Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

Chemotherapy-Related Cardiac Dysfunction: Quantitative Cardiac Magnetic Resonance Image Parameters and Their Prognostic Implications

  • Jinhee Kim (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • Yoo Jin Hong (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • Kyunghwa Han (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • Jin Young Kim (Department of Radiology, Dongsan Medical Center, Keimyung University College of Medicine) ;
  • Hye-Jeong Lee (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • Jin Hur (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • Young Jin Kim (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine) ;
  • Byoung Wook Choi (Department of Radiology and Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine)
  • Received : 2022.10.28
  • Accepted : 2023.06.29
  • Published : 2023.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: To quantitatively analyze the cardiac magnetic resonance imaging (CMR) characteristics of chemotherapy-related cardiac dysfunction (CTRCD) and explore their prognostic value for major adverse cardiovascular events (MACE). Materials and Methods: A total of 145 patients (male:female = 76:69, mean age = 63.0 years) with cancer and heart failure who underwent CMR between January 2015 and January 2021 were included. CMR was performed using a 3T scanner (Siemens). Biventricular functions, native T1 T2, extracellular volume fraction (ECV) values, and late gadolinium enhancement (LGE) of the left ventricle (LV) were compared between those with and without CTRCD. These were compared between patients with mild-to-moderate CTRCD and those with severe CTRCD. Cox proportional hazard regression analysis was used to evaluate the association between the CMR parameters and MACE occurrence during follow-up in the CTRCD patients. Results: Among 145 patients, 61 had CTRCD and 84 did not have CTRCD. Native T1, ECV, and T2 were significantly higher in the CTRCD group (1336.9 ms, 32.5%, and 44.7 ms, respectively) than those in the non-CTRCD group (1303.4 ms, 30.5%, and 42.0 ms, respectively; P = 0.013, 0.010, and < 0.001, respectively). They were not significantly different between patients with mild-to-moderate and severe CTRCD. Indexed LV mass was significantly smaller in the CTRCD group (65.0 g/m2 vs. 78.9 g/mm2; P < 0.001). According to the multivariable Cox regression analysis, T2 (hazard ratio [HR]: 1.14, 95% confidence interval [CI]: 1.01-1.27; P = 0.028) and quantified LGE (HR: 1.07, 95% CI: 1.01-1.13; P = 0.021) were independently associated with MACE in the CTRCD patients. Conclusion: Quantitative parameters from CMR have the potential to evaluate myocardial changes in CTRCD. Increased T2 with reduced LV mass was demonstrated in CTRCD patients even before the development of severe cardiac dysfunction. T2 and quantified LGE may be independent prognostic factors for MACE in patients with CTRCD.

Keywords

Acknowledgement

This research was supported by a Basic Science Research Program through the National Research Foundation of Korea, funded by the Ministry of Science, Information and Communication Technology, and Future Planning (Grant Nos. NRF-2017R1A2B4009661, NRF-2020R1F1A1074983) and faculty research grant of Yonsei University College of Medicine (Grant No. 6-2020-0223).

References

  1. Dent SF, Kikuchi R, Kondapalli L, Ismail-Khan R, Brezden-Masley C, Barac A, et al. Optimizing cardiovascular health in patients with cancer: a practical review of risk assessment, monitoring, and prevention of cancer treatment-related cardiovascular toxicity. Am Soc Clin Oncol Educ Book 2020;40:1-15
  2. Yoon DW, Shin DW, Cho JH, Yang JH, Jeong SM, Han K, et al. Increased risk of coronary heart disease and stroke in lung cancer survivors: a Korean nationwide study of 20,458 patients. Lung Cancer 2019;136:115-121
  3. Liu D, Ma Z, Yang J, Zhao M, Ao H, Zheng X, et al. Prevalence and prognosis significance of cardiovascular disease in cancer patients: a population-based study. Aging (Albany NY) 2019;11:7948-7960
  4. Lyon AR, Lopez-Fernandez T, Couch LS, Asteggiano R, Aznar MC, Bergler-Klein J, et al. 2022 ESC Guidelines on cardiooncology developed in collaboration with the European Hematology Association (EHA), the European Society for Therapeutic Radiology and Oncology (ESTRO) and the International Cardio-Oncology Society (IC-OS): Developed by the task force on cardio-oncology of the European Society of Cardiology (ESC). Eur Heart J 2022;43:4229-4361
  5. Nolan MT, Lowenthal RM, Venn A, Marwick TH. Chemotherapy-related cardiomyopathy: a neglected aspect of cancer survivorship. Intern Med J 2014;44:939-950
  6. Perez IE, Taveras Alam S, Hernandez GA, Sancassani R. Cancer therapy-related cardiac dysfunction: an overview for the clinician. Clin Med Insights Cardiol 2019;13:1179546819866445
  7. 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 2014;27:911-939
  8. Rabbat MG, Kwong RY, Heitner JF, Young AA, Shanbhag SM, Petersen SE, et al. The future of cardiac magnetic resonance clinical trials. JACC Cardiovasc Imaging 2022;15:2127-2138
  9. Altaha MA, Nolan M, Marwick TH, Somerset E, Houbois C, Amir E, et al. Can quantitative CMR tissue characterization adequately identify cardiotoxicity during chemotherapy?: Impact of temporal and observer variability. JACC Cardiovasc Imaging 2020;13:951-962
  10. Park HS, Hong YJ, Han K, Kim PK, An E, Lee JY, et al. Ultrahigh-field cardiovascular magnetic resonance T1 and T2 mapping for the assessment of anthracycline-induced cardiotoxicity in rat models: validation against histopathologic changes. J Cardiovasc Magn Reson 2021;23:76
  11. Naresh NK, Misener S, Zhang Z, Yang C, Ruh A, Bertolino N, et al. Cardiac MRI myocardial functional and tissue characterization detects early cardiac dysfunction in a mouse model of chemotherapy-induced cardiotoxicity. NMR Biomed 2020;33:e4327
  12. Heidenreich PA, Bozkurt B, Aguilar D, Allen LA, Byun JJ, Colvin MM, et al. 2022 AHA/ACC/HFSA guideline for the management of heart failure: executive summary: a report of the American College of Cardiology/American Heart Association Joint Committee on clinical practice cuidelines. J Am Coll Cardiol 2022;79:1757-1780
  13. Lam CSP, Solomon SD. Classification of heart failure according to ejection fraction: JACC review topic of the week. J Am Coll Cardiol 2021;77:3217-3225
  14. Petersen SE, Aung N, Sanghvi MM, Zemrak F, Fung K, Paiva JM, et al. Reference ranges for cardiac structure and function using cardiovascular magnetic resonance (CMR) in Caucasians from the UK Biobank population cohort. J Cardiovasc Magn Reson 2017;19:18
  15. Armstrong AC, Gidding S, Gjesdal O, Wu C, Bluemke DA, Lima JA. LV mass assessed by echocardiography and CMR, cardiovascular outcomes, and medical practice. JACC Cardiovasc Imaging 2012;5:837-848
  16. Youn JC, Hong YJ, Lee HJ, Han K, Shim CY, Hong GR, et al. Contrast-enhanced T1 mapping-based extracellular volume fraction independently predicts clinical outcome in patients with non-ischemic dilated cardiomyopathy: a prospective cohort study. Eur Radiol 2017;27:3924-3933
  17. Park EA, Lee W, Kim HK, Chung JW. Effect of papillary muscles and trabeculae on left ventricular measurement using cardiovascular magnetic resonance imaging in patients with hypertrophic cardiomyopathy. Korean J Radiol 2015;16:4-12
  18. Cadour F, Cautela J, Rapacchi S, Varoquaux A, Habert P, Arnaud F, et al. Cardiac MRI features and prognostic value in immune checkpoint inhibitor-induced myocarditis. Radiology 2022;303:512-521
  19. Zhao SH, Yun H, Chen CZ, Chen YY, Lin JY, Zeng MS, et al. The prognostic value of global myocardium strain by CMR-feature tracking in immune checkpoint inhibitor-associated myocarditis. Eur Radiol 2022;32:7657-7667
  20. Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 2016;15:155-163
  21. Hong YJ, Park HS, Park JK, Han K, Park CH, Kim TK, et al. Early detection and serial monitoring of anthracycline-induced cardiotoxicity using T1-mapping cardiac magnetic resonance imaging: an animal study. Sci Rep 2017;7:2663
  22. Galan-Arriola C, Lobo M, Vilchez-Tschischke JP, Lopez GJ, de Molina-Iracheta A, Perez-Martinez C, et al. Serial magnetic resonance imaging to identify early stages of anthracycline-induced cardiotoxicity. J Am Coll Cardiol 2019;73:779-791
  23. O'Brien AT, Gil KE, Varghese J, Simonetti OP, Zareba KM. T2 mapping in myocardial disease: a comprehensive review. J Cardiovasc Magn Reson 2022;24:33
  24. Chaikriangkrai K, Abbasi MA, Sarnari R, Dolan R, Lee D, Anderson AS, et al. Prognostic value of myocardial extracellular volume fraction and T2-mapping in heart transplant patients. JACC Cardiovasc Imaging 2020;13:1521-1530
  25. Xu Y, Li W, Wan K, Liang Y, Jiang X, Wang J, et al. Myocardial tissue reverse remodeling after guideline-directed medical therapy in idiopathic dilated cardiomyopathy. Circ Heart Fail 2021;14:e007944
  26. Terui Y, Sugimura K, Ota H, Tada H, Nochioka K, Sato H, et al. Usefulness of cardiac magnetic resonance for early detection of cancer therapeutics-related cardiac dysfunction in breast cancer patients. Int J Cardiol 2023;371:472-479
  27. 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;5:620-629
  28. Cuspidi C, Sala C, Negri F, Mancia G, Morganti A; Italian Society of Hypertension. Prevalence of left-ventricular hypertrophy in hypertension: an updated review of echocardiographic studies. J Hum Hypertens 2012;26:343-349
  29. Marketou ME, Parthenakis F, Vardas PE. Pathological left ventricular hypertrophy and stem cells: current evidence and new perspectives. Stem Cells Int 2016;2016:5720758
  30. Garg S, de Lemos JA, Matulevicius SA, Ayers C, Pandey A, Neeland IJ, et al. Association of concentric left ventricular hypertrophy with subsequent change in left ventricular enddiastolic volume: the Dallas Heart Study. Circ Heart Fail 2017;10:e003959
  31. Ferreira de Souza T, Quinaglia A C Silva T, Osorio Costa F, Shah R, Neilan TG, Velloso L, et al. Anthracycline therapy is associated with cardiomyocyte atrophy and preclinical manifestations of heart disease. JACC Cardiovasc Imaging 2018;11:1045-1055
  32. Jordan JH, Castellino SM, Melendez GC, Klepin HD, Ellis LR, Lamar Z, et al. Left ventricular mass change after anthracycline chemotherapy. Circ Heart Fail 2018;11:e004560 
  33. 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;110:1679-1686
  34. Assomull RG, Prasad SK, Lyne J, Smith G, Burman ED, Khan M, et al. Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy. J Am Coll Cardiol 2006;48:1977-1985
  35. Cau R, Bassareo P, Cherchi V, Palmisano V, Suri JS, Porcu M, et al. Early diagnosis of chemotherapy-induced cardiotoxicity by cardiac MRI. Eur J Radiol 2020;130:109158
  36. Harries I, Biglino G, Baritussio A, De Garate E, Dastidar A, Plana JC, et al. Long term cardiovascular magnetic resonance phenotyping of anthracycline cardiomyopathy. Int J Cardiol 2019;292:248-252
  37. Cardinale D, Iacopo F, Cipolla CM. Cardiotoxicity of anthracyclines. Front Cardiovasc Med 2020;7:26
  38. Kamphuis JAM, Linschoten M, Cramer MJ, Doevendans PA, Asselbergs FW, Teske AJ. Early- and late anthracycline-induced cardiac dysfunction: echocardiographic characterization and response to heart failure therapy. Cardiooncology 2020;6:23