Bevacizumab is an effective treatment for symptomatic cerebral necrosis after carbon ion therapy for recurrent intracranial malignant tumours: A case report

Liu,Ruifeng; Luo,Hongtao; Zhang,Qiuning; Sun,Shilong; Liu,Zhiqiang; Wang,Xiaohu; Geng,Yichao; Zhao,Xueshan

doi:10.3892/mco.2022.2547

Bevacizumab is an effective treatment for symptomatic cerebral necrosis after carbon ion therapy for recurrent intracranial malignant tumours: A case report

Authors:
- Ruifeng Liu
- Hongtao Luo
- Qiuning Zhang
- Shilong Sun
- Zhiqiang Liu
- Xiaohu Wang
- Yichao Geng
- Xueshan Zhao
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Affiliations: Institute of Modern Physics, Chinese Academy of Sciences, Lanzhou, Gansu 730000, P.R. China, The First School of Clinical Medicine, Lanzhou University, Lanzhou, Gansu 730000, P.R. China
Published online on: May 19, 2022 https://doi.org/10.3892/mco.2022.2547
Article Number: 114
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Carbon ion therapy (CIT) is a form of particle therapy, which not only spares normal tissues but may also improve local control of recurrent intracranial tumours. Cerebral radiation necrosis (RN) is one of the most serious adverse reactions of recurrent brain tumours following reirradiation, which may lead to neurological decline or even death. Bevacizumab is an anti‑vascular endothelial growth factor antibody, which has been used to treat symptomatic RN. However, studies on bevacizumab for the treatment of CIT‑induced RN are sparse. The present study described two cases that were successfully treated with bevacizumab for symptomatic RN following CIT for recurrent intracranial malignant tumours. The two recurrent intracranial malignant tumours, a chondrosarcoma in the right cavernous sinus and an anaplastic meningioma in the right frontal lobe, were enrolled in a clinical trial of CIT. Both cases were treated intravenously with bevacizumab when deterioration that appeared to be symptomatic brain RN was observed. Just before CIT, enhanced magnetic resonance imaging (MRI) was performed in each case to confirm tumour recurrence. Both cases exhibited a deterioration in symptoms, as well as on MRI, at 12‑month intervals following CIT. The first case underwent positron emission tomography/computed tomography to confirm no increase in fluorodeoxyglucose uptake in lesion areas. Both cases were diagnosed as having symptomatic brain RN and began intravenous administration of four cycles of 5 mg/kg bevacizumab biweekly. The patients responded well, with rapid and marked improvements on MRI, and in clinical symptoms. No tumour progression was observed 24 months after CIT. In conclusion, bevacizumab was revealed to exert marked effects on symptomatic brain RN following CIT. Notably, cycles of bevacizumab should be administered specifically based on the aim of treating brain necrosis, and long‑term or prophylactic applications are not recommended.

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1	Lapointe S, Perry A and Butowski NA: Primary brain tumours in adults. Lancet. 392:432–446. 2018.PubMed/NCBI View Article : Google Scholar
2	Krauze AV, Peters C, Cheng J, Ning H, Mackey M, Rowe L, Cooley-Zgela T, Smart DD and Camphausen K: Re-irradiation for recurrent glioma- the NCI experience in tumor control, OAR toxicity and proposal of a novel prognostic scoring system. Radiat Oncol. 12(191)2017.PubMed/NCBI View Article : Google Scholar
3	Nieder C, Andratschke NH and Grosu AL: Re-irradiation for recurrent primary brain tumors. Anticancer Res. 36:4985–4995. 2016.PubMed/NCBI View Article : Google Scholar
4	Kanai T, Endo M, Minohara S, Miyahara N, Koyama-ito H, Tomura H, Matsufuji N, Futami Y, Fukumura A, Hiraoka T, et al: Biophysical characteristics of HIMAC clinical irradiation system for heavy-ion radiation therapy. Int J Radiat Oncol Biol Phys. 44:201–210. 1999.PubMed/NCBI View Article : Google Scholar
5	Miyatake S, Nonoguchi N, Furuse M, Yoritsune E, Miyata T, Kawabata S and Kuroiwa T: Pathophysiology, diagnosis, and treatment of radiation necrosis in the brain. Neurol Med Chir (Tokyo). 55:50–59. 2015.PubMed/NCBI
6	Soliman HM, ElBeheiry AA, Abdel-Kerim AA, Farhoud AH and Reda MI: Recurrent brain tumor versus radiation necrosis; can dynamic susceptibility contrast (DSC) perfusion magnetic resonance imaging differentiate? Egyptian J Radiol Nuclear Med. 49:719–726. 2018.
7	Delishaj D, Ursino S, Pasqualetti F, Cristaudo A, Cosottini M, Fabrini MG and Paiar F: Bevacizumab for the treatment of radiation-induced cerebral necrosis: A systematic review of the literature. J Clin Med Res. 9:273–280. 2017.PubMed/NCBI View Article : Google Scholar
8	Amin MB, Edge SB, Greene FL, Byrd DR, Brookland RK, Washington MK, Gershenwald JE, Compton CC, Hess KR, Sullivan DC eds..et al: AJCC cancer staging manual. 8th ed. NewYork: Springer; 2017.
9	Cox JD, Stetz J and Pajak TF: Toxicity criteria of the radiation therapy oncology group (RTOG) and the European organization for research and treatment of cancer (EORTC). Int J Radiat Oncol Biol Phys. 31:1341–1346. 1995.PubMed/NCBI View Article : Google Scholar
10	Gritsch S, Batchelor TT and Gonzalez Castro LN: Diagnostic, therapeutic, and prognostic implications of the 2021 World Health Organization classification of tumors of the central nervous system. Cancer. 128:47–58. 2022.PubMed/NCBI View Article : Google Scholar
11	Parvez K, Parvez A and Zadeh G: The diagnosis and treatment of pseudoprogression, radiation necrosis and brain tumor recurrence. Int J Mol Sci. 15:11832–11846. 2014.PubMed/NCBI View Article : Google Scholar
12	Rahmathulla G, Marko NF and Weil RJ: Cerebral radiation necrosis: A review of the pathobiology, diagnosis and management considerations. J Clin Neurosci. 20:485–502. 2013.PubMed/NCBI View Article : Google Scholar
13	Ali FS, Arevalo O, Zorofchian S, Patrizz A, Riascos R, Tandon N, Blanco A, Ballester LY and Esquenazi Y: Cerebral radiation necrosis: incidence, pathogenesis, diagnostic challenges, and future opportunities. Curr Oncol Rep. 21(66)2019.PubMed/NCBI View Article : Google Scholar
14	Tessonnier T, Mairani A, Brons S, Haberer T, Debus J and Parodi K: Experimental dosimetric comparison of ¹H, ⁴He, ¹²C and ¹⁶O scanned ion beams. Phys Med Biol. 62:3958–3982. 2017.PubMed/NCBI View Article : Google Scholar
15	Suit H, DeLaney T, Goldberg S, Paganetti H, Clasie B, Gerweck L, Niemierko A, Hall E, Flanz J, Hallman J and Trofimov A: Proton vs. carbon ion beams in the definitive radiation treatment of cancer patients. Radiother Oncol. 95:3–22. 2010.PubMed/NCBI View Article : Google Scholar
16	Tinganelli W and Durante M: Carbon ion radiobiology. Cancers (Basel). 12(3022)2020.PubMed/NCBI View Article : Google Scholar
17	Sakama M and Kanematsu N: An evaluation method of clinical impact with setup, range, and radiosensitivity uncertainties in fractionated carbon-ion therapy. Phys Med Biol. 63(135003)2018.PubMed/NCBI View Article : Google Scholar
18	Eley JG, Newhauser WD, Richter D, Lüchtenborg R, Saito N and Bert C: Robustness of target dose coverage to motion uncertainties for scanned carbon ion beam tracking therapy of moving tumors. Phys Med Biol. 60:1717–1740. 2015.PubMed/NCBI View Article : Google Scholar
19	Kamp F, Brüningk S, Cabal G, Mairani A, Parodi K and Wilkens JJ: Variance-based sensitivity analysis of biological uncertainties in carbon ion therapy. Phys Med. 30:583–587. 2014.PubMed/NCBI View Article : Google Scholar
20	Meyer J, Bluett J, Amos R, Levy L, Choi S, Nguyen QN, Zhu XR, Gillin M and Lee A: Spot scanning proton beam therapy for prostate cancer: Treatment planning technique and analysis of consequences of rotational and translational alignment errors. Int J Radiat Oncol Biol Phys. 78:428–434. 2010.PubMed/NCBI View Article : Google Scholar
21	Lomax AJ: Intensity modulated proton therapy and its sensitivity to treatment uncertainties 1: The potential effects of calculational uncertainties. Phys Med Biol. 53:1027–1042. 2008.PubMed/NCBI View Article : Google Scholar
22	Malouff TD, Mahajan A, Krishnan S, Beltran C, Seneviratne DS and Trifiletti DM: Carbon ion therapy: A modern review of an emerging technology. Front Oncol. 10(82)2020.PubMed/NCBI View Article : Google Scholar
23	Kondo N, Sakurai Y, Takata T, Takai N, Nakagawa Y, Tanaka H, Watanabe T, Kume K, Toho T, Miyatake S, et al: Localized radiation necrosis model in mouse brain using proton ion beams. Appl Radiat Isot. 106:242–246. 2015.PubMed/NCBI View Article : Google Scholar
24	Sun XZ, Takahashi S, Kubota Y, Zhang R, Cui C, Nojima K and Fukui Y: Experimental model for irradiating a restricted region of the rat brain using heavy-ion beams. J Med Invest. 51:103–107. 2004.PubMed/NCBI View Article : Google Scholar
25	Takahashi S, Sun XZ, Kubota Y, Takai N and Nojima K: Histological and elemental changes in the rat brain after local irradiation with carbon ion beams. J Radiat Res. 43:143–152. 2002.PubMed/NCBI View Article : Google Scholar
26	Grosshans DR, Duman JG, Gaber MW and Sawakuchi G: Particle radiation induced neurotoxicity in the central nervous system. Int J Part Ther. 5:74–83. 2018.PubMed/NCBI View Article : Google Scholar
27	Mayer R and Sminia P: Reirradiation tolerance of the human brain. Int J Radiat Oncol Biol Phys. 70:1350–1360. 2008.PubMed/NCBI View Article : Google Scholar
28	Nonoguchi N, Miyatake S, Fukumoto M, Furuse M, Hiramatsu R, Kawabata S, Kuroiwa T, Tsuji M, Fukumoto M and Ono K: The distribution of vascular endothelial growth factor-producing cells in clinical radiation necrosis of the brain: Pathological consideration of their potential roles. J Neurooncol. 105:423–431. 2011.PubMed/NCBI View Article : Google Scholar
29	Zhuang H, Shi S, Yuan Z and Chang JY: Bevacizumab treatment for radiation brain necrosis: Mechanism, efficacy and issues. Mol Cancer. 18(21)2019.PubMed/NCBI View Article : Google Scholar
30	Shaw EG and Robbins ME: The management of radiation-induced brain injury. Cancer Treat Res. 128:7–22. 2006.PubMed/NCBI View Article : Google Scholar
31	Lam TC, Wong FC, Leung TW, Ng SH and Tung SY: Clinical outcomes of 174 nasopharyngeal carcinoma patients with radiation-induced temporal lobe necrosis. Int J Radiat Oncol Biol Phys. 82:e57–e65. 2012.PubMed/NCBI View Article : Google Scholar
32	Zhuo X, Huang X, Yan M, Li H, Li Y, Rong X, Lin J, Cai J, Xie F, Xu Y, et al: Comparison between high-dose and low-dose intravenous methylprednisolone therapy in patients with brain necrosis after radiotherapy for nasopharyngeal carcinoma. Radiother Oncol. 137:16–23. 2019.PubMed/NCBI View Article : Google Scholar
33	Khan M, Zhao Z, Arooj S and Liao G: Bevacizumab for radiation necrosis following radiotherapy of brain metastatic disease: A systematic review & meta-analysis. BMC Cancer. 21(167)2021.PubMed/NCBI View Article : Google Scholar
34	Levin VA, Bidaut L, Hou P, Kumar AJ, Wefel JS, Bekele BN, Grewal J, Prabhu S, Loghin M, Gilbert MR and Jackson EF: Randomized double-blind placebo-controlled trial of bevacizumab therapy for radiation necrosis of the central nervous system. Int J Radiat Oncol Biol Phys. 79:1487–1495. 2011.PubMed/NCBI View Article : Google Scholar
35	Lubelski D, Abdullah KG, Weil RJ and Marko NF: Bevacizumab for radiation necrosis following treatment of high grade glioma: A systematic review of the literature. J Neurooncol. 115:317–322. 2013.PubMed/NCBI View Article : Google Scholar
36	Tye K, Engelhard HH, Slavin KV, Nicholas MK, Chmura SJ, Kwok Y, Ho DS, Weichselbaum RR and Koshy M: An analysis of radiation necrosis of the central nervous system treated with bevacizumab. J Neurooncol. 117:321–327. 2014.PubMed/NCBI View Article : Google Scholar
37	Bodensohn R, Hadi I, Fleischmann DF, Corradini S, Thon N, Rauch J, Belka C and Niyazi M: Bevacizumab as a treatment option for radiation necrosis after cranial radiation therapy: A retrospective monocentric analysis. Strahlenther Onkol. 196:70–76. 2020.PubMed/NCBI View Article : Google Scholar
38	Wang Y, Pan L, Sheng X, Mao Y, Yao Y, Wang E, Zhang N and Dai J: Reversal of cerebral radiation necrosis with bevacizumab treatment in 17 Chinese patients. Eur J Med Res. 17(25)2012.PubMed/NCBI View Article : Google Scholar
39	Gonzalez J, Kumar AJ, Conrad CA and Levin VA: Effect of bevacizumab on radiation necrosis of the brain. Int J Radiat Oncol Biol Phys. 67:323–326. 2007.PubMed/NCBI View Article : Google Scholar
40	Furuse M, Nonoguchi N, Kawabata S, Yoritsune E, Takahashi M, Inomata T, Kuroiwa T and Miyatake S: Bevacizumab treatment for symptomatic radiation necrosis diagnosed by amino acid PET. Jpn J Clin Oncol. 43:337–341. 2013.PubMed/NCBI View Article : Google Scholar
41	Tejpar S, Prenen H and Mazzone M: Overcoming resistance to antiangiogenic therapies. Oncologist. 17:1039–1050. 2012.PubMed/NCBI View Article : Google Scholar
42	Vasudev NS and Reynolds AR: Anti-angiogenic therapy for cancer: Current progress, unresolved questions and future directions. Angiogenesis. 17:471–494. 2014.PubMed/NCBI View Article : Google Scholar
43	Jeyaretna DS, Curry WT Jr, Batchelor TT, Stemmer-Rachamimov A and Plotkin SR: Exacerbation of cerebral radiation necrosis by bevacizumab. J Clin Oncol. 29:e159–e162. 2011.PubMed/NCBI View Article : Google Scholar