heart failure care. Eur J Heart Fail. 2011;13:235-241.
166. Munoz Martin AJ, Font Puig C, Navarro Martin LM, Borrega Garcia P, Martin Jimenez M; Spanish Society for Medical Oncology. Clinical guide SEOM on venous thromboembolism in cancer patients. Clin Transl Oncol. 2014;16:1079-1090.
167. Khorana AA, Kuderer NM, Culakova E, Lyman GH, Francis CW. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood. 2008;111:4902-4907.
168. Mandala M, Falanga A, Roila F. Management of venous thromboembolism (VTE) in cancer patients: ESMO Clinical Practice Guidelines. Ann Oncol. 2011;22(suppl 6):vi85-vi92.