DOI QR코드

DOI QR Code

Radiation induced secondary malignancies: a review article

  • Received : 2018.06.17
  • Accepted : 2018.06.27
  • Published : 2018.06.30

Abstract

Radiation-induced second malignancies (RISM) is one of the important late side effects of radiation therapy and has an impact on optimal treatment decision-making. Many factors contribute to the development of RISM such as age at radiation, dose and volume of irradiated area, type of irradiated organ and tissue, radiation technique and individual and family history of cancer. Exact mechanism of RISM is unknown. But nowadays, it is a growing concern in oncology because of the increased number of cancer survivors and efforts are being made to prevent or decrease the incidence of RISM. The primary search for articles was carried via Google Scholar and PubMed with keywords included 'radiation induced malignancies, second malignancies, and chemotherapy induced malignancies'. Additional papers were found through references from relevant articles. In this review article, we have discussed about the pathogenesis, factors contributing to RISM, screening and prevention strategies of RISM.

Keywords

References

  1. Morton LM, Onel K, Curtis RE, Hungate EA, Armstrong GT. The rising incidence of second cancers: patterns of occurrence and identification of risk factors for children and adults. Am Soc Clin Oncol Educ Book 2014:e57-67.
  2. Armstrong GT, Liu Q, Yasui Y, et al. Late mortality among 5-year survivors of childhood cancer: a summary from the Childhood Cancer Survivor Study. J Clin Oncol 2009;27:2328-38. https://doi.org/10.1200/JCO.2008.21.1425
  3. Mertens AC, Liu Q, Neglia JP, 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. https://doi.org/10.1093/jnci/djn310
  4. Kaufman EL, Jacobson JS, Hershman DL, Desai M, Neugut AI. Effect of breast cancer radiotherapy and cigarette smoking on risk of second primary lung cancer. J Clin Oncol 2008;26:392-8. https://doi.org/10.1200/JCO.2007.13.3033
  5. Prochazka M, Hall P, Gagliardi G, et al. Ionizing radiation and tobacco use increases the risk of a subsequent lung carcinoma in women with breast cancer: case-only design. J Clin Oncol 2005;23:7467-74. https://doi.org/10.1200/JCO.2005.01.7335
  6. Travis LB, Gospodarowicz M, Curtis RE, et al. Lung cancer following chemotherapy and radiotherapy for Hodgkin's disease. J Natl Cancer Inst 2002;94:182-92. https://doi.org/10.1093/jnci/94.3.182
  7. Cooke R, Jones ME, Cunningham D, et al. Breast cancer risk following Hodgkin lymphoma radiotherapy in relation to menstrual and reproductive factors. Br J Cancer 2013;108:2399-406. https://doi.org/10.1038/bjc.2013.219
  8. De Bruin ML, Sparidans J, van't Veer MB, et al. Breast cancer risk in female survivors of Hodgkin's lymphoma: lower risk after smaller radiation volumes. J Clin Oncol 2009;27:4239-46. https://doi.org/10.1200/JCO.2008.19.9174
  9. Varszegi D, Duga B, Melegh BI, et al. Hodgkin disease therapy induced second malignancy susceptibility 6q21 functional variants in roma and hungarian population samples. Pathol Oncol Res 2014;20:529-33. https://doi.org/10.1007/s12253-013-9724-z
  10. Knight JA, Skol AD, Shinde A, et al. Genome-wide association study to identify novel loci associated with therapy-related myeloid leukemia susceptibility. Blood 2009;113:5575-82.
  11. Mullenders L, Atkinson M, Paretzke H, Sabatier L, Bouffler S. Assessing cancer risks of low-dose radiation. Nat Rev Cancer 2009;9:596-604. https://doi.org/10.1038/nrc2677
  12. Taylor AM, Byrd PJ. Molecular pathology of ataxia telangiectasia. J Clin Pathol 2005;58:1009-15. https://doi.org/10.1136/jcp.2005.026062
  13. Preston DL, Ron E, Tokuoka S, et al. Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat Res 2007;168:1-64. https://doi.org/10.1667/RR0763.1
  14. Berrington de Gonzalez A, Gilbert E, Curtis R, et al. Second solid cancers after radiation therapy: a systematic review of the epidemiologic studies of the radiation dose-response relationship. Int J Radiat Oncol Biol Phys 2013;86:224-33. https://doi.org/10.1016/j.ijrobp.2012.09.001
  15. Hodgson DC, Gilbert ES, Dores GM, et al. Long-term solid cancer risk among 5-year survivors of Hodgkin's lymphoma. J Clin Oncol 2007;25:1489-97. https://doi.org/10.1200/JCO.2006.09.0936
  16. Travis LB, Fossa SD, Schonfeld SJ, et al. Second cancers among 40,576 testicular cancer patients: focus on long-term survivors. J Natl Cancer Inst 2005;97:1354-65. https://doi.org/10.1093/jnci/dji278
  17. Vardiman JW. The World Health Organization (WHO) classification of tumors of the hematopoietic and lymphoid tissues: an overview with emphasis on the myeloid neoplasms. Chem Biol Interact 2010;184:16-20. https://doi.org/10.1016/j.cbi.2009.10.009
  18. Kayser S, Dohner K, Krauter J, et al. The impact of therapyrelated acute myeloid leukemia (AML) on outcome in 2853 adult patients with newly diagnosed AML. Blood 2011;117:2137-45. https://doi.org/10.1182/blood-2010-08-301713
  19. Swerdlow AJ, Higgins CD, Smith P, et al. Second cancer risk after chemotherapy for Hodgkin's lymphoma: a collaborative British cohort study. J Clin Oncol 2011;29:4096-104. https://doi.org/10.1200/JCO.2011.34.8268
  20. Mackey JR, Martin M, Pienkowski T, et al. Adjuvant docetaxel, doxorubicin, and cyclophosphamide in node-positive breast cancer: 10-year follow-up of the phase 3 randomised BCIRG 001 trial. Lancet Oncol 2013;14:72-80. https://doi.org/10.1016/S1470-2045(12)70525-9
  21. Palumbo A, Bringhen S, Kumar SK, et al. Second primary malignancies with lenalidomide therapy for newly diagnosed myeloma: a meta-analysis of individual patient data. Lancet Oncol 2014;15:333-42. https://doi.org/10.1016/S1470-2045(13)70609-0
  22. Zhao J, Xu Z, Liu D, Lu Q. Rituximab and new regimens for indolent lymphoma: a brief update from 2012 ASCO Annual Meeting. Cancer Cell Int 2012;12:38. https://doi.org/10.1186/1475-2867-12-38
  23. Early Breast Cancer Trialists' Collaborative Group (EBCTCG), Davies C, Godwin J, et al. Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet 2011;378:771-84. https://doi.org/10.1016/S0140-6736(11)60993-8
  24. Hall EJ. Intensity-modulated radiation therapy, protons, and the risk of second cancers. Int J Radiat Oncol Biol Phys 2006;65:1-7. https://doi.org/10.1016/j.ijrobp.2006.01.027
  25. 1990 Recommendations of the International Commission on Radiological Protection. Ann ICRP 1991;21:1-201. https://doi.org/10.1016/0146-6453(91)90009-6
  26. Friedman DL, Whitton J, Leisenring W, et al. Subsequent neoplasms in 5-year survivors of childhood cancer: the Childhood Cancer Survivor Study. J Natl Cancer Inst 2010;102:1083-95. https://doi.org/10.1093/jnci/djq238
  27. Armstrong GT, Sklar CA, Hudson MM, Robison LL. Long-term health status among survivors of childhood cancer: does sex matter? J Clin Oncol 2007;25:4477-89. https://doi.org/10.1200/JCO.2007.11.2003
  28. Meadows AT, Friedman DL, Neglia JP, et al. Second neoplasms in survivors of childhood cancer: findings from the Childhood Cancer Survivor Study cohort. J Clin Oncol 2009;27:2356-62. https://doi.org/10.1200/JCO.2008.21.1920
  29. Bhatia S, Sklar C. Second cancers in survivors of childhood cancer. Nat Rev Cancer 2002;2:124-32. https://doi.org/10.1038/nrc722
  30. Krueger SA, Joiner MC, Weinfeld M, Piasentin E, Marples B. Role of apoptosis in low-dose hyper-radiosensitivity. Radiat Res 2007;167:260-7. https://doi.org/10.1667/RR0776.1
  31. Harrison RM, Wilkinson M, Rawlings DJ, Moore M. Doses to critical organs following radiotherapy and concomitant imaging of the larynx and breast. Br J Radiol 2007;80:989-95. https://doi.org/10.1259/bjr/32814323
  32. Newhauser WD, Durante M. Assessing the risk of second malignancies after modern radiotherapy. Nat Rev Cancer 2011;11:438-48. https://doi.org/10.1038/nrc3069
  33. Chung CS, Yock TI, Nelson K, Xu Y, Keating NL, Tarbell NJ. Incidence of second malignancies among patients treated with proton versus photon radiation. Int J Radiat Oncol Biol Phys 2013;87:46-52. https://doi.org/10.1016/j.ijrobp.2013.04.030
  34. Yock TI, Yeap BY, Ebb DH, et al. Long-term toxic effects of proton radiotherapy for paediatric medulloblastoma: a phase 2 single-arm study. Lancet Oncol 2016;17:287-98. https://doi.org/10.1016/S1470-2045(15)00167-9
  35. Eaton BR, Esiashvili N, Kim S, et al. Clinical outcomes among children with standard-risk medulloblastoma treated with proton and photon radiation therapy: a comparison of disease control and overall survival. Int J Radiat Oncol Biol Phys 2016;94:133-8. https://doi.org/10.1016/j.ijrobp.2015.09.014
  36. Sethi RV, Shih HA, Yeap BY, et al. Second nonocular tumors among survivors of retinoblastoma treated with contemporary photon and proton radiotherapy. Cancer 2014;120:126-33. https://doi.org/10.1002/cncr.28387
  37. Tubiana M. Can we reduce the incidence of second primary malignancies occurring after radiotherapy? A critical review. Radiother Oncol 2009;91:4-15. https://doi.org/10.1016/j.radonc.2008.12.016
  38. Grantzau T, Mellemkjær L, Overgaard J. Second primary cancers after adjuvant radiotherapy in early breast cancer patients: a national population based study under the Danish Breast Cancer Cooperative Group (DBCG). Radiother Oncol 2013;106:42-9. https://doi.org/10.1016/j.radonc.2013.01.002
  39. Berrington de Gonzalez A, Curtis RE, Gilbert E, et al. Second solid cancers after radiotherapy for breast cancer in SEER cancer registries. Br J Cancer 2010;102:220-6. https://doi.org/10.1038/sj.bjc.6605435
  40. Grantzau T, Overgaard J. Risk of second non-breast cancer after radiotherapy for breast cancer: a systematic review and meta-analysis of 762,468 patients. Radiother Oncol 2015;114:56-65.
  41. Hamilton SN, Tyldesley S, Li D, Olson R, McBride M. Second malignancies after adjuvant radiation therapy for early stage breast cancer: is there increased risk with addition of regional radiation to local radiation? Int J Radiat Oncol Biol Phys 2015;91:977-85. https://doi.org/10.1016/j.ijrobp.2014.12.051
  42. Brenner DJ, Curtis RE, Hall EJ, Ron E. Second malignancies in prostate carcinoma patients after radiotherapy compared with surgery. Cancer 2000;88:398-406. https://doi.org/10.1002/(SICI)1097-0142(20000115)88:2<398::AID-CNCR22>3.0.CO;2-V
  43. Berrington de Gonzalez A, Wong J, Kleinerman R, Kim C, Morton L, Bekelman JE. Risk of second cancers according to radiation therapy technique and modality in prostate cancer survivors. Int J Radiat Oncol Biol Phys 2015;91:295-302.
  44. Chaturvedi AK, Engels EA, Gilbert ES, et al. Second cancers among 104,760 survivors of cervical cancer: evaluation of long-term risk. J Natl Cancer Inst 2007;99:1634-43. https://doi.org/10.1093/jnci/djm201
  45. Creutzberg CL, Nout RA, Lybeert ML, et al. Fifteen-year radiotherapy outcomes of the randomized PORTEC-1 trial for endometrial carcinoma. Int J Radiat Oncol Biol Phys 2011;81:e631-8. https://doi.org/10.1016/j.ijrobp.2011.04.013
  46. O'Brien MM, Donaldson SS, Balise RR, Whittemore AS, Link MP. Second malignant neoplasms in survivors of pediatric Hodgkin's lymphoma treated with low-dose radiation and chemotherapy. J Clin Oncol 2010;28:1232-9. https://doi.org/10.1200/JCO.2009.24.8062
  47. Tward JD, Wendland MM, Shrieve DC, Szabo A, Gaffney DK. The risk of secondary malignancies over 30 years after the treatment of non-Hodgkin lymphoma. Cancer 2006;107:108-15. https://doi.org/10.1002/cncr.21971
  48. Foss Abrahamsen A, Andersen A, Nome O, et al. Long-term risk of second malignancy after treatment of Hodgkin's disease: the influence of treatment, age and follow-up time. Ann Oncol 2002;13:1786-91. https://doi.org/10.1093/annonc/mdf289
  49. Reulen RC, Frobisher C, Winter DL, et al. Long-term risks of subsequent primary neoplasms among survivors of childhood cancer. JAMA 2011;305:2311-9. https://doi.org/10.1001/jama.2011.747
  50. Henderson TO, Oeffinger KC, Whitton J, et al. Secondary gastrointestinal cancer in childhood cancer survivors: a cohort study. Ann Intern Med 2012;156:757-66, W-260. https://doi.org/10.7326/0003-4819-156-11-201206050-00002
  51. Walter AW, Hancock ML, Pui CH, et al. Secondary brain tumors in children treated for acute lymphoblastic leukemia at St Jude Children's Research Hospital. J Clin Oncol 1998;16:3761-7. https://doi.org/10.1200/JCO.1998.16.12.3761
  52. Ralleigh G, Given-Wilson R. Breast cancer risk and possible screening strategies for young women following supradiaphragmatic irradiation for Hodgkin's disease. Clin Radiol 2004;59:647-50. https://doi.org/10.1016/j.crad.2004.04.003
  53. Mulder RL, Kremer LC, Hudson MM, et al. Recommendations for breast cancer surveillance for female survivors of childhood, adolescent, and young adult cancer given chest radiation: a report from the International Late Effects of Childhood Cancer Guideline Harmonization Group. Lancet Oncol 2013;14:e621-9. https://doi.org/10.1016/S1470-2045(13)70303-6
  54. Howell SJ, Searle C, Goode V, et al. The UK national breast cancer screening programme for survivors of Hodgkin lymphoma detects breast cancer at an early stage. Br J Cancer 2009;101:582-8. https://doi.org/10.1038/sj.bjc.6605215
  55. Page V, Gardner A, Karzmark CJ. Physical and dosimetric aspects of the radiotherapy of malignant lymphomas. I. The mantle technique. Radiology 1970;96:609-18. https://doi.org/10.1148/96.3.609
  56. Engert A, Plutschow A, Eich HT, et al. Reduced treatment intensity in patients with early-stage Hodgkin's lymphoma. N Engl J Med 2010;363:640-52. https://doi.org/10.1056/NEJMoa1000067
  57. Girinsky T, van der Maazen R, Specht L, et al. Involved-node radiotherapy (INRT) in patients with early Hodgkin lymphoma: concepts and guidelines. Radiother Oncol 2006;79:270-7. https://doi.org/10.1016/j.radonc.2006.05.015
  58. Hoskin PJ, Diez P, Williams M, Lucraft H, Bayne M; Participants of the Lymphoma Radiotherapy Group. Recommendations for the use of radiotherapy in nodal lymphoma. Clin Oncol (R Coll Radiol) 2013;25:49-58. https://doi.org/10.1016/j.clon.2012.07.011
  59. Swerdlow AJ, Cooke R, Bates A, et al. Breast cancer risk after supradiaphragmatic radiotherapy for Hodgkin's lymphoma in England and Wales: a National Cohort Study. J Clin Oncol 2012;30:2745-52. https://doi.org/10.1200/JCO.2011.38.8835
  60. Hartmann LC, Schaid DJ, Woods JE, et al. Efficacy of bilateral prophylactic mastectomy in women with a family history of breast cancer. N Engl J Med 1999;340:77-84. https://doi.org/10.1056/NEJM199901143400201
  61. Travis LB, Demark Wahnefried W, Allan JM, Wood ME, Ng AK. Aetiology, genetics and prevention of secondary neoplasms in adult cancer survivors. Nat Rev Clin Oncol 2013;10:289-301. https://doi.org/10.1038/nrclinonc.2013.41
  62. Inskip PD, Robison LL, Stovall M, et al. Radiation dose and breast cancer risk in the childhood cancer survivor study. J Clin Oncol 2009;27:3901-7. https://doi.org/10.1200/JCO.2008.20.7738
  63. Bhatti P, Veiga LH, Ronckers CM, et al. Risk of second primary thyroid cancer after radiotherapy for a childhood cancer in a large cohort study: an update from the childhood cancer survivor study. Radiat Res 2010;174:741-52. https://doi.org/10.1667/RR2240.1
  64. Travis LB, Hill DA, Dores GM, et al. Breast cancer following radiotherapy and chemotherapy among young women with Hodgkin disease. JAMA 2003;290:465-75. https://doi.org/10.1001/jama.290.4.465
  65. Rubino C, Shamsaldin A, Le MG, et al. Radiation dose and risk of soft tissue and bone sarcoma after breast cancer treatment. Breast Cancer Res Treat 2005;89:277-88. https://doi.org/10.1007/s10549-004-2472-8
  66. Boice JD Jr, Engholm G, Kleinerman RA, et al. Radiation dose and second cancer risk in patients treated for cancer of the cervix. Radiat Res 1988;116:3-55. https://doi.org/10.2307/3577477
  67. Gilbert ES, Stovall M, Gospodarowicz M, et al. Lung cancer after treatment for Hodgkin's disease: focus on radiation effects. Radiat Res 2003;159:161-73. https://doi.org/10.1667/0033-7587(2003)159[0161:LCATFH]2.0.CO;2
  68. Taylor AJ, Little MP, Winter DL, et al. Population-based risks of CNS tumors in survivors of childhood cancer: the British Childhood Cancer Survivor Study. J Clin Oncol 2010;28:5287-93. https://doi.org/10.1200/JCO.2009.27.0090
  69. Morton LM, Gilbert ES, Hall P, et al. Risk of treatment-related esophageal cancer among breast cancer survivors. Ann Oncol 2012;23:3081-91. https://doi.org/10.1093/annonc/mds144

Cited by

  1. Reduction of Delayed Homologous Recombination by Induction of Radioadaptive Response in RaDR-GFP Mice (Yonezawa Effect): An Old Player With a New Role vol.17, pp.1, 2019, https://doi.org/10.1177/1559325819833840
  2. A Case of Histiocytic Sarcoma Arising from Mycosis Fungoides vol.2019, pp.None, 2018, https://doi.org/10.1155/2019/7834728
  3. Effect of dose constraint on the thyroid gland during locoregional intensity‐modulated radiotherapy in breast cancer patients vol.20, pp.7, 2019, https://doi.org/10.1002/acm2.12668
  4. Heart‐sparing radiotherapy with three‐dimensional printing technology after mastectomy for patients with left breast cancer vol.25, pp.4, 2018, https://doi.org/10.1111/tbj.13304
  5. Mutational landscape in genetically engineered, carcinogen-induced, and radiation-induced mouse sarcoma vol.4, pp.13, 2019, https://doi.org/10.1172/jci.insight.128698
  6. Zweitmalignomrisiko nach Behandlung von lokal begrenzten Prostatakarzinomen mit Kohlenstoffionen möglicherweise niedriger als nach Photonenbestrahlung vol.195, pp.11, 2018, https://doi.org/10.1007/s00066-019-01510-0
  7. The mutational footprints of cancer therapies vol.51, pp.12, 2018, https://doi.org/10.1038/s41588-019-0525-5
  8. Angiosarcomaafteradjuvantradiotherapy in high-risksquamouscell carcinoma of the vulva: a case report vol.18, pp.4, 2019, https://doi.org/10.5114/pm.2019.93114
  9. Graphene Quantum Dot-Based Electrochemical Immunosensors for Biomedical Applications vol.13, pp.1, 2018, https://doi.org/10.3390/ma13010096
  10. Peptide-Drug Conjugates and Their Targets in Advanced Cancer Therapies vol.8, pp.None, 2018, https://doi.org/10.3389/fchem.2020.00571
  11. Cancer Risk of Low Dose Ionizing Radiation vol.8, pp.None, 2018, https://doi.org/10.3389/fphy.2020.00234
  12. Clinical and epidemiological observations on individual radiation sensitivity and susceptibility vol.96, pp.3, 2020, https://doi.org/10.1080/09553002.2019.1665209
  13. Nanoparticles as Tools to Target Redox Homeostasis in Cancer Cells vol.9, pp.3, 2018, https://doi.org/10.3390/antiox9030211
  14. Modern radiotherapy for pediatric rhabdomyosarcoma vol.71, pp.1, 2018, https://doi.org/10.5937/mp71-24163
  15. Role of Rad51 and DNA repair in cancer: A molecular perspective vol.208, pp.None, 2020, https://doi.org/10.1016/j.pharmthera.2020.107492
  16. Combining Angiogenesis Inhibitors with Radiation: Advances and Challenges in Cancer Treatment vol.26, pp.None, 2018, https://doi.org/10.2174/1381612826666201002145454
  17. Radiation-Induced Brachial Plexopathy in Breast Cancer and the Role of Surgical Treatment vol.9, pp.2, 2018, https://doi.org/10.1055/s-0040-1712272
  18. Examination of a dose evaluation method for floor-mounted kV X-ray image-guided radiation therapy systems vol.13, pp.3, 2020, https://doi.org/10.1007/s12194-020-00570-7
  19. Updated Understanding of Cancer as a Metabolic and Telomere-Driven Disease, and Proposal for Complex Personalized Treatment, a Hypothesis vol.21, pp.18, 2020, https://doi.org/10.3390/ijms21186521
  20. Current trends in the management of subependymal giant cell astrocytomas in tuberous sclerosis vol.36, pp.10, 2020, https://doi.org/10.1007/s00381-020-04889-9
  21. The diagnosis and management of primary and iatrogenic soft tissue sarcomas of the sella vol.23, pp.5, 2018, https://doi.org/10.1007/s11102-020-01062-y
  22. Radiation therapy and secondary malignancy in Li‐Fraumeni syndrome: A hereditary cancer registry study vol.9, pp.21, 2020, https://doi.org/10.1002/cam4.3427
  23. BCL‐XL exerts a protective role against anemia caused by radiation‐induced kidney damage vol.39, pp.24, 2018, https://doi.org/10.15252/embj.2020105561
  24. Rare presentation of radiation-induced sarcoma detected on F-18 FDG positron emission tomography/computed tomography in a treated case of giant cell tumor vol.36, pp.4, 2018, https://doi.org/10.4103/ijnm.ijnm_61_21
  25. Impact of Advanced Radiotherapy on Second Primary Cancer Risk in Prostate Cancer Survivors: A Nationwide Cohort Study vol.11, pp.None, 2021, https://doi.org/10.3389/fonc.2021.771956
  26. Telomere Length Dynamics and Chromosomal Instability for Predicting Individual Radiosensitivity and Risk via Machine Learning vol.11, pp.3, 2021, https://doi.org/10.3390/jpm11030188
  27. Laryngeal Langerhans Cell Histiocytosis: A Case Report and Literature Review vol.130, pp.4, 2018, https://doi.org/10.1177/0003489420954883
  28. Management of tenosynovial giant cell tumour of the foot and ankle vol.b103, pp.4, 2021, https://doi.org/10.1302/0301-620x.103b4.bjj-2020-1582.r1
  29. Second Malignancies after Radiation Therapy: Update on Pathogenesis and Cross-sectional Imaging Findings vol.41, pp.3, 2021, https://doi.org/10.1148/rg.2021200171
  30. Risk of second cancer among young prostate cancer survivors vol.39, pp.2, 2018, https://doi.org/10.3857/roj.2020.00857
  31. Radioactive Iodine Treatment for Children and Young Adults with Thyroid Cancer in South Korea: A Population-based Study vol.106, pp.7, 2018, https://doi.org/10.1210/clinem/dgab192
  32. CANCER-INDUCED DIAGNOSTIC AND THERAPEUTIC INTERVENTIONS vol.20, pp.4, 2018, https://doi.org/10.21294/1814-4861-2021-20-4-146-151
  33. Radiation and Androgen Deprivation Therapy With or Without Docetaxel in the Management of Nonmetastatic Unfavorable-Risk Prostate Cancer: A Prospective Randomized Trial vol.39, pp.26, 2018, https://doi.org/10.1200/jco.21.00596
  34. Spleen angiosarcoma: a world review vol.15, pp.10, 2021, https://doi.org/10.1080/17474124.2021.1945920
  35. Unintended dose to the lower axilla in adjuvant radiotherapy for breast cancer: Differences between tangential beam and VMAT vol.164, pp.None, 2021, https://doi.org/10.1016/j.radonc.2021.10.005
  36. 3D Breast Tumor Models for Radiobiology Applications vol.13, pp.22, 2018, https://doi.org/10.3390/cancers13225714
  37. Cardiovascular mortality among cancer survivors who developed breast cancer as a second primary malignancy vol.125, pp.10, 2018, https://doi.org/10.1038/s41416-021-01549-w
  38. May Different Treatment Volumes and Technical Approaches Have an Impact on Second Malignancies Risk? vol.39, pp.33, 2021, https://doi.org/10.1200/jco.21.01790
  39. Dosimetry and outcomes in patients receiving radiotherapy for synchronous bilateral breast cancers vol.52, pp.4, 2018, https://doi.org/10.1016/j.jmir.2021.08.013
  40. Mathematical model for the thermal enhancement of radiation response: thermodynamic approach vol.11, pp.1, 2018, https://doi.org/10.1038/s41598-021-84620-z
  41. Analysis of lncRNA-miRNA-mRNA expression pattern in heart tissue after total body radiation in a mouse model vol.19, pp.1, 2018, https://doi.org/10.1186/s12967-021-02998-w
  42. Implications of targeted next-generation sequencing for bladder cancer: report of four cases vol.19, pp.1, 2018, https://doi.org/10.1186/s43141-021-00182-7
  43. Relapsed Medulloblastoma in Pre-Irradiated Patients: Current Practice for Diagnostics and Treatment vol.14, pp.1, 2018, https://doi.org/10.3390/cancers14010126