Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Detection of Myocardial Metabolic Abnormalities by 18F-FDG PET/CT and Corresponding Pathological Changes in Beagles with Local Heart Irradiation

  • Yan, Rui (Nursing College of Shanxi Medical University) ;
  • Song, Jianbo (Department of Nuclear Medicine, First Hospital of Shanxi Medical University) ;
  • Wu, Zhifang (Department of Nuclear Medicine, First Hospital of Shanxi Medical University) ;
  • Guo, Min (Department of Cardiology, First Hospital of Shanxi Medical University) ;
  • Liu, Jianzhong (Department of Nuclear Medicine, First Hospital of Shanxi Medical University) ;
  • Li, Jianguo (Department of Radiological and Environmental Medicine, China Institute for Radiation Protection) ;
  • Hao, Xinzhong (Department of Nuclear Medicine, First Hospital of Shanxi Medical University) ;
  • Li, Sijin (Department of Nuclear Medicine, First Hospital of Shanxi Medical University)
  • Received : 2014.10.14
  • Accepted : 2015.04.24
  • Published : 2015.08.01
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Abstract

Objective: To determine the efficacy of 18F-fluorodeoxyglucose positron emission tomography/computed tomography (18F-FDG PET/CT) in the detection of radiation-induced myocardial damage in beagles by comparing two pre-scan preparation protocols as well as to determine the correlation between abnormal myocardial FDG uptake and pathological findings. Materials and Methods: The anterior myocardium of 12 beagles received radiotherapy locally with a single X-ray dose of 20 Gy. 18F-FDG cardiac PET/CT was performed at baseline and 3 months after radiation. Twelve beagles underwent two protocols before PET/CT: 12 hours of fasting (12H-F), 12H-F followed by a high-fat diet (F-HFD). Regions of interest were drawn on the irradiation and the non-irradiation fields to obtain their maximal standardized uptake values (SUVmax). Then the ratio of the SUV of the irradiation to the non-irradiation fields (INR) was computed. Histopathological changes were identified by light and electron microscopy. Results: Using the 12H-F protocol, the average INRs were $1.18{\pm}0.10$ and $1.41{\pm}0.18$ before and after irradiation, respectively (p = 0.021). Using the F-HFD protocol, the average INRs were $0.99{\pm}0.15$ and $2.54{\pm}0.43$, respectively (p < 0.001). High FDG uptake in irradiation field was detected in 33.3% (4/12) of 12H-F protocol and 83.3% (10/12) of F-HFD protocol in visual analysis, respectively (p = 0.031). The pathology of the irradiated myocardium showed obvious perivascular fibrosis and changes in mitochondrial vacuoles. Conclusion: High FDG uptake in an irradiated field may be related with radiation-induced myocardial damage resulting from microvascular damage and mitochondrial injury. An F-HFD preparation protocol used before obtaining PET/CT can improve the sensitivity of the detection of cardiotoxicity associated with radiotherapy.

Keywords

References

  1. Favourable and unfavourable effects on long-term survival of radiotherapy for early breast cancer: an overview of the randomised trials. Early Breast Cancer Trialists' Collaborative Group. Lancet 2000;355:1757-1770 https://doi.org/10.1016/S0140-6736(00)02263-7
  2. Aleman BM, van den Belt-Dusebout AW, De Bruin ML, van't Veer MB, Baaijens MH, de Boer JP, et al. Late cardiotoxicity after treatment for Hodgkin lymphoma. Blood 2007;109:1878-1886 https://doi.org/10.1182/blood-2006-07-034405
  3. Lally BE, Detterbeck FC, Geiger AM, Thomas CR Jr, Machtay M, Miller AA, et al. The risk of death from heart disease in patients with nonsmall cell lung cancer who receive postoperative radiotherapy: analysis of the Surveillance, Epidemiology, and End Results database. Cancer 2007;110:911-917 https://doi.org/10.1002/cncr.22845
  4. Hardy D, Liu CC, Cormier JN, Xia R, Du XL. Cardiac toxicity in association with chemotherapy and radiation therapy in a large cohort of older patients with non-small-cell lung cancer. Ann Oncol 2010;21:1825-1833 https://doi.org/10.1093/annonc/mdq042
  5. Mukherjee S, Aston D, Minett M, Brewster AE, Crosby TD. The significance of cardiac doses received during chemoradiation of oesophageal and gastro-oesophageal junctional cancers. Clin Oncol (R Coll Radiol) 2003;15:115-120 https://doi.org/10.1053/clon.2003.0218
  6. Early Breast Cancer Trialists' Collaborative Group (EBCTCG), Darby S, McGale P, Correa C, Taylor C, Arriagada R, et al. Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: meta-analysis of individual patient data for 10,801 women in 17 randomised trials. Lancet 2011;378:1707-1716 https://doi.org/10.1016/S0140-6736(11)61629-2
  7. 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;366:2087-2106 https://doi.org/10.1016/S0140-6736(05)67887-7
  8. Townsend DW, Carney JP, Yap JT, Hall NC. PET/CT today and tomorrow. J Nucl Med 2004;45 Suppl 1:4S-14S
  9. Jingu K, Kaneta T, Nemoto K, Ichinose A, Oikawa M, Takai Y, et al. The utility of 18F-fluorodeoxyglucose positron emission tomography for early diagnosis of radiation-induced myocardial damage. Int J Radiat Oncol Biol Phys 2006;66:845-851 https://doi.org/10.1016/j.ijrobp.2006.06.007
  10. Zophel K, Holzel C, Dawel M, Holscher T, Evers C, Kotzerke J. PET/CT demonstrates increased myocardial FDG uptake following irradiation therapy. Eur J Nucl Med Mol Imaging 2007;34:1322-1323 https://doi.org/10.1007/s00259-007-0469-3
  11. Unal K, Unlu M, Akdemir O, Akmansu M. 18F-FDG PET/CT findings of radiotherapy-related myocardial changes in patients with thoracic malignancies. Nucl Med Commun 2013;34:855-859
  12. Inglese E, Leva L, Matheoud R, Sacchetti G, Secco C, Gandolfo P, et al. Spatial and temporal heterogeneity of regional myocardial uptake in patients without heart disease under fasting conditions on repeated whole-body 18F-FDG PET/CT. J Nucl Med 2007;48:1662-1669 https://doi.org/10.2967/jnumed.107.041574
  13. Fragasso G, Lucignani G, Fazio F. Nonuniformity in myocardial accumulation of fluorine-18-fluorodeoxyglucose in normal fasted humans. J Nucl Med 1991;32:1832-1833
  14. Williams G, Kolodny GM. Suppression of myocardial 18F-FDG uptake by preparing patients with a high-fat, low-carbohydrate diet. AJR Am J Roentgenol 2008;190:W151-W156 https://doi.org/10.2214/AJR.07.2409
  15. Fukuchi K, Ohta H, Matsumura K, Ishida Y. Benign variations and incidental abnormalities of myocardial FDG uptake in the fasting state as encountered during routine oncology positron emission tomography studies. Br J Radiol 2007;80:3-11 https://doi.org/10.1259/bjr/92105597
  16. Kobayashi Y, Kumita S, Fukushima Y, Ishihara K, Suda M, Sakurai M. Significant suppression of myocardial (18)F-fluorodeoxyglucose uptake using 24-h carbohydrate restriction and a low-carbohydrate, high-fat diet. J Cardiol 2013;62:314-319 https://doi.org/10.1016/j.jjcc.2013.05.004
  17. Harisankar CN, Mittal BR, Agrawal KL, Abrar ML, Bhattacharya A. Utility of high fat and low carbohydrate diet in suppressing myocardial FDG uptake. J Nucl Cardiol 2011;18:926-936 https://doi.org/10.1007/s12350-011-9422-8
  18. Frayn KN. The glucose-fatty acid cycle: a physiological perspective. Biochem Soc Trans 2003;31(Pt 6):1115-1119 https://doi.org/10.1042/bst0311115
  19. Kaneta T, Hakamatsuka T, Takanami K, Yamada T, Takase K, Sato A, et al. Evaluation of the relationship between physiological FDG uptake in the heart and age, blood glucose level, fasting period, and hospitalization. Ann Nucl Med 2006;20:203-208 https://doi.org/10.1007/BF03027431
  20. de Groot M, Meeuwis AP, Kok PJ, Corstens FH, Oyen WJ. Influence of blood glucose level, age and fasting period on non-pathological FDG uptake in heart and gut. Eur J Nucl Med Mol Imaging 2005;32:98-101 https://doi.org/10.1007/s00259-004-1670-2
  21. Krueger EA, Schipper MJ, Koelling T, Marsh RB, Butler JB, Pierce LJ. Cardiac chamber and coronary artery doses associated with postmastectomy radiotherapy techniques to the chest wall and regional nodes. Int J Radiat Oncol Biol Phys 2004;60:1195-1203 https://doi.org/10.1016/j.ijrobp.2004.04.026
  22. Schultz-Hector S, Trott KR. Radiation-induced cardiovascular diseases: is the epidemiologic evidence compatible with the radiobiologic data? Int J Radiat Oncol Biol Phys 2007;67:10-18 https://doi.org/10.1016/j.ijrobp.2006.08.071
  23. Lauk S, Kiszel Z, Buschmann J, Trott KR. Radiation-induced heart disease in rats. Int J Radiat Oncol Biol Phys 1985;11:801-808 https://doi.org/10.1016/0360-3016(85)90314-1
  24. Boerma M, Hauer-Jensen M. Preclinical research into basic mechanisms of radiation-induced heart disease. Cardiol Res Pract 2010;2011. http://dx.doi.org/10.4061/2011/858262
  25. Yarnold J, Brotons MC. Pathogenetic mechanisms in radiation fibrosis. Radiother Oncol 2010;97:149-161 https://doi.org/10.1016/j.radonc.2010.09.002
  26. Umezawa R, Takase K, Jingu K, Takanami K, Ota H, Kaneta T, et al. Evaluation of radiation-induced myocardial damage using iodine-123 ${\beta}$-methyl-iodophenyl pentadecanoic acid scintigraphy. J Radiat Res 2013;54:880-889 https://doi.org/10.1093/jrr/rrt011
  27. Schultz-Hector S, Kallfass E, Sund M. [Radiation sequelae in the large arteries. A review of clinical and experimental data]. Strahlenther Onkol 1995;171:427-436
  28. Lauk S, Trott KR. Endothelial cell proliferation in the rat heart following local heart irradiation. Int J Radiat Biol 1990;57:1017-1030 https://doi.org/10.1080/09553009014551131
  29. Schultz-Hector S. Experimental studies on the pathogenesis of damage in the heart. Recent Results Cancer Res 1993;130:145-156 https://doi.org/10.1007/978-3-642-84892-6_13
  30. Vos J, Aarnoudse MW, Dijk F, Lamberts HB. On the cellular origin and development of atheromatous plaques. A light and electron microscopic study of combined X-ray and hypercholesterolemia-induced atheromatosis in the carotid artery of the rabbit. Virchows Arch B Cell Pathol Incl Mol Pathol 1983;43:1-16 https://doi.org/10.1007/BF02932938
  31. Shankar SM, Marina N, Hudson MM, Hodgson DC, Adams MJ, Landier W, et al. Monitoring for cardiovascular disease in survivors of childhood cancer: report from the Cardiovascular Disease Task Force of the Children's Oncology Group. Pediatrics 2008;121:e387-e396 https://doi.org/10.1542/peds.2007-0575
  32. Fajardo LF, Stewart JR. Experimental radiation-induced heart disease. I. Light microscopic studies. Am J Pathol 1970;59:299-316
  33. Barjaktarovic Z, Schmaltz D, Shyla A, Azimzadeh O, Schulz S, Haagen J, et al. Radiation-induced signaling results in mitochondrial impairment in mouse heart at 4 weeks after exposure to X-rays. PLoS One 2011;6:e27811 https://doi.org/10.1371/journal.pone.0027811
  34. Dogan I, Sezen O, Sonmez B, Zengin AY, Yenilmez E, Yulug E, et al. Myocardial perfusion alterations observed months after radiotherapy are related to the cellular damage. Nuklearmedizin 2010;49:209-215 https://doi.org/10.3413/nukmed-0315-10-05
  35. Bateman TM. Advantages and disadvantages of PET and SPECT in a busy clinical practice. J Nucl Cardiol 2012;19 Suppl 1:S3-S11 https://doi.org/10.1007/s12350-011-9490-9

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