Advertisement

Cardiac MRI: a Promising Diagnostic Tool to Detect Cancer Therapeutics–Related Cardiac Dysfunction

  • Jasmin D. Haslbauer
  • Sarah Lindner
  • Gesine Bug
  • Eike Nagel
  • Valentina O. PuntmannEmail author
Cardiac Magnetic Resonance (E Nagel and V Puntmann, Section Editors)
  • 25 Downloads
Part of the following topical collections:
  1. Topical Collection on Cardiac Magnetic Resonance

Abstract

Purpose of Review

Recent advances in oncological research have led to a major improvement of mortality amongst cancer patients. However, survivors are at an increased risk to develop cancer therapeutics–related cardiac dysfunction (CTRCD). The management of CTRCD may pose a challenge due to its heterogeneous clinical presentation. This warrants the need for a multi-modality diagnostic tool to objectively acquire prognostic information for timely commencement of cardio-protective treatment. Cardiac magnetic resonance (CMR) imaging offers considerable potential due to its non-invasive, reproducible protocol. Moreover, biomarkers such as T1 and T2 mapping allow discrimination between oedematous and fibrotic myocardium, providing an invaluable diagnostic algorithm to track the temporal evolution of CTRCD.

Recent Findings

In this review, we appraise current evidence for the role of CMR in the management of CTRCD, placing emphasis on ventricular function, strain, late gadolinium enhancement and parametric mapping.

Summary

We recommend a central role for CMR in the interdisciplinary management of CTRCD.

Keywords

Cardio-oncology Cardiac magnetic resonance Cancer therapeutics Cardiotoxicity Anthracyclines 

Abbreviations

2/3DE

2D/3D echocardiography

AI

Artificial intelligence

ATP

Adenosine triphosphate

CMR

Cardiac magnetic resonance

CTLA-4

Cytotoxic T lymphocyte–associated Protein 4

CTRCD

Cancer therapeutics–related cardiac dysfunction

CV

Cardiovascular

ECV

Extracellular volume

EDV

End-diastolic volume

ESV

End-systolic volume

EMB

Endomyocardial biopsy

ESC

European Society of Cardiology

GCS

Global circumferential strain

GLS

Global longitudinal strain

HF

Heart failure

hs-troponinT

High-sensitive troponin T

LGE

Late gadolinium enhancement

LV

Left ventricular

LVEF

Left ventricular ejection fraction

NT-proBNP

N-terminal pro-brain natriuretic peptide

NSCLC

Non-small cell lung cancer

PD1

Programmed cell death protein 1

PDL1

Programmed cell death protein ligand 1

PWV

Pulse wave velocity

QOL

Quality of life

ROS

Reactive oxygen species

RVEF

Right ventricular ejection fraction

SSFP

Steady-state free precession

TKI

Tyrosine kinase inhibitors

Notes

Compliance with Ethical Standards

Conflict of Interest

Jasmin D. Haslbauer, Gesine Bug, Eike Nagel and Valentina O. Puntmann declare that they have no conflict of interest.

Sarah Lindner receives travel support from Celgene, Sanofi and Neovii.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    Hashim D, Boffetta P, La Vecchia C, Rota M, Bertuccio P, Malvezzi M, et al. The global decrease in cancer mortality: trends and disparities. Ann Oncol. 2016;27(5):926–33.PubMedGoogle Scholar
  2. 2.
    Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30.Google Scholar
  3. 3.
    Manrique CR, Park M, Tiwari N, Plana JC, Garcia MJ. Diagnostic strategies for early recognition of cancer therapeutics-related cardiac dysfunction. Clin Med Insights Cardiol. 2017;11:1179546817697983.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Koutsoukis A, Ntalianis A, Repasos E, Kastritis E, Dimopoulos M-A, Paraskevaidis I. Cardio-oncology: a focus on cardiotoxicity. Eur Cardiol. 2018;13(1):64–9.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Plana JC, Thavendiranathan P, Bucciarelli-Ducci C, Lancellotti P. Multi-modality imaging in the assessment of cardiovascular toxicity in the cancer patient. JACC Cardiovasc Imaging. 2018;11(8):1173–86.PubMedGoogle Scholar
  6. 6.
    • Zamorano JL, Lancellotti P, Rodriguez Muñoz D, Aboyans V, Asteggiano R, Galderisi M, et al. 2016 ESC Position Paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines: the task force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur Heart J. 2016;37(36):2768–801 This ESC practice guideline provides an in-depth, critical review on current diagnostic tools to screen, diagnose and manage patients with CTRCD.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Kostakou PM, Kouris NT, Kostopoulos VS, Damaskos DS, Olympios CD. Cardio-oncology: a new and developing sector of research and therapy in the field of cardiology. Heart Fail Rev 2018Google Scholar
  8. 8.
    McGowan JV, Chung R, Maulik A, Piotrowska I, Walker JM, Yellon DM. Anthracycline chemotherapy and cardiotoxicity. Cardiovasc Drugs Ther. 2017;31(1):63–75.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Pai VB, Nahata MC. Cardiotoxicity of chemotherapeutic agents: incidence, treatment and prevention. Drug Saf. 2000;22(4):263–302.PubMedGoogle Scholar
  10. 10.
    Jain D, Ahmad T, Cairo M, Aronow W. Cardiotoxicity of cancer chemotherapy: identification, prevention and treatment. Ann Transl Med [Internet]. 2017[cited 2018 May 25];5(17). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5599271/
  11. 11.
    Zeglinski M, Ludke A, Jassal DS, Singal PK. Trastuzumab-induced cardiac dysfunction: a ‘dual-hit’. Exp Clin Cardiol. 2011;16(3):70–4.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Lee W-S, Kim J. Cardiotoxicity associated with tyrosine kinase-targeted anticancer therapy. Mol Cell Toxicol. 2018;14(3):247–54.Google Scholar
  13. 13.
    Gilda V, Rosaria GM, Tocchetti Carlo G. Cardiac toxicity of immune checkpoint inhibitors. Circulation. 2017;136(21):1989–92.Google Scholar
  14. 14.
    Hamo CE, Bloom MW. Getting to the heart of the matter: an overview of cardiac toxicity related to cancer therapy. Clin Med Insights Cardiol. 2015;9(Suppl 2):47–51.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Sawyer DB, Peng X, Chen B, Pentassuglia L, Lim CC. Mechanisms of anthracycline cardiac injury: can we identify strategies for cardio-protection? Prog Cardiovasc Dis. 2010;53(2):105–13.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Berry GJ, Jorden M. Pathology of radiation and anthracycline cardiotoxicity. Pediatr Blood Cancer. 2005;44(7):630–7.PubMedGoogle Scholar
  17. 17.
    Bernaba BN, Chan JB, Lai CK, Fishbein MC. Pathology of late-onset anthracycline cardiomyopathy. Cardiovasc Pathol Off J Soc Cardiovasc Pathol. 2010;19(5):308–11.Google Scholar
  18. 18.
    Lemmens K, Doggen K, De Keulenaer GW. Role of neuregulin-1/ErbB signaling in cardiovascular physiology and disease: implications for therapy of heart failure. Circulation. 2007;116(8):954–60.Google Scholar
  19. 19.
    Florido R, Smith KL, Cuomo KK, Russell SD. Cardiotoxicity from human epidermal growth factor receptor-2 (HER2) targeted therapies. J Am Heart Assoc Cardiovasc Cerebrovasc Dis [Internet]. 2017[cited 2018 Nov 25];6(9). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5634312/
  20. 20.
    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(24):2504–12.PubMedGoogle Scholar
  21. 21.
    Bloom MW, Hamo CE, Cardinale D, Ky B, Nohria A, Baer L, et al. Cancer therapy-related cardiac dysfunction and heart failure part 1: definitions, pathophysiology, risk factors, and imaging. Circ Heart Fail. 2016;9(1):e002661.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Tanaka S, Ikari A, Nitta T, Horiuchi T. Long-term irreversible trastuzumab-induced cardiotoxicity for metastatic breast cancer in a patient without cardiac risk factors. Oxf Med Case Rep [Internet]. 2017[cited 2018 Nov 25];2017(7). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5499211/
  23. 23.
    Slamon D, Eiermann W, Robert N, Pienkowski T, Martin M, Press M, et al. Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med. 2011;365(14):1273–83.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Romond EH, Perez EA, Bryant J, Suman VJ, Geyer CE, Davidson NE, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med. 2005;353(16):1673–84.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Martin M, Pienkowski T, Mackey J, Pawlicki M, Guastalla J-P, Weaver C, et al. Adjuvant docetaxel for node-positive breast cancer. N Engl J Med. 2005;352(22):2302–13.PubMedGoogle Scholar
  26. 26.
    Martín M, Seguí MA, Antón A, Ruiz A, Ramos M, Adrover E, et al. Adjuvant docetaxel for high-risk, node-negative breast cancer. N Engl J Med. 2010;363(23):2200–10.PubMedGoogle Scholar
  27. 27.
    Fisher B, Jeong J-H, Dignam J, Anderson S, Mamounas E, Wickerham DL, et al. Findings from recent National Surgical Adjuvant Breast and Bowel Project adjuvant studies in stage I breast cancer. JNCI Monogr. 2001;2001(30):62–6.Google Scholar
  28. 28.
    Martin M, Villar A, Sole-Calvo A, Gonzalez R, Massuti B, Lizon J, et al. Doxorubicin in combination with fluorouracil and cyclophosphamide (i.v. FAC regimen, day 1, 21) versus methotrexate in combination with fluorouracil and cyclophosphamide (i.v. CMF regimen, day 1, 21) as adjuvant chemotherapy for operable breast cancer: a study by the GEICAM group. Ann Oncol Off J Eur Soc Med Oncol. 2003;14(6):833–42.Google Scholar
  29. 29.
    Sparano JA, Wang M, Martino S, Jones V, Perez EA, Saphner T, et al. Weekly paclitaxel in the adjuvant treatment of breast cancer. N Engl J Med. 2008;358(16):1663–71.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Roché H, Fumoleau P, Spielmann M, Canon J-L, Delozier T, Serin D, et al. Sequential adjuvant epirubicin-based and docetaxel chemotherapy for node-positive breast cancer patients: the FNCLCC PACS 01 trial. J Clin Oncol Off J Am Soc Clin Oncol. 2006;24(36):5664–71.Google Scholar
  31. 31.
    Citron ML, Berry DA, Cirrincione C, Hudis C, Winer EP, Gradishar WJ, et al. Randomized trial of dose-dense versus conventionally scheduled and sequential versus concurrent combination chemotherapy as postoperative adjuvant treatment of node-positive primary breast cancer: first report of Intergroup Trial C9741/Cancer and Leukemia Group B Trial 9741. J Clin Oncol Off J Am Soc Clin Oncol. 2003;21(8):1431–9.Google Scholar
  32. 32.
    Sessa C, Pagani O. Docetaxel and epirubicin in advanced breast cancer. Oncologist. 2001;6(Supplement 3):13–6.PubMedGoogle Scholar
  33. 33.
    Julka PK, Awasthy BS, Sharma DN, Gairola M, Rath GK. Paclitaxel-epirubicin in advanced breast cancer. J Assoc Physicians India. 1999;47(5):499–502.PubMedGoogle Scholar
  34. 34.
    Gehl J, Boesgaard M, Paaske T, Vittrup Jensen B, Dombernowsky P. Combined doxorubicin and paclitaxel in advanced breast cancer: effective and cardiotoxic. Ann Oncol Off J Eur Soc Med Oncol. 1996;7(7):687–93.Google Scholar
  35. 35.
    Baltali E, Ozişik Y, Güler N, Firat D, Altundağ K. Combination of docetaxel and doxorubicin as first-line chemotherapy in metastatic breast cancer. Tumori. 2001;87(1):18–9.PubMedGoogle Scholar
  36. 36.
    Chan S, Davidson N, Juozaityte E, Erdkamp F, Pluzanska A, Azarnia N, et al. Phase III trial of liposomal doxorubicin and cyclophosphamide compared with epirubicin and cyclophosphamide as first-line therapy for metastatic breast cancer. Ann Oncol Off J Eur Soc Med Oncol. 2004;15(10):1527–34.Google Scholar
  37. 37.
    Monk BJ, Herzog TJ, Kaye SB, Krasner CN, Vermorken JB, Muggia FM, et al. Trabectedin plus pegylated liposomal doxorubicin in recurrent ovarian cancer. J Clin Oncol Off J Am Soc Clin Oncol. 2010;28(19):3107–14.Google Scholar
  38. 38.
    Ueda Y, Miyake T, Egawa-Takata T, Miyatake T, Matsuzaki S, Yokoyama T, et al. Second-line chemotherapy for advanced or recurrent endometrial carcinoma previously treated with paclitaxel and carboplatin, with or without epirubicin. Cancer Chemother Pharmacol. 2011;67(4):829–35.PubMedGoogle Scholar
  39. 39.
    He Q, Zhao J, Yuan J, Gong Z, Yi T. Combined perioperative EOX chemotherapy and postoperative chemoradiotherapy for locally advanced gastric cancer. Mol Clin Oncol. 2017;7(2):211–6.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Gunturu KS, Woo Y, Beaubier N, Remotti HE, Saif MW. Gastric cancer and trastuzumab: first biologic therapy in gastric cancer. Ther Adv Med Oncol. 2013;5(2):143–51.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Chan BA, Coward JIG. Chemotherapy advances in small-cell lung cancer. J Thorac Dis. 2013;5(Suppl 5):S565–78.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Pacini F, Castagna MG, Brilli L, Pentheroudakis G, ESMO Guidelines Working Group. Thyroid cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol Off J Eur Soc Med Oncol. 2010;21(Suppl 5):v214–9.Google Scholar
  43. 43.
    Okuno SH, Mailliard JA, Suman VJ, Edmonson JH, Creagan ET, Nair S, et al. Phase II study of methotrexate, vinblastine, doxorubicin, and cisplatin in patients with squamous cell carcinoma of the upper respiratory or alimentary passages of the head and neck. Cancer. 2002;94(8):2224–31.PubMedGoogle Scholar
  44. 44.
    Hoelzer D, Bassan R, Dombret H, Fielding A, Ribera JM, Buske C, et al. Acute lymphoblastic leukaemia in adult patients: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol Off J Eur Soc Med Oncol. 2016;27(suppl 5):v69–82.Google Scholar
  45. 45.
    Fey MF, Buske C, ESMO Guidelines Working Group. Acute myeloblastic leukaemias in adult patients: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol Off J Eur Soc Med Oncol. 2013;24(Suppl 6):vi138–43.Google Scholar
  46. 46.
    Oakervee HE, Popat R, Curry N, Smith P, Morris C, Drake M, et al. PAD combination therapy (PS-341/bortezomib, doxorubicin and dexamethasone) for previously untreated patients with multiple myeloma. Br J Haematol. 2005;129(6):755–62.PubMedGoogle Scholar
  47. 47.
    Boleti E, Mead GM. ABVD for Hodgkin’s lymphoma: full-dose chemotherapy without dose reductions or growth factors. Ann Oncol. 2007;18(2):376–80.PubMedGoogle Scholar
  48. 48.
    Kelly KM, Sposto R, Hutchinson R, Massey V, McCarten K, Perkins S, et al. BEACOPP chemotherapy is a highly effective regimen in children and adolescents with high-risk Hodgkin lymphoma: a report from the Children’s Oncology Group. Blood. 2011;117(9):2596–603.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Fisher RI, Gaynor ER, Dahlberg S, Oken MM, Grogan TM, Mize EM, et al. Comparison of a standard regimen (CHOP) with three intensive chemotherapy regimens for advanced non-Hodgkin’s lymphoma. N Engl J Med. 1993;328(14):1002–6.PubMedGoogle Scholar
  50. 50.
    Pfreundschuh M, Zwick C, Zeynalova S, Duhrsen U, Pfluger K-H, Vrieling T, et al. Dose-escalated CHOEP for the treatment of young patients with aggressive non-Hodgkin’s lymphoma: II. Results of the randomized high-CHOEP trial of the German High-Grade Non-Hodgkin’s Lymphoma Study Group (DSHNHL). Ann Oncol. 2007;19(3):545–52.PubMedGoogle Scholar
  51. 51.
    Keating GM. Pixantrone: a review in relapsed or refractory aggressive non-Hodgkin’s lymphoma. Drugs. 2016;76(16):1579–86.PubMedGoogle Scholar
  52. 52.
    Information NC for B, Pike USNL of M 8600 R, MD B, Usa 20894. Evidence and recommendations on Kaposi sarcoma (KS) [Internet]. World Health Organization; 2014 [cited 2018 Dec 10]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK305418/
  53. 53.
    Sagaster P, Flamm J, Flamm M, Mayer A, Donner G, Oberleitner S, et al. Neoadjuvant chemotherapy (MVAC) in locally invasive bladder cancer. Eur J Cancer Oxf Engl 1990. 1996;32A(8):1320–4.Google Scholar
  54. 54.
    Bamias A, Dimitriadis I. Systemic chemotherapy for urothelial cancer – how to select systemic therapy in bladder cancer. Syst Chemother Urothelial Cancer – Sel Syst Ther Bladder Cancer [Internet]. 2017 [cited 2018 Dec 10]; Available from: https://www.touchoncology.com/articles/systemic-chemotherapy-urothelial-cancer-how-select-systemic-therapy-bladder-cancer
  55. 55.
    Dangoor A, Seddon B, Gerrand C, Grimer R, Whelan J, Judson I. UK guidelines for the management of soft tissue sarcomas. Clin Sarcoma Res. 2016;6(1):20.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Pender A, Jones RL. Olaratumab: a platelet-derived growth factor receptor-α-blocking antibody for the treatment of soft tissue sarcoma. Clin Pharmacol Adv Appl. 2017;9:159–64.Google Scholar
  57. 57.
    Whelan J, Khan A, Sharma A, Rothermundt C, Dileo P, Michelagnoli M, et al. Interval compressed vincristine, doxorubicin, cyclophosphamide alternating with ifosfamide, etoposide in patients with advanced Ewing’s and other small round cell sarcomas. Clin Sarcoma Res. 2012;2:12.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Kleinerman E. Maximum benefit of chemotherapy for osteosarcoma achieved—what are the next steps? Lancet Oncol. 2016;17(10):1340–2.PubMedGoogle Scholar
  59. 59.
    Bhatnagar S. Management of Wilms’ tumor: NWTS vs SIOP. J Indian Assoc Pediatr Surg. 2009;14(1):6–14.PubMedPubMedCentralGoogle Scholar
  60. 60.
    McWilliams NB, Hayes FA, Green AA, Smith EI, Nitschke R, Altshuler GA, et al. Cyclophosphamide/doxorubicin vs. cisplatin/teniposide in the treatment of children older than 12 months of age with disseminated neuroblastoma: a pediatric oncology group randomized phase II study. Med Pediatr Oncol. 1995;24(3):176–80.PubMedGoogle Scholar
  61. 61.
    Amoroso L, Erminio G, Makin G, Pearson ADJ, Brock P, Valteau-Couanet D, et al. Topotecan-vincristine-doxorubicin in stage 4 high-risk neuroblastoma patients failing to achieve a complete metastatic response to rapid COJEC: a SIOPEN study. Cancer Res Treat. 2017;50(1):148–55.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Orphanos GS, Ioannidis GN, Ardavanis AG. Cardiotoxicity induced by tyrosine kinase inhibitors. Acta Oncol Stockh Swed. 2009;48(7):964–70.Google Scholar
  63. 63.
    Varricchi G, Galdiero MR, Marone G, Criscuolo G, Triassi M, Bonaduce D, et al. Cardiotoxicity of immune checkpoint inhibitors. ESMO Open [Internet]. 2017[cited 2018 Nov 18];2(4). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5663252/ PubMedPubMedCentralGoogle Scholar
  64. 64.
    Plana JC, Galderisi M, Barac A, Ewer MS, Ky B, Scherrer-Crosbie M, 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 Off Publ Am Soc Echocardiogr. 2014;27(9):911–39.Google Scholar
  65. 65.
    Löffler AI, Salerno M. Cardiac MRI for the evaluation of oncologic cardiotoxicity. J Nucl Cardiol Off Publ Am Soc Nucl Cardiol 2018.Google Scholar
  66. 66.
    Thavendiranathan P, Wintersperger BJ, Flamm SD, Marwick TH. Cardiac MRI in the assessment of cardiac injury and toxicity from cancer chemotherapy: a systematic review. Circ Cardiovasc Imaging. 2013;6(6):1080–91.PubMedGoogle Scholar
  67. 67.
    Oreto L, Todaro MC, Umland MM, Kramer C, Qamar R, Carerj S, et al. Use of echocardiography to evaluate the cardiac effects of therapies used in cancer treatment: what do we know? J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr. 2012;25(11):1141–52.Google Scholar
  68. 68.
    Armstrong GT, Plana JC, Zhang N, Srivastava D, Green DM, Ness KK, et al. Screening adult survivors of childhood cancer for cardiomyopathy: comparison of echocardiography and cardiac magnetic resonance imaging. J Clin Oncol Off J Am Soc Clin Oncol. 2012;30(23):2876–84.Google Scholar
  69. 69.
    Armstrong AC, Gidding S, Gjesdal O, Wu C, Bluemke DA, Lima JAC. LV mass assessed by echocardiography and CMR, cardiovascular outcomes, and medical practice. JACC Cardiovasc Imaging. 2012;5(8):837–48.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Fallah-Rad N, Walker JR, Wassef A, Lytwyn M, Bohonis S, Fang T, 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(22):2263–70.PubMedGoogle Scholar
  71. 71.
    Henri C, Heinonen T, Tardif J-C. The role of biomarkers in decreasing risk of cardiac toxicity after cancer therapy. Biomark Cancer. 2016;8(Suppl 2):39–45.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Riddell E, Lenihan D. The role of cardiac biomarkers in cardio-oncology. Curr Probl Cancer. 2018;42(4):375–85.PubMedGoogle Scholar
  73. 73.
    Tan L-L, Lyon AR. Role of biomarkers in prediction of cardiotoxicity during cancer treatment. Curr Treat Options Cardiovasc Med [Internet]. 2018 [cited 2018 Nov 25];20(7). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6008350/
  74. 74.
    Berridge BR, Pettit S, Walker DB, Jaffe AS, Schultze AE, Herman E, et al. A translational approach to detecting drug-induced cardiac injury with cardiac troponins: consensus and recommendations from the cardiac troponins biomarker working group of the health and environmental sciences institute. Am Heart J. 2009;158(1):21–9.PubMedGoogle Scholar
  75. 75.
    • Haslbauer JD, Lindner S, Valbuena-Lopez S, Zainal H, Zhou H, D’Angelo T, et al. CMR imaging biosignature of cardiac involvement due to cancer-related treatment by T1 and T2 mapping. Int J Cardiol. 2018. This study unravels novel imaging biosignatures (T1 and T2 mapping) as a diagnostic algorithm to characterise the extent of myocardial oedema and/or fibrosis in CTRCD patients, thus highlighting the potential of CMR to manage CTRCD. Google Scholar
  76. 76.
    Gong IY, Ong G, Brezden-Masley C, Dhir V, Deva DP, Chan KKW, et al. Early diastolic strain rate measurements by cardiac MRI in breast cancer patients treated with trastuzumab: a longitudinal study. Int J Card Imaging 2018.Google Scholar
  77. 77.
    Kimball A, Patil S, Koczwara B, Raman KS, Perry R, Grover S, et al. Late characterisation of cardiac effects following anthracycline and trastuzumab treatment in breast cancer patients. Int J Cardiol. 2018;261:159–61.PubMedGoogle Scholar
  78. 78.
    Grover S, Leong DP, Chakrabarty A, Joerg L, Kotasek D, Cheong K, et al. Left and right ventricular effects of anthracycline and trastuzumab chemotherapy: a prospective study using novel cardiac imaging and biochemical markers. Int J Cardiol. 2013;168(6):5465–7.PubMedGoogle Scholar
  79. 79.
    Ferreira de Souza T, Quinaglia AC, Silva T, Osorio Costa F, Shah R, Neilan TG, et al. Anthracycline therapy is associated with cardiomyocyte atrophy and preclinical manifestations of heart disease. JACC Cardiovasc Imaging. 2018;11(8):1045–55.PubMedGoogle Scholar
  80. 80.
    Muehlberg F, Funk S, Zange L, von Knobelsdorff-Brenkenhoff F, Blaszczyk E, Schulz A, et al. Native myocardial T1 time can predict development of subsequent anthracycline-induced cardiomyopathy. ESC Heart Fail 2018.Google Scholar
  81. 81.
    Ong G, Brezden-Masley C, Dhir V, Deva DP, Chan KKW, Chow C-M, et al. Myocardial strain imaging by cardiac magnetic resonance for detection of subclinical myocardial dysfunction in breast cancer patients receiving trastuzumab and chemotherapy. Int J Cardiol. 2018;261:228–33.PubMedGoogle Scholar
  82. 82.
    Jolly M-P, Jordan JH, Meléndez GC, McNeal GR, D’Agostino RB, Hundley WG. Automated assessments of circumferential strain from cine CMR correlate with LVEF declines in cancer patients early after receipt of cardio-toxic chemotherapy. J Cardiovasc Magn Reson [Internet]. 2017 [cited 2018 Nov 17];19. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5541737/
  83. 83.
    Barthur A, Brezden-Masley C, Connelly KA, Dhir V, Chan KKW, Haq R, et al. Longitudinal assessment of right ventricular structure and function by cardiovascular magnetic resonance in breast cancer patients treated with trastuzumab: a prospective observational study. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson. 2017;19(1):44.Google Scholar
  84. 84.
    Nakano S, Takahashi M, Kimura F, Senoo T, Saeki T, Ueda S, et al. Cardiac magnetic resonance imaging-based myocardial strain study for evaluation of cardiotoxicity in breast cancer patients treated with trastuzumab: a pilot study to evaluate the feasibility of the method. Cardiol J. 2016;23(3):270–80.PubMedGoogle Scholar
  85. 85.
    Jordan JH, Vasu S, Morgan TM, D’Agostino RB, Meléndez GC, Hamilton CA, et al. Anthracycline-associated T1 mapping characteristics are elevated independent of the presence of cardiovascular comorbidities in cancer survivors. Circ Cardiovasc Imaging. 2016;9(8).Google Scholar
  86. 86.
    Grover S, Lou PW, Bradbrook C, Cheong K, Kotasek D, Leong DP, et al. Early and late changes in markers of aortic stiffness with breast cancer therapy. Intern Med J. 2015;45(2):140–7.PubMedGoogle Scholar
  87. 87.
    Drafts BC, Twomley KM, D’Agostino R, Lawrence J, Avis N, Ellis LR, 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(8):877–85.PubMedPubMedCentralGoogle Scholar
  88. 88.
    Tham EB, Haykowsky MJ, Chow K, Spavor M, Kaneko S, Khoo NS, et al. Diffuse myocardial fibrosis by T1-mapping in children with subclinical anthracycline cardiotoxicity: relationship to exercise capacity, cumulative dose and remodeling. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson. 2013;15:48.Google Scholar
  89. 89.
    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.PubMedPubMedCentralGoogle Scholar
  90. 90.
    Ylänen K, Poutanen T, Savikurki-Heikkilä P, Rinta-Kiikka I, Eerola A, Vettenranta K. Cardiac magnetic resonance imaging in the evaluation of the late effects of anthracyclines among long-term survivors of childhood cancer. J Am Coll Cardiol. 2013;61(14):1539–47.PubMedGoogle Scholar
  91. 91.
    Toro-Salazar OH, Gillan E, O’Loughlin MT, Burke GS, Ferranti J, Stainsby J, et al. Occult cardiotoxicity in childhood cancer survivors exposed to anthracycline therapy. Circ Cardiovasc Imaging. 2013;6(6):873–80.PubMedGoogle Scholar
  92. 92.
    Seidman A, Hudis C, Pierri MK, Shak S, Paton V, Ashby M, et al. Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin Oncol Off J Am Soc Clin Oncol. 2002;20(5):1215–21.Google Scholar
  93. 93.
    Grothues F, Smith GC, Moon JCC, Bellenger NG, Collins P, Klein HU, et al. Comparison of interstudy reproducibility of cardiovascular magnetic resonance with two-dimensional echocardiography in normal subjects and in patients with heart failure or left ventricular hypertrophy. Am J Cardiol. 2002;90(1):29–34.PubMedGoogle Scholar
  94. 94.
    Rasool HJ, Tak T, Gill P, Novotny JE, Jaekel C, Elkhatib RT, et al. Cardiovascular magnetic resonance imaging compared to echocardiogram for detecting doxorubicin-induced cardiotoxicity. J Clin Oncol. 2014;32(15_suppl):1068.Google Scholar
  95. 95.
    • Puntmann VO, Valbuena S, Hinojar R, Petersen SE, Greenwood JP, Kramer CM, et al. Society for Cardiovascular Magnetic Resonance (SCMR) expert consensus for CMR imaging endpoints in clinical research: part I - analytical validation and clinical qualification. J Cardiovasc Magn Reson. 2018;20(1):67 This SCMR expert consensus offers appraisal on current evidence surrounding CMR imaging endpoints, discussing the key strengths this image modality has to offer, as well as transferability of acquisition and post-processing into clinical practice.PubMedPubMedCentralGoogle Scholar
  96. 96.
    Almutairi HM, Boubertakh R, Miquel ME, Petersen SE. Myocardial deformation assessment using cardiovascular magnetic resonance-feature tracking technique. Br J Radiol. 2017;90(1080):20170072.PubMedPubMedCentralGoogle Scholar
  97. 97.
    Scatteia A, Baritussio A, Bucciarelli-Ducci C. Strain imaging using cardiac magnetic resonance. Heart Fail Rev. 2017;22(4):465–76.PubMedPubMedCentralGoogle Scholar
  98. 98.
    Burridge PW, Li YF, Matsa E, Wu H, Ong S-G, Sharma A, et al. Human induced pluripotent stem cell-derived cardiomyocytes recapitulate the predilection of breast cancer patients to doxorubicin-induced cardiotoxicity. Nat Med. 2016;22(5):547–56.PubMedPubMedCentralGoogle Scholar
  99. 99.
    Gulati G, Heck SL, Ree AH, Hoffmann P, Schulz-Menger J, Fagerland MW, et al. Prevention of cardiac dysfunction during adjuvant breast cancer therapy (PRADA): a 2 × 2 factorial, randomized, placebo-controlled, double-blind clinical trial of candesartan and metoprolol. Eur Heart J. 2016;37(21):1671–80.PubMedPubMedCentralGoogle Scholar
  100. 100.
    Cardinale D, Colombo A, Bacchiani G, Tedeschi I, Meroni CA, Veglia F, et al. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation. 2015;131(22):1981–8.PubMedGoogle Scholar
  101. 101.
    Schulz-Menger J, Bluemke DA, Bremerich J, Flamm SD, Fogel MA, Friedrich MG, et al. Standardized image interpretation and post processing in cardiovascular magnetic resonance: Society for Cardiovascular Magnetic Resonance (SCMR) board of trustees task force on standardized post processing. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson. 2013;15:35.Google Scholar
  102. 102.
    Wadhwa D, Fallah-Rad N, Grenier D, Krahn M, Fang T, Ahmadie R, et al. Trastuzumab mediated cardiotoxicity in the setting of adjuvant chemotherapy for breast cancer: a retrospective study. Breast Cancer Res Treat. 2009;117(2):357–64.PubMedGoogle Scholar
  103. 103.
    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 Off J Soc Cardiovasc Magn Reson. 2008;10:5.Google Scholar
  104. 104.
    Puntmann VO, Peker E, Chandrashekhar Y, Nagel E. T1 mapping in characterizing myocardial disease: a comprehensive review. Circ Res. 2016;119(2):277–99.PubMedGoogle Scholar
  105. 105.
    Taylor AJ, Salerno M, Dharmakumar R, Jerosch-Herold M. T1 mapping: basic techniques and clinical applications. JACC Cardiovasc Imaging. 2016;9(1):67–81.PubMedGoogle Scholar
  106. 106.
    Lurz P, Luecke C, Eitel I, Föhrenbach F, Frank C, Grothoff M, et al. Comprehensive cardiac magnetic resonance imaging in patients with suspected myocarditis: the MyoRacer-trial. J Am Coll Cardiol. 2016;67(15):1800–11.PubMedGoogle Scholar
  107. 107.
    Child N, Suna G, Dabir D, Yap M-L, Rogers T, Kathirgamanathan M, et al. Comparison of MOLLI, shMOLLLI, and SASHA in discrimination between health and disease and relationship with histologically derived collagen volume fraction. Eur Heart J Cardiovasc Imaging. 2018;19(7):768–76.PubMedGoogle Scholar
  108. 108.
    Hinojar R, Foote L, Arroyo Ucar E, Jackson T, Jabbour A, Yu C-Y, et al. Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis: a proposed diagnostic algorithm using CMR. JACC Cardiovasc Imaging. 2015;8(1):37–46.PubMedGoogle Scholar
  109. 109.
    Winau L, Hinojar Baydes R, Braner A, Drott U, Burkhardt H, Sangle S, D'Cruz DP, Carr-White G, Marber M, Schnoes K, Arendt C, Klingel K, Vogl TJ, Zeiher AM, Nagel E, Puntmann VO. Ann Rheum Dis. 2018 Nov;77(11):1590-1598. High-sensitive troponin is associated with subclinical imaging biosignature of inflammatory cardiovascular involvement in systemic lupus erythematosus. Ann Rheum Dis. 2018 Nov;77(11):1590-1598.PubMedGoogle Scholar
  110. 110.
    Bohnen S, Radunski UK, Lund GK, Kandolf R, Stehning C, Schnackenburg B, et al. Performance of T1 and T2 mapping cardiovascular magnetic resonance to detect active myocarditis in patients with recent-onset heart failure. Circ Cardiovasc Imaging. 2015;8(6).Google Scholar
  111. 111.
    Puntmann VO, Carr-White G, Jabbour A, Yu CY, Gebker R, Kelle S, Rolf A, Zitzmann S, Peker E, D'Angelo T, Pathan F, Elen, Valbuena S, Hinojar R, Arendt C, Narula J, Herrmann E, Zeiher AM, Nagel E. Native T1 and ECV of Noninfarcted Myocardium and Outcome in Patients With Coronary Artery Disease. International T1 Multicentre CMR Outcome Study. J Am Coll Cardiol. 2018 Feb 20;71(7):766-778.Google Scholar
  112. 112.
    Farhad H, Staziaki PV, Addison D, Coelho-Filho OR, Shah RV, Mitchell RN, et al. Characterization of the changes in cardiac structure and function in mice treated with anthracyclines using serial cardiac magnetic resonance imaging. Circ Cardiovasc Imaging. 2016;9(12).Google Scholar
  113. 113.
    Moslehi JJ, Salem J-E, Sosman JA, Lebrun-Vignes B, Johnson DB. Increased reporting of fatal immune checkpoint inhibitor-associated myocarditis. Lancet. 2018;391(10124):933.PubMedGoogle Scholar
  114. 114.
    Mukai-Yatagai N, Haruki N, Kinugasa Y, Ohta Y, Ishibashi-Ueda H, Akasaka T, et al. Assessment of myocardial fibrosis using T1-mapping and extracellular volume measurement on cardiac magnetic resonance imaging for the diagnosis of radiation-induced cardiomyopathy. J Cardiol Cases. 2018;18(4):132–5.PubMedPubMedCentralGoogle Scholar
  115. 115.
    Valbuena-López S, Hinojar R, Puntmann VO. Cardiovascular magnetic resonance in cardiology practice: a concise guide to image acquisition and clinical interpretation. Rev Espanola Cardiol Engl Ed. 2016;69(2):202–10.Google Scholar
  116. 116.
    Skitch A, Mital S, Mertens L, Liu P, Kantor P, Grosse-Wortmann L, et al. Novel approaches to the prediction, diagnosis and treatment of cardiac late effects in survivors of childhood cancer: a multi-centre observational study. BMC Cancer. 2017;17(1):519.PubMedPubMedCentralGoogle Scholar
  117. 117.
    Heck SL, Gulati G, Hoffmann P, von Knobelsdorff-Brenkenhoff F, Storås TH, Ree AH, et al. Effect of candesartan and metoprolol on myocardial tissue composition during anthracycline treatment: the PRADA trial. Eur Heart J Cardiovasc Imaging 2017.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Jasmin D. Haslbauer
    • 1
  • Sarah Lindner
    • 2
  • Gesine Bug
    • 2
  • Eike Nagel
    • 1
  • Valentina O. Puntmann
    • 1
    Email author
  1. 1.Institute of Experimental and Translational Cardiovascular Imaging, DZHK Centre for Cardiovascular ImagingGoethe University Hospital FrankfurtFrankfurtGermany
  2. 2.Department of Haematology and OncologyGoethe University Hospital FrankfurtFrankfurtGermany

Personalised recommendations