The emerging issue of cardiac dysfunction induced by antineoplastic angiogenesis inhibitors

European Journal of Heart Failure

Volumn 15, Issue 5, 2013, Pages 482-489

  Tocchetti, Carlo G ^a   Gallucci, Giuseppina ^b   Coppola, Carmela ^a   Piscopo, Giovanna ^a   Cipresso, Clemente ^a   Maurea, Carlo ^a   Giudice, Aldo ^a   Iaffaioli, Rosario V ^a   Arra, Claudio ^a   Maurea, Nicola ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b Arcispedale Santa Maria Nuova   (Italy)

Author keywords

Anti angiogenic drugs; Cardiovascular risk factors; Hypertension; Left ventricular dysfunction; Multitargeted tyrosine kinase inhibitors; VEGF

Indexed keywords

ANGIOGENESIS INHIBITOR; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIHYPERTENSIVE AGENT; BEVACIZUMAB; CALCIUM CHANNEL BLOCKING AGENT; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; NITRATE; PACLITAXEL; PAZOPANIB; PLATELET DERIVED GROWTH FACTOR RECEPTOR; SORAFENIB; SUNITINIB; VANDETANIB; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN INHIBITOR;

ADVANCED CANCER; ANTIANGIOGENIC ACTIVITY; ANTIHYPERTENSIVE THERAPY; ARTICLE; BLOOD PRESSURE MONITORING; BREAST CANCER; CANCER GROWTH; CANCER SURVIVAL; CARDIOTOXICITY; COLORECTAL CARCINOMA; DRUG EFFECT; GASTROINTESTINAL STROMAL TUMOR; GENOTYPE; HEART ARRHYTHMIA; HEART FAILURE; HEART LEFT VENTRICLE FAILURE; HUMAN; HYPERTENSION; KIDNEY CANCER; LIVER CELL CARCINOMA; LUNG CANCER; METASTASIS; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; QT PROLONGATION; THROMBOEMBOLISM; THYROID MEDULLARY CARCINOMA; TORSADE DES POINTES; VASODILATATION;

ANGIOGENESIS INHIBITORS; ANTINEOPLASTIC AGENTS; CARDIOVASCULAR SYSTEM; HUMANS; RISK FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR DYSFUNCTION, LEFT;

EID: 84877153703     PISSN: 13889842     EISSN: 18790844     Source Type: Journal    
DOI: 10.1093/eurjhf/hft008     Document Type: Article

References (60)

1. Eschenhagen T, Force T, Ewer MS, de Keulenaer GW, Suter TM, Anker SD, Avkiran M, de Azambuja E, Balligand JL, Brutsaert DL, Condorelli G, Hansen A, Heymans S, Hill JA, Hirsch E, Hilfiker-Kleiner D, Janssens S, de Jong S, Neubauer G, Pieske B, Ponikowski P, Pirmohamed M, Rauchhaus M, Sawyer D, Sugden PH, Wojta J, Zannad F, Shah AM. Cardiovascular side effects of cancer therapies: a position statement from the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail 2011; 13: 1-10.
2. Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol 2009; 53: 2231-2247.
3. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL. Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 2012; 52: 1213-1225.
4. Tocchetti CG, Ragone G, Coppola C, Rea D, Piscopo G, Scala S, De Lorenzo C, Iaffaioli RV, Arra C, Maurea N. Detection, monitoring and management of trastuzumab-induced left ventricular dysfunction: an actual challenge. Eur J Heart Fail 2012; 14: 130-137.
5. Steingart RM, Bakris GL, Chen HX, Chen MH, Force T, Ivy SP, Leier CV, Liu G, Lenihan D, Lindenfeld J, Maitland ML, Remick SC, Tang WH. Management of cardiac toxicity in patients receiving vascular endothelial growth factor signaling pathway inhibitors. Am Heart J 2012; 163: 156-163.
6. Cheng H, Force T. Molecular mechanisms of cardiovascular toxicity of targeted cancer therapeutics. Circ Res 2010; 106: 21-34.
7. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, Lilenbaum R, Johnson DH. Paclitaxel-carboplatin alone or with bevacizumab for nonsmall-cell lung cancer. N Engl J Med 2006; 355: 2542-2550.
8. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004; 350: 2335-2342.
9. Miller KD, Chap LI, Holmes FA, Cobleigh MA, Marcom PK, Fehrenbacher L, Dickler M, Overmoyer BA, Reimann JD, Sing AP, Langmuir V, Rugo HS. Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. J Clin Oncol 2005; 23: 792-799.
10. Miller K, Wang M, Gralow J, Dickler M, Cobleigh M, Perez EA, Shenkier T, Cella D, Davidson NE. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med 2007; 357: 2666-2676.
11. Choueiri TK, Mayer EL, Je Y, Rosenberg JE, Nguyen PL, Azzi GR, Bellmunt J, Burstein HJ, Schutz FA. Congestive heart failure risk in patients with breast cancer treated with bevacizumab. J Clin Oncol 2011; 29: 632-638.
12. Chintalgattu V, Ai D, Langley RR, Zhang J, Bankson JA, Shih TL, Reddy AK, Coombes KR, Daher IN, Pati S, Patel SS, Pocius JS, Taffet GE, Buja LM, Entman ML, Khakoo AY. Cardiomyocyte PDGFR-beta signaling is an essential component of the mouse cardiac response to load-induced stress. J Clin Invest 2010; 120: 472-484.
13. Chu TF, Rupnick MA, Kerkela R, Dallabrida SM, Zurakowski D, Nguyen L, Woulfe K, Pravda E, Cassiola F, Desai J, George S, Morgan JA, Harris DM, Ismail NS, Chen JH, Schoen FJ, Van den Abbeele AD, Demetri GD, Force T, Chen MH. Cardiotoxicity associated with the tyrosine kinase inhibitor sunitinib. Lancet 2007; 370: 2011-2019.
14. Khakoo AY, Kassiotis CM, Tannir N, Plana JC, Halushka M, Bickford C, Trent J 2nd, Champion JC, Durand JB, Lenihan DJ. Heart failure associated with sunitinib malate: a multitargeted receptor tyrosine kinase inhibitor. Cancer 2008; 112: 2500-2508.
15. Motzer RJ, Hutson TE, Tomczak P, Michaelson MD, Bukowski RM, Rixe O, Oudard S, Negrier S, Szczylik C, Kim ST, Chen I, Bycott PW, Baum CM, Figlin RA. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007; 356: 115-124.
16. Telli ML, Witteles RM, Fisher GA, Srinivas S. Cardiotoxicity associated with the cancer therapeutic agent sunitinib malate. Ann Oncol 2008; 19: 1613-1618.
17. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, Chen C, Zhang X, Vincent P, McHugh M, Cao Y, Shujath J, Gawlak S, Eveleigh D, Rowley B, Liu L, Adnane L, Lynch M, Auclair D, Taylor I, Gedrich R, Voznesensky A, Riedl B, Post LE, Bollag G, Trail PA. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004; 64: 7099-7109.
18. Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Siebels M, Negrier S, Chevreau C, Solska E, Desai AA, Rolland F, Demkow T, Hutson TE, Gore M, Freeman S, Schwartz B, Shan M, Simantov R, Bukowski RM; TARGET Study Group. Sorafenib in advanced clear-cell renal-cell carcinoma. N Engl J Med 2007; 356: 125-134.
19. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Ha?ussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J; SHARP Investigators Study Group. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359: 378-390.
20. 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.
21. Hutson TE, Davis ID, Machiels JP, De Souza PL, Rottey S, Hong BF, Epstein RJ, Baker KL, McCann L, Crofts T, Pandite L, Figlin RA. Efficacy and safety of pazopanib in patients with metastatic renal cell carcinoma. J Clin Oncol 2010; 28: 475-480.
22. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-1186.
23. Loges S, Roncal C, Carmeliet P. Development of targeted angiogenic medicine. J Thromb Haemost 2009; 7: 21-33.
24. Anisimov A, Alitalo A, Korpisalo P, Soronen J, Kaijalainen S, Leppanen VM, Jeltsch M, Yla?-Herttuala S, Alitalo K. Activated forms of VEGF-C and VEGF-D provide improved vascular function in skeletal muscle. Circ Res 2009; 104: 1302-1312.
25. Folkman J. Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 2007; 6: 273-286.
26. Izumiya Y, Shiojima I, Sato K, Sawyer DB, Colucci WS, Walsh K. Vascular endothelial growth factor blockade promotes the transition from compensatory cardiac hypertrophy to failure in response to pressure overload. Hypertension 2006; 47: 887-893.
27. Levy BI. Microvascular plasticity and experimental heart failure. Hypertension 2006; 47: 827-829.
28. Zentilin L, Puligadda U, Lionetti V, Zacchigna S, Collesi C, Pattarini L, Ruozi G, Camporesi S, Sinagra G, Pepe M, Recchia FA, Giacca M. Cardiomyocyte VEGFR-1 activation by VEGF-B induces compensatory hypertrophy and preserves cardiac function after myocardial infarction. FASEB J 2010; 24: 1467-1478.
29. Chiusa M, Hool SL, Truetsch P, Djafarzadeh S, Jakob SM, Seifriz F, Scherer SJ, Suter TM, Zuppinger C, Zbinden S. Cancer therapy modulates VEGF signaling and viability in adult rat cardiac microvascular endothelial cells and cardiomyocytes. J Mol Cell Cardiol 2012; 52: 1164-1175.
30. Bry M, Kivela? R, Holopainen T, Anisimov A, Tammela T, Soronen J, Silvola J, Saraste A, Jeltsch M, Korpisalo P, Carmeliet P, Lemstro?m KB, Shibuya M, Yla-Herttuala S, Alhonen L, Mervaala E, Andersson LC, Knuuti J, Alitalo K. Vascular endothelial growth factor-B acts as a coronary growth factor in transgenic rats without inducing angiogenesis, vascular leak, or inflammation. Circulation 2010; 122: 1725-1733.
31. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, Chorianopoulos E, Liesenborghs L, Koch M, De Mol M, Autiero M, Wyns S, Plaisance S, Moons L, van Rooijen N, Giacca M, Stassen JM, Dewerchin M, Collen D, Carmeliet P. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 2007; 131: 463-475.
32. Force T, Krause DS, Van Etten RA. Molecular mechanisms of cardiotoxicity of tyrosine kinase inhibition. Nat Rev Cancer 2007; 7: 332-344.
33. Rainer PP, Doleschal B, Kirk JA, Sivakumaran V, Saad Z, Groschner K, Maechler H, Hoefler G, Bauernhofer T, Samonigg H, Hutterer G, Kass DA, Pieske B, von Lewinski D, Pichler M. Sunitinib causes dose-dependent negative functional effects on myocardium and cardiomyocytes. BJU Int 2012; 110: 1455-1462.
34. Yamaguchi O, Watanabe T, Nishida K, Kashiwase K, Higuchi Y, Takeda T, Hikoso S, Hirotani S, Asahi M, Taniike M, Nakai A, Tsujimoto I, Matsumura Y, Miyazaki J, Chien KR, Matsuzawa A, Sadamitsu C, Ichijo H, Baccarini M, Hori M, Otsu K. Cardiac-specific disruption of the c-raf-1 gene induces cardiac dysfunction and apoptosis. J Clin Invest 2004; 114: 937-943.
35. Suter TM, Ewer MS. Cancer drugs and the heart: importance and management. Eur Heart J 2012; in press.
36. De Boer RA, Pinto YM, Van Veldhuisen DJ. The imbalance between oxygen demand and supply as a potential mechanism in the pathophysiology of heart failure: the role of microvascular growth and abnormalities. Microcirculation 2003; 10: 113-126.
37. van Veldhuisen DJ, van den Heuvel AF, Blanksma PK, Crijns HJ. Ischemia and left ventricular dysfunction: a reciprocal relation? J Cardiovasc Pharmacol 1998; 32 Suppl 1: S46-S51.
38. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, Ferrara N, Gerber HP, Kikkawa Y, Miner JH, Quaggin SE. Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 2003; 111: 707-716.
39. Maynard S, Epstein FH, Karumanchi SA. Preeclampsia and angiogenic imbalance. Annu Rev Med 2008; 59: 61-78.
40. Gurski MR, Gonzalez E, Brown EG. Immunochemical localization of plateletderived growth factor in placenta and its possible role in pre-eclampsia. J Invest Med 1999; 47: 128-133.
41. Patten IS, Rana S, Shahul S, Rowe GC, Jang C, Liu L, Hacker MR, Rhee JS, Mitchell J, Mahmood F, Hess P, Farrell C, Koulisis N, Khankin EV, Burke SD, Tudorache I, Bauersachs J, del Monte F, Hilfiker-Kleiner D, Karumanchi SA, Arany Z. Cardiac angiogenic imbalance leads to peripartum cardiomyopathy. Nature 2012; 485: 333-338.
42. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 2008; 451: 1008-1012.
43. Chinsomboon J, Ruas J, Gupta RK, Thom R, Shoag J, Rowe GC, Sawada N, Raghuram S, Arany Z. The transcriptional coactivator PGC-1alpha mediates exercise-induced angiogenesis in skeletal muscle. Proc Natl Acad Sci USA 2009; 106: 21401-21406.
44. Maitland ML, Bakris GL, Black HR, Chen HX, Durand JB, Elliott WJ, Ivy SP, Leier CV, Lindenfeld J, Liu G, Remick SC, Steingart R, Tang WH; Cardiovascular Toxicities Panel, Convened by the Angiogenesis Task Force of the National Cancer Institute Investigational Drug Steering Committee. Initial assessment, surveillance, and management of blood pressure in patients receiving vascular endothelial growth factor signaling pathway inhibitors. J Natl Cancer Inst 2010; 102: 596-604.
45. Scartozzi M, Galizia E, Chiorrini S, Giampieri R, Berardi R, Pierantoni C, Cascinu S. Arterial hypertension correlates with clinical outcome in colorectal cancer patients treated with first-line bevacizumab. Ann Oncol 2009; 20: 227-230.
46. Schneider BP, Wang M, Radovich M, Sledge GW, Badve S, Thor A, Flockhart DA, Hancock B, Davidson N, Gralow J, Dickler M, Perez EA, Cobleigh M, Shenkier T, Edgerton S, Miller KD; ECOG 2100. Association of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 genetic polymorphisms with outcome in a trial of paclitaxel compared with paclitaxel plus bevacizumab in advanced breast cancer: ECOG 2100. J Clin Oncol 2008; 26: 4672-4678.
47. 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.
48. Ewer MS, Lenihan DJ. Left ventricular ejection fraction and cardiotoxicity: is our ear really to the ground? J Clin Oncol 2008; 26: 1201-1203.
49. Fallah-Rad N, Walker JR, Wassef A, Lytwyn M, Bohonis S, Fang T, Tian G, Kirkpatrick ID, Singal PK, Krahn M, Grenier D, Jassal DS. 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.
50. Fedele C, Riccio G, Coppola C, Barbieri A, Monti MG, Arra C, Tocchetti CG, D'Alessio G, Maurea N, De Lorenzo C. Comparison of preclinical cardiotoxic effects of different ErbB2 inhibitors. Breast Cancer Res Treat 2012; 133: 511-521.
51. Cardinale D, Colombo A, Torrisi R, Sandri MT, Civelli M, Salvatici M, Lamantia G, Colombo N, Cortinovis S, Dessanai MA, Nole F, Veglia F, Cipolla CM. Trastuzumab-induced cardiotoxicity: clinical and prognostic implications of troponin I evaluation. J Clin Oncol 2010; 28: 3910-3916.
52. Ewer MS, Ewer SM. Troponin I provides insight into cardiotoxicity and the anthracycline- trastuzumab interaction. J Clin Oncol 2010; 28: 3901-3904.
53. Oliveira PJ, Gonçalves L, Monteiro P, Providencia LA, Moreno AJ. Are the antioxidant properties of carvedilol important for the protection of cardiac mitochondria? Curr Vasc Pharmacol 2005; 3: 147-158.
54. van Dalen EC, Caron HN, Dickinson HO, Kremer LC. Cardioprotective interventions for cancer patients receiving anthracyclines. Cochrane Database Syst Rev 2011; 6: CD003917.
55. Jessup M, Abraham WT, Casey DE, Feldman AM, Francis GS, Ganiats TG, Konstam MA, Mancini DM, Rahko PS, Silver MA, Stevenson LW, Yancy CW. 2009 focused update: ACCF/AHA Guidelines for the Diagnosis and Management of Heart Failure in Adults: a report of the American College of Cardiology Foundation/ American Heart Association Task Force on Practice Guidelines: developed in collaboration with the International Society for Heart and Lung Transplantation. Circulation 2009; 119: 1977-2016.
56. Ederhy S, Izzedine H, Massard C, Dufaitre G, Spano JP, Milano G, Meuleman C, Besse B, Boccara F, Kahyat D, Cohen A, Soria JC. Cardiac side effects of molecular targeted therapies: towards a better dialogue between oncologists and cardiologists. Crit Rev Oncol Hematol 2011; 80: 369-379.
57. van den Heuvel AF, Blanksma PK, Siebelink HM, van Wijk LM, Boomsma F, Vaalburg W, Crijns HJ, van Veldhuisen DJ. Impairment of myocardial blood flow reserve in patients with asymptomatic left ventricular dysfunction: effects of ACE-inhibition with perindopril. Int J Cardiovasc Imaging 2001; 17: 353-359.
58. Zannad F, McMurray JJ, Krum H, van Veldhuisen DJ, Swedberg K, Shi H, Vincent J, Pocock SJ, Pitt B; EMPHASIS-HF Study Group. Eplerenone in patients with systolic heart failure and mild symptoms. N Engl J Med 2011; 364: 11-21.
59. Authors/Task Force Members, McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Bo?hm M, Dickstein K, Falk V, Filippatos G, Fonseca C, Gomez-Sanchez MA, Jaarsma T, Køber L, Lip GY, Maggioni AP, Parkhomenko A, Pieske BM, Popescu BA, Rønnevik PK, Rutten FH, Schwitter J, Seferovic P, Stepinska J, Trindade PT, Voors AA, Zannad F, Zeiher A; ESC Committee for Practice Guidelines (CPG), Bax JJ, Baumgartner H, Ceconi C, Dean V, Deaton C, Fagard R, Funck-Brentano C, Hasdai D, Hoes A, Kirchhof P, Knuuti J, Kolh P, McDonagh T, Moulin C, Popescu BA, Reiner Z, Sechtem U, Sirnes PA, Tendera M, Torbicki A, Vahanian A, Windecker S; Document Reviewers, McDonagh T, Sechtem U, Bonet LA, Avraamides P, Ben Lamin HA, Brignole M, Coca A, Cowburn P, Dargie H, Elliott P, Flachskampf FA, Guida GF, Hardman S, Iung B, Merkely B, Mueller C, Nanas JN, Nielsen OW, Orn S, Parissis JT, Ponikowski P. ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: the Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur J Heart Fail 2012; 14: 803-869.
60. Tocchetti CG, Coppola C, Rea D, Piscopo G, Riccio G, Barbieri A, Giudice A, De Lorenzo C, Arra C, Maurea N. Ranolazine blunts anthracyclines- cardiotoxicity in experimental models in vitro and in vivo. Eur J Heart Fail Suppl 2012; 11 (suppl 1): S190-S191.