Radiation-induced heart disease: Pathologic abnormalities and putative mechanisms

Frontiers in Oncology

Volumn 5, Issue FEB, 2015, Pages

  Taunk, Neil K ^a   Haffty, Bruce G ^b   Kostis, John B ^c   Goyal, Sharad ^b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c University of Medicine and Dentistry of New Jersey   (United States)

Author keywords

Breast cancer; Radiation fibrosis; Radiation side effects; Radiation therapy

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 3; CONNECTIVE TISSUE GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBRONECTIN; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN; PLATELET DERIVED GROWTH FACTOR; PROTEOGLYCAN; SOMATOMEDIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR;

BLOOD VESSEL INJURY; CANCER RADIOTHERAPY; CARDIOMYOPATHY; CORONARY ARTERY DISEASE; FIBROSIS; HEART; HEART ARRHYTHMIA; HEART DISEASE; HEART FUNCTION; HEART MUSCLE FIBROSIS; HUMAN; IONIZING RADIATION; NONHUMAN; PATHOPHYSIOLOGY; PERICARDIAL DISEASE; RADIATION INDUCED HEART DISEASE; REVIEW; VALVULAR HEART DISEASE; VASCULITIS; WOUND HEALING;

EID: 84923559134     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2015.00039     Document Type: Review

References (58)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin (2014) 64(1):9-29. doi: 10.3322/caac.21208
2. Clarke M, Collins R, Darby S, Davies C, Elphinstone P, Evans E, et al. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet (2005) 366(9503):2087-106. doi:10.1016/S0140-6736(05)67887-7
3. Darby SC, Cutter DJ, Boerma M, Constine LS, Fajardo LF, Kodama K, et al. Radiation-related heart disease: current knowledge and future prospects. Int J Radiat Oncol Biol Phys (2010) 76(3):656-65. doi:10.1016/j.ijrobp.2009.09.064
4. Fajardo LF, Stewart JR, Cohn KE. Morphology of radiation-induced heart disease. Arch Pathol (1968) 86(5):512-9.
5. Stewart JR, Fajardo LF. Radiation-induced heart disease. Clinical and experimental aspects. Radiol Clin North Am (1971) 9(3):511-31.
6. Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, et al. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med (2013) 368(11):987-98. doi:10.1056/NEJMoa1209825
7. Adams MJ, Hardenbergh PH, Constine LS, Lipshultz SE. Radiation-associated cardiovascular disease. Crit Rev Oncol Hematol (2003) 45(1):55-75. doi:10.1016/S1040-8428(01)00227-X
8. Cameron J, Oesterle SN, Baldwin JC, Hancock EW. The etiologic spectrum of constrictive pericarditis. Am Heart J (1987) 113(2 Pt 1):354-60. doi:10.1016/0002-8703(87)90278-X
9. Martin RG, Ruckdeschel JC, Chang P, Byhardt R, Bouchard RJ, Wiernik PH. Radiation-related pericarditis. Am J Cardiol (1975) 35(2):216-20. doi:10.1016/0002-9149(75)90004-1
10. McEniery PT, Dorosti K, Schiavone WA, Pedrick TJ, Sheldon WC. Clinical and angiographic features of coronary artery disease after chest irradiation. Am J Cardiol (1987) 60(13):1020-4. doi:10.1016/0002-9149(87)90345-6
11. Stewart JR, Fajardo LF, Gillette SM, Constine LS. Radiation injury to the heart. Int J Radiat Oncol Biol Phys (1995) 31(5):1205-11. doi:10.1016/0360-3016(94)00656-6
12. Borges-Neto S, Coleman RE, Jones RH. Perfusion and function at rest and treadmill exercise using technetium-99m-sestamibi: comparison of one- and two-day protocols in normal volunteers. J Nucl Med (1990) 31(7):1128-32.
13. Brosius FC III, Waller BF, Roberts WC. Radiation heart disease. Analysis of 16 young (aged 15 to 33 years) necropsy patients who received over 3,500 rads to the heart. Am J Med (1981) 70(3):519-30. doi:10.1016/0002-9343(81)90574-X
14. Burns RJ, Bar-Shlomo BZ, Druck MN, Herman JG, Gilbert BW, Perrault DJ, et al. Detection of radiation cardiomyopathy by gated radionuclide angiography. Am J Med (1983) 74(2):297-302. doi:10.1016/0002-9343(83)90631-9
15. James TN. Anatomy of the coronary arteries in health and disease. Circulation (1965) 32(6):1020-33. doi:10.1161/01.CIR.32.6.1020
16. Nilsson G, Holmberg L, Garmo H, Duvernoy O, Sjögren I, Lagerqvist B, et al. Distribution of coronary artery stenosis after radiation for breast cancer. J Clin Oncol (2012) 30(4):380-6. doi:10.1200/JCO.2011.34.5900
17. Wynn TA. Fibrotic disease and the TH1/TH2 paradigm. Nat Rev Immunol (2004) 4(8):583-94. doi:10.1038/nri1412
18. Schultz-Hector S, Trott K-R. Radiation-induced cardiovascular diseases: is the epidemiologic evidence compatible with the radiobiologic data? Int J Radiat Oncol Biol Phys (2007) 67(1):10-8. doi:10.1016/j.ijrobp.2006.08.071
19. Yarnold J, Vozenin Brotons M-C. Pathogenetic mechanisms in radiation fibrosis. Radiother Oncol (2010) 97(1):149-61. doi:10.1016/j.radonc.2010.09.002
20. Neta R, Douches S, Oppenheim JJ. Interleukin 1 is a radioprotector. J Immunol (1986) 136(7):2483-5.
21. Stewart JR, Fajardo LF. Radiation-induced heart disease: an update. Prog Cardiovasc Dis (1984) 27(3):173-94. doi:10.1016/0033-0620(84)90003-3
22. Rodemann HP, Bamberg M. Cellular basis of radiation-induced fibrosis. Radiother Oncol (1995) 35(2):83-90. doi:10.1016/0167-8140(95)01540-W
23. Sherman ML, Datta R, Hallahan DE, Weichselbaum RR, Kufe DW. Ionizing radiation regulates expression of the c-jun protooncogene. Proc Natl Acad Sci U S A (1990) 87(15):5663-6. doi:10.1073/pnas.87.15.5663
24. Martin M, Lefaix J-L, Delanian S. TGF-ß1 and radiation fibrosis: a master switch and a specific therapeutic target? Int J Radiat Oncol Biol Phys (2000) 47(2):277-90. doi:10.1016/S0360-3016(00)00435-1
25. Rodemann HP, Binder A, Bamberg M. Radiation-induced fibrosis: experimental studies. In: Dunst J, Sauer R, editors. Late Sequelae in Oncology. Berlin: Springer (1995). p. 93-7.
26. Rodemann HP, Peterson HP, Schwenke K, von Wangenheim KH. Terminal differentiation of human fibroblasts is induced by radiation. Scanning Microsc (1991) 5(4):1135-42.
27. Weigel C, Schmezer P, Plass C, Popanda O. Epigenetics in radiation-induced fibrosis. Oncogene (2014) 55(12):1237-9. doi:10.1038/onc.2014.145
28. Weintraub NL, Jones WK, Manka D. Understanding radiation-induced vascular disease. J Am Coll Cardiol (2010) 55(12):1237-9. doi:10.1016/j.jacc.2009.11.053
29. Halle M, Gabrielsen A, Paulsson-Berne G, Gahm C, Agardh HE, Farnebo F, et al. Sustained inflammation due to nuclear factor-kappa B activation in irradiated human arteries. J Am Coll Cardiol (2010) 55(12):1227-36. doi:10.1016/j.jacc.2009.10.047
30. Cardiovasc Radiat Med (1999) 1(1):108-10.
31. Fajardo LF. The pathology of ionizing radiation as defined by morphologic patterns. Acta Oncol (2005) 44(1):13-22. doi:10.1080/02841860510007440
32. Fajardo L-G LF, Prionas SD, Kaluza GL, Raizner AE. Acute vasculitis after endovascular brachytherapy. Int J Radiat Oncol Biol Phys (2002) 53(3):714-9. doi:10.1016/S0360-3016(02)02759-1
33. Brosius Iii FC, Waller BF, Roberts WC. Radiation heart disease: analysis of 16 young (aged 15 to 33 years) necropsy patients who received over 3,500 rads to the heart. Am J Med (1981) 70(3):519-30. doi:10.1016/0002-9343(81)90574-X
34. Fajardo LF, Stewart JR. Pathogenesis of radiation-induced myocardial fibrosis. Lab Invest (1973) 29(2):244-57.
35. Stewart FA, Heeneman S, Te Poele J, Kruse J, Russell NS, Gijbels M, et al. Ionizing radiation accelerates the development of atherosclerotic lesions in ApoE-/- mice and predisposes to an inflammatory plaque phenotype prone to hemorrhage. Am J Pathol (2006) 168(2):649-58. doi:10.2353/ajpath.2006.050409
36. Mulrooney DA, Yeazel MW, Kawashima T, Mertens AC, Mitby P, Stovall M, et al. 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. doi:10.1136/bmj.b4606
37. Tukenova M, Guibout C, Oberlin O, Doyon F, Mousannif A, Haddy N, et al. Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer. J Clin Oncol (2010) 28(8):1308-15. doi:10.1200/JCO.2008.20.2267
38. Mitchel RE, Hasu M, Bugden M, Wyatt H, Little MP, Gola A, et al. Low-dose radiation exposure and atherosclerosis in ApoE-/- mice. Radiat Res (2011) 175(5):665-76. doi:10.1667/RR2176.1
39. Chello M, Mastroroberto P, Romano R, Zofrea S, Bevacqua I, Marchese AR. Changes in the proportion of types I and III collagen in the left ventricular wall of patients with post-irradiative pericarditis. Cardiovasc Surg (1996) 4(2):222-6. doi:10.1016/0967-2109(96)82320-9
40. Marks LB, Yu X, Prosnitz RG, Zhou SM, Hardenbergh PH, Blazing M, et al. The incidence and functional consequences of RT-associated cardiac perfusion defects. Int J Radiat Oncol Biol Phys (2005) 63(1):214-23. doi:10.1016/j.ijrobp.2005.01.029
41. Schultz-Hector S. Radiation-induced heart disease: review of experimental data on dose response and pathogenesis. Int J Radiat Biol (1992) 61(2):149-60. doi:10.1080/09553009214550761
42. Schultz-Hector S, Böhm M, Blöchel A, Dominiak P, Erdmann E, Müller-Schauenburg W, et al. Radiation-induced heart disease: morphology, changes in catecholamine synthesis and content, beta-adrenoceptor density, and hemodynamic function in an experimental model. Radiat Res (1992) 129(3):281-9. doi:10.2307/3578027
43. Schultz-Hector S, Sund M, Thames HD. Fractionation response and repair kinetics of radiation-induced heart failure in the rat. Radiother Oncol (1992) 23(1):33-40. doi:10.1016/0167-8140(92)90303-C
44. Chung E, Corbett JR, Moran JM, Griffith KA, Marsh RB, Feng M, et al. Is there a dose-response relationship for heart disease with low-dose radiation therapy? Int J Radiat Oncol Biol Phys (2013) 85(4):959-64. doi:10.1016/j.ijrobp.2012.08.002
45. Hardenbergh PH, Munley MT, Bentel GC, Kedem R, Borges-Neto S, Hollis D, et al. Cardiac perfusion changes in patients treated for breast cancer with radiation therapy and doxorubicin: preliminary results. Int J Radiat Oncol Biol Phys (2001) 49(4):1023-8. doi:10.1016/S0360-3016(00)01531-5
46. Veinot JP, Edwards WD. Pathology of radiation-induced heart disease: a surgical and autopsy study of 27 cases. Hum Pathol (1996) 27(8):766-73. doi:10.1016/S0046-8177(96)90447-5
47. Carmel RJ, Kaplan HS. Mantle irradiation in Hodgkin's disease. An analysis of technique, tumor eradication, and complications. Cancer (1976) 37(6):2813-25. doi:10.1002/1097-0142(197606)37:6<2813::AID-CNCR2820370637>3.0.CO;2-S
48. Yusuf SW, Sami S, Daher IN. Radiation-induced heart disease: a clinical update. Cardiol Res Pract (2011) 2011:317659. doi:10.4061/2011/317659
49. Tötterman KJ, Pesonen E, Siltanen P. Radiation-related chronic heart disease. Chest (1983) 83(6):875-8. doi:10.1378/chest.83.6.875
50. Slama MS, Le Guludec D, Sebag C, Leenhardt AR, Davy JM, Pellerin DE, et al. Complete atrioventricular block following mediastinal irradiation: a report of six cases. Pacing Clin Electrophysiol (1991) 14(7):1112-8. doi:10.1111/j.1540-8159.1991.tb02842.x
51. Strender LE, Lindahl J, Larsson LE. Incidence of heart disease and functional significance of changes in the electrocardiogram 10 years after radiotherapy for breast cancer. Cancer (1986) 57(5):929-34. doi:10.1002/1097-0142(19860301)57:5<929::AID-CNCR2820570509>3.0.CO;2-6
52. Ng GA. Treating patients with ventricular ectopic beats. Heart (2006) 92(11):1707-12. doi:10.1136/hrt.2005.067843
53. Kostis JB, McCrone K, Moreyra AE, Gotzoyannis S, Aglitz NM, Natarajan N, et al. Premature ventricular complexes in the absence of identifiable heart disease. Circulation (1981) 63(6):1351-6. doi:10.1161/01.CIR.63.6.1351
54. Shapiro CL, Hardenbergh PH, Gelman R, Blanks D, Hauptman P, Recht A, et al. Cardiac effects of adjuvant doxorubicin and radiation therapy in breast cancer patients. J Clin Oncol (1998) 16(11):3493-501.
55. Horton JA, Hudak KE, Chung EJ, White AO, Scroggins BT, Burkeen JF, et al. Mesenchymal stem cells inhibit cutaneous radiation-induced fibrosis by suppressing chronic inflammation. Stem Cells (2013) 31(10):2231-41. doi:10.1002/stem.1483
56. Gürses I, Özeren M, Serin M, Yücel N, Erkal H. Histopathological evaluation of melatonin as a protective agent in heart injury induced by radiation in a rat model. Pathol Res Pract (2014) 210(12):863-71. doi:10.1016/j.prp.2014.08.006
57. Hoving S, Seemann I, Visser NL, te Poele JA, Stewart FA. Thalidomide is not able to inhibit radiation-induced heart disease. Int J Radiat Biol (2013) 89(9):685-91. doi:10.3109/09553002.2013.788797
58. Fajardo LF. RAdiation-induced coronary artery disease. Chest (1977) 71(5):563-4. doi:10.1378/chest.71.5.563