Journal of Nuclear Cardiology

, Volume 24, Issue 3, pp 906–935 | Cite as

Comprehensive review on cardio-oncology: Role of multimodality imaging

  • Carol Chen-Scarabelli
  • Chad McRee
  • Massoud A. Leesar
  • Fadi G. Hage
  • Tiziano M. Scarabelli
Review Article


Cancer and cardiovascular disease are the two leading causes of mortality worldwide. Evolving oncologic therapy, including the use of newer targeted agents, has led to an improvement in survival from childhood- and adult-onset cancers. Consequently, there has been a growing realization of cardiotoxic complications related to cancer therapy, with some complications manifesting over months to decades after completion of cancer treatment. This paper reviews cancer therapeutics-related cardiovascular toxicity and its manifestations, multimodality imaging techniques for surveillance and detection of this complication, and the current state of knowledge in this emerging field.


Cancer cardiotoxicity chemotherapy imaging radiation 



2D echocardiography


3D echocardiography


American Society of Echocardiography


Angiotensin receptor blocker


Angiotensin-converting enzyme inhibitor


Cancer therapeutics–related cardiac dysfunction


Cardiac computed tomography


Cardiac magnetic resonance imaging




Coronary artery disease


Ejection fraction


Epidermal growth factor receptor type 2


European Association of Cardiovascular Imaging


Fibroblast growth factor receptors


Functional magnetic resonance imaging


Global longitudinal strain


Glomerular Filtration Rate


Heart failure


Hepatocyte growth factor receptors

HER2 or erbb2

Human epidermal growth factor receptor 2


Insulin growth factor receptors


Insulin-like growth factor receptors


Intima-media thickness


Left ventricular/left ventricle


Multi-gated acquisition with blood pool imaging


Myocardial infarction


Platelet-derived growth factor receptors


Positron emission tomography


Single photon emission computed tomography


Society for Cardiovascular Angiography and Interventions


Speckle-tracking echocardiography


Tissue Doppler imaging


Transient ischemic attack


Vascular endothelial growth factor



All the listed authors reported no relationships relevant to the contents of this paper to disclose.

Supplementary material

12350_2016_535_MOESM1_ESM.pptx (578 kb)
Supplementary material 1 (PPTX 578 kb)


  1. 1.
    Eschenhagen T, Force T, Ewer MS, de Keulenaer GW, Suter TM, Anker SD, Avkiran M, de Azambuja E, Balligand JL, Brutsaert DL, et al. 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.PubMedCrossRefGoogle Scholar
  2. 2.
    Billingham M, Bristow MR. Evaluation of anthracycline cardiotoxicity: predictive ability and functional correlation of endomyocardial biopsy. Cancer Treat Symptoms. 1984;3:71–6.Google Scholar
  3. 3.
    Billingham ME, Mason JW, Bristol MR, et al. Anthracycline cardiomyopathy monitored by morphologic changes. Cancer Treat Rep. 1978;62:865–72.PubMedGoogle Scholar
  4. 4.
    Kendal WS. Dying with cancer: the influence of age, comorbidity, and cancer site. Cancer. 2008;112:1354–62.PubMedCrossRefGoogle Scholar
  5. 5.
    Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, Das SR, de Ferranti S, Després JP, Fullerton HJ, Howard VJ, Huffman MD, Isasi CR, Jiménez MC, Judd SE, Kissela BM, Lichtman JH, Lisabeth LD, Liu S, Mackey RH, Magid DJ, McGuire DK, Mohler ER 3rd, Moy CS, Muntner P, Mussolino ME, Nasir K, Neumar RW, Nichol G, Palaniappan L, Pandey DK, Reeves MJ, Rodriguez CJ, Rosamond W, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Woo D, Yeh RW, Turner MB, American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2016 Update: A Report From the American Heart Association. Circulation. 2016;133(4):e38–360. doi: 10.1161/CIR.0000000000000350.PubMedCrossRefGoogle Scholar
  6. 6.
  7. 7.
    American Cancer Society Leading Sites of New Cancer Cases and Deaths—2015 Estimates.
  8. 8.
    Ainger LE, Bushore J, Johnson WW, Ito J. Daunomycin: a cardiotoxic agent. J Natl Med Assoc. 1971;63(4):261–7.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Lefrak EA, Pitha J, Rosenheim S, Gottlieb JA. A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer. 1973;32(2):302–14.PubMedCrossRefGoogle Scholar
  10. 10.
    Armstrong GT, Kawashima T, Leisenring W, Stratton K, Stovall M, Hudson MM, Sklar CA, Robison LL, Oeffinger KC. Aging and risk of severe, disabling, life-threatening, and fatal events in the childhood cancer survivor study. J Clin Oncol. 2014;32(12):1218–27. doi: 10.1200/JCO.2013.51.1055.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Schmitz KH, Prosnitz RG, Schwartz AL, Carver JR. Prospective surveillance and management of cardiac toxicity and health in breast cancer survivors. Cancer. 2012;118(8 Suppl):2270–6. doi: 10.1002/cncr.27462.PubMedCrossRefGoogle Scholar
  12. 12.
    Carver JR, Shapiro CL, Ng A, Jacobs L, Schwartz C, Virgo KS, Hagerty KL, Somerfield MR, Vaughn DJ. DJ; ASCO Cancer Survivorship Expert Panel. 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(25):3991–4008.PubMedCrossRefGoogle Scholar
  13. 13.
    Sulpher J, Mathur S, Lenihan D, Johnson C, Turek M, Law A, Stadnick E, Dattilo F, Graham N, Dent SF. An international survey of health care providers involved in the management of cancer patients exposed to cardiotoxic therapy. J Oncol. 2015;2015:391848. doi: 10.1155/2015/391848.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Daher IN, Daigle TR, Bhatia N, Durand JB. The prevention of cardiovascular disease in cancer survivors. Tex Heart Inst J. 2012;39(2):190–8.PubMedPubMedCentralGoogle Scholar
  15. 15.
    National Comprehensive Cancer Network (NCCN), Accessed 20 Feb 2016.
  16. 16.
    National Cancer Institute (NCI), Accessed 20 Feb 2016.
  17. 17.
    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, Magalhães 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. J Am Soc Echocardiogr. 2014;27(9):911–39. doi: 10.1016/j.echo.2014.07.012.PubMedCrossRefGoogle Scholar
  18. 18.
    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(5):1215–21.PubMedCrossRefGoogle Scholar
  19. 19.
    Tan-Chiu E, Yothers G, Romond E, Geyer CE Jr, Ewer M, Keefe D, Shannon RP, Swain SM, Brown A, Fehrenbacher L, Vogel VG, Seay TE, Rastogi P, Mamounas EP, Wolmark N, Bryant J. Assessment of cardiac dysfunction in a randomized trial comparing doxorubicin and cyclophosphamide followed by paclitaxel, with or without trastuzumab as adjuvant therapy in node-positive, human epidermal growth factor receptor 2-overexpressing breast cancer: NSABP B-31. J Clin Oncol. 2005;23(31):7811–9.PubMedCrossRefGoogle Scholar
  20. 20.
    Mitani I, Jain D, Joska TM, Burtness B, Zaret BL. Doxorubicin cardiotoxicity: prevention of congestive heart failure with serial cardiac function monitoring with equilibrium radionuclide angiocardiography in the cur- rent era. J Nucl Cardiol. 2003;10:132–9.PubMedCrossRefGoogle Scholar
  21. 21.
    Nousiainen T, Jantunen E, Vanninen E, Hartikainen J. Early decline in left ventricular ejection fraction predicts doxorubicin cardiotoxicity in lymphoma patients. Br J Cancer. 2002;86:1697–700.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Schuchter LM, Hensley ML, Meropol NJ, Winer EP, American Society of Clinical Oncology Chemotherapy and Radiotherapy Expert Panel. 2002 update of recommendations for the use of chemotherapy and radiotherapy protectants: clinical practice guidelines of the American Society of Clinical Oncology. J Clin Oncol. 2002;20:2895–903.PubMedCrossRefGoogle Scholar
  23. 23.
    Ewer MS, Lippman SM. Type II chemotherapy-related cardiac dysfunction: time to recognize a new entity. J Clin Oncol. 2005;23(13):2900–2.PubMedCrossRefGoogle Scholar
  24. 24.
    Ewer MS, Vooletich MT, Durand JB, Woods ML, Davis JR, Valero V, Lenihan DJ. Reversibility of trastuzumab-related cardiotoxicity: new insights based on clinical course and response to medical treatment. J Clin Oncol. 2005;23(31):7820–6.PubMedCrossRefGoogle Scholar
  25. 25.
    Yeh ET, Tong AT, Lenihan DJ, Yusuf SW, Swafford J, Champion C, Durand JB, Gibbs H, Zafarmand AA, Ewer MS. Cardiovascular complications of cancer therapy: diagnosis, pathogenesis, and management. Circulation. 2004;109(25):3122–31.PubMedCrossRefGoogle Scholar
  26. 26.
    Schmitz KH, Prosnitz RG, Schwartz AL, Carver JR. Prospective surveillance and management of cardiac toxicity and health in breast cancer survivors. Cancer. 2012;118(8 Suppl):2270–6. doi: 10.1002/cncr.27462.PubMedCrossRefGoogle Scholar
  27. 27.
    Bovelli D, Plataniotis G, Roila F, ESMO Guidelines Working Group. Cardiotoxicity of chemotherapeutic agents and radiotherapy-related heart disease: ESMO Clinical Practice Guidelines. Ann Oncol. 2010;21(Suppl 5):v277–82. doi: 10.1093/annonc/mdq200.PubMedCrossRefGoogle Scholar
  28. 28.
    Swain SM, Whaley FS, Ewer MS. Congestive heart failure in patients treated with doxorubicin: a retrospective analysis of three trials. Cancer. 2003;97:2869–79.PubMedCrossRefGoogle Scholar
  29. 29.
    van Dalen EC, van der Pal HJ, Caron HN, Kremer LC. Different dosage schedules for reducing cardiotoxicity in cancer patients receiving anthracycline chemotherapy. Cochrane Database Syst Rev. 2009;4:CD005008. doi: 10.1002/14651858.CD005008.pub3.Google Scholar
  30. 30.
    Rosa GM, Gigli L, Tagliasacchi MI, Di Iorio C, Carbone F, Nencioni A, Montecucco F, Brunelli C. Update on cardiotoxicity of anti-cancer treatments. Eur J Clin Invest. 2016;46(3):264–84. doi: 10.1111/eci.12589.PubMedCrossRefGoogle Scholar
  31. 31.
    Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009;53(24):2231–47. doi: 10.1016/j.jacc.2009.02.050.PubMedCrossRefGoogle Scholar
  32. 32.
    Regad T, Targeting RTK. Signaling pathways in cancer. Cancers. 2015;7(3):1758–84. doi: 10.3390/cancers7030860.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    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 tyrosine kinase inhibitor sunitinib. Lancet. 2007;370(9604):2011–9.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    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(12):2162–70. doi: 10.1016/j.ejca.2014.05.013.PubMedCrossRefGoogle Scholar
  35. 35.
    Richardson PG, Mitsiades C, Hideshima T, Anderson KC. Proteasome inhibition in the treatment of cancer. Cell Cycle. 2005;4(2):290–6.PubMedCrossRefGoogle Scholar
  36. 36.
    Enrico O, Gabriele B, Nadia C, Sara G, Daniele V, Giulia C, Antonio S, Mario P. Unexpected cardiotoxicity in haematological bortezomib treated patients. Br J Haematol. 2007;138(3):396–7.PubMedCrossRefGoogle Scholar
  37. 37.
    Nowis D, Maczewski M, Mackiewicz U, Kujawa M, Ratajska A, Wieckowski MR, Wilczyński GM, Malinowska M, Bil J, Salwa P, Bugajski M, Wójcik C, Siński M, Abramczyk P, Winiarska M, Dabrowska-Iwanicka A, Duszyński J, Jakóbisiak M, Golab J. Cardiotoxicity of the anticancer therapeutic agent bortezomib. Am J Pathol. 2010;176(6):2658–68. doi: 10.2353/ajpath.2010.090690 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Bockorny M, Chakravarty S, Schulman P, Bockorny B, Bona R. Severe heart failure after bortezomib treatment in a patient with multiple myeloma: a case report and review of the literature. Acta Haematol. 2012;128(4):244–7. doi: 10.1159/000340050.PubMedCrossRefGoogle Scholar
  39. 39.
    Hacihanefioglu A, Tarkun P, Gonullu E. Acute severe cardiac failure in a myeloma patient due to proteasome inhibitor bortezomib. Int J Hematol. 2008;88(2):219–22. doi: 10.1007/s12185-008-0139-7.PubMedCrossRefGoogle Scholar
  40. 40.
    Subedi A, Sharma LR, Shah BK. Bortezomib-induced acute congestive heart failure: a case report and review of literature. Ann Hematol. 2014;93(10):1797–9. doi: 10.1007/s00277-014-2026-z.PubMedCrossRefGoogle Scholar
  41. 41.
    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(1):e87671. doi: 10.1371/journal.pone.0087671. eCollection 2014.
  42. 42.
    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(2):138–44. doi: 10.1016/j.cardfail.2014.11.008.PubMedCrossRefGoogle Scholar
  43. 43.
    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. 2015. doi: 10.1111/ejh.12677.PubMedGoogle Scholar
  44. 44.
    Scarabelli TM, Chen-Scarabelli C, Gavazzoni M, Sahni G, Saravolatz L, Raddino R, Narula J (2015) Cardiovascular effects of carfilzomib, a new proteasome inhibitor, on coronary resistances, vascular tone and vascular reactivity. J Am Coll Cardiol 65 (10); Supplement pp. A2143Google Scholar
  45. 45.
    Scarabelli T, Gavazzoni M, Chen-Scarabelli C, Sahni G, Saravolatz L, Narula J, Raddino R. Cardiovascular Toxicity of Carfilzomib on Vascular Tone. Vascular Reactivity and Endothelial Function. Circulation. 2014;130:A12193.Google Scholar
  46. 46.
    Lancellotti P, Nkomo VT, Badano LP, Bergler-Klein J, Bogaert J, Davin L, Cosyns B, Coucke P, Dulgheru R, Edvardsen T, Gaemperli O, Galderisi M, Griffin B, Heidenreich PA, Nieman K, Plana JC, Port SC, Scherrer-Crosbie M, Schwartz RG, Sebag IA, Voigt JU, Wann S, Yang PC, European Society of Cardiology Working Groups on Nuclear Cardiology and Cardiac Computed Tomography and Cardiovascular Magnetic Resonance, American Society of Nuclear Cardiology, Society for Cardiovascular Magnetic Resonance, and Society of Cardiovascular Computed Tomography. Expert consensus for multi-modality imaging evaluation of cardiovascular complications of radiotherapy in adults: a report from the European Association of Cardiovascular Imaging and the American Society of Echocardiography. J Am Soc Echocardiogr. 2013;26(9):1013–32. doi: 10.1016/j.echo.2013.07.005.PubMedCrossRefGoogle Scholar
  47. 47.
    Iliescu CA, Grines CL, Herrmann J, Yang EH, Cilingiroglu M, Charitakis K, Hakeem A, Toutouzas KP, Leesar MA, Marmagkiolis K. SCAI Expert consensus statement: Evaluation, management, and special considerations of cardio-oncology patients in the cardiac catheterization laboratory (endorsed by the cardiological society of india, and sociedad Latino Americana de Cardiologıa intervencionista). Catheter Cardiovasc Interv. 2016;. doi: 10.1002/ccd.26379.Google Scholar
  48. 48.
    Cheitlin MD, Armstrong WF, Aurigemma GP, Beller GA, Bierman FZ, Davis JL, et al. ACC/AHA/ASE 2003 Guideline Update for the Clinical Application of Echocardiography: summary article. A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (ACC/AHA/ASE Committee to Update the 1997 Guidelines for the Clinical Application of Echocardiography). J Am Soc Echocardiogr. 2003;16:1091–110.PubMedGoogle Scholar
  49. 49.
    American College of Cardiology Foundation Appropriate Use Criteria Task Force, American Society of Echocardiography, American Heart Association, American Society of Nuclear Cardiology, Heart Failure Society of America, Heart Rhythm Society, et al. (2011) ACCF/ASE/AHA/ASNC/HFSA/HRS/SCAI/SCCM/SCCT/SCMR 2011 Appropriate Use Criteria for Echocardiography. A Report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, American Society of Echocardiography, American Heart Association, American Society of Nuclear Cardiology, Heart Failure Society of America, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, Society of Critical Care Medicine, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance American College of Chest Physicians. J Am Soc Echocardiogr 24:229–67Google Scholar
  50. 50.
    Steingart RM, Bakris GL, Chen HX, Chen MH, Force T, Ivy SP, et al. Management of cardiac toxicity in patients receiving vascular endothelial growth factor signaling pathway inhibitors. Am Heart J. 2012;163:156–63.PubMedCrossRefGoogle Scholar
  51. 51.
    D’Amore C, Gargiulo P, Paolillo S, Pellegrino AM, Formisano T, Mariniello A, Della Ratta G, Iardino E, D’Amato M, La Mura L, Fabiani I, Fusco F, Perrone Filardi P. Nuclear imaging in detection and monitoring of cardiotoxicity. World J Radiol. 2014;6(7):486–92. doi: 10.4329/wjr.v6.i7.486.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28(1):1-39.e14. doi: 10.1016/j.echo.2014.10.003.PubMedCrossRefGoogle Scholar
  53. 53.
    Onishi T, Saha SK, Delgado-Montero A, Ludwig DR, Onishi T, Schelbert EB, Schwartzman D, Gorcsan J 3rd. Global longitudinal strain and global circumferential strain by speckle-tracking echocardiography and feature-tracking cardiac magnetic resonance imaging: comparison with left ventricular ejection fraction. J Am Soc Echocardiogr. 2015;28(5):587–96. doi: 10.1016/j.echo.2014.11.018.PubMedCrossRefGoogle Scholar
  54. 54.
    Toro-Salazar OH, Ferranti J, Lorenzoni R, Walling S, Mazur W, Raman SV, Davey BT, Gillan E, O’Loughlin M, Klas B, Hor KN. Feasibility of echocardiographic techniques to detect subclinical cancer therapeutics-related cardiac dysfunction among high-dose patients when compared with cardiac magnetic resonance imaging. J Am Soc Echocardiogr. 2016;29(2):119–31. doi: 10.1016/j.echo.2015.10.008.PubMedCrossRefGoogle Scholar
  55. 55.
    Thavendiranathan P, Grant AD, Negishi T, Plana JC, Popovic 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.PubMedCrossRefGoogle Scholar
  56. 56.
    Kongbundansuk S, Hundley WG. Noninvasive imaging of cardiovascular injury related to the treatment of cancer. JACC Cardiovasc Imaging. 2014;7(8):824–38. doi: 10.1016/j.jcmg.2014.06.007.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Mor-Avi V, Lang RM, Badano LP, Belohlavek M, Cardim NM, Derumeaux G, Galderisi M, Marwick T, Nagueh SF, Sengupta PP, Sicari R, Smiseth OA, Smulevitz B, Takeuchi M, Thomas JD, Vannan M, Voigt JU, Zamorano JL. Current and evolving echocardiographic techniques for the quantitative evaluation of cardiac mechanics: ASE/EAE consensus statement on methodology and indications endorsed by the Japanese Society of Echocardiography. J Am Soc Echocardiogr. 2011;24(3):277–313. doi: 10.1016/j.echo.2011.01.015.PubMedCrossRefGoogle Scholar
  58. 58.
    Thavendiranathan P, Poulin F, Lim KD, 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):2751–68. doi: 10.1016/j.jacc.2014.01.073.PubMedCrossRefGoogle Scholar
  59. 59.
    Brown PD, Foote RL, McLaughlin MP, Halyard MY, Ballman KV, Collie AC, Miller RC, Flemming KD, Hallett JW. A historical prospective cohort study of carotid artery stenosis after radiotherapy for head and neck malignancies. Int J Radiat Oncol Biol Phys. 2005;63(5):1361–7.PubMedCrossRefGoogle Scholar
  60. 60.
    Plummer C, Henderson RD, O’Sullivan JD, Read SJ. Ischemic stroke and transient ischemic attack after head and neck radiotherapy: a review. Stroke. 2011;42(9):2410–8. doi: 10.1161/STROKEAHA.111.615203.PubMedCrossRefGoogle Scholar
  61. 61.
    Walker J, Bhullar N, Fallah-Rad N, et al. Role of three-dimensional echocardiography in breast cancer: comparison with two-dimensional echocardiography, multiple-gated acquisition scans, and cardiac magnetic resonance imaging. J Clin Oncol. 2010;28:3429–36.PubMedCrossRefGoogle Scholar
  62. 62.
    Pizzino F, Vizzari G, Qamar R, Bomzer C, Carerj S, Zito C, Khandheria BK. Multimodality imaging in cardiooncology. J Oncol. 2015;2015:263950. doi: 10.1155/2015/263950.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    American College of Cardiology Foundation Task Force on Expert Consensus Documents, Hundley WG, Bluemke DA, Finn JP, Flamm SD, Fogel MA, Friedrich MG, Ho VB, Jerosch-Herold M, Kramer CM, Manning WJ, Patel M, Pohost GM, Stillman AE, White RD, Woodard PK. ACCF/ACR/AHA/NASCI/SCMR 2010 expert consensus document on cardiovascular magnetic resonance: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol. 2010;55(23):2614–62. doi: 10.1016/j.jacc.2009.11.011.CrossRefGoogle Scholar
  64. 64.
    Hendel RC, Patel MR, Kramer CM, Poon M, Hendel RC, Carr JC, Gerstad NA, Gillam LD, Hodgson JM, Kim RJ, et al. ACCF/ACR/SCCT/SCMR/ASNC/NASCI/SCAI/SIR 2006 appropriateness criteria for cardiac computed tomography and cardiac magnetic resonance imaging: a report of the American College of Cardiology Foundation Quality Strategic Directions Committee Appropriateness Criteria Working Group, American College of Radiology, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, American Society of Nuclear Cardiology, North American Society for Cardiac Imaging, Society for Cardiovascular Angiography and Interventions, and Society of Interventional Radiology. J Am Coll Cardiol. 2006;48:1475–97.PubMedCrossRefGoogle Scholar
  65. 65.
    Fallah-Rad N, Lytwyn M, Fang T, Kirkpatrick I, Jassal DS. Delayed contrast enhancement cardiac magnetic resonance imaging in trastuzumab induced cardiomyopathy. J Cardiovasc Magn Reson. 2008;10:5.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Neilan TG, Coelho-Filho OR, Pena-Herrera D, Shah RV, Jerosch-Herold M, Francis SA, et al. Left ventricular mass in patients with a cardiomyopathy after treatment with anthracyclines. Am J Cardiol. 2012;110(11):1679–86.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    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(22):2263–70. doi: 10.1016/j.jacc.2010.11.063.PubMedCrossRefGoogle Scholar
  68. 68.
    Wagner A, Mahrholdt H, Holly TA, Elliott MD, Regenfus M, Parker M, Klocke FJ, Bonow RO, Kim RJ, Judd RM. Contrast-enhanced MRI and routine single photon emission computed tomography (SPECT) perfusion imaging for detection of subendocardial myocardial infarcts: an imaging study. Lancet. 2003;361(9355):374–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Klein AL, Abbara S, Agler DA, Appleton CP, Asher CR, Hoit B, et al. American society of echocardiography clinical recommendations for multimodality cardiovascular imaging of patients with pericardial disease: endorsed by the society for cardiovascular magnetic resonance and society of cardiovascular computed tomography. J Am Soc Echocardiogr. 2013;26(965–1012):e15.Google Scholar
  70. 70.
    Walker CM, Saldana DA, Gladish GW, Dicks DL, Kicska G, Mitsumori LM, et al. Cardiac complications of oncologic therapy. Radiographics. 2013;33(6):1801–15.PubMedCrossRefGoogle Scholar
  71. 71.
    Hassan W, Al-Sergani H, Mourad W, Tabbaa R. Amyloid heart disease. New frontiers and insights in pathophysiology, diagnosis, and management. Tex Heart Inst J. 2005;32(2):178–84.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Müller AM, Geibel A, Neumann HP, Kühnemund A, Schmitt-Gräff A, Böhm J, Engelhardt M. Primary (AL) amyloidosis in plasma cell disorders. Oncologist. 2006;11(7):824–30.PubMedCrossRefGoogle Scholar
  73. 73.
    Mohty D, Damy T, Cosnay P, Echahidi N, Casset-Senon D, Virot P, Jaccard A. Cardiac amyloidosis: updates in diagnosis and management. Arch Cardiovasc Dis. 2013;106(10):528–40. doi: 10.1016/j.acvd.2013.06.051.PubMedCrossRefGoogle Scholar
  74. 74.
    Syed IS, Glockner JF, Feng D, Araoz PA, Martinez MW, Edwards WD, Gertz MA, Dispenzieri A, Oh JK, Bellavia D, Tajik AJ, Grogan M. Role of cardiac magnetic resonance imaging in the detection of cardiac amyloidosis. JACC Cardiovasc Imaging. 2010;3(2):155–64. doi: 10.1016/j.jcmg.2009.09.023.PubMedCrossRefGoogle Scholar
  75. 75.
    Cowper SE, Robin HS, Steinberg SM, Su LD, Gupta S, LeBoit PE. Scleromyxoedema-like cutaneous diseases in renal-dialysis patients. Lancet. 2000;356(9234):1000–1.PubMedCrossRefGoogle Scholar
  76. 76.
    Thomsen HS (2014) Nephrogenic systemic fibrosis and gadolinium-based contrast media. In: Thomsen HS, Webb JAW (eds), Contrast media: safety issues and ESUR guidelines, pp 207–217. Springer, Berlin. doi: 10.1007/978-3-642-36724-3.
  77. 77.
    Khawaja AZ, Cassidy DB, Al Shakarchi J, McGrogan DG, Inston NG, Jones RG. Revisiting the risks of MRI with Gadolinium based contrast agents-review of literature and guidelines. Insights Imaging. 2015;6(5):553–8. doi: 10.1007/s13244-015-0420-2.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Jung W, Zvereva V, Hajredini B, Jäckle S. Safe magnetic resonance image scanning of the pacemaker patient: current technologies and future directions. Europace. 2012;14(5):631–7. doi: 10.1093/europace/eur391.PubMedCrossRefGoogle Scholar
  79. 79.
    Cohen JD, Costa HS, Russo RJ. Determining the risks of magnetic resonance imaging at 1.5 tesla for patients with pacemakers and implantable cardioverter defibrillators. Am J Cardiol. 2012;110(11):1631–6. doi: 10.1016/j.amjcard.2012.07.030.PubMedCrossRefGoogle Scholar
  80. 80.
    Russo RJ, Costa HS, Kabra AN, Uretsky S, Wolff SD, et al. (2013) Is a Change in cardiac device lead impedance after magnetic resonance imaging at 1.5 tesla associated with other parameter changes?: Preliminary results from the MagnaSafe registry. Abstract presented at Heart Rhythm Society 34th Annual Scientific Sessions 2013, Denver, CO.Google Scholar
  81. 81.
    Russo RJ, Costa HS, Birgersdotter-Green U, Bloomgarden DC, Florin T, Machado C, Martin ET, Porter M, Tominaga GT, Uretsky S, Wolff SD (2011) Determining the Risks of Magnetic Resonance Imaging at 1.5 Tesla for Patients with Pacemakers and Implantable Cardioverter Defibrillators (The MagnaSafe Registry) Circulation. 124:A10674. Abstract presented at the AHA Annual Scientific Sessions November 2013 Dallas, TX.Google Scholar
  82. 82.
    Kaasalainen T, Pakarinen S, Kivistö S, Holmström M, Hänninen H, Peltonen J, Lauerma K, Sipilä O. MRI with cardiac pacing devices - safety in clinical practice. Eur J Radiol. 2014;83(8):1387–95. doi: 10.1016/j.ejrad.2014.04.022.PubMedCrossRefGoogle Scholar
  83. 83.
    Wollmann CG, Thudt K, Kaiser B, Salomonowitz E, Mayr H, Globits S. Safe performance of magnetic resonance of the heart in patients with magnetic resonance conditional pacemaker systems: the safety issue of the ESTIMATE study. J Cardiovasc Magn Reson. 2014;16:30. doi: 10.1186/1532-429X-16-30.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Gold MR, Sommer T, Schwitter J, Fagih A, Albert T, Merkely B, Peterson M, Ciuffo A, Lee S, Landborg L, Cerkvenik J, Kanal E, Evera MRI, Study Investigators. Full-body MRI in patients with an implantable cardioverter-defibrillator: primary results of a randomized study. J Am Coll Cardiol. 2015;65(24):2581–8. doi: 10.1016/j.jacc.2015.04.047.PubMedCrossRefGoogle Scholar
  85. 85.
    Hesse B, Lindhardt TB, Acampa W, Anagnostopoulos C, Ballinger J, Bax JJ, Edenbrandt L, Flotats A, Germano G, Stopar TG, et al. EANM/ESC guidelines for radionuclide imaging of cardiac function. Eur J Nucl Med Mol Imaging. 2008;35:851–85.PubMedCrossRefGoogle Scholar
  86. 86.
    Schwartz RG, McKenzie WB, Alexander J, Sager P, D’Souza A, Manatunga A, et al. Congestive heart failure and left ventricular dysfunction complicating doxorubicin therapy. Seven-year experience using serial radionuclide angiocardiography. Am J Med. 1987;82:1109–18.PubMedCrossRefGoogle Scholar
  87. 87.
    Naik MM, Diamond GA, Pai T, Soffer A, Siegel RJ. Correspondence of left ventricular ejection fraction determinations from two-dimensional echocardiography, radionuclide angiography and contrast cineangiography. J Am Coll Cardiol. 1995;25:937–42.PubMedCrossRefGoogle Scholar
  88. 88.
    Bellenger NG, Burgess MI, Ray SG, Lahiri A, Coats AJ, Cleland JG, et al. Comparison of left ventricular ejection fraction and volumes in heart failure by echocardiography, radionuclide ventriculography and cardiovascular magnetic resonance; are they interchangeable? Eur Heart J. 2000;21:1387–96.PubMedCrossRefGoogle Scholar
  89. 89.
    Mogelvang J, Stokholm KH, Saunamaki K, Reimer A, Stubgaard M, Thomsen C, et al. Assessment of left ventricular volumes by magnetic resonance in comparison with radionuclide angiography, contrast angiography and echocardiography. Eur Heart J. 1992;13:1677–83.PubMedCrossRefGoogle Scholar
  90. 90.
    van Royen N, Jaffe CC, Krumholz HM, Johnson KM, Lynch PJ, Natale D, Atkinson P, Deman P, Wackers FJ. Comparison and reproducibility of visual echocardiographic and quantitative radionuclide left ventricular ejection fractions. Am J Cardiol. 1996;77(10):843–50.PubMedCrossRefGoogle Scholar
  91. 91.
    Cubbona RM, Lyons AR. Cardio-oncology: concepts and practice. Indian Heart J. 2016. doi: 10.1016/j.ihj.2016.01.022.Google Scholar
  92. 92.
    Swain SM, Whaley FS. Ewer MS Congestive heart failure in patients treated with doxorubicin: a retrospective analysis of three trials. Cancer. 2003;97(11):2869–79.PubMedCrossRefGoogle Scholar
  93. 93.
    Groch MW, DePuey EG, Belzberg AC, Erwin WD, Kamran M, Barnett CA, Hendel RC, Spies SM, Ali A, Marshall RC. Planar imaging versus gated blood-pool SPECT for the assessment of ventricular performance: a multicenter study. J Nucl Med. 2001;42(12):1773–9.PubMedGoogle Scholar
  94. 94.
    Hacker M, Hoyer X, Kupzyk S, La Fougere C, Kois J, Stempfle HU, Tiling R, Hahn K, Störk S. Clinical validation of the gated blood pool SPECT QBS processing software in congestive heart failure patients: correlation with MUGA, first-pass RNV and 2D-echocardiography. Int J Cardiovasc Imaging. 2006;22(3–4):407–16.PubMedCrossRefGoogle Scholar
  95. 95.
    Joergensen T, Hansson SH. Evaluation of the Left ventricular ejection fraction with gated IQ-SPECT myocardial perfusion imaging. J Nucl Med Technol. 2015;43(3):193–200. doi: 10.2967/jnmt.115.155382.PubMedCrossRefGoogle Scholar
  96. 96.
    Schaefer WM, Lipke CS, Standke D, Kühl HP, Nowak B, Kaiser HJ, Koch KC, Buell U. Quantification of left ventricular volumes and ejection fraction from gated 99mTc-MIBI SPECT: MRI validation and comparison of the Emory Cardiac Tool Box with QGS and 4D-MSPECT. J Nucl Med. 2005;46(8):1256–63.PubMedGoogle Scholar
  97. 97.
    Lipke CS, Kühl HP, Nowak B, Kaiser HJ, Reinartz P, Koch KC, Buell U, Schaefer WM. Validation of 4D-MSPECT and QGS for quantification of left ventricular volumes and ejection fraction from gated 99mTc-MIBI SPET: comparison with cardiac magnetic resonance imaging. Eur J Nucl Med Mol Imaging. 2004;31(4):482–90.PubMedCrossRefGoogle Scholar
  98. 98.
    Wang F, Zhang J, Fang W, Zhao SH, Lu MJ, He ZX. Evaluation of left ventricular volumes and ejection fraction by gated SPECT and cardiac MRI in patients with dilated cardiomyopathy. Eur J Nucl Med Mol Imaging. 2009;36(10):1611–21. doi: 10.1007/s00259-009-1136-7.PubMedCrossRefGoogle Scholar
  99. 99.
    Estorch M, Carrió I, Martínez-Duncker D, Berná L, Torres G, Alonso C, Ojeda B. Myocyte cell damage after administration of doxorubicin or mitoxantrone in breast cancer patients assessed by indium 111 antimyosin monoclonal antibody studies. J Clin Oncol. 1993;11(7):1264–8.PubMedCrossRefGoogle Scholar
  100. 100.
    Carrió I, Lopez-Pousa A, Estorch M, Duncker D, Berná L, Torres G, de Andrés L. Detection of doxorubicin cardiotoxicity in patients with sarcomas by indium-111-antimyosin monoclonal antibody studies. J Nucl Med. 1993;34(9):1503–7.PubMedGoogle Scholar
  101. 101.
    Valdés Olmos RA, Carrió I, Hoefnagel CA, Estorch M, ten Bokkel Huinink WW, López-Pousa J, Dalesio O. High sensitivity of radiolabelled antimyosin scintigraphy in assessing anthracycline related early myocyte damage preceding cardiac dysfunction. Nucl Med Commun. 2002;23(9):871–7.PubMedCrossRefGoogle Scholar
  102. 102.
    Erselcan T, Kairemo KJ, Wiklund TA, Hernberg M, Blomqvist CP, Tenhunen M, Bergh J, Joensuu H. Subclinical cardiotoxicity following adjuvant dose-escalated FEC, high-dose chemotherapy, or CMF in breast cancer. Br J Cancer. 2000;82(4):777–81.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Kremer LC, Tiel-van Buul MM, Ubbink MC, Offringa M, Ottenkamp J, Olmos RV, Voûte PA. Indium-111-antimyosin scintigraphy in the early detection of heart damage after anthracycline therapy in children. J Clin Oncol. 1999;17(4):1208.PubMedCrossRefGoogle Scholar
  104. 104.
    Francis GS, Cohn JN. The autonomic nervous system in congestive heart failure. Annu Rev Med. 1986;37:235–47.PubMedCrossRefGoogle Scholar
  105. 105.
    Triposkiadis F, Karayannis G, Giamouzis G, Skoularigis J, Louridas G, Butler J. The sympathetic nervous system in heart failure physiology, pathophysiology, and clinical implications. J Am Coll Cardiol. 2009;54(19):1747–62. doi: 10.1016/j.jacc.2009.05.015.PubMedCrossRefGoogle Scholar
  106. 106.
    Valdés Olmos RA, ten Bokkel Huinink WW, ten Hoeve RF, van Tinteren H, Bruning PF, van Vlies B, Hoefnagel CA. Assessment of anthracycline-related myocardial adrenergic derangement by [123I]metaiodobenzylguanidine scintigraphy. Eur J Cancer. 1995;31(1):26–31.CrossRefGoogle Scholar
  107. 107.
    Carrió I, Estorch M, Berná L, López-Pousa J, Tabernero J, Torres G. Indium-111-antimyosin and iodine-123-MIBG studies in early assessment of doxorubicin cardiotoxicity. J Nucl Med. 1995;36(11):2044–9.PubMedGoogle Scholar
  108. 108.
    Hudis CA. Trastuzumab–mechanism of action and use in clinical practice. N Engl J Med. 2007;357(1):39–51.PubMedCrossRefGoogle Scholar
  109. 109.
    Crone SA, Zhao YY, Fan L, Gu Y, Minamisawa S, Liu Y, Peterson KL, Chen J, Kahn R, Condorelli G, Ross J Jr, Chien KR, Lee KF. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat Med. 2002;8(5):459–65.PubMedCrossRefGoogle Scholar
  110. 110.
    Perik PJ, Lub-De Hooge MN, Gietema JA, van der Graaf WT, de Korte MA, Jonkman S, Kosterink JG, van Veldhuisen DJ, Sleijfer DT, Jager PL, de Vries EG. Indium-111-labeled trastuzumab scintigraphy in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer. J Clin Oncol. 2006;24(15):2276–82.PubMedCrossRefGoogle Scholar
  111. 111.
    Behr TM, Béhé M, Wörmann B. Trastuzumab and breast cancer. N Engl J Med. 2001;345(13):995–6.PubMedCrossRefGoogle Scholar
  112. 112.
    Lee JC, Platts DG, Huang YT, Slaughter RE. Positron emission tomography combined with computed tomography as an integral component in evaluation of primary cardiac lymphoma. Clin Cardiol. 2010;33(6):E106–8.PubMedCrossRefGoogle Scholar
  113. 113.
    Weijs LE, Arsos G, Baarslag HJ, Wittebol S, de Klerk JM. Pericardial involvement in a non-Hodgkin lymphoma patient: coregistered FDG-PET and CT imaging. Eur Heart J. 2007;28(22):2698.PubMedCrossRefGoogle Scholar
  114. 114.
    Kenk M, Thackeray JT, Thorn SL, Dhami K, Chow BJ, Ascah KJ, DaSilva JN, Beanlands RS. Alterations of pre- and postsynaptic noradrenergic signaling in a rat model of adriamycin-induced cardiotoxicity. J Nucl Cardiol. 2010;17(2):254–63.PubMedCrossRefGoogle Scholar
  115. 115.
    Su H, Gorodny N, Gomez LF, Gangadharmath U, Mu F, Chen G, Walsh JC, Szardenings K, Kolb HC, Tamarappoo B. Noninvasive molecular imaging of apoptosis in a mouse model of anthracycline-induced cardiotoxicity. Circ Cardiovasc Imaging. 2015;8(2):e001952. doi: 10.1161/CIRCIMAGING.114.001952.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Herrmann J, Yang EH, Iliescu CA, Cilingiroglu M, Charitakis K, Hakeem A, Toutouzas K, Leesar MA, Grines CL, Marmagkiolis K. Vascular Toxicities of Cancer Therapies: The Old and the New - An Evolving Avenue. Circulation. 2016;133(13):1272–89. doi: 10.1161/CIRCULATIONAHA.115.018347.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    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):vii155–66.CrossRefGoogle Scholar
  118. 118.
    Fradgley EA, Paul CL, Bryant J. A systematic review of barriers to optimal outpatient specialist services for individuals with prevalent chronic diseases: what are the unique and common barriers experienced by patients in high income countries? Int J Equity Health. 2015;14:52. doi: 10.1186/s12939-015-0179-6.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Yoon GJ, Telli ML, Kao DP, Matsuda KY, Carlson RW, Witteles RM. Left ventricular dysfunction in patients receiving cardiotoxic cancer therapies are clinicians responding optimally? J Am Coll Cardiol. 2010;56(20):1644–50. doi: 10.1016/j.jacc.2010.07.023.PubMedCrossRefGoogle Scholar
  120. 120.
    Zibrik K, Laskin J, Ho C. Implementation of a lung cancer nurse navigator enhances patient care and delivery of systemic therapy at the british columbia cancer agency, Vancouver. J Oncol Pract. 2016;12(3):e344–9. doi: 10.1200/JOP.2015.008813.PubMedCrossRefGoogle Scholar
  121. 121.
    McAllister KA, Schmitt ML. Impact of a nurse navigator on genomic testing and timely treatment decision making in patients with breast cancer. Clin J Oncol Nurs. 2015;19(5):510–2. doi: 10.1188/15.CJON.510-512.PubMedCrossRefGoogle Scholar
  122. 122.
    Holmes DR, Major J, Lyonga DE, Alleyne RS, Clayton SM. Increasing minority patient participation in cancer clinical trials using oncology nurse navigation. Am J Surg. 2012;203(4):415–22. doi: 10.1016/j.amjsurg.2011.02.005.PubMedCrossRefGoogle Scholar

Copyright information

© American Society of Nuclear Cardiology 2016

Authors and Affiliations

  • Carol Chen-Scarabelli
    • 1
  • Chad McRee
    • 2
  • Massoud A. Leesar
    • 1
    • 2
  • Fadi G. Hage
    • 1
    • 2
  • Tiziano M. Scarabelli
    • 1
    • 2
  1. 1.Birmingham Veterans Affairs Medical CenterUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Division of Cardiovascular DiseaseUniversity of Alabama at BirminghamBirminghamUSA

Personalised recommendations