Skip to main content

Advertisement

Log in

Imaging of early modification in cardiomyopathy: the doxorubicin-induced model

  • Published:
The International Journal of Cardiovascular Imaging Aims and scope Submit manuscript

Abstract

Doxorubicin chemotherapy is effective and widely used to treat acute lymphoblastic leukemia. However, its effectiveness is hampered by a wide spectrum of dose-dependent cardiotoxicity including both morphological and functional changes, affecting primarily the myocardium. Non-invasive imaging techniques are used for the diagnosis and monitoring of these cardiotoxic effects. The purpose of this review is to summarize and compare the most common imaging techniques used in early detection and therapeutic monitoring of doxorubicin-induced cardiotoxicity and the suggested mechanisms of such side effects. Imaging techniques using echocardiography including conventional 2D and 3D echocardiography along with MRI sequences including Tagging, Cine, and quantitative MRI in detecting early myocardial damage are also reviewed. As there is a multitude of reported indices and imaging methods to assess particular functional alterations, we limit this review to the most relevant techniques based on their clinical application and their potential to early detection of doxorubicin-induced cardiotoxic effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Singal PK, Iliskovic N (1998) Doxorubicin-induced cardiomyopathy. N Engl J Med 339(13):900–905. doi:10.1056/NEJM199809243391307

    PubMed  CAS  Google Scholar 

  2. Chatterjee K, Zhang J, Honbo N, Karliner JS (2010) Doxorubicin cardiomyopathy. Cardiology 115(2):155–162. doi:10.1159/000265166

    PubMed  CAS  Google Scholar 

  3. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56(2):185–229. doi:10.1124/pr.56.2.6

    PubMed  CAS  Google Scholar 

  4. Lefrak EA, Pitha J, Rosenheim S, Gottlieb JA (1973) A clinicopathologic analysis of adriamycin cardiotoxicity. Cancer 32(2):302–314

    PubMed  CAS  Google Scholar 

  5. Von Hoff DD, Rozencweig M, Piccart M (1982) The cardiotoxicity of anticancer agents. Semin Oncol 9(1):23–33

    Google Scholar 

  6. Allen A (1992) The cardiotoxicity of chemotherapeutic drugs. Semin Oncol 19(5):529–542

    PubMed  CAS  Google Scholar 

  7. Eksborg S, Palm C, Bjork O (2000) A comparative pharmacokinetic study of doxorubicin and 4’-epi-doxorubicin in children with acute lymphocytic leukemia using a limited sampling procedure. Anticancer Drugs 11(2):129–136

    PubMed  CAS  Google Scholar 

  8. Von Hoff DD, Layard MW, Basa P, Davis HL Jr, Von Hoff AL, Rozencweig M, Muggia FM (1979) Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med 91(5):710–717

    Google Scholar 

  9. Isner JM, Ferrans VJ, Cohen SR, Witkind BG, Virmani R, Gottdiener JS, Beck JR, Roberts WC (1983) Clinical and morphologic cardiac findings after anthracycline chemotherapy. Analysis of 64 patients studied at necropsy. Am J Cardiol 51(7):1167–1174

    PubMed  CAS  Google Scholar 

  10. Wojtacki J, Lewicka-Nowak E, Lesniewski-Kmak K (2000) Anthracycline-induced cardiotoxicity: clinical course, risk factors, pathogenesis, detection and prevention—review of the literature. Med Sci Monit 6(2):411–420

    PubMed  CAS  Google Scholar 

  11. Lipshultz SE, Lipsitz SR, Sallan SE, Dalton VM, Mone SM, Gelber RD, Colan SD (2005) Chronic progressive cardiac dysfunction years after doxorubicin therapy for childhood acute lymphoblastic leukemia. J Clin Oncol 23(12):2629–2636. doi:10.1200/JCO.2005.12.121

    PubMed  CAS  Google Scholar 

  12. Gianni L, Herman EH, Lipshultz SE, Minotti G, Sarvazyan N, Sawyer DB (2008) Anthracycline cardiotoxicity: from bench to bedside. J Clin Oncol 26(22):3777–3784. doi:10.1200/JCO.2007.14.9401

    PubMed  Google Scholar 

  13. Franco VI, Henkel JM, Miller TL, Lipshultz SE (2011) Cardiovascular effects in childhood cancer survivors treated with anthracyclines. Cardiol Res Pract 2011:134679. doi:10.4061/2011/134679

    PubMed  Google Scholar 

  14. Deng S, Wojnowski L (2007) Genotyping the risk of anthracycline-induced cardiotoxicity. Cardiovasc Toxicol 7(2):129–134. doi:10.1007/s12012-007-0024-2

    PubMed  CAS  Google Scholar 

  15. Blanco JG, Leisenring WM, Gonzalez-Covarrubias VM, Kawashima TI, Davies SM, Relling MV, Robison LL, Sklar CA, Stovall M, Bhatia S (2008) Genetic polymorphisms in the carbonyl reductase 3 gene CBR3 and the NAD(P)H:quinone oxidoreductase 1 gene NQO1 in patients who developed anthracycline-related congestive heart failure after childhood cancer. Cancer 112(12):2789–2795. doi:10.1002/cncr.23534

    PubMed  Google Scholar 

  16. Blanco JG, Sun CL, Landier W, Chen L, Esparza-Duran D, Leisenring W, Mays A, Friedman DL, Ginsberg JP, Hudson MM, Neglia JP, Oeffinger KC, Ritchey AK, Villaluna D, Relling MV, Bhatia S (2012) Anthracycline-related cardiomyopathy after childhood cancer: role of polymorphisms in carbonyl reductase genes—a report from the Children’s Oncology Group. J Clin Oncol 30(13):1415–1421. doi:10.1200/JCO.2011.34.8987

    PubMed  CAS  Google Scholar 

  17. Kim Y, Ma AG, Kitta K, Fitch SN, Ikeda T, Ihara Y, Simon AR, Evans T, Suzuki YJ (2003) Anthracycline-induced suppression of GATA-4 transcription factor: implication in the regulation of cardiac myocyte apoptosis. Mol Pharmacol 63(2):368–377

    PubMed  CAS  Google Scholar 

  18. Sachidanandam K, Gayle AA, Robins HI, Kolesar JM (2012) Unexpected doxorubicin-mediated cardiotoxicity in sisters: possible role of polymorphisms in histamine n-methyl transferase. J Oncol Pharm Pract. doi:10.1177/1078155212461022

    PubMed  Google Scholar 

  19. Jeyaseelan R, Poizat C, Wu HY, Kedes L (1997) Molecular mechanisms of doxorubicin-induced cardiomyopathy. Selective suppression of Reiske iron-sulfur protein, ADP/ATP translocase, and phosphofructokinase genes is associated with ATP depletion in rat cardiomyocytes. J Biol Chem 272(9):5828–5832

    PubMed  CAS  Google Scholar 

  20. Druck MN, Gulenchyn KY, Evans WK, Gotlieb A, Srigley JR, Bar-Shlomo BZ, Feiglin DH, McEwan P, Silver MD, Millband L et al (1984) Radionuclide angiography and endomyocardial biopsy in the assessment of doxorubicin cardiotoxicity. Cancer 53(8):1667–1674

    PubMed  CAS  Google Scholar 

  21. Arola OJ, Saraste A, Pulkki K, Kallajoki M, Parvinen M, Voipio-Pulkki LM (2000) Acute doxorubicin cardiotoxicity involves cardiomyocyte apoptosis. Cancer Res 60(7):1789–1792

    PubMed  CAS  Google Scholar 

  22. Zhou S, Starkov A, Froberg MK, Leino RL, Wallace KB (2001) Cumulative and irreversible cardiac mitochondrial dysfunction induced by doxorubicin. Cancer Res 61(2):771–777

    PubMed  CAS  Google Scholar 

  23. Migrino RQ, Aggarwal D, Konorev E, Brahmbhatt T, Bright M, Kalyanaraman B (2008) Early detection of doxorubicin cardiomyopathy using two-dimensional strain echocardiography. Ultrasound Med Biol 34(2):208–214. doi:10.1016/j.ultrasmedbio.2007.07.018

    PubMed  Google Scholar 

  24. Cigremis Y, Parlakpinar H, Polat A, Colak C, Ozturk F, Sahna E, Ermis N, Acet A (2006) Beneficial role of aminoguanidine on acute cardiomyopathy related to doxorubicin-treatment. Mol Cell Biochem 285(1–2):149–154. doi:10.1007/s11010-005-9072-8

    PubMed  CAS  Google Scholar 

  25. Panjrath GS, Jain D (2006) Monitoring chemotherapy-induced cardiotoxicity: role of cardiac nuclear imaging. J Nucl Cardiol 13(3):415–426. doi:10.1016/j.nuclcard.2006.03.002

    PubMed  Google Scholar 

  26. Ali MK, Ewer MS, Gibbs HR, Swafford J, Graff KL (1994) Late doxorubicin-associated cardiotoxicity in children. The possible role of intercurrent viral infection. Cancer 74(1):182–188

    PubMed  CAS  Google Scholar 

  27. Bu’Lock FA, Mott MG, Oakhill A, Martin RP (1995) Left ventricular diastolic function after anthracycline chemotherapy in childhood: relation with systolic function, symptoms, and pathophysiology. Br Heart J 73(4):340–350

    PubMed  Google Scholar 

  28. Koiwa Y, Kanai H, Hasegawa H, Saitoh Y, Shirato K (2002) Left ventricular transmural systolic function by high-sensitivity velocity measurement “phased-tracking method” across the septum in doxorubicin cardiomyopathy. Ultrasound Med Biol 28(11–12):1395–1403

    PubMed  Google Scholar 

  29. Steinherz LJ, Steinherz PG, Tan CT, Heller G, Murphy ML (1991) Cardiac toxicity 4 to 20 years after completing anthracycline therapy. JAMA, J Am Med Assoc 266(12):1672–1677

    CAS  Google Scholar 

  30. Hequet O, Le QH, Moullet I, Pauli E, Salles G, Espinouse D, Dumontet C, Thieblemont C, Arnaud P, Antal D, Bouafia F, Coiffier B (2004) Subclinical late cardiomyopathy after doxorubicin therapy for lymphoma in adults. J Clin Oncol 22(10):1864–1871. doi:10.1200/JCO.2004.06.033

    PubMed  CAS  Google Scholar 

  31. Lipshultz SE, Colan SD, Gelber RD, Perez-Atayde AR, Sallan SE, Sanders SP (1991) Late cardiac effects of doxorubicin therapy for acute lymphoblastic leukemia in childhood. N Engl J Med 324(12):808–815. doi:10.1056/NEJM199103213241205

    PubMed  CAS  Google Scholar 

  32. Tallaj JA, Franco V, Rayburn BK, Pinderski L, Benza RL, Pamboukian S, Foley B, Bourge RC (2005) Response of doxorubicin-induced cardiomyopathy to the current management strategy of heart failure. J Heart Transplant 24(12):2196–2201. doi:10.1016/j.healun.2004.12.108

    Google Scholar 

  33. Adams MJ, Lipshultz SE (2005) Pathophysiology of anthracycline- and radiation-associated cardiomyopathies: implications for screening and prevention. Pediatr Blood Cancer 44(7):600–606. doi:10.1002/pbc.20352

    PubMed  Google Scholar 

  34. Olson RD, Gambliel HA, Vestal RE, Shadle SE, Charlier HA Jr, Cusack BJ (2005) Doxorubicin cardiac dysfunction: effects on calcium regulatory proteins, sarcoplasmic reticulum, and triiodothyronine. Cardiovasc Toxicol 5(3):269–283

    PubMed  CAS  Google Scholar 

  35. Vandecruys E, Mondelaers V, De Wolf D, Benoit Y, Suys B (2012) Late cardiotoxicity after low dose of anthracycline therapy for acute lymphoblastic leukemia in childhood. J Cancer Surviv 6(1):95–101. doi:10.1007/s11764-011-0186-6

    PubMed  Google Scholar 

  36. Elbl L, Hrstkova H, Chaloupka V (2003) The late consequences of anthracycline treatment on left ventricular function after treatment for childhood cancer. Eur J Pediatr 162(10):690–696. doi:10.1007/s00431-003-1275-y

    PubMed  CAS  Google Scholar 

  37. Giantris A, Abdurrahman L, Hinkle A, Asselin B, Lipshultz SE (1998) Anthracycline-induced cardiotoxicity in children and young adults. Crit Rev Oncol Hematol 27(1):53–68

    PubMed  CAS  Google Scholar 

  38. Ito T, Fujio Y, Takahashi K, Azuma J (2007) Degradation of NFAT5, a transcriptional regulator of osmotic stress-related genes, is a critical event for doxorubicin-induced cytotoxicity in cardiac myocytes. J Biol Chem 282(2):1152–1160. doi:10.1074/jbc.M609547200

    PubMed  CAS  Google Scholar 

  39. Zhang J, Clark JR Jr, Herman EH, Ferrans VJ (1996) Doxorubicin-induced apoptosis in spontaneously hypertensive rats: differential effects in heart, kidney and intestine, and inhibition by ICRF-187. J Mol Cell Cardiol 28(9):1931–1943. doi:10.1006/jmcc.1996.0186

    PubMed  CAS  Google Scholar 

  40. Berthiaume JM, Wallace KB (2007) Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol Toxicol 23(1):15–25. doi:10.1007/s10565-006-0140-y

    PubMed  CAS  Google Scholar 

  41. Myers CE, McGuire WP, Liss RH, Ifrim I, Grotzinger K, Young RC (1977) Adriamycin: the role of lipid peroxidation in cardiac toxicity and tumor response. Science 197(4299):165–167

    PubMed  CAS  Google Scholar 

  42. Mimnaugh EG, Gram TE, Trush MA (1983) Stimulation of mouse heart and liver microsomal lipid peroxidation by anthracycline anticancer drugs: characterization and effects of reactive oxygen scavengers. J Pharmacol Exp Ther 226(3):806–816

    PubMed  CAS  Google Scholar 

  43. Li T, Singal PK (2000) Adriamycin-induced early changes in myocardial antioxidant enzymes and their modulation by probucol. Circulation 102(17):2105–2110

    PubMed  CAS  Google Scholar 

  44. Pacher P, Liaudet L, Bai P, Mabley JG, Kaminski PM, Virag L, Deb A, Szabo E, Ungvari Z, Wolin MS, Groves JT, Szabo C (2003) Potent metalloporphyrin peroxynitrite decomposition catalyst protects against the development of doxorubicin-induced cardiac dysfunction. Circulation 107(6):896–904

    PubMed  CAS  Google Scholar 

  45. Ahmed HH, Mannaa F, Elmegeed GA, Doss SH (2005) Cardioprotective activity of melatonin and its novel synthesized derivatives on doxorubicin-induced cardiotoxicity. Bioorg Med Chem 13(5):1847–1857. doi:10.1016/j.bmc.2004.10.066

    PubMed  CAS  Google Scholar 

  46. Naidu MU, Kumar KV, Mohan IK, Sundaram C, Singh S (2002) Protective effect of Gingko biloba extract against doxorubicin-induced cardiotoxicity in mice. Indian J Exp Biol 40(8):894–900

    PubMed  CAS  Google Scholar 

  47. Zhu SG, Kukreja RC, Das A, Chen Q, Lesnefsky EJ, Xi L (2011) Dietary nitrate supplementation protects against Doxorubicin-induced cardiomyopathy by improving mitochondrial function. J Am Coll Cardiol 57(21):2181–2189. doi:10.1016/j.jacc.2011.01.024

    PubMed  CAS  Google Scholar 

  48. Janero DR (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radical Biol Med 9(6):515–540

    CAS  Google Scholar 

  49. Takemura G, Fujiwara H (2007) Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog Cardiovasc Dis 49(5):330–352. doi:10.1016/j.pcad.2006.10.002

    PubMed  CAS  Google Scholar 

  50. Davies KJ, Doroshow JH (1986) Redox cycling of anthracyclines by cardiac mitochondria. I. Anthracycline radical formation by NADH dehydrogenase. J Biol Chem 261(7):3060–3067

    PubMed  CAS  Google Scholar 

  51. Berlin V, Haseltine WA (1981) Reduction of adriamycin to a semiquinone-free radical by NADPH cytochrome P-450 reductase produces DNA cleavage in a reaction mediated by molecular oxygen. J Biol Chem 256(10):4747–4756

    PubMed  CAS  Google Scholar 

  52. Bachur NR, Gordon SL, Gee MV, Kon H (1979) NADPH cytochrome P-450 reductase activation of quinone anticancer agents to free radicals. Proc Natl Acad Sci USA 76(2):954–957

    PubMed  CAS  Google Scholar 

  53. Green PS, Leeuwenburgh C (2002) Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim Biophys Acta 1588(1):94–101

    PubMed  CAS  Google Scholar 

  54. Danz ED, Skramsted J, Henry N, Bennett JA, Keller RS (2009) Resveratrol prevents doxorubicin cardiotoxicity through mitochondrial stabilization and the Sirt1 pathway. Free Radical Biol Med 46(12):1589–1597. doi:10.1016/j.freeradbiomed.2009.03.011

    Google Scholar 

  55. Kluza J, Marchetti P, Gallego MA, Lancel S, Fournier C, Loyens A, Beauvillain JC, Bailly C (2004) Mitochondrial proliferation during apoptosis induced by anticancer agents: effects of doxorubicin and mitoxantrone on cancer and cardiac cells. Oncogene 23(42):7018–7030. doi:10.1038/sj.onc.1207936

    PubMed  CAS  Google Scholar 

  56. Chandran K, Aggarwal D, Migrino RQ, Joseph J, McAllister D, Konorev EA, Antholine WE, Zielonka J, Srinivasan S, Avadhani NG, Kalyanaraman B (2009) Doxorubicin inactivates myocardial cytochrome c oxidase in rats: cardioprotection by Mito-Q. Biophys J 96(4):1388–1398. doi:10.1016/j.bpj.2008.10.042

    PubMed  CAS  Google Scholar 

  57. L’Ecuyer T, Sanjeev S, Thomas R, Novak R, Das L, Campbell W, Heide RV (2006) DNA damage is an early event in doxorubicin-induced cardiac myocyte death. Am J Physiol Heart Circ Physiol 291(3):H1273–H1280. doi:10.1152/ajpheart.00738.2005

    PubMed  Google Scholar 

  58. Kalyanaraman B, Joseph J, Kalivendi S, Wang S, Konorev E, Kotamraju S (2002) Doxorubicin-induced apoptosis: implications in cardiotoxicity. Mol Cell Biochem 234–235(1–2):119–124

    PubMed  Google Scholar 

  59. Wang S, Kotamraju S, Konorev E, Kalivendi S, Joseph J, Kalyanaraman B (2002) Activation of nuclear factor-kappaB during doxorubicin-induced apoptosis in endothelial cells and myocytes is pro-apoptotic: the role of hydrogen peroxide. Biochem J 367(Pt 3):729–740. doi:10.1042/BJ20020752

    PubMed  CAS  Google Scholar 

  60. Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, Kalyanaraman B (2004) Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. intermediacy of H(2)O(2)- and p53-dependent pathways. J Biol Chem 279(24):25535–25543. doi:10.1074/jbc.M400944200

    PubMed  CAS  Google Scholar 

  61. Eom YW, Kim MA, Park SS, Goo MJ, Kwon HJ, Sohn S, Kim WH, Yoon G, Choi KS (2005) Two distinct modes of cell death induced by doxorubicin: apoptosis and cell death through mitotic catastrophe accompanied by senescence-like phenotype. Oncogene 24(30):4765–4777. doi:10.1038/sj.onc.1208627

    PubMed  CAS  Google Scholar 

  62. Tsang WP, Chau SP, Kong SK, Fung KP, Kwok TT (2003) Reactive oxygen species mediate doxorubicin induced p53-independent apoptosis. Life Sci 73(16):2047–2058

    PubMed  CAS  Google Scholar 

  63. Gilleron M, Marechal X, Montaigne D, Franczak J, Neviere R, Lancel S (2009) NADPH oxidases participate to doxorubicin-induced cardiac myocyte apoptosis. Biochem Biophys Res Commun 388(4):727–731. doi:10.1016/j.bbrc.2009.08.085

    PubMed  CAS  Google Scholar 

  64. Dartsch DC, Schaefer A, Boldt S, Kolch W, Marquardt H (2002) Comparison of anthracycline-induced death of human leukemia cells: programmed cell death versus necrosis. Apoptosis 7(6):537–548

    PubMed  CAS  Google Scholar 

  65. Pentassuglia L, Graf M, Lane H, Kuramochi Y, Cote G, Timolati F, Sawyer DB, Zuppinger C, Suter TM (2009) Inhibition of ErbB2 by receptor tyrosine kinase inhibitors causes myofibrillar structural damage without cell death in adult rat cardiomyocytes. Exp Cell Res 315(7):1302–1312. doi:10.1016/j.yexcr.2009.02.001

    PubMed  CAS  Google Scholar 

  66. Holmberg SR, Williams AJ (1990) Patterns of interaction between anthraquinone drugs and the calcium-release channel from cardiac sarcoplasmic reticulum. Circ Res 67(2):272–283

    PubMed  CAS  Google Scholar 

  67. Dodd DA, Atkinson JB, Olson RD, Buck S, Cusack BJ, Fleischer S, Boucek RJ Jr (1993) Doxorubicin cardiomyopathy is associated with a decrease in calcium release channel of the sarcoplasmic reticulum in a chronic rabbit model. J Clin Investig 91(4):1697–1705. doi:10.1172/JCI116379

    PubMed  CAS  Google Scholar 

  68. Shadle SE, Bammel BP, Cusack BJ, Knighton RA, Olson SJ, Mushlin PS, Olson RD (2000) Daunorubicin cardiotoxicity: evidence for the importance of the quinone moiety in a free-radical-independent mechanism. Biochem Pharmacol 60(10):1435–1444

    PubMed  CAS  Google Scholar 

  69. Arai M, Tomaru K, Takizawa T, Sekiguchi K, Yokoyama T, Suzuki T, Nagai R (1998) Sarcoplasmic reticulum genes are selectively down-regulated in cardiomyopathy produced by doxorubicin in rabbits. J Mol Cell Cardiol 30(2):243–254. doi:10.1006/jmcc.1997.0588

    PubMed  CAS  Google Scholar 

  70. DeAtley SM, Aksenov MY, Aksenova MV, Harris B, Hadley R, Cole Harper P, Carney JM, Butterfield DA (1999) Antioxidants protect against reactive oxygen species associated with adriamycin-treated cardiomyocytes. Cancer Lett 136(1):41–46

    PubMed  CAS  Google Scholar 

  71. Bers DM (2008) Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70:23–49. doi:10.1146/annurev.physiol.70.113006.100455

    PubMed  CAS  Google Scholar 

  72. Octavia Y, Tocchetti CG, Gabrielson KL, Janssens S, Crijns HJ, Moens AL (2012) Doxorubicin-induced cardiomyopathy: from molecular mechanisms to therapeutic strategies. J Mol Cell Cardiol 52(6):1213–1225. doi:10.1016/j.yjmcc.2012.03.006

    PubMed  CAS  Google Scholar 

  73. Olson RD, Li X, Palade P, Shadle SE, Mushlin PS, Gambliel HA, Fill M, Boucek RJ Jr, Cusack BJ (2000) Sarcoplasmic reticulum calcium release is stimulated and inhibited by daunorubicin and daunorubicinol. Toxicol Appl Pharmacol 169(2):168–176. doi:10.1006/taap.2000.9065

    PubMed  CAS  Google Scholar 

  74. Torti FM, Bristow MM, Lum BL, Carter SK, Howes AE, Aston DA, Brown BW Jr, Hannigan JF Jr, Meyers FJ, Mitchell EP et al (1986) Cardiotoxicity of epirubicin and doxorubicin: assessment by endomyocardial biopsy. Cancer Res 46(7):3722–3727

    PubMed  CAS  Google Scholar 

  75. Ludke AR, Al-Shudiefat AA, Dhingra S, Jassal DS, Singal PK (2009) A concise description of cardioprotective strategies in doxorubicin-induced cardiotoxicity. Can J Physiol Pharmacol 87(10):756–763. doi:10.1139/Y09-059

    PubMed  Google Scholar 

  76. Billingham ME, Mason JW, Bristow MR, Daniels JR (1978) Anthracycline cardiomyopathy monitored by morphologic changes. Cancer Treat Rep 62(6):865–872

    PubMed  CAS  Google Scholar 

  77. Bristow MR, Sageman WS, Scott RH, Billingham ME, Bowden RE, Kernoff RS, Snidow GH, Daniels JR (1980) Acute and chronic cardiovascular effects of doxorubicin in the dog: the cardiovascular pharmacology of drug-induced histamine release. J Cardiovasc Pharmacol 2(5):487–515

    PubMed  CAS  Google Scholar 

  78. Shankar SM, Marina N, Hudson MM, Hodgson DC, Adams MJ, Landier W, Bhatia S, Meeske K, Chen MH, Kinahan KE, Steinberger J, Rosenthal D (2008) Monitoring for cardiovascular disease in survivors of childhood cancer: report from the Cardiovascular Disease Task Force of the Children’s Oncology Group. Pediatrics 121(2):e387–e396. doi:10.1542/peds.2007-0575

    PubMed  Google Scholar 

  79. Lipshultz SE, Scully RE, Lipsitz SR, Sallan SE, Silverman LB, Miller TL, Barry EV, Asselin BL, Athale U, Clavell LA, Larsen E, Moghrabi A, Samson Y, Michon B, Schorin MA, Cohen HJ, Neuberg DS, Orav EJ, Colan SD (2010) Assessment of dexrazoxane as a cardioprotectant in doxorubicin-treated children with high-risk acute lymphoblastic leukaemia: long-term follow-up of a prospective, randomised, multicentre trial. Lancet Oncol 11(10):950–961. doi:10.1016/S1470-2045(10)70204-7

    PubMed  CAS  Google Scholar 

  80. Jensen BV, Skovsgaard T, Nielsen SL (2002) Functional monitoring of anthracycline cardiotoxicity: a prospective, blinded, long-term observational study of outcome in 120 patients. Ann Oncol 13(5):699–709

    PubMed  CAS  Google Scholar 

  81. Albini A, Pennesi G, Donatelli F, Cammarota R, De Flora S, Noonan DM (2010) Cardiotoxicity of anticancer drugs: the need for cardio-oncology and cardio-oncological prevention. J Natl Cancer Inst 102(1):14–25. doi:10.1093/jnci/djp440

    PubMed  CAS  Google Scholar 

  82. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ (2005) Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18(12):1440–1463. doi:10.1016/j.echo.2005.10.005

    PubMed  Google Scholar 

  83. Hauser M, Gibson BS, Wilson N (2001) Diagnosis of anthracycline-induced late cardiomyopathy by exercise-spiroergometry and stress-echocardiography. Eur J Pediatr 160(10):607–610

    PubMed  CAS  Google Scholar 

  84. Steinherz LJ, Wexler LH (1998) The prevention of anthracycline cardiomyopathy. Prog Pediatr Cardiol 8(3):97–108. doi:10.1016/s1058-9813(98)00006-x

    Google Scholar 

  85. 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 (2012) Screening adult survivors of childhood cancer for cardiomyopathy: comparison of echocardiography and cardiac magnetic resonance imaging. J Clin Oncol 30(23):2876–2884. doi:10.1200/JCO.2011.40.3584

    PubMed  Google Scholar 

  86. Khoo NS, Young A, Occleshaw C, Cowan B, Zeng IS, Gentles TL (2009) Assessments of right ventricular volume and function using three-dimensional echocardiography in older children and adults with congenital heart disease: comparison with cardiac magnetic resonance imaging. J Am Soc Echocardiogr 22(11):1279–1288. doi:10.1016/j.echo.2009.08.011

    PubMed  Google Scholar 

  87. Piegari E, Di Salvo G, Castaldi B, Vitelli MR, Rodolico G, Golino P, Calabro R, Rossi F, Berrino L (2008) Myocardial strain analysis in a doxorubicin-induced cardiomyopathy model. Ultrasound Med Biol 34(3):370–378. doi:10.1016/j.ultrasmedbio.2007.08.002

    PubMed  Google Scholar 

  88. Tassan-Mangina S, Codorean D, Metivier M, Costa B, Himberlin C, Jouannaud C, Blaise AM, Elaerts J, Nazeyrollas P (2006) Tissue Doppler imaging and conventional echocardiography after anthracycline treatment in adults: early and late alterations of left ventricular function during a prospective study. Eur J Echocardiogr 7(2):141–146. doi:10.1016/j.euje.2005.04.009

    PubMed  Google Scholar 

  89. Mavinkurve-Groothuis AM, Weijers G, Groot-Loonen J, Pourier M, Feuth T, de Korte CL, Hoogerbrugge PM, Kapusta L (2009) Interobserver, intraobserver and intrapatient reliability scores of myocardial strain imaging with 2-d echocardiography in patients treated with anthracyclines. Ultrasound Med Biol 35(4):697–704. doi:10.1016/j.ultrasmedbio.2008.09.026

    PubMed  Google Scholar 

  90. Watts RG, George M, Johnson WH Jr (2012) 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 118(7):1919–1924. doi:10.1002/cncr.26481

    PubMed  Google Scholar 

  91. Avelar T, Pauliks LB, Freiberg AS (2011) Clinical impact of the baseline echocardiogram in children with high-risk acute lymphoblastic leukemia. Pediatr Blood Cancer 57(2):227–230. doi:10.1002/pbc.23066

    PubMed  Google Scholar 

  92. Cottin Y, L’Huillier I, Casasnovas O, Geoffroy C, Caillot D, Zeller M, Solary E, Guy H, Wolf JE (2000) Dobutamine stress echocardiography identifies anthracycline cardiotoxicity. Eur J Echocardiogr 1(3):180–183. doi:10.1053/euje.2000.0037

    PubMed  CAS  Google Scholar 

  93. Weesner KM, Bledsoe M, Chauvenet A, Wofford M (1991) Exercise echocardiography in the detection of anthracycline cardiotoxicity. Cancer 68(2):435–438

    PubMed  CAS  Google Scholar 

  94. Smibert E, Carlin JB, Vidmar S, Wilkinson LC, Newton M, Weintraub RG (2004) Exercise echocardiography reflects cumulative anthracycline exposure during childhood. Pediatr Blood Cancer 42(7):556–562. doi:10.1002/pbc.20016

    PubMed  Google Scholar 

  95. Hamada H, Ohkubo T, Maeda M, Ogawa S (2006) Evaluation of cardiac reserved function by high-dose dobutamine-stress echocardiography in asymptomatic anthracycline-treated survivors of childhood cancer. Pediatr Int 48(3):313–320. doi:10.1111/j.1442-200X.2006.02210.x

    PubMed  CAS  Google Scholar 

  96. De Wolf D, Suys B, Maurus R, Benoit Y, Verhaaren H, Matthijs D, Otten J (1996) Dobutamine stress echocardiography in the evaluation of late anthracycline cardiotoxicity in childhood cancer survivors. Pediatr Res 39(3):504–512. doi:10.1203/00006450-199603000-00020

    PubMed  CAS  Google Scholar 

  97. Tei C, Ling LH, Hodge DO, Bailey KR, Oh JK, Rodeheffer RJ, Tajik AJ, Seward JB (1995) New index of combined systolic and diastolic myocardial performance: a simple and reproducible measure of cardiac function—a study in normals and dilated cardiomyopathy. J Cardiol 26(6):357–366

    PubMed  CAS  Google Scholar 

  98. Lakoumentas JA, Panou FK, Kotseroglou VK, Aggeli KI, Harbis PK (2005) The Tei index of myocardial performance: applications in cardiology. Hellenic J Cardiol 46(1):52–58

    PubMed  Google Scholar 

  99. Ishii M, Tsutsumi T, Himeno W, Eto G, Furui J, Hashino K, Sugahara Y, Muta H, Akagi T, Ando A, Eguchi H, Kato H (2000) Sequential evaluation of left ventricular myocardial performance in children after anthracycline therapy. Am J Cardiol 86(11):1279–1281, A1279

    Google Scholar 

  100. Sato T, Harada K, Tamura M, Watanabe A, Ishii M, Takada G (2001) Cardiorespiratory exercise capacity and its relation to a new Doppler index in children previously treated with anthracycline. J Am Soc Echocardiogr 14(4):256–263

    PubMed  CAS  Google Scholar 

  101. Senju N, Ikeda S, Koga S, Miyahara Y, Tsukasaki K, Tomonaga M, Kohno S (2007) The echocardiographic Tei-index reflects early myocardial damage induced by anthracyclines in patients with hematological malignancies. Heart Vessels 22(6):393–397. doi:10.1007/s00380-007-0985-x

    PubMed  Google Scholar 

  102. Bicudo LS, Tsutsui JM, Shiozaki A, Rochitte CE, Arteaga E, Mady C, Ramires JA, Mathias W Jr (2008) Value of real time three-dimensional echocardiography in patients with hypertrophic cardiomyopathy: comparison with two-dimensional echocardiography and magnetic resonance imaging. Echocardiography 25(7):717–726. doi:10.1111/j.1540-8175.2008.00684.x

    PubMed  Google Scholar 

  103. Hung J, Lang R, Flachskampf F, Shernan SK, McCulloch ML, Adams DB, Thomas J, Vannan M, Ryan T (2007) 3D echocardiography: a review of the current status and future directions. J Am Soc Echocardiogr 20(3):213–233. doi:10.1016/j.echo.2007.01.010

    PubMed  Google Scholar 

  104. Mulvagh SL, DeMaria AN, Feinstein SB, Burns PN, Kaul S, Miller JG, Monaghan M, Porter TR, Shaw LJ, Villanueva FS (2000) Contrast echocardiography: current and future applications. J Am Soc Echocardiogr 13(4):331–342

    PubMed  CAS  Google Scholar 

  105. Eitel I, von Knobelsdorff-Brenkenhoff F, Bernhardt P, Carbone I, Muellerleile K, Aldrovandi A, Francone M, Desch S, Gutberlet M, Strohm O, Schuler G, Schulz-Menger J, Thiele H, Friedrich MG (2011) Clinical characteristics and cardiovascular magnetic resonance findings in stress (takotsubo) cardiomyopathy. JAMA, J Am Med Assoc 306(3):277–286. doi:10.1001/jama.2011.992

    CAS  Google Scholar 

  106. Wassmuth R, Lentzsch S, Erdbruegger U, Schulz-Menger J, Doerken B, Dietz R, Friedrich MG (2001) Subclinical cardiotoxic effects of anthracyclines as assessed by magnetic resonance imaging-a pilot study. Am Heart J 141(6):1007–1013. doi:10.1067/mhj.2001.115436

    PubMed  CAS  Google Scholar 

  107. Jurcut R, Wildiers H, Ganame J, D’Hooge J, Paridaens R, Voigt JU (2008) Detection and monitoring of cardiotoxicity-what does modern cardiology offer? Support Care Cancer 16(5):437–445. doi:10.1007/s00520-007-0397-6

    PubMed  Google Scholar 

  108. Childs H, Ma L, Ma M, Clarke J, Cocker M, Green J, Strohm O, Friedrich MG (2011) Comparison of long and short axis quantification of left ventricular volume parameters by cardiovascular magnetic resonance, with ex vivo validation. J Cardiovasc Magn Reson 13:40. doi:10.1186/1532-429X-13-40

    PubMed  Google Scholar 

  109. 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 (2010) 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 121(22):2462–2508. doi:10.1161/CIR.0b013e3181d44a8f

    PubMed  Google Scholar 

  110. Perie D, Dahdah N, Foudis A, Curnier D (2013) Multi-parametric MRI as an indirect evaluation tool of the mechanical properties of in vitro cardiac tissues. BMC Cardiovasc Disord 13:24. doi:10.1186/1471-2261-13-24

    PubMed  Google Scholar 

  111. Grenier R, Périé D, Gilbert G, Beaudoin G, Curnier D (2013) Assessment of mechanical properties of muscles from multi-parametric magnetic resonance imaging. J Biomed Sci Eng (in press)

  112. Wang VY, Lam HI, Ennis DB, Cowan BR, Young AA, Nash MP (2009) Modelling passive diastolic mechanics with quantitative MRI of cardiac structure and function. Med Image Anal 13(5):773–784. doi:10.1016/j.media.2009.07.006

    PubMed  Google Scholar 

  113. Zhong X, Spottiswoode BS, Meyer CH, Kramer CM, Epstein FH (2010) Imaging three-dimensional myocardial mechanics using navigator-gated volumetric spiral cine DENSE MRI. Magn Reson Med 64(4):1089–1097. doi:10.1002/mrm.22503

    PubMed  Google Scholar 

  114. Young AA, Frangi AF (2009) Computational cardiac atlases: from patient to population and back. Exp Physiol 94(5):578–596. doi:10.1113/expphysiol.2008.044081

    PubMed  Google Scholar 

  115. Fonseca CG, Backhaus M, Bluemke DA, Britten RD, Chung JD, Cowan BR, Dinov ID, Finn JP, Hunter PJ, Kadish AH, Lee DC, Lima JA, Medrano-Gracia P, Shivkumar K, Suinesiaputra A, Tao W, Young AA (2011) The Cardiac Atlas Project—an imaging database for computational modeling and statistical atlases of the heart. Bioinformatics 27(16):2288–2295. doi:10.1093/bioinformatics/btr360

    PubMed  CAS  Google Scholar 

  116. Bistoquet A, Oshinski J, Škrinjar O (2008) Myocardial deformation recovery from cine MRI using a nearly incompressible biventricular model. Med Image Anal 12(1):69–85

    PubMed  Google Scholar 

  117. Niederer SA, Plank G, Chinchapatnam P, Ginks M, Lamata P, Rhode KS, Rinaldi CA, Razavi R, Smith NP (2011) Length-dependent tension in the failing heart and the efficacy of cardiac resynchronization therapy. Cardiovasc Res 89(2):336–343

    PubMed  CAS  Google Scholar 

  118. Chabiniok R, Moireau P, Lesault P-F, Rahmouni A, Deux J-F, Chapelle D (2012) Estimation of tissue contractility from cardiac cine-MRI using a biomechanical heart model. Biomech Model Mechanobiol 11(5):609–630

    PubMed  CAS  Google Scholar 

  119. Chapelle D, Fernández MA, Gerbeau J-F, Moireau P, Sainte-Marie J, Zemzemi N (2009) Numerical simulation of the electromechanical activity of the heart. Functional Imaging and Modeling of the Heart. Springer, In, pp 357–365

    Google Scholar 

  120. Aguado-Sierra J, Krishnamurthy A, Villongco C, Chuang J, Howard E, Gonzales MJ, Omens J, Krummen DE, Narayan S, Kerckhoffs RC (2011) Patient-specific modeling of dyssynchronous heart failure: a case study. Prog Biophys Mol Biol 107(1):147–155

    PubMed  Google Scholar 

  121. Sermesant M, Chabiniok R, Chinchapatnam P, Mansi T, Billet F, Moireau P, Peyrat J-M, Wong K, Relan J, Rhode K (2012) Patient-specific electromechanical models of the heart for the prediction of pacing acute effects in CRT: a preliminary clinical validation. Med Image Anal 16(1):201–215

    PubMed  CAS  Google Scholar 

  122. Stanisz GJ, Odrobina EE, Pun J, Escaravage M, Graham SJ, Bronskill MJ, Henkelman RM (2005) T1, T2 relaxation and magnetization transfer in tissue at 3T. Magn Reson Med 54(3):507–512. doi:10.1002/mrm.20605

    PubMed  Google Scholar 

  123. Iles L, Pfluger H, Phrommintikul A, Cherayath J, Aksit P, Gupta SN, Kaye DM, Taylor AJ (2008) Evaluation of diffuse myocardial fibrosis in heart failure with cardiac magnetic resonance contrast-enhanced T1 mapping. J Am Coll Cardiol 52(19):1574–1580. doi:10.1016/j.jacc.2008.06.049

    PubMed  Google Scholar 

  124. Mewton N, Liu CY, Croisille P, Bluemke D, Lima JA (2011) Assessment of myocardial fibrosis with cardiovascular magnetic resonance. J Am Coll Cardiol 57(8):891–903. doi:10.1016/j.jacc.2010.11.013

    PubMed  Google Scholar 

  125. Messroghli DR, Niendorf T, Schulz-Menger J, Dietz R, Friedrich MG (2003) T1 mapping in patients with acute myocardial infarction: myocardial infarction and scar. J Cardiovasc Magn Reson 5(2):353–359

    PubMed  Google Scholar 

  126. Messroghli DR, Walters K, Plein S, Sparrow P, Friedrich MG, Ridgway JP, Sivananthan MU (2007) Myocardial T1 mapping: application to patients with acute and chronic myocardial infarction. Magn Reson Med 58(1):34–40

    PubMed  Google Scholar 

  127. Giri S, Chung YC, Merchant A, Mihai G, Rajagopalan S, Raman SV, Simonetti OP (2009) T2 quantification for improved detection of myocardial edema. J Cardiovasc Magn Reson 11:56. doi:10.1186/1532-429X-11-56

    PubMed  Google Scholar 

  128. Francone M, Carbone I, Agati L, Bucciarelli Ducci C, Mangia M, Iacucci I, Catalano C, Passariello R (2011) Utility of T2-weighted short-tau inversion recovery (STIR) sequences in cardiac MRI: an overview of clinical applications in ischaemic and non-ischaemic heart disease. Radiol Med (Torino) 116(1):32–46. doi:10.1007/s11547-010-0594-0

    CAS  Google Scholar 

  129. Sparrow P, Amirabadi A, Sussman MS, Paul N, Merchant N (2009) Quantitative assessment of myocardial T2 relaxation times in cardiac amyloidosis. J Magn Reson Imaging 30(5):942–946

    PubMed  Google Scholar 

  130. Anderson LJ, Holden S, Davis B, Prescott E, Charrier CC, Bunce NH, Firmin DN, Wonke B, Porter J, Walker JM, Pennell DJ (2001) Cardiovascular T2-star (T2*) magnetic resonance for the early diagnosis of myocardial iron overload. Eur Heart J 22(23):2171–2179

    PubMed  CAS  Google Scholar 

  131. Wood JC, Otto-Duessel M, Aguilar M, Nick H, Nelson MD, Coates TD, Pollack H, Moats R (2005) Cardiac iron determines cardiac T2*, T2, and T1 in the gerbil model of iron cardiomyopathy. Circulation 112(4):535–543. doi:10.1161/CIRCULATIONAHA.104.504415

    PubMed  CAS  Google Scholar 

  132. Kondur AK, Li T, Vaitkevicius P, Afonso L (2009) Quantification of myocardial iron overload by cardiovascular magnetic resonance imaging T2* and review of the literature. Clin Cardiol 32(6):E55–E59. doi:10.1002/clc.20310

    PubMed  Google Scholar 

  133. Weber OM, Speier P, Scheffler K, Bieri O (2009) Assessment of magnetization transfer effects in myocardial tissue using balanced steady-state free precession (bSSFP) cine MRI. Magn Reson Med 62(3):699–705. doi:10.1002/mrm.22053

    PubMed  Google Scholar 

  134. Atanasijevic T, Shusteff M, Fam P, Jasanoff A (2006) Calcium-sensitive MRI contrast agents based on superparamagnetic iron oxide nanoparticles and calmodulin. Proc Natl Acad Sci USA 103(40):14707–14712. doi:10.1073/pnas.0606749103

    PubMed  CAS  Google Scholar 

  135. Positano V, Pingitore A, Giorgetti A, Favilli B, Santarelli MF, Landini L, Marzullo P, Lombardi M (2005) A fast and effective method to assess myocardial necrosis by means of contrast magnetic resonance imaging. J Cardiovasc Magn Reson 7(2):487–494

    PubMed  Google Scholar 

  136. Sosnovik DE, Garanger E, Aikawa E, Nahrendorf M, Figuiredo JL, Dai G, Reynolds F, Rosenzweig A, Weissleder R, Josephson L (2009) Molecular MRI of cardiomyocyte apoptosis with simultaneous delayed-enhancement MRI distinguishes apoptotic and necrotic myocytes in vivo: potential for midmyocardial salvage in acute ischemia. Circ Cardiovasc Imaging 2(6):460–467. doi:10.1161/CIRCIMAGING.109.859678

    PubMed  Google Scholar 

  137. Kim YJ, Choi BW, Hur J, Lee HJ, Seo JS, Kim TH, Choe KO, Ha JW (2008) Delayed enhancement in hypertrophic cardiomyopathy: comparison with myocardial tagging MRI. J Magn Reson Imaging 27(5):1054–1060. doi:10.1002/jmri.21366

    PubMed  Google Scholar 

  138. Teraoka K, Hirano M, Ookubo H, Sasaki K, Katsuyama H, Amino M, Abe Y, Yamashina A (2004) Delayed contrast enhancement of MRI in hypertrophic cardiomyopathy. Magn Reson Imaging 22(2):155–161. doi:10.1016/j.mri.2003.08.009

    PubMed  Google Scholar 

  139. Tandri H, Saranathan M, Rodriguez ER, Martinez C, Bomma C, Nasir K, Rosen B, Lima JA, Calkins H, Bluemke DA (2005) Noninvasive detection of myocardial fibrosis in arrhythmogenic right ventricular cardiomyopathy using delayed-enhancement magnetic resonance imaging. J Am Coll Cardiol 45(1):98–103. doi:10.1016/j.jacc.2004.09.053

    PubMed  Google Scholar 

  140. Perel RD, Slaughter RE, Strugnell WE (2006) Subendocardial late gadolinium enhancement in two patients with anthracycline cardiotoxicity following treatment for Ewing’s sarcoma. J Cardiovasc Magn Reson 8(6):789–791. doi:10.1080/10976640600737664

    PubMed  Google Scholar 

  141. Skjold A, Amundsen BH, Wiseth R, Stoylen A, Haraldseth O, Larsson HB, Jynge P (2007) Manganese dipyridoxyl-diphosphate (MnDPDP) as a viability marker in patients with myocardial infarction. J Magn Reson Imaging 26(3):720–727. doi:10.1002/jmri.21065

    PubMed  Google Scholar 

  142. Hu TC, Pautler RG, MacGowan GA, Koretsky AP (2001) Manganese-enhanced MRI of mouse heart during changes in inotropy. Magn Reson Med 46(5):884–890

    PubMed  CAS  Google Scholar 

  143. Nordhoy W, Anthonsen HW, Bruvold M, Jynge P, Krane J, Brurok H (2003) Manganese ions as intracellular contrast agents: proton relaxation and calcium interactions in rat myocardium. NMR Biomed 16(2):82–95. doi:10.1002/nbm.817

    PubMed  CAS  Google Scholar 

  144. Waghorn B, Edwards T, Yang Y, Chuang KH, Yanasak N, Hu TC (2008) Monitoring dynamic alterations in calcium homeostasis by T (1)-weighted and T (1)-mapping cardiac manganese-enhanced MRI in a murine myocardial infarction model. NMR Biomed 21(10):1102–1111. doi:10.1002/nbm.1287

    PubMed  CAS  Google Scholar 

  145. Bers DM (2000) Calcium fluxes involved in control of cardiac myocyte contraction. Circ Res 87(4):275–281

    PubMed  CAS  Google Scholar 

  146. Zhukov L, Barr AH (2003) Heart-muscle fiber reconstruction from diffusion tensor MRI. In: Visualization, 2003. VIS 2003. IEEE, 24–24 Oct. 2003. pp 597–602. doi:10.1109/visual.2003.1250425

  147. Holloway CJ, Suttie J, Dass S, Neubauer S (2011) Clinical cardiac magnetic resonance spectroscopy. Prog Cardiovasc Dis 54(3):320–327. doi:10.1016/j.pcad.2011.08.002

    PubMed  Google Scholar 

  148. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelisa A (2009) Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr 10(2):165–193. doi:10.1093/ejechocard/jep007

    PubMed  Google Scholar 

  149. Senior R, Becher H, Monaghan M, Agati L, Zamorano J, Vanoverschelde JL, Nihoyannopoulos P (2009) Contrast echocardiography: evidence-based recommendations by European Association of Echocardiography. Eur J Echocardiogr 10(2):194–212. doi:10.1093/ejechocard/jep005

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by The Cole Foundation, the Natural Sciences and Engineering Research Council (NSERC) of Canada and the MEDITIS training program (Ecole Polytechnique of Montreal and NSERC).

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Delphine Périé.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aissiou, M., Périé, D., Cheriet, F. et al. Imaging of early modification in cardiomyopathy: the doxorubicin-induced model. Int J Cardiovasc Imaging 29, 1459–1476 (2013). https://doi.org/10.1007/s10554-013-0248-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10554-013-0248-0

Keywords

Navigation