DOI QR코드

DOI QR Code

Appraisal of re-irradiation for the recurrent glioblastoma in the era of MGMT promotor methylation

  • Kim, Il Han (Department of Radiation Oncology, Seoul National University College of Medicine)
  • Received : 2019.03.19
  • Accepted : 2019.03.21
  • Published : 2019.03.31

Abstract

Despite recent innovation in treatment techniques and subsequently improved outcomes, the majority of glioblastoma (GBL) have relapses, especially in locoregional areas. Local re-irradiation (re-RT) has been established as a feasible option for recurrent GBL of all ages with safety, tolerability, and effectiveness both in survival and quality of life regardless of fractionation schedule. To keep adverse effects under acceptable range, cumulative dose limit in equivalent dose at 2 Gy fractions by the linear-quadratic model at α/β = 2 for normal brain tissue (EQD2) with narrow margin should be observed and single/hypofractionated re-RT should be undertaken very carefully to recurrent tumor with large volume or adjacent to the brainstem. Promising outcome of re-operation (re-Op) plus re-RT (re-Op/RT) need to be validated and result from re-RT with temozolomide/bevacizumab (TMZ/BV) or new strategy is expected. Development of new-concept prognostic scoring or risk group is required to select patients properly and make use of predictive biomarkers such as O(6)-methylguanine-DNA methyltransferase (MGMT) promotor methylation that influence outcomes of re-RT, re-Op/RT, or re-RT with TMZ/BV.

Keywords

References

  1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96. https://doi.org/10.1056/NEJMoa043330
  2. Gaspar LE, Fisher BJ, Macdonald DR, et al. Supratentorial malignant glioma: patterns of recurrence and implications for external beam local treatment. Int J Radiat Oncol Biol Phys 1992;24:55-7. https://doi.org/10.1016/0360-3016(92)91021-E
  3. Chan JL, Lee SW, Fraass BA, et al. Survival and failure patterns of high-grade gliomas after three-dimensional conformal radiotherapy. J Clin Oncol 2002;20:1635-42. https://doi.org/10.1200/JCO.20.6.1635
  4. Minniti G, Amelio D, Amichetti M, et al. Patterns of failure and comparison of different target volume delineations in patients with glioblastoma treated with conformal radiotherapy plus concomitant and adjuvant temozolomide. Radiother Oncol 2010;97:377-81. https://doi.org/10.1016/j.radonc.2010.08.020
  5. Brandes AA, Tosoni A, Franceschi E, et al. Recurrence pattern after temozolomide concomitant with and adjuvant to radiotherapy in newly diagnosed patients with glioblastoma: correlation With MGMT promoter methylation status. J Clin Oncol 2009;27:1275-9. https://doi.org/10.1200/JCO.2008.19.4969
  6. Shi W, Bryan MS, Gilbert MR, et al. Investigating the effect of reirradiation or systemic therapy in patients with glioblastoma after tumor progression: a secondary analysis of NRG Oncology/Radiation Therapy Oncology Group Trial 0525. Int J Radiat Oncol Biol Phys 2018;100:38-44. https://doi.org/10.1016/j.ijrobp.2017.08.038
  7. Kazmi F, Soon YY, Leong YH, et al. Re-irradiation for recurrent glioblastoma (GBM): a systematic review and meta-analysis. J Neurooncol 2019;142:79-90. https://doi.org/10.1007/s11060-018-03064-0
  8. Shrieve DC, Alexander E 3rd, Wen PY, et al. Comparison of stereotactic radiosurgery and brachytherapy in the treatment of recurrent glioblastoma multiforme. Neurosurgery 1995;36:275-84. https://doi.org/10.1227/00006123-199502000-00006
  9. Combs SE, Widmer V, Thilmann C, et al. Stereotactic radiosurgery (SRS): treatment option for recurrent glioblastoma multiforme (GBM). Cancer 2005;104:2168-73. https://doi.org/10.1002/cncr.21429
  10. Hsieh PC, Chandler JP, Bhangoo S, et al. Adjuvant gamma knife stereotactic radiosurgery at the time of tumor progression potentially improves survival for patients with glioblastoma multiforme. Neurosurgery 2005;57:684-92. https://doi.org/10.1227/01.NEU.0000175550.96901.A3
  11. Kong DS, Lee JI, Park K, et al. Efficacy of stereotactic radiosurgery as a salvage treatment for recurrent malignant gliomas. Cancer 2008;112:2046-51. https://doi.org/10.1002/cncr.23402
  12. Patel M, Siddiqui F, Jin JY, et al. Salvage reirradiation for recurrent glioblastoma with radiosurgery: radiographic response and improved survival. J Neurooncol 2009;92:185-91. https://doi.org/10.1007/s11060-008-9752-9
  13. Hudes RS, Corn BW, Werner-Wasik M, et al. A phase I dose escalation study of hypofractionated stereotactic radiotherapy as salvage therapy for persistent or recurrent malignant glioma. Int J Radiat Oncol Biol Phys 1999;43:293-8. https://doi.org/10.1016/S0360-3016(98)00416-7
  14. Vordermark D, Kolbl O, Ruprecht K, et al. Hypofractionated stereotactic re-irradiation: treatment option in recurrent malignant glioma. BMC Cancer 2005;5:55. https://doi.org/10.1186/1471-2407-5-55
  15. Combs SE, Gutwein S, Thilmann C, et al. Stereotactically guided fractionated re-irradiation in recurrent glioblastoma multiforme. J Neurooncol 2005;74:167-71. https://doi.org/10.1007/s11060-004-2463-y
  16. Kohshi K, Yamamoto H, Nakahara A, et al. Fractionated stereotactic radiotherapy using gamma unit after hyperbaric oxygenation on recurrent high-grade gliomas. J Neurooncol 2007;82:297-303. https://doi.org/10.1007/s11060-006-9283-1
  17. Fokas E, Wacker U, Gross MW, et al. Hypofractionated stereotactic reirradiation of recurrent glioblastomas : a beneficial treatment option after high-dose radiotherapy? Strahlenther Onkol 2009;185:235-40. https://doi.org/10.1007/s00066-009-1753-x
  18. Combs SE, Edler L, Rausch R, et al. Generation and validation of a prognostic score to predict outcome after re-irradiation of recurrent glioma. Acta Oncol 2013;52:147-52. https://doi.org/10.3109/0284186X.2012.692882
  19. Yazici G, Cengiz M, Ozyigit G, et al. Hypofractionated stereotactic reirradiation for recurrent glioblastoma. J Neurooncol 2014;120:117-23. https://doi.org/10.1007/s11060-014-1524-0
  20. Dincoglan F, Beyzadeoglu M, Sager O, et al. Management of patients with recurrent glioblastoma using hypofractionated stereotactic radiotherapy. Tumori 2015;101:179-84. https://doi.org/10.5301/tj.5000236
  21. Combs SE, Niyazi M, Adeberg S, et al. Re-irradiation of recurrent gliomas: pooled analysis and validation of an established prognostic score-report of the Radiation Oncology Group (ROG) of the German Cancer Consortium (DKTK). Cancer Med 2018;7:1742-9. https://doi.org/10.1002/cam4.1425
  22. Straube C, Elpula G, Gempt J, et al. Re-irradiation after gross total resection of recurrent glioblastoma : Spatial pattern of recurrence and a review of the literature as a basis for target volume definition. Strahlenther Onkol 2017;193:897-909. https://doi.org/10.1007/s00066-017-1161-6
  23. Grosu AL, Weber WA, Franz M, et al. Reirradiation of recurrent high-grade gliomas using amino acid PET (SPECT)/CT/MRI image fusion to determine gross tumor volume for stereotactic fractionated radiotherapy. Int J Radiat Oncol Biol Phys 2005;63:511-9. https://doi.org/10.1016/j.ijrobp.2005.01.056
  24. Miwa K, Matsuo M, Ogawa S, et al. Re-irradiation of recurrent glioblastoma multiforme using 11C-methionine PET/CT/MRI image fusion for hypofractionated stereotactic radiotherapy by intensity modulated radiation therapy. Radiat Oncol 2014;9:181. https://doi.org/10.1186/1748-717X-9-181
  25. Moller S, af Rosenschold PM, Costa J, et al. Toxicity and efficacy of re-irradiation of high-grade glioma in a phase I dose- and volume escalation trial. Radiother Oncol 2017;125:223-7. https://doi.org/10.1016/j.radonc.2017.09.039
  26. Sminia P, Mayer R. External beam radiotherapy of recurrent glioma: radiation tolerance of the human brain. Cancers (Basel) 2012;4:379-99. https://doi.org/10.3390/cancers4020379
  27. Shen CJ, Kummerlowe MN, Redmond KJ, et al. Re-irradiation for malignant glioma: Toward patient selection and defining treatment parameters for salvage. Adv Radiat Oncol 2018;3:582-90. https://doi.org/10.1016/j.adro.2018.06.005
  28. Klobukowski L, Falkov A, Chelimo C, et al. A retrospective review of re-irradiating patients' recurrent high-grade gliomas. Clin Oncol (R Coll Radiol) 2018;30:563-70. https://doi.org/10.1016/j.clon.2018.05.004
  29. Nieder C, Astner ST, Mehta MP, et al. Improvement, clinical course, and quality of life after palliative radiotherapy for recurrent glioblastoma. Am J Clin Oncol 2008;31:300-5. https://doi.org/10.1097/COC.0b013e31815e3fdc
  30. Ernst-Stecken A, Ganslandt O, Lambrecht U, et al. Survival and quality of life after hypofractionated stereotactic radiotherapy for recurrent malignant glioma. J Neurooncol 2007;81:287-94. https://doi.org/10.1007/s11060-006-9231-0
  31. Laack NN, Brown PD. Cognitive sequelae of brain radiation. In: Shrieve DC, Loeffler JS, editors. Human radiation Injury. Philadelphia, PA: Lippincott Williams & Wilkins; 2011. pp. 454-81.
  32. Scoccianti S, Francolini G, Carta GA, et al. Re-irradiation as salvage treatment in recurrent glioblastoma: a comprehensive literature review to provide practical answers to frequently asked questions. Crit Rev Oncol Hematol 2018;126:80-91. https://doi.org/10.1016/j.critrevonc.2018.03.024
  33. Zwirner K, Paulsen F, Schittenhelm J, et al. Prognostic parameters and outcome after re-irradiation for progressive glioblastoma. Acta Neurol Scand 2017;136:239-45. https://doi.org/10.1111/ane.12719
  34. Post CCB, Kramer MCA, Smid EJ, et al. Patterns of reirradiation for recurrent gliomas and validation of a prognostic score. Radiother Oncol 2019;130:156-63. https://doi.org/10.1016/j.radonc.2018.10.034
  35. Cho KH, Hall WA, Gerbi BJ, et al. Single dose versus fractionated stereotactic radiotherapy for recurrent highgrade gliomas. Int J Radiat Oncol Biol Phys 1999;45:1133-41. https://doi.org/10.1016/S0360-3016(99)00336-3
  36. Delgado-Lopez PD, Rinones-Mena E, Corrales-Garcia EM. Treatment-related changes in glioblastoma: a review on the controversies in response assessment criteria and the concepts of true progression, pseudoprogression, pseudoresponse and radionecrosis. Clin Transl Oncol 2018;20:939-53. https://doi.org/10.1007/s12094-017-1816-x
  37. Straube C, Antoni S, Gempt J, et al. Re-irradiation in elderly patients with glioblastoma: a single institution experience. J Neurooncol. 2019 Jan 18 [Epub]. http://doi.org/10.1007/s11060-019-03101-6.
  38. Fontanilla HP, Pinnix CC, Ketonen LM, et al. Palliative reirradiation for progressive diffuse intrinsic pontine glioma. Am J Clin Oncol 2012;35:51-7. https://doi.org/10.1097/COC.0b013e318201a2b7
  39. Freese C, Takiar V, Fouladi M, et al. Radiation and subsequent reirradiation outcomes in the treatment of diffuse intrinsic pontine glioma and a systematic review of the reirradiation literature. Pract Radiat Oncol 2017;7:86-92. https://doi.org/10.1016/j.prro.2016.11.005
  40. Janssens GO, Gandola L, Bolle S, et al. Survival benefit for patients with diffuse intrinsic pontine glioma (DIPG) undergoing re-irradiation at first progression: a matchedcohort analysis on behalf of the SIOP-E-HGG/DIPG working group. Eur J Cancer 2017;73:38-47. https://doi.org/10.1016/j.ejca.2016.12.007
  41. Tsang DS, Laperriere NJ. Re-irradiation for Paediatric Tumours. Clin Oncol (R Coll Radiol) 2019;31:191-8. https://doi.org/10.1016/j.clon.2018.10.003
  42. Muller K, Scheithauer H, Pietschmann S, et al. Reirradiation as part of a salvage treatment approach for progressive nonpontine pediatric high-grade gliomas: preliminary experiences from the German HIT-HGG study group. Radiat Oncol 2014;9:177. https://doi.org/10.1186/1748-717X-9-177
  43. Tsang DS, Burghen E, Klimo P Jr, et al. Outcomes after reirradiation for recurrent pediatric intracranial ependymoma. Int J Radiat Oncol Biol Phys 2018;100:507-15. https://doi.org/10.1016/j.ijrobp.2017.10.002
  44. Bouffet E, Hawkins CE, Ballourah W, et al. Survival benefit for pediatric patients with recurrent ependymoma treated with reirradiation. Int J Radiat Oncol Biol Phys 2012;83:1541-8. https://doi.org/10.1016/j.ijrobp.2011.10.039
  45. Rao AD, Rashid AS, Chen Q, et al. Reirradiation for recurrent pediatric central nervous system malignancies: a multiinstitutional review. Int J Radiat Oncol Biol Phys 2017;99:634-41. https://doi.org/10.1016/j.ijrobp.2017.07.026
  46. Hoffman LM, Plimpton SR, Foreman NK, et al. Fractionated stereotactic radiosurgery for recurrent ependymoma in children. J Neurooncol 2014;116:107-11. https://doi.org/10.1007/s11060-013-1259-3
  47. Merchant TE, Boop FA, Kun LE, et al. A retrospective study of surgery and reirradiation for recurrent ependymoma. Int J Radiat Oncol Biol Phys 2008;71:87-97. https://doi.org/10.1016/j.ijrobp.2007.09.037
  48. Krauze AV, Attia A, Braunstein S, et al. Expert consensus on reirradiation for recurrent glioma. Radiat Oncol 2017;12:194. https://doi.org/10.1186/s13014-017-0928-3
  49. Carson KA, Grossman SA, Fisher JD, et al. Prognostic factors for survival in adult patients with recurrent glioma enrolled onto the new approaches to brain tumor therapy CNS consortium phase I and II clinical trials. J Clin Oncol 2007;25:2601-6. https://doi.org/10.1200/JCO.2006.08.1661
  50. Kessel KA, Hesse J, Straube C, et al. Validation of an established prognostic score after re-irradiation of recurrent glioma. Acta Oncol 2017;56:422-6. https://doi.org/10.1080/0284186X.2016.1276621
  51. Muller K, Henke G, Compter I, et al. External validation of a prognostic model estimating the survival of patients with recurrent high-grade gliomas after reirradiation. Pract Radiat Oncol 2015;5:e143-50. https://doi.org/10.1016/j.prro.2014.10.001
  52. Kessel KA, Hesse J, Straube C, et al. Modification and optimization of an established prognostic score after reirradiation of recurrent glioma. PLoS One 2017;12:e0180457. https://doi.org/10.1371/journal.pone.0180457
  53. Scholtyssek F, Zwiener I, Schlamann A, et al. Reirradiation in progressive high-grade gliomas: outcome, role of concurrent chemotherapy, prognostic factors and validation of a new prognostic score with an independent patient cohort. Radiat Oncol 2013;8:161. https://doi.org/10.1186/1748-717X-8-161
  54. Niyazi M, Flieger M, Ganswindt U, et al. Validation of the prognostic Heidelberg re-irradiation score in an independent mono-institutional patient cohort. Radiat Oncol 2014;9:128. https://doi.org/10.1186/1748-717X-9-128
  55. Niyazi M, Adeberg S, Kaul D, et al. Independent validation of a new reirradiation risk score (RRRS) for glioma patients predicting post-recurrence survival: a multicenter DKTK/ROG analysis. Radiother Oncol 2018;127:121-7. https://doi.org/10.1016/j.radonc.2018.01.011
  56. Krauze AV, Peters C, Cheng J, et al. Re-irradiation for recurrent glioma- the NCI experience in tumor control, OAR toxicity and proposal of a novel prognostic scoring system. Radiat Oncol 2017;12:191. https://doi.org/10.1186/s13014-017-0930-9
  57. Chun SJ, Park SH, Park CK, et al. Survival gain with re-Op/RT for recurred high-grade gliomas depends upon risk groups. Radiother Oncol 2018;128:254-9. https://doi.org/10.1016/j.radonc.2018.05.024
  58. Wee CW, Kim E, Kim N, et al. Novel recursive partitioning analysis classification for newly diagnosed glioblastoma: a multi-institutional study highlighting the MGMT promoter methylation and IDH1 gene mutation status. Radiother Oncol 2017;123:106-11. https://doi.org/10.1016/j.radonc.2017.02.014
  59. Bell EH, Pugh SL, McElroy JP, et al. Molecular-based recursive partitioning analysis model for glioblastoma in the temozolomide era: a correlative analysis based on NRG Oncology RTOG 0525. JAMA Oncol 2017;3:784-92. https://doi.org/10.1001/jamaoncol.2016.6020
  60. Wee CW, Kim IH, Park CK, et al. Validation of a novel molecular RPA classification in glioblastoma (GBM-molRPA) treated with chemoradiation: a multi-institutional collaborative study. Radiother Oncol 2018;129:347-51. https://doi.org/10.1016/j.radonc.2018.09.001
  61. Skeie BS, Enger PO, Brogger J, et al. $\gamma$ knife surgery versus reoperation for recurrent glioblastoma multiforme. World Neurosurg 2012;78:658-69. https://doi.org/10.1016/j.wneu.2012.03.024
  62. Kim BS, Kong D-S, Seol HJ, et al. MGMT promoter methylation status as a prognostic factor for the outcome of gamma knife radiosurgery for recurrent glioblastoma. J Neurooncol 2017;133:615-22. https://doi.org/10.1007/s11060-017-2478-9
  63. Azoulay M, Santos F, Shenouda G, et al. Benefit of reoperation and salvage therapies for recurrent glioblastoma multiforme: results from a single institution. J Neurooncol 2017;132:419-26. https://doi.org/10.1007/s11060-017-2383-2
  64. Lee J, Ahn SS, Chang JH, et al. Hypofractionated re-irradiation after maximal surgical resection for recurrent glioblastoma: therapeutic adequacy and its prognosticators of survival. Yonsei Med J 2018;59:194-201. https://doi.org/10.3349/ymj.2018.59.2.194
  65. Lee J, Cho J, Chang JH, et al. Re-irradiation for recurrent gliomas: treatment outcomes and prognostic factors. Yonsei Med J 2016;57:824-30. https://doi.org/10.3349/ymj.2016.57.4.824
  66. Combs SE, Kessel KA, Hesse J, et al. Moving second courses of radiotherapy forward: early re-irradiation after surgical resection for recurrent gliomas improves efficacy with excellent tolerability. Neurosurgery 2018;83:1241-8.
  67. Straube C, Scherb H, Gempt J, et al. Adjuvant stereotactic fractionated radiotherapy to the resection cavity in recurrent glioblastoma: the GlioCave study (NOA 17 - ARO 2016/3 - DKTK ROG trial). BMC Cancer 2018;18:15. https://doi.org/10.1186/s12885-017-3928-7
  68. Weller M, Tabatabai G, Kastner B, et al. MGMT promoter methylation is a strong prognostic biomarker for benefit from dose-intensified temozolomide rechallenge in progressive glioblastoma: the DIRECTOR trial. Clin Cancer Res 2015;21:2057-64. https://doi.org/10.1158/1078-0432.CCR-14-2737
  69. Tipping M, Eickhoff J, Robins HI. Clinical outcomes in recurrent glioblastoma with bevacizumab therapy: an analysis of the literature. J Clin Neurosci 2017;44:101-6. https://doi.org/10.1016/j.jocn.2017.06.070
  70. Taal W, Oosterkamp HM, Walenkamp AM, et al. Singleagent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): a randomised controlled phase 2 trial. Lancet Oncol 2014;15:943-53. https://doi.org/10.1016/S1470-2045(14)70314-6
  71. Zhang G, Huang S, Wang Z. A meta-analysis of bevacizumab alone and in combination with irinotecan in the treatment of patients with recurrent glioblastoma multiforme. J Clin Neurosci 2012;19:1636-40. https://doi.org/10.1016/j.jocn.2011.12.028
  72. Kim HR, Kim KH, Kong DS, et al. Outcome of salvage treatment for recurrent glioblastoma. J Clin Neurosci 2015;22:468-73. https://doi.org/10.1016/j.jocn.2014.09.018
  73. Minniti G, Armosini V, Salvati M, et al. Fractionated stereotactic reirradiation and concurrent temozolomide in patients with recurrent glioblastoma. J Neurooncol 2011;103:683-91. https://doi.org/10.1007/s11060-010-0446-8
  74. Cabrera AR, Cuneo KC, Desjardins A, et al. Concurrent stereotactic radiosurgery and bevacizumab in recurrent malignant gliomas: a prospective trial. Int J Radiat Oncol Biol Phys 2013;86:873-9. https://doi.org/10.1016/j.ijrobp.2013.04.029
  75. Flieger M, Ganswindt U, Schwarz SB, et al. Re-irradiation and bevacizumab in recurrent high-grade glioma: an effective treatment option. J Neurooncol 2014;117:337-45. https://doi.org/10.1007/s11060-014-1394-5
  76. Minniti G, Agolli L, Falco T, et al. Hypofractionated stereotactic radiotherapy in combination with bevacizumab or fotemustine for patients with progressive malignant gliomas. J Neurooncol 2015;122:559-66. https://doi.org/10.1007/s11060-015-1745-x
  77. Schernberg A, Dhermain F, Ammari S, et al. Reirradiation with concurrent bevacizumab for recurrent high-grade gliomas in adult patients. Cancer Radiother 2018;22:9-16. https://doi.org/10.1016/j.canrad.2017.06.013
  78. Seystahl K, Wick W, Weller M. Therapeutic options in recurrent glioblastoma: an update. Crit Rev Oncol Hematol 2016;99:389-408. https://doi.org/10.1016/j.critrevonc.2016.01.018
  79. Desai BM, Rockne RC, Helenowski IB, et al. (PO34) Proton Therapy (PT) Large-volume re-irradiation for recurrent glioma: overall Survival (OS) and Toxicity Outcomes. Oncology (Williston Park) 2015;29(4 Suppl 1):205176.
  80. Combs SE, Burkholder I, Edler L, et al. Randomised phase I/II study to evaluate carbon ion radiotherapy versus fractionated stereotactic radiotherapy in patients with recurrent or progressive gliomas: the CINDERELLA trial. BMC Cancer 2010;10:533. https://doi.org/10.1186/1471-2407-10-533
  81. Miyatake S, Kawabata S, Yokoyama K, et al. Survival benefit of Boron neutron capture therapy for recurrent malignant gliomas. J Neurooncol 2009;91:199-206. https://doi.org/10.1007/s11060-008-9699-x
  82. Stupp R, Wong ET, Kanner AA, et al. NovoTTF-100A versus physician's choice chemotherapy in recurrent glioblastoma: a randomized phase III trial of a novel treatment modality. Eur J Cancer 2012;48:2192-202. https://doi.org/10.1016/j.ejca.2012.04.011

Cited by

  1. Role of Hyperbaric Oxygenation Plus Hypofractionated Stereotactic Radiotherapy in Recurrent High-Grade Glioma vol.11, 2019, https://doi.org/10.3389/fonc.2021.643469