Cardiotoxicity and cardioprotection in childhood cancer

Acta Haematologica

Volumn 132, Issue 3-4, 2014, Pages 391-399

  Lipshultz, Steven E ^a,b,c   Sambatakos, Peter ^a,b   Maguire, Michael ^a,b   Karnik, Ruchika ^a,b   Ross, Samuel W ^a,b   Franco, Vivian I ^a   Miller, Tracie L ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Miami Jackson Memorial Medical Center   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardioprotection; Cardiotoxicity; Childhood cancer survivors

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMINO TERMINAL PRO BRAIN NATRIURETIC PEPTIDE; ANTHRACYCLINE DERIVATIVE; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CARDIOLIPIN; CARNITINE; CARVEDILOL; DNA TOPOISOMERASE (ATP HYDROLYSING); FREE RADICAL; GLUTATHIONE; RAZOXANE; TROPONIN T; UBIQUINONE; ANTHRACYCLINE; ANTINEOPLASTIC AGENT; CARDIOTONIC AGENT;

AGE; ALCOHOL CONSUMPTION; ALLELE; ALTERNATIVE MEDICINE; ARTICLE; BLOOD VESSEL WALL; C282Y ALLELE; CANCER SURVIVAL; CANCER SURVIVOR; CARDIOTOXICITY; CARDIOVASCULAR MAGNETIC RESONANCE; CARDIOVASCULAR PARAMETERS; CBR3 HOMOZYGOUS G GENOTYPE; CHILD; CHILDHOOD CANCER; DNA DAMAGE; ENDOCRINE DISEASE; ENERGY DRINK; ENZYME ACTIVITY; EVENT FREE SURVIVAL; FAILURE TO THRIVE; FEMININITY; GENETIC DISORDER; GENOTYPE; HEART LEFT VENTRICLE MASS; HEART MUSCLE BIOPSY; HEART PROTECTION; HEART VENTRICLE REMODELING; HIGH RISK POPULATION; HUMAN; INFLAMMATION; KIDNEY DISEASE; LEFT VENTRICLE DIMENSION; LEFT VENTRICLE FRACTIONAL SHORTENING; LIPID PEROXIDATION; LIVER DISEASE; LUNG DISEASE; METABOLIC DISORDER; MUSCULOSKELETAL DISEASE; OBESITY; OXIDATIVE STRESS; PATIENT MONITORING; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION INJURY; RISK FACTOR; SCREENING TEST; SEDENTARY LIFESTYLE; SINGLE NUCLEOTIDE POLYMORPHISM; TOBACCO USE; TRISOMY 21; WALL STRESS; EVIDENCE BASED PRACTICE; GAMMA RADIATION; HEART DISEASE; NEOPLASM; PATHOLOGY; REVIEW;

ANTHRACYCLINES; ANTINEOPLASTIC AGENTS; CARDIOTONIC AGENTS; EVIDENCE-BASED PRACTICE; GAMMA RAYS; HEART DISEASES; HUMANS; NEOPLASMS; RISK FACTORS;

EID: 84908617799     PISSN: 00015792     EISSN: 14219662     Source Type: Journal    
DOI: 10.1159/000360238     Document Type: Article

References (70)

1. American Cancer Society: Cancer Facts and Figures 2012. Atlanta, American Cancer Society, 2012.
2. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds): SEER Cancer Statistics Review, 1975-2010. Bethesda, National Cancer Institute. http://seer.cancer.gov/csr/1975-2010/(based on November 2012 SEER data submission, posted to the SEER web site, April 2013).
3. Oeffinger KC, Mertens AC, Sklar CA, Kawashima T, Hudson MM, Meadows AT, Friedman DL, Marina N, Hobbie W, Kadan-Lottick NS, Schwartz CL, Leisenring W, Robison LL; Childhood Cancer Survivor Study: Chronic health conditions in adult survivors of childhood cancer. N Engl J Med 2006; 355: 1572-1582.
4. Mulrooney DA, Yeazel MW, Kawashima T, Mertens AC, Mitby P, Stovall M, Donaldson SS, Green DM, Sklar CA, Robison LL, Leisenring WM: Cardiac outcomes in a cohort of adult survivors of childhood and adolescent cancer: Retrospective analysis of the Childhood Cancer Survivor Study cohort. BMJ 2009; 339:b4606.
5. Tukenova M, Guibout C, Oberlin O, Doyon F, Mousannif A, Haddy N, Guérin S, Pacquement H, Aouba A, Hawkins M, Winter D, Bourhis J, Lefkopoulos D, Diallo I, de Vathaire F: Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer. J Clin Oncol 2010; 28: 1308-1315.
6. Armstrong GT, Oeffinger KC, Chen Y, Kawashima T, Yasui Y, Leisenring W, Stovall M, Chow EJ, Sklar CA, Mulrooney DA, Mertens AC, Border W, Durand JB, Robison LL, Meacham LR: Modifiable risk factors and major cardiac events among adult survivors of childhood cancer. J Clin Oncol 2013; 31: 3673-3680.
7. 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.
8. Landy DC, Miller TL, Lipsitz SR, Lopez-Mitnik G, Hinkle AS, Constine LS, Adams MJ, Lipshultz SE: Cranial irradiation as an additional risk factor for anthracycline cardiotoxicity in childhood cancer survivors: An analysis from the cardiac risk factors in childhood cancer survivors study. Pediatr Cardiol 2013; 34: 826-834.
9. Adão R, de Keulenaer G, Leite-Moreira A, Brás-Silva C: Cardiotoxicity associated with cancer therapy: Pathophysiology and prevention. Rev Portug Cardiol (English ed) 2013; 32: 395-409.
10. Diamond M, Franco V: Preventing and treating anthracycline-related cardiotoxicity in survivors of childhood cancer. Curr Cancer Ther Rev 2012; 8: 141-151.
11. Franco VI, Henkel JM, Miller TL, Lipshultz SE: Cardiovascular effects in childhood cancer survivors treated with anthracyclines. Cardiol Res Pract 2011; 2011: 134679.
12. Dillenburg RF, Nathan P, Mertens L: Educational paper: Decreasing the burden of cardiovascular disease in childhood cancer survivors: An update for the pediatrician. Eur J Pediatr 2013; 172: 1149-1160.
13. Von Hoff DD, Layard MW, Basa P, Davis HL Jr, Von Hoff AL, Rozencweig M, Muggia FM: Risk factors for doxorubicin-induced congestive heart failure. Ann Intern Med 1979; 91: 710-717.
14. Nysom K, Holm K, Lipsitz SR, Mone SM, Colan SD, Orav EJ, Sallan SE, Olsen JH, Hertz H, Jacobsen JR, Lipshultz SE: Relationship between cumulative anthracycline dose and late cardiotoxicity in childhood acute lymphoblastic leukemia. J Clin Oncol 1998; 16: 545-550.
15. Vandecruys E, Mondelaers V, De Wolf D, Benoit Y, Suys B: Late cardiotoxicity after low dose of anthracycline therapy for acute lymphoblastic leukemia in childhood. J Cancer Surviv 2012; 6: 95-101.
16. Lipshultz SE, Adams MJ: Cardiotoxicity after childhood cancer: Beginning with the end in mind. J Clin Oncol 2010; 28: 1276-1281.
17. Van der Pal HJ, van Dalen EC, Hauptmann M, Kok WE, Caron HN, van den Bos C, Oldenburger F, Koning CC, van Leeuwen FE, Kremer LC: Cardiac function in 5-year survivors of childhood cancer: A long-term followup study. Arch Intern Med 2010; 170: 1247-1255.
18. Swain SM, Whaley FS, Ewer MS: Congestive heart failure in patients treated with doxorubicin: A retrospective analysis of three trials. Cancer 2003; 97: 2869-2879.
19. Lipshultz SE, Lipsitz SR, Sallan SE, Dalton VM, Mone SM, Gelber RD, Colan SD: Chronic progressive cardiac dysfunction years after doxorubicin therapy for childhood acute lymphoblastic leukemia. J Clin Oncol 2005; 23: 2629-2636.
20. Krischer JP, Epstein S, Cuthbertson DD, Goorin AM, Epstein ML, Lipshultz SE: Clinical cardiotoxicity following anthracycline treatment for childhood cancer: The Pediatric Oncology Group experience. J Clin Oncol 1997; 15: 1544-1552.
21. Wang L, Weinshilboum R: Thiopurine Smethyltransferase pharmacogenetics: Insights, challenges and future directions. Oncogene 2006; 25: 1629-1638.
22. Deng S, Wojnowski L: Genotyping the risk of anthracycline-induced cardiotoxicity. Cardiovasc Toxicol 2007; 7: 129-134.
23. Blanco JG, Leisenring WM, Gonzalez-Covarrubias VM, Kawashima TI, Davies SM, Relling MV, Robison LL, Sklar CA, Stovall M, Bhatia S: 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 2008; 112: 2789-2795.
24. Lipshultz SE, Lipsitz SR, Kutok JL, Miller TL, Colan SD, Neuberg DS, Stevenson KE, Fleming MD, Sallan SE, Franco VI, Henkel JM, Asselin BL, Athale UH, Clavell LA, Michon B, Laverdiere C, Larsen E, Kelly KM, Silverman LB: Impact of hemochromatosis gene mutations on cardiac status in doxorubicin-treated survivors of childhood high-risk leukemia. Cancer 2013; 119: 3555-3562.
25. Miranda CJ, Makui H, Soares RJ, Bilodeau M, Mui J, Vali H, Bertrand R, Andrews NC, Santos MM: Hfe deficiency increases susceptibility to cardiotoxicity and exacerbates changes in iron metabolism induced by doxorubicin. Blood 2003; 102: 2574-2580.
26. 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: Anthracycline-related cardiomyopathy after childhood cancer: Role of polymorphisms in carbonyl reductase genes-A report from the Children's Oncology Group. J Clin Oncol 2012; 30: 1415-1421.
27. Qureshi MY, Wilkinson JD, Lipshultz SE: The relationship of childhood obesity with cardiomyopathy and heart failure; in Lipshultz SE, Messiah SE, Miller TL (eds): Pediatric Metabolic Syndrome. London, Springer, 2012, pp 199-215.
28. Miller TL, Lipsitz SR, Lopez-Mitnik G, Hinkle AS, Constine LS, Adams MJ, French C, Proukou C, Rovitelli A, Lipshultz SE: Characteristics and determinants of adiposity in pediatric cancer survivors. Cancer Epidemiol Biomarkers Prev 2010; 19: 2013-2022.
29. Landy DC, Lipsitz SR, Kurtz JM, Hinkle AS, Constine LS, Adams MJ, Lipshultz SE, Miller TL: Dietary quality, caloric intake, and adiposity of childhood cancer survivors and their siblings: An analysis from the Cardiac Risk Factors in Childhood Cancer Survivors Study. Nutr Cancer 2013; 65: 547-555.
30. Miller AM, Lopez-Mitnik G, Somarriba G, Lipsitz SR, Hinkle AS, Constine LS, Lipshultz SE, Miller TL: Exercise capacity in long-term survivors of pediatric cancer: An analysis from the Cardiac Risk Factors in Childhood Cancer Survivors Study. Pediatr Blood Cancer 2013; 60: 663-668.
31. Klosky JL, Howell CR, Li Z, Foster RH, Mertens AC, Robison LL, Ness KK: Risky health behavior among adolescents in the Childhood Cancer Survivor Study cohort. J Pediatr Psychol 2012; 37: 634-646.
32. Kahalley LS, Robinson LA, Tyc VL, Hudson MM, Leisenring W, Stratton K, Mertens AC, Zeltzer L, Robison LL, Hinds PS: Risk factors for smoking among adolescent survivors of childhood cancer: A report from the Childhood Cancer Survivor Study. Pediatr Blood Cancer 2012; 58: 428-434.
33. Lakier JB: Smoking and cardiovascular disease. Am J Med 1992; 93(1A):8S-12S.
34. Silber JH, Jakacki RI, Larsen RL, Goldwein JW, Barber G: Increased risk of cardiac dysfunction after anthracyclines in girls. Med Pediatr Oncol 1993; 21: 477-479.
35. Lipshultz SE, Lipsitz SR, Mone SM, Goorin AM, Sallan SE, Sanders SP, Orav EJ, Gelber RD, Colan SD: Female sex and drug dose as risk factors for late cardiotoxic effects of doxorubicin therapy for childhood cancer. N Engl J Med 1995; 332: 1738-1743.
36. Bovelli D, Plataniotis G, Roila F: Cardiotoxicity of chemotherapeutic agents and radiotherapy-related heart disease: ESMO Clinical Practice Guidelines. Ann Oncol 2010; 21 (suppl 5):v277-v282.
37. Trachtenberg BH, Landy DC, Franco VI, Henkel JM, Pearson EJ, Miller TL, Lipshultz SE: Anthracycline-associated cardiotoxicity in survivors of childhood cancer. Pediatr Cardiol 2011; 32: 342-353.
38. Gottsauner-Wolf M, Schedlmayer-Duit J, Porenta G, Gwechenberger M, Huber K, Glogar D, Probst P, Sochor H: Assessment of left ventricular function: Comparison between radionuclide angiography and semiquantitative two-dimensional echocardiographic analysis. Eur J Nucl Med 1996; 23: 1613-1618.
39. Lipshultz SE, Miller TL, Scully RE, Lipsitz SR, Rifai N, Silverman LB, Colan SD, Neuberg DS, Dahlberg SE, Henkel JM, Asselin BL, Athale UH, Clavell LA, Laverdière C, Michon B, Schorin MA, Sallan SE: Changes in cardiac biomarkers during doxorubicin treatment of pediatric patients with high-risk acute lymphoblastic leukemia: Associations with longterm echocardiographic outcomes. J Clin Oncol 2012; 30: 1042-1049.
40. Legha SS, Benjamin RS, Mackay B, Ewer M, Wallace S, Valdivieso M, Rasmussen SL, Blumenschein GR, Freireich EJ: Reduction of doxorubicin cardiotoxicity by prolonged continuous intravenous infusion. Ann Intern Med 1982; 96: 133-139.
41. Lipshultz SE, Miller TL, Lipsitz SR, Neuberg DS, Dahlberg SE, Colan SD, Silverman LB, Henkel JM, Franco VI, Cushman LL, Asselin BL, Clavell LA, Athale U, Michon B, Laverdière C, Schorin MA, Larsen E, Usmani N, Sallan SE; Dana-Farber Cancer Institute Acute Lymphoblastic Leukemia Consortium: Continuous versus bolus infusion of doxorubicin in children with ALL: Long-term cardiac outcomes. Pediatrics 2012; 130: 1003-1011.
42. Lipshultz SE, Giantris AL, Lipsitz SR, Kimball Dalton V, Asselin BL, Barr RD, Clavell LA, Hurwitz CA, Moghrabi A, Samson Y, Schorin MA, Gelber RD, Sallan SE, Colan SD: Doxorubicin administration by continuous infusion is not cardioprotective: The Dana-Farber 91-01 Acute Lymphoblastic Leukemia protocol. J Clin Oncol 2002; 20: 1677-1682.
43. Barry E, Alvarez JA, Scully RE, Miller TL, Lipshultz SE: Anthracycline-induced cardiotoxicity: Course, pathophysiology, prevention and management. Expert Opin Pharmacother 2007; 8: 1039-1058.
44. French Epirubicin Study Group: A prospective randomized phase III trial comparing combination chemotherapy with cyclophosphamide, fluorouracil, and either doxorubicin or epirubicin. J Clin Oncol 1988; 6: 679-688.
45. Phase III randomized study of fluorouracil, epirubicin, and cyclophosphamide versus fluorouracil, doxorubicin, and cyclophosphamide in advanced breast cancer: An Italian multicentre trial. Italian Multicentre Breast Study with Epirubicin. J Clin Oncol 1988; 6: 976-982.
46. Van Dalen EC, Michiels EM, Caron HN, Kremer LC: Different anthracycline derivates for reducing cardiotoxicity in cancer patients. Cochrane Database Syst Rev 2010; 5: CD005006.
47. Meinardi MT, van Veldhuisen DJ, Gietema JA, Dolsma WV, Boomsma F, van den Berg MP, Volkers C, Haaksma J, de Vries EG, Sleijfer DT, van der Graaf WT: Prospective evaluation of early cardiac damage induced by epirubicin-containing adjuvant chemotherapy and locoregional radiotherapy in breast cancer patients. J Clin Oncol 2001; 19: 2746-2753.
48. Cowan JD, Neidhart J, McClure S, Coltman CA Jr, Gumbart C, Martino S, Hutchins LF, Stephens RL, Vaughan CB, Osborne CK: Randomized trial of doxorubicin, bisantrene, and mitoxantrone in advanced breast cancer: A Southwest Oncology Group study. J Natl Cancer Inst 1991; 83: 1077-1084.
49. Gabizon AA, Lyass O, Berry GJ, Wildgust M: Cardiac safety of pegylated liposomal doxorubicin (Doxil/Caelyx) demonstrated by endomyocardial biopsy in patients with advanced malignancies. Cancer Invest 2004; 22: 663-669.
50. Leonard RC, Williams S, Tulpule A, Levine AM, Oliveros S: Improving the therapeutic index of anthracycline chemotherapy: Focus on liposomal doxorubicin (Myocet). Breast 2009; 18: 218-224.
51. Sieswerda E, Kremer LC, Caron HN, van Dalen EC: The use of liposomal anthracycline analogues for childhood malignancies: A systematic review. Eur J Cancer 2011; 47: 2000-2008.
52. Safra T, Muggia F, Jeffers S, Tsao-Wei DD, Lyass O, Henderson R, Berry G, Gabizon A: Pegylated liposomal doxorubicin (Doxil): Reduced clinical cardiotoxicity in patients reaching or exceeding cumulative doses of 500 mg/m 2 . Ann Oncol 2000; 11: 1029-1033.
53. Kaspers GJ, Zimmermann M, Reinhardt D, Gibson BE, Tamminga RY, Aleinikova O, Armendariz H, Dworzak M, Ha SY, Hasle H, Hovi L, Maschan A, Bertrand Y, Leverger GG, Razzouk BI, Rizzari C, Smisek P, Smith O, Stark B, Creutzig U: Improved outcome in pediatric relapsed acute myeloid leukemia: Results of a randomized trial on liposomal daunorubicin by the International BFM Study Group. J Clin Oncol 2013; 31: 599-607.
54. Lipshultz SE, Rifai N, Dalton VM, Levy DE, Silverman LB, Lipsitz SR, Colan SD, Asselin BL, Barr RD, Clavell LA, Hurwitz CA, Moghrabi A, Samson Y, Schorin MA, Gelber RD, Sallan SE: The effect of dexrazoxane on myocardial injury in doxorubicin-treated children with acute lymphoblastic leukemia. N Engl J Med 2004; 351: 145-153.
55. Lipshultz SE, Scully RE, Lipsitz SR, Sallan SE, Silverman LB, Millter 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: 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.
56. Lyu YL, Kerrigan JE, Lin CP, Azarova AM, Tsai YC, Ban Y, Liu LF: Topoisomerase II-beta mediated DNA double-strand breaks: Implications in doxorubicin cardiotoxicity and prevention by dexrazoxane. Cancer Res 2007; 67: 8839-8846.
57. Van Dalen EC, Caron HN, Dickinson HO, Kremer LC: Cardioprotective interventions for cancer patients receiving anthracyclines. Cochrane Database Syst Rev 2011; 6: CD003917.
58. Wouters KA, Kremer LC, Miller TL, Herman EH, Lipshultz SE: Protecting against anthracycline-induced myocardial damage: A review of the most promising strategies. Br J Haematol 2005; 131: 561-578.
59. Feuerstein GZ, Ruffolo RR Jr: Carvedilol, a novel multiple action antihypertensive agent with antioxidant activity and the potential for myocardial and vascular protection. Eur Heart J 1995; 16(suppl F):38-42.
60. Spallarossa P, Garibaldi S, Altieri P, Fabbi P, Manca V, Nasti S, Rossettin P, Ghigliotti G, Ballestrero A, Patrone F, Barsotti A, Brunelli C: Carvedilol prevents doxorubicin-induced free radical release and apoptosis in cardiomyocytes in vitro. J Mol Cell Cardiol 2004; 37: 837-846.
61. Matsui H, Morishima I, Numaguchi Y, Toki Y, Okumura K, Hayakawa T: Protective effects of carvedilol against doxorubicin-induced cardiomyopathy in rats. Life Sci 1999; 65: 1265-1274.
62. Granados-Principal S, Quiles JL, Ramirez-Tortosa CL, Sanchez-Rovira P, Ramirez-Tortosa MC: New advances in molecular mechanisms and the prevention of Adriamycin toxicity by antioxidant nutrients. Food Chem Toxicol 2010; 48: 1425-1438.
63. Iarussi D, Auricchio U, Agretto A, Murano A, Giuliano M, Casale F, Indolfi P, Iacono A: Protective effect of coenzyme Q on anthracyclines cardiotoxicity: Control study in children with acute lymphoblastic leukemia and non-Hodgkin lymphoma. Mol Aspects Med 1994; 15(suppl):s207-s212.
64. De Leonardis V, Neri B, Bacalli S, Cinelli P: Reduction of cardiac toxicity of anthracyclines by L-carnitine: Preliminary overview of clinical data. Int J Clin Pharmacol Res 1985; 5: 137-142.
65. Doroshow JH, Locker GY, Myers CE: Enzymatic defenses of the mouse heart against reactive oxygen metabolites: Alterations produced by doxorubicin. J Clin Invest 1980; 65: 128-135.
66. Arrick BA, Nathan CF, Griffith OW, Cohn ZA: Glutathione depletion sensitizes tumor cells to oxidative cytolysis. J Biol Chem 1982; 257: 1231-1237.
67. Suttorp N, Toepfer W, Roka L: Antioxidant defense mechanisms of endothelial cells: Glutathione redox cycle versus catalase. Am J Physiol 1986; 251:C671-C680.
68. Mohamed HE, El-Swefy SE, Hagar HH: The protective effect of glutathione administration on Adriamycin-induced acute cardiac toxicity in rats. Pharmacol Res 2000; 42: 115-121.
69. Ferrari R, Ceconi C, Curello S, Cargnoni A, Alfieri O, Pardini A, Marzollo P, Visioli O: Oxygen free radicals and myocardial damage: Protective role of thiol-containing agents. Am J Med 1991; 91(3C):95S-105S.
70. Lipshultz SE, Cochran TR, Franco VI, Miller TL: Treatment-related cardiotoxicity in survivors of childhood cancer. Nat Rev Clin Oncol 2013; 10: 697-710.