Anthracycline Chemotherapy and Cardiotoxicity

John V McGowan, Robin Chung, Angshuman Maulik, Izabela Piotrowska, J Malcolm Walker, Derek M Yellon, John V McGowan, Robin Chung, Angshuman Maulik, Izabela Piotrowska, J Malcolm Walker, Derek M Yellon

Abstract

Anthracycline chemotherapy maintains a prominent role in treating many forms of cancer. Cardiotoxic side effects limit their dosing and improved cancer outcomes expose the cancer survivor to increased cardiovascular morbidity and mortality. The basic mechanisms of cardiotoxicity may involve direct pathways for reactive oxygen species generation and topoisomerase 2 as well as other indirect pathways. Cardioprotective treatments are few and those that have been examined include renin angiotensin system blockade, beta blockers, or the iron chelator dexrazoxane. New treatments exploiting the ErbB or other novel pro-survival pathways, such as conditioning, are on the cardioprotection horizon. Even in the forthcoming era of targeted cancer therapies, the substantial proportion of today's anthracycline-treated cancer patients may become tomorrow's cardiac patient.

Keywords: Cancer anthracycline doxorubicin chemotherapy cardiotoxicity cardioprotection.

Conflict of interest statement

Conflict of Interest

All authors (JVM, RC, AM, IP, JMW, DMY) declare that they have no conflicts of interest.

Ethical Approval

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

Funding

This article does not contain any studies conducted by the authors and thus there are no direct funding disclosures. Two authors (RC, IP) were supported by funding from the Biomedical Research Centre (grant number BRC233/CM/SD/101320). This manuscript was undertaken at University College London Hospitals / University College London (UCLH/UCL) who received a proportion of funding from the Department of Health’s National Institute for Health Research Biomedical Research Centres funding scheme.

Informed Consent

Not applicable to this article-- as this article does not contain any studies with human participants or animals performed by any of the authors.

Figures

Fig. 1
Fig. 1
The four anthracycline derivatives Doxorubicn (DOX), Daunarubicin (DNR), Epirubicin (EPI) and Idarubicin (IDA). The anthracyclines share a tetracyclic aglycone structure of four cyclohexane chains with a daunosamine sugar moiety at carbon C7 of ring a; adjacent quinone-hydroquinone groups in rings b and c; a methoxy substituent carbon C4 in ring D; a carbonyl group at C13; and a short side chain in C9. Doxorubicin and daunorubicin differ in their short chains. Doxorubicin has a primary alcohol, whereas daunorubicin has a methyl group. Epirubicin is derived from doxorubicin by axial-to-equitorial epimerisation of the hydroxyl group in the daunosamine moiety. Idarubicin is identical to daunorubicin except the 4-methoxy group in ring D is removed
Fig. 2
Fig. 2
Doxorubicin staining shows sequestration in (L) cardiomyocytes and (R) malignant cervical cancer cells (courtesy Dr. I Piotrowska)

References

    1. Rimal H, Lee SW, Lee JH, Oh TJ. Understanding of real alternative redox partner of Streptomyces peucetius DoxA: prediction and validation using in silico and in vitro analyses. Arch Biochem Biophys. 2015;585:64–74. doi: 10.1016/j.abb.2015.08.019.
    1. Organization WH. WHO Model List of Essential Medicines. April 2015 ed2015.
    1. Coleman MP, Forman D, Bryant H, Butler J, Rachet B, Maringe C, et al. Cancer survival in Australia, Canada, Denmark, Norway, Sweden, and the UK, 1995-2007 (the international cancer benchmarking partnership): an analysis of population-based cancer registry data. Lancet. 2011;377:127–38.
    1. CancerResearchUK. Cancer mortality in the UK 2012. In: Cancer Statistics Report. London UK. 2014. . Accessed 27th October 2014.
    1. Kantarjian H, Sawyers C, Hochhaus A, Guilhot F, Schiffer C, Gambacorti-Passerini C, et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med. 2002;346:645–52.
    1. Richardson PG, Sonneveld P, Schuster MW, Irwin D, Stadtmauer EA, Facon T, et al. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med. 2005;352:2487–98.
    1. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med. 2001;344:783–92.
    1. Giordano SH, Lin YL, Kuo YF, Hortobagyi GN, Goodwin JS. Decline in the use of anthracyclines for breast cancer. J Clin Oncol. 2012;30:2232–9.
    1. Nabhan C, Byrtek M, Rai A, Dawson K, Zhou X, Link BK, et al. Disease characteristics, treatment patterns, prognosis, outcomes and lymphoma-related mortality in elderly follicular lymphoma in the United States. Br J Haematol. 2015;170:85–95.
    1. Chihara D, Westin JR, Oki Y, Ahmed MA, Do B, Fayad LE, et al. Management strategies and outcomes for very elderly patients with diffuse large B-cell lymphoma. Cancer. 2016;
    1. Smith LA, Cornelius VR, Plummer CJ, Levitt G, Verrill M, Canney P, et al. Cardiotoxicity of anthracycline agents for the treatment of cancer: systematic review and meta-analysis of randomised controlled trials. BMC Cancer. 2010;10:337. doi: 10.1186/1471-2407-10-337.
    1. Armstrong GT, Chen Y, Yasui Y, Leisenring W, Gibson TM, Mertens AC, et al. Reduction in late mortality among 5-year survivors of childhood cancer. N Engl J Med. 2016;374:833–42.
    1. Patnaik JL, Byers T, DiGuiseppi C, Dabelea D, Denberg TD. Cardiovascular disease competes with breast cancer as the leading cause of death for older females diagnosed with breast cancer: a retrospective cohort study. Breast Cancer Res. 2011;13:R64.
    1. Singal PK, Iliskovic N. Doxorubicin-induced cardiomyopathy. N Engl J Med. 1998;339:900–5.
    1. Davies KJ, Doroshow JH. Redox cycling of anthracyclines by cardiac mitochondria. I. Anthracycline radical formation by NADH dehydrogenase. J Biol Chem. 1986;261(7):3060–3067.
    1. Berthiaume JM, Wallace KB. Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol Toxicol. 2007;23:15–25.
    1. Ichikawa Y, Ghanefar M, Bayeva M, Wu R, Khechaduri A, Naga Prasad SV, et al. Cardiotoxicity of doxorubicin is mediated through mitochondrial iron accumulation. J Clin Invest. 2014;124:617–30.
    1. Hahn VS, Lenihan DJ, Ky B. Cancer therapy-induced cardiotoxicity: basic mechanisms and potential cardioprotective therapies. J Am Heart Assoc. 2014;3:e000665.
    1. Champoux JJ. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem. 2001;70:369–413. doi: 10.1146/annurev.biochem.70.1.369.
    1. Wang JC. Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol. 2002;3:430–40.
    1. Carpenter AJ, Porter AC. Construction, characterization, and complementation of a conditional-lethal DNA topoisomerase IIalpha mutant human cell line. Mol Biol Cell. 2004;15:5700–11.
    1. Tewey KMRT, Yang L, Halligan DB, Liu LF. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science. 1984;226:466–468. doi: 10.1126/science.6093249.
    1. Finck BN, Kelly DP. Peroxisome proliferator-activated receptor gamma coactivator-1 (PGC-1) regulatory cascade in cardiac physiology and disease. Circulation. 2007;115:2540–8.
    1. Lyu YL, Kerrigan JE, Lin CP, Azarova AM, Tsai YC, Ban Y, et al. Topoisomerase IIbeta mediated DNA double-strand breaks: implications in doxorubicin cardiotoxicity and prevention by dexrazoxane. Cancer Res. 2007;67:8839–46.
    1. Zhang S, Liu X, Bawa-Khalfe T, Lu LS, Lyu YL, Liu LF, et al. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat Med. 2012;18:1639–42.
    1. Staal SP. Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma. Proc Natl Acad Sci U S A. 1987;84:5034–7.
    1. Wadugu B, Kuhn B. The role of neuregulin/ErbB2/ErbB4 signaling in the heart with special focus on effects on cardiomyocyte proliferation. Am J Physiol Heart Circ Physiol. 2012;302:H2139–47.
    1. Crone SA, Zhao YY, Fan L, Gu Y, Minamisawa S, Liu Y, et al. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat Med. 2002;8:459–65.
    1. Ma J, Wang Y, Zheng D, Wei M, Xu H, Peng T. Rac1 signalling mediates doxorubicin-induced cardiotoxicity through both reactive oxygen species-dependent and -independent pathways. Cardiovasc Res. 2013;97:77–87.
    1. Huang C, Zhang X, Ramil JM, Rikka S, Kim L, Lee Y, et al. Juvenile exposure to anthracyclines impairs cardiac progenitor cell function and vascularization resulting in greater susceptibility to stress-induced myocardial injury in adult mice. Circulation. 2010;121:675–83.
    1. Lipshultz SE, Lipsitz SR, Sallan SE, Dalton VM, Mone SM, Gelber RD, et al. Chronic progressive cardiac dysfunction years after doxorubicin therapy for childhood acute lymphoblastic leukemia. J Clin Oncol. 2005;23:2629–36.
    1. Von Hoff DD, Layard MW, Basa P, Davis Jr HL, Von Hoff AL, Rozencweig M, et al. Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med. 1979;91:710–7.
    1. Swain SM, Whaley FS, Ewer MS. Congestive heart failure in patients treated with doxorubicin: a retrospective analysis of three trials. Cancer. 2003;97:2869–79.
    1. Felker GM, Thompson RE, Hare JM, Hruban RH, Clemetson DE, Howard DL, et al. Underlying causes and long-term survival in patients with initially unexplained cardiomyopathy. N Engl J Med. 2000;342:1077–84.
    1. Hequet O, Le QH, Moullet I, Pauli E, Salles G, Espinouse D, et al. Subclinical late cardiomyopathy after doxorubicin therapy for lymphoma in adults. J Clin Oncol. 2004;22:1864–71.
    1. Thavendiranathan P, Grant AD, Negishi T, Plana JC, Popovic ZB, Marwick TH. Reproducibility of echocardiographic techniques for sequential assessment of left ventricular ejection fraction and volumes: application to patients undergoing cancer chemotherapy. J Am Coll Cardiol. 2013;61:77–84.
    1. Cardinale D, Colombo A, Bacchiani G, Tedeschi I, Meroni CA, Veglia F, et al. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation. 2015;
    1. Zamorano JL, Lancellotti P, Rodriguez Muñoz D, Aboyans V, Asteggiano R, Galderisi M, Habib G, et al. Authors/task force members; ESC Committee for Practice Guidelines (CPG): ESC position paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines: the task force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur Heart J. 2016;37:2768–2801.
    1. Ahmed AN, Blonde K, Hackam D, Iansavichene A, Mrkobrada M. Prognostic significance of elevated troponin in non-cardiac hospitalized patients: a systematic review and meta-analysis. Ann Med. 2014;46:653–63.
    1. Grinstein J, Bonaca MP, Jarolim P, Conrad MJ, Bohula-May E, Deenadayalu N, et al. Prognostic implications of low level cardiac troponin elevation using high-sensitivity cardiac troponin T. Clin Cardiol. 2015;38:230–5.
    1. Grodin JL, Neale S, Wu Y, Hazen SL, Tang WH. Prognostic comparison of different sensitivity cardiac troponin assays in stable heart failure. Am J Med. 2014;
    1. Hochholzer W, Valina CM, Stratz C, Amann M, Schlittenhardt D, Buttner HJ, et al. High-sensitivity cardiac troponin for risk prediction in patients with and without coronary heart disease. Int J Cardiol. 2014;176:444–9.
    1. Kuster N, Monnier K, Baptista G, Dupuy AM, Badiou S, Bargnoux AS, et al. Estimation of age- and comorbidities-adjusted percentiles of high-sensitivity cardiac troponin T levels in the elderly. Clin Chem Lab Med. 2014;
    1. Qian G, Wu C, Zhang Y, Chen YD, Dong W, Ren YH. Prognostic value of high-sensitivity cardiac troponin T in patients with endomyocardial-biopsy proven cardiac amyloidosis. J Geriatr Cardiol. 2014;11:136–40.
    1. Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD. Third universal definition of myocardial infarction. Circulation. 2012;126:2020–35.
    1. Yiu KH, Lau KK, Zhao CT, Chan YH, Chen Y, Zhen Z, et al. Predictive value of high-sensitivity troponin-I for future adverse cardiovascular outcome in stable patients with type 2 diabetes mellitus. Cardiovasc Diabetol. 2014;13:63. doi: 10.1186/1475-2840-13-63.
    1. Auner HW, Tinchon C, Linkesch W, Tiran A, Quehenberger F, Link H, et al. Prolonged monitoring of troponin T for the detection of anthracycline cardiotoxicity in adults with hematological malignancies. Ann Haematol. 2003;82:218–222.
    1. Cardinale D, Sandri MT, Colombo A, Colombo N, Boeri M, Lamantia G, et al. Prognostic value of troponin I in cardiac risk stratification of cancer patients undergoing high-dose chemotherapy. Circ. 2004;109:2749–2754. doi: 10.1161/.
    1. Kilickap S, Barista I, Akgul E, Aytemir K, Aksoyek S, Aksoy S, et al. cTnT can be a useful marker for early detection of anthracycline cardiotoxicity. Ann Oncol. 2005;16:798–804.
    1. Cardinale D, Sandri MT, Martinoni A, Tricca A, Civelli M, Lamantia G, et al. Left ventricular dysfunction predicted by early troponin I release after high-dose chemotherapy. J Am Coll Cardiol. 2000;36:517–22.
    1. Cardinale D, Sandri MT, Martinoni A, Borghini E, Civelli M, Lamantia G, et al. Myocardial injury revealed by plasma troponin I in breast cancer with high-dose chemotherapy. Ann Oncol. 2002;13:710–715. doi: 10.1093/annonc/mdf170.
    1. Sandri MT, Cardinale D, Zorzino L, Passerini R, Lentati P, Martinoni A, et al. Minor increases in plasma troponin I predict decreased left ventricular ejection fraction after high-dose chemotherapy. Clin Chem. 2003;49:248–52.
    1. Lipshultz SE, Rifai N, Dalton VM, Levy DE, Silverman LB, Lipsitz SR, et al. The effect of dexrazoxane on myocardial injury in doxorubicin-treated children with acute lymphoblastic leukemia. N Engl J Med. 2004;351:145–53.
    1. Haney S, Cresti N, Verrill M, Plummer C. Cardiac troponin release following standard dose anthracycline-based adjuvant chemotherapy (abstr) Eur Heart J. 2013;34(Suppl 1):1074. doi: 10.1093/eurheartj/eht310.P5752.
    1. Katsurada K, Ichida M, Sakuragi M, Takehara M, Hozumi Y, Kario K. High-sensitivity troponin T as a marker to predict cardiotoxicity in breast cancer patients with adjuvant trastuzumab therapy. Springerplus. 2014;3:620. doi: 10.1186/2193-1801-3-620.
    1. Chung R, Maulik A, Hamarneh A, Hochhauser D, Hausenloy DJ, Walker JM, et al. Effect of remote ischaemic conditioning in oncology patients undergoing chemotherapy: rationale and design of the ERIC-ONC study--a single-center, blinded. Randomized Controlled Trial Clin Cardiol. 2016;39:72–82.
    1. Auner HW, Tinchon C, Linkesch W, Halwachs-Baumann G, Sill H. Correspondence re: O. J. Arola et al., acute doxorubicin cardiotoxicity involves cardiomyocyte apoptosis. Cancer res., 60: 1789-1792, 2000. Cancer Res. 2001;61:2335–6.
    1. Colovic N, Bogdanovic A, Virijevic M, Vidovic A, Tomin D. Acute myocardial infarction during induction chemotherapy for acute MLL t(4;11) leukemia with lineage switch and extreme leukocytosis. Srp Arh Celok Lek. 2015;143:734–8.
    1. Landolfi R, Di Gennaro L, Barbui T, De Stefano V, Finazzi G, Marfisi R, et al. Leukocytosis as a major thrombotic risk factor in patients with polycythemia vera. Blood. 2007;109:2446–52.
    1. Schmid-Schonbein GW. The damaging potential of leukocyte activation in the microcirculation. Angiology. 1993;44:45–56.
    1. Hidalgo JD, Krone R, Rich MW, Blum K, Adkins D, Fan MY, et al. Supraventricular tachyarrhythmias after hematopoietic stem cell transplantation: incidence, risk factors and outcomes. Bone Marrow Transplant. 2004;34:615–9.
    1. Kilickap S, Barista I, Akgul E, Aytemir K, Aksoy S, Tekuzman G. Early and late arrhythmogenic effects of doxorubicin. South Med J. 2007;100:262–265. doi: 10.1097/01.smj.0000257382.89910.fe.
    1. Hu YF, Liu CJ, Chang PM, Tsao HM, Lin YJ, Chang SL, et al. Incident thromboembolism and heart failure associated with new-onset atrial fibrillation in cancer patients. Int J Cardiol. 2013;165:355–7.
    1. Kero AE, Jarvela LS, Arola M, Malila N, Madanat-Harjuoja LM, Matomaki J, et al. Cardiovascular morbidity in long-term survivors of early-onset cancer: a population-based study. Int J Cancer. 2014;134:664–73.
    1. Jones LW, Courneya KS, Mackey JR, Muss HB, Pituskin EN, Scott JM, et al. Cardiopulmonary function and age-related decline across the breast cancer survivorship continuum. J Clin Oncol. 2012;30:2530–7.
    1. Lipshultz SE, Scully RE, Lipsitz SR, Sallan SE, Silverman LB, Miller TL, et al. 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. 2010;11:950–961. doi: 10.1016/S1470-2045(10)70204-7.
    1. Lipshultz SE, Lipsitz SR, Mone SM, Goorin AM, Sallan SE, Sanders SP, et al. Female sex and drug dose as risk factors for late cardiotoxic effects of doxorubicin therapy for childhood cancer. N Engl J Med. 1995;332:1738–43.
    1. Stewart DJ, Grewaal D, Green RM, Mikhael N, Goel R, Montpetit VA, et al. Concentrations of doxorubicin and its metabolites in human autopsy heart and other tissues. Anticancer Res. 1993;13:1945–52.
    1. Sarosiek KA, Letai A. Directly targeting the mitochondrial pathway of apoptosis for cancer therapy using BH3 mimetics - recent successes, current challenges and future promise. FEBS J. 2016;283:3523–33.
    1. Ewer MS, Ewer SM. Cardiotoxicity of anticancer treatments: what the cardiologist needs to know. Nat Rev Cardiol. 2010;7:564–75.
    1. Cardinale D, Colombo A, Lamantia G, Colombo N, Civelli M, De Giacomi G, et al. Anthracycline-induced cardiomyopathy: clinical relevance and response to pharmacologic therapy. J Am Coll Cardiol. 2010;55:213–20.
    1. Cardinale D, Colombo A, Sandri MT, Lamantia G, Colombo N, Civelli M, et al. Prevention of high-dose chemotherapy-induced cardiotoxicity in high-risk patients by angiotensin-converting enzyme inhibition. Circulation. 2006;114:2474–81.
    1. Armstrong GT, Oeffinger KC, Chen Y, Kawashima T, Yasui Y, Leisenring W, et al. Modifiable risk factors and major cardiac events among adult survivors of childhood cancer. J Clin Oncol. 2013;31:3673–80.
    1. StJude. Children's Hospital CCSS CHF Risk Calculator. 2015. . Accessed 13/06/16 2016.
    1. Ryberg M, Nielsen D, Skovsgaard T, Hansen J, Jensen BV, Dombernowsky P. Epirubicin cardiotoxicity: an analysis of 469 patients with metastatic breast cancer. J Clin Oncol. 1998;16:3502–8.
    1. Mertens AC, Liu Q, Neglia JP, Wasilewski K, Leisenring W, Armstrong GT, et al. Cause-specific late mortality among 5-year survivors of childhood cancer: the childhood cancer survivor study. J Natl Cancer Inst. 2008;100:1368–79.
    1. Pavlidis NA. Coexistence of pregnancy and malignancy. Oncologist. 2002;7:279–87.
    1. Pereg D, Koren G, Lishner M. The treatment of Hodgkin’s and non-Hodgkin’s lymphoma in pregnancy. Haematologica. 2007;92:1230–7.
    1. Lipshultz SE, Miller TL, Lipsitz SR, Neuberg DS, Dahlberg SE, Colan SD, et al. Continuous versus bolus infusion of doxorubicin in children with ALL: long-term cardiac outcomes. Pediatrics. 2012;130:1003–11.
    1. Dresdale AR, Barr LH, Bonow RO, Mathisen DJ, Myers CE, Schwartz DE, et al. Prospective randomized study of the role of N-acetyl cysteine in reversing doxorubicin-induced cardiomyopathy. Am J Clin Oncol. 1982;5:657–63.
    1. Myers C, Bonow R, Palmeri S, Jenkins J, Corden B, Locker G, et al. A randomized controlled trial assessing the prevention of doxorubicin cardiomyopathy by N-acetylcysteine. Semin Oncol. 1983;10:53–5.
    1. Milei J, Marantz A, Ale J, Vazquez A, Buceta JE. Prevention of adriamycin-induced cardiotoxicity by prenylamine: a pilot double blind study. Cancer Drug Deliv. 1987;4:129–36.
    1. Kraft J, Grille W, Appelt M, Hossfeld DK, Eichelbaum M, Koslowski B, et al. Effects of verapamil on anthracycline-induced cardiomyopathy: preliminary results of a prospective multicenter trial. Haematol Blood Transfus. 1990;33:566–570.
    1. Nazeyrollas P, Frances C, Prevost A, Costa B, Lorenzato M, Kantelip JP, et al. Efficiency of amifostine as a protection against doxorubicin toxicity in rats during a 12-day treatment. Anticancer Res. 2003;23:405–9.
    1. Dragojevic-Simic VM, Dobric SL, Bokonjic DR, Vucinic ZM, Sinovec SM, Jacevic VM, et al. Amifostine protection against doxorubicin cardiotoxicity in rats. Anti-Cancer Drugs. 2004;15:169–78.
    1. Iarussi D, Auricchio U, Agretto A, Murano A, Giuliano M, Casale F, et al. Protective effect of coenzyme Q10 on anthracyclines cardiotoxicity: control study in children with acute lymphoblastic leukemia and non-Hodgkin lymphoma. Mol Asp Med. 1994;15:s207–12.
    1. Ammar el SM, Said SA, Suddek GM, El-Damarawy SL. Amelioration of doxorubicin-induced cardiotoxicity by deferiprone in rats. Can J Physiol Pharmacol. 2011;89:269–76.
    1. Popelova O, Sterba M, Simunek T, Mazurova Y, Guncova I, Hroch M, et al. Deferiprone does not protect against chronic anthracycline cardiotoxicity in vivo. J Pharmacol Exp Ther. 2008;326:259–69.
    1. Hasinoff BB, Patel D, Wu X. The oral iron chelator ICL670A (deferasirox) does not protect myocytes against doxorubicin. Free Radic Biol Med. 2003;35:1469–79.
    1. Asselin BL, Devidas M, Chen L, Franco VI, Pullen J, Borowitz MJ, et al. Cardioprotection and safety of dexrazoxane in patients treated for newly diagnosed T-cell acute lymphoblastic leukemia or advanced-stage lymphoblastic non-Hodgkin lymphoma: a report of the Children's oncology group randomized trial pediatric oncology group 9404. J Clin Oncol. 2016;34:854–62.
    1. Schupp N, Schmid U, Heidland A, Stopper H. Rosuvastatin protects against oxidative stress and DNA damage in vitro via upregulation of glutathione synthesis. Atherosclerosis. 2008;199:278–87.
    1. Acar Z, Kale A, Turgut M, Demircan S, Durna K, Demir S, et al. Efficiency of atorvastatin in the protection of anthracycline-induced cardiomyopathy. J Am Coll Cardiol. 2011;58(9):988–989. doi: 10.1016/j.jacc.2011.05.025.
    1. Seicean S, Seicean A, Plana JC, Budd GT, Marwick TH. Effect of statin therapy on the risk for incident heart failure in patients with breast cancer receiving anthracycline chemotherapy: an observational clinical cohort study. J Am Coll Cardiol. 2012;60:2384–90.
    1. Bosch X, Rovira M, Sitges M, Domenech A, Ortiz-Perez JT, de Caralt TM, et al. 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;61:2355–62.
    1. Cardinale D, Colombo A, Bacchiani G, Tedeschi I, Meroni CA, Veglia F, et al. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation. 2015;131:1981–8.
    1. Tashakori Beheshti A, Mostafavi Toroghi H, Hosseini G, Zarifian A, Homaei Shandiz F, Fazlinezhad A. Carvedilol administration can prevent doxorubicin-induced cardiotoxicity: a double-blind randomized trial. Cardiology. 2016;134:47–53.
    1. El-Shitany NA, Tolba OA, El-Shanshory MR, El-Hawary EE. Protective effect of carvedilol on adriamycin-induced left ventricular dysfunction in children with acute lymphoblastic leukemia. J Card Fail. 2012;18:607–13.
    1. Ewer MS, Ali MK, Gibbs HR, Swafford J, Graff KL, Cangir A, et al. Cardiac diastolic function in pediatric patients receiving doxorubicin. Acta Oncol. 1994;33:645–9.
    1. Kaya MG, Ozkan M, Gunebakmaz O, Akkaya H, Kaya EG, Akpek M, et al. Protective effects of nebivolol against anthracycline-induced cardiomyopathy: a randomized control study. Int J Cardiol. 2013;167:2306–10.
    1. Gulati G, Heck SL, Ree AH, Hoffmann P, Schulz-Menger J, Fagerland MW, et al. Prevention of cardiac dysfunction during adjuvant breast cancer therapy (PRADA): a 2 × 2 factorial, randomized, placebo-controlled, double-blind clinical trial of candesartan and metoprolol. Eur Heart J. 2016;37:1671–80.
    1. Bautin AE, Galagudza MM, Datsenko SV, Tashkhanov DM, Marichev AO, Bakanov A, et al. Effects of remote ischemic preconditioning on perioperative period in elective aortic valve replacement. Anesteziol Reanimatol. 2014:11–7.
    1. Davies WR, Brown AJ, Watson W, McCormick LM, West NE, Dutka DP, et al. Remote ischemic preconditioning improves outcome at 6 years after elective percutaneous coronary intervention: the CRISP stent trial long-term follow-up. Circ Cardiovasc Interv. 2013;6:246–251. doi: 10.1161/CIRCINTERVENTIONS.112.000184.
    1. Li C, Xu M, Wu Y, Li YS, Huang WQ, Liu KX. Limb remote ischemic preconditioning attenuates lung injury after pulmonary resection under propofol-remifentanil anesthesia: a randomized controlled study. Anesthesiology. 2014;121:249–59.
    1. Pryzklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P. Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993;87:893–899. doi: 10.1161/01.CIR.87.3.893.
    1. Sloth AD, Schmidt MR, Munk K, Kharbanda RK, Redington AN, Schmidt M, et al. CONDI investigators. Improved long-term clinical outcomes in patients with ST-elevation myocardial infarction undergoing remote ischaemic conditioning as an adjunct to primary percutaneous coronary intervention. Eur Heart J. 2014;35:168–175. doi: 10.1093/eurheartj/eht369.
    1. White SK, Frohlich GM, Sado DM, Maestrini V, Fontana M, Treibel TA, et al. Remote ischemic conditioning reduces myocardial infarct size and edema in patients with ST-segment elevation myocardial infarction. JACC Cardiovasc Interv. 2014;14:01073–01075.
    1. Zuo B, Wang F, Song Z, Xu M, Wang G. Using remote ischemic conditioning to reduce acute kidney injury in patients undergoing percutaneous coronary intervention: a meta-analysis. Curr Med Res Opin. 2015:1–20.
    1. Pickard JM, Davidson SM, Hausenloy DJ, Yellon DM. Co-dependence of the neural and humoral pathways in the mechanism of remote ischemic conditioning. Basic Res Cardiol. 2016;111:50.

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