Characterization of the changes in cardiac structure and function in mice treated with anthracyclines using serial cardiac magnetic resonance imaging

Circulation: Cardiovascular Imaging

Volumn 9, Issue 12, 2016, Pages

  Farhad, Hoshang ^a   Staziaki, Pedro V ^c   Addison, Daniel ^c   Coelho Filho, Otavio R ^b   Shah, Ravi V ^a   Mitchell, Richard N ^a   Szilveszter, Balint ^c   Abbasi, Siddique A ^a   Kwong, Raymond Y ^a   Scherrer Crosbie, Marielle ^c   Hoffmann, Udo ^c   Jerosch Herold, Michael ^a   Neilan, Tomas G ^c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

anthracyclines; cardiotoxicity; doxorubicin; magnetic resonance imaging; myocardium

Indexed keywords

COLLAGEN; DOXORUBICIN; PLACEBO;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE; CARDIOTOXICITY; CARDIOVASCULAR MAGNETIC RESONANCE; CARDIOVASCULAR PARAMETERS; CONTROLLED STUDY; HEART EDEMA; HEART FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE MASS; HEART LEFT VENTRICLE VOLUME; HEART MUSCLE FIBROSIS; HEART WEIGHT; HISTOPATHOLOGY; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DIAGNOSTIC IMAGING; DISEASE MODEL; FIBROSIS; HEART DISEASE; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; HEART VENTRICLE REMODELING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PREDICTIVE VALUE; TIME FACTOR;

ANIMALS; CARDIOTOXICITY; DISEASE MODELS, ANIMAL; DOXORUBICIN; EDEMA, CARDIAC; FIBROSIS; HEART DISEASES; MAGNETIC RESONANCE IMAGING; MALE; MICE, INBRED C57BL; MYOCARDIUM; PREDICTIVE VALUE OF TESTS; STROKE VOLUME; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 85007049708     PISSN: 19419651     EISSN: 19420080     Source Type: Journal    
DOI: 10.1161/CIRCIMAGING.115.003584     Document Type: Article

References (48)

1. Lipshultz SE, Colan SD, Gelber RD, Perez-Atayde AR, Sallan SE, Sanders SP, Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood. N Engl J Med 1991 324 808 815. doi: 10.1056/NEJM199103213241205.
2. Bosch X, Rovira M, Sitges M, Domènech A, Ortiz-Pérez JT, de Caralt TM, Morales-Ruiz M, Perea RJ, Monzó M, Esteve J, Enalapril and carvedilol for preventing chemotherapy-induced left ventricular systolic dysfunction in patients with malignant hemopathies: the OVERCOME trial (preventiOn of left Ventricular dysfunction with Enalapril and caRvedilol in patients submitted to intensive ChemOtherapy for the treatment of Malignant hEmopathies). J Am Coll Cardiol 2013 61 2355 2362. doi: 10.1016/j.jacc.2013.02.072.
3. Limat S, Demesmay K, Voillat L, Bernard Y, Deconinck E, Brion A, Sabbah A, Woronoff-Lemsi MC, Cahn JY, Early cardiotoxicity of the CHOP regimen in aggressive non-Hodgkin's lymphoma. Ann Oncol 2003 14 277 281
4. Jensen BV, Skovsgaard T, Nielsen SL, Functional monitoring of anthracycline cardiotoxicity: a prospective, blinded, long-Term observational study of outcome in 120 patients. Ann Oncol 2002 13 699 709
5. Felker GM, Thompson RE, Hare JM, Hruban RH, Clemetson DE, Howard DL, Baughman KL, Kasper EK, Underlying causes and long-Term survival in patients with initially unexplained cardiomyopathy. N Engl J Med 2000 342 1077 1084. doi: 10.1056/NEJM200004133421502.
6. Henderson IC, Allegra JC, Woodcock T, Wolff S, Bryan S, Cartwright K, Dukart G, Henry D, Randomized clinical trial comparing mitoxantrone with doxorubicin in previously treated patients with metastatic breast cancer. J Clin Oncol 1989 7 560 571. doi: 10.1200/jco.1989.7.5.560.
7. Feher O, Vodvarka P, Jassem J, Morack G, Advani SH, Khoo KS, Doval DC, Ermisch S, Roychowdhury D, Miller MA, von Minckwitz G, First-line gemcitabine versus epirubicin in postmenopausal women aged 60 or older with metastatic breast cancer: a multicenter, randomized, phase III study. Ann Oncol 2005 16 899 908. doi: 10.1093/annonc/mdi181.
8. Ewer MS, Ali MK, Mackay B, Wallace S, Valdivieso M, Legha SS, Benjamin RS, Haynie TP, A comparison of cardiac biopsy grades and ejection fraction estimations in patients receiving Adriamycin. J Clin Oncol 1984 2 112 117. doi: 10.1200/jco.1984.2.2.112.
9. Cardinale D, Sandri MT, Martinoni A, Tricca A, Civelli M, Lamantia G, Cinieri S, Martinelli G, Cipolla CM, Fiorentini C, Left ventricular dysfunction predicted by early troponin I release after high-dose chemotherapy. J Am Coll Cardiol 2000 36 517 522
10. 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. J Am Coll Cardiol 2010 55 213 220. doi: 10.1016/j.jacc.2009.03.095.
11. Lefrak EA, Pitha J, Rosenheim S, Gottlieb JA, A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer 1973 32 302 314
12. Billingham ME, Mason JW, Bristow MR, Daniels JR, Anthracycline cardiomyopathy monitored by morphologic changes. Cancer Treat Rep 1978 62 865 872
13. Ferrans VJ, Overview of cardiac pathology in relation to anthracycline cardiotoxicity. Cancer Treat Rep 1978 62 955 961
14. Unverferth DV, Fetters JK, Unverferth BJ, Leier CV, Magorien RD, Arn AR, Baker PB, Human myocardial histologic characteristics in congestive heart failure. Circulation 1983 68 1194 1200
15. Lightfoot JC, D'Agostino RB Jr, Hamilton CA, Jordan J, Torti FM, Kock ND, Jordan J, Workman S, Hundley WG, Novel approach to early detection of doxorubicin cardiotoxicity by gadolinium-enhanced cardiovascular magnetic resonance Imaging in an experimental model. Circ Cardiovasc Imaging 2010 3 550 558. doi: 10.1161/CIRCIMAGING.109.918540.
16. Neilan TG, Jassal DS, Perez-Sanz TM, Raher MJ, Pradhan AD, Buys ES, Ichinose F, Bayne DB, Halpern EF, Weyman AE, Derumeaux G, Bloch KD, Picard MH, Scherrer-Crosbie M, Tissue Doppler Imaging predicts left ventricular dysfunction and mortality in a murine model of cardiac injury. Eur Heart J 2006 27 1868 1875. doi: 10.1093/eurheartj/ehl013.
17. Neilan TG, Coelho-Filho OR, Shah RV, Abbasi SA, Heydari B, Watanabe E, Chen Y, Mandry D, Pierre-Mongeon F, Blankstein R, Kwong RY, Jerosch-Herold M, Myocardial extracellular volume fraction from T1 measurements in healthy volunteers and mice: relationship to aging and cardiac dimensions. JACC Cardiovasc Imaging 2013 6 672 683. doi: 10.1016/j.jcmg.2012.09.020.
18. Coelho-Filho OR, Shah RV, Mitchell R, Neilan TG, Moreno H Jr, Simonson B, Kwong R, Rosenzweig A, Das S, Jerosch-Herold M, Quantification of cardiomyocyte hypertrophy by cardiac magnetic resonance: implications for early cardiac remodeling. Circulation 2013 128 1225 1233. doi: 10.1161/CIRCULATIONAHA.112.000438.
19. Coelho-Filho OR, Mongeon FP, Mitchell R, Moreno H Jr, Nadruz W Jr, Kwong R, Jerosch-Herold M, Role of transcytolemmal water-exchange in magnetic resonance measurements of diffuse myocardial fibrosis in hypertensive heart disease. Circ Cardiovasc Imaging 2013 6 134 141. doi: 10.1161/CIRCIMAGING.112.979815.
20. Abdel-Aty H, Cocker M, Meek C, Tyberg JV, Friedrich MG, Edema as a very early marker for acute myocardial ischemia: a cardiovascular magnetic resonance study. J Am Coll Cardiol 2009 53 1194 1201. doi: 10.1016/j.jacc.2008.10.065.
21. Milford D, Rosbach N, Bendszus M, Heiland S, Mono-exponential fitting in T2-relaxometry: relevance of offset and first echo. PLoS One 2015 10 e0145255. doi: 10.1371/journal.pone.0145255.
22. Neilan TG, Coelho-Filho OR, Shah RV, Feng JH, Pena-Herrera D, Mandry D, Pierre-Mongeon F, Heydari B, Francis SA, Moslehi J, Kwong RY, Jerosch-Herold M, Myocardial extracellular volume by cardiac magnetic resonance Imaging in patients treated with anthracycline-based chemotherapy. Am J Cardiol 2013 111 717 722. doi: 10.1016/j.amjcard.2012.11.022.
23. Friedman MA, Bozdech MJ, Billingham ME, Rider AK, Doxorubicin cardiotoxicity. Serial endomyocardial biopsies and systolic time intervals. JAMA 1978 240 1603 1606
24. Bernaba BN, Chan JB, Lai CK, Fishbein MC, Pathology of late-onset anthracycline cardiomyopathy. Cardiovasc Pathol 2010 19 308 311. doi: 10.1016/j.carpath.2009.07.004.
25. Zhao Y, McLaughlin D, Robinson E, Harvey AP, Hookham MB, Shah AM, McDermott BJ, Grieve DJ, Nox2 NADPH oxidase promotes pathologic cardiac remodeling associated with Doxorubicin chemotherapy. Cancer Res 2010 70 9287 9297. doi: 10.1158/0008-5472.CAN-10-2664.
26. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, White JA, Abdel-Aty H, Gutberlet M, Prasad S, Aletras A, Laissy JP, Paterson I, Filipchuk NG, Kumar A, Pauschinger M, Liu P, International Consensus Group on Cardiovascular Magnetic Resonance in Myocarditis Cardiovascular magnetic resonance in myocarditis: A JACC White Paper. J Am Coll Cardiol 2009 53 1475 1487. doi: 10.1016/j.jacc.2009.02.007.
27. Hendel RC, Patel MR, Kramer CM, Poon M, Hendel RC, Carr JC, Gerstad NA, Gillam LD, Hodgson JM, Kim RJ, Kramer CM, Lesser JR, Martin ET, Messer JV, Redberg RF, Rubin GD, Rumsfeld JS, Taylor AJ, Weigold WG, Woodard PK, Brindis RG, Hendel RC, Douglas PS, Peterson ED, Wolk MJ, Allen JM, Patel MR, 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 1497
28. Abdel-Aty H, Boyé P, Zagrosek A, Wassmuth R, Kumar A, Messroghli D, Bock P, Dietz R, Friedrich MG, Schulz-Menger J, Diagnostic performance of cardiovascular magnetic resonance in patients with suspected acute myocarditis: comparison of different approaches. J Am Coll Cardiol 2005 45 1815 1822. doi: 10.1016/j.jacc.2004.11.069.
29. Wassmuth R, Lentzsch S, Erdbruegger U, Schulz-Menger J, Doerken B, Dietz R, Friedrich MG, Subclinical cardiotoxic effects of anthracyclines as assessed by magnetic resonance Imaging-A pilot study. Am Heart J 2001 141 1007 1013. doi: 10.1067/mhj.2001.115436.
30. Doroshow JH, Tallent C, Schechter JE, Ultrastructural features of Adriamycin-induced skeletal and cardiac muscle toxicity. Am J Pathol 1985 118 288 297
31. Fedrigo M, Perazzolo M, Frigo A, Cacciavillani L, Corbetti F, Zilio F, Tarantini F, Tona F, Iliceto S, Gambino A, Gerosa G, Thiene G, Angelini A, Abstract 402: Myocardial fibrosis in dilated cardiomyopathy: comparison between magnetic resonance and histological findings. Circulation 2009;120 S335 336
32. Mewton N, Liu CY, Croisille P, Bluemke D, Lima JA, Assessment of myocardial fibrosis with cardiovascular magnetic resonance. J Am Coll Cardiol 2011 57 891 903. doi: 10.1016/j.jacc.2010.11.013.
33. Neilan TG, Mongeon FP, Shah RV, Coelho-Filho O, Abbasi SA, Dodson JA, McMullan CJ, Heydari B, Michaud GF, John RM, Blankstein R, Jerosch-Herold M, Kwong RY, Myocardial extracellular volume expansion and the risk of recurrent atrial fibrillation after pulmonary vein isolation. JACC Cardiovasc Imaging 2014 7 1 11. doi: 10.1016/j.jcmg.2013.08.013.
34. Ugander M, Oki AJ, Hsu LY, Kellman P, Greiser A, Aletras AH, Sibley CT, Chen MY, Bandettini WP, Arai AE, Extracellular volume Imaging by magnetic resonance Imaging provides insights into overt and sub-clinical myocardial pathology. Eur Heart J 2012 33 1268 1278. doi: 10.1093/eurheartj/ehr481.
35. Flett AS, Hayward MP, Ashworth MT, Hansen MS, Taylor AM, Elliott PM, McGregor C, Moon JC, Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation 2010 122 138 144. doi: 10.1161/CIRCULATIONAHA.109.930636.
36. Kim RJ, Wu E, Rafael A, Chen EL, Parker MA, Simonetti O, Klocke FJ, Bonow RO, Judd RM, The use of contrast-enhanced magnetic resonance Imaging to identify reversible myocardial dysfunction. N Engl J Med 2000 343 1445 1453. doi: 10.1056/NEJM200011163432003.
37. Neilan TG, Coelho-Filho OR, Pena-Herrera D, Shah RV, Jerosch-Herold M, Francis SA, Moslehi J, Kwong RY, Left ventricular mass in patients with a cardiomyopathy after treatment with anthracyclines. Am J Cardiol 2012 110 1679 1686. doi: 10.1016/j.amjcard.2012.07.040.
38. Tham EB, Haykowsky MJ, Chow K, Spavor M, Kaneko S, Khoo NS, Pagano JJ, Mackie AS, Thompson RB, Diffuse myocardial fibrosis by T1-mapping in children with subclinical anthracycline cardiotoxicity: relationship to exercise capacity, cumulative dose and remodeling. J Cardiovasc Magn Reson 2013 15 48. doi: 10.1186/1532-429X-15-48.
39. Armstrong GT, Plana JC, Zhang N, Srivastava D, Green DM, Ness KK, Daniel Donovan F, Metzger ML, Arevalo A, Durand JB, Joshi V, Hudson MM, Robison LL, Flamm SD, Screening adult survivors of childhood cancer for cardiomyopathy: comparison of echocardiography and cardiac magnetic resonance Imaging. J Clin Oncol 2012 30 2876 2884. doi: 10.1200/JCO.2011.40.3584.
40. 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. Circulation 2010 121 2462 2508
41. Ritchie JL, Bateman TM, Bonow RO, Crawford MH, Gibbons RJ, Hall RJ, O'Rourke RA, Parisi AF, Verani MS, Guidelines for clinical use of cardiac radionuclide Imaging. Report of the American College of Cardiology/American Heart Association Task Force on Assessment of Diagnostic and Therapeutic Cardiovascular Procedures (Committee on Radionuclide Imaging), developed in collaboration with the American Society of Nuclear Cardiology. Circulation 1995 91 1278 303
42. Alexander J, Dainiak N, Berger HJ, Goldman L, Johnstone D, Reduto L, Duffy T, Schwartz P, Gottschalk A, Zaret BL, Serial assessment of doxorubicin cardiotoxicity with quantitative radionuclide angiocardiography. N Engl J Med 1979 300 278 283. doi: 10.1056/NEJM197902083000603.
43. Schwartz RG, McKenzie WB, Alexander J, Sager P, D'Souza A, Manatunga A, Schwartz PE, Berger HJ, Setaro J, Surkin L, Congestive heart failure and left ventricular dysfunction complicating doxorubicin therapy. Seven-year experience using serial radionuclide angiocardiography. Am J Med 1987 82 1109 1118
44. Steinherz LJ, Steinherz PG, Tan CT, Heller G, Murphy ML, Cardiac toxicity 4 to 20 years after completing anthracycline therapy. JAMA 1991 266 1672 1677
45. Cintron G, Johnson G, Francis G, Cobb F, Cohn JN, Prognostic significance of serial changes in left ventricular ejection fraction in patients with congestive heart failure. The V-HeFT VA Cooperative Studies Group. Circulation 1993 87 6 suppl VI17 VI23
46. Watts RG, George M, Johnson WH Jr, Pretreatment and routine echocardiogram monitoring during chemotherapy for anthracycline-induced cardiotoxicity rarely identifies significant cardiac dysfunction or alters treatment decisions: a 5-year review at a single pediatric oncology center. Cancer 2012 118 1919 1924. doi: 10.1002/cncr.26481.
47. Mason JW, Bristow MR, Billingham ME, Daniels JR, Invasive and noninvasive methods of assessing adriamycin cardiotoxic effects in man: superiority of histopathologic assessment using endomyocardial biopsy. Cancer Treat Rep 1978 62 857 864
48. Ewer MS, Lenihan DJ, Left ventricular ejection fraction and cardiotoxicity: is our ear really to the ground? J Clin Oncol 2008 26 1201 1203. doi: 10.1200/JCO.2007.14.8742.