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British Society for Echocardiography and British Cardio-Oncology Society guideline for transthoracic echocardiographic assessment of adult cancer patients receiving anthracyclines and/or trastuzumab

Guidelines and Recommendations

Abstract

The subspecialty of cardio-oncology aims to reduce cardiovascular morbidity and mortality in patients with cancer or following cancer treatment. Cancer therapy can lead to a variety of cardiovascular complications, including left ventricular systolic dysfunction, pericardial disease, and valvular heart disease. Echocardiography is a key diagnostic imaging tool in the diagnosis and surveillance for many of these complications. The baseline assessment and subsequent surveillance of patients undergoing treatment with anthracyclines and/or human epidermal growth factor (EGF) receptor (HER) 2-positive targeted treatment (e.g. trastuzumab and pertuzumab) form a significant proportion of cardio-oncology patients undergoing echocardiography. This guideline from the British Society of Echocardiography and British Cardio-Oncology Society outlines a protocol for baseline and surveillance echocardiography of patients undergoing treatment with anthracyclines and/or trastuzumab. The methodology for acquisition of images and the advantages and disadvantages of techniques are discussed. Echocardiographic definitions for considering cancer therapeutics-related cardiac dysfunction are also presented.

References

  1. Barros-Gomes S, Herrmann J, Mulvagh SL, Lerman A, Lin G, Villarraga HR. Rationale for setting up a cardio-oncology unit: our experience at Mayo Clinic. Cardio-Oncology 2016 2 5. (https://doi.org/10.1186/s40959-016-0014-2)

  2. Ghosh AK, Walker JM. Cardio-oncology–a new subspecialty with collaboration at its heart. Indian Heart Journal 2017 69 556–562. (https://doi.org/10.1016/j.ihj.2017.05.006)

    PubMed  PubMed Central  Article  Google Scholar 

  3. Robinson S, Rana B, Oxborough D, Steeds R, Monaghan M, Stout M, Pearce K, Harkness A, Ring L, Paton M.et al. A practical guideline for performing a comprehensive transthoracic echocardiogram in adults: the British Society of Echocardiography minimum dataset. Echo Research and Practice 2020 7 G59–G93. (https://doi.org/10.1530/ERP-20-0026)

    PubMed  PubMed Central  Article  Google Scholar 

  4. Chang HM, Moudgil R, Scarabelli T, Okwuosa TM, Yeh ETH. Cardiovascular complications of cancer therapy: best practices in diagnosis, prevention, and management: Part 1. Journal of the American College of Cardiology 2017 70 2536–2551. (https://doi.org/10.1016/j.jacc.2017.09.1096)

    PubMed  PubMed Central  Article  Google Scholar 

  5. Sendur MAN, Aksoy S, Altundag K. Pertuzumab-induced cardiotoxicity: safety compared with trastuzumab. Future Oncology 2015 11 13–15. (https://doi.org/10.2217/fon.14.184)

    CAS  PubMed  Article  Google Scholar 

  6. Han X, Zhou Y, Liu W. Precision cardio-oncology: understanding the cardiotoxicity of cancer therapy. NPJ Precision Oncology 2017 1 31. (https://doi.org/10.1038/s41698-017-0034-x)

  7. Odiete O, Hill MF, Sawyer DB. Neuregulin in cardiovascular development and disease. Circulation Research 2012 111 1376–1385. (https://doi.org/10.1161/CIRCRESAHA.112.267286)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 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. Journal of Clinical Oncology 2005 23 7820–7826. (https://doi.org/10.1200/JCO.2005.13.300)

    CAS  PubMed  Article  Google Scholar 

  9. 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. European Journal of Heart Failure 2011 13 1–10. (https://doi.org/10.1093/eurjhf/hfq213)

    PubMed  Article  Google Scholar 

  10. Zamorano JL, Lancellotti P, Rodriguez Muñoz D, Aboyans V, Asteggiano R, Galderisi M, Habib G, Lenihan DJ, Lip GYH, Lyon AR. 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). European Heart Journal 2016 37 2768–2801. (https://doi.org/10.1093/eurheartj/ehw211)

    PubMed  Article  Google Scholar 

  11. Gudmundsdottir T, Winther JF, de Fine Licht S, Bonnesen TG, Asdahl PH, Tryggvadottir L, Anderson H, Wesenberg F, Malila N, Hasle H. et al. Cardiovascular disease in adult life after childhood cancer in Scandinavia: a population-based cohort study of 32,308 one-year survivors. International Journal of Cancer 2015 137 1176–1186. (https://doi.org/10.1002/ijc.29468)

    CAS  PubMed  Article  Google Scholar 

  12. Yu AF, Flynn JR, Moskowitz CS, Scott JM, Oeffinger KC, Dang CT, Liu JE, Jones LW, Steingart RM. Long-term cardiopulmonary consequences of treatment-induced cardiotoxicity in survivors of ERBB2-positive breast cancer. JAMA Cardiology 2020 5 309–317. (https://doi.org/10.1001/jamacardio.2019.5586)

    PubMed  PubMed Central  Article  Google Scholar 

  13. Thavendiranathan P, Grant AD, Negishi T, Plana JC, Popović ZB, Marwick TH. Reproducibility of echocardiographic techniques for sequential assessment of left ventricular ejection fraction and volumes: application to patients undergoing cancer chemotherapy. Journal of the American College of Cardiology 2013 61 77–84. (https://doi.org/10.1016/j.jacc.2012.09.035)

    PubMed  Article  Google Scholar 

  14. Lyon AR, Dent S, Stanway S, Earl H, Brezden-Masley C, Cohen-Solal A, Tocchetti CG, Moslehi JJ, Groarke JD, Bergler-Klein J. et al. Baseline cardiovascular risk assessment in cancer patients scheduled to receive cardiotoxic cancer therapies: a position statement and new risk assessment tools from the Cardio-Oncology Study Group of the Heart Failure Association of the European Society of Cardiology in collaboration with the International Cardio-Oncology Society. European Journal of Heart Failure 2020 22 1945–1960. (https://doi.org/10.1002/ejhf.1920)

    PubMed  Article  Google Scholar 

  15. Čelutkienė J, Pudil R, López-Fernández T. et al. Role of cardiovascular imaging in cancer patients receiving cardiotoxic therapies: a position statement on behalf of the Heart Failure Association (HFA), the European Association of Cardiovascular Imaging (EACVI) and the Cardio-Oncology Council of the European Society of Cardiology (ESC). European Journal of Heart Failure 2020 22 1504–1524.

    PubMed  Article  CAS  Google Scholar 

  16. Armenian SH, Lacchetti C, Barac A, Carver J, Constine LS, Denduluri N, Dent S, Douglas PS, Durand JB, Ewer M. et al. Prevention and monitoring of cardiac dysfunction in survivors of adult cancers: American Society of Clinical Oncology Clinical Practice Guideline. Journal of Clinical Oncology 2017 35 893–911. (https://doi.org/10.1200/JCO.2016.70.5400)

    PubMed  Article  Google Scholar 

  17. Calvillo-Argüelles O, Abdel-Qadir H, Ky B, Liu JE, Lopez-Mattei JC, Amir E, Thavendiranathan P. Modified routine cardiac imaging surveillance of adult cancer patients and survivors during the COVID-19 pandemic. JACC: Cardio-Oncology 2020 2 345–349. (https://doi.org/10.1016/j.jaccao.2020.04.001)

    Google Scholar 

  18. Addison D, Campbell CM, Guha A, Ghosh AK, Dent SF, Jneid H. Cardio-oncology in the era of the COVID-19 pandemic and beyond. Journal of the American Heart Association 2020 9 e017787. (https://doi.org/10.1161/JAHA.120.017787)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Chung R, Ghosh AK, Banerjee A. Cardiotoxicity: precision medicine with imprecise definitions. Open Heart 2018 5 e000774. (https://doi.org/10.1136/openhrt-2018-000774)

    PubMed  PubMed Central  Article  Google Scholar 

  20. Liu J, Banchs J, Mousavi N, Plana JC, Scherrer-Crosbie M, Thavendiranathan P, Barac A. Contemporary role of echocardiography for clinical decision making in patients during and after cancer therapy. JACC: Cardiovascular Imaging 2018 11 1122–1131. (https://doi.org/10.1016/j.jcmg.2018.03.025)

    PubMed  Google Scholar 

  21. Curigliano G, Cardinale D, Suter T, Plataniotis G, de Azambuja E, Sandri MT, Criscitiello C, Goldhirsch A, Cipolla C, Roila F. et al. Cardiovascular toxicity induced by chemotherapy, targeted agents and radiotherapy: ESMO clinical practice guidelines. Annals of Oncology 2012 23 (Supplement 7) vii155–vii166. (https://doi.org/10.1093/annonc/mds293)

    PubMed  Article  Google Scholar 

  22. Dang CT, Yu AF, Jones LW, Liu J, Steingart RM, Argolo DF, Norton L, Hudis CA. Cardiac surveillance guidelines for trastuzumab-containing therapy in early-stage breast cancer: getting to the heart of the matter. Journal of Clinical Oncology 2016 34 1030–1033. (https://doi.org/10.1200/JCO.2015.64.5515)

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. Chavez-MacGregor M, Niu J, Zhang N, Elting LS, Smith BD, Banchs J, Hortobagyi GN, Giordano SH. Cardiac monitoring during adjuvant trastuzumab-based chemotherapy among older patients with breast cancer. Journal of Clinical Oncology 2015 33 2176–2183. (https://doi.org/10.1200/JCO.2014.58.9465)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Lynce F, Barac A, Geng X, Dang C, Yu AF, Smith KL, Gallagher C, Pohlmann PR, Nunes R, Herbolsheimer P. et al. Prospective evaluation of the cardiac safety of HER2-targeted therapies in patients with HER2-positive breast cancer and compromised heart function: the SAFE-HEaRt study. Breast Cancer Research and Treatment 2019 175 595–603. (https://doi.org/10.1007/s10549-019-05191-2)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. Leong DP, Cosman T, Alhussein MM, Kumar Tyagi N, Karampatos S, Barron CC, Wright D, Tandon V, Magloire P, Joseph P. et al. Safety of continuing trastuzumab despite mild cardiotoxicity. JACC: Cardio-Oncology 2019 1 1–10. (https://doi.org/10.1016/j.jaccao.2019.06.004)

    Google Scholar 

  26. Curigliano G, Lenihan D, Fradley M, Ganatra S, Barac A, Blaes A, Herrmann J, Porter C, Lyon AR, Lancellotti P. et al. Management of cardiac disease in cancer patients throughout oncological treatment: ESMO consensus recommendations. Annals of Oncology 2020 31 171–190. (https://doi.org/10.1016/j.annonc.2019.10.023)

    CAS  PubMed  Article  Google Scholar 

  27. Harkness A, Ring L, Augustine DX, Oxborough D, Robinson S, Sharma V.Education Committee of the British Society of Echocardiography. Normal reference intervals for cardiac dimensions and function for use in echocardiographic practice: a guideline from the British Society of Echocardiography. Echo Research and Practice 2020 7 G1–G18.

    PubMed  PubMed Central  Article  Google Scholar 

  28. Santoro C, Arpino G, Esposito R, Lembo M, Paciolla I, Cardalesi C, de Simone G, Trimarco B, De Placido S, Galderisi M. 2D and 3D strain for detection of subclinical anthracycline cardiotoxicity in breast cancer patients: a balance with feasibility. European Heart Journal Cardiovascular Imaging 2017 18 930–936. (https://doi.org/10.1093/ehjci/jex033)

    PubMed  Article  Google Scholar 

  29. Zhang KW, Finkelman BS, Gulati G, Narayan HK, Upshaw J, Narayan V, Plappert T, Englefield V, Smith AM, Zhang C. et al. Abnormalities in 3-dimensional left ventricular mechanics with anthracycline chemotherapy are associated with systolic and diastolic dysfunction. JACC: Cardiovascular Imaging 2018 11 1059–1068. (https://doi.org/10.1016/j.jcmg.2018.01.015)

    PubMed  Google Scholar 

  30. Yang H, Wright L, Negishi T, Negishi K, Liu J, Marwick TH. Research to practice: assessment of left ventricular global longitudinal strain for surveillance of cancer chemotherapeutic-related cardiac dysfunction. JACC: Cardiovascular Imaging 2018 11 1196–1201. (https://doi.org/10.1016/j.jcmg.2018.07.005)

    PubMed  Google Scholar 

  31. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T. et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. European Heart Journal Cardiovascular Imaging 2015 16 233–270. (https://doi.org/10.1093/ehjci/jev014)

    PubMed  Article  Google Scholar 

  32. Asch FM, Miyoshi T, Addetia K, Citro R, Daimon M, Desale S, Fajardo PG, Kasliwal RR, Kirkpatrick JN, Monaghan MJ. et al. Similarities and differences in left ventricular size and function among races and nationalities: results of the World Alliance Societies of Echocardiography normal values study. Journal of the American Society of Echocardiography 2019 32 1396.e2–1406.e2. (https://doi.org/10.1016/j.echo.2019.08.012)

    Google Scholar 

  33. Plana JC, Galderisi M, Barac A, Ewer MS, Ky B, Scherrer-Crosbie M, Ganame J, Sebag IA, Agler DA, Badano LP. 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. European Heart Journal Cardiovascular Imaging 2014 15 1063–1093. (https://doi.org/10.1093/ehjci/jeu192)

    PubMed  PubMed Central  Article  Google Scholar 

  34. Thavendiranathan P, Negishi T, Somerset E, Negishi K, Penicka M, Lemieux J, Aakhus S, Miyazaki S, Shirazi M, Galderisi M. et al. Strain-guided management of potentially cardiotoxic cancer therapy. Journal of the American College of Cardiology 2021 77 392–401. (https://doi.org/10.1016/j.jacc.2020.11.020)

    CAS  PubMed  Article  Google Scholar 

  35. 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. Journal of the American College of Cardiology 2014 63 2751–2768. (https://doi.org/10.1016/j.jacc.2014.01.073)

    PubMed  Article  Google Scholar 

  36. Kang Y, Xu X, Cheng L, Li L, Sun M, Chen H, Pan C, Shu X. Two-dimensional speckle tracking echocardiography combined with high-sensitive cardiac troponin T in early detection and prediction of cardiotoxicity during epirubicine-based chemotherapy. European Journal of Heart Failure 2014 16 300–308. (https://doi.org/10.1002/ejhf.8)

    CAS  PubMed  Article  Google Scholar 

  37. Mousavi N, Tan TC, Ali M, Halpern EF, Wang L, Scherrer-Crosbie M. Echocardiographic parameters of left ventricular size and function as predictors of symptomatic heart failure in patients with a left ventricular ejection fraction of 50–59% treated with anthracyclines. European Heart Journal Cardiovascular Imaging 2015 16 977–984. (https://doi.org/10.1093/ehjci/jev113)

    PubMed  Google Scholar 

  38. Liu JE, Barac A, Thavendiranathan P, Scherrer-Crosbie M. Strain imaging in cardio-oncology. JACC: CardioOncology 2020 2 677–689. (https://doi.org/10.1016/j.jaccao.2020.10.011)

    PubMed  PubMed Central  Google Scholar 

  39. Kotecha D, Mohamed M, Shantsila E, Popescu BA, Steeds RP. Is echocardiography valid and reproducible in patients with atrial fibrillation? A systematic review. Europace 2017 19 1427–1438. (https://doi.org/10.1093/europace/eux027)

    PubMed  PubMed Central  Article  Google Scholar 

  40. Liu H, Wang J, Pan Y, Ge Y, Guo Z, Zhao S. Early and quantitative assessment of myocardial deformation in essential hypertension patients by using cardiovascular magnetic resonance feature tracking. Scientific Reports 2020 10 1–9.

    Article  CAS  Google Scholar 

  41. Otterstad JE, Froeland G, St John Sutton M, Holme I. Accuracy and reproducibility of biplane two-dimensional echocardiographic measurements of left ventricular dimensions and function. European Heart Journal 1997 18 507–513. (https://doi.org/10.1093/oxfordjournals.eurheartj.a015273)

    CAS  PubMed  Article  Google Scholar 

  42. Muraru D, Cecchetto A, Cucchini U, Zhou X, Lang RM, Romeo G, Vannan M, Mihaila S, Miglioranza MH, Iliceto S. et al. Intervendor consistency and accuracy of left ventricular volume measurements using three-dimensional echocardiography. Journal of the American Society of Echocardiography 2018 31 158.e1–168.e1. (https://doi.org/10.1016/j.echo.2017.10.010)

    Article  Google Scholar 

  43. Wood PW, Choy JB, Nanda NC, Becher H. Left ventricular ejection fraction and volumes: it depends on the imaging method. Echocardiography 2014 31 87–100. (https://doi.org/10.1111/echo.12331)

    PubMed  Article  Google Scholar 

  44. Spitzer E, Ren B, Zijlstra F, Van Miegham NMV, Geleijnse ML. The role of automated 3D echocardiography for left ventricular ejection fraction assessment. Cardiac Failure Review 2017 3 97–101. (https://doi.org/10.15420/cfr.2017:14.1)

    PubMed  PubMed Central  Article  Google Scholar 

  45. Senior R, Becher H, Monaghan M, Agati L, Zamorano J, Vanoverschelde JL, Nihoyannopoulos P, Edvardsen T, Lancellotti P. EACVI Scientific Documents Committee for 2014–16 and 2016–18, et al. Clinical Practice of Contrast Echocardiography: recommendation by the European Association of Cardiovascular Imaging (EACVI) 2017. European Heart Journal Cardiovascular Imaging 2017 18 1205–1205af. (https://doi.org/10.1093/ehjci/jex182)

  46. Suwatanaviroj T, He W, Pituskin E, Paterson I, Choy J, Becher H. What is the minimum change in left ventricular ejection fraction, which can be measured with contrast echocardiography? Echo Research and Practice 2018 5 71–77. (https://doi.org/10.1530/ERP-18-0003)

    PubMed  PubMed Central  Article  Google Scholar 

  47. Upshaw JN, Finkelman B, Hubbard RA, Smith AM, Narayan HK, Arndt L, Domchek S, DeMichele A, Fox K, Shah P. et al. Comprehensive assessment of changes in left ventricular diastolic function with contemporary breast cancer therapy. JACC: Cardiovascular Imaging 2020 13 198–210. (https://doi.org/10.1016/j.jcmg.2019.07.018)

    PubMed  Google Scholar 

  48. Mathew T, Steeds R, Jones R, Kanagala P, Lloyd G, Knight D, O’Gallagher K, Oxborough D, Rana B., Ring L. A Guideline Protocol for the Echocardiographic Assessment of Diastolic Dysfunction. British Society of Echocardiography, 2013. (available at: https://www.bsecho.org/Public/Education/Protocols-and-guidelines/Public/Education/Protocols-and-guidelines.aspx?hkey=75710d32-ef9f-4e7d-aa76-eb89a082829f)

    Google Scholar 

  49. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, Dokainish H, Edvardsen T, Flachskampf FA, Gillebert TC, Klein AL, Lancellotti P. et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Journal of the American Society of Echocardiography 2016 29 277–314. (https://doi.org/10.1016/j.echo.2016.01.011)

    PubMed  Article  Google Scholar 

  50. Abraham TP, Dimaano VL, Liang HY. Role of tissue Doppler and strain echocardiography in current clinical practice. Circulation 2007 116 2597–2609. (https://doi.org/10.1161/CIRCULATIONAHA.106.647172)

    PubMed  Article  Google Scholar 

  51. Marwick TH. Clinical applications of tissue Doppler imaging: a promise fulfilled. Heart 2003 89 1377–1378. (https://doi.org/10.1136/heart.89.12.1377)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. Johnson C, Kuyt K, Oxborough D, Stout M. Practical tips and tricks in measuring strain, strain rate and twist for the left and right ventricles. Echo Research and Practice 2019 6 R87–R98. (https://doi.org/10.1530/ERP-19-0020)

    PubMed  PubMed Central  Article  Google Scholar 

  53. King A, Thambyrajah J, Leng E, Stewart MJ. Global longitudinal strain: a useful everyday measurement? Echo Research and Practice 2016 3 85–93. (https://doi.org/10.1530/ERP-16-0022)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. Karlsen S, Dahlslett T, Grenne B, Sjøli B, Smiseth O, Edvardsen T, Brunvand H. Global longitudinal strain is a more reproducible measure of left ventricular function than ejection fraction regardless of echocardiographic training. Cardiovascular Ultrasound 2019 17 18. (https://doi.org/10.1186/s12947-019-0168-9)

  55. Mirea O, Pagourelias ED, Duchenne J, Bogaert J, Thomas JD, Badano LP, Voigt JU.EACVI-ASE-Industry Standardization Task Force. Variability and reproducibility of segmental longitudinal strain measurement: a report from the EACVI-ASE Strain Standardization Task Force. JACC: Cardiovascular Imaging 2018 11 15–24. (https://doi.org/10.1016/j.jcmg.2017.01.027)

    PubMed  Google Scholar 

  56. Shiino K, Yamada A, Ischenko M, Khandheria BK, Hudaverdi M, Speranza V, Harten M, Benjamin A, Hamilton-Craig CR, Platts DG. et al. Intervendor consistency and reproducibility of left ventricular 2D global and regional strain with two different high-end ultrasound systems. European Heart Journal Cardiovascular Imaging 2017 18 707–716. (https://doi.org/10.1093/ehjci/jew120)

    PubMed  Google Scholar 

  57. Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann R, Pedri S, Ito Y, Abe Y, Metz S. et al. Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/Ase/Industry Task Force to standardize deformation imaging. European Heart Journal Cardiovascular Imaging 2015 16 1–11. (https://doi.org/10.1093/ehjci/jeu184)

    CAS  PubMed  Article  Google Scholar 

  58. Tadic M, Cuspidi C, Hering D, Venneri L, Danylenko O. The influence of chemotherapy on the right ventricle: did we forget something? Clinical Cardiology 2017 40 437–443. (https://doi.org/10.1002/clc.22672)

    PubMed  PubMed Central  Article  Google Scholar 

  59. Zhao R, Shu F, Zhang C, Song F, Xu Y, Guo Y, Xue K, Lin J, Shu X, Hsi DH. et al. Early detection and prediction of anthracycline-induced right ventricular cardiotoxicity by 3-dimensional echocardiography. JACC: CardioOncology 2020 2 13–22. (https://doi.org/10.1016/j.jaccao.2020.01.007)

    PubMed  PubMed Central  Google Scholar 

  60. Zaidi A, Knight DS, Augustine DX, Harkness A, Oxborough D, Pearce K, Ring L, Robinson S, Stout M, Willis J. et al. Echocardiographic assessment of the right heart in adults: a practical guideline from the British Society of Echocardiography. Echo Research and Practice 2020 7 G19–G41. (https://doi.org/10.1530/ERP-19-0051)

    PubMed  PubMed Central  Article  Google Scholar 

  61. Augustine DX, Coates-Bradshaw LD, Willis J, Harkness A, Ring L, Grapsa J, Coghlan G, Kaye N, Oxborough D, Robinson S. et al. Echocardiographic assessment of pulmonary hypertension: a guideline protocol from the British Society of Echocardiography. Echo Research and Practice 2018 5 G11–G24. (https://doi.org/10.1530/ERP-17-0071)

    PubMed  PubMed Central  Article  Google Scholar 

  62. Plana JC, Thavendiranathan P, Bucciarelli-Ducci C, Lancellotti P. Multi-modality imaging in the assessment of cardiovascular toxicity in the cancer patient. JACC: Cardiovascular Imaging 2018 11 1173–1186. (https://doi.org/10.1016/j.jcmg.2018.06.003)

    PubMed  Google Scholar 

  63. Seraphim A, Westwood M, Bhuva AN, Crake T, Moon JC, Menezes LJ, Lloyd G, Ghosh AK, Slater S, Oakervee H. et al. Advanced imaging modalities to monitor for cardiotoxicity. Current Treatment Options in Oncology 2019 20 73. (https://doi.org/10.1007/s11864-019-0672-z)

  64. Moody WE, Edwards NC, Chue CD, Taylor RJ, Ferro CJ, Townend JN, Steeds RP. Variability in cardiac MR measurement of left ventricular ejection fraction, volumes and mass in healthy adults: defining a significant change at 1 year. British Journal of Radiology 2015 88 20140831. (https://doi.org/10.1259/bjr.20140831)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. Layoun ME, Yang EH, Herrmann J, Iliescu CA, Lopez-Mattei JC, Marmagkiolis K, Budoff MJ, Ferencik M. Applications of cardiac computed tomography in the cardio-oncology population. Current Treatment Options in Oncology 2019 20 47. (https://doi.org/10.1007/s11864-019-0645-2)

  66. Rosmini S, Aggarwal A, Chen DH, Conibear J, Davies CL, Dey AK, Edwards P, Guha A, Ghosh AK. Cardiac computed tomography in cardio-oncology: an update on recent clinical applications. European Heart Journal Cardiovascular Imaging 2021 [epub]. (https://doi.org/10.1093/ehjci/jeaa351)

    Google Scholar 

  67. Michel L, Rassaf T, Totzeck M. Biomarkers for the detection of apparent and subclinical cancer therapy-related cardiotoxicity. Journal of Thoracic Disease 2018 10 (Supplement 35) S4282–S4295. (https://doi.org/10.21037/jtd.2018.08.15)

    PubMed  PubMed Central  Article  Google Scholar 

  68. Cardinale D, Sandri MT, Colombo A, Colombo N, Boeri M, Lamantia G, Civelli M, Peccatori F, Martinelli G, Fiorentini C. et al. Prognostic value of troponin I in cardiac risk stratification of cancer patients undergoing high-dose chemotherapy. Circulation 2004 109 2749–2754. (https://doi.org/10.1161/01.CIR.0000130926.51766.CC)

    CAS  PubMed  Article  Google Scholar 

  69. Stachowiak P, Kornacewicz-Jach Z, Safranow K. Prognostic role of troponin and natriuretic peptides as biomarkers for deterioration of left ventricular ejection fraction after chemotherapy. Archives of Medical Science 2014 10 1007–1018. (https://doi.org/10.5114/aoms.2013.34987)

    PubMed  Article  Google Scholar 

  70. Cardinale D, Sandri MT, Martinoni A, Borghini E, Civelli M, Lamantia G, Cinieri S, Martinelli G, Fiorentini C, Cipolla CM. Myocardial injury revealed by plasma troponin I in breast cancer treated with high-dose chemotherapy. Annals of Oncology 2002 13 710–715. (https://doi.org/10.1093/annonc/mdf170)

    CAS  PubMed  Article  Google Scholar 

  71. Sandri MT, Salvatici M, Cardinale D, Zorzino L, Passerini R, Lentati P, Leon M, Civelli M, Martinelli G, Cipolla CM. N-terminal pro-B-type natriuretic peptide after high-dose chemotherapy: a marker predictive of cardiac dysfunction? Clinical Chemistry 2005 51 1405–1410. (https://doi.org/10.1373/clinchem.2005.050153)

    CAS  PubMed  Article  Google Scholar 

  72. Demissei BG, Hubbard RA, Zhang L, Smith AM, Sheline K, McDonald C, Narayan V, Domchek SM, DeMichele A, Shah P. et al. Changes in cardiovascular biomarkers with breast cancer therapy and associations with cardiac dysfunction. Journal of the American Heart Association 2020 9 e014708. (https://doi.org/10.1161/JAHA.119.014708)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Abdel-Qadir H, Thavendiranathan P, Austin PC, Lee DS, Amir E, Tu JV, Fung K, Anderson GM. Development and validation of a multivariable prediction model for major adverse cardiovascular events after early stage breast cancer: a population-based cohort study. European Heart Journal 2019 40 3913–3920. (https://doi.org/10.1093/eurheartj/ehz460)

    PubMed  Google Scholar 

  74. Lancellotti P, Suter TM, López-Fernández T, Galderisi M, Lyon AR, Van der Meer P, Cohen Solal A, Zamorano JL, Jerusalem G, Moonen M. et al. Cardio-oncology services: rationale, organization, and implementation. European Heart Journal 2019 40 1756–1763. (https://doi.org/10.1093/eurheartj/ehy453)

    PubMed  Article  Google Scholar 

  75. Ghosh AK, Walker JM. Cardio-oncology. British Journal of Hospital Medicine 2017 78 C11–C13. (https://doi.org/10.12968/hmed.2017.78.1.C11)

    PubMed  Article  Google Scholar 

  76. Cardinale D, Colombo A, Lamantia G, Colombo N, Civelli M, De Giacomi G, Rubino M, Veglia F, Fiorentini C, Cipolla CM. Anthracycline-induced cardiomyopathy. clinical relevance and response to pharmacologic therapy. Journal of the American College of Cardiology 2010 55 213–220. (https://doi.org/10.1016/j.jacc.2009.03.095)

    CAS  PubMed  Article  Google Scholar 

  77. Cardinale D, Colombo A, Bacchiani G, Tedeschi I, Meroni CA, Veglia F, Civelli M, Lamantia G, Colombo N, Curigliano G. et al. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation 2015 131 1981–1988. (https://doi.org/10.1161/CIRCULATIONAHA.114.013777)

    CAS  PubMed  Article  Google Scholar 

  78. Ponikowski P, Voors AA, Anker SD, Bueno H, Cleland JGF, Coats AJS, Falk V, González-Juanatey JR, Harjola VP, Jankowska EA. et al. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC). European Heart Journal 2016 37 2129–2200. (https://doi.org/10.1093/eurheartj/ehw128)

    PubMed  Article  Google Scholar 

  79. Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE, Colvin MM, Drazner MH, Filippatos GS, Fonarow GC, Givertz MM. et al. ACC/AHA/HFSA focused update of the 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Failure Society of America. Journal of the American College of Cardiology 2017 70 776–803. (https://doi.org/10.1016/j.jacc.2017.04.025)

    PubMed  Article  Google Scholar 

  80. Negishi K, Negishi T, Hare JL, Haluska BA, Plana JC, Marwick TH. Independent and incremental value of deformation indices for prediction of trastuzumab-induced cardiotoxicity. Journal of the American Society of Echocardiography 2013 26 493–498. (https://doi.org/10.1016/j.echo.2013.02.008)

    PubMed  Article  Google Scholar 

  81. Gulati G, Heck SL, Ree AH, Hoffmann P, Schulz-Menger J, Fagerland MW, Gravdehaug B, von Knobelsdorff-Brenkenhoff F, Bratland Å, Storås TH. 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. European Heart Journal 2016 37 1671–1680. (https://doi.org/10.1093/eurheartj/ehw022)

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  82. Pituskin E, Mackey JR, Koshman S, Jassal D, Pitz M, Haykowsky MJ, Pagano JJ, Chow K, Thompson RB, Vos LJ. et al. Multidisciplinary approach to novel therapies in cardio-oncology research (MANTICORE 101-Breast): a randomized trial for the prevention of trastuzumab-associated cardiotoxicity. Journal of Clinical Oncology 2017 35 870–877. (https://doi.org/10.1200/JCO.2016.68.7830)

    CAS  PubMed  Article  Google Scholar 

  83. Avila MS, Ayub-Ferreira SM, de Barros Wanderley MR, das Dores Cruz F, Gonçalves Brandão SM, Rigaud VOC, Higuchi-Dos-Santos MH, Hajjar LA, Kalil Filho R, Hoff PM. et al. Carvedilol for prevention of chemotherapy-related cardiotoxicity: the CECCY trial. Journal of the American College of Cardiology 2018 71 2281–2290. (https://doi.org/10.1016/j.jacc.2018.02.049)

    CAS  PubMed  Article  Google Scholar 

  84. Russo G, Cioffi G, Di Lenarda A, Tuccia F, Bovelli D, Di Tano G, Alunni G, Gori S, Faggiano P, Tarantini L. Role of renal function on the development of cardiotoxicity associated with trastuzumab-based adjuvant chemotherapy for early breast cancer. Internal and Emergency Medicine 2012 7 439–446. (https://doi.org/10.1007/s11739-012-0794-9)

    PubMed  Article  Google Scholar 

  85. Virani SA, Dent S, Brezden-Masley C, Clarke B, Davis MK, Jassal DS, Johnson C, Lemieux J, Paterson I, Sebag IA. et al. Canadian Cardiovascular Society guidelines for evaluation and management of cardiovascular complications of cancer therapy. Canadian Journal of Cardiology 2016 32 831–841. (https://doi.org/10.1016/j.cjca.2016.02.078)

    PubMed  Article  Google Scholar 

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Correspondence to Rebecca Dobson MBChB (Hons) MD.

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(R Dobson and A K Ghosh contributed equally to this work)

Anju Nohria, MD, served as the Editor-in-Chief for this paper. Juan Carlos Plana Gomez, MD, served as the Guest Associate Editor for this paper. The authors attest they are in compliance with human studies committees and animal welfare regulations of the authors’ institutions and Food and Drug

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Dobson, R., Ghosh, A.K., Ky, B. et al. British Society for Echocardiography and British Cardio-Oncology Society guideline for transthoracic echocardiographic assessment of adult cancer patients receiving anthracyclines and/or trastuzumab. Echo Res Pract 8, G1–G18 (2021). https://doi.org/10.1530/ERP-21-0001

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Keywords

  • anthracycline
  • echocardiography
  • guidelines
  • HER2 therapy
  • imaging